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Review

Monoclonal Antibody Therapies for High Risk Neuroblastoma

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Pages 205-219 | Published online: 09 Jun 2021

References

  • Yoshida S, Kawaguchi H, Sato S, Ueda R, Furukawa K. An anti-GD2 monoclonal antibody enhances apoptotic effects of anti-cancer drugs against small cell lung cancer cells via JNK (c-Jun terminal kinase) activation. Jpn J Cancer Res. 2002;93(7):816–824. doi:10.1111/j.1349-7006.2002.tb01324.x
  • Kowalczyk A, Gil M, Horwacik I, Odrowaz Z, Kozbor D, Rokita H. The GD2-specific 14G2a monoclonal antibody induces apoptosis and enhances cytotoxicity of chemotherapeutic drugs in IMR-32 human neuroblastoma cells. Cancer Lett. 2009;281(2):171–182. doi:10.1016/j.canlet.2009.02.040
  • Doronin II, Vishnyakova PA, Kholodenko IV, et al. Ganglioside GD2 in reception and transduction of cell death signal in tumor cells. BMC Cancer. 2014;14:295. doi:10.1186/1471-2407-14-295
  • Weiner LM, Surana R, Wang S. Monoclonal antibodies: versatile platforms for cancer immunotherapy. Nat Rev Immunol. 2010;10(5):317–327. doi:10.1038/nri2744
  • Shuptrine CW, Surana R, Weiner LM. Monoclonal antibodies for the treatment of cancer. Semin Cancer Biol. 2012;22(1):3–13. doi:10.1016/j.semcancer.2011.12.009
  • Dickson PV, Hamner JB, Sims TL, et al. Bevacizumab-induced transient remodeling of the vasculature in neuroblastoma xenografts results in improved delivery and efficacy of systemically administered chemotherapy. Clin Cancer Res. 2007;13(13):3942–3950. doi:10.1158/1078-0432.CCR-07-0278
  • Sano R, Krytska K, Larmour CE, et al. An antibody-drug conjugate directed to the ALK receptor demonstrates efficacy in preclinical models of neuroblastoma. Sci Transl Med. 2019;11:483. doi:10.1126/scitranslmed.aau9732
  • Brown BS, Patanam T, Mobli K, et al. Etoposide-loaded immunoliposomes as active targeting agents for GD2-positive malignancies. Cancer Biol Ther. 2014;15(7):851–861. doi:10.4161/cbt.28875
  • Tur MK, Sasse S, Stocker M, et al. An anti-GD2 single chain Fv selected by phage display and fused to Pseudomonas exotoxin A develops specific cytotoxic activity against neuroblastoma derived cell lines. Int J Mol Med. 2001;8(5):579–584. doi:10.3892/ijmm.8.5.579
  • Kramer K, Kushner BH, Modak S, et al. Compartmental intrathecal radioimmunotherapy: results for treatment for metastatic CNS neuroblastoma. J Neurooncol. 2010;97(3):409–418. doi:10.1007/s11060-009-0038-7
  • Kramer K, Humm JL, Souweidane MM, et al. Phase I study of targeted radioimmunotherapy for leptomeningeal cancers using intra-Ommaya 131-I-3F8. J Clin Oncol. 2007;25(34):5465–5470. doi:10.1200/JCO.2007.11.1807
  • Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer. 2012;12(4):252–264. doi:10.1038/nrc3239
  • Hoehner JC, Gestblom C, Hedborg F, Sandstedt B, Olsen L, Pahlman S. A developmental model of neuroblastoma: differentiating stroma-poor tumors’ progress along an extra-adrenal chromaffin lineage. Lab Investig. 1996;75(5):659–675.
  • Maris JM, Hogarty MD, Bagatell R, Cohn SL. Neuroblastoma. Lancet. 2007;369(9579):2106–2120. doi:10.1016/S0140-6736(07)60983-0
  • Matthay KK, Maris JM, Schleiermacher G, et al. Neuroblastoma. Nat Rev Dis Primers. 2016;2:16078. doi:10.1038/nrdp.2016.78
  • Maris JM. The biologic basis for neuroblastoma heterogeneity and risk stratification. Curr Opin Pediatr. 2005;17(1):7–13. doi:10.1097/01.mop.0000150631.60571.89
  • Maris JM. Recent advances in neuroblastoma. N Engl J Med. 2010;362(23):2202–2211. doi:10.1056/NEJMra0804577
  • Schultz LM, Majzner R, Davis KL, Mackall C. New developments in immunotherapy for pediatric solid tumors. Curr Opin Pediatr. 2018;30(1):30–39. doi:10.1097/MOP.0000000000000564
  • Mujoo K, Cheresh DA, Yang HM, Reisfeld RA. Disialoganglioside GD2 on human neuroblastoma cells: target antigen for monoclonal antibody-mediated cytolysis and suppression of tumor growth. Cancer Res. 1987;47(4):1098–1104.
  • Wu ZL, Schwartz E, Seeger R, Ladisch S. Expression of GD2 ganglioside by untreated primary human neuroblastomas. Cancer Res. 1986;46(1):440–443.
