{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,4]],"date-time":"2026-08-04T05:47:30Z","timestamp":1785822450167,"version":"3.56.0"},"reference-count":45,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2026,8,4]],"date-time":"2026-08-04T00:00:00Z","timestamp":1785801600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Immunol."],"abstract":"<jats:sec>\n                    <jats:title>Introduction<\/jats:title>\n                    <jats:p>Primary bone sarcomas, including Osteosarcoma (OS) and Ewing sarcoma (ES), are rare pediatric malignancies with limited therapeutic advances over recent decades and poor outcomes, especially for patients with metastatic and refractory\/relapsed disease. Disialoganglioside 2 (GD2) has emerged as a promising immunotherapeutic target due to its high expression in pediatric bone sarcomas and its role in tumor progression and treatment resistance. This systematic review summarizes current evidence on GD2-targeted therapies and combination strategies in pediatric bone sarcomas.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>A systematic review was conducted according to PRISMA 2020 guidelines using PubMed, Embase, Web of Science, and ClinicalTrials.gov. Preclinical and clinical studies investigating GD2-targeted therapies in pediatric bone sarcomas were included, together with registered clinical trials.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>Twenty-six studies met inclusion criteria, including 17 preclinical and 9 clinical studies, alongside 15 ongoing clinical trials. Preclinical evidence consistently demonstrated antitumor activity of GD2-directed approaches, including monoclonal antibodies (mAbs), CAR-T cells, bispecific antibodies, and radio-immunotherapy. Combination strategies, particularly anti-GD2 mAbs with chemotherapy, enhanced antitumor efficacy through induction of apoptosis, activation of endoplasmic reticulum stress pathways, and inhibition of tumor invasiveness. Clinical evidence, although limited and heterogeneous, suggested encouraging activity of Dinutuximab beta-based chemo-immunotherapy, especially in ES. Several clinical trials are ongoing, mainly early-phase and focusing on relapsed or refractory diseases.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Discussion<\/jats:title>\n                    <jats:p>GD2 represents a biologically relevant and clinically promising target in pediatric bone sarcomas. However, major translational challenges remain, including limited clinical data, heterogeneous study designs, and the lack of standardized assays for GD2 expression assessment. Further collaborative international studies are needed to optimize patient selection and accelerate the development of GD2-targeted combination immunotherapy strategies.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.3389\/fimmu.2026.1895000","type":"journal-article","created":{"date-parts":[[2026,8,4]],"date-time":"2026-08-04T05:38:53Z","timestamp":1785821933000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":0,"title":["GD2-targeted immunotherapy in pediatric bone sarcomas: a systematic review of emerging strategies and combination approaches"],"prefix":"10.3389","volume":"17","author":[{"given":"Elisa","family":"Tirtei","sequence":"first","affiliation":[{"name":"Pediatric Onco-Hematology Department, Regina Margherita Children\u2019s Hospital","place":["Turin, Italy"]},{"name":"Department of Public Health and Pediatrics, University of Turin","place":["Turin, Italy"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sofia","family":"Poggi Longostrevi","sequence":"additional","affiliation":[{"name":"Pediatric Onco-Hematology Department, Regina Margherita Children\u2019s Hospital","place":["Turin, Italy"]},{"name":"Department of Public Health and Pediatrics, University of Turin","place":["Turin, Italy"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sabrina","family":"Bombaci","sequence":"additional","affiliation":[{"name":"Pediatric Onco-Hematology Department, Regina Margherita Children\u2019s Hospital","place":["Turin, Italy"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Federico","family":"Mercolini","sequence":"additional","affiliation":[{"name":"Pediatric Hematology and Oncology, IRCCS Azienda Ospedaliero-Universitaria di Bologna","place":["Bologna, Italy"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria Grazia","family":"Pionelli","sequence":"additional","affiliation":[{"name":"Pediatric Oncology Unit, Department of Pediatric Onco-Hematology, Santobono-Pausilipon Children\u2019s Hospital","place":["AORN, Naples, Italy"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sebastian