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52Mn-labelled Beta-cyclodextrin for Melanoma Imaging: A Proof-of-concept Preclinical Study | In Vivo
<!DOCTYPE html> <html lang="en" dir="ltr" xmlns="http://www.w3.org/1999/xhtml" xmlns:mml="http://www.w3.org/1998/Math/MathML"> <head prefix="og: http://ogp.me/ns# article: http://ogp.me/ns/article# book: http://ogp.me/ns/book#" > <!--[if IE]><![endif]--> <link rel="dns-prefetch" href="//cdn.jsdelivr.net" /> <link rel="dns-prefetch" href="//cdn.foxycart.com" /> <link rel="dns-prefetch" href="//scholar.google.com" /> <meta http-equiv="Content-Type" content="text/html; charset=utf-8" /> <meta name="Generator" content="Drupal 7 (http://drupal.org)" /> <link rel="canonical" href="https://iv.iiarjournals.org/content/38/6/2591" /> <link rel="alternate" type="application/pdf" title="Full Text (PDF)" href="/content/38/6/2591.full.pdf" /> <link rel="alternate" type="text/plain" title="Full Text (Plain)" href="/content/38/6/2591.full.txt" /> <link rel="alternate" type="application/vnd.ms-powerpoint" title="Powerpoint" href="/content/38/6/2591.ppt" /> <meta name="issue_cover_image" content="https://iv.iiarjournals.org/sites/default/files/highwire/invivo/38/6.cover-source.jpg" /> <meta name="type" content="article" /> <meta name="category" content="research-article" /> <meta name="HW.identifier" content="/invivo/38/6/2591.atom" /> <meta name="HW.pisa" content="invivo;38/6/2591" /> <meta name="DC.Format" content="text/html" /> <meta name="DC.Language" content="en" /> <meta name="DC.Title" content="52Mn-labelled Beta-cyclodextrin for Melanoma Imaging: A Proof-of-concept Preclinical Study" /> <meta name="DC.Identifier" content="10.21873/invivo.13735" /> <meta name="DC.Date" content="2024-11-01" /> <meta name="DC.Publisher" content="International Institute of Anticancer Research" /> <meta name="DC.Rights" content="Copyright © 2024, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (https://creativecommons.org/licenses/by-nc-nd/4.0)." /> <meta name="DC.AccessRights" content="open-access" /> <meta name="DC.Description" content="Background/Aim: As prostaglandin E2 (PGE2) and its receptors (EP2) are over-expressed on tumor cells and microenvironment, radiolabeled cyclodextrins targeting such biomolecules are valuable vector candidates in molecular cancer diagnostics. Using experimental melanoma models, we evaluated the in vivo imaging behavior of novel Manganese-52-labeled (52Mn) randomly methylated beta-cyclodextrin ([52Mn]Mn-DOTAGA-RAMEB) and compared it with the following well-established tumor-specific probes: melanocortin-1 receptor (MC1-R)-affine [68Ga]Ga-DOTA-NAPamide and PGE2 selective [68Ga]Ga-DOTAGA-RAMEB cyclodextrin. Materials and Methods: Post-injection of [68Ga]Ga-DOTA-NAPamide, [68Ga]Ga-DOTAGA-RAMEB, and [52Mn]Mn-DOTAGA-RAMEB into MC1-R positive B16F10 melanoma-bearing mice, tumor radio-pharmaceutical uptake was quantified in vivo and ex vivo using preclinical positron emission tomography (PET) and high-performance gamma counter. Results: Although all tracers performed well in tumor identification, the highest standardized uptake values were detected in the [68Ga]Ga-DOTA-NAPamide scans. Corresponding to the ex vivo data, meaningful [52Mn]Mn-DOTAGA-RAMEB accumulation 1 h post-injection confirmed the tumor-targeting potential of the tracer. Temporal changes in PGE2/EP2 expression of the neoplasms may explain the significant differences observed between the tumor uptake of the two cyclodextrin probes and that of the 52Mn-labelled compound measured 1 h, 4 h, and 3 days post-injection (p≤0.01, p≤0.05). Conclusion: Although further pharmacokinetical optimization may be required, 52Mn-labelled cyclodextrin holds potential in melanoma diagnostics and the PET-based longitudinal assessment of tumor-associated PGE2/EP2 expression." /> <meta name="DC.Contributor" content="ZITA KÉPES" /> <meta name="DC.Contributor" content="JUDIT P. SZABÓ" /> <meta name="DC.Contributor" content="IBOLYA KÁLMÁN-SZABÓ" /> <meta name="DC.Contributor" content="TAMÁS SASS" /> <meta name="DC.Contributor" content="REGINA ESZE" /> <meta name="DC.Contributor" content="GÁBOR OPPOSITS" /> <meta name="DC.Contributor" content="ISTVÁN JÓSZAI" /> <meta name="DC.Contributor" content="DEZSŐ SZIKRA" /> <meta name="DC.Contributor" content="FERENC FENYVESI" /> <meta name="DC.Contributor" content="ISTVÁN HAJDU" /> <meta name="DC.Contributor" content="GYÖRGY TRENCSÉNYI" /> <meta name="article:published_time" content="2024-11-01" /> <meta name="article:section" content="Experimental Studies" /> <meta name="citation_title" content="52Mn-labelled Beta-cyclodextrin for Melanoma Imaging: A Proof-of-concept Preclinical Study" /> <meta name="citation_abstract" lang="en" content="<p>Background/Aim: As prostaglandin E2 (PGE2) and its receptors (EP2) are over-expressed on tumor cells and microenvironment, radiolabeled cyclodextrins targeting such biomolecules are valuable vector candidates in molecular cancer diagnostics. Using experimental melanoma models, we evaluated the in vivo imaging behavior of novel Manganese-52-labeled (<sup>52</sup>Mn) randomly methylated beta-cyclodextrin ([<sup>52</sup>Mn]Mn-DOTAGA-RAMEB) and compared it with the following well-established tumor-specific probes: melanocortin-1 receptor (MC1-R)-affine [<sup>68</sup>Ga]Ga-DOTA-NAPamide and PGE2 selective [<sup>68</sup>Ga]Ga-DOTAGA-RAMEB cyclodextrin. Materials and Methods: Post-injection of [<sup>68</sup>Ga]Ga-DOTA-NAPamide, [<sup>68</sup>Ga]Ga-DOTAGA-RAMEB, and [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB into MC1-R positive B16F10 melanoma-bearing mice, tumor radio-pharmaceutical uptake was quantified in vivo and ex vivo using preclinical positron emission tomography (PET) and high-performance gamma counter. Results: Although all tracers performed well in tumor identification, the highest standardized uptake values were detected in the [<sup>68</sup>Ga]Ga-DOTA-NAPamide scans. Corresponding to the ex vivo data, meaningful [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB accumulation 1 h post-injection confirmed the tumor-targeting potential of the tracer. Temporal changes in PGE2/EP2 expression of the neoplasms may explain the significant differences observed between the tumor uptake of the two cyclodextrin probes and that of the <sup>52</sup>Mn-labelled compound measured 1 h, 4 h, and 3 days post-injection (p≤0.01, p≤0.05). Conclusion: Although further pharmacokinetical optimization may be required, <sup>52</sup>Mn-labelled cyclodextrin holds potential in melanoma diagnostics and the PET-based longitudinal assessment of tumor-associated PGE2/EP2 expression.</p>" /> <meta name="citation_journal_title" content="In Vivo" /> <meta name="citation_publisher" content="International Institute of Anticancer Research" /> <meta name="citation_publication_date" content="2024/11/01" /> <meta name="citation_mjid" content="invivo;38/6/2591" /> <meta name="citation_id" content="38/6/2591" /> <meta name="citation_public_url" content="https://iv.iiarjournals.org/content/38/6/2591" /> <meta name="citation_abstract_html_url" content="https://iv.iiarjournals.org/content/38/6/2591.abstract" /> <meta name="citation_full_html_url" content="https://iv.iiarjournals.org/content/38/6/2591.full" /> <meta name="citation_pdf_url" content="https://iv.iiarjournals.org/content/invivo/38/6/2591.full.pdf" /> <meta name="citation_issn" content="0258-851X" /> <meta name="citation_issn" content="1791-7549" /> <meta name="citation_doi" content="10.21873/invivo.13735" /> <meta name="citation_pmid" content="39477386" /> <meta name="citation_volume" content="38" /> <meta name="citation_issue" content="6" /> <meta name="citation_article_type" content="Research Article" /> <meta name="citation_section" content="Experimental Studies" /> <meta name="citation_firstpage" content="2591" /> <meta name="citation_lastpage" content="2600" /> <meta name="citation_access" content="all" /> <meta name="citation_author" content="ZITA KÉPES" /> <meta name="citation_author_institution" content="Division of Nuclear Medicine and Translational Imaging, Department of Medical Imaging, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;" /> <meta name="citation_author_institution" content="Gyula Petrányi Doctoral School of Clinical Immunology and Allergology, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;" /> <meta name="citation_author_email" content="kepes.zita@med.unideb.hu" /> <meta name="citation_author" content="JUDIT P. SZABÓ" /> <meta name="citation_author_institution" content="Division of Nuclear Medicine and Translational Imaging, Department of Medical Imaging, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;" /> <meta name="citation_author" content="IBOLYA KÁLMÁN-SZABÓ" /> <meta name="citation_author_institution" content="Division of Nuclear Medicine and Translational Imaging, Department of Medical Imaging, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;" /> <meta name="citation_author_institution" content="Gyula Petrányi Doctoral School of Clinical Immunology and Allergology, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;" /> <meta name="citation_author" content="TAMÁS SASS" /> <meta name="citation_author_institution" content="Department of Surgery, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;" /> <meta name="citation_author" content="REGINA ESZE" /> <meta name="citation_author_institution" content="Division of Metabolic Diseases, Department of Internal Medicine, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;" /> <meta name="citation_author" content="GÁBOR OPPOSITS" /> <meta name="citation_author_institution" content="Division of Nuclear Medicine and Translational Imaging, Department of Medical Imaging, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;" /> <meta name="citation_author" content="ISTVÁN JÓSZAI" /> <meta name="citation_author_institution" content="Division of Nuclear Medicine and Translational Imaging, Department of Medical Imaging, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;" /> <meta name="citation_author" content="DEZSŐ SZIKRA" /> <meta name="citation_author_institution" content="Division of Nuclear Medicine and Translational Imaging, Department of Medical Imaging, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;" /> <meta name="citation_author" content="FERENC FENYVESI" /> <meta name="citation_author_institution" content="Department of Pharmaceutical Technology, Faculty of Pharmacy, University of Debrecen, Debrecen, Hungary" /> <meta name="citation_author" content="ISTVÁN HAJDU" /> <meta name="citation_author_institution" content="Division of Nuclear Medicine and Translational Imaging, Department of Medical Imaging, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;" /> <meta name="citation_author" content="GYÖRGY TRENCSÉNYI" /> <meta name="citation_author_institution" content="Division of Nuclear Medicine and Translational Imaging, Department of Medical Imaging, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;" /> <meta name="citation_author_institution" content="Gyula Petrányi Doctoral School of Clinical Immunology and Allergology, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;" /> <meta name="citation_reference" content="citation_journal_title=Front Oncol;citation_author=LC. 