  • Cheung NK, Lazarus H, Miraldi FD, et al. Ganglioside GD2 specific monoclonal antibody 3F8: a phase I study in patients with neuroblastoma and malignant melanoma. J Clin Oncol. 1987;5(9):1430–1440. doi:10.1200/JCO.1987.5.9.1430
  • Mujoo K, Kipps TJ, Yang HM, et al. Functional properties and effect on growth suppression of human neuroblastoma tumors by isotype switch variants of monoclonal antiganglioside GD2 antibody 14.18. Cancer Res. 1989;49(11):2857–2861.
  • Murray JL, Cunningham JE, Brewer H, et al. Phase I trial of murine monoclonal antibody 14G2a administered by prolonged intravenous infusion in patients with neuroectodermal tumors. J Clin Oncol. 1994;12(1):184–193. doi:10.1200/JCO.1994.12.1.184
  • Barker E, Mueller BM, Handgretinger R, Herter M, Yu AL, Reisfeld RA. Effect of a chimeric anti-ganglioside GD2 antibody on cell-mediated lysis of human neuroblastoma cells. Cancer Res. 1991;51(1):144–149.
  • Yu AL, Gilman AL, Ozkaynak MF, et al. Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med. 2010;363(14):1324–1334. doi:10.1056/NEJMoa0911123
  • Zeng Y, Fest S, Kunert R, et al. Anti-neuroblastoma effect of ch14.18 antibody produced in CHO cells is mediated by NK-cells in mice. Mol Immunol. 2005;42(11):1311–1319. doi:10.1016/j.molimm.2004.12.018
  • Horta ZP, Goldberg JL, Sondel PM. Anti-GD2 mAbs and next-generation mAb-based agents for cancer therapy. Immunotherapy. 2016;8(9):1097–1117. doi:10.2217/imt-2016-0021
  • Alvarez-Rueda N, Leprieur S, Clemenceau B, et al. Binding activities and antitumor properties of a new mouse/human chimeric antibody specific for GD2 ganglioside antigen. Clin Cancer Res. 2007;13(18):5613s–5620s. doi:10.1158/1078-0432.CCR-07-1057
  • Nazha B, Inal C, Owonikoko TK. Disialoganglioside GD2 expression in solid tumors and role as a target for cancer therapy. Front Oncol. 2020;10:1000. doi:10.3389/fonc.2020.01000
  • Cheung NK, Saarinen UM, Neely JE, Landmeier B, Donovan D, Coccia PF. Monoclonal antibodies to a glycolipid antigen on human neuroblastoma cells. Cancer Res. 1985;45(6):2642–2649.
  • Lammie G, Cheung N, Gerald W, Rosenblum M, Cordoncardo C. Ganglioside gd(2) expression in the human nervous-system and in neuroblastomas - an immunohistochemical study. Int J Oncol. 1993;3(5):909–915. doi:10.3892/ijo.3.5.909
  • Jin HJ, Nam HY, Bae YK, et al. GD2 expression is closely associated with neuronal differentiation of human umbilical cord blood-derived mesenchymal stem cells. Cell Mol Life Sci. 2010;67(11):1845–1858. doi:10.1007/s00018-010-0292-z
  • Martinez C, Hofmann TJ, Marino R, Dominici M, Horwitz EM. Human bone marrow mesenchymal stromal cells express the neural ganglioside GD2: a novel surface marker for the identification of MSCs. Blood. 2007;109(10):4245–4248. doi:10.1182/blood-2006-08-039347
  • Suzuki M, Cheung NK. Disialoganglioside GD2 as a therapeutic target for human diseases. Expert Opin Ther Targets. 2015;1–14.
  • Cavdarli S, Groux-Degroote S, Delannoy P. Gangliosides: the double-edge sword of neuro-ectodermal derived tumors. Biomolecules. 2019;9(8):311. doi:10.3390/biom9080311
  • Navid F, Santana VM, Barfield RC. Anti-GD2 antibody therapy for GD2-expressing tumors. Curr Cancer Drug Targets. 2010;10(2):200–209. doi:10.2174/156800910791054167
  • Cheresh DA, Pierschbacher MD, Herzig MA, Mujoo K. Disialogangliosides GD2 and GD3 are involved in the attachment of human melanoma and neuroblastoma cells to extracellular matrix proteins. J Cell Biol. 1986;102(3):688–696. doi:10.1083/jcb.102.3.688
  • Yuki N, Yamada M, Tagawa Y, Takahashi H, Handa S. Pathogenesis of the neurotoxicity caused by anti-GD2 antibody therapy. J Neurol Sci. 1997;149(2):127–130. doi:10.1016/S0022-510X(97)05390-2
  • Sorkin LS, Otto M, Baldwin WM, et al. Anti-GD(2) with an FC point mutation reduces complement fixation and decreases antibody-induced allodynia. Pain. 2010;149(1):135–142. doi:10.1016/j.pain.2010.01.024
  • Baluna R, Vitetta ES. Vascular leak syndrome: a side effect of immunotherapy. Immunopharmacology. 1997;37(2–3):117–132. doi:10.1016/S0162-3109(97)00041-6
  • Matthay KK. Interleukin 2 plus anti-GD2 immunotherapy: helpful or harmful? Lancet Oncol. 2018;19(12):1549–1551. doi:10.1016/S1470-2045(18)30627-2
  • Kushner BH, Cheung NK. GM-CSF enhances 3F8 monoclonal antibody-dependent cellular cytotoxicity against human melanoma and neuroblastoma. Blood. 1989;73(7):1936–1941. doi:10.1182/blood.V73.7.1936.1936