Dorin","family":"Asaftei","sequence":"additional","affiliation":[{"name":"Pediatric Onco-Hematology Department, Regina Margherita Children\u2019s Hospital","place":["Turin, Italy"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Franca","family":"Fagioli","sequence":"additional","affiliation":[{"name":"Pediatric Onco-Hematology Department, Regina Margherita Children\u2019s Hospital","place":["Turin, Italy"]},{"name":"Department of Public Health and Pediatrics, University of Turin","place":["Turin, Italy"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2026,8,4]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","DOI":"10.1002\/PBC.29442","article-title":"Current approaches to management of bone sarcoma in adolescent and young adult patients","volume":"69","author":"Ingley","year":"2022","journal-title":"Pediatr Blood Cancer"},{"key":"B2","doi-asserted-by":"publisher","DOI":"10.3390\/IJMS23073817","article-title":"Recent and ongoing research into metastatic osteosarcoma treatments","volume":"23","author":"Harris","year":"2022","journal-title":"Int J Mol Sci"},{"key":"B3","doi-asserted-by":"publisher","DOI":"10.3390\/LIFE12122099","article-title":"Improving osteosarcoma treatment: Comparative oncology in action","volume":"12","author":"Tarone","year":"2022","journal-title":"Life"},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejca.2025.116093","article-title":"Paediatric strategy forum for medicinal product development of agents targeting GD2 ganglioside in children and adolescents with cancer","volume":"231","author":"DuBois","year":"2025","journal-title":"Eur J Cancer"},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.3389\/FONC.2020.01000","article-title":"Disialoganglioside GD2 expression in solid tumors and role as a target for cancer therapy","volume":"10","author":"Nazha","year":"2020","journal-title":"Front Oncol"},{"key":"B6","doi-asserted-by":"publisher","first-page":"548","DOI":"10.1002\/CNCR.28461","article-title":"Ganglioside GD2 as a therapeutic target for antibody-mediated therapy in osteosarcoma","volume":"120","author":"Roth","year":"2013","journal-title":"Cancer"},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.1136\/bmj.n71","article-title":"The PRISMA 2020 statement: An updated guideline for reporting systematic reviews","volume":"372","author":"Page","year":"2021","journal-title":"BMJ"},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2288-14-43","article-title":"SYRCLE\u2019s risk of bias tool for animal studies","volume":"14","author":"Hooijmans","year":"2014","journal-title":"BMC Med Res Methodol"},{"key":"B9","unstructured":"Risk of Bias Tools - Archive: Rob 2.0 (2016)\n          \n          2016"},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.1136\/BMJ.I4919","article-title":"ROBINS-I: A tool for assessing risk of bias in non-randomised studies of interventions","volume":"355","author":"Sterne","year":"2016","journal-title":"BMJ (Online)"},{"key":"B11","unstructured":"Jbi Critical Appraisal Tools | Jbi"},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.1007\/S00259-023-06528-2","article-title":"Therapeutic efficacy of an alpha-particle emitter labeled anti-GD2 humanized antibody against osteosarcoma-a proof of concept study","volume":"51","author":"Liatsou","year":"2024","journal-title":"Eur J Nucl Med Mol Imaging"},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.1186\/S40364-025-00800-3","article-title":"A novel therapeutic strategy for osteosarcoma using anti-GD2 ADC and EZH2 inhibitor","volume":"13","author":"Shan","year":"2025","journal-title":"biomark Res"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.1038\/s41591-021-01625-x","article-title":"Anti-GD2 synergizes with CD47 blockade to mediate tumor eradication","volume":"28","author":"Theruvath","year":"2022","journal-title":"Nat Med"},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.1691\/PH.2018.7836","article-title":"Anti-ganglioside GD2 monoclonal antibody synergizes with cisplatin to induce endoplasmic reticulum-associated apoptosis in osteosarcoma cells","volume":"73","author":"Zhu","year":"2018","journal-title":"Pharmazie"},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.1371\/JOURNAL.PONE.0093576","article-title":"Endothelin A receptor antagonism enhances inhibitory effects of anti-ganglioside GD2 monoclonal antibody on invasiveness and viability of human osteosarcoma cells","volume":"9","author":"Liu","year":"2014","journal-title":"PloS One"},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.1136\/JITC-2020-002267","article-title":"Combinatorial immunotherapy of N-803 (IL-15 superagonist) and dinutuximab with ex vivo expanded natural killer cells significantly enhances in