Skip to main content
SpringerLink
Log in

Immunotherapy of Neuroblastoma Targeting GD2 and Beyond

  • Chapter
  • First Online:
Glycosignals in Cancer

  • 281 Accesses

Abstract

Neuroblastoma is the most common extracranial solid tumor in children. Although low-risk neuroblastoma is mostly curable, the outcome of high-risk neuroblastoma, which comprises ~50% of neuroblastoma, is dismal. Abundant expression of disialoganglioside GD2 antigens is a feature of neuroblastoma. The success of immunotherapy targeting the GD2 antigen with dinutuximab has fueled the interest in developing improved immunotherapeutics including humanized anti-GD2 antibodies, GD2 mimotopes, cytokine-fused GD2-specific antibodies, GD2-specific chimeric antigen receptor T/NKT cells, GD2 vaccine, anti-GD2 idiotype monoclonal antibody, and anti-O-acetyl GD2 antibody. Advance in these active or passive cancer immunotherapies hold promises to further improve the outcome of neuroblastoma.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Ahmed M, Cheng M, Cheung IY, Cheung NK (2015) Human derived dimerization tag enhances tumor killing potency of a T-cell engaging bispecific antibody. Onco Targets Ther 4:e989776. https://doi.org/10.4161/2162402X.2014.989776

    Article  CAS  Google Scholar 

  • Alfonso S, Valdes-Zayas A, Santiesteban ER, Flores YI, Areces F, Hernandez M, Viada CE, Mendoza IC, Guerra PP, Garcia E, Ortiz RA, de la Torre AV, Cepeda M, Perez K, Chong E, Hernandez AM, Toledo D, Gonzalez Z, Mazorra Z, Crombet T, Perez R, Vazquez AM, Macias AE (2014) A randomized, multicenter, placebo-controlled clinical trial of racotumomab-alum vaccine as switch maintenance therapy in advanced non-small cell lung cancer patients. Clin Cancer Res 20:3660–3671. https://doi.org/10.1158/1078-0432.CCR-13-1674

    Article  CAS  PubMed  Google Scholar 

  • Alvarez-Rueda N, Desselle A, Cochonneau D, Chaumette T, Clemenceau B, Leprieur S, Bougras G, Supiot S, Mussini JM, Barbet J, Saba J, Paris F, Aubry J, Birkle S (2011) A monoclonal antibody to O-acetyl-GD2 ganglioside and not to GD2 shows potent anti-tumor activity without peripheral nervous system cross-reactivity. PLoS One 6:e25220. https://doi.org/10.1371/journal.pone.0025220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amler LC, Schwab M (1989) Amplified N-myc in human neuroblastoma cells is often arranged as clustered tandem repeats of differently recombined DNA. Mol Cell Biol 9:4903–4913. https://doi.org/10.1128/mcb.9.11.4903-4913.1989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barker E, Mueller BM, Handgretinger R, Herter M, Yu AL, Reisfeld RA (1991) Effect of a chimeric anti-ganglioside GD2 antibody on cell-mediated lysis of human neuroblastoma cells. Cancer Res 51:144–149

    CAS  PubMed  Google Scholar 

  • Battula VL, Shi Y, Evans KW, Wang RY, Spaeth EL, Jacamo RO, Guerra R, Sahin AA, Marini FC, Hortobagyi G, Mani SA, Andreeff M (2012) Ganglioside GD2 identifies breast cancer stem cells and promotes tumorigenesis. J Clin Invest 122:2066–2078. https://doi.org/10.1172/JCI59735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhandari S, Cheung NK, Kushner BH, Kramer K, Modak S, Larson SM, Yeh S, Heller G, Sklar CA (2010) Hypothyroidism after 131I-monoclonal antibody treatment of neuroblastoma. Pediatr Blood Cancer 55:76–80. https://doi.org/10.1002/pbc.22452

    Article  PubMed  Google Scholar 

  • Biswas S, Biswas K, Richmond A, Ko J, Ghosh S, Simmons M, Rayman P, Rini B, Gill I, Tannenbaum CS, Finke JH (2009) Elevated levels of select gangliosides in T cells from renal cell carcinoma patients is associated with T cell dysfunction. J Immunol 183:5050–5058. https://doi.org/10.4049/jimmunol.0900259

    Article  CAS  PubMed  Google Scholar 

  • Bolesta E, Kowalczyk A, Wierzbicki A, Rotkiewicz P, Bambach B, Tsao CY, Horwacik I, Kolinski A, Rokita H, Brecher M, Wang X, Ferrone S, Kozbor D (2005) DNA vaccine expressing the mimotope of GD2 ganglioside induces protective GD2 cross-reactive antibody responses. Cancer Res 65:3410–3418. https://doi.org/10.1158/0008-5472.CAN-04-2164

    Article  CAS  PubMed  Google Scholar 

  • Buhtoiarov IN, Neal ZC, Gan J, Buhtoiarova TN, Patankar MS, Gubbels JA, Hank JA, Yamane B, Rakhmilevich AL, Reisfeld RA, Gillies SD, Sondel PM (2011) Differential internalization of hu14.18-IL2 immunocytokine by NK and tumor cell: impact on conjugation, cytotoxicity, and targeting. J Leukoc Biol 89:625–638. https://doi.org/10.1189/jlb.0710422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cacciavillano W, Sampor C, Venier C, Gabri MR, de Davila MT, Galluzzo ML, Guthmann MD, Fainboim L, Alonso DF, Chantada GL (2015) A phase I study of the anti-idiotype vaccine racotumomab in neuroblastoma and other pediatric refractory malignancies. Pediatr Blood Cancer 62:2120–2124. https://doi.org/10.1002/pbc.25631

    Article  CAS  PubMed  Google Scholar 

  • Cerato E, Birkle S, Portoukalian J, Mezazigh A, Chatal JF, Aubry J (1997) Variable region gene segments of nine monoclonal antibodies specific to disialogangliosides (GD2, GD3) and their O-acetylated derivatives. Hybridoma 16:307–316

    Article  CAS  PubMed  Google Scholar 

  • Cheng M, Ahmed M, Xu H, Cheung NK (2015) Structural design of disialoganglioside GD2 and CD3-bispecific antibodies to redirect T cells for tumor therapy. Int J Cancer 136:476–486. https://doi.org/10.1002/ijc.29007

    Article  CAS  PubMed  Google Scholar 

  • Cheng JY, Hung JT, Lin J, Lo FY, Huang JR, Chiou SP, Wang YH, Lin RJ, Wu JC, Yu J, Yu AL (2021) O-acetyl-GD2 as a therapeutic target for breast cancer stem cells. Front Immunol 12:791551. https://doi.org/10.3389/fimmu.2021.791551

    Article  CAS  PubMed  Google Scholar 

  • Cheung NK, Modak S (2002) Oral (1-->3),(1-->4)-beta-D-glucan synergizes with antiganglioside GD2 monoclonal antibody 3F8 in the therapy of neuroblastoma. Clin Cancer Res 8:1217–1223

    CAS  PubMed  Google Scholar 

  • Cheung NK, Landmeier B, Neely J, Nelson AD, Abramowsky C, Ellery S, Adams RB, Miraldi F (1986) Complete tumor ablation with iodine 131-radiolabeled disialoganglioside GD2-specific monoclonal antibody against human neuroblastoma xenografted in nude mice. J Natl Cancer Inst 77:739–745

    Article  CAS  PubMed  Google Scholar 

  • Cheung NK, Lazarus H, Miraldi FD, Abramowsky CR, Kallick S, Saarinen UM, Spitzer T, Strandjord SE, Coccia PF, Berger NA (1987) Ganglioside GD2 specific monoclonal antibody 3F8: a phase I study in patients with neuroblastoma and malignant melanoma. J Clin Oncol 5:1430–1440