  • Cheung NK, Kushner BH, Cheung IY, et al. Anti-G(D2) antibody treatment of minimal residual stage 4 neuroblastoma diagnosed at more than 1 year of age. J Clin Oncol. 1998;16(9):3053–3060. doi:10.1200/JCO.1998.16.9.3053
  • Kushner BH, Kramer K, Cheung NK. Phase II trial of the anti-G(D2) monoclonal antibody 3F8 and granulocyte-macrophage colony-stimulating factor for neuroblastoma. J Clin Oncol. 2001;19(22):4189–4194. doi:10.1200/JCO.2001.19.22.4189
  • Cheung IY, Hsu K, Cheung NK. Activation of peripheral-blood granulocytes is strongly correlated with patient outcome after immunotherapy with anti-GD2 monoclonal antibody and granulocyte-macrophage colony-stimulating factor. J Clin Oncol. 2012;30(4):426–432. doi:10.1200/JCO.2011.37.6236
  • Cheung NK, Modak S. Oral (1–>3),(1–>4)-beta-D-glucan synergizes with antiganglioside GD2 monoclonal antibody 3F8 in the therapy of neuroblastoma. Clin Cancer Res. 2002;8(5):1217–1223.
  • Cheung NK, Kushner BH, Yeh SD, Larson SM. 3F8 monoclonal antibody treatment of patients with stage 4 neuroblastoma: a phase II study. Int J Oncol. 1998;12(6):1299–1306. doi:10.3892/ijo.12.6.1299
  • Johnson E, Dean SM, Sondel PM. Antibody-based immunotherapy in high-risk neuroblastoma. Expert Rev Mol Med. 2007;9(34):1–21. doi:10.1017/S1462399407000518
  • Cheung NK, Cheung IY, Kramer K, et al. 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. 2014;135(9):2199–2205.
  • Cheung NK, Cheung IY, Kushner BH, et al. 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. 2012;30(26):3264–3270. doi:10.1200/JCO.2011.41.3807
  • Kushner BH, Ostrovnaya I, Cheung IY, et al. Prolonged progression-free survival after consolidating second or later remissions of neuroblastoma with anti-GD2 immunotherapy and isotretinoin: a prospective Phase II study. Oncoimmunology. 2015;4(7):e1016704. doi:10.1080/2162402X.2015.1016704
  • Cheung IY, Kushner BH, Modak S, Basu EM, Roberts SS, Cheung NV. 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. Oncoimmunology. 2017;6(11):e1358331. doi:10.1080/2162402X.2017.1358331
  • Handgretinger R, Baader P, Dopfer R, et al. A phase I study of neuroblastoma with the anti-ganglioside GD2 antibody 14.G2a. Cancer Immunol Immunother. 1992;35(3):199–204. doi:10.1007/BF01756188
  • Frost JD, Hank JA, Reaman GH, et al. A phase I/IB trial of murine monoclonal anti-GD2 antibody 14.G2a plus interleukin-2 in children with refractory neuroblastoma: a report of the Children’s Cancer Group. Cancer. 1997;80(2):317–333. doi:10.1002/(SICI)1097-0142(19970715)80:2<317::AID-CNCR21>3.0.CO;2-W
  • Cheung NK, Cheung IY, Canete A, et al. Antibody response to murine anti-GD2 monoclonal antibodies: correlation with patient survival. Cancer Res. 1994;54(8):2228–2233.
  • Lu RM, Hwang YC, Liu IJ, et al. Development of therapeutic antibodies for the treatment of diseases. J Biomed Sci. 2020;27(1):1.
  • Mueller BM, Romerdahl CA, Gillies SD, Reisfeld RA. Enhancement of antibody-dependent cytotoxicity with a chimeric anti-GD2 antibody. J Immunol. 1990;144(4):1382–1386.
  • Handgretinger R, Anderson K, Lang P, et al. A phase I study of human/mouse chimeric antiganglioside GD2 antibody ch14.18 in patients with neuroblastoma. EurJ Cancer. 1995;31(2):261–267. doi:10.1016/0959-8049(94)00413-Y
  • Yu AL, Uttenreuther-Fischer MM, Huang CS, et al. Phase I trial of a human-mouse chimeric anti-disialoganglioside monoclonal antibody ch14.18 in patients with refractory neuroblastoma and osteosarcoma. J Clin Oncol. 1998;16(6):2169–2180. doi:10.1200/JCO.1998.16.6.2169
  • Murray JL, Kleinerman ES, Jia SF, et al. Phase Ia/Ib trial of anti-GD2 chimeric monoclonal antibody 14.18 (ch14.18) and recombinant human granulocyte-macrophage colony-stimulating factor (rhGM-CSF) in metastatic melanoma. J Immunother Emphasis Tumor Immunol. 1996;19(3):206–217. doi:10.1097/00002371-199605000-00005
  • Saleh MN, Khazaeli MB, Wheeler RH, et al. Phase I trial of the chimeric anti-GD2 monoclonal antibody ch14.18 in patients with malignant melanoma. Hum Antibodies Hybridomas. 1992;3(1):19–24. doi:10.3233/HAB-1992-3104
  • Albertini MR, Gan J, Jaeger P, et al. Systemic interleukin-2 modulates the anti-idiotypic response to chimeric anti-GD2 antibody in patients with melanoma. J Immunother Emphasis Tumor Immunol. 1996;19(4):278–295.