vitro cytotoxicity against GD2+ pediatric solid tumors and in vivo survival of xenografted immunodeficient NSG \u2026","volume":"9","author":"Chu","year":"2021","journal-title":"J Immunother Cancer"},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.1007\/S12672-024-01166-Y","article-title":"Combined use of niraparib enhanced the inhibitory effect of anti-GD2 antibody on osteosarcoma cells","volume":"15","author":"Wenyao","year":"2024","journal-title":"Discover Oncol"},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.1016\/J.ISCI.2025.114449","article-title":"Dinutuximab beta effectively treats Ewing sarcoma when combined with chemotherapy","volume":"29","author":"Frapolli","year":"2025","journal-title":"iScience"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.1186\/S13045-020-01012-Y","article-title":"GD2 or HER2 targeting T cell engaging bispecific antibodies to treat osteosarcoma","volume":"13","author":"Park","year":"2020","journal-title":"J Hematol Oncol"},{"key":"B21","first-page":"674","article-title":"GD2 chimeric antigen receptor modified T cells in synergy with sub-toxic level of doxorubicin targeting osteosarcomas","volume":"10","author":"Chulanetra","year":"2020","journal-title":"Am J Cancer Res"},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1002\/IJC.32743","article-title":"GD2-directed CAR-T cells in combination with HGF-targeted neutralizing antibody (AMG102) prevent primary tumor growth and metastasis in Ewing sarcoma","volume":"146","author":"Charan","year":"2020","journal-title":"Int J Cancer"},{"key":"B23","doi-asserted-by":"publisher","DOI":"10.1038\/BJC.2013.356","article-title":"Ewing sarcoma dissemination and response to T-cell therapy in mice assessed by whole-body magnetic resonance imaging","volume":"109","author":"Liebsch","year":"2013","journal-title":"Br J Cancer"},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.1016\/J.TRANON.2021.101240","article-title":"Anti-GD2 CAR MSCs against metastatic Ewing\u2019s sarcoma","volume":"15","author":"Golinelli","year":"2022","journal-title":"Transl Oncol"},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.1080\/2162402X.2016.1250050","article-title":"Targeting Ewing sarcoma with activated and GD2-specific chimeric antigen receptor-engineered human NK cells induces upregulation of immune-inhibitory HLA-G","volume":"6","author":"Kailayangiri","year":"2016","journal-title":"Oncoimmunology"},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.1097\/MPH.0000000000002488","article-title":"First-line anti-GD2 therapy combined with consolidation chemotherapy in 3 patients with newly diagnosed metastatic Ewing sarcoma or Ewing-like sarcoma","volume":"44","author":"Spasov","year":"2022","journal-title":"J Pediatr Hematol Oncol"},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.1097\/MPH.0000000000003126","article-title":"Off-label use of dinutuximab beta in combination with chemotherapy in patients with Ewing sarcoma: A retrospective single-center case series","volume":"47","author":"Spasov","year":"2025","journal-title":"J Pediatr Hematol Oncol"},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1136\/JITC-2023-008744","article-title":"Targeting refractory\/recurrent neuroblastoma and osteosarcoma with anti-CD3\u00d7anti-GD2 bispecific antibody armed T cells","volume":"12","author":"Yankelevich","year":"2024","journal-title":"J Immunother Cancer"},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.1080\/19420862.2020.1773751","article-title":"A phase 1 and pharmacokinetic study evaluating daily or weekly schedules of the humanized anti-GD2 antibody hu14.18K322A in recurrent\/refractory solid tumors","volume":"12","author":"Bishop","year":"2020","journal-title":"MAbs"},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.3389\/FONC.2023.1164949","article-title":"Novel infusion strategy reduces severe adverse events caused by the anti-GD2 monoclonal antibody naxitamab","volume":"13","author":"Varo","year":"2023","journal-title":"Front Oncol"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejca.2022.05.035","article-title":"Phase 2 study of anti-disialoganglioside antibody, dinutuximab, in combination with GM-CSF in patients with recurrent osteosarcoma: A report from the Children\u2019s Oncology Group","volume":"172","author":"Hingorani","year":"2022","journal-title":"Eur J Cancer"},{"key":"B32","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1186\/S13063-019-4026-8","article-title":"International randomised controlled trial for the treatment of newly diagnosed EWING sarcoma family of tumours \u2013 EURO EWING 2012 