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Immunoliposomes for Neuroblastoma: Review of the Past Experience and Design of a Novel Nanoparticle | Anticancer Research
<!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://ar.iiarjournals.org/content/44/11/4665" /> <link rel="alternate" type="application/pdf" title="Full Text (PDF)" href="/content/44/11/4665.full.pdf" /> <link rel="alternate" type="text/plain" title="Full Text (Plain)" href="/content/44/11/4665.full.txt" /> <link rel="alternate" type="application/vnd.ms-powerpoint" title="Powerpoint" href="/content/44/11/4665.ppt" /> <meta name="issue_cover_image" content="https://ar.iiarjournals.org/sites/default/files/highwire/anticanres/44/11.cover-source.jpg" /> <meta name="type" content="article" /> <meta name="category" content="review-article" /> <meta name="HW.identifier" content="/anticanres/44/11/4665.atom" /> <meta name="HW.pisa" content="anticanres;44/11/4665" /> <meta name="DC.Format" content="text/html" /> <meta name="DC.Language" content="en" /> <meta name="DC.Title" content="Immunoliposomes for Neuroblastoma: Review of the Past Experience and Design of a Novel Nanoparticle" /> <meta name="DC.Identifier" content="10.21873/anticanres.17294" /> <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: High-risk/refractory neuro-blastoma (NBL) treatments include anti-GD2-monoclonal antibodies (mAbs). Several immunoliposomes (ILs) covered with anti-GD2-mAbs (GD2-ILs) have been tested pre-clinically. We aimed to review literature on GD2-IL for characteristics of nanoparticles/payloads, conjugation of mAb/fragments and preclinical data, as well as to explore the feasibility of a recently proposed GD2-IL loaded with the antimetabolite oxamate. Materials and Methods: Initial PubMed search was generalized for immunoliposomes in cancer. Further search was focused on papers for GD2-IL [keywords: “Immunoliposomes and cancer (or neuroblastoma)”]. Results: There were 811 results on “immunoliposomes”; >50% were on “immunoliposomes, cancer” (n=439, June 2024). Seventeen items resulted from “immunoliposomes, neuroblastoma” (one was “publishers’ correction”). Sixteen GD2-IL references were reviewed (1993-current). The mean±SD GD2-ILs size was 124.8±31 nm (range=86-171). Six papers described GD2-ILs with DNA-damaging agents [doxorubicin (n=4), etoposide (n=1), irinotecan+HDAC inhibitor (n=1)]. Other payloads included: fenretinide (n=4 papers), C-myb antisense (n=2), survivin inhibitor (n=1), tyrosine kinase inhibitor (n=1), IL15 (n=1), and oxamate (n=1). These 9 drug-loads included both hydrophilic and hydrophobic molecules. Except for IL15 and C-myb antisense with high molecular weights (MWs), and oxamate with low MW, the remaining compounds had comparable MWs (496±100 g/mol, range=349-588.6). The overall encapsulation efficiency was 66.2±25.6%. There were 17-30 mAb molecules attached to an IL with PEGylation. Experiments with GD2-positive/GD2-negative cells demonstrated selective efficacy/tropism of GD2-ILs. Mouse models confirmed efficacy, GD2-specific tumor accumulation, decreased toxicity, and improved pharmacokinetic-pharmacodynamics. Conclusion: PEGylated anti-GD2-IL may allow NBL tropism. A size of approximately 100 nm could allow vascular permeability and packaging of oxamate in amounts needed for profound/selective lactate dehydrogenase-A inhibition. Thus, oxamate-loaded GD2-ILs may allow exploring the great translational potential of Warburg effect inhibition in GD2-positive cancers." /> <meta name="DC.Contributor" content="WILLIAM S. PANOSYAN" /> <meta name="DC.Contributor" content="DANIEL E. PANOSYAN" /> <meta name="article:published_time" content="2024-11-01" /> <meta name="article:section" content="Review" /> <meta name="citation_title" content="Immunoliposomes for Neuroblastoma: Review of the Past Experience and Design of a Novel Nanoparticle" /> <meta name="citation_abstract" lang="en" content="<p>Background/Aim: High-risk/refractory neuro-blastoma (NBL) treatments include anti-GD2-monoclonal antibodies (mAbs). Several immunoliposomes (ILs) covered with anti-GD2-mAbs (GD2-ILs) have been tested pre-clinically. We aimed to review literature on GD2-IL for characteristics of nanoparticles/payloads, conjugation of mAb/fragments and preclinical data, as well as to explore the feasibility of a recently proposed GD2-IL loaded with the antimetabolite oxamate. Materials and Methods: Initial PubMed search was generalized for immunoliposomes in cancer. Further search was focused on papers for GD2-IL [keywords: “Immunoliposomes and cancer (or neuroblastoma)”]. Results: There were 811 results on “immunoliposomes”; &gt;50% were on “immunoliposomes, cancer” (n=439, June 2024). Seventeen items resulted from “immunoliposomes, neuroblastoma” (one was “publishers’ correction”). Sixteen GD2-IL references were reviewed (1993-current). The mean±SD GD2-ILs size was 124.8±31 nm (range=86-171). Six papers described GD2-ILs with DNA-damaging agents [doxorubicin (n=4), etoposide (n=1), irinotecan+HDAC inhibitor (n=1)]. Other payloads included: fenretinide (n=4 papers), C-myb antisense (n=2), survivin inhibitor (n=1), tyrosine kinase inhibitor (n=1), IL15 (n=1), and oxamate (n=1). These 9 drug-loads included both hydrophilic and hydrophobic molecules. Except for IL15 and C-myb antisense with high molecular weights (MWs), and oxamate with low MW, the remaining compounds had comparable MWs (496±100 g/mol, range=349-588.6). The overall encapsulation efficiency was 66.2±25.6%. There were 17-30 mAb molecules attached to an IL with PEGylation. Experiments with GD2-positive/GD2-negative cells demonstrated selective efficacy/tropism of GD2-ILs. Mouse models confirmed efficacy, GD2-specific tumor accumulation, decreased toxicity, and improved pharmacokinetic-pharmacodynamics. Conclusion: PEGylated anti-GD2-IL may allow NBL tropism. A size of approximately 100 nm could allow vascular permeability and packaging of oxamate in amounts needed for profound/selective lactate dehydrogenase-A inhibition. Thus, oxamate-loaded GD2-ILs may allow exploring the great translational potential of Warburg effect inhibition in GD2-positive cancers.</p>" /> <meta name="citation_journal_title" content="Anticancer Research" /> <meta name="citation_publisher" content="International Institute of Anticancer Research" /> <meta name="citation_publication_date" content="2024/11/01" /> <meta name="citation_mjid" content="anticanres;44/11/4665" /> <meta name="citation_id" content="44/11/4665" /> <meta name="citation_public_url" content="https://ar.iiarjournals.org/content/44/11/4665" /> <meta name="citation_abstract_html_url" content="https://ar.iiarjournals.org/content/44/11/4665.abstract" /> <meta name="citation_full_html_url" content="https://ar.iiarjournals.org/content/44/11/4665.full" /> <meta name="citation_pdf_url" content="https://ar.iiarjournals.org/content/anticanres/44/11/4665.full.pdf" /> <meta name="citation_issn" content="0250-7005" /> <meta name="citation_issn" content="1791-7530" /> <meta name="citation_doi" content="10.21873/anticanres.17294" /> <meta name="citation_pmid" content="39477321" /> <meta name="citation_volume" content="44" /> <meta name="citation_issue" content="11" /> <meta name="citation_article_type" content="Review Article" /> <meta name="citation_section" content="Review" /> <meta name="citation_firstpage" content="4665" /> <meta name="citation_lastpage" content="4675" /> <meta name="citation_access" content="all" /> <meta name="citation_author" content="WILLIAM S. 