  • Albertini MR, Hank JA, Schiller JH, et al. Phase IB trial of chimeric antidisialoganglioside antibody plus interleukin 2 for melanoma patients. Clin Cancer Res. 1997;3(8):1277–1288.
  • Yu AL, Batova A, Alvarado C, et al. Usefulness of a chimeric anti-GD2 (ch14.18) and GM-CSF for refractory neuroblastoma: a POG phase II study. PROC ASCO. 1997;16:1846.
  • Ozkaynak MF, Sondel PM, Krailo MD, et al. Phase I study of chimeric human/murine anti-ganglioside G(D2) monoclonal antibody (ch14.18) with granulocyte-macrophage colony-stimulating factor in children with neuroblastoma immediately after hematopoietic stem-cell transplantation: a Children’s Cancer Group Study. J Clin Oncol. 2000;18(24):4077–4085. doi:10.1200/JCO.2000.18.24.4077
  • Simon T, Hero B, Faldum A, et al. Consolidation treatment with chimeric anti-GD2-antibody ch14.18 in children older than 1 year with metastatic neuroblastoma. J Clin Oncol. 2004;22(17):3549–3557. doi:10.1200/JCO.2004.08.143
  • Gilman AL, Ozkaynak MF, Matthay KK, et al. 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. 2009;27(1):85–91. doi:10.1200/JCO.2006.10.3564
  • Mody R, Naranjo A, Van Ryn C, et al. Irinotecan-temozolomide with temsirolimus or dinutuximab in children with refractory or relapsed neuroblastoma (COG ANBL1221): an open-label, randomised, Phase 2 trial. Lancet Oncol. 2017;18(7):946–957. doi:10.1016/S1470-2045(17)30355-8
  • Mody R, Yu AL, Naranjo A, et al. 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. 2020;38(19):2160–2169. doi:10.1200/JCO.20.00203
  • EMA approval of dinutuximab beta; 2020. Available from: https://www.ema.europa.eu/en/medicines/human/EPAR/qarziba. Accessed September 10, 2020.
  • Ladenstein R, Weixler S, Baykan B, et al. Ch14.18 antibody produced in CHO cells in relapsed or refractory Stage 4 neuroblastoma patients: a SIOPEN Phase 1 study. mAbs. 2013;5(5):801–809. doi:10.4161/mabs.25215
  • Ladenstein R, Potschger U, Valteau-Couanet D, et al. Investigation of the role of dinutuximab beta-based immunotherapy in the SIOPEN high-risk neuroblastoma 1 trial (HR-NBL1). Cancers. 2020;12(2):309. doi:10.3390/cancers12020309
  • Ladenstein R, Potschger U, Valteau-Couanet D, et al. 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. 2018;19(12):1617–1629. doi:10.1016/S1470-2045(18)30578-3
  • Mueller I, Ehlert K, Endres S, et al. Tolerability, response and outcome of high-risk neuroblastoma patients treated with long-term infusion of anti-GD2 antibody ch14.18/CHO. mAbs. 2018;10(1):55–61. doi:10.1080/19420862.2017.1402997
  • Harding FA, Stickler MM, Razo J, DuBridge RB. The immunogenicity of humanized and fully human antibodies: residual immunogenicity resides in the CDR regions. mAbs. 2010;2(3):256–265. doi:10.4161/mabs.2.3.11641
  • Thommesen JE, Michaelsen TE, Loset GA, Sandlie I, Brekke OH. Lysine 322 in the human IgG3 C(H)2 domain is crucial for antibody dependent complement activation. MolImmunol. 2000;37(16):995–1004.