    Article  CAS  PubMed  Google Scholar 

  • Cheung NK, Canete A, Cheung IY, Ye JN, Liu C (1993) Disialoganglioside GD2 anti-idiotypic monoclonal antibodies. Int J Cancer 54:499–505

    Article  CAS  PubMed  Google Scholar 

  • Cheung NK, Kushner BH, Yeh SD, Larson SM (1998) 3F8 monoclonal antibody treatment of patients with stage 4 neuroblastoma: a phase II study. Int J Oncol 12:1299–1306. https://doi.org/10.3892/ijo.12.6.1299

    Article  CAS  PubMed  Google Scholar 

  • Cheung NK, Sowers R, Vickers AJ, Cheung IY, Kushner BH, Gorlick R (2006) FCGR2A polymorphism is correlated with clinical outcome after immunotherapy of neuroblastoma with anti-GD2 antibody and granulocyte macrophage colony-stimulating factor. J Clin Oncol 24:2885–2890. https://doi.org/10.1200/JCO.2005.04.6011

    Article  CAS  PubMed  Google Scholar 

  • Cheung NK, Cheung IY, Kushner BH, Ostrovnaya I, Chamberlain E, Kramer K, Modak S (2012a) Murine anti-GD2 monoclonal antibody 3F8 combined with granulocyte-macrophage colony-stimulating factor and 13-cis-retinoic acid in high-risk patients with stage 4 neuroblastoma in first remission. J Clin Oncol 30:3264–3270. https://doi.org/10.1200/JCO.2011.41.3807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheung NK, Guo H, Hu J, Tassev DV, Cheung IY (2012b) Humanizing murine IgG3 anti-GD2 antibody m3F8 substantially improves antibody-dependent cell-mediated cytotoxicity while retaining targeting in vivo. Onco Targets Ther 1:477–486

    Google Scholar 

  • Cheung NK, Cheung IY, Kramer K, Modak S, Kuk D, Pandit-Taskar N, Chamberlain E, Ostrovnaya I, Kushner BH (2014) Key role for myeloid cells: phase II results of anti-G(D2) antibody 3F8 plus granulocyte-macrophage colony-stimulating factor for chemoresistant osteomedullary neuroblastoma. Int J Cancer 135:2199–2205. https://doi.org/10.1002/ijc.28851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheung IY, Kushner BH, Modak S, Basu EM, Roberts SS, Cheung NV (2017) Phase I trial of anti-GD2 monoclonal antibody hu3F8 plus GM-CSF: impact of body weight, immunogenicity and anti-GD2 response on pharmacokinetics and survival. Onco Targets Ther 6:e1358331. https://doi.org/10.1080/2162402X.2017.1358331

    Article  Google Scholar 

  • Cheung IY, Cheung NV, Modak S, Mauguen A, Feng Y, Basu E, Roberts SS, Ragupathi G, Kushner BH (2021) Survival impact of anti-GD2 antibody response in a phase II ganglioside vaccine trial among patients with high-risk neuroblastoma with prior disease progression. J Clin Oncol 39:215–226. https://doi.org/10.1200/JCO.20.01892

    Article  CAS  PubMed  Google Scholar 

  • Cochonneau D, Terme M, Michaud A, Dorvillius M, Gautier N, Frikeche J, Alvarez-Rueda N, Bougras G, Aubry J, Paris F, Birkle S (2013) Cell cycle arrest and apoptosis induced by O-acetyl-GD2-specific monoclonal antibody 8B6 inhibits tumor growth in vitro and in vivo. Cancer Lett 333:194–204. https://doi.org/10.1016/j.canlet.2013.01.032

    Article  CAS  PubMed  Google Scholar 

  • Cohn SL, Pearson AD, London WB, Monclair T, Ambros PF, Brodeur GM, Faldum A, Hero B, Iehara T, Machin D, Mosseri V, Simon T, Garaventa A, Castel V, Matthay KK, Force IT (2009) The international neuroblastoma risk group (INRG) classification system: an INRG task force report. J Clin Oncol 27:289–297. https://doi.org/10.1200/JCO.2008.16.6785

    Article  PubMed  PubMed Central  Google Scholar 

  • Dambuza IM, Brown GD (2015) C-type lectins in immunity: recent developments. Curr Opin Immunol 32:21–27. https://doi.org/10.1016/j.coi.2014.12.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davis KL, Fox E, Merchant MS, Reid JM, Kudgus RA, Liu X, Minard CG, Voss S, Berg SL, Weigel BJ, Mackall CL (2020) Nivolumab in children and young adults with relapsed or refractory solid tumours or lymphoma (ADVL1412): a multicentre, open-label, single-arm, phase 1-2 trial. Lancet Oncol 21:541–550. https://doi.org/10.1016/S1470-2045(20)30023-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delgado DC, Hank JA, Kolesar J, Lorentzen D, Gan J, Seo S, Kim K, Shusterman S, Gillies SD, Reisfeld RA, Yang R, Gadbaw B, DeSantes KB, London WB, Seeger RC, Maris JM, Sondel PM (2010) Genotypes of NK cell KIR receptors, their ligands, and Fc-gamma receptors in the response of neuroblastoma patients to Hu14.18-IL2 immunotherapy. Cancer Res 70:9554–9561. https://doi.org/10.1158/0008-5472.CAN-10-2211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deppisch N, Ruf P, Eissler N, Neff F, Buhmann R, Lindhofer H, Mocikat R (2015) Efficacy and tolerability of a GD2-directed trifunctional bispecific antibody in a preclinical model: subcutaneous administration is superior to intravenous delivery. Mol Cancer Ther 14:1877–1883. https://doi.org/10.1158/1535-7163.MCT-15-0156

    Article  CAS  PubMed  Google Scholar 

  • Desai AV, Gilman AL, Ozkaynak MF, Naranjo A, London WB, Tenney SC, Diccianni M, Hank JA, Parisi MT, Shulkin BL, Smith M, Moscow JA, Shimada H, Matthay KK, Cohn SL, Maris JM, Bagatell R, Sondel PM, Park JR, Yu AL (2022) Outcomes following anti-GD2 antibody-based post-consolidation therapy after cessation of randomization on ANBL0032: a report from the children’s oncology group. J Clin Oncol

    Google Scholar 

  • Doronin II, Vishnyakova PA, Kholodenko IV, Ponomarev ED, Ryazantsev DY, Molotkovskaya IM, Kholodenko RV (2014) Ganglioside GD2 in reception and transduction of cell death signal in tumor cells. BMC Cancer 14:295. https://doi.org/10.1186/1471-2407-14-295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durbas M, Horwacik I, Boratyn E, Kamycka E, Rokita H (2015) GD2 ganglioside specific antibody treatment downregulates PI3K/Akt/mTOR signaling network in human neuroblastoma cell lines. Int J Oncol 47:1143–1159. https://doi.org/10.3892/ijo.2015.3070

    Article  CAS  PubMed  Google Scholar 

  • Ehlert K, Hansjuergens I, Zinke A, Otto S, Siebert N, Henze G, Lode H (2020) Nivolumab and dinutuximab beta in two patients with refractory neuroblastoma. J Immunother Cancer 8(1):e000540. https://doi.org/10.1136/jitc-2020-000540

    Article  PubMed  PubMed Central  Google Scholar 

  • Eissler N, Ruf P, Mysliwietz J, Lindhofer H, Mocikat R (2012) Trifunctional bispecific antibodies induce tumor-specific T cells and elicit a vaccination effect. Cancer Res 72:3958–3966. https://doi.org/10.1158/0008-5472.CAN-12-0146