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Eslin;citation_author=VI. Brown;citation_author=W. Roberts;citation_author=P. Zage;citation_author=VL. Harrod;citation_author=DS. Mitchell;citation_author=D. Hanson;citation_author=GL. Saulnier Sholler;citation_title=Eflornithine as postimmunotherapy maintenance in high-risk neuroblastoma: externally controlled, propensity score-matched survival outcome comparisons;citation_volume=42;citation_year=2024;citation_issue=1;citation_doi=10.1200/JCO.22.02875" /> <meta name="citation_reference" content="citation_journal_title=ACS Chem Neurosci;citation_author=AY. Mochizuki;citation_author=IM. Frost;citation_author=MB. Mastrodimos;citation_author=AS. Plant;citation_author=AC. Wang;citation_author=TB. Moore;citation_author=RM. Prins;citation_author=PS. Weiss;citation_author=SJ. Jonas;citation_title=Precision medicine in pediatric neurooncology: a review;citation_pages=11-28;citation_volume=9;citation_year=2018;citation_issue=1;citation_pmid=29199818;citation_doi=10.1021/acschemneuro.7b00388" /> <meta name="citation_fulltext_world_readable" content="" /> <meta name="twitter:title" content="Immunoliposomes for Neuroblastoma: Review of the Past Experience and Design of a Novel Nanoparticle" /> <meta name="twitter:card" content="summary_large_image" /> <meta name="twitter:image" content="https://ar.iiarjournals.org/sites/default/files/highwire/anticanres/44/11.cover-source.jpg" /> <meta name="twitter:description" content="Background/Aim: High-risk/refractory neuro-blastoma (NBL) treatments include anti-GD2-monoclonal antibodies (mAbs). Several immunoliposomes (ILs) covered with anti-GD2-mAbs (GD2-ILs) have been tested pre-clinically. We aimed to review literature on GD2-IL for characteristics of nanoparticles/payloads, conjugation of mAb/fragments and preclinical data, as well as to explore the feasibility of a recently proposed GD2-IL loaded with the antimetabolite oxamate. Materials and Methods: Initial PubMed search was generalized for immunoliposomes in cancer. Further search was focused on papers for GD2-IL [keywords: “Immunoliposomes and cancer (or neuroblastoma)”]. Results: There were 811 results on “immunoliposomes”; >50% were on “immunoliposomes, cancer” (n=439, June 2024). Seventeen items resulted from “immunoliposomes, neuroblastoma” (one was “publishers’ correction”). Sixteen GD2-IL references were reviewed (1993-current). The mean±SD GD2-ILs size was 124.8±31 nm (range=86-171). Six papers described GD2-ILs with DNA-damaging agents [doxorubicin (n=4), etoposide (n=1), irinotecan+HDAC inhibitor (n=1)]. Other payloads included: fenretinide (n=4 papers), C-myb antisense (n=2), survivin inhibitor (n=1), tyrosine kinase inhibitor (n=1), IL15 (n=1), and oxamate (n=1). These 9 drug-loads included both hydrophilic and hydrophobic molecules. Except for IL15 and C-myb antisense with high molecular weights (MWs), and oxamate with low MW, the remaining compounds had comparable MWs (496±100 g/mol, range=349-588.6). The overall encapsulation efficiency was 66.2±25.6%. There were 17-30 mAb molecules attached to an IL with PEGylation. Experiments with GD2-positive/GD2-negative cells demonstrated selective efficacy/tropism of GD2-ILs. Mouse models confirmed efficacy, GD2-specific tumor accumulation, decreased toxicity, and improved pharmacokinetic-pharmacodynamics. Conclusion: PEGylated anti-GD2-IL may allow NBL tropism. A size of approximately 100 nm could allow vascular permeability and packaging of oxamate in amounts needed for profound/selective lactate dehydrogenase-A inhibition. Thus, oxamate-loaded GD2-ILs may allow exploring the great translational potential of Warburg effect inhibition in GD2-positive cancers." /> <meta name="og-title" property="og:title" content="Immunoliposomes for Neuroblastoma: Review of the Past Experience and Design of a Novel Nanoparticle" /> <meta name="og-url" property="og:url" content="https://ar.iiarjournals.org/content/44/11/4665" /> <meta name="og-site-name" property="og:site_name" content="Anticancer Research" /> <meta name="og-description" property="og:description" content="Background/Aim: High-risk/refractory neuro-blastoma (NBL) treatments include anti-GD2-monoclonal antibodies (mAbs). Several immunoliposomes (ILs) covered with anti-GD2-mAbs (GD2-ILs) have been tested pre-clinically. We aimed to review literature on GD2-IL for characteristics of nanoparticles/payloads, conjugation of mAb/fragments and preclinical data, as well as to explore the feasibility of a recently proposed GD2-IL loaded with the antimetabolite oxamate. Materials and Methods: Initial PubMed search was generalized for immunoliposomes in cancer. Further search was focused on papers for GD2-IL [keywords: “Immunoliposomes and cancer (or neuroblastoma)”]. Results: There were 811 results on “immunoliposomes”; >50% were on “immunoliposomes, cancer” (n=439, June 2024). Seventeen items resulted from “immunoliposomes, neuroblastoma” (one was “publishers’ correction”). Sixteen GD2-IL references were reviewed (1993-current). The mean±SD GD2-ILs size was 124.8±31 nm (range=86-171). Six papers described GD2-ILs with DNA-damaging agents [doxorubicin (n=4), etoposide (n=1), irinotecan+HDAC inhibitor (n=1)]. Other payloads included: fenretinide (n=4 papers), C-myb antisense (n=2), survivin inhibitor (n=1), tyrosine kinase inhibitor (n=1), IL15 (n=1), and oxamate (n=1). These 9 drug-loads included both hydrophilic and hydrophobic molecules. Except for IL15 and C-myb antisense with high molecular weights (MWs), and oxamate with low MW, the remaining compounds had comparable MWs (496±100 g/mol, range=349-588.6). The overall encapsulation efficiency was 66.2±25.6%. There were 17-30 mAb molecules attached to an IL with PEGylation. Experiments with GD2-positive/GD2-negative cells demonstrated selective efficacy/tropism of GD2-ILs. Mouse models confirmed efficacy, GD2-specific tumor accumulation, decreased toxicity, and improved pharmacokinetic-pharmacodynamics. Conclusion: PEGylated anti-GD2-IL may allow NBL tropism. A size of approximately 100 nm could allow vascular permeability and packaging of oxamate in amounts needed for profound/selective lactate dehydrogenase-A inhibition. Thus, oxamate-loaded