  • Navid F, Sondel PM, Barfield R, et al. 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. 2014;32(14):1445–1452. doi:10.1200/JCO.2013.50.4423
  • Anghelescu DL, Goldberg JL, Faughnan LG, et al. Comparison of pain outcomes between two anti-GD2 antibodies in patients with neuroblastoma. Pediatr Blood Cancer. 2015;62(2):224–228. doi:10.1002/pbc.25280
  • Furman WL, Federico SM, McCarville MB, et al. A phase II Trial of Hu14.18K322A in combination with induction chemotherapy in children with newly diagnosed high-risk neuroblastoma. Clin Cancer Res. 2019;25(21):6320–6328. doi:10.1158/1078-0432.CCR-19-1452
  • Ady N, Zucker JM, Asselain B, et al. A new 123I-MIBG whole body scan scoring method–application to the prediction of the response of metastases to induction chemotherapy in stage IV neuroblastoma. Eur J Cancer. 1995;31(2):256–261. doi:10.1016/0959-8049(94)00509-4
  • Cheung NK, Guo H, Hu J, Tassev DV, Cheung IY. Humanizing murine IgG3 anti-GD2 antibody m3F8 substantially improves antibody-dependent cell-mediated cytotoxicity while retaining targeting in vivo. Oncoimmunology. 2012;1(4):477–486. doi:10.4161/onci.19864
  • Kushner BH, Cheung IY, Modak S, Basu EM, Roberts SS, Cheung NK. Humanized 3F8 Anti-G D2 monoclonal antibody dosing with granulocyte-macrophage colony-stimulating factor in patients with resistant neuroblastoma. JAMA Oncol. 2018;4:1729. doi:10.1001/jamaoncol.2018.4005
  • Wang W, Wang EQ, Balthasar JP. Monoclonal antibody pharmacokinetics and pharmacodynamics. Clin Pharmacol Ther. 2008;84(5):548–558. doi:10.1038/clpt.2008.170
  • Ryman JT, Meibohm B. Pharmacokinetics of monoclonal antibodies. CPT Pharmacometr Syst Pharmacol. 2017;6(9):576–588. doi:10.1002/psp4.12224
  • Dostalek M, Gardner I, Gurbaxani BM, Rose RH, Chetty M. Pharmacokinetics, pharmacodynamics and physiologically-based pharmacokinetic modelling of monoclonal antibodies. Clin Pharmacokinet. 2013;52(2):83–124.
  • Deng R, Jin F, Prabhu S, Iyer S. Monoclonal antibodies: what are the pharmacokinetic and pharmacodynamic considerations for drug development? Expert Opin Drug Metab Toxicol. 2012;8(2):141–160. doi:10.1517/17425255.2012.643868
  • Lobo ED, Hansen RJ, Balthasar JP. Antibody pharmacokinetics and pharmacodynamics. J Pharm Sci. 2004;93(11):2645–2668. doi:10.1002/jps.20178
  • Siebert N, Eger C, Seidel D, et al. Pharmacokinetics and pharmacodynamics of ch14.18/CHO in relapsed/refractory high-risk neuroblastoma patients treated by long-term infusion in combination with IL-2. mAbs. 2016.
  • Ladenstein RL, Poetschger U, Valteau-Couanet D, et al. Randomization of dose-reduced subcutaneous interleukin-2 (scIL2) in maintenance immunotherapy (IT) with anti-GD2 antibody dinutuximab beta (DB) long-term infusion (LTI) in front line high-risk neuroblastoma patients: early results from the HR-NBL1/SIOPEN trial. J Clin Oncol. 2019;37(15).
  • Desai AV, Fox E, Smith LM, Lim AP, Maris JM, Balis FM. Pharmacokinetics of the chimeric anti-GD2 antibody, ch14.18, in children with high-risk neuroblastoma. Cancer Chemother Pharmacol. 2014;74(5):1047–1055. doi:10.1007/s00280-014-2575-9
  • Yeh SD, Larson SM, Burch L, et al. Radioimmunodetection of neuroblastoma with iodine-131-3F8: correlation with biopsy, iodine-131-metaiodobenzylguanidine and standard diagnostic modalities. J Nucl Med. 1991;32(5):769–776.
  • Reuland P, Geiger L, Thelen MH, et al. Follow-up in neuroblastoma: comparison of metaiodobenzylguanidine and a chimeric anti-GD2 antibody for detection of tumor relapse and therapy response. J Pediatr Hematol Oncol. 2001;23(7):437–442. doi:10.1097/00043426-200110000-00009
  • Vavere AL, Butch ER, Dearling JL, et al. 64Cu-p-NH2-Bn-DOTA-hu14.18K322A, a PET radiotracer targeting neuroblastoma and melanoma. J Nucl Med. 2012;53(11):1772–1778. doi:10.2967/jnumed.112.104208
  • Modak S, Cheung NK. Antibody-based targeted radiation to pediatric tumors. J Nucl Med. 2005;46(Suppl 1):157S–163S.
  • Cheung NK, Kushner BH, LaQuaglia M, et al. N7: a novel multi-modality therapy of high risk neuroblastoma (NB) in children diagnosed over 1 year of age. Med Pediatr Oncol. 2001;36(1):227–230. doi:10.1002/1096-911X(20010101)36:1<227::AID-MPO1055>3.0.CO;2-U
  • Sondel PM, Hank JA. Combination therapy with interleukin-2 and antitumor monoclonal antibodies. Cancer J Sci Am. 1997;3(Suppl 1):S121–127.