    Article  CAS  PubMed  Google Scholar 

  • Erbe AK, Wang W, Reville PK, Carmichael L, Kim K, Mendonca EA, Song Y, Hank JA, London WB, Naranjo A, Hong F, Hogarty MD, Maris JM, Park JR, Ozkaynak MF, Miller JS, Gilman AL, Kahl B, Yu AL, Sondel PM (2017) HLA-Bw4-I-80 isoform differentially influences clinical outcome as compared to HLA-Bw4-T-80 and HLA-A-Bw4 isoforms in rituximab or dinutuximab-based cancer immunotherapy. Front Immunol 8:675. https://doi.org/10.3389/fimmu.2017.00675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erbe AK, Wang W, Carmichael L, Kim K, Mendonca EA, Song Y, Hess D, Reville PK, London WB, Naranjo A, Hank JA, Diccianni MB, Reisfeld RA, Gillies SD, Matthay KK, Cohn SL, Hogarty MD, Maris JM, Park JR, Ozkaynak MF, Gilman AL, Yu AL, Sondel PM (2018) Neuroblastoma patients’ KIR and KIR-ligand genotypes influence clinical outcome for dinutuximab-based immunotherapy: a report from the children’s oncology group. Clin Cancer Res 24:189–196. https://doi.org/10.1158/1078-0432.CCR-17-1767

    Article  CAS  PubMed  Google Scholar 

  • FDA (2020) FDA grants accelerated approval to naxitamab for high-risk neuroblastoma in bone or bone marrow Journal 2022:U.S. Food & Drug

    Google Scholar 

  • Federico SM, McCarville MB, Shulkin BL, Sondel PM, Hank JA, Hutson P, Meagher M, Shafer A, Ng CY, Leung W, Janssen WE, Wu J, Mao S, Brennan RC, Santana VM, Pappo AS, Furman WL (2017) A pilot trial of humanized anti-GD2 monoclonal antibody (hu14.18K322A) with chemotherapy and natural killer cells in children with recurrent/refractory neuroblastoma. Clin Cancer Res 23:6441–6449. https://doi.org/10.1158/1078-0432.CCR-17-0379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fest S, Huebener N, Weixler S, Bleeke M, Zeng Y, Strandsby A, Volkmer-Engert R, Landgraf C, Gaedicke G, Riemer AB, Michalsky E, Jaeger IS, Preissner R, Forster-Wald E, Jensen-Jarolim E, Lode HN (2006) Characterization of GD2 peptide mimotope DNA vaccines effective against spontaneous neuroblastoma metastases. Cancer Res 66:10567–10575. https://doi.org/10.1158/0008-5472.CAN-06-1158

    Article  CAS  PubMed  Google Scholar 

  • Foon KA, Sen G, Hutchins L, Kashala OL, Baral R, Banerjee M, Chakraborty M, Garrison J, Reisfeld RA, Bhattacharya-Chatterjee M (1998) Antibody responses in melanoma patients immunized with an anti-idiotype antibody mimicking disialoganglioside GD2. Clin Cancer Res 4:1117–1124

    CAS  PubMed  Google Scholar 

  • Foon KA, Lutzky J, Baral RN, Yannelli JR, Hutchins L, Teitelbaum A, Kashala OL, Das R, Garrison J, Reisfeld RA, Bhattacharya-Chatterjee M (2000) Clinical and immune responses in advanced melanoma patients immunized with an anti-idiotype antibody mimicking disialoganglioside GD2. J Clin Oncol 18:376–384

    Article  CAS  PubMed  Google Scholar 

  • Forster-Waldl E, Riemer AB, Dehof AK, Neumann D, Bramswig K, Boltz-Nitulescu G, Pehamberger H, Zielinski CC, Scheiner O, Pollak A, Lode H, Jensen-Jarolim E (2005) Isolation and structural analysis of peptide mimotopes for the disialoganglioside GD2, a neuroblastoma tumor antigen. Mol Immunol 42:319–325. https://doi.org/10.1016/j.molimm.2004.07.011

    Article  CAS  PubMed  Google Scholar 

  • Furman WL, Federico SM, McCarville MB, Shulkin BL, Davidoff AM, Krasin MJ, Sahr N, Sykes A, Wu J, Brennan RC, Bishop MW, Helmig S, Stewart E, Navid F, Triplett B, Santana VM, Bahrami A, Anthony G, Yu AL, Hank J, Gillies SD, Sondel PM, Leung WH, Pappo AS (2019) A phase II trial of Hu14.18K322A in combination with induction chemotherapy in children with newly diagnosed high-risk neuroblastoma. Clin Cancer Res 25:6320–6328. https://doi.org/10.1158/1078-0432.CCR-19-1452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furman WL, McCarville B, Shulkin BL, Davidoff A, Krasin M, Hsu CW, Pan H, Wu J, Brennan R, Bishop MW, Helmig S, Stewart E, Navid F, Triplett B, Santana V, Santiago T, Hank JA, Gillies SD, Yu A, Sondel PM, Leung WH, Pappo A, Federico SM (2022) Improved outcome in children with newly diagnosed high-risk neuroblastoma treated with chemoimmunotherapy: updated results of a phase II study using hu14.18K322A. J Clin Oncol 40:335–344. https://doi.org/10.1200/JCO.21.01375

    Article  CAS  PubMed  Google Scholar 

  • Furukawa K, Takamiya K, Furukawa K (2002) Beta1,4-N-acetylgalactosaminyltransferase--GM2/GD2 synthase: a key enzyme to control the synthesis of brain-enriched complex gangliosides. Biochim Biophys Acta 1573:356–362

    Article  CAS  PubMed  Google Scholar 

  • Gillies SD, Lo KM, Wesolowski J (1989) High-level expression of chimeric antibodies using adapted cDNA variable region cassettes. J Immunol Methods 125:191–202

    Article  CAS  PubMed  Google Scholar 

  • Gilman AL, Ozkaynak MF, Matthay KK, Krailo M, Yu AL, Gan J, Sternberg A, Hank JA, Seeger R, Reaman GH, Sondel PM (2009) Phase I study of ch14.18 with granulocyte-macrophage colony-stimulating factor and interleukin-2 in children with neuroblastoma after autologous bone marrow transplantation or stem-cell rescue: a report from the children’s oncology group. J Clin Oncol 27:85–91. https://doi.org/10.1200/JCO.2006.10.3564

    Article  CAS  PubMed  Google Scholar 

  • Handgretinger R, Anderson K, Lang P, Dopfer R, Klingebiel T, Schrappe M, Reuland P, Gillies SD, Reisfeld RA, Neithammer D (1995) A phase I study of human/mouse chimeric antiganglioside GD2 antibody ch14.18 in patients with neuroblastoma. Eur J Cancer 31A:261–267

    Article  CAS  PubMed  Google Scholar 

  • Hank JA, Robinson RR, Surfus J, Mueller BM, Reisfeld RA, Cheung NK, Sondel PM (1990) Augmentation of antibody dependent cell mediated cytotoxicity following in vivo therapy with recombinant interleukin 2. Cancer Res 50:5234–5239

    CAS  PubMed  Google Scholar 

  • Heczey A, Liu D, Tian G, Courtney AN, Wei J, Marinova E, Gao X, Guo L, Yvon E, Hicks J, Liu H, Dotti G, Metelitsa LS (2014) Invariant NKT cells with chimeric antigen receptor provide a novel platform for safe and effective cancer immunotherapy. Blood 124:2824–2833. https://doi.org/10.1182/blood-2013-11-541235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heczey A, Courtney AN, Montalbano A, Robinson S, Liu K, Li M, Ghatwai N, Dakhova O, Liu B, Raveh-Sadka T, Chauvin-Fleurence CN, Xu X, Ngai H, Di Pierro EJ, Savoldo B, Dotti G, Metelitsa LS (2020) Anti-GD2 CAR-NKT cells in patients with relapsed or refractory neuroblastoma: an interim analysis. Nat Med 26:1686–1690. https://doi.org/10.1038/s41591-020-1074-2

