Adoptive immunotherapy with haploidentical natural killer cells and Anti-GD2 monoclonal antibody m3F8 for resistant neuroblastoma: Results of a phase I study

References

• Maris JM, Hogarty MD, Bagatell R, Cohn SL. Neuroblastoma. Lancet. 2007;369:2106–20. doi:10.1016/S0140-6736(07)60983-0. PMID:17586306.
   PubMed Web of Science ®Google Scholar
• Kreissman SG, Seeger RC, Matthay KK, London WB, Sposto R, Grupp SA, Haas-Kogan DA, Laquaglia MP, Yu AL, Diller L, et al. Purged versus non-purged peripheral blood stem-cell transplantation for high-risk neuroblastoma (COG A3973): a randomised phase 3 trial. Lancet Oncol. 2013;14:999–1008. doi:10.1016/S1470-2045(13)70309-7. PMID:23890779.
   PubMed Web of Science ®Google Scholar
• Moreno L, Rubie H, Varo A, Le Deley MC, Amoroso L, Chevance A, Garaventa A, Gambart M, Bautista F, Valteau-Couanet D, et al. Outcome of children with relapsed or refractory neuroblastoma: A meta-analysis of ITCC/SIOPEN European phase II clinical trials. Pediatr Blood Cancer. 2017;64:25–31. doi:10.1002/pbc.26192. PMID:27555472.
   PubMed Web of Science ®Google Scholar
• Yu AL, Gilman AL, Ozkaynak MF, London WB, Kreissman SG, Chen HX, Smith M, Anderson B, Villablanca JG, Matthay KK, et al. Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med. 2010;363:1324–34. doi:10.1056/NEJMoa0911123. PMID:20879881.
   PubMed Web of Science ®Google Scholar
• Cheung NK, Cheung IY, Kramer K, Modak S, Kuk D, Pandit-Taskar N, Chamberlain E, Ostrovnaya I, Kushner BH. 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;135:2199–205. doi:10.1002/ijc.28851. PMID:24644014.
   PubMed Web of Science ®Google Scholar
• Cheung NK, Cheung IY, Kushner BH, Ostrovnaya I, Chamberlain E, Kramer K, Modak S. 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;30:3264–70. doi:10.1200/JCO.2011.41.3807. PMID:22869886.
   PubMed Web of Science ®Google Scholar
• Kushner BH, Ostrovnaya I, Cheung IY, Kuk D, Kramer K, Modak S, Yataghene K, Cheung NK. 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:e1016704. doi:10.1080/2162402X.2015.1016704. PMID:26140243.
   PubMed Web of Science ®Google Scholar
• Suzuki M, Cheung NK. Disialoganglioside GD2 as a therapeutic target for human diseases. Expert opinion on therapeutic targets. 2015;19:349–62. doi:10.1517/14728222.2014.986459. PMID:25604432.
   PubMed Web of Science ®Google Scholar
• Andre P, Castriconi R, Espeli M, Anfossi N, Juarez T, Hue S, Conway H, Romagné F, Dondero A, Nanni M, et al. Comparative analysis of human NK cell activation induced by NKG2D and natural cytotoxicity receptors. Eur J Immunol. 2004;34:961–71. doi:10.1002/eji.200324705. PMID:15048706.
   PubMed Web of Science ®Google Scholar
• Ogbomo H, Hahn A, Geiler J, Michaelis M, Doerr HW, Cinatl J, Jr. NK sensitivity of neuroblastoma cells determined by a highly sensitive coupled luminescent method. Biochem Biophys Res Commun. 2006;339:375–9. doi:10.1016/j.bbrc.2005.11.025. PMID:16297863.
   PubMed Web of Science ®Google Scholar
• Sivori S, Parolini S, Marcenaro E, Castriconi R, Pende D, Millo R, Moretta A. Involvement of natural cytotoxicity receptors in human natural killer cell-mediated lysis of neuroblastoma and glioblastoma cell lines. J Neuroimmuno. 2000;107:220–5. PMID:10854660.
   PubMed Web of Science ®Google Scholar
• Yokoyama WM, Kim S. Licensing of natural killer cells by self-major histocompatibility complex class I. Immunol Rev. 2006;214:143–54. doi:10.1111/j.1600-065X.2006.00458.x. PMID:17100882.
   PubMed Web of Science ®Google Scholar
• Kim S, Poursine-Laurent J, Truscott SM, Lybarger L, Song YJ, Yang L, French AR, Sunwoo JB, Lemieux S, Hansen TH, et al. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature. 2005;436:709–13. doi:10.1038/nature03847. PMID:16079848.