GD2-ILs may allow exploring the great translational potential of Warburg effect inhibition in GD2-positive cancers." /> <meta name="og-type" property="og:type" content="article" /> <meta name="og-image" property="og:image" content="https://ar.iiarjournals.org/sites/default/files/highwire/anticanres/44/11.cover-source.jpg" /> <link rel="shortlink" href="/node/81997" /> <link rel="shortcut icon" href="https://ar.iiarjournals.org/sites/default/files/images/favicon.ico" type="image/vnd.microsoft.icon" /> <meta name="viewport" content="width=device-width, initial-scale=1" /> <title>Immunoliposomes for Neuroblastoma: Review of the Past Experience and Design of a Novel Nanoparticle | Anticancer Research</title> <link type="text/css" rel="stylesheet" href="/sites/default/files/advagg_css/css__QEy_BpbtMcsqv3xURK855GSs2fFjOibU10yA758Mn4c__NucWi_bEk5E3BNVDtTt2nhiPtE1A5I24YwRDQ2fojJ0__M8F9fri-b1QX8RwJbNRiWvN_bqCXCQEG9-9ZZDMJpyg.css" media="all" /> <link type="text/css" 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PANOSYAN</span></span></div> <div class="highwire-cite-metadata"><span class="highwire-cite-metadata-journal highwire-cite-metadata">Anticancer Research </span><span class="highwire-cite-metadata-date highwire-cite-metadata">November 2024, </span><span class="highwire-cite-metadata-volume highwire-cite-metadata">44 </span><span class="highwire-cite-metadata-issue highwire-cite-metadata">(11) </span><span class="highwire-cite-metadata-pages highwire-cite-metadata">4665-4675; </span><span class="highwire-cite-metadata-doi highwire-cite-metadata">DOI: https://doi.org/10.21873/anticanres.17294 </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="/anticanres/44/11/4665.atom" data-type="link" data-font-icon="" data-parent-id="81985"></span></div> </div> <div id="hw-article-author-popups-top-node-81997--63099816" style="display: none;"><div class="author-tooltip-0"><div class="author-tooltip-name">WILLIAM S. PANOSYAN </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'>University of California Los Angeles, UCLA College of Letters & Science, Los Angeles, CA, U.S.A.</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=WILLIAM%2BS.%2BPANOSYAN%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=PANOSYAN%20WS&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%3AWILLIAM%2BS.%2BPANOSYAN%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:williampanosyan@ucla.edu" class="" data-icon-position="" data-hide-link-title="0">williampanosyan@ucla.edu</a></span></li></ul></div><div class="author-tooltip-1"><div class="author-tooltip-name">DANIEL E. PANOSYAN </div><div class="author-tooltip-affiliation"><span class="author-tooltip-text"><div class='author-affiliation'>University of California Los Angeles, UCLA College of Letters & Science, Los Angeles, CA, U.S.A.</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=DANIEL%2BE.%2BPANOSYAN%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=PANOSYAN%20DE&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%3ADANIEL%2BE.%2BPANOSYAN%2B" rel="nofollow" class="" data-icon-position="" data-hide-link-title="0">Search for this author on this site</a></li></ul></div></div></div> </div> </div> </div> </div> </div> </div> <!-- /.panel-row-wrapper --> <div class="panel-row-wrapper clearfix"> <div class="main-content-wrapper grid-17 suffix-1 alpha"> <div class="panel-panel panel-region-content"> <div class="inside"><div class="panel-pane pane-highwire-panel-tabs pane-panels-ajax-tab-tabs" > <div class="pane-content"> <div class="item-list"><ul class="tabs inline panels-ajax-tab"><li class="first"><a href="/content/44/11/4665" class="panels-ajax-tab-tab" data-panel-name="jnl_iiar_tab_art" data-target-id="highwire_article_tabs" data-entity-context="node:81997" data-trigger="" data-url-enabled="1">Article</a><a href="/panels_ajax_tab/jnl_iiar_tab_art/node:81997/1" rel="nofollow" style="display:none" class="js-crawler-link"></a></li><li><a href="/content/44/11/4665/tab-figures-data" class="panels-ajax-tab-tab" data-panel-name="jnl_iiar_tab_data" data-target-id="highwire_article_tabs" data-entity-context="node:81997" data-trigger="tab-figures-data" data-url-enabled="1">Figures & Data</a><a href="/panels_ajax_tab/jnl_iiar_tab_data/node:81997/1" rel="nofollow" style="display:none" class="js-crawler-link"></a></li><li><a href="/content/44/11/4665/tab-article-info" class="panels-ajax-tab-tab" data-panel-name="jnl_iiar_tab_info" data-target-id="highwire_article_tabs" data-entity-context="node:81997" data-trigger="tab-article-info" data-url-enabled="1">Info & Metrics</a><a href="/panels_ajax_tab/jnl_iiar_tab_info/node:81997/1" rel="nofollow" style="display:none" class="js-crawler-link"></a></li><li class="last"><a href="/content/anticanres/44/11/4665.full.pdf" class="panels-ajax-tab-tab" data-panel-name="jnl_iiar_tab_pdf" data-target-id="highwire_article_tabs" data-entity-context="node:81997" data-trigger="tab-pdf" data-url-enabled="1"><i class="icon-file-alt"></i> PDF</a><a href="/panels_ajax_tab/jnl_iiar_tab_pdf/node:81997/1" rel="nofollow" style="display:none" class="js-crawler-link"></a></li></ul></div> </div> </div> <div class="panel-separator"></div><div class="panel-pane pane-highwire-panel-tabs-container" > <div class="pane-content"> <div data-panels-ajax-tab-preloaded="jnl_iiar_tab_art" id="panels-ajax-tab-container-highwire_article_tabs" class="panels-ajax-tab-container"><div class="panels-ajax-tab-loading" style ="display:none"><img class="loading" src="https://ar.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: High-risk/refractory neuro-blastoma (NBL) treatments include anti-GD2-monoclonal antibodies (mAbs). Several immunoliposomes (ILs) covered with anti-GD2-mAbs (GD2-ILs) have been tested pre-clinically. We aimed to review literature on GD2-IL for characteristics of nanoparticles/payloads, conjugation of mAb/fragments and preclinical data, as well as to explore the feasibility of a recently proposed GD2-IL loaded with the antimetabolite oxamate. Materials and Methods: Initial PubMed search was generalized for immunoliposomes in cancer. Further search was focused on papers for GD2-IL [keywords: “Immunoliposomes and cancer (or neuroblastoma)”]. Results: There were 811 results on “immunoliposomes”; >50% were on “immunoliposomes, cancer” (n=439, June 2024). Seventeen items resulted from “immunoliposomes, neuroblastoma” (one was “publishers’ correction”). Sixteen GD2-IL references were reviewed (1993-current). The mean±SD GD2-ILs size was 124.8±31 nm (range=86-171). Six papers described GD2-ILs with DNA-damaging agents [doxorubicin (n=4), etoposide (n=1), irinotecan+HDAC inhibitor (n=1)]. Other payloads included: fenretinide (n=4 papers), C-myb antisense (n=2), survivin inhibitor (n=1), tyrosine kinase inhibitor (n=1), IL15 (n=1), and oxamate (n=1). These 9 drug-loads included both hydrophilic and hydrophobic molecules. Except for IL15 and C-myb antisense with high molecular weights (MWs), and oxamate with low MW, the remaining compounds had comparable MWs (496±100 g/mol, range=349-588.6). The overall encapsulation efficiency was 66.2±25.6%. There were 17-30 mAb molecules attached to an IL with PEGylation. Experiments with GD2-positive/GD2-negative cells demonstrated selective efficacy/tropism of GD2-ILs. Mouse models confirmed efficacy, GD2-specific tumor accumulation, decreased toxicity, and improved pharmacokinetic-pharmacodynamics. Conclusion: PEGylated anti-GD2-IL may allow NBL tropism. A size of approximately 100 nm could allow vascular permeability and packaging of oxamate in amounts needed for profound/selective lactate dehydrogenase-A inhibition. Thus, oxamate-loaded GD2-ILs may allow exploring the great translational potential of Warburg effect inhibition in GD2-positive cancers.