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Fenyvesi;citation_title=Radiochemical synthesis and preclinical evaluation of 68Ga-labeled NODAGA-hydroxypropyl-beta-cyclodextrin (68Ga-NODAGA-HPBCD);citation_pages=202-208;citation_volume=128;citation_year=2019;citation_pmid=30521943;citation_doi=10.1016/j.ejps.2018.12.001" /> <meta name="citation_fulltext_world_readable" content="" /> <meta name="twitter:title" content="52Mn-labelled Beta-cyclodextrin for Melanoma Imaging: A Proof-of-concept Preclinical Study" /> <meta name="twitter:card" content="summary_large_image" /> <meta name="twitter:image" content="https://iv.iiarjournals.org/sites/default/files/highwire/invivo/38/6.cover-source.jpg" /> <meta name="twitter:description" content="Background/Aim: As prostaglandin E2 (PGE2) and its receptors (EP2) are over-expressed on tumor cells and microenvironment, radiolabeled cyclodextrins targeting such biomolecules are valuable vector candidates in molecular cancer diagnostics. Using experimental melanoma models, we evaluated the in vivo imaging behavior of novel Manganese-52-labeled (52Mn) randomly methylated beta-cyclodextrin ([52Mn]Mn-DOTAGA-RAMEB) and compared it with the following well-established tumor-specific probes: melanocortin-1 receptor (MC1-R)-affine [68Ga]Ga-DOTA-NAPamide and PGE2 selective [68Ga]Ga-DOTAGA-RAMEB cyclodextrin. Materials and Methods: Post-injection of [68Ga]Ga-DOTA-NAPamide, [68Ga]Ga-DOTAGA-RAMEB, and [52Mn]Mn-DOTAGA-RAMEB into MC1-R positive B16F10 melanoma-bearing mice, tumor radio-pharmaceutical uptake was quantified in vivo and ex vivo using preclinical positron emission tomography (PET) and high-performance gamma counter. Results: Although all tracers performed well in tumor identification, the highest standardized uptake values were detected in the [68Ga]Ga-DOTA-NAPamide scans. Corresponding to the ex vivo data, meaningful [52Mn]Mn-DOTAGA-RAMEB accumulation 1 h post-injection confirmed the tumor-targeting potential of the tracer. Temporal changes in PGE2/EP2 expression of the neoplasms may explain the significant differences observed between the tumor uptake of the two cyclodextrin probes and that of the 52Mn-labelled compound measured 1 h, 4 h, and 3 days post-injection (p≤0.01, p≤0.05). Conclusion: Although further pharmacokinetical optimization may be required, 52Mn-labelled cyclodextrin holds potential in melanoma diagnostics and the PET-based longitudinal assessment of tumor-associated PGE2/EP2 expression." /> <meta name="og-title" property="og:title" content="52Mn-labelled Beta-cyclodextrin for Melanoma Imaging: A Proof-of-concept Preclinical Study" /> <meta name="og-url" property="og:url" content="https://iv.iiarjournals.org/content/38/6/2591" /> <meta name="og-site-name" property="og:site_name" content="In Vivo" /> <meta name="og-description" property="og:description" content="Background/Aim: As prostaglandin E2 (PGE2) and its receptors (EP2) are over-expressed on tumor cells and microenvironment, radiolabeled cyclodextrins targeting such biomolecules are valuable vector candidates in molecular cancer diagnostics. Using experimental melanoma models, we evaluated the in vivo imaging behavior of novel Manganese-52-labeled (52Mn) randomly methylated beta-cyclodextrin ([52Mn]Mn-DOTAGA-RAMEB) and compared it with the following well-established tumor-specific probes: melanocortin-1 receptor (MC1-R)-affine [68Ga]Ga-DOTA-NAPamide and PGE2 selective [68Ga]Ga-DOTAGA-RAMEB cyclodextrin. Materials and Methods: Post-injection of [68Ga]Ga-DOTA-NAPamide, [68Ga]Ga-DOTAGA-RAMEB, and [52Mn]Mn-DOTAGA-RAMEB into MC1-R positive B16F10 melanoma-bearing mice, tumor radio-pharmaceutical uptake was quantified in vivo and ex vivo using preclinical positron emission tomography (PET) and high-performance gamma counter. Results: Although all tracers performed well in tumor identification, the highest standardized uptake values were detected in the [68Ga]Ga-DOTA-NAPamide scans. Corresponding to the ex vivo data, meaningful [52Mn]Mn-DOTAGA-RAMEB accumulation 1 h post-injection confirmed the tumor-targeting potential of the tracer. Temporal changes in PGE2/EP2 expression of the neoplasms may explain the significant differences observed between the tumor uptake of the two cyclodextrin probes and that of the 52Mn-labelled compound measured 1 h, 4 h, and 3 days post-injection (p≤0.01, p≤0.05). Conclusion: Although further pharmacokinetical optimization may be required, 52Mn-labelled cyclodextrin holds potential in melanoma diagnostics and the PET-based longitudinal assessment of tumor-associated PGE2/EP2 expression." /> <meta name="og-type" property="og:type" content="article" /> <meta name="og-image" property="og:image" content="https://iv.iiarjournals.org/sites/default/files/highwire/invivo/38/6.cover-source.jpg" /> <link rel="shortlink" href="/node/24529" /> <link rel="shortcut icon" href="https://iv.iiarjournals.org/sites/default/files/images/favicon.ico" type="image/vnd.microsoft.icon" /> <meta name="viewport" content="width=device-width, initial-scale=1" /> <title>52Mn-labelled Beta-cyclodextrin for Melanoma Imaging: A Proof-of-concept Preclinical Study | In Vivo</title> <link type="text/css" rel="stylesheet" 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highwire-cite-highwire-article highwire-citation-jcore-article-title-complete clearfix has-author-tooltip highwire-citation-highwire-article-top-a"> <div class="highwire-cite-overline"><span class="highwire-cite-metadata-article-type highwire-cite-metadata">Research Article</span><span class="separator-pipe"></span><span class="highwire-cite-metadata-art-cat highwire-cite-metadata"><span class="wrapper">Experimental Studies</span></span></div> <div class="highwire-cite-access"><span class="highwire-citation-access"><i class="highwire-access-icon highwire-access-icon-open-access open-access hw-icon-open-access" title="Open Access" aria-hidden="true"></i><span class="element-invisible highwire-access-icon highwire-access-icon-open-access" style="">Open Access</span></span></div> <h1 class="highwire-cite-title" id="page-title"><sup>52</sup>Mn-labelled Beta-cyclodextrin for Melanoma Imaging: A Proof-of-concept Preclinical Study</h1> <div class="highwire-cite-authors"><span class="highwire-citation-authors"><span class="highwire-citation-author first" data-delta="0">ZITA KÉPES</span>, <span class="highwire-citation-author" data-delta="1">JUDIT P. SZABÓ</span>, <span class="highwire-citation-author" data-delta="2">IBOLYA KÁLMÁN-SZABÓ</span>, <span class="highwire-citation-author" data-delta="3">TAMÁS SASS</span>, <span class="highwire-citation-author" data-delta="4">REGINA ESZE</span>, <span class="highwire-citation-author" data-delta="5">GÁBOR OPPOSITS</span>, <span class="highwire-citation-author" data-delta="6">ISTVÁN JÓSZAI</span>, <span class="highwire-citation-author" data-delta="7">DEZSŐ SZIKRA</span>, <span class="highwire-citation-author" data-delta="8">FERENC FENYVESI</span>, <span class="highwire-citation-author" data-delta="9">ISTVÁN HAJDU</span> and <span class="highwire-citation-author" data-delta="10">GYÖRGY TRENCSÉNYI</span></span></div> <div class="highwire-cite-metadata"><span class="highwire-cite-metadata-journal highwire-cite-metadata">In Vivo </span><span class="highwire-cite-metadata-date highwire-cite-metadata">November 2024, </span><span class="highwire-cite-metadata-volume highwire-cite-metadata">38 </span><span class="highwire-cite-metadata-issue highwire-cite-metadata">(6) </span><span class="highwire-cite-metadata-pages highwire-cite-metadata">2591-2600; </span><span class="highwire-cite-metadata-doi highwire-cite-metadata">DOI: https://doi.org/10.21873/invivo.13735 </span></div> <div class="highwire-cite-extras"><span class="highwire-foxycart-add-to-cart-ahah highwire-foxycart-add-to-cart-ahah" data-text="Add to Cart (%short-price)" data-apath="/invivo/38/6/2591.atom" data-type="link" data-font-icon="" data-parent-id="24486"></span></div> </div> <div id="hw-article-author-popups-top-node-24529--4404697164" style="display: none;"><div class="author-tooltip-0"><div class="author-tooltip-name">ZITA KÉPES </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'><span class='nlm-sup'>1</span>Division of Nuclear Medicine and Translational Imaging, Department of Medical Imaging, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;</div><div class='author-affiliation'><span class='nlm-sup'>2</span>Gyula Petrányi Doctoral School of Clinical Immunology and Allergology, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;</div></span></div><ul class="author-tooltip-find-more"><li class="author-tooltip-gs-link first"><a href="/lookup/google-scholar?link_type=googlescholar&gs_type=author&author%5B0%5D=ZITA%2BK%C3%89PES%2B" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on Google Scholar</a></li><li class="author-tooltip-pubmed-link"><a href="/lookup/external-ref?access_num=K%C3%89PES%20Z&link_type=AUTHORSEARCH" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on PubMed</a></li><li class="author-site-search-link"><a href="/search/author1%3AZITA%2BK%25C3%2589PES%2B" rel="nofollow" class="" data-icon-position="" data-hide-link-title="0">Search for this author on this site</a></li><li class="author-corresp-email-link last"><span>For correspondence: <a href="mailto:kepes.zita@med.unideb.hu" class="" data-icon-position="" data-hide-link-title="0">kepes.zita@med.unideb.hu</a></span></li></ul></div><div class="author-tooltip-1"><div class="author-tooltip-name">JUDIT P. SZABÓ </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'><span class='nlm-sup'>1</span>Division of Nuclear Medicine and Translational Imaging, Department of Medical Imaging, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;</div></span></div><ul class="author-tooltip-find-more"><li class="author-tooltip-gs-link first"><a href="/lookup/google-scholar?link_type=googlescholar&gs_type=author&author%5B0%5D=JUDIT%2BP.