   PubMed Web of Science ®Google Scholar
• Anfossi N, Andre P, Guia S, Falk CS, Roetynck S, Stewart CA, Breso V, Frassati C, Reviron D, Middleton D, et al. Human NK cell education by inhibitory receptors for MHC class I. Immunity. 2006;25:331–42. PMID:16901727.
   PubMed Web of Science ®Google Scholar
• Yu J, Heller G, Chewning J, Kim S, Yokoyama WM, Hsu KC. Hierarchy of the human natural killer cell response is determined by class and quantity of inhibitory receptors for self-HLA-B and HLA-C ligands. J Immunol. 2007;179:5977–89. PMID:17947671.
   PubMed Web of Science ®Google Scholar
• Venstrom JM, Zheng J, Noor N, Danis KE, Yeh AW, Cheung IY, Dupont B, O'Reilly RJ, Cheung NK, Hsu KC. KIR and HLA genotypes are associated with disease progression and survival following autologous hematopoietic stem cell transplantation for high-risk neuroblastoma. Clin Cancer Res. 2009;15:7330–4. doi:10.1158/1078-0432.CCR-09-1720. PMID:19934297.
   PubMed Web of Science ®Google Scholar
• Tarek N, Le Luduec JB, Gallagher MM, Zheng J, Venstrom JM, Chamberlain E, Modak S, Heller G, Dupont B, Cheung NK, et al. Unlicensed NK cells target neuroblastoma following anti-GD2 antibody treatment. J Clin invest. 2012;122:3260–70. doi:10.1172/JCI62749. PMID:22863621.
   PubMed Web of Science ®Google Scholar
• Delgado DC, Hank JA, Kolesar J, Lorentzen D, Gan J, Seo S, Kim K, Shusterman S, Gillies SD, Reisfeld RA, et al. Genotypes of NK cell KIR receptors, their ligands, and Fcgamma receptors in the response of neuroblastoma patients to Hu14.18-IL2 immunotherapy. Cancer Res. 2010;70:9554–61. doi:10.1158/0008-5472.CAN-10-2211. PMID:20935224.
   PubMed Web of Science ®Google Scholar
• Erbe AK, Wang W, Carmichael L, Kim K, Mendonca EA, Song Y, Hess D, Reville PK, London WB, Naranjo A, et al. 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. 2018;24:189–96. doi:10.1158/1078-0432.CCR-17-1767. PMID:28972044.
   PubMed Web of Science ®Google Scholar
• Coudert JD, Scarpellino L, Gros F, Vivier E, Held W. Sustained NKG2D engagement induces cross-tolerance of multiple distinct NK cell activation pathways. Blood. 2008;111:3571–8. doi:10.1182/blood-2007-07-100057. PMID:18198346.
   PubMed Web of Science ®Google Scholar
• Miller JS, Soignier Y, Panoskaltsis-Mortari A, McNearney SA, Yun GH, Fautsch SK, McKenna D, Le C, Defor TE, Burns LJ, et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood. 2005;105:3051–7. doi:10.1182/blood-2004-07-2974. PMID:15632206.
   PubMed Web of Science ®Google Scholar
• Rubnitz JE, Inaba H, Ribeiro RC, Pounds S, Rooney B, Bell T, Pui CH, Leung W. NKAML: a pilot study to determine the safety and feasibility of haploidentical natural killer cell transplantation in childhood acute myeloid leukemia. J Clin Oncol. 2010;28:955–9. doi:10.1200/JCO.2009.24.4590. PMID:20085940.
   PubMed Web of Science ®Google Scholar
• Talleur AC, Triplett BM, Federico S, Mamcarz E, Janssen W, Wu J, Shook D, Leung W, Furman WL. Consolidation therapy for newly diagnosed pediatric patients with high-risk neuroblastoma using Busulfan/Melphalan, Autologous hematopoietic cell transplantation, Anti-GD2 Antibody, granulocyte-macrophage colony-stimulating factor, Interleukin-2, and haploidentical natural killer cells. Biol Blood Marrow Transplant. 2017;23:1910–7. doi:10.1016/j.bbmt.2017.07.011. PMID:28733263.
   PubMed Web of Science ®Google Scholar
• Federico SM, McCarville MB, Shulkin BL, Sondel PM, Hank JA, Hutson P, Meagher M, Shafer A, Ng CY, Leung W, et al. 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. 2017;23:6441–9. doi:10.1158/1078-0432.CCR-17-0379. PMID:28939747.