</p></div><span class="kwd-group-title">Key Words:</span><ul class="kwd-group"><li class="kwd"><a href="/keyword/neuroblastoma" class="hw-term hw-article-keyword hw-article-keyword-neuroblastoma" rel="nofollow">Neuroblastoma</a></li><li class="kwd"><a href="/keyword/anti-gd2-antibody-0" class="hw-term hw-article-keyword hw-article-keyword-anti-gd2-antibody" rel="nofollow">anti-GD2 antibody</a></li><li class="kwd"><a href="/keyword/immunoliposomes" class="hw-term hw-article-keyword hw-article-keyword-immunoliposomes" rel="nofollow">immunoliposomes</a></li><li class="kwd"><a href="/keyword/oxamate" class="hw-term hw-article-keyword hw-article-keyword-oxamate" rel="nofollow">oxamate</a></li><li class="kwd"><a href="/keyword/review" class="hw-term hw-article-keyword hw-article-keyword-review" rel="nofollow">review</a></li></ul><p id="p-6">Present cure rates for high risk and refractory neuroblastoma (NBL) are poor, which necessitates research for better therapeutics (<a id="xref-ref-1-1" class="xref-bibr" href="#ref-1">1</a>). Traditional high-intensity DNA-damaging regiments, which are designed for destruction of resistant NBL cells, indiscriminately trigger collateral damage to normal tissues, resulting in undesirable side effects such as profound myelosuppression. Therefore, the discovery of cell surface molecules that are relatively specific to particular cancer groups presented great opportunities for developing targeted therapies (<a id="xref-ref-2-1" class="xref-bibr" href="#ref-2">2</a>). Targeted molecular therapies are revolutionizing cancer treatment, including within pediatrics, and providing opportunities to patients with relapsed and/or refractory disease who previously had few options outside of palliative care. One such target molecule is GD2, which is present in higher amounts on NBL, Ewing sarcoma, melanoma, and other cancer cells, compared to normal tissues (<a id="xref-ref-3-1" class="xref-bibr" href="#ref-3">3</a>).</p><p id="p-7">Technological advancement for production of monoclonal antibodies has provided an additional armamentarium for furthering cancer-specific therapies (<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>). In addition to clinically approved monoclonal antibodies (mAbs) (<a id="xref-ref-3-2" class="xref-bibr" href="#ref-3">3</a>), the anti-GD2-directed approach incorporated preclinical development of immunoliposomes covered with anti-GD2 mAbs (GD2-IL) (<a id="xref-ref-6-1" class="xref-bibr" href="#ref-6">6</a>-<a id="xref-ref-21-1" class="xref-bibr" href="#ref-21">21</a>). Contrary to direct conjugation of therapeutic substances to mAbs, immunoliposomes (IL) allow significantly higher number of small molecules for “packaged delivery” into cancer cells (<a id="xref-ref-22-1" class="xref-bibr" href="#ref-22">22</a>, <a id="xref-ref-23-1" class="xref-bibr" href="#ref-23">23</a>), which can be of particular interest in certain pathophysiological situations. One such pathophysiological/biochemical alteration characterized by increased lactate production in many cancers is the Warburg effect (<a id="xref-ref-24-1" class="xref-bibr" href="#ref-24">24</a>), which can be suppressed with therapeutic intention (<a id="xref-ref-25-1" class="xref-bibr" href="#ref-25">25</a>), including in combination with mAbs (<a id="xref-ref-26-1" class="xref-bibr" href="#ref-26">26</a>). This can be achieved by oxamate-induced inhibition of the central enzyme in the Warburg effect called lactate dehydrogenase-A (LDHA), which is not only elevated in NBL but is also linked with poor prognosis (<a id="xref-ref-21-2" class="xref-bibr" href="#ref-21">21</a>, <a id="xref-ref-27-1" class="xref-bibr" href="#ref-27">27</a>, <a id="xref-ref-28-1" class="xref-bibr" href="#ref-28">28</a>). Therefore, packaging the LDHA inhibitor oxamate into lipid nanoparticles covered with anti-GD2 mAb theoretically represents a perfect fit for the development of an anti-NBL specific anti-metabolite approach (<a id="xref-ref-21-3" class="xref-bibr" href="#ref-21">21</a>, <a id="xref-ref-29-1" class="xref-bibr" href="#ref-29">29</a>).</p><p id="p-8">As noted, similar GD2-IL approach with drug loads other than oxamate historically have been developed and tested pre-clinically (<a id="xref-ref-6-2" class="xref-bibr" href="#ref-6">6</a>-<a id="xref-ref-20-1" class="xref-bibr" href="#ref-20">20</a>). Although we found no reports that any of these GD2-ILs have passed the testing threshold for clinical application, few ILs for other cancers have made it into early phase clinical trials, including some with encouraging results (<a id="xref-ref-23-2" class="xref-bibr" href="#ref-23">23</a>, <a id="xref-ref-30-1" class="xref-bibr" href="#ref-30">30</a>-<a id="xref-ref-34-1" class="xref-bibr" href="#ref-34">34</a>). Thus, in order to learn the details from past experiences, we conducted a review summarizing published data on GD2-ILs, including sizes of nanoparticles, characteristics of the loaded drugs, types of the mAb/fragment conjugation, and other preclinical data if available (such as efficacy, tropism, and pharmacokinetic (PK)/pharmacodynamic (PD) data). Dissection of the results from past research helps to optimize preclinical design and plan testing of a novel GD2-IL with an alternative payload such as anti-metabolite oxamate, which may allow selective targeting of LDHA in NBL.</p><div class="section materials-methods" id="sec-1"><h2 class="">Materials and Methods</h2><p id="p-9"><em>Literature search strategy</em>. Our initial PubMed search was briefly directed to overall immunoliposomes, followed by “immunoliposomes and cancer” in general. The subsequent efforts were pointed towards more specific and commonly occurring cancer groups such as breast, lung, prostate, skin, <em>etc</em>. Number of articles for immunoliposomes for each of these groups, as well as frequently targeted cell-surface molecules and drug-loads, were extracted for the overall description of the landscape in this research field. Sequentially, the main focus was concentrated on the literature review for all the accessible papers on GD2-IL for NBL. Keywords “Immunoliposomes and neuroblastoma” were used for this more dedicated search.