%2BSZAB%C3%93%2B" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on Google Scholar</a></li><li class="author-tooltip-pubmed-link"><a href="/lookup/external-ref?access_num=SZAB%C3%93%20JP&link_type=AUTHORSEARCH" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on PubMed</a></li><li class="author-site-search-link last"><a href="/search/author1%3AJUDIT%2BP.%2BSZAB%25C3%2593%2B" rel="nofollow" class="" data-icon-position="" data-hide-link-title="0">Search for this author on this site</a></li></ul></div><div class="author-tooltip-2"><div class="author-tooltip-name">IBOLYA KÁLMÁN-SZABÓ </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'><span class='nlm-sup'>1</span>Division of Nuclear Medicine and Translational Imaging, Department of Medical Imaging, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;</div><div class='author-affiliation'><span class='nlm-sup'>2</span>Gyula Petrányi Doctoral School of Clinical Immunology and Allergology, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;</div></span></div><ul class="author-tooltip-find-more"><li class="author-tooltip-gs-link first"><a href="/lookup/google-scholar?link_type=googlescholar&gs_type=author&author%5B0%5D=IBOLYA%2BK%C3%81LM%C3%81N-SZAB%C3%93%2B" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on Google Scholar</a></li><li class="author-tooltip-pubmed-link"><a href="/lookup/external-ref?access_num=K%C3%81LM%C3%81N-SZAB%C3%93%20I&link_type=AUTHORSEARCH" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on PubMed</a></li><li class="author-site-search-link last"><a href="/search/author1%3AIBOLYA%2BK%25C3%2581LM%25C3%2581N-SZAB%25C3%2593%2B" rel="nofollow" class="" data-icon-position="" data-hide-link-title="0">Search for this author on this site</a></li></ul></div><div class="author-tooltip-3"><div class="author-tooltip-name">TAMÁS SASS </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'><span class='nlm-sup'>3</span>Department of Surgery, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;</div></span></div><ul class="author-tooltip-find-more"><li class="author-tooltip-gs-link first"><a href="/lookup/google-scholar?link_type=googlescholar&gs_type=author&author%5B0%5D=TAM%C3%81S%2BSASS%2B" 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Debrecen, Hungary;</div></span></div><ul class="author-tooltip-find-more"><li class="author-tooltip-gs-link first"><a href="/lookup/google-scholar?link_type=googlescholar&gs_type=author&author%5B0%5D=G%C3%81BOR%2BOPPOSITS%2B" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on Google Scholar</a></li><li class="author-tooltip-pubmed-link"><a href="/lookup/external-ref?access_num=OPPOSITS%20G&link_type=AUTHORSEARCH" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on PubMed</a></li><li class="author-site-search-link last"><a href="/search/author1%3AG%25C3%2581BOR%2BOPPOSITS%2B" rel="nofollow" class="" data-icon-position="" data-hide-link-title="0">Search for this author on this site</a></li></ul></div><div class="author-tooltip-6"><div class="author-tooltip-name">ISTVÁN JÓSZAI </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'><span 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class="author-tooltip-name">DEZSŐ SZIKRA </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'><span class='nlm-sup'>1</span>Division of Nuclear Medicine and Translational Imaging, Department of Medical Imaging, Faculty of Medicine, University of Debrecen, Debrecen, Hungary;</div></span></div><ul class="author-tooltip-find-more"><li class="author-tooltip-gs-link first"><a href="/lookup/google-scholar?link_type=googlescholar&gs_type=author&author%5B0%5D=DEZS%C5%90%2BSZIKRA%2B" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on Google Scholar</a></li><li class="author-tooltip-pubmed-link"><a href="/lookup/external-ref?access_num=SZIKRA%20D&link_type=AUTHORSEARCH" target="_blank" class="" data-icon-position="" data-hide-link-title="0">Find this author on PubMed</a></li><li class="author-site-search-link last"><a href="/search/author1%3ADEZS%25C5%2590%2BSZIKRA%2B" rel="nofollow" class="" 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class="panels-ajax-tab-container"><div class="panels-ajax-tab-loading" style ="display:none"><img class="loading" src="https://iv.iiarjournals.org/sites/all/modules/contrib/panels_ajax_tab/images/loading.gif" alt="Loading" title="Loading" /></div><div class="panels-ajax-tab-wrap-jnl_iiar_tab_art"><div class="panel-display panel-1col clearfix" > <div class="panel-panel panel-col"> <div><div class="panel-pane pane-highwire-markup" > <div class="pane-content"> <div class="highwire-markup"><div xmlns="http://www.w3.org/1999/xhtml" data-highwire-cite-ref-tooltip-instance="highwire_reflinks_tooltip" class="content-block-markup" xmlns:xhtml="http://www.w3.org/1999/xhtml"><div class="article fulltext-view "><span class="highwire-journal-article-marker-start"></span><div class="section abstract" id="abstract-1"><h2>Abstract</h2><p id="p-5">Background/Aim: As prostaglandin E2 (PGE2) and its receptors (EP2) are over-expressed on tumor cells and microenvironment, radiolabeled cyclodextrins targeting such biomolecules are valuable vector candidates in molecular cancer diagnostics. Using experimental melanoma models, we evaluated the in vivo imaging behavior of novel Manganese-52-labeled (<sup>52</sup>Mn) randomly methylated beta-cyclodextrin ([<sup>52</sup>Mn]Mn-DOTAGA-RAMEB) and compared it with the following well-established tumor-specific probes: melanocortin-1 receptor (MC1-R)-affine [<sup>68</sup>Ga]Ga-DOTA-NAPamide and PGE2 selective [<sup>68</sup>Ga]Ga-DOTAGA-RAMEB cyclodextrin. Materials and Methods: Post-injection of [<sup>68</sup>Ga]Ga-DOTA-NAPamide, [<sup>68</sup>Ga]Ga-DOTAGA-RAMEB, and [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB into MC1-R positive B16F10 melanoma-bearing mice, tumor radio-pharmaceutical uptake was quantified in vivo and ex vivo using preclinical positron emission tomography (PET) and high-performance gamma counter. Results: Although all tracers performed well in tumor identification, the highest standardized uptake values were detected in the [<sup>68</sup>Ga]Ga-DOTA-NAPamide scans. Corresponding to the ex vivo data, meaningful [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB accumulation 1 h post-injection confirmed the tumor-targeting potential of the tracer. Temporal changes in PGE2/EP2 expression of the neoplasms may explain the significant differences observed between the tumor uptake of the two cyclodextrin probes and that of the <sup>52</sup>Mn-labelled compound measured 1 h, 4 h, and 3 days post-injection (p≤0.01, p≤0.05). Conclusion: Although further pharmacokinetical optimization may be required, <sup>52</sup>Mn-labelled cyclodextrin holds potential in melanoma diagnostics and the PET-based longitudinal assessment of tumor-associated PGE2/EP2 expression.</p></div><span class="kwd-group-title">Key Words:</span><ul class="kwd-group"><li class="kwd"><a href="/keyword/cyclodextrin" class="hw-term hw-article-keyword hw-article-keyword-cyclodextrin" rel="nofollow">Cyclodextrin</a></li><li class="kwd"><a xmlns:default="http://www.w3.org/1999/xhtml" href="/keyword/manganese-52-52mn" class="hw-term hw-article-keyword hw-article-keyword-manganese-52-52mn" rel="nofollow">Manganese-52 (<sup xmlns:default="http://www.w3.org/1999/xhtml">52</sup>Mn)</a></li><li class="kwd"><a href="/keyword/malignant-melanoma" class="hw-term hw-article-keyword hw-article-keyword-malignant-melanoma" rel="nofollow">malignant melanoma</a></li><li class="kwd"><a href="/keyword/positron-emission-tomography-pet" class="hw-term hw-article-keyword hw-article-keyword-positron-emission-tomography-pet" rel="nofollow">positron emission tomography (PET)</a></li><li class="kwd"><a href="/keyword/preclinical" class="hw-term hw-article-keyword hw-article-keyword-preclinical" rel="nofollow">preclinical</a></li><li class="kwd"><a href="/keyword/prostaglandin-e2-pge2" class="hw-term hw-article-keyword hw-article-keyword-prostaglandin-e2-pge2" rel="nofollow">prostaglandin E2 (PGE2)</a></li></ul><p id="p-6">Being a highly aggressive malignant skin cancer (<a id="xref-ref-1-1" class="xref-bibr" href="#ref-1">1</a>-<a id="xref-ref-3-1" class="xref-bibr" href="#ref-3">3</a>), cutaneous melanoma has been a dynamic area of research over the last several decades (<a id="xref-ref-4-1" class="xref-bibr" href="#ref-4">4</a>, <a id="xref-ref-5-1" class="xref-bibr" href="#ref-5">5</a>). Due to its ever-growing incidence (<a id="xref-ref-6-1" class="xref-bibr" href="#ref-6">6</a>, <a id="xref-ref-7-1" class="xref-bibr" href="#ref-7">7</a>) and metastatic potential (<a id="xref-ref-8-1" class="xref-bibr" href="#ref-8">8</a>, <a id="xref-ref-9-1" class="xref-bibr" href="#ref-9">9</a>) timely disease diagnostics seems straightforward (<a id="xref-ref-10-1" class="xref-bibr" href="#ref-10">10</a>-<a id="xref-ref-12-1" class="xref-bibr" href="#ref-12">12</a>). Although 2-[<sup>18</sup>F]Fluoro-2-deoxy-d-glucose ([<sup>18</sup>F]F-FDG) positron emission tomography (PET)-based molecular imaging still remains the mainstay imaging modality for primary disease staging, and monitoring (<a id="xref-ref-13-1" class="xref-bibr" href="#ref-13">13</a>, <a id="xref-ref-14-1" class="xref-bibr" href="#ref-14">14</a>), given its non-specificity (<a id="xref-ref-15-1" class="xref-bibr" href="#ref-15">15</a>, <a id="xref-ref-16-1" class="xref-bibr" href="#ref-16">16</a>), the development of tumor-specific radio-pharmaceuticals has attained notable interest.