   PubMed Web of Science ®Google Scholar
• Kushner BH, Kramer K, Modak S, Cheung NK. Camptothecin analogs (irinotecan or topotecan) plus high-dose cyclophosphamide as preparative regimens for antibody-based immunotherapy in resistant neuroblastoma. Clin Cancer Res. 2004;10:84–7. PMID:14734455.
   PubMed Web of Science ®Google Scholar
• Fernandez NC, Treiner E, Vance RE, Jamieson AM, Lemieux S, Raulet DH. A subset of natural killer cells achieves self-tolerance without expressing inhibitory receptors specific for self-MHC molecules. Blood. 2005;105:4416–23. PMID:15728129.
   PubMed Web of Science ®Google Scholar
• Yu J, Venstrom JM, Liu XR, Pring J, Hasan RS, O'Reilly RJ, Hsu KC. Breaking tolerance to self, circulating natural killer cells expressing inhibitory KIR for non-self HLA exhibit effector function after T cell-depleted allogeneic hematopoietic cell transplantation. Blood. 2009;113:3875–84. doi:10.1182/blood-2008-09-177055. PMID:19179302.
   PubMed Web of Science ®Google Scholar
• Beziat V, Descours B, Parizot C, Debre P, Vieillard V. NK cell terminal differentiation: correlated stepwise decrease of NKG2A and acquisition of KIRs. PLoS One. 2010;5:e11966. doi:10.1371/journal.pone.0011966. PMID:20700504.
   PubMed Web of Science ®Google Scholar
• Carlson LM, Pahlman S, De Geer A, Kogner P, Levitskaya J. Differentiation induced by physiological and pharmacological stimuli leads to increased antigenicity of human neuroblastoma cells. Cell Res. 2008;18:398–411. doi:10.1038/cr.2008.27. PMID:18268541.
   PubMed Web of Science ®Google Scholar
• Romee R, Rosario M, Berrien-Elliott MM, Wagner JA, Jewell BA, Schappe T, Leong JW, Abdel-Latif S, Schneider SE, Willey S, et al. Cytokine-induced memory-like natural killer cells exhibit enhanced responses against myeloid leukemia. Sci Transl Med. 2016;8:357ra123. doi:10.1126/scitranslmed.aaf2341. PMID:27655849.
   PubMed Web of Science ®Google Scholar
• Mody R, Naranjo A, Van Ryn C, Yu AL, London WB, Shulkin BL, Parisi MT, Servaes SE, Diccianni MB, Sondel PM, 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;18:946–57. doi:10.1016/S1470-2045(17)30355-8. PMID:28549783.
   PubMed Web of Science ®Google Scholar
• Denman CJ, Senyukov VV, Somanchi SS, Phatarpekar PV, Kopp LM, Johnson JL, Singh H, Hurton L, Maiti SN, Huls MH, et al. Membrane-bound IL-21 promotes sustained ex vivo proliferation of human natural killer cells. PLoS One. 2012;7:e30264. doi:10.1371/journal.pone.0030264. PMID:22279576.
   PubMed Web of Science ®Google Scholar
• Conlon KC, Lugli E, Welles HC, Rosenberg SA, Fojo AT, Morris JC, Fleisher TA, Dubois SP, Perera LP, Stewart DM, et al. Redistribution, hyperproliferation, activation of natural killer cells and CD8 T cells, and cytokine production during first-in-human clinical trial of recombinant human interleukin-15 in patients with cancer. J Clin Oncol. 2015;33:74–82. doi:10.1200/JCO.2014.57.3329. PMID:25403209.
   PubMed Web of Science ®Google Scholar
• Felices M, Chu S, Kodal B, Bendzick L, Ryan C, Lenvik AJ, Boylan KLM, Wong HC, Skubitz APN, Miller JS, et al. IL-15 super-agonist (ALT-803) enhances natural killer (NK) cell function against ovarian cancer. Gynecol Oncol. 2017;145:453–61. doi:10.1016/j.ygyno.2017.02.028. PMID:28236454.
   PubMed Web of Science ®Google Scholar
• Muntasell A, Vilches C, Angulo A, Lopez-Botet M. Adaptive reconfiguration of the human NK-cell compartment in response to cytomegalovirus: a different perspective of the host-pathogen interaction. Eur J Immunol. 2013;43:1133–41. doi:10.1002/eji.201243117. PMID:23552990.
   PubMed Web of Science ®Google Scholar
• Rey J, Fauriat C, Kochbati E, Orlanducci F, Charbonnier A, D'Incan E, Andre P, Romagne F, Barbarat B, Vey N, et al. Kinetics of cytotoxic lymphocytes reconstitution after induction chemotherapy in Elderly AML patients reveals progressive recovery of normal phenotypic and functional features in NK Cells. Front Immunol. 2017;8:64. doi:10.3389/fimmu.2017.00064. PMID:28210257.