Protocol","volume":"21","author":"Anderton","year":"2020","journal-title":"Trials"},{"key":"B33","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3390\/CANCERS13030520","article-title":"Exploiting gangliosides for the therapy of Ewing\u2019s sarcoma and H3K27M-mutant diffuse midline glioma","volume":"13","author":"Wingerter","year":"2021","journal-title":"Cancers (Basel)"},{"key":"B34","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/j.ccell.2023.11.011","article-title":"Immune determinants of CAR-T cell expansion in solid tumor patients receiving GD2 CAR-T cell therapy","volume":"42","author":"Kaczanowska","year":"2024","journal-title":"Cancer Cell"},{"key":"B35","doi-asserted-by":"publisher","DOI":"10.1016\/J.EJCA.2022.09.003","article-title":"A randomised phase II trial of a trivalent ganglioside vaccine targeting GM2, GD2 and GD3 combined with immunological adjuvant OPT-821 versus OPT-821 alone in metastatic sarcoma patients rendered disease-free by surgery","volume":"176","author":"Rosenbaum","year":"2022","journal-title":"Eur J Cancer"},{"key":"B36","doi-asserted-by":"publisher","first-page":"551","DOI":"10.1007\/S11523-025-01155-3","article-title":"Efficacy and safety of anti-GD2 immunotherapy with dinutuximab beta in the treatment of relapsed\/refractory high-risk neuroblastoma","volume":"20","author":"Wieczorek","year":"2025","journal-title":"Target Oncol"},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.1016\/S1470-2045(17)30355-8","article-title":"Irinotecan\u2013temozolomide with temsirolimus or dinutuximab in children with refractory or relapsed neuroblastoma (COG ANBL1221): An open-label, randomised, phase 2 trial","volume":"18","author":"Mody","year":"2017","journal-title":"Lancet Oncol"},{"key":"B38","doi-asserted-by":"publisher","first-page":"10002","DOI":"10.1200\/JCO.2022.40.16_SUPPL.10002","article-title":"BEACON-Immuno: Results of the dinutuximab beta (dB) randomization of the BEACON-Neuroblastoma phase 2 trial\u2014A European Innovative Therapies for Children with Cancer (ITCC\u2013International Society of Paediatric Oncology Europe Neuroblastoma Group (SIOPEN) tr\u2026","volume":"40","author":"Gray","year":"2022","journal-title":"J Clin Oncol"},{"key":"B39","unstructured":"Siopen High Risk Neuroblastoma Study 2 (Hr-2) \u2014 Siopen Research Network"},{"key":"B40","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejca.2024.114001","article-title":"Chemo-immunotherapy with dinutuximab beta in patients with relapsed\/progressive high-risk neuroblastoma: Does chemotherapy backbone matter","volume":"202","author":"Raiser","year":"2024","journal-title":"Eur J Cancer"},{"key":"B41","doi-asserted-by":"publisher","DOI":"10.1038\/S41571-022-00643-Z","article-title":"Advancing therapy for neuroblastoma","volume":"19","author":"Qiu","year":"2022","journal-title":"Nat Rev Clin Oncol"},{"key":"B42","doi-asserted-by":"publisher","DOI":"10.1093\/ONCOLO\/OYAF008","article-title":"Detection of plasma circulating GD2 ganglioside in patients with neuroblastoma and age-matched healthy children. Diagnostic and prognostic evaluation","volume":"30","author":"Morini","year":"2025","journal-title":"Oncologist"},{"key":"B43","doi-asserted-by":"publisher","DOI":"10.1038\/bjc.2012.57","article-title":"The ganglioside antigen GD2 is surface-expressed in Ewing sarcoma and allows for MHC-independent immune targeting","volume":"106","author":"Kailayangiri","year":"2012","journal-title":"Br J Cancer"},{"key":"B44","doi-asserted-by":"publisher","DOI":"10.1080\/2162402X.2015.1025194","article-title":"Effective combination treatment of GD2-expressing neuroblastoma and Ewing\u2019s sarcoma using anti-GD2 ch14.18\/CHO antibody with V\u03b39V\u03b42+ \u03b3\u03b4T cells","volume":"5","author":"Fisher","year":"2015","journal-title":"Oncoimmunology"},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.1186\/S13045-024-01641-7","article-title":"Tumor-derived G-CSF induces an immunosuppressive microenvironment in an osteosarcoma model, reducing response to CAR.GD2 T-cells","volume":"17","author":"Pezzella","year":"2024","journal-title":"J Hematol Oncol"}],"container-title":["Frontiers in Immunology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2026.1895000\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,4]],"date-time":"2026-08-04T05:38:55Z","timestamp":1785821935000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2026.1895000\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,4]]},"references-count":45,"alternative-id":["10.3389\/fimmu.2026.1895000"],"URL":"https:\/\/doi.org\/10.3389\/fimmu.2026.1895000","relation":{},"ISSN":["1664-3224"],"issn-type":[{"value":"1664-3224","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,4]]},"article-number":"1895000"}}