</p><p id="p-7">As melanocortin-1 receptor (MC1-R) shows over-expression on most of the primary and metastatic melanoma tumor cells (<a id="xref-ref-17-1" class="xref-bibr" href="#ref-17">17</a>-<a id="xref-ref-20-1" class="xref-bibr" href="#ref-20">20</a>), MC1-R ligands furnished with a radioisotope could be potential candidates in melanoma detection. Several preclinical studies confirmed the diagnostic feasibility of radiolabeled (<sup>68</sup>Ga, <sup>111</sup>In, <sup>18</sup>F, <sup>213</sup>Bi, <sup>64</sup>Cu, <sup>44</sup>Sc, <sup>99m</sup>Tc) amide derivatives targeting MC1-R (NAP,- HOLD,- MARS, -FOLDamide) in the identification of experimental melanoma tumors (<a id="xref-ref-21-1" class="xref-bibr" href="#ref-21">21</a>-<a id="xref-ref-29-1" class="xref-bibr" href="#ref-29">29</a>). The favorable imaging properties of <sup>68</sup>Ga-labelled NAPamide ([<sup>68</sup>Ga]Ga-DOTA-NAPamide) for example is exemplified by high uptake in B16-F10 melanoma tumors coupled with faint non target activity (<a id="xref-ref-24-1" class="xref-bibr" href="#ref-24">24</a>, <a id="xref-ref-28-1" class="xref-bibr" href="#ref-28">28</a>).</p><p id="p-8">As prostaglandin E2 (PGE2), and PGE2 receptors (EPs) are firmly related to tumorigenesis (<a id="xref-ref-30-1" class="xref-bibr" href="#ref-30">30</a>-<a id="xref-ref-35-1" class="xref-bibr" href="#ref-35">35</a>), the role of PGE2 in cancer diagnostics is pivotal (<a id="xref-ref-36-1" class="xref-bibr" href="#ref-36">36</a>). In addition, given the inert capability of cyclodextrin molecules to form host-guest complexes with PGE2, they seem precious molecular platforms for developing tumor-selective probes that target PGE2 positive malignancies (<a id="xref-ref-37-1" class="xref-bibr" href="#ref-37">37</a>-<a id="xref-ref-40-1" class="xref-bibr" href="#ref-40">40</a>). Our previous findings strengthen the hypothesis that randomly-methylated-beta-cyclodextrin (RAMEB) labelled with <sup>68</sup>Ga ([<sup>68</sup>Ga]Ga-NODAGA-RAMEB) could be effectively used for the <em>in vivo</em> identification of PGE2 positive B16F10 melanoma tumors (<a id="xref-ref-41-1" class="xref-bibr" href="#ref-41">41</a>). Further, high [<sup>205/206</sup>Bi]Bi-DOTAGA-RAMEB uptake of PGE2 expressing BxPC-3 xenografts proved that the change of the labelling entity has no significant impact on the imaging behavior of cyclodextrins (<a id="xref-ref-38-1" class="xref-bibr" href="#ref-38">38</a>). Despite these promising initial results, however, the use of short-lived <sup>68</sup>Ga or <sup>205/206</sup>Bi isotopes suffers the limitation of not covering extended imaging periods (<a id="xref-ref-42-1" class="xref-bibr" href="#ref-42">42</a>-<a id="xref-ref-44-1" class="xref-bibr" href="#ref-44">44</a>). To overcome this shortcoming, long-lived Manganese-52 (<sup>52</sup>Mn; T<sub>1/2</sub>=5.59 days, <em>β</em><sup>+</sup>=242KeV) seems to be a viable alternative PET radionuclide for radiolabeling purposes (<a id="xref-ref-45-1" class="xref-bibr" href="#ref-45">45</a>-<a id="xref-ref-47-1" class="xref-bibr" href="#ref-47">47</a>). The half-life of <sup>52</sup>Mn not only allows for the <em>in vivo</em> monitoring of molecules with slower kinetics (<em>e.g.</em>, cyclodextrins in complexation with liposomes) (<a id="xref-ref-48-1" class="xref-bibr" href="#ref-48">48</a>-<a id="xref-ref-50-1" class="xref-bibr" href="#ref-50">50</a>), but it also gives enough room for transportation to distant laboratories. Furthermore, the accomplishment of longitudinal studies is also possible using <sup>52</sup>Mn for radiosynthesis. Additionally, former studies with <sup>52</sup>Mn-labelled DOTA complexes and DOTA-TRC105 (chimeric human/murine immunoglobulin G (IgG1) proved that <sup>52</sup>Mn could be a strong candidate for use in PET imaging (<a id="xref-ref-51-1" class="xref-bibr" href="#ref-51">51</a>, <a id="xref-ref-52-1" class="xref-bibr" href="#ref-52">52</a>). Considering the above, we hypothesize that cyclodextrins labelled with positron emitter <sup>52</sup>Mn may have a clear added value in the PET diagnostics of melanoma malignum.</p><p id="p-9">In the present work we assessed the <em>in vivo</em> imaging behavior of <sup>52</sup>Mn-labelled RAMEB cyclodextrin ([<sup>52</sup>Mn]Mn-DOTAGA-RAMEB) using an MC1-R positive experimental melanoma model and <em>in vivo</em> PET technique. In addition, its diagnostic performance was compared to that of melanoma specific [<sup>68</sup>Ga]Ga-DOTA-NAPamide and another tumor selective cyclodextrin-based radiotracer ([<sup>68</sup>Ga]Ga-DOTAGA-RAMEB).</p><div class="section materials-methods" id="sec-1"><h2 class="">Materials and Methods</h2><p id="p-10"><em>[<sup>52</sup>Mn]Mn-DOTAGA-RAMEB radiolabeling</em>. For radiolabeling, <sup>52</sup>Mn in 0.1 M HCl solution (V=100 μl) was mixed with 2 M sodium-acetate buffer (V=500 μl) to adjust the pH to the required 7.0. Thereafter, DOTAGA-RAMEB (c=3 mM, V=10 μl) was added to the reaction mixture in a reaction vial, which was heated at 95°C for 10 min and cooled to ambient temperature for 5 min.</p><p id="p-11">For the formulation, the solution was dropped to a Light C18 Sep-Pak Cartridge (Waters Ltd. Budapest, Hungary) and washed with 1 ml of water. The radiolabeled product ([<sup>52</sup>Mn]Mn-DOTAGA-RAMEB) was eluted with 300 μl of 96% EtOH. The entire eluate was evaporated to near dryness at 95°C with nitrogen flow and redissolved in isotonic NaCl solution.</p><p id="p-12">Instant thin layer chromatography (iTLC-SG, Varian) was performed using sodium citrate 0.5 M, pH 5.5 as a mobile phase to determine the yield of radiolabeling. Three μl of the formulated product ([<sup>52</sup>Mn]Mn-DOTAGA-RAMEB) was deposited on iTLC-SG strips at 2 cm of the bottom and the solvent was allowed to rise to 10 cm from the bottom of the strips. The radiolabeled RAMEB remained at the application point, while free <sup>52</sup>Mn migrated with the solvent front. The strips were then analyzed using the MiniGITAa* TLC scanning device (Elysia-raytest GmbH, Straubenhardt, Germany). The radiolabeled product was sterile filtered and diluted with isotonic (0.9%) saline solution before the accomplishment of the biological experiments.</p><p id="p-13"><em>Determination of the partition coefficient (LogP)</em>. The determination of the partition coefficient (<em>LogP values</em>) of <sup>52</sup>Mn labelled DOTAGA-RAMEB was performed in a separate experiment. [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB (10 μl, 4.8±0.3 MBq) was diluted to 500 μl with PBS solution (pH=7.4), and after that, 1-octanol (V=500 μl) was added to the reaction mixture under continuous stirring. Thereafter, it was stirred at room temperature for 20 min and then centrifuged at 22,400×<em>g</em>/min for 5 min at 4°C to achieve the complete separation of the layers. Samples (V=100 μl) were pipetted from the separated layers into test tubes, and this was followed by the measurement of the radioactivity of these aliquots using a high-performance calibrated gamma counter (Perkin-Elmer Packard Cobra, Waltham, MA, USA). All experiments were performed in triplicate.</p><p id="p-14"><em>Determination of in vitro and in vivo metabolic stability</em>. Mouse serum was used to test the <em>in vitro</em> stability of the novel radiotracer. Following the addition of [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB (10.0±0.5 MBq) into mouse serum, the reaction mixture was incubated at 37°C without stirring. Samples (V=50 μl) taken from this mixture at different time points (30, 60, 90, and 240 min) were mixed with ice-cold abs. ethanol (V=50 μl) and centrifuged at 10,000 rpm for 5 min at 4°C. The supernatant was then collected, diluted with water and evaluated with iTLC.</p><p id="p-15">To determine <em>in vivo</em> metabolic stability, 12-week-old healthy C57BL/6J mice were used. Sixty min after the intravenous administration of 7.5±0.4 MBq [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB into the study mice <em>via</em> the lateral tail vein, urine samples were collected. Thereafter, ice-cold absolute ethanol (50 μl) was added to the obtained urine samples (50 μl) and centrifuged at 5,600×<em>g</em> for 5 min. As previously, iTLC was used for the evaluation of all supernatants. As part of both metabolic stability investigations, the iTLC chromatograms were compared to the initial chromatograms of the intact radiotracer to detect the presence of any new radio-metabolite forms.</p><p id="p-16"><em>Cell lines</em>. Mouse B16F10 (MC1-R positive) melanoma cell lines were obtained from American Type Culture Collection (ATCC, Manassas, VA, USA). The cells were cultured in Dulbecco’s Modified Eagle’s medium (DMEM, Merck Life Science Ltd., Budapest, Hungary) supplemented with 1% (v/v) MEM Non Essential Amino Acid solution (Merck Life Science Ltd.), 1% MEM Vitamins solution (Merck Life Science Ltd.), 10% Fetal Bovine Serum (FBS, GIBCO Life Technologies, Billings, MT, USA) and 1% Antibiotic and Antimicotic solution (Merck Life Science Ltd.). Humidified atmosphere containing 5% CO<sub>2</sub> and a temperature of 37°C were ensured for cell culturing. Cells were used at 85% confluence for <em>in vivo</em> studies. Viability was assessed using trypan blue staining, and only cells with viability higher than 90% were subjected to further procedures.</p><p id="p-17"><em>Animal housing, tumor induction</em>. Twelve-week-old female C57BL/6J (n=5) mice purchased from Charles River Laboratories (Animalab Ltd., Budapest, Hungary) were used in the present study. All mice lived in a facility with 12 h light–dark cycle under sterile conditions in Individually Ventilated Cages (5/cage, Techniplast, Akronom Ltd., Budapest, Hungary) with free access to sterile semi-synthetic food (Akronom Ltd.) and sterile water. An ambient temperature of 26±2°C and relative humidity of 55±10% was maintained in the housing facility. The laboratory animals were kept and treated in accordance with all applicable sections of the Hungarian Laws and regulations of the European Union. The Ethics Committee for Animal Experimentation of the University of Debrecen, (Debrecen, Hungary) approved this study (study number: 28/2023/DEMÁB).</p><p id="p-18">B16F10 mouse melanoma cells (3×10<sup>6</sup> in 100 μl NaCl) were subcutaneously (<em>sc</em>.) injected into the left shoulder area of 12-week-old C57BL/6J mice (n=5) to generate MC1-R positive melanoma tumors. The tumors were allowed to grow for 8±1 days before microPET imaging and post imaging biodistribution studies.</p><p id="p-19"><em>In vivo imaging and analyses</em>. PET imaging sessions were accomplished using the MiniPET-II scanner of the preclinical laboratory of the Division of Nuclear Medicine and Translational Imaging (University of Debrecen, Debrecen, Hungary).