</p><p id="p-10"><em>Selection and analysis of GD2-IL studies</em>. Primarily full article texts were used for data extraction. Critical review of this selected literature served as a basis to extract the main information presented in results, mostly in the form of <a id="xref-table-wrap-1-1" class="xref-table" href="#T1">Table I</a>, <a id="xref-table-wrap-2-1" class="xref-table" href="#T2">Table II</a>, <a id="xref-table-wrap-3-1" class="xref-table" href="#T3">Table III</a> and <a id="xref-table-wrap-4-1" class="xref-table" href="#T4">Table IV</a>. Collected numerical parameters included sizes of ILs, molecular weights of payloads, mAb: IL ratios, encapsulation efficacy, as well as polydispersity index, Zeta Potential, and drug loading data whenever applicable. Descriptive data were summarized in the form of types of Ab/fragments, payloads, cells used, and <em>in vitro</em>/<em>in vivo</em> experiment results, which included changes of IC<sub>50</sub>s and PK/PD data. Accumulative findings in consideration with the current-era technological achievements intended to deliberate the development, potential efficacy and advantages of a novel nanoparticle. For example, past experiences can be used to project the anticipated effects <em>in vitro</em> and <em>in vivo</em>. These include possible shifts of the IC<sub>50</sub>s, comparing an unmodified payload, payload encapsulated in a non-specific liposomal nanoparticle, and GD2-IL loaded with oxamate. The <em>in vivo</em> effects of the payload encapsulated in a non-specific liposomal nanoparticle, and GD2-IL loaded with oxamate on mouse weight (as a surrogate for toxicity), tumor size, and mice survival can be further studied based on articles reviewed here.</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/82191/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/82191/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/82191" 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-11" class="first-child">Summary of GD2-immunoliposomes (GD2-ILs) based on therapeutic payloads.</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/82025/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/82025/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/82025" 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-12" class="first-child">Summary of GD2-immunoliposomes (GD2-ILs) with pertinent in vitro and in vivo effects.</p><div class="sb-div caption-clear"></div></div></div><div id="T3" 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/82162/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/82162/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/82162" 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 III.</span> <p id="p-13" class="first-child">Commonly used and selected cell lines used for immunoliposome testing.</p><div class="sb-div caption-clear"></div></div></div><div id="T4" 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/82341/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/82341/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/82341" 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 IV.</span> <p id="p-14" class="first-child">Animal studies with anti-GD2 immunoliposomes.</p><div class="sb-div caption-clear"></div></div></div></div><div class="section results" id="sec-2"><h2 class="">Results</h2><p id="p-15"><em>Literature search: Immunoliposomes and common adult cancers</em>. As of June 2024, there were 811 PubMed results on “immunoliposomes”, starting from 1977. More than half of these items for immunoliposomes projected to be related to cancer as supported by “immunoliposomes and cancer” search (n=439, starting since 1983) (<a id="xref-fig-1-1" class="xref-fig" href="#F1">Figure 1</a> and <a id="xref-fig-2-1" class="xref-fig" href="#F2">Figure 2</a>). The majority of those items were related to the more common adult-onset cancers other than NBL [for NBL, n=16 articles, last column of <a id="xref-table-wrap-1-2" class="xref-table" href="#T1">Table I</a> (<a id="xref-ref-6-3" class="xref-bibr" href="#ref-6">6</a>-<a id="xref-ref-21-4" class="xref-bibr" href="#ref-21">21</a>)]. Combining the keywords “immunoliposome” with the most common cancer types (<a href="https://www.cancer.gov/types/common-cancers">https://www.cancer.gov/types/common-cancers</a>) produced 335 articles: breast (92), prostate (9), lung (34), colorectal (27), melanoma (27), bladder (6), kidney (5), ovarian (18), pancreatic (12), thyroid (1), liver (35) cancers, leukemia (33), and lymphoma (36) (<a id="xref-fig-2-2" class="xref-fig" href="#F2">Figure 2B</a>). The search for “brain tumor or glioblastoma with immunoliposomes” produced an additional 35 and 9 items, respectively (<a id="xref-fig-2-3" class="xref-fig" href="#F2">Figure 2B</a>). Examples of commonly targeted cell-surface markers included EGFR and HER2 for glioblastoma (GBM) and breast cancer, as well as GD2 for NBL and melanoma. First paper on “immunoliposome and neuroblastoma” appeared in 1993, 10 years after the initial publications on “immunoliposome and cancer”.</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://ar.iiarjournals.org/content/anticanres/44/11/4665/F1.large.jpg?width=800&height=600&carousel=1" title="Bar graphs A-C demonstrate PubMed search results for corresponding key words and total numbers shown below." class="highwire-fragment fragment-images colorbox-load" rel="gallery-fragment-images-593669173" data-figure-caption="<div class="highwire-markup">Bar graphs A-C demonstrate PubMed search results for corresponding key words and total numbers shown below.</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://ar.iiarjournals.org/content/anticanres/44/11/4665/F1.medium.gif" width="167" height="440"/><noscript><img class="highwire-fragment fragment-image" alt="Figure 1." src="https://ar.iiarjournals.org/content/anticanres/44/11/4665/F1.medium.gif" width="167" height="440"/></noscript></span></a></div></div><ul class="highwire-figure-links inline"><li class="download-fig first"><a href="https://ar.iiarjournals.org/content/anticanres/44/11/4665/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://ar.iiarjournals.org/content/anticanres/44/11/4665/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/82226" 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-16" class="first-child">Bar graphs A-C demonstrate PubMed search results for corresponding key words and total numbers shown below.