    Article  CAS  PubMed  Google Scholar 

  • Heiner JP, Miraldi F, Kallick S, Makley J, Neely J, Smith-Mensah WH, Cheung NK (1987) Localization of GD2-specific monoclonal antibody 3F8 in human osteosarcoma. Cancer Res 47:5377–5381

    CAS  PubMed  Google Scholar 

  • Horwacik I, Durbas M, Boratyn E, Wegrzyn P, Rokita H (2013) Targeting GD2 ganglioside and aurora A kinase as a dual strategy leading to cell death in cultures of human neuroblastoma cells. Cancer Lett 341:248–264. https://doi.org/10.1016/j.canlet.2013.08.018

    Article  CAS  PubMed  Google Scholar 

  • Horwacik I, Durbas M, Boratyn E, Sawicka A, Wegrzyn P, Krzanik S, Gorka A, Drozniak J, Augustyniak E, Kowalczyk A, Rokita H (2015) Analysis of genes involved in response to doxorubicin and a GD2 ganglioside-specific 14G2a monoclonal antibody in IMR-32 human neuroblastoma cells. Acta Biochim Pol 62:423–433. https://doi.org/10.18388/abp.2015_1035

    Article  CAS  PubMed  Google Scholar 

  • Irie A, Koyama S, Kozutsumi Y, Kawasaki T, Suzuki A (1998) The molecular basis for the absence of N-glycolylneuraminic acid in humans. J Biol Chem 273:15866–15871. https://doi.org/10.1074/jbc.273.25.15866

    Article  CAS  PubMed  Google Scholar 

  • Jerne NK (1974) Towards a network theory of the immune system. Ann Immunol (Paris) 125C:373–389

    CAS  PubMed  Google Scholar 

  • Kailayangiri S, Altvater B, Meltzer J, Pscherer S, Luecke A, Dierkes C, Titze U, Leuchte K, Landmeier S, Hotfilder M, Dirksen U, Hardes J, Gosheger G, Juergens H, Rossig C (2012) The ganglioside antigen G(D2) is surface-expressed in Ewing sarcoma and allows for MHC-independent immune targeting. Br J Cancer 106:1123–1133. https://doi.org/10.1038/bjc.2012.57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolter T, Proia RL, Sandhoff K (2002) Combinatorial ganglioside biosynthesis. J Biol Chem 277:25859–25862. https://doi.org/10.1074/jbc.R200001200

    Article  CAS  PubMed  Google Scholar 

  • Kowalczyk A, Gil M, Horwacik I, Odrowaz Z, Kozbor D, Rokita H (2009) The GD2-specific 14G2a monoclonal antibody induces apoptosis and enhances cytotoxicity of chemotherapeutic drugs in IMR-32 human neuroblastoma cells. Cancer Lett 281:171–182. https://doi.org/10.1016/j.canlet.2009.02.040

    Article  CAS  PubMed  Google Scholar 

  • Kramer K, Kushner BH, Modak S, Pandit-Taskar N, Smith-Jones P, Zanzonico P, Humm JL, Xu H, Wolden SL, Souweidane MM, Larson SM, Cheung NK (2010) Compartmental intrathecal radioimmunotherapy: results for treatment for metastatic CNS neuroblastoma. J Neuro-Oncol 97:409–418. https://doi.org/10.1007/s11060-009-0038-7

    Article  Google Scholar 

  • Kremens B, Hero B, Esser J, Weinel P, Filger-Brillinger J, Fleischhack G, Graf N, Gruttner HP, Niemeyer C, Schulz A, Wickmann L, Berthold F (2002) Ocular symptoms in children treated with human-mouse chimeric anti-GD2 mAb ch14.18 for neuroblastoma. Cancer Immunol Immunother 51:107–110. https://doi.org/10.1007/s00262-001-0259-x

    Article  CAS  PubMed  Google Scholar 

  • Kushner BH, Cheung IY, Modak S, Kramer K, Ragupathi G, Cheung NK (2014) Phase I trial of a bivalent gangliosides vaccine in combination with beta-glucan for high-risk neuroblastoma in second or later remission. Clin Cancer Res 20:1375–1382. https://doi.org/10.1158/1078-0432.CCR-13-1012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kushner BH, Cheung IY, Modak S, Basu EM, Roberts SS, Cheung NK (2018) Humanized 3F8 anti-GD2 monoclonal antibody dosing with granulocyte-macrophage Colony-stimulating factor in patients with resistant neuroblastoma: A phase 1 clinical trial. JAMA Oncol 4:1729–1735. https://doi.org/10.1001/jamaoncol.2018.4005

    Article  PubMed  PubMed Central  Google Scholar 

  • Ladenstein R, Weixler S, Baykan B, Bleeke M, Kunert R, Katinger D, Pribill I, Glander P, Bauer S, Pistoia V, Michon J, Garaventa A, Lode HN (2013) Ch14.18 antibody produced in CHO cells in relapsed or refractory stage 4 neuroblastoma patients: a SIOPEN phase 1 study. MAbs 5:801–809. https://doi.org/10.4161/mabs.25215

    Article  PubMed  PubMed Central  Google Scholar 

  • Ladenstein R, Potschger U, Valteau-Couanet D, Luksch R, Castel V, Yaniv I, Laureys G, Brock P, Michon JM, Owens C, Trahair T, Chan GCF, Ruud E, Schroeder H, Beck Popovic M, Schreier G, Loibner H, Ambros P, Holmes K, Castellani MR, Gaze MN, Garaventa A, Pearson ADJ, Lode HN (2018) Interleukin 2 with anti-GD2 antibody ch14.18/CHO (dinutuximab beta) in patients with high-risk neuroblastoma (HR-NBL1/SIOPEN): a multicentre, randomised, phase 3 trial. Lancet Oncol 19:1617–1629. https://doi.org/10.1016/S1470-2045(18)30578-3

    Article  CAS  PubMed  Google Scholar 

  • Ladisch S, Becker H, Ulsh L (1992) Immunosuppression by human gangliosides: I. Relationship of carbohydrate structure to the inhibition of T cell responses. Biochim Biophys Acta 1125:180–188

    Article  CAS  PubMed  Google Scholar 

  • Liang YJ, Ding Y, Levery SB, Lobaton M, Handa K, Hakomori SI (2013) Differential expression profiles of glycosphingolipids in human breast cancer stem cells vs. cancer non-stem cells. Proc Natl Acad Sci U S A 110:4968–4973. https://doi.org/10.1073/pnas.1302825110

    Article  PubMed  PubMed Central  Google Scholar 

  • Liao YM, Hung TH, Tung JK, Yu J, Hsu YL, Hung JT, Yu AL (2021) Low expression of IL-15 and NKT in tumor microenvironment predicts poor outcome of MYCN-non-amplified neuroblastoma. J Pers Med 11(2):122. https://doi.org/10.3390/jpm11020122