  • Nguyen R, Houston J, Chan WK, Finkelstein D, Dyer MA. The role of interleukin-2, all-trans retinoic acid, and natural killer cells: surveillance mechanisms in anti-GD2 antibody therapy in neuroblastoma. Cancer Immunol Immunother. 2018;67(4):615–626. doi:10.1007/s00262-017-2108-6
  • Ribeiro RC, Rill D, Roberson PK, et al. Continuous infusion of interleukin-2 in children with refractory malignancies. Cancer. 1993;72(2):623–628. doi:10.1002/1097-0142(19930715)72:2<623::AID-CNCR2820720248>3.0.CO;2-S
  • Yang RK, Kalogriopoulos NA, Rakhmilevich AL, et al. Intratumoral hu14.18-IL-2 (IC) induces local and systemic antitumor effects that involve both activated T and NK cells as well as enhanced IC retention. J Immunol. 2012;189(5):2656–2664. doi:10.4049/jimmunol.1200934
  • Yamane BH, Hank JA, Albertini MR, Sondel PM. The development of antibody-IL-2 based immunotherapy with hu14.18-IL2 (EMD-273063) in melanoma and neuroblastoma. Expert Opin Investig Drugs. 2009;18(7):991–1000. doi:10.1517/13543780903048911
  • Osenga KL, Hank JA, Albertini MR, et al. 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. 2006;12(6):1750–1759. doi:10.1158/1078-0432.CCR-05-2000
  • Shusterman S, London WB, Gillies SD, et al. Antitumor activity of hu14.18-IL2 in patients with relapsed/refractory neuroblastoma: a Children’s Oncology Group (COG) phase II study. J Clin Oncol. 2010;28(33):4969–4975. doi:10.1200/JCO.2009.27.8861
  • Alvarez-Rueda N, Desselle A, Cochonneau D, et al. 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. 2011;6(9):e25220. doi:10.1371/journal.pone.0025220
  • Terme M, Dorvillius M, Cochonneau D, et al. 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. 2014;9(2):e87210. doi:10.1371/journal.pone.0087210
  • Fleurence J, Fougeray S, Bahri M, et al. Targeting O-Acetyl-GD2 ganglioside for cancer immunotherapy. J Immunol Res. 2017;2017:5604891. doi:10.1155/2017/5604891
  • Castriconi R, Dondero A, Augugliaro R, et al. Identification of 4Ig-B7-H3 as a neuroblastoma-associated molecule that exerts a protective role from an NK cell-mediated lysis. Proc Natl Acad Sci U S A. 2004;101(34):12640–12645. doi:10.1073/pnas.0405025101
  • Gregorio A, Corrias MV, Castriconi R, et al. Small round blue cell tumours: diagnostic and prognostic usefulness of the expression of B7-H3 surface molecule. Histopathology. 2008;53(1):73–80. doi:10.1111/j.1365-2559.2008.03070.x
  • Picarda E, Ohaegbulam KC, Zang X. Molecular pathways: targeting B7-H3 (CD276) for human cancer immunotherapy. Clin Cancer Res. 2016;22(14):3425–3431. doi:10.1158/1078-0432.CCR-15-2428
  • Du H, Hirabayashi K, Ahn S, et al. Antitumor responses in the absence of toxicity in solid tumors by targeting B7-H3 via chimeric antigen receptor T cells. Cancer Cell. 2019;35(2):221–237 e228. doi:10.1016/j.ccell.2019.01.002
  • Modak S, Kramer K, Gultekin SH, Guo HF, Cheung NK. Monoclonal antibody 8H9 targets a novel cell surface antigen expressed by a wide spectrum of human solid tumors. Cancer Res. 2001;61(10):4048–4054.
  • Ahmed M, Cheng M, Zhao Q, et al. Humanized affinity-matured monoclonal antibody 8H9 has potent antitumor activity and binds to FG loop of tumor antigen B7-H3. J Biol Chem. 2015;290(50):30018–30029. doi:10.1074/jbc.M115.679852
  • Kramer K, Kushner B, Modak S, et al. A curative approach to central nervous system metastases of neuroblastoma. Pediatr Blood Cancer. 2019;66:S56–S56.