</p><p id="p-20">We commenced the imaging protocol with the intravenous (<em>iv</em>.) injection of B16F10 tumor-bearing mice with 6.90±1.19 MBq of [<sup>68</sup>Ga]Ga-DOTAGA-RAMEB that was followed by PET imaging 60 min after the injection. Twenty-four hours after the first acquisition, 20-min PET scans were acquired on all study mice 80 min post <em>iv</em>. administration of 10.07±0.07 MBq of [<sup>68</sup>Ga]Ga-DOTA-NAPamide. A day later, we finally injected the mice with 3.50±0.16 MBq of [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB and 1 h, 4 h, and 3 days post injection, 20-min static PET scans were acquired. Isoflurane-induced anesthesia was maintained throughout all imaging periods [3% isoflurane (Forane), AbbVie, Budapest, Hungary; OGYI-T-1414/01]. All PET scans were assessed using the BrainCad image analysis software (Version: 1.124). Following image reconstruction, regions of interests (ROIs) over the tumors and the major tissues/organs on the coronal images were carefully delineated, and radioactivity concentrations in the ROIs were determined and presented as SUVmean and SUVmax. T/M SUVmean and T/M SUVmax were also recorded from the activity of the tumors and the background muscle tissue.</p><p id="p-21"><em>Biodistribution</em>. For biodistribution studies, 30, 60, 90, and 240 min after the <em>iv</em>. administration of 3.50±0.16 MBq [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB B16F10 healthy control mice were sacrificed and the major organs were harvested to determine their radioactivity using a calibrated gamma counter (PerkinElmer). To measure the <em>ex vivo</em> uptake of the B16F10 tumors, tumor-bearing mice underwent the same process 60 min post-injection. We expressed the decay-corrected radioactivity concentrations as the percentage of injected dose per gram of tissue (% ID/g). Data are presented as mean±standard deviation (SD).</p><p id="p-22"><em>Statistical analyses</em>. MedCalc 18.5 (MedCalc Software, Mariakerke, Belgium) software package was used for statistical analyses, and all statistical data are displayed as mean±SD. Mann-Whitney <em>U</em>-test, student’s two-tailed <em>t</em>-test, and two-way ANOVA were applied to evaluate statistical significance, with a <em>p</em>-value of less than 0.05 being considered statistically significant.</p></div><div class="section results" id="sec-2"><h2 class="">Results</h2><p id="p-23"><em>Radiolabeling</em>. The radiolabeling of DOTAGA-RAMEB precursor was performed manually (<a id="xref-fig-1-1" class="xref-fig" href="#F1">Figure 1</a>). The total time needed for the whole radiolabeling process was approximately 25 min. Our quality control applying iTLC chromatography identified >99% radiochemical purity (RCP) for the novel [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB radiopharmaceutical.</p><div id="F1" class="fig pos-float odd"><div class="highwire-figure"><div class="fig-inline-img-wrapper"><div class="fig-inline-img"><a href="https://iv.iiarjournals.org/content/invivo/38/6/2591/F1.large.jpg?width=800&height=600&carousel=1" title="Schematic representation of the radiolabeling of precursor DOTAGA-RAMEB with Manganese-52 (52Mn)." class="highwire-fragment fragment-images colorbox-load" rel="gallery-fragment-images-116935362" data-figure-caption="<div class="highwire-markup"><div xmlns="http://www.w3.org/1999/xhtml">Schematic representation of the radiolabeling of precursor DOTAGA-RAMEB with Manganese-52 (<sup>52</sup>Mn).</div></div>" data-icon-position="" data-hide-link-title="0"><span class="hw-responsive-img"><img class="highwire-fragment fragment-image lazyload" alt="Figure 1." src="data:image/gif;base64,R0lGODlhAQABAIAAAAAAAP///yH5BAEAAAAALAAAAAABAAEAAAIBRAA7" data-src="https://iv.iiarjournals.org/content/invivo/38/6/2591/F1.medium.gif" width="440" height="191"/><noscript><img class="highwire-fragment fragment-image" alt="Figure 1." src="https://iv.iiarjournals.org/content/invivo/38/6/2591/F1.medium.gif" width="440" height="191"/></noscript></span></a></div></div><ul class="highwire-figure-links inline"><li class="download-fig first"><a href="https://iv.iiarjournals.org/content/invivo/38/6/2591/F1.large.jpg?download=true" class="highwire-figure-link highwire-figure-link-download" title="Download Figure 1." data-icon-position="" data-hide-link-title="0">Download figure</a></li><li class="new-tab"><a href="https://iv.iiarjournals.org/content/invivo/38/6/2591/F1.large.jpg" class="highwire-figure-link highwire-figure-link-newtab" target="_blank" data-icon-position="" data-hide-link-title="0">Open in new tab</a></li><li class="download-ppt last"><a href="/highwire/powerpoint/24933" class="highwire-figure-link highwire-figure-link-ppt" data-icon-position="" data-hide-link-title="0">Download powerpoint</a></li></ul></div><div class="fig-caption" xmlns:xhtml="http://www.w3.org/1999/xhtml"><span class="fig-label">Figure 1.</span> <p id="p-24" class="first-child">Schematic representation of the radiolabeling of precursor DOTAGA-RAMEB with Manganese-52 (<sup>52</sup>Mn).</p><div class="sb-div caption-clear"></div></div></div><p id="p-25"><em>LogP and stability</em>. The LogP value of [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB was determined to be −2.873, that indicates the highly hydrophilic character of the radiopharmaceutical. Analyzing the <em>in vitro</em> stability of the newly constructed probe in mouse serum with iTLC at 30-, 60-, 90-, and 240-min measurement points, we observed that the [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB product remained stable during the whole investigation period. In addition, the RCP of the radiotracer was over 97% even at the 240-min time point. Urine samples of C57BL/6J mice taken 60 min after [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB injection were used for <em>in vivo</em> stability measurements. The iTLC chromatograms showed that the radiotracer remained stable, and no measurable amount of a metabolite could be detected, that confirms outstanding <em>in vivo</em> metabolic stability.</p><p id="p-26"><em>In vivo PET imaging of B16F10 melanoma tumors</em>. Representative decay-corrected PET scans are displayed in <a id="xref-fig-2-1" class="xref-fig" href="#F2">Figure 2</a>. Visually, all compounds performed well in the identification of B16F10 melanoma tumors, but the tumors were most clearly visible with the administration of [<sup>68</sup>Ga]Ga-DOTA-NAPamide. We noted less intense uptake for the cyclodextrin derivatives, in particular for the delayed time points of the <sup>52</sup>Mn-labelled probe. Of note, heterogenous tumor uptake pattern was detected 1 h post-injection of [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB, while the accumulation of the other two radiopharmaceuticals showed homogenous distribution in the examined tumors. As with all radiopharmaceuticals, notable tracer accumulation was observed in the kidneys and urinary bladder. Regarding other healthy abdominal and thoracic organs, no radioactivity was observed.</p><div id="F2" class="fig pos-float odd"><div class="highwire-figure"><div class="fig-inline-img-wrapper"><div class="fig-inline-img"><a href="https://iv.iiarjournals.org/content/invivo/38/6/2591/F2.large.jpg?width=800&height=600&carousel=1" title="In vivo evaluation of Melanocortin-1 receptor (MC1-R) positive B16F10 melanoma tumors with [68Ga]Ga-DOTAGA-RAMEB (Panel A), [68Ga]Ga-DOTA-NAPamide (Panel B), and [52Mn]Mn-DOTAGA-RAMEB (Panel C) positron emission tomography (PET) imaging. Representative decay-corrected coronal (upper row) and transaxial (lower row) PET images demonstrate the melanoma tumor uptake after the intravenous injection of the tracers. Red arrows indicate the subcutaneously growing B16F10 melanoma tumors. Black arrow (Panel A) points to the left kidney. p.i.: Post-injection; SUV: standardizes uptake value." class="highwire-fragment fragment-images colorbox-load" rel="gallery-fragment-images-116935362" data-figure-caption="<div class="highwire-markup"><div xmlns="http://www.w3.org/1999/xhtml">In vivo evaluation of Melanocortin-1 receptor (MC1-R) positive B16F10 melanoma tumors with [<sup>68</sup>Ga]Ga-DOTAGA-RAMEB (Panel A), [<sup>68</sup>Ga]Ga-DOTA-NAPamide (Panel B), and [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB (Panel C) positron emission tomography (PET) imaging. Representative decay-corrected coronal (upper row) and transaxial (lower row) PET images demonstrate the melanoma tumor uptake after the intravenous injection of the tracers. Red arrows indicate the subcutaneously growing B16F10 melanoma tumors. Black arrow (Panel A) points to the left kidney. p.i.: Post-injection; SUV: standardizes uptake value.</div></div>" data-icon-position="" data-hide-link-title="0"><span class="hw-responsive-img"><img class="highwire-fragment fragment-image lazyload" alt="Figure 2." src="data:image/gif;base64,R0lGODlhAQABAIAAAAAAAP///yH5BAEAAAAALAAAAAABAAEAAAIBRAA7" data-src="https://iv.iiarjournals.org/content/invivo/38/6/2591/F2.medium.gif" width="440" height="196"/><noscript><img class="highwire-fragment fragment-image" alt="Figure 2." src="https://iv.iiarjournals.org/content/invivo/38/6/2591/F2.medium.gif" width="440" height="196"/></noscript></span></a></div></div><ul class="highwire-figure-links inline"><li class="download-fig first"><a href="https://iv.iiarjournals.org/content/invivo/38/6/2591/F2.large.jpg?download=true" class="highwire-figure-link highwire-figure-link-download" title="Download Figure 2." data-icon-position="" data-hide-link-title="0">Download figure</a></li><li class="new-tab"><a href="https://iv.iiarjournals.org/content/invivo/38/6/2591/F2.large.jpg" class="highwire-figure-link highwire-figure-link-newtab" target="_blank" data-icon-position="" data-hide-link-title="0">Open in new tab</a></li><li class="download-ppt last"><a href="/highwire/powerpoint/24593" class="highwire-figure-link highwire-figure-link-ppt" data-icon-position="" data-hide-link-title="0">Download powerpoint</a></li></ul></div><div class="fig-caption"><span class="fig-label">Figure 2.</span> <p id="p-27" class="first-child">In vivo evaluation of Melanocortin-1 receptor (MC1-R) positive B16F10 melanoma tumors with [<sup>68</sup>Ga]Ga-DOTAGA-RAMEB (Panel A), [<sup>68</sup>Ga]Ga-DOTA-NAPamide (Panel B), and [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB (Panel C) positron emission tomography (PET) imaging. Representative decay-corrected coronal (upper row) and transaxial (lower row) PET images demonstrate the melanoma tumor uptake after the intravenous injection of the tracers. Red arrows indicate the subcutaneously growing B16F10 melanoma tumors. Black arrow (Panel A) points to the left kidney. p.i.: Post-injection; SUV: standardizes uptake value.