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin JJ, Huang CS, Yu J, Liao GS, Lien HC, Hung JT, Lin RJ, Chou FP, Yeh KT, Yu AL (2014) Malignant phyllodes tumors display mesenchymal stem cell features and aldehyde dehydrogenase/disialoganglioside identify their tumor stem cells. Breast Cancer Res 16:R29. https://doi.org/10.1186/bcr3631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu B, Wu Y, Zhou Y, Peng D (2014) Endothelin A receptor antagonism enhances inhibitory effects of anti-ganglioside GD2 monoclonal antibody on invasiveness and viability of human osteosarcoma cells. PLoS One 9:e93576. https://doi.org/10.1371/journal.pone.0093576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Louis CU, Savoldo B, Dotti G, Pule M, Yvon E, Myers GD, Rossig C, Russell HV, Diouf O, Liu E, Liu H, Wu MF, Gee AP, Mei Z, Rooney CM, Heslop HE, Brenner MK (2011) Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood 118:6050–6056. https://doi.org/10.1182/blood-2011-05-354449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mao Y, Eissler N, Blanc KL, Johnsen JI, Kogner P, Kiessling R (2016) Targeting suppressive myeloid cells potentiates checkpoint inhibitors to control spontaneous neuroblastoma. Clin Cancer Res 22:3849–3859. https://doi.org/10.1158/1078-0432.CCR-15-1912

    Article  CAS  PubMed  Google Scholar 

  • Merchant MS, Wright M, Baird K, Wexler LH, Rodriguez-Galindo C, Bernstein D, Delbrook C, Lodish M, Bishop R, Wolchok JD, Streicher H, Mackall CL (2016) Phase I clinical trial of ipilimumab in pediatric patients with advanced solid tumors. Clin Cancer Res 22:1364–1370. https://doi.org/10.1158/1078-0432.CCR-15-0491

    Article  CAS  PubMed  Google Scholar 

  • Metelitsa LS, Gillies SD, Super M, Shimada H, Reynolds CP, Seeger RC (2002) Antidisialoganglioside/granulocyte macrophage-colony-stimulating factor fusion protein facilitates neutrophil antibody-dependent cellular cytotoxicity and depends on FcgammaRII (CD32) and Mac-1 (CD11b/CD18) for enhanced effector cell adhesion and azurophil granule exocytosis. Blood 99:4166–4173

    Article  CAS  PubMed  Google Scholar 

  • Metelitsa LS, Wu HW, Wang H, Yang Y, Warsi Z, Asgharzadeh S, Groshen S, Wilson SB, Seeger RC (2004) Natural killer T cells infiltrate neuroblastomas expressing the chemokine CCL2. J Exp Med 199:1213–1221. https://doi.org/10.1084/jem.20031462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michon J, Moutel S, Barbet J, Romet-Lemonne JL, Deo YM, Fridman WH, Teillaud JL (1995) In vitro killing of neuroblastoma cells by neutrophils derived from granulocyte colony-stimulating factor-treated cancer patients using an anti-disialoganglioside/anti-Fc gamma RI bispecific antibody. Blood 86:1124–1130

    Article  CAS  PubMed  Google Scholar 

  • Mody R, Naranjo A, Van Ryn C, Yu AL, London WB, Shulkin BL, Parisi MT, Servaes SE, Diccianni MB, Sondel PM, Bender JG, Maris JM, Park JR, Bagatell R (2017) Irinotecan-temozolomide with temsirolimus or dinutuximab in children with refractory or relapsed neuroblastoma (COG ANBL1221): an open-label, randomised, phase 2 trial. Lancet Oncol 18:946–957. https://doi.org/10.1016/S1470-2045(17)30355-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mody R, Yu AL, Naranjo A, Zhang FF, London WB, Shulkin BL, Parisi MT, Servaes SE, Diccianni MB, Hank JA, Felder M, Birstler J, Sondel PM, Asgharzadeh S, Glade-Bender J, Katzenstein H, Maris JM, Park JR, Bagatell R (2020) Irinotecan, temozolomide, and dinutuximab with GM-CSF in children with refractory or relapsed neuroblastoma: A report from the children’s oncology group. J Clin Oncol 38:2160–2169. https://doi.org/10.1200/JCO.20.00203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Molenaar JJ, Domingo-Fernandez R, Ebus ME, Lindner S, Koster J, Drabek K, Mestdagh P, van Sluis P, Valentijn LJ, van Nes J, Broekmans M, Haneveld F, Volckmann R, Bray I, Heukamp L, Sprussel A, Thor T, Kieckbusch K, Klein-Hitpass L, Fischer M, Vandesompele J, Schramm A, van Noesel MM, Varesio L, Speleman F, Eggert A, Stallings RL, Caron HN, Versteeg R, Schulte JH (2012) LIN28B induces neuroblastoma and enhances MYCN levels via let-7 suppression. Nat Genet 44:1199–1206. https://doi.org/10.1038/ng.2436

    Article  CAS  PubMed  Google Scholar 

  • Mosse YP, Laudenslager M, Longo L, Cole KA, Wood A, Attiyeh EF, Laquaglia MJ, Sennett R, Lynch JE, Perri P, Laureys G, Speleman F, Kim C, Hou C, Hakonarson H, Torkamani A, Schork NJ, Brodeur GM, Tonini GP, Rappaport E, Devoto M, Maris JM (2008) Identification of ALK as a major familial neuroblastoma predisposition gene. Nature 455:930–935. https://doi.org/10.1038/nature07261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mueller BM, Romerdahl CA, Gillies SD, Reisfeld RA (1990) Enhancement of antibody-dependent cytotoxicity with a chimeric anti-GD2 antibody. J Immunol 144:1382–1386

    Article  CAS  PubMed  Google Scholar 

  • Mujoo K, Kipps TJ, Yang HM, Cheresh DA, Wargalla U, Sander DJ, Reisfeld RA (1989) Functional properties and effect on growth suppression of human neuroblastoma tumors by isotype switch variants of monoclonal antiganglioside GD2 antibody 14.18. Cancer Res 49:2857–2861

    CAS  PubMed  Google Scholar 

  • Mullard A (2021) FDA approves fourth CAR-T cell therapy. Nat Rev Drug Discov 20:166. https://doi.org/10.1038/d41573-021-00031-9

    Article  CAS  PubMed  Google Scholar 

  • Murray JL, Cunningham JE, Brewer H, Mujoo K, Zukiwski AA, Podoloff DA, Kasi LP, Bhadkamkar V, Fritsche HA, Benjamin RS et al (1994) Phase I trial of murine monoclonal antibody 14G2a administered by prolonged intravenous infusion in patients with neuroectodermal tumors. J Clin Oncol 12:184–193

    Article  CAS  PubMed  Google Scholar 

  • Navid F, Sondel PM, Barfield R, Shulkin BL, Kaufman RA, Allay JA, Gan J, Hutson P, Seo S, Kim K, Goldberg J, Hank JA, Billups CA, Wu J, Furman WL, McGregor LM, Otto M, Gillies SD, Handgretinger R, Santana VM (2014) Phase I trial of a novel anti-GD2 monoclonal antibody, Hu14.18K322A, designed to decrease toxicity in children with refractory or recurrent neuroblastoma. J Clin Oncol 32:1445–1452. https://doi.org/10.1200/JCO.2013.50.4423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neal ZC, Imboden M, Rakhmilevich AL, Kim KM, Hank JA, Surfus J, Dixon JR, Lode HN, Reisfeld RA, Gillies SD, Sondel PM (2004a) NXS2 murine neuroblastomas express increased levels of MHC class I antigens upon recurrence following NK-dependent immunotherapy. Cancer Immunol Immunother 53:41–52. https://doi.org/10.1007/s00262-003-0435-2

    Article  CAS  PubMed  Google Scholar 

  • Neal ZC, Yang JC, Rakhmilevich AL, Buhtoiarov IN, Lum HE, Imboden M, Hank JA, Lode HN, Reisfeld RA, Gillies SD, Sondel PM (2004b) Enhanced activity of hu14.18-IL2 immunocytokine against murine NXS2 neuroblastoma when combined with interleukin 2 therapy. Clin Cancer Res 10:4839–4847. https://doi.org/10.1158/1078-0432.CCR-03-0799