  • Kramer K, Kushner BH, Modak S, et al. A curative approach to central nervous system metastases of neuroblastoma. J Clin Oncol. 2017;35:10545. doi:10.1200/JCO.2017.35.15_suppl.10545
  • Desantes K, Maris JM, McDowell K, et al. A phase 1, open-label, dose escalation study of enoblituzumab (MGA271) in pediatric patients with B7-H3-expressing relapsed or refractory solid tumors. J Clin Oncol. 2017;35:TPS2596–TPS2596. doi:10.1200/JCO.2017.35.15_suppl.TPS2596
  • Bresler SC, Weiser DA, Huwe PJ, et al. ALK mutations confer differential oncogenic activation and sensitivity to ALK inhibition therapy in neuroblastoma. Cancer Cell. 2014;26(5):682–694. doi:10.1016/j.ccell.2014.09.019
  • Carpenter EL, Haglund EA, Mace EM, et al. Antibody targeting of anaplastic lymphoma kinase induces cytotoxicity of human neuroblastoma. Oncogene. 2012;31(46):4859–4867. doi:10.1038/onc.2011.647
  • Dondero A, Pastorino F, Della Chiesa M, et al. PD-L1 expression in metastatic neuroblastoma as an additional mechanism for limiting immune surveillance. Oncoimmunology. 2016;5(1):e1064578. doi:10.1080/2162402X.2015.1064578
  • Siebert N, Zumpe M, Juttner M, Troschke-Meurer S, Lode HN. PD-1 blockade augments anti-neuroblastoma immune response induced by anti-GD2 antibody ch14.18/CHO. Oncoimmunology. 2017;6(10):e1343775. doi:10.1080/2162402X.2017.1343775
  • Ehlert K, Hansjuergens I, Zinke A, et al. Nivolumab and dinutuximab beta in two patients with refractory neuroblastoma. J Immunother Cancer. 2020;8(1):e000540. doi:10.1136/jitc-2020-000540
  • Li N, Gao W, Zhang YF, Ho M. Glypicans as cancer therapeutic targets. Trends Cancer. 2018;4(11):741–754. doi:10.1016/j.trecan.2018.09.004
  • Bosse KR, Raman P, Zhu Z, et al. Identification of GPC2 as an oncoprotein and candidate immunotherapeutic target in high-risk neuroblastoma. Cancer Cell. 2017;32(3):295–309 e212. doi:10.1016/j.ccell.2017.08.003
  • Theocharopoulos C, Lialios PP, Gogas H, Ziogas DC. An overview of antibody-drug conjugates in oncological practice. Ther Adv Med Oncol. 2020;12:1758835920962997. doi:10.1177/1758835920962997
  • Zhang W, Huang Q, Xiao W, et al. Advances in anti-tumor treatments targeting the CD47/SIRPalpha axis. Front Immunol. 2020;11:18. doi:10.3389/fimmu.2020.00018
  • Aktas S, Ozdemir A, Serinan E, Altun Z, Olgun N. “Don’t Eat Me” signals of neuroblastoma by CD47 for immune escape: a novel prognostic biomarker. Proceedings. 2018;2(25):1538. doi:10.3390/proceedings2251538
  • Oronsky B, Carter C, Reid T, Brinkhaus F, Knox SJ. Just eat it: a review of CD47 and SIRP-alpha antagonism. Semin Oncol. 2020;47(2–3):117–124. doi:10.1053/j.seminoncol.2020.05.009
  • Jaiswal S, Jamieson CH, Pang WW, et al. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell. 2009;138(2):271–285. doi:10.1016/j.cell.2009.05.046
  • Asgharzadeh S, Salo JA, Ji L, et al. Clinical significance of tumor-associated inflammatory cells in metastatic neuroblastoma. J Clin Oncol. 2012;30(28):3525–3532. doi:10.1200/JCO.2011.40.9169
  • Theruvath J, Smith B, Linde MH, et al. Abstract PR07: GD2 is a macrophage checkpoint molecule and combined GD2/CD47 blockade results in synergistic effects and tumor clearance in xenograft models of neuroblastoma and osteosarcoma. Cancer Res. 2020;80(14Supplement):PR07.
  • Labrijn AF, Janmaat ML, Reichert JM, Parren P. Bispecific antibodies: a mechanistic review of the pipeline. Nat Rev Drug Discov. 2019;18(8):585–608. doi:10.1038/s41573-019-0028-1
  • Yankelevich M, Kondadasula SV, Thakur A, Buck S, Cheung NK, Lum LG. Anti-CD3 x anti-GD2 bispecific antibody redirects T-cell cytolytic activity to neuroblastoma targets. Pediatr Blood Cancer. 2012;59(7):1198–1205. doi:10.1002/pbc.24237
  • Hernandez R, Erbe A, Gerhardt D, et al. GD2/B7-H3 bispecific antibodies for next-generation neuroblastoma treatment</strong>. J Nucl Med. 2020;61(supplement1):376.
  • Erbe A, Gerhardt D, Hernandez R, et al. Improving specific targeting of tumors through bispecific sniper antibodies. J Immunother Cancer. 2020;8:A280–A280. doi:10.1136/jitc-2020-SITC2020.0461
  • Mori K, Iida S, Yamane-Ohnuki N, et al. Non-fucosylated therapeutic antibodies: the next generation of therapeutic antibodies. Cytotechnology. 2007;55(2–3):109–114. doi:10.1007/s10616-007-9103-2
  • Shields RL, Lai J, Keck R, et al. Lack of fucose on human IgG1 N-linked oligosaccharide improves binding to human Fcgamma RIII and antibody-dependent cellular toxicity. J Biol Chem. 2002;277(30):26733–26740. doi:10.1074/jbc.M202069200
  • Hank JA, Robinson RR, Surfus J, et al. Augmentation of antibody dependent cell mediated cytotoxicity following in vivo therapy with recombinant interleukin 2. Cancer Res. 1990;50(17):5234–5239.
  • Tanaka A, Sakaguchi S. Regulatory T cells in cancer immunotherapy. Cell Res. 2017;27(1):109–118. doi:10.1038/cr.2016.151
  • Lode H, Siebert N, Troschke-Meurer S, et al. Administration of subcutaneous IL-2 is associated with strong induction of regulatory T cells in high-risk neuroblastoma patients treated with dinutuximab beta, a SIOPEN study. Pediatr Blood Cancer. 2019;66:S55–S56.