</p><div class="sb-div caption-clear"></div></div></div><p id="p-28">The visual observations were strengthened by quantitative PET data assessment. The standardized uptake values (SUV) values and the tumor-to-muscle (T/M) ratios for the tracers in MC1-R positive B16F10 tumors are given in <a id="xref-table-wrap-1-1" class="xref-table" href="#T1">Table I</a>. Comparing the three imaging probes, the SUVmean and SUVmax values were the highest for the NAPamide derivative (SUVmean and SUVmax were 0.37±0.07 and 0.56±0.09, respectively) that significantly differed from those of both labelled cyclodextrin molecules (<em>p</em>≤0.01, <a id="xref-table-wrap-1-2" class="xref-table" href="#T1">Table I</a>). The second highest tumor retention was found for the [<sup>68</sup>Ga]Ga-DOTAGA-RAMEB scans (SUVmean: 0.16±0.04; SUVmax: 0.24±0.05), while [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB showed the least radioconcentrations. Although the B16F10 tumors were clearly visible with the <sup>52</sup>Mn-cyclodextrin with peak SUV values 1 h post-injection (SUVmean and SUVmax were 0.6±0.01 and 0.09±0.02, respectively), at later time points hardly any activity was detected (At 4 h, SUVmean and SUVmax were 0.02±0.01 and 0.03±0.01, respectively and at 3 d 0.01±0.01 and 0.01±0.01, respectively). In addition, quantitative PET data revealed significant differences between the tracer uptake values of the two cyclodextrin probes <em>(p</em>≤0.01<em>)</em> and the accretion of the <sup>52</sup>Mn-labelled compound measured at the different investigation time points (<em>p</em>≤0.01 and <em>p</em>≤0.05). Compared to all uptake values of [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB (1 h, 4 h, and 3 d), the <sup>68</sup>Ga-labelled cyclodextrin molecule displayed considerably higher radioactivity in the B16F10 tumors (<em>p</em>≤0.01). The highest SUVmean and SUVmax data for [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB registered 1 h post-injection significantly differed from the 4 h and 3 d SUV values with a <em>p</em>≤0.01. Although the SUVmean figures of the later time points (4 h and 3 d) were comparable (<em>p</em>≤0.01), at lower significance level (<em>p</em>≤0.05), we recorded notable difference between their SUVmax values.</p><div id="T1" class="table pos-float"><div class="table-inline table-callout-links"><div class="callout"><span>View this table:</span><ul class="callout-links"><li class="view-inline first"><a href="" class="table-expand-inline" data-table-url="/highwire/markup/24924/expansion?postprocessors=highwire_tables%2Chighwire_reclass%2Chighwire_figures%2Chighwire_math%2Chighwire_inline_linked_media%2Chighwire_embed&table-expand-inline=1" data-icon-position="" data-hide-link-title="0">View inline</a></li><li class="view-popup"><a href="/highwire/markup/24924/expansion?width=1000&height=500&iframe=true&postprocessors=highwire_tables%2Chighwire_reclass%2Chighwire_figures%2Chighwire_math%2Chighwire_inline_linked_media%2Chighwire_embed" class="colorbox colorbox-load table-expand-popup" rel="gallery-fragment-tables" data-icon-position="" data-hide-link-title="0">View popup</a></li><li class="download-ppt last"><a href="/highwire/powerpoint/24924" class="highwire-figure-link highwire-figure-link-ppt" data-icon-position="" data-hide-link-title="0">Download powerpoint</a></li></ul></div></div><div class="table-caption"><span class="table-label">Table I.</span> <p id="p-29" class="first-child">In vivo quantitative PET data analyses of [<sup>68</sup>Ga]Ga-DOTAGA-RAMEB, [<sup>68</sup>Ga]Ga-DOTA-NAPamide and [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB in the subcutaneously growing B16F10 tumors. Radiotracer accumulation is expressed in SUV values. Data are presented as mean±SD, n=3 mice/PET probe/time point. PET: Positron emission tomography; SUV: standardized uptake value; SD: standard deviation; T/M: tumor-to muscle ratio.</p><div class="sb-div caption-clear"></div></div></div><p id="p-30">As shown in <a id="xref-table-wrap-1-3" class="xref-table" href="#T1">Table I</a>, mean tumor-to-background ratios were significantly different between [<sup>68</sup>Ga]Ga-DOTA-NAPamide and the radiolabeled cyclodextrin probes (<em>p</em>≤0.01), with maximum values of 9.25±1.07 for the MC1-R targeting NAPamide. Comparing the mean tumor-to-contrast ratios of the two cyclodextrin radiopharmaceuticals, higher 1 h mean value was recorded for the <sup>52</sup>Mn-cyclodextrin (T/M SUVmean: 5.34±1.07) than for the <sup>68</sup>Ga-labelled one (T/M SUVmean: 4.03±0.44); however, it was statistically not significant. On the contrary, compared to the 4 h (T/M SUVmean: 2.04±0.37) and 3 d (T/M SUVmean: 1.04±0.03) ratios of the <sup>52</sup>Mn-compound, the values for [<sup>68</sup>Ga]Ga-DOTAGA-RAMEB were notably more elevated (<em>p</em>≤0.01). The 1 h mean T/M values of the newly synthesized [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB were as high as 5.34±1.07 and were reduced over time to 1.04±0.03 (3 d). Although, this considerably differed from the ratios measured at later imaging time points (<em>p</em>≤0.01; T/M SUVmean 2.04±0.37 and 1.04±0.03 at 4 h and 3 d after the injection, respectively), a significant difference was only detected between the two later time points at <em>p</em>=0.05.</p><p id="p-31">Similar trend was found for the maximum T/M ratios of the investigated tracers, however, contrasting the mean T/M data, the <sup>52</sup>Mn-cyclodextrin molecule presented similar maximum tumor-to-off target ratio at later acquisition times without any significance even at <em>p</em>≤0.05 (the 4 h SUVmean and SUVmax were 2.04±0.37 and 1.50±0.24, respectively; the 3 d SUVmean and SUVmax were 1.04±0.03 and: 1.02±0.02, respectively). Calculated tumor-to-muscle ratios are presented in <a id="xref-table-wrap-1-4" class="xref-table" href="#T1">Table I</a>.</p><p id="p-32"><em>Ex vivo biodistribution studies in healthy control and B16F10 melanoma tumor-bearing mice</em>. The biodistribution of the novel [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB is demonstrated in <a id="xref-fig-3-1" class="xref-fig" href="#F3">Figure 3</a> and <a id="xref-table-wrap-2-1" class="xref-table" href="#T2">Table II</a>. To determine the radioactivity pattern of [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB <em>ex vivo</em>, organ distribution data were gathered using a high-performance calibrated gamma-counter 30, 60, 90, and 240 min after the intravenous injection of the <sup>52</sup>Mn-labelled cyclodextrin into the lateral tail vein of healthy control mice. As seen in <a id="xref-fig-3-2" class="xref-fig" href="#F3">Figure 3</a> and <a id="xref-table-wrap-2-2" class="xref-table" href="#T2">Table II</a> the highest tracer accumulation was registered 30 min post administration for all control organs and tissues. Even though the 30-min <em>ex vivo</em> data significantly differed from those of the other investigation time points (60, 90, and 240 min; <em>p</em>≤0.01<em>)</em>, no meaningful distinctions were found between the %ID/g values measured 60-, 90-, and 240-min post tracer injection. Generally, the radioactivity concentration of the investigated healthy tissues/organs gradually decreased over time (<a id="xref-fig-3-3" class="xref-fig" href="#F3">Figure 3</a> and <a id="xref-table-wrap-2-3" class="xref-table" href="#T2">Table II</a>).</p><div id="F3" class="fig pos-float odd"><div class="highwire-figure"><div class="fig-inline-img-wrapper"><div class="fig-inline-img"><a href="https://iv.iiarjournals.org/content/invivo/38/6/2591/F3.large.jpg?width=800&height=600&carousel=1" title="ITime-dependent ex vivo biodistribution of [52Mn]Mn-DOTAGA-RAMEB in healthy control mice. Significance level between the 30-min data and the three other investigated time points: p≤0.01 (*). Followed by autopsy, the radioactivity pattern was investigated 30, 60, 90, and 240 min after the intravenous injection of 3.50±0.16 MBq of [52Mn]Mn-DOTAGA-RAMEB (n=3 animals/time point). The uptake values are expressed as mean %ID/g±SD." class="highwire-fragment fragment-images colorbox-load" rel="gallery-fragment-images-116935362" data-figure-caption="<div class="highwire-markup"><div xmlns="http://www.w3.org/1999/xhtml">ITime-dependent ex vivo biodistribution of [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB in healthy control mice. Significance level between the 30-min data and the three other investigated time points: p≤0.01 (*). Followed by autopsy, the radioactivity pattern was investigated 30, 60, 90, and 240 min after the intravenous injection of 3.50±0.16 MBq of [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB (n=3 animals/time point). The uptake values are expressed as mean %ID/g±SD.</div></div>" data-icon-position="" data-hide-link-title="0"><span class="hw-responsive-img"><img class="highwire-fragment fragment-image lazyload" alt="Figure 3." src="data:image/gif;base64,R0lGODlhAQABAIAAAAAAAP///yH5BAEAAAAALAAAAAABAAEAAAIBRAA7" data-src="https://iv.iiarjournals.org/content/invivo/38/6/2591/F3.medium.gif" width="440" height="288"/><noscript><img class="highwire-fragment fragment-image" alt="Figure 3." src="https://iv.iiarjournals.org/content/invivo/38/6/2591/F3.medium.gif" width="440" height="288"/></noscript></span></a></div></div><ul class="highwire-figure-links inline"><li class="download-fig first"><a href="https://iv.iiarjournals.org/content/invivo/38/6/2591/F3.large.jpg?download=true" class="highwire-figure-link highwire-figure-link-download" title="Download Figure 3." data-icon-position="" data-hide-link-title="0">Download figure</a></li><li class="new-tab"><a href="https://iv.iiarjournals.org/content/invivo/38/6/2591/F3.large.jpg" class="highwire-figure-link highwire-figure-link-newtab" target="_blank" data-icon-position="" data-hide-link-title="0">Open in new tab</a></li><li class="download-ppt last"><a href="/highwire/powerpoint/24936" class="highwire-figure-link highwire-figure-link-ppt" data-icon-position="" data-hide-link-title="0">Download powerpoint</a></li></ul></div><div class="fig-caption"><span class="fig-label">Figure 3.