    Article  CAS  PubMed  Google Scholar 

  • Nishio N, Dotti G (2015) Oncolytic virus expressing RANTES and IL-15 enhances function of CAR-modified T cells in solid tumors. Onco Targets Ther 4:e988098. https://doi.org/10.4161/21505594.2014.988098

    Article  CAS  Google Scholar 

  • Niwa R, Shoji-Hosaka E, Sakurada M, Shinkawa T, Uchida K, Nakamura K, Matsushima K, Ueda R, Hanai N, Shitara K (2004) Defucosylated chimeric anti-CC chemokine receptor 4 IgG1 with enhanced antibody-dependent cellular cytotoxicity shows potent therapeutic activity to T-cell leukemia and lymphoma. Cancer Res 64:2127–2133. https://doi.org/10.1158/0008-5472.can-03-2068

    Article  CAS  PubMed  Google Scholar 

  • Osenga KL, Hank JA, Albertini MR, Gan J, Sternberg AG, Eickhoff J, Seeger RC, Matthay KK, Reynolds CP, Twist C, Krailo M, Adamson PC, Reisfeld RA, Gillies SD, Sondel PM, Children’s Oncology Group (2006) A phase I clinical trial of the hu14.18-IL2 (EMD 273063) as a treatment for children with refractory or recurrent neuroblastoma and melanoma: a study of the children’s oncology group. Clin Cancer Res 12:1750–1759. https://doi.org/10.1158/1078-0432.CCR-05-2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prapa M, Caldrer S, Spano C, Bestagno M, Golinelli G, Grisendi G, Petrachi T, Conte P, Horwitz EM, Campana D, Paolucci P, Dominici M (2015) A novel anti-GD2/4-1BB chimeric antigen receptor triggers neuroblastoma cell killing. Oncotarget 6:24884–24894. https://doi.org/10.18632/oncotarget.4670

    Article  PubMed  PubMed Central  Google Scholar 

  • Pule MA, Savoldo B, Myers GD, Rossig C, Russell HV, Dotti G, Huls MH, Liu E, Gee AP, Mei Z, Yvon E, Weiss HL, Liu H, Rooney CM, Heslop HE, Brenner MK (2008) Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med 14:1264–1270. https://doi.org/10.1038/nm.1882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rafiq S, Hackett CS, Brentjens RJ (2020) Engineering strategies to overcome the current roadblocks in CAR T cell therapy. Nat Rev Clin Oncol 17:147–167. https://doi.org/10.1038/s41571-019-0297-y

    Article  PubMed  Google Scholar 

  • Reis CA, Osorio H, Silva L, Gomes C, David L (2010) Alterations in glycosylation as biomarkers for cancer detection. J Clin Pathol 63:322–329. https://doi.org/10.1136/jcp.2009.071035

    Article  CAS  PubMed  Google Scholar 

  • Riemer AB, Forster-Waldl E, Bramswig KH, Pollak A, Zielinski CC, Pehamberger H, Lode HN, Scheiner O, Jensen-Jarolim E (2006) Induction of IgG antibodies against the GD2 carbohydrate tumor antigen by vaccination with peptide mimotopes. Eur J Immunol 36:1267–1274. https://doi.org/10.1002/eji.200535279

    Article  CAS  PubMed  Google Scholar 

  • Rigo V, Emionite L, Daga A, Astigiano S, Corrias MV, Quintarelli C, Locatelli F, Ferrini S, Croce M (2017) Combined immunotherapy with anti-PDL-1/PD-1 and anti-CD4 antibodies cures syngeneic disseminated neuroblastoma. Sci Rep 7:14049. https://doi.org/10.1038/s41598-017-14417-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruf P, Jager M, Ellwart J, Wosch S, Kusterer E, Lindhofer H (2004) Two new trifunctional antibodies for the therapy of human malignant melanoma. Int J Cancer 108:725–732. https://doi.org/10.1002/ijc.11630

    Article  CAS  PubMed  Google Scholar 

  • Ruf P, Schafer B, Eissler N, Mocikat R, Hess J, Ploscher M, Wosch S, Suckstorff I, Zehetmeier C, Lindhofer H (2012) Ganglioside GD2-specific trifunctional surrogate antibody Surek demonstrates therapeutic activity in a mouse melanoma model. J Transl Med 10:219. https://doi.org/10.1186/1479-5876-10-219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saleh MN, Khazaeli MB, Wheeler RH, Dropcho E, Liu T, Urist M, Miller DM, Lawson S, Dixon P, Russell CH et al (1992) Phase I trial of the murine monoclonal anti-GD2 antibody 14G2a in metastatic melanoma. Cancer Res 52:4342–4347

    CAS  PubMed  Google Scholar 

  • Saleh MN, Stapleton JD, Khazaeli MB, LoBuglio AF (1993) Generation of a human anti-idiotypic antibody that mimics the GD2 antigen. J Immunol 151:3390–3398

    Article  CAS  PubMed  Google Scholar 

  • Saletta F, Vilain RE, Gupta AK, Nagabushan S, Yuksel A, Catchpoole D, Scolyer RA, Byrne JA, McCowage G (2017) Programmed death-ligand 1 expression in a large cohort of pediatric patients with solid tumor and association with clinicopathologic features in neuroblastoma. JCO Precis Oncol 1:1–12. https://doi.org/10.1200/PO.16.00049

    Article  PubMed  Google Scholar 

  • Schulz G, Cheresh DA, Varki NM, Yu A, Staffileno LK, Reisfeld RA (1984) Detection of ganglioside GD2 in tumor tissues and sera of neuroblastoma patients. Cancer Res 44:5914–5920

    CAS  PubMed  Google Scholar 

  • Scursoni AM, Galluzzo L, Camarero S, Lopez J, Lubieniecki F, Sampor C, Segatori VI, Gabri MR, Alonso DF, Chantada G, de Davila MT (2011) Detection of N-glycolyl GM3 ganglioside in neuroectodermal tumors by immunohistochemistry: an attractive vaccine target for aggressive pediatric cancer. Clin Dev Immunol 2011:245181. https://doi.org/10.1155/2011/245181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seeger RC, Brodeur GM, Sather H, Dalton A, Siegel SE, Wong KY, Hammond D (1985) Association of multiple copies of the N-myc oncogene with rapid progression of neuroblastomas. N Engl J Med 313:1111–1116. https://doi.org/10.1056/NEJM198510313131802

    Article  CAS  PubMed  Google Scholar 

  • Shirinbak S, Chan RY, Shahani S, Muthugounder S, Kennedy R, Hung LT, Fernandez GE, Hadjidaniel MD, Moghimi B, Sheard MA, Epstein AL, Fabbri M, Shimada H, Asgharzadeh S (2021) Combined immune checkpoint blockade increases CD8+CD28+PD-1+ effector T cells and provides a therapeutic strategy for patients with neuroblastoma. Onco Targets Ther 10:1838140. https://doi.org/10.1080/2162402X.2020.1838140

    Article  Google Scholar 

  • Shusterman S, London WB, Gillies SD, Hank JA, Voss SD, Seeger RC, Reynolds CP, Kimball J, Albertini MR, Wagner B, Gan J, Eickhoff J, DeSantes KB, Cohn SL, Hecht T, Gadbaw B, Reisfeld RA, Maris JM, Sondel PM (2010) Antitumor activity of hu14.18-IL2 in patients with relapsed/refractory neuroblastoma: a children’s oncology group (COG) phase II study. J Clin Oncol 28:4969–4975. https://doi.org/10.1200/JCO.2009.27.8861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siebert N, Zumpe M, Juttner M, Troschke-Meurer S, Lode HN (2017) PD-1 blockade augments anti-neuroblastoma immune response induced by anti-GD2 antibody ch14.18/CHO. Onco Targets Ther 6:e1343775. https://doi.org/10.1080/2162402X.2017.1343775

