The novel agonistic iNKT-cell antibody NKT14m induces a therapeutic antitumor response against B-cell lymphoma

References

• Terabe M, Berzofsky JA. The role of NKT cells in tumor immunity. Adv Cancer Res. 2008;101:277–348. doi:10.1016/S0065-230X(08)00408-9.
   PubMed Web of Science ®Google Scholar
• Vivier E, Ugolini S, Blaise D, Chabannon C, Brossay L. Targeting natural killer cells and natural killer T cells in cancer. Nat Rev Immunol. 2012;12:239–252. doi:10.1038/nri3174.
   PubMed Web of Science ®Google Scholar
• Smyth MJ, Thia KY, Street SE, Cretney E, Trapani JA, Taniguchi M, Kawano T, Pelikan SB, Crowe NY, Godfrey DI. Differential tumor surveillance by natural killer (NK) and NKT cells. J Exp Med. 2000;191:661–668.
   PubMed Web of Science ®Google Scholar
• Brennan PJ, Brigl M, Brenner MB. Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions. Nat Rev Immunol. 2013;13:101–117. doi:10.1038/nri3369.
   PubMed Web of Science ®Google Scholar
• Cerundolo V, Silk JD, Masri SH, Salio M. Harnessing invariant NKT cells in vaccination strategies. Nat Rev Immunol. 2009;9:28–38. doi:10.1038/nri2451.
   PubMed Web of Science ®Google Scholar
• Mattarollo SR, West AC, Steegh K, Duret H, Paget C, Martin B, Matthews GM, Shortt J, Chesi M, Bergsagel PL, et al. NKT cell adjuvant-based tumor vaccine for treatment of myc oncogene-driven mouse B-cell lymphoma. Blood. 2012;120:3019–3029. doi:10.1182/blood-2012-04-426643.
   PubMed Web of Science ®Google Scholar
• Eberl G, MacDonald HR. Selective induction of NK cell proliferation and cytotoxicity by activated NKT cells. Eur J Immunol. 2000;30:985–992. doi:10.1002/(SICI)1521-4141(200004)30:4<985::AID-IMMU985>3.0.CO;2-E.
   PubMed Web of Science ®Google Scholar
• Gebremeskel S, Clattenburg DR, Slauenwhite D, Lobert L, Johnston B. Natural killer T cell activation overcomes immunosuppression to enhance clearance of postsurgical breast cancer metastasis in mice. Oncoimmunology. 2015;4. doi:10.1080/2162402X.2015.1008371.
   PubMed Web of Science ®Google Scholar
• Fujii S, Shimizu K, Smith C, Bonifaz L, Steinman RM. Activation of natural killer T cells by alpha-galactosylceramide rapidly induces the full maturation of dendritic cells in vivo and thereby acts as an adjuvant for combined CD4 and CD8 T cell immunity to a coadministered protein. J Exp Med. 2003;198:267–279. doi:10.1084/jem.20030324.
   PubMed Web of Science ®Google Scholar
• Hermans IF, Silk JD, Gileadi U, Salio M, Mathew B, Ritter G, Schmidt R, Harris AL, Old L, Cerundolo V. NKT cells enhance CD4+ and CD8+ T cell responses to soluble antigen in vivo through direct interaction with dendritic cells. J Immunol. 2003;171:5140–5147.
   PubMed Web of Science ®Google Scholar
• Galli G, Pittoni P, Tonti E, Malzone C, Uematsu Y, Tortoli M, Maione D, Volpini G, Finco O, Nuti S, et al. Invariant NKT cells sustain specific B cell responses and memory. Proc Natl Acad Sci USA. 2007;104:3984–3989. doi:10.1073/pnas.0700191104.
   PubMed Web of Science ®Google Scholar
• Hayakawa Y, Takeda K, Yagita H, Smyth MJ, Van Kaer L, Okumura K, Saiki I. IFN-gamma-mediated inhibition of tumor angiogenesis by natural killer T-cell ligand, alpha-galactosylceramide. Blood. 2002;100:1728–1733.
   PubMed Web of Science ®Google Scholar
• Tachibana T, Onodera H, Tsuruyama T, Mori A, Nagayama S, Hiai H, Imamura M. Increased intratumor Valpha24-positive natural killer T cells: a prognostic factor for primary colorectal carcinomas. Clin Cancer Res. 2005;11:7322–7327. doi:10.1158/1078-0432.CCR-05-0877.
   PubMed Web of Science ®Google Scholar
• Gorini F, Azzimonti L, Delfanti G, Scarfo L, Scielzo C, Bertilaccio MT, Ranghetti P, Gulino A, Doglioni C, Di Napoli A, et al. Invariant NKT cells contribute to chronic lymphocytic leukemia surveillance and prognosis. Blood. 2017;129:3440–3451. doi:10.1182/blood-2016-11-751065.
   PubMed Web of Science ®Google Scholar
• Fujii S, Shimizu K, Kronenberg M, Steinman RM. Prolonged IFN-gamma-producing NKT response induced with alpha-galactosylceramide-loaded DCs. Nat Immunol. 2002;3:867–874. doi:10.1038/ni827.
   PubMed Web of Science ®Google Scholar
• Spada FM, Koezuka Y, Porcelli SA. CD1d-restricted recognition of synthetic glycolipid antigens by human natural killer T cells. J Exp Med. 1998;188:1529–1534.