</span> <p id="p-33" class="first-child">ITime-dependent ex vivo biodistribution of [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB in healthy control mice. Significance level between the 30-min data and the three other investigated time points: p≤0.01 (*). Followed by autopsy, the radioactivity pattern was investigated 30, 60, 90, and 240 min after the intravenous injection of 3.50±0.16 MBq of [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB (n=3 animals/time point). The uptake values are expressed as mean %ID/g±SD.</p><div class="sb-div caption-clear"></div></div></div><div id="T2" class="table pos-float"><div class="table-inline table-callout-links"><div class="callout"><span>View this table:</span><ul class="callout-links"><li class="view-inline first"><a href="" class="table-expand-inline" data-table-url="/highwire/markup/24826/expansion?postprocessors=highwire_tables%2Chighwire_reclass%2Chighwire_figures%2Chighwire_math%2Chighwire_inline_linked_media%2Chighwire_embed&table-expand-inline=1" data-icon-position="" data-hide-link-title="0">View inline</a></li><li class="view-popup"><a href="/highwire/markup/24826/expansion?width=1000&height=500&iframe=true&postprocessors=highwire_tables%2Chighwire_reclass%2Chighwire_figures%2Chighwire_math%2Chighwire_inline_linked_media%2Chighwire_embed" class="colorbox colorbox-load table-expand-popup" rel="gallery-fragment-tables" data-icon-position="" data-hide-link-title="0">View popup</a></li><li class="download-ppt last"><a href="/highwire/powerpoint/24826" class="highwire-figure-link highwire-figure-link-ppt" data-icon-position="" data-hide-link-title="0">Download powerpoint</a></li></ul></div></div><div class="table-caption"><span class="table-label">Table II.</span> <p id="p-34" class="first-child">Ex vivo biodistribution data (%ID/g) of [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB in healthy control mice (n=3 animals/time point). The accumulated activities of the extracted organs/tissues were determined using a calibrated gamma counter 30, 60, 90, and 240 min after the intravenous injection of 3.50±0.16 MBq of [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB. *Significance between the 30-min data and the three other investigation time points, p≤0.01. Data are presented as mean±SD. SD: Standard deviation.</p><div class="sb-div caption-clear"></div></div></div><p id="p-35">Among all organs, the highest tracer retention was detected in the liver and the kidneys at all measurement points with the highest uptake values being 7.12±0.85 and 6.62±2.25 %ID/g for the liver and the kidneys, respectively, 30 min post radiotracer injection. Furthermore, the relatively high 30-min radioactivity of the blood (%ID/g: 1.30±0.44) and the lungs (%ID/g: 1.22±0.41) showed a sharp decline until the end of the experiment.</p><p id="p-36">The most suitable time point for the <em>ex vivo</em> determination of intratumoral [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB uptake was selected on the basis of the <em>in vivo</em> PET analyses. Since both the tumor SUV values and the tumor-to-background ratio were the highest 60 min after the administration of the radiotracer, we performed <em>ex vivo</em> measurements with B16F10 tumor-bearing mice at the same investigation time point. Apart from the liver and the kidneys, significantly higher %ID/g values were registered for the tumors (0.82±0.09) in comparison with all investigated organs/tissues (<em>p</em>≤0.01). <em>Ex vivo</em> T/M ratios (3.91±0.12) were comparable to those of the <em>in vivo</em> data.</p></div><div class="section discussion" id="sec-3"><h2 class="">Discussion</h2><p id="p-37"><em>In vivo PET imaging</em>. Considering melanoma-associated high mortality and poor outcomes, early disease diagnostics using PET imaging and tumor-selective radioactive probes is in the forefront of current research. Due to its suitable physics and long biological half-life, <sup>52</sup>Mn has recently gained widespread interest in nuclear medical fields as a potential isotope to develop PET radiopharmaceuticals for oncological imaging (<a id="xref-ref-53-1" class="xref-bibr" href="#ref-53">53</a>, <a id="xref-ref-54-1" class="xref-bibr" href="#ref-54">54</a>). With a half-life of 5.56 days, the isotope facilitates the linkage of larger molecules or those with extended pharmacokinetics, allowing for longer acquisition times (<a id="xref-ref-55-1" class="xref-bibr" href="#ref-55">55</a>). To date, several <sup>52</sup>Mn PET tracers including [<sup>52</sup>Mn]Mn-PyC3A, [<sup>52</sup>Mn]Mn-DOTABA-bevacizumab or [<sup>52</sup>Mn]Mn-BPPA-trastuzumab have been successfully used in preclinical studies (<a id="xref-ref-45-2" class="xref-bibr" href="#ref-45">45</a>, <a id="xref-ref-56-1" class="xref-bibr" href="#ref-56">56</a>, <a id="xref-ref-57-1" class="xref-bibr" href="#ref-57">57</a>). Hence, we evaluated the <em>in vivo</em> diagnostic capability of the novel <sup>52</sup>Mn-labelled RAMEB cyclodextrin in MC1-R positive melanoma models and compared it with other well-stablished tumor-specific PET radiopharmaceuticals used in melanoma PET imaging ([<sup>68</sup>Ga]Ga-DOTA-NAPamide and [<sup>68</sup>Ga]Ga-DOTAGA-RAMEB).</p><p id="p-38">In line with former literature findings, notable [<sup>68</sup>Ga]Ga-DOTA-NAPamide accumulation was found in our MC1-R positive B16F10 melanoma tumors (<a id="xref-fig-2-2" class="xref-fig" href="#F2">Figure 2</a>) that strengthened the receptor specificity and the diagnostic potential of the radiotracer in the imaging of melanoma tumors with high MC1-R expression (<a id="xref-ref-22-1" class="xref-bibr" href="#ref-22">22</a>-<a id="xref-ref-24-2" class="xref-bibr" href="#ref-24">24</a>, <a id="xref-ref-28-2" class="xref-bibr" href="#ref-28">28</a>). In previous PET/MRI studies with the same preclinical model systems, [<sup>68</sup>Ga]Ga-DOTA-NAPamide also showed MC1-R selectivity and outstanding tumor targeting capability (<a id="xref-ref-24-3" class="xref-bibr" href="#ref-24">24</a>, <a id="xref-ref-28-3" class="xref-bibr" href="#ref-28">28</a>). In addition, radionuclides other than <sup>68</sup>Ga including Copper-64/61, Fluorine-18, Bismuth-213 or Scandium-44 could be similarly used for the radiolabeling of MC1-R-affine NAPamide compounds, as well as for melanoma detection (<a id="xref-ref-22-2" class="xref-bibr" href="#ref-22">22</a>-<a id="xref-ref-24-4" class="xref-bibr" href="#ref-24">24</a>, <a id="xref-ref-26-1" class="xref-bibr" href="#ref-26">26</a>, <a id="xref-ref-28-4" class="xref-bibr" href="#ref-28">28</a>, <a id="xref-ref-58-1" class="xref-bibr" href="#ref-58">58</a>). Likewise, alternative alpha-MSH analogues (HOLDamide, FOLDamide, MARSamide) labelled with Bismuth-213 are considered as promising vector candidates for diagnostic purposes in malignant melanoma (<a id="xref-ref-24-5" class="xref-bibr" href="#ref-24">24</a>, <a id="xref-ref-26-2" class="xref-bibr" href="#ref-26">26</a>).</p><p id="p-39">Besides the NAPamide derivative, the <em>in vivo</em> results pointed out that the <em>sc</em>. growing tumors could be clearly delineated with both the <sup>68</sup>Ga and the <sup>52</sup>Mn-labelled cyclodextrin molecules. This demonstrates the potential applicability of the investigated probes in the <em>in vivo</em> PET imaging of malignant melanoma. Furthermore, given the high affinity of RAMEB cyclodextrin to complex with PGE2 receptors, our observation may also indicate the PGE2 positivity of the investigated neoplasms. Although the receptor profile of B16F10 tumors still remains to be fully uncovered, earlier immunohistochemical results reported strong PGE2 positivity for such tumor types (<a id="xref-ref-41-2" class="xref-bibr" href="#ref-41">41</a>). In addition, the findings of Kim <em>et al.</em> on B16F10 cells indicating reduced PGE2 and EP receptor levels in association with timosaponin AIII administration also suggest the presence of PGE2 and its receptors on melanoma tumor cells (<a id="xref-ref-59-1" class="xref-bibr" href="#ref-59">59</a>). Although the PGE2 expression of the examined melanoma tumors may suggest an association with the accumulation of the radiolabeled cyclodextrins, further research is needed to explore the relationship between radiotracer uptake and the receptor expression of melanoma tumors.</p><p id="p-40">In line with the present results, Szabó <em>et al.</em> also showed meaningful tumor uptake for <sup>68</sup>Ga-labelled cyclodextrin derivatives ([<sup>68</sup>Ga]Ga-NODAGA-RAMEB and [<sup>68</sup>Ga]Ga-NODAGA-HPβCD) in a proof-of-concept study with experimental melanoma models (<a id="xref-ref-41-3" class="xref-bibr" href="#ref-41">41</a>). Comparable accumulation of <sup>52</sup>Mn-labelled RAMEB in the B16F10 tumors measured 1 h post-injection to that of [<sup>68</sup>Ga]Ga-NODAGA-RAMEB (<a id="xref-ref-41-4" class="xref-bibr" href="#ref-41">41</a>) indicates that the type of the labelling radionuclide does not influence the tumor-homing ability of the cyclodextrin probes ([<sup>52</sup>Mn]Mn-DOTAGA-RAMEB: 0.06±0.01 and 0.09±0.02 for SUVmean and SUVmax, respectively; [<sup>68</sup>Ga]Ga-NODAGA-RAMEB SUVmean: 0.06±0.02 and SUVmax: 0.10±0.03). Nevertheless, we registered significantly higher tumor uptake for the [<sup>68</sup>Ga]Ga-DOTAGA-RAMEB scans (SUVmean: 0.16±0.04; SUVmax: 0.24±0.05) relative to the PET images with the NODAGA-chelated counterpart [[<sup>68</sup>Ga]Ga-NODAGA-RAMEB SUVmean: 0.06±0.02; SUVmax: 0.10±0.03; (<a id="xref-ref-41-5" class="xref-bibr" href="#ref-41">41</a>)], which could possibly be attributed to structural variations or the distinct stability of the applied chelators (NODAGA <em>vs</em>. DOTAGA). Despite these discrete differences between the SUV values, we may conclude that the change of the linker (NODAGA to DOTAGA) does not have a meaningful impact on the tumor-targeting of the cyclodextrin-based vectors.