    Article  Google Scholar 

  • Sjoberg ER, Varki A (1993) Kinetic and spatial interrelationships between ganglioside glycosyltransferases and O-acetyltransferase(s) in human melanoma cells. J Biol Chem 268:10185–10196

    Article  CAS  PubMed  Google Scholar 

  • Song L, Ara T, Wu HW, Woo CW, Reynolds CP, Seeger RC, DeClerck YA, Thiele CJ, Sposto R, Metelitsa LS (2007) Oncogene MYCN regulates localization of NKT cells to the site of disease in neuroblastoma. J Clin Invest 117:2702–2712. https://doi.org/10.1172/JCI30751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sorkin LS, Otto M, Baldwin WM 3rd, Vail E, Gillies SD, Handgretinger R, Barfield RC, Ming Yu H, Yu AL (2010) Anti-GD(2) with an FC point mutation reduces complement fixation and decreases antibody-induced allodynia. Pain 149:135–142. https://doi.org/10.1016/j.pain.2010.01.024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Svennerholm L, Bostrom K, Fredman P, Jungbjer B, Lekman A, Mansson JE, Rynmark BM (1994) Gangliosides and allied glycosphingolipids in human peripheral nerve and spinal cord. Biochim Biophys Acta 1214:115–123

    Article  CAS  PubMed  Google Scholar 

  • Swaminathan A, Lucas RM, Dear K, McMichael AJ (2014) Keyhole limpet haemocyanin - a model antigen for human immunotoxicological studies. Br J Clin Pharmacol 78:1135–1142. https://doi.org/10.1111/bcp.12422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tarr PE (1996) Granulocyte-macrophage colony-stimulating factor and the immune system. Med Oncol 13:133–140. https://doi.org/10.1007/BF02990841

    Article  CAS  PubMed  Google Scholar 

  • Terme M, Dorvillius M, Cochonneau D, Chaumette T, Xiao W, Diccianni MB, Barbet J, Yu AL, Paris F, Sorkin LS, Birkle S (2014) Chimeric antibody c.8B6 to O-acetyl-GD2 mediates the same efficient anti-neuroblastoma effects as therapeutic ch14.18 antibody to GD2 without antibody induced allodynia. PLoS One 9:e87210. https://doi.org/10.1371/journal.pone.0087210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Theruvath J, Menard M, Smith BAH, Linde MH, Coles GL, Dalton GN, Wu W, Kiru L, Delaidelli A, Sotillo E, Silberstein JL, Geraghty AC, Banuelos A, Radosevich MT, Dhingra S, Heitzeneder S, Tousley A, Lattin J, Xu P, Huang J, Nasholm N, He A, Kuo TC, Sangalang ERB, Pons J, Barkal A, Brewer RE, Marjon KD, Vilches-Moure JG, Marshall PL, Fernandes R, Monje M, Cochran JR, Sorensen PH, Daldrup-Link HE, Weissman IL, Sage J, Majeti R, Bertozzi CR, Weiss WA, Mackall CL, Majzner RG (2022) Anti-GD2 synergizes with CD47 blockade to mediate tumor eradication. Nat Med 28:333–344. https://doi.org/10.1038/s41591-021-01625-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tong W, Maira M, Gagnon M, Saragovi HU (2015) Ligands binding to cell surface ganglioside GD2 cause Src-dependent activation of N-methyl-D-aspartate receptor signaling and changes in cellular morphology. PLoS One 10:e0134255. https://doi.org/10.1371/journal.pone.0134255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trochet D, Bourdeaut F, Janoueix-Lerosey I, Deville A, de Pontual L, Schleiermacher G, Coze C, Philip N, Frebourg T, Munnich A, Lyonnet S, Delattre O, Amiel J (2004) Germline mutations of the paired-like homeobox 2B (PHOX2B) gene in neuroblastoma. Am J Hum Genet 74:761–764. https://doi.org/10.1086/383253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsao CY, Sabbatino F, Cheung NV, Hsu JC, Villani V, Wang X, Ferrone S (2015) Anti-proliferative and pro-apoptotic activity of GD2 ganglioside-specific monoclonal antibody 3F8 in human melanoma cells. Onco Targets Ther 4:e1023975. https://doi.org/10.1080/2162402X.2015.1023975

    Article  CAS  Google Scholar 

  • Tse BC, Navid F, Billups CA, O’Donnell T, Hoehn ME (2015) Ocular abnormalities in patients treated with a novel anti-GD2 monoclonal antibody, hu14.18K322A. J AAPOS 19:112–115. https://doi.org/10.1016/j.jaapos.2014.11.005

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsuchida T, Saxton RE, Morton DL, Irie RF (1987) Gangliosides of human melanoma. J Natl Cancer Inst 78:45–54

    Article  CAS  PubMed  Google Scholar 

  • Tumino N, Weber G, Besi F, Del Bufalo F, Bertaina V, Paci P, Quatrini L, Antonucci L, Sinibaldi M, Quintarelli C, Maggi E, De Angelis B, Locatelli F, Moretta L, Vacca P, Caruana I (2021) Polymorphonuclear myeloid-derived suppressor cells impair the anti-tumor efficacy of GD2.CAR T-cells in patients with neuroblastoma. J Hematol Oncol 14:191. https://doi.org/10.1186/s13045-021-01193-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uttenreuther-Fischer MM, Huang CS, Reisfeld RA, Yu AL (1995a) Pharmacokinetics of anti-ganglioside GD2 mAb 14G2a in a phase I trial in pediatric cancer patients. Cancer Immunol Immunother 41:29–36

    Article  CAS  PubMed  Google Scholar 

  • Uttenreuther-Fischer MM, Huang CS, Yu AL (1995b) Pharmacokinetics of human-mouse chimeric anti-GD2 mAb ch14.18 in a phase I trial in neuroblastoma patients. Cancer Immunol Immunother 41:331–338

    Article  CAS  PubMed  Google Scholar 

  • Vazquez AM, Alfonso M, Lanne B, Karlsson KA, Carr A, Barroso O, Fernandez LE, Rengifo E, Lanio ME, Alvarez C et al (1995) Generation of a murine monoclonal antibody specific for N-glycolylneuraminic acid-containing gangliosides that also recognizes sulfated glycolipids. Hybridoma 14:551–556. https://doi.org/10.1089/hyb.1995.14.551

    Article  CAS  PubMed  Google Scholar 

  • Vazquez AM, Perez A, Hernandez AM, Macias A, Alfonso M, Bombino G, Perez R (1998) Syngeneic anti-idiotypic monoclonal antibodies to an anti-NeuGc-containing ganglioside monoclonal antibody. Hybridoma 17:527–534. https://doi.org/10.1089/hyb.1998.17.527

    Article  CAS  PubMed  Google Scholar 

  • Vazquez AM, Gabri MR, Hernandez AM, Alonso DF, Beausoleil I, Gomez DE, Perez R (2000) Antitumor properties of an anti-idiotypic monoclonal antibody in relation to N-glycolyl-containing gangliosides. Oncol Rep 7:751–756. https://doi.org/10.3892/or.7.4.751

    Article  CAS  PubMed  Google Scholar 

  • Wierzbicki A, Gil M, Ciesielski M, Fenstermaker RA, Kaneko Y, Rokita H, Lau JT, Kozbor D (2008) Immunization with a mimotope of GD2 ganglioside induces CD8+ T cells that recognize cell adhesion molecules on tumor cells. J Immunol 181:6644–6653