   PubMed Web of Science ®Google Scholar
• Muntasell A, Ochoa MC, Cordeiro L, Berraondo P, Lopez-Diaz de Cerio A, Cabo M, López-Botet M, Melero I. Targeting NK-cell checkpoints for cancer immunotherapy. Curr Opin Immunol. 2017;45:73–81. doi:10.1016/j.coi.2017.01.003. PMID:28236750.
   PubMed Web of Science ®Google Scholar
• Schlums H, Cichocki F, Tesi B, Theorell J, Beziat V, Holmes TD, Han H, Chiang SC, Foley B, Mattsson K, et al. Cytomegalovirus infection drives adaptive epigenetic diversification of NK cells with altered signaling and effector function. Immunity. 2015;42:443–56. doi:10.1016/j.immuni.2015.02.008. PMID:25786176.
   PubMed Web of Science ®Google Scholar
• Lee J, Zhang T, Hwang I, Kim A, Nitschke L, Kim M, Scott JM, Kamimura Y, Lanier LL, Kim S. Epigenetic modification and antibody-dependent expansion of memory-like NK cells in human cytomegalovirus-infected individuals. Immunity. 2015;42:431–42. doi:10.1016/j.immuni.2015.02.013. PMID:25786175.
   PubMed Web of Science ®Google Scholar
• 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;1:477–86. PMID:22754766.
   PubMed Web of Science ®Google Scholar
• Hsu KC, Liu XR, Selvakumar A, Mickelson E, O'Reilly RJ, Dupont B. Killer Ig-like receptor haplotype analysis by gene content: evidence for genomic diversity with a minimum of six basic framework haplotypes, each with multiple subsets. J Immunol. 2002;169:5118–29. PMID:12391228.
   PubMed Web of Science ®Google Scholar
• Cooley S, Weisdorf DJ, Guethlein LA, Klein JP, Wang T, Le CT, Marsh SG, Geraghty D, Spellman S, Haagenson MD, et al. Donor selection for natural killer cell receptor genes leads to superior survival after unrelated transplantation for acute myelogenous leukemia. Blood. 2010;116:2411–9. doi:10.1182/blood-2010-05-283051. PMID:20581313.
   PubMed Web of Science ®Google Scholar
• Cheung NK, Guo HF, Heller G, Cheung IY. Induction of Ab3 and Ab3′ antibody was associated with long-term survival after anti-G(D2) antibody therapy of stage 4 neuroblastoma. Clinical Can Res. 2000;6:2653–60. PMID:10914706.
   PubMed Web of Science ®Google Scholar
• Rowlings PA, Przepiorka D, Klein JP, Gale RP, Passweg JR, Henslee-Downey PJ, Cahn JY, Calderwood S, Gratwohl A, Socié G, et al. IBMTR Severity Index for grading acute graft-versus-host disease: retrospective comparison with Glucksberg grade. Br J Haematol. 1997;97:855–64. PMID:9217189.
   PubMed Web of Science ®Google Scholar
• Brodeur G, Pritchard J, Berthold F, Carlen NLT, Castel V, Castleberry RP, De Bernardi B, Evans AE, Favrot M, Hedborg F, et al. Revisions of the international criteria for neuroblastoma diagnosis, staging and response to treatment. J Clin Oncol. 1993;11:1466–77. PMID:8336186.
   PubMed Web of Science ®Google Scholar
• Naranjo A, Parisi MT, Shulkin BL, London WB, Matthay KK, Kreissman SG, Yanik GA. Comparison of (1)(2)(3)I-metaiodobenzylguanidine (MIBG) and (1)(3)(1)I-MIBG semi-quantitative scores in predicting survival in patients with stage 4 neuroblastoma: a report from the Children's Oncology Group. Pediatr Blood Cancer. 2011;56:1041–5. doi:10.1002/pbc.22991. PMID:21328522.
   PubMed Web of Science ®Google Scholar
• Cheung NK, Guo HF, Cheung IY. Correlation of anti-idiotype network with survival following anti-G(D2) monoclonal antibody 3F8 therapy of stage 4 neuroblastoma. Med Pediatr Oncol. 2000;35:635–7. PMID:11107135.
   PubMedGoogle Scholar
• 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;30:426–32. doi:10.1200/JCO.2011.37.6236. PMID:22203761.
   PubMed Web of Science ®Google Scholar