  • Nguyen R, Moustaki A, Norrie JL, et al. Interleukin-15 enhances anti-GD2 antibody-mediated cytotoxicity in an orthotopic PDX model of neuroblastoma. Clin Cancer Res. 2019;25(24):7554–7564. doi:10.1158/1078-0432.CCR-19-1045
  • Heinze A, Grebe B, Bremm M, et al. The synergistic use of IL-15 and IL-21 for the generation of NK cells from CD3/CD19-depleted grafts improves their ex vivo expansion and cytotoxic potential against neuroblastoma: perspective for optimized immunotherapy post haploidentical stem cell transplantation. Front Immunol. 2019;10. doi:10.3389/fimmu.2019.02816
  • Nowak AK, Robinson BW, Lake RA. Synergy between chemotherapy and immunotherapy in the treatment of established murine solid tumors. Cancer Res. 2003;63(15):4490–4496.
  • Lake RA, Robinson BW. Immunotherapy and chemotherapy–a practical partnership. Nat Rev Cancer. 2005;5(5):397–405. doi:10.1038/nrc1613
  • Buhtoiarov IN, Sondel PM, Wigginton JM, et al. Anti-tumour synergy of cytotoxic chemotherapy and anti-CD40 plus CpG-ODN immunotherapy through repolarization of tumour-associated macrophages. Immunology. 2011;132(2):226–239. doi:10.1111/j.1365-2567.2010.03357.x
  • Holden SA, Lan Y, Pardo AM, Wesolowski JS, Gillies SD. Augmentation of antitumor activity of an antibody-interleukin 2 immunocytokine with chemotherapeutic agents. Clin Cancer Res. 2001;7(9):2862–2869.
  • Ghiringhelli F, Larmonier N, Schmitt E, et al. CD4+CD25+ regulatory T cells suppress tumor immunity but are sensitive to cyclophosphamide which allows immunotherapy of established tumors to be curative. Eur J Immunol. 2004;34(2):336–344. doi:10.1002/eji.200324181
  • Menard C, Martin F, Apetoh L, Bouyer F, Ghiringhelli F. Cancer chemotherapy: not only a direct cytotoxic effect, but also an adjuvant for antitumor immunity. Cancer Immunol Immunother. 2008;57(11):1579–1587. doi:10.1007/s00262-008-0505-6
  • Zitvogel L, Apetoh L, Ghiringhelli F, Kroemer G. Immunological aspects of cancer chemotherapy. Nat Rev Immunol. 2008;8(1):59–73. doi:10.1038/nri2216
  • Raffaghello L, Marimpietri D, Pagnan G, et al. Anti-GD2 monoclonal antibody immunotherapy: a promising strategy in the prevention of neuroblastoma relapse. Cancer Lett. 2003;197(1–2):205–209. doi:10.1016/S0304-3835(03)00100-9
  • Nowak AK, Lake RA, Marzo AL, et al. Induction of tumor cell apoptosis in vivo increases tumor antigen cross-presentation, cross-priming rather than cross-tolerizing host tumor-specific CD8 T cells. J Immunol. 2003;170(10):4905–4913. doi:10.4049/jimmunol.170.10.4905
  • Park JA, Cheung NV. Targets and antibody formats for immunotherapy of neuroblastoma. J Clin Oncol. 2020;38(16):1836–1848. doi:10.1200/JCO.19.01410
  • Richards RM, Sotillo E, Majzner RG. CAR T cell therapy for neuroblastoma. Front Immunol. 2018;9:2380. doi:10.3389/fimmu.2018.02380
  • Heczey A, Louis CU. Advances in chimeric antigen receptor immunotherapy for neuroblastoma. Discov Med. 2013;16(90):287–294.
  • Louis CU, Savoldo B, Dotti G, et al. Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood. 2011;118(23):6050–6056. doi:10.1182/blood-2011-05-354449
  • Oh S, Lee JH, Kwack K, Choi SW. Natural killer cell therapy: a new treatment paradigm for solid tumors. Cancers. 2019;11(10):1534. doi:10.3390/cancers11101534
  • Mehta RS, Rezvani K. Chimeric antigen receptor expressing natural killer cells for the immunotherapy of cancer. Front Immunol. 2018;9:283. doi:10.3389/fimmu.2018.00283
  • Modak S, Le Luduec JB, Cheung IY, et al. Adoptive immunotherapy with haploidentical natural killer cells and Anti-GD2 monoclonal antibody m3F8 for resistant neuroblastoma: results of a phase I study. Oncoimmunology. 2018;7(8):e1461305. doi:10.1080/2162402X.2018.1461305
  • Barry WE, Jackson JR, Asuelime GE, et al. Activated natural killer cells in combination with anti-GD2 antibody dinutuximab improve survival of mice after surgical resection of primary neuroblastoma. Clin Cancer Res. 2018;25:325–333. doi:10.1158/1078-0432.CCR-18-1317
  • Uttenreuther-Fischer MM, Huang CS, Reisfeld RA, Yu AL. Pharmacokinetics of anti-ganglioside GD2 mAb 14G2a in a phase 1 trial in pediatric cancer patients. Cancer Immunol Immunother. 1995;41:29–36.
  • Kramer K, Cheung NK, Humm JL, et al. Targeted radioimmunotherapy for leptomeningeal cancer using (131)I-3F8. Med Pediatr Oncol. 2000;35:716–8.