</p><div class="sb-div caption-clear"></div></div></div><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://ar.iiarjournals.org/content/anticanres/44/11/4665/F2.large.jpg?width=800&height=600&carousel=1" title="(A) The total number of articles on immunoliposomes (ILs), IL and cancer (CA), IL and specific CA, IL and neuroblastoma (NBL), as well as clinical trials. (B) The number of articles based on specific cancer types." class="highwire-fragment fragment-images colorbox-load" rel="gallery-fragment-images-593669173" data-figure-caption="<div class="highwire-markup">(A) The total number of articles on immunoliposomes (ILs), IL and cancer (CA), IL and specific CA, IL and neuroblastoma (NBL), as well as clinical trials. (B) The number of articles based on specific cancer types.</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://ar.iiarjournals.org/content/anticanres/44/11/4665/F2.medium.gif" width="440" height="361"/><noscript><img class="highwire-fragment fragment-image" alt="Figure 2." src="https://ar.iiarjournals.org/content/anticanres/44/11/4665/F2.medium.gif" width="440" height="361"/></noscript></span></a></div></div><ul class="highwire-figure-links inline"><li class="download-fig first"><a href="https://ar.iiarjournals.org/content/anticanres/44/11/4665/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://ar.iiarjournals.org/content/anticanres/44/11/4665/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/82214" 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-17" class="first-child">(A) The total number of articles on immunoliposomes (ILs), IL and cancer (CA), IL and specific CA, IL and neuroblastoma (NBL), as well as clinical trials. (B) The number of articles based on specific cancer types.</p><div class="sb-div caption-clear"></div></div></div><p id="p-18"><em>Clinical trials</em>. There were only 6 clinical trials starting since 2003 for “immunoliposomes and cancer” – on EGFR, HER2−, or GAH-targeted liposomal doxorubicin formulations for breast cancer, GBM, and advanced solid tumors including metastatic stomach cancer (<a id="xref-ref-23-3" class="xref-bibr" href="#ref-23">23</a>, <a id="xref-ref-30-2" class="xref-bibr" href="#ref-30">30</a>-<a id="xref-ref-34-2" class="xref-bibr" href="#ref-34">34</a>). There was a 20-year gap between the initial publications on “immunoliposome and cancer” until the first clinical trial publication.</p><p id="p-19"><em>Papers on GD2-IL for neuroblastoma</em>. Seventeen items resulted from “immunoliposomes, neuroblastoma”, with one being a “publisher’s correction”. Another paper was eliminated as it used the transferrin receptor, which is non-specific to NBL. An abstract was added <em>via</em> a separate online search (<a id="xref-ref-18-1" class="xref-bibr" href="#ref-18">18</a>), totaling GD2-IL references to 16, dated from 1993-current (see the last column of <a id="xref-table-wrap-1-3" class="xref-table" href="#T1">Table I</a>, which summarizes key findings from these 16 papers). First, we looked at the size of these nanoparticles. Average GD2-IL size range was 86-171 nm, mean±SD of means was 125.5±32.2, (100 nm liposome presumably contains about 100,000 molecules of phospholipids). Next, we examined the payloads in the GD2-ILs.</p><p id="p-20"><em>Therapeutic payloads</em>. Six out of 16 papers described GD2-ILs with DNA-damaging agents (4 with doxorubicin, 1 with etoposide, 1 with irinotecan +an HDAC inhibitor), <a id="xref-table-wrap-1-4" class="xref-table" href="#T1">Table I</a>. Four were with fenretinide, 2 with C-myb antisense, 2 with inhibitors of (i) survivin and (ii) tyrosine kinase (<a id="xref-table-wrap-1-5" class="xref-table" href="#T1">Table I</a>). Our own paper suggested the anti-metabolite oxamate as a load (<a id="xref-ref-21-5" class="xref-bibr" href="#ref-21">21</a>), and the abstract-only reference (<a id="xref-ref-18-2" class="xref-bibr" href="#ref-18">18</a>) used IL15-loaded ILs as an adjunct to cellular therapy. Therefore, altogether there were 9 kinds of GD2-ILs based on the drug load (<a id="xref-table-wrap-1-6" class="xref-table" href="#T1">Table I</a>). The drugs were both hydrophilic (<em>i.e.</em>, YM155, oxamate), and hydrophobic (<em>i.e.</em>, doxorubicin). With the exclusion of the IL15 (MW=13kDa), C-myb antisense (MW=3.16kDa), and oxamate (MW=88 g/mol), the remaining 7 compounds had comparable sizes with an average MW of 496±100 g/mol (range=391.5-588.6). The number of mAb molecules per GD2-IL was reported to be within 17 to 30, all practically attached with PEGylation.</p><p id="p-21"><a id="xref-table-wrap-2-2" class="xref-table" href="#T2">Table II</a> summarizes few other key parameters for ILs, as well as a brief description of <em>in vitro</em> and <em>in vivo</em> results. Multiple cell lines, both GD2-positive and GD2−, were used to demonstrate the selective efficacy and tropism of GD2-ILs (<a id="xref-table-wrap-3-2" class="xref-table" href="#T3">Table III</a>). Dose-response curves were generated from commonly used MTT (<a id="xref-ref-8-1" class="xref-bibr" href="#ref-8">8</a>, <a id="xref-ref-10-1" class="xref-bibr" href="#ref-10">10</a>, <a id="xref-ref-20-2" class="xref-bibr" href="#ref-20">20</a>) and MTS assays (<a id="xref-ref-11-1" class="xref-bibr" href="#ref-11">11</a>). Also, other assays, such as <sup>51</sup>Cr release assay (<a id="xref-ref-16-1" class="xref-bibr" href="#ref-16">16</a>), flow cytometry for cell apoptosis, BCA protein assay (<a id="xref-ref-17-1" class="xref-bibr" href="#ref-17">17</a>), and alamar Blue viability assay (<a id="xref-ref-19-1" class="xref-bibr" href="#ref-19">19</a>) were used. Mouse models were also implemented to show <em>in vivo</em> efficacy and tumor tropism, as well as for exploration of bioavailability and/or PK-PD data (<a id="xref-table-wrap-4-2" class="xref-table" href="#T4">Table IV</a>). In vivo experiments in general confirmed the efficacy, GD2-specific tumor accumulation, as well as lessened toxicity, improved PK-PD, and bioavailability profiles.</p><p id="p-22"><em>Neuroblastoma and GD2 targeting</em>. High risk and refractory NBL was the first childhood cancer to be approved for antibody-mediated immunotherapy (<a id="xref-ref-3-3" class="xref-bibr" href="#ref-3">3</a>). The carbohydrate-containing sphingolipid disialoganglioside GD2 is expressed on the surface of NBL cells (limitedly expressed in normal tissues) and has led to the incorporation of anti-GD2 mAbs into complex therapies (<a id="xref-ref-35-1" class="xref-bibr" href="#ref-35">35</a>). However, suboptimal clinical outcomes (<a id="xref-ref-1-2" class="xref-bibr" href="#ref-1">1</a>) and drug resistance (<a id="xref-ref-35-2" class="xref-bibr" href="#ref-35">35</a>) justify continuing search and development efforts of an alternative approach such as GD2-directed immunoliposomes (IL). Literature on GD2-targeted delivery of various compounds, shows that ILs loaded with an anti-NBL agent predominantly affect the GD2-positive NBL cells, while sparing normal tissues.