    Article  CAS  PubMed  Google Scholar 

  • Wu ZL, Schwartz E, Seeger R, Ladisch S (1986) Expression of GD2 ganglioside by untreated primary human neuroblastomas. Cancer Res 46:440–443

    CAS  PubMed  Google Scholar 

  • Xu H, Cheng M, Guo H, Chen Y, Huse M, Cheung NK (2015) Retargeting T cells to GD2 pentasaccharide on human tumors using bispecific humanized antibody. Cancer Immunol Res 3:266–277. https://doi.org/10.1158/2326-6066.CIR-14-0230-T

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Huang W, Heczey A, Liu D, Guo L, Wood M, Jin J, Courtney AN, Liu B, Di Pierro EJ, Hicks J, Barragan GA, Ngai H, Chen Y, Savoldo B, Dotti G, Metelitsa LS (2019) NKT cells co-expressing a GD2-specific chimeric antigen receptor and IL15 show enhanced in vivo persistence and antitumor activity against neuroblastoma. Clin Cancer Res 25:7126–7138. https://doi.org/10.1158/1078-0432.CCR-19-0421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yankelevich M, Kondadasula SV, Thakur A, Buck S, Cheung NK, Lum LG (2012) Anti-CD3 x anti-GD2 bispecific antibody redirects T-cell cytolytic activity to neuroblastoma targets. Pediatr Blood Cancer 59:1198–1205. https://doi.org/10.1002/pbc.24237

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu AL, Uttenreuther-Fischer MM, Kamps A (1995) Combined use of a human mouse chimeric anti-GD2 (ch14.18) and GM-CSF in the treatment of refractory neuroblastoma. Antibody Immunocon Radiopharm 8:12

    Google Scholar 

  • Yu AL, Batova A, Alvarado C, Rao VJ, Castleberry RP (1997) Usefulness of a chimeric anti-GD2 (ch14.18) and GM-CSF for refractory neuroblastoma: a POG phase II study. PROC ASCO 16:1846

    Google Scholar 

  • Yu AL, Uttenreuther-Fischer MM, Huang CS, Tsui CC, Gillies SD, Reisfeld RA, Kung FH (1998) Phase I trial of a human-mouse chimeric anti-disialoganglioside monoclonal antibody ch14.18 in patients with refractory neuroblastoma and osteosarcoma. J Clin Oncol 16:2169–2180

    Article  CAS  PubMed  Google Scholar 

  • Yu AL, Eskenazi A, Strother D (2001) A piot study of anti-idiotype monoclonal antibody as tumor vaccine in patients with high risk neuroblastoma. Proc Am Soc Clin Oncol 20(abstr 1470):18s

    Google Scholar 

  • Yu AL, Gilman AL, Ozkaynak MF, London WB, Kreissman SG, Chen HX, Smith M, Anderson B, Villablanca JG, Matthay KK, Shimada H, Grupp SA, Seeger R, Reynolds CP, Buxton A, Reisfeld RA, Gillies SD, Cohn SL, Maris JM, Sondel PM (2010) Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med 363:1324–1334. https://doi.org/10.1056/NEJMoa0911123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu AL, Gilman AL, Ozkaynak MF, Naranjo A, Diccianni MB, Gan J, Hank JA, Batova A, London WB, Tenney SC, Smith M, Shulkin BL, Parisi M, Matthay KK, Cohn SL, Maris JM, Bagatell R, Park JR, Sondel PM (2021) Long-term follow-up of a phase III study of ch14.18 (dinutuximab) + cytokine immunotherapy in children with high-risk neuroblastoma: COG study ANBL0032. Clin Cancer Res 27:2179–2189. https://doi.org/10.1158/1078-0432.CCR-20-3909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu L, Huang L, Lin D, Lai X, Wu L, Liao X, Liu J, Zeng Y, Liang L, Zhang G, Wang B, Wu Z, Tao S, Liu Y, Jiao C, Chang LJ, Yang L (2022) GD2-specific chimeric antigen receptor-modified T cells for the treatment of refractory and/or recurrent neuroblastoma in pediatric patients. J Cancer Res Clin Oncol 148(10):2643–2652. https://doi.org/10.1007/s00432-021-03839-5

    Article  CAS  PubMed  Google Scholar 

  • Yuki N, Yamada M, Tagawa Y, Takahashi H, Handa S (1997) Pathogenesis of the neurotoxicity caused by anti-GD2 antibody therapy. J Neurol Sci 149:127–130

    Article  CAS  PubMed  Google Scholar 

  • Zeng Y, Fest S, Kunert R, Katinger H, Pistoia V, Michon J, Lewis G, Ladenstein R, Lode HN (2005) Anti-neuroblastoma effect of ch14.18 antibody produced in CHO cells is mediated by NK-cells in mice. Mol Immunol 42:1311–1319. https://doi.org/10.1016/j.molimm.2004.12.018

    Article  CAS  PubMed  Google Scholar 

  • Zeytin HE, Tripathi PK, Bhattacharya-Chatterjee M, Foon KA, Chatterjee SK (2000) Construction and characterization of DNA vaccines encoding the single-chain variable fragment of the anti-idiotype antibody 1A7 mimicking the tumor-associated antigen disialoganglioside GD2. Cancer Gene Ther 7:1426–1436. https://doi.org/10.1038/sj.cgt.7700240

    Article  CAS  PubMed  Google Scholar 

  • Zhao Q, Ahmed M, Guo HF, Cheung IY, Cheung NK (2015) Alteration of electrostatic surface potential enhances affinity and tumor killing properties of anti-ganglioside GD2 monoclonal antibody hu3F8. J Biol Chem 290:13017–13027. https://doi.org/10.1074/jbc.M115.650903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zirngibl F, Ivasko SM, Grunewald L, Klaus A, Schwiebert S, Ruf P, Lindhofer H, Astrahantseff K, Andersch L, Schulte JH, Lode HN, Eggert A, Anders K, Hundsdoerfer P, Kunkele A (2021) GD2-directed bispecific trifunctional antibody outperforms dinutuximab beta in a murine model for aggressive metastasized neuroblastoma. J Immunother Cancer 9(7):e002923. https://doi.org/10.1136/jitc-2021-002923

    Article  PubMed  PubMed Central  Google Scholar 

  • Zuo S, Sho M, Sawai T, Kanehiro H, Maeda K, Yoshida M, Tsukada R, Nomura M, Okuyama H (2020) Potential role of the PD-L1 expression and tumor-infiltrating lymphocytes on neuroblastoma. Pediatr Surg Int 36:137–143. https://doi.org/10.1007/s00383-019-04616-9

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Stem Cell and Translational Cancer Research, Chang Gung Memorial Hospital at Linkou, Taoyuan, Taiwan

    Jung-Tung Hung & Alice L. Yu

  2. Department of Pediatric, University of California San Diego, La Jolla, CA, USA

    Alice L. Yu

Authors
  1. Jung-Tung Hung
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alice L. Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alice L. Yu .

Editor information

Editors and Affiliations

  1. Department of Biomedical Sciences, Chubu University College of Life and Health Sciences, Kasugai, Aichi, Japan

    Koichi Furukawa

  2. Glycobiology Unit, Sanford-Burnham Medical Research Institute, La Jolla, CA, USA

    Minoru Fukuda

Rights and permissions

Reprints and permissions

Copyright information

© 2023 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Hung, JT., Yu, A.L. (2023). Immunotherapy of Neuroblastoma Targeting GD2 and Beyond. In: Furukawa, K., Fukuda, M. (eds) Glycosignals in Cancer. Springer, Singapore. https://doi.org/10.1007/978-981-19-7732-9_10

Download citation

Publish with us

Policies and ethics

Search

Navigation