</p><p id="p-41">We suppose that significantly lower [<sup>52</sup>Mn]Mn-DOATAGA-RAMEB accumulation at later acquisition time points could be associated with temporal changes in the expression of tumor cell surface receptors during tumor growth and development (0.02±0.01 and 0.03±0.01 SUVmean and SUVmax; respectively, at 4 h and 0.01±0.01 and 0.01±0.01 SUVmean and SUVmax, respectively, at 3 d). Changes in PGE2/EP2 expression, tumor-related hypoxia, and chronic inflammation could help explain the uptake kinetics of the <sup>52</sup>Mn-labeled compounds. Based on this, we suggest that follow-up imaging with <sup>52</sup>Mn-cyclodextrin may correctly represent changes in EP receptor presence and PGE2 concentration in the tumor niche. Better exploration of tumor-related biomarkers (receptors, soluble molecules) could in the long run lead to the discovery of novel candidate targets for diagnostic as well as therapeutic applications. In addition, hypoxia and necrosis especially in the central subregions could be accountable for the heterogenous distribution of [<sup>52</sup>Mn]Mn-DOATAGA-RAMEB. Even if [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB activity was notably reduced compared to the <sup>68</sup>Ga-labelled counterpart at all time points, labelling with <sup>52</sup>Mn may have some advantages over <sup>68</sup>Ga. Allowing an extended scanning time, long-lived <sup>52</sup>Mn may permit the investigation of slower tumor-associated pathophysiological processes as well as better identification of lesions that may not be visible in early time-point images. Since the fast elimination kinetics and prominent renal uptake of [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB may preclude this tracer from being used for such purposes, the improvement of its pharmacokinetics for example with the incorporation of an albumin binding moiety – may aid to extend its biological life-time and therefore its tumor retention. Moreover, [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB holds promise in the PET-based visualization of melanoma tumors that lack MC1-R.</p><p id="p-42">As previously mentioned, significant disproportions observed between the extents of the tracer uptakes of [<sup>68</sup>Ga]Ga-DOTAGA-RAMEB and [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB (<a id="xref-fig-2-3" class="xref-fig" href="#F2">Figure 2</a>) may in part also be due to alterations in PGE2 concentrations and the presence of PGE2 receptors within the tumor microenvironment. Of note, differences between the PGE2-binding affinity of the two molecules must be addressed as well. Even though both MC1-R targeting NAPamide and PGE2-selective cyclodextrins could be applicable for melanoma imaging, based on the uptake values, the NAPamide probe seems to be superior. Stronger MC1-R presence of the melanoma tumors compared to EP2 might explain the increased activity of [<sup>68</sup>Ga]Ga-DOTA-NAPamide. Additionally, the extended tumor retention of the NAPamide-based tracer may contribute to more pronounced alpha-MSH analogue uptake.</p><p id="p-43"><em>Ex vivo organ distribution</em>. In line with the <em>in vivo</em> PET results, the rapid renal clearance of [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB is evidenced by low blood activities measurements from 30 min post-injection, significant kidney uptake, and notable radioactivity in the bladder. Similarly to our findings, biodistribution data of [<sup>205/206</sup>Bi]Bi-DOTAGA-RAMEB (<a id="xref-ref-38-2" class="xref-bibr" href="#ref-38">38</a>), [<sup>68</sup>Ga]Ga-DOTAGA-RAMEB (<a id="xref-ref-38-3" class="xref-bibr" href="#ref-38">38</a>) and [<sup>68</sup>Ga]Ga-NODAGA-HPβCD (<a id="xref-ref-60-1" class="xref-bibr" href="#ref-60">60</a>) also revealed elimination through the urine. Based on the relatively high hepatic uptake we suppose the possible role of the gastrointestinal system in tracer excretion as well, however, future studies are required to provide a conclusive explanation for this observation. Corresponding to prior data with [<sup>68</sup>Ga]Ga-NODAGA-HPβCD (0.99±0.13 %ID/g) (<a id="xref-ref-60-2" class="xref-bibr" href="#ref-60">60</a>), we unexpectedly found relatively high retention in the lungs at early time points (1.22±0.41 %ID/g). Although the exact reason remains to be fully uncovered, based on the hypothesis of Hajdu <em>et al.</em> (<a id="xref-ref-60-3" class="xref-bibr" href="#ref-60">60</a>), prolonged accumulation of [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB in water-filled pulmonary areas may impede tracer re-entrance into systemic circulation that leads to increased uptake values. Consistent with the results with other radiolabeled RAMEB molecules ([<sup>68</sup>Ga]Ga-DOTAGA-RAMEB and [<sup>205/206</sup>Bi]Bi-DOTAGA-RAMEB), the rest of the examined organs/tissues showed discrete tracer accretion (<a id="xref-ref-38-4" class="xref-bibr" href="#ref-38">38</a>).</p><p id="p-44">In agreement with <em>in vivo</em> PET data, elevated tumor uptake of [<sup>52</sup>Mn]Mn-DOTAGA-RAMEB further verified the tumor-targeting ability of the probe as well as the possible presence of PGE2 and EP receptors in the tumorous microenvironment. Assessing the <em>ex vivo</em> biodistribution of B16F10 tumors, Szabó <em>et al.</em> also reported considerable accumulation for [<sup>68</sup>Ga]Ga-NODAGA-HPβCD and [<sup>68</sup>Ga]Ga-NODAGA-RAMEB, that was comparable to our results (<a id="xref-ref-41-6" class="xref-bibr" href="#ref-41">41</a>). Nevertheless, significantly lower RAMEB retention found in their experiment (0.32±0.10 %ID/g) compared to that of ours (0.82±0.09 %ID/g) could presumably be due to the fact that the <em>ex vivo</em> uptake measurements were conducted at different time points. While we discuss 60-min <em>ex vivo</em> data, <em>Szabó and colleagues</em> presented their results 90 min after injection, and we suppose that significant tracer washout between 60 and 90 min may explain the observed differences between the tracer concentrations (<a id="xref-ref-41-7" class="xref-bibr" href="#ref-41">41</a>). High tumor accumulation along with negligible background activity (except for the kidneys and the liver) resulted in optimal tumor-to-background ratios, that is of crucial importance in terms of image evaluation. Nevertheless, the identification of renal or hepatic malignancies may be hampered by the physiological high uptake of the corresponding organs. Overall, <em>ex vivo</em> data also confirmed the tumor specificity of the <sup>52</sup>Mn-labelled RAMEB and its viability in melanoma imaging. Although our pioneering findings may be encouraging, future studies focusing on pharmacokinetical optimization are required.</p></div><div class="section conclusion" id="sec-4"><h2 class="">Conclusion</h2><p id="p-45">Considering all above, we showed the diagnostic feasibility of the newly established cyclodextrin PET imaging probe labelled with <sup>52</sup>Mn using experimental melanoma tumors. Since the <sup>68</sup>Ga- and <sup>52</sup>Mn-labelled cyclodextrin PET radiopharmaceuticals are both promising agents for melanoma detection, further cyclodextrin-based molecular probes labelled with other radionuclides should be constructed and evaluated.</p></div><div class="section fn-group" id="fn-group-1"><h2>Footnotes</h2><ul><li class="fn" id="fn-2"><p id="p-2"><strong>Authors’ Contributions</strong></p><p id="p-3">Conceptualization, G.T., I.H., Z.K.; Data curation, G.O., T.S., R.E.; Investigation, J.P.S., D.Sz., I.K-Sz.; Methodology, G.T., I.H.; Validation, I.J., Z.K.; Visualization, Z.K, G.T., F.F; Writing original draft, Z.K.; Writing review & editing, T.G. All Authors have read and agreed to the published version of the manuscript.</p></li><li class="fn" id="fn-3"><p id="p-46"><strong>Funding</strong></p><p id="p-47">This research was supported by the ÚNKP-23-4-II (Z.K.) and the ÚNKP-23-5 (I.H.) New National Excellence Program of the Ministry for Culture and Innovation from the National Research, Development and Innovation Fund. Funding was received from the János Bolyai Research Scholarship of the Hungarian Academy of Sciences (bo_328_21) as well as from the KDP-2021 program of the Ministry for Innovation and Technology from the national research, development and innovation fund (Gy.T. and I. K-SZ.).</p></li><li class="fn" id="fn-4"><p id="p-48"><strong>Conflicts of Interest</strong></p><p id="p-49">The Authors declare no conflicts of interest in relation to this study.</p></li></ul></div><ul class="history-list"><li xmlns:hwp="http://schema.highwire.org/Journal" class="received" hwp:start="2024-07-04"><span class="received-label">Received </span>July 4, 2024.</li><li xmlns:hwp="http://schema.highwire.org/Journal" class="rev-recd" hwp:start="2024-07-28"><span class="rev-recd-label">Revision received </span>July 28, 2024.</li><li xmlns:hwp="http://schema.highwire.org/Journal" class="accepted" hwp:start="2024-07-29"><span class="accepted-label">Accepted </span>July 29, 2024.</li></ul><ul class="copyright-statement"><li class="fn" id="copyright-statement-1">Copyright © 2024, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved</li></ul><div class="license" id="license-1"><p id="p-4">This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (<a href="https://creativecommons.org/licenses/by-nc-nd/4.0" rel="license">https://creativecommons.org/licenses/by-nc-nd/4.0</a>).</p></div><div class="section ref-list" id="ref-list-1"><h2 class="">References</h2><ol class="cit-list"><li><a class="rev-xref-ref" href="#xref-ref-1-1" title="View reference 1 in text" id="ref-1">↵</a><div class="cit ref-cit ref-journal" id="cit-38.6.2591.1" data-doi="10.3389/fonc.2022.887366"><div class="cit-metadata"><ol class="cit-auth-list"><li><span class="cit-auth"><span class="cit-name-surname">Cabaço</span> <span class="cit-name-given-names">LC</span></span>, </li><li><span class="cit-auth"><span class="cit-name-surname">Tomás</span> <span class="cit-name-given-names">A</span></span>, </li><li><span 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class="nlm-surname">FENYVESI</span></span>, <span class="highwire-citation-author" data-delta="9"><span class="nlm-given-names">ISTVÁN</span> <span class="nlm-surname">HAJDU</span></span>, <span class="highwire-citation-author" data-delta="10"><span class="nlm-given-names">GYÖRGY</span> <span class="nlm-surname">TRENCSÉNYI</span></span></span></div> <div class="highwire-cite-metadata"><span class="highwire-cite-metadata-oa-ind highwire-cite-metadata"><i class="highwire-oa-indicator"></i> </span><span class="highwire-cite-metadata-journal highwire-cite-metadata">In Vivo </span><span class="highwire-cite-metadata-date highwire-cite-metadata">Nov 2024, </span><span class="highwire-cite-metadata-volume highwire-cite-metadata">38 </span><span class="highwire-cite-metadata-issue highwire-cite-metadata">(6) </span><span class="highwire-cite-metadata-pages highwire-cite-metadata">2591-2600; </span><span class="highwire-cite-metadata-doi highwire-cite-metadata"><span class="label">DOI:</span> 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