</p><p id="p-23"><em>The central enzyme of Warburg effect as a potential target for NBL</em>. While also present in many healthy cells, the enzyme LDHA responsible for fermentation of glucose to lactate is known to play a key role in the growth and progression of several cancers (<a id="xref-ref-27-2" class="xref-bibr" href="#ref-27">27</a>, <a id="xref-ref-36-1" class="xref-bibr" href="#ref-36">36</a>), including NBL (<a id="xref-ref-21-6" class="xref-bibr" href="#ref-21">21</a>, <a id="xref-ref-28-2" class="xref-bibr" href="#ref-28">28</a>). Therefore, efforts to improve targeted therapies for NBL included an appreciation of the potentially crucial role that LDHA regulation plays in cancer cell proliferation (<a id="xref-ref-27-3" class="xref-bibr" href="#ref-27">27</a>, <a id="xref-ref-36-2" class="xref-bibr" href="#ref-36">36</a>). The depletion of LDHA has been shown to decrease the growth of NBL cells in <em>in vivo</em> mouse models (<a id="xref-ref-28-3" class="xref-bibr" href="#ref-28">28</a>) and has been confirmed to be a significant predictor of event-free survival probability, independent of age, stage, and genomics (<a id="xref-ref-21-7" class="xref-bibr" href="#ref-21">21</a>, <a id="xref-ref-28-4" class="xref-bibr" href="#ref-28">28</a>). These data suggest that targeted and profound suppression of LDHA may be a strong candidate for NBL therapy development. Treatment of NBL cells with a drug known to suppress LDHA may help to answer this question.</p><p id="p-24"><em>Oxamate and its delivery with help of lipid nanoparticles (LNPs)</em>. The small molecule drug named oxamate has been identified as a potentially clinically relevant LDHA inhibitor (<a id="xref-ref-29-2" class="xref-bibr" href="#ref-29">29</a>). The conjugation of LDHA inhibitors directly to anti-GD2 mAbs has not been explored previously. However, the estimated optimal molar ratio of anti-GD2 mAb and the LDHA inhibitor, oxamate, exceeds 1:10,000 (<a id="xref-ref-21-8" class="xref-bibr" href="#ref-21">21</a>), whereas most FDA-approved mAb-drug conjugates have fewer than 10 molecules attached to a single mAb. In contrast, LNPs provide a vehicle to encapsulate and protect cargo, delivering higher amounts of small molecules directly into cells <em>via</em> endosomal escape. As successfully exemplified by mRNA-based SARS-CoV2 vaccines, LNP synthesis allows for affordable, scalable, and tunable self-assembly of this cargo, with a wide spectrum of targets (<a id="xref-ref-37-1" class="xref-bibr" href="#ref-37">37</a>). Therefore, the therapeutic potential of oxamate against NBL can be elucidated by an LNP-based carrier encapsulating large amounts of the drug for eventual delivery to NBL cells (<a id="xref-fig-2-4" class="xref-fig" href="#F2">Figure 2</a>, Step 1). Further considerations for development of such an LNP may include a method that will reverse-engineer a lipid-coupling strategy, which was employed previously to identify and capture molecular cargo in circulating extracellular vesicles (<a id="xref-ref-38-1" class="xref-bibr" href="#ref-38">38</a>). Tuning of oxamate encapsulation for optimal biocompatibility and stability of LNP conformation with preserved endosomal escape (<a id="xref-fig-2-5" class="xref-fig" href="#F2">Figure 2</a>, Steps 1-2) will be crucial. Screening of commercially available, sterol, ionizable, cationic, and PEGylated lipid components, along with their molecular weight ratios, will allow this fine tuning. LNPs can be mixed using a microfluidic mixing system, and their morphology can be analyzed <em>via</em> transmission electron microscopy and dynamic light scattering. LDH cytotoxicity and enzyme activity assays (<a id="xref-ref-25-2" class="xref-bibr" href="#ref-25">25</a>, <a id="xref-ref-28-5" class="xref-bibr" href="#ref-28">28</a>) can be used to quantify the effect of oxamate on GD2-positive NBL cells, such as IMR32. Nevertheless, despite the tunable configuration of LNPs, indiscriminate delivery of the amount of oxamate required to maximize anti-NBL effects is likely to have a negative effect on non-cancerous, healthy cells, which also express some amount of LDHA. Thus, a key challenge in determining the clinical potential of LHDA inhibitors lies in the targeted delivery of oxamate to NBL cells.</p><p id="p-25"><em>Nanoparticle functionalization to enable neuroblastoma targeting</em>. To direct the packaged oxamate molecules towards NBL cells, liposomes encapsulating oxamate in LNP-based carriers can be efficiently functionalized with anti-GD2 mAbs to target GD2-positive NBL cells, as strongly supported by our review. Targeting LPNs towards GD2, a unique identifying surface marker present on NBL cells, allowed delivering variety of small molecule payloads directly to NBL cells with high specificity while sparing non-cancerous cells, and this principle should work for oxamate. Anti-GD2 mAbs (FDA approved dinutuximab or naxitamab) can be attached to oxamate-loaded and PEGylated LNPs (<a id="xref-ref-38-2" class="xref-bibr" href="#ref-38">38</a>) to enable targeted delivery as well as specificity of this platform towards GD2-positive NBL cells (<a id="xref-fig-2-6" class="xref-fig" href="#F2">Figure 2</a>, Steps 2-3). <em>In vitro</em> specificity of PEGylated lipid-anti-GD2 mAbs towards NBL cells and optimal dosing parameters can be estimated by monitoring LDHA suppression efficacy, <em>via</em> LDH cytotoxicity and enzyme activity assays, in IMR32 and other NBL cells co-cultured with non-GD2 expressing cells as used in reviewed papers [<a id="xref-table-wrap-3-3" class="xref-table" href="#T3">Table III</a>, (<a id="xref-ref-39-1" class="xref-bibr" href="#ref-39">39</a>)].</p></div><div class="section discussion" id="sec-3"><h2 class="">Discussion</h2><p id="p-26">Anti-GD2 mAb-covered liposomes have been used with a variety of payloads. Our review aimed to learn from past experiences and to use this knowledge for designing a novel immunoliposome, as shown in <a id="xref-fig-3-1" class="xref-fig" href="#F3">Figure 3</a>. Summaries of this review are presented in <a id="xref-table-wrap-1-7" class="xref-table" href="#T1">Table I</a>, <a id="xref-table-wrap-2-3" class="xref-table" href="#T2">Table II</a>, <a id="xref-table-wrap-3-4" class="xref-table" href="#T3">Table III</a> and <a id="xref-table-wrap-4-3" class="xref-table" href="#T4">Table IV</a>, and the overall results support both feasibility as well as efficacy of this design. An equivalent mass of the oxamate that can be loaded per an IL molecule can be extrapolated/estimated based on that of up to 15,000-doxorubicin molecules per one 100 nm liposomal particle (<a id="xref-ref-40-1" class="xref-bibr" href="#ref-40">40</a>). Considering the 6-fold difference between the molecular weights of doxorubicin (540 g/mol) <em>versus</em> oxamate (88 g/mol), up to >90,000 molecules of oxamate may be possible to load into one molecule of a 100 nm IL, a size that also allows vascular permeability, based on preclinical data on tumor accumulation. The ability to deliver these amounts of oxamate directly to NBL cells should enable elucidation of the full effect of LDHA suppression on NBL cell growth. Upon specific mAb-GD2 interaction, LNPs will be internalized by endocytosis, releasing cargo directly into NBL cells. Recent precedent validated the proposed technology, with mAb LNPs shown to successfully deliver RNA <em>in vivo</em>, in mouse models (<a id="xref-ref-38-3" class="xref-bibr" href="#ref-38">38</a>). After development and confirmation of <em>in vitro</em> efficacy, these can serve as a foundation for <em>in vivo</em> studies with an LPN-based, anti-GD2-directed anti-metabolic therapy, targeting NBL xenografts in existing mouse models. Recent approval of eflornithine for NBL maintenance therapy (<a id="xref-ref-41-1" class="xref-bibr" href="#ref-41">41</a>, <a id="xref-ref-42-1" class="xref-bibr" href="#ref-42">42</a>) supports the concept that anti-metabolic/enzyme-inhibiting molecules can serve as a novel adjuvant and be combined with other modalities, with less overlapping toxicity and without additional myelosuppression. The strategy of nanoparticles covered with specific mAbs and anti-metabolic payloads may also be applied to refractory hematological malignancies such as relapsed acute lymphoblastic and myeloid leukemias. This may also allow development of novel therapies with promising translational potential to enhance the existing armamentarium of precision medicine in pediatric neurooncology (<a id="xref-ref-43-1" class="xref-bibr" href="#ref-43">43</a>) and other solid tumors.</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://ar.iiarjournals.org/content/anticanres/44/11/4665/F3.large.jpg?width=800&height=600&carousel=1" title="Schematic illustration of loading liposomes with oxamate molecules. Step 1: loading oxamate molecules into liposomal nanoparticles; Step 2: PEGylation of oxamate-containing liposomes; and Step 3: generation of immunoliposomes (ILs) by attachment of anti-GD2 monoclonal antibodies (mAbs) resulting in anti-GD2 mAb functionalized LNPs, i.e., GD2-Immunoliposomes. NBL: Neuroblastoma." class="highwire-fragment fragment-images colorbox-load" rel="gallery-fragment-images-593669173" data-figure-caption="<div class="highwire-markup">Schematic illustration of loading liposomes with oxamate molecules. Step 1: loading oxamate molecules into liposomal nanoparticles; Step 2: PEGylation of oxamate-containing liposomes; and Step 3: generation of immunoliposomes (ILs) by attachment of anti-GD2 monoclonal antibodies (mAbs) resulting in anti-GD2 mAb functionalized LNPs, i.e., GD2-Immunoliposomes. NBL: Neuroblastoma.</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://ar.iiarjournals.org/content/anticanres/44/11/4665/F3.medium.gif" width="440" height="339"/><noscript><img class="highwire-fragment fragment-image" alt="Figure 3." src="https://ar.iiarjournals.org/content/anticanres/44/11/4665/F3.medium.gif" width="440" height="339"/></noscript></span></a></div></div><ul class="highwire-figure-links inline"><li class="download-fig first"><a href="https://ar.iiarjournals.org/content/anticanres/44/11/4665/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://ar.iiarjournals.org/content/anticanres/44/11/4665/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/82027" 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-27" class="first-child">Schematic illustration of loading liposomes with oxamate molecules. Step 1: loading oxamate molecules into liposomal nanoparticles; Step 2: PEGylation of oxamate-containing liposomes; and Step 3: generation of immunoliposomes (ILs) by attachment of anti-GD2 monoclonal antibodies (mAbs) resulting in anti-GD2 mAb functionalized LNPs, i.e., GD2-Immunoliposomes. NBL: Neuroblastoma.</p><div class="sb-div caption-clear"></div></div></div></div><div class="section conclusion" id="sec-4"><h2 class="">Conclusion</h2><p id="p-28">The development of a GD2-targeting LNP platform appears feasible and can be improved <em>via</em> novel technologies for the encapsulation and delivery of the LDHA inhibitor oxamate. Proposed LNPs can be tested on a spectrum of GD2-positive cells, such as from the Children’s Oncology Group Cell Line and Xenograft Repository, along with GD2-negative cells (<a id="xref-table-wrap-3-5" class="xref-table" href="#T3">Table III</a>). The next potential target can be NBL-utilizing anti-GD2 mAbs-lipid conjugation for the delivery of oxamate. Nevertheless, this type of antibody-LNP conjugation with an anti-metabolite load may offer an elegant solution across a broad scope of pediatric and adult cancers. Deployment of such tools in good manufacturing practice-compliant settings would empower oncology research, providing new insight into the treatment of refractory malignancies, and potentially enabling translation into clinical use. In summary, combination of past experiences and novel technologies permits the design and development of an effective novel GD2-IL. Oxamate payload of these LPNs will allow exploring the therapeutic potential of LDHA inhibition in NBL and other GD2-positive malignancies.</p></div><div class="section ack" id="ack-1"><h2 class="">Acknowledgements</h2><p id="p-31">Authors thank Dr. Ruby A. Sims, Ph.D. and Dr. Steven J. Jonas, M.D., Ph.D. for manuscript review and constructive criticism, as well as Dr. Eduard H. Panosyan, M.D. for help with the figures and general guidance.</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">Both Authors contributed to writing and editing the manuscript. They have conducted the initial literature review, data extraction, analyses and drafting the manuscript. They received further detailed and critical insights for re-writing the manuscript into its presented form as acknowledged below.</p></li><li class="fn" id="fn-3"><p id="p-29"><strong>Conflicts of Interest</strong></p><p id="p-30">The Authors have no conflicts of interest to declare 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="2024-06-30"><span class="received-label">Received </span>June 30, 2024.</li><li xmlns:hwp="http://schema.highwire.org/Journal" class="rev-recd" hwp:start="2024-08-09"><span class="rev-recd-label">Revision received </span>August 9, 2024.</li><li xmlns:hwp="http://schema.highwire.org/Journal" class="accepted" hwp:start="2024-09-16"><span class="accepted-label">Accepted </span>September 16, 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-44.11.4665.1" data-doi="10.1002/pbc.28473"><div class="cit-metadata"><ol class="cit-auth-list"><li><span class="cit-auth"><span class="cit-name-surname">Chung</span> <span class="cit-name-given-names">C</span></span>, </li><li><span class="cit-auth"><span class="cit-name-surname">Boterberg</span> <span class="cit-name-given-names">T</span></span>, </li><li><span 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