   PubMed Web of Science ®Google Scholar
• Kobayashi E, Motoki K, Uchida T, Fukushima H, Koezuka Y. KRN7000, a novel immunomodulator, and its antitumor activities. Oncol Res. 1995;7:529–534.
   PubMed Web of Science ®Google Scholar
• Chang WS, Kim JY, Kim YJ, Kim YS, Lee JM, Azuma M, Yagita H, Kang C-Y. Cutting edge: programmed death-1/programmed death ligand 1 interaction regulates the induction and maintenance of invariant NKT cell anergy. J Immunol. 2008;181:6707–6710.
   PubMed Web of Science ®Google Scholar
• Chung Y, Qin H, Kang CY, Kim S, Kwak LW, Dong C. An NKT-mediated autologous vaccine generates CD4 T-cell dependent potent antilymphoma immunity. Blood. 2007;110:2013–2019. doi:10.1182/blood-2006-12-061309.
   PubMed Web of Science ®Google Scholar
• Matsuyoshi H, Hirata S, Yoshitake Y, Motomura Y, Fukuma D, Kurisaki A, Nakatsura T, Nishimura Y, Senju S. Therapeutic effect of alpha-galactosylceramide-loaded dendritic cells genetically engineered to express SLC/CCL21 along with tumor antigen against peritoneally disseminated tumor cells. Cancer Sci. 2005;96:889–896. doi:10.1111/j.1349-7006.2005.00123.x.
   PubMed Web of Science ®Google Scholar
• Parekh VV, Wilson MT, Olivares-Villagomez D, Singh AK, Wu L, Wang CR, Joyce S, Van Kaer L. Glycolipid antigen induces long-term natural killer T cell anergy in mice. J Clin Invest. 2005;115:2572–2583. doi:10.1172/JCI24762.
   PubMed Web of Science ®Google Scholar
• Shimizu K, Kurosawa Y, Taniguchi M, Steinman RM, Fujii S. Cross-presentation of glycolipid from tumor cells loaded with alpha-galactosylceramide leads to potent and long-lived T cell mediated immunity via dendritic cells. J Exp Med. 2007;204:2641–2653. doi:10.1084/jem.20070458.
   PubMed Web of Science ®Google Scholar
• Chang DH, Osman K, Connolly J, Kukreja A, Krasovsky J, Pack M, Hutchinson A, Geller M, Liu N, Annable R, et al. Sustained expansion of NKT cells and antigen-specific T cells after injection of alpha-galactosyl-ceramide loaded mature dendritic cells in cancer patients. J Exp Med. 2005;201:1503–1517. doi:10.1084/jem.20042592.
   PubMed Web of Science ®Google Scholar
• Giaccone G, Punt CJ, Ando Y, Ruijter R, Nishi N, Peters M, von Blomberg BME, Scheper RJ, van der Vliet HJJ, van Den Eertwegh AJM, et al. A phase I study of the natural killer T-cell ligand alpha-galactosylceramide (KRN7000) in patients with solid tumors. Clin Cancer Res. 2002;8:3702–3709.
   PubMed Web of Science ®Google Scholar
• Nieda M, Okai M, Tazbirkova A, Lin H, Yamaura A, Ide K, Abraham R, Juji T, Macfarlane DJ, Nicol AJ. Therapeutic activation of Valpha24+Vbeta11+ NKT cells in human subjects results in highly coordinated secondary activation of acquired and innate immunity. Blood. 2004;103:383–389. doi:10.1182/blood-2003-04-1155.
   PubMed Web of Science ®Google Scholar
• Uchida T, Horiguchi S, Tanaka Y, Yamamoto H, Kunii N, Motohashi S, Taniguchi M, Nakayama T, Okamoto Y. Phase I study of alpha-galactosylceramide-pulsed antigen presenting cells administration to the nasal submucosa in unresectable or recurrent head and neck cancer. Cancer Immunol Immunother. 2008;57:337–345. doi:10.1007/s00262-007-0373-5.
   PubMed Web of Science ®Google Scholar
• Schneiders FL, Scheper RJ, von Blomberg BM, Woltman AM, Janssen HLA, van Den Eertwegh AJM, Verheul HMW, de Gruijl TD, van der Vliet HJ. Clinical experience with α-galactosylceramide (KRN7000) in patients with advanced cancer and chronic hepatitis B/C infection. Clin Immunol. 2011;140:130–141. doi:10.1016/j.clim.2010.11.010.
   PubMed Web of Science ®Google Scholar
• Ishikawa A, Motohashi S, Ishikawa E, Fuchida H, Higashino K, Otsuji M, Iizasa T, Nakayama T, Taniguchi M, Fujisawa T. A phase I study of alpha-galactosylceramide (KRN7000)-pulsed dendritic cells in patients with advanced and recurrent non-small cell lung cancer. Clin Cancer Res. 2005;11:1910–1917. doi:10.1158/1078-0432.CCR-04-1453.
   PubMed Web of Science ®Google Scholar
• Richter J, Neparidze N, Zhang L, Nair S, Monesmith T, Sundaram R, Miesowicz F, Dhodapkar KM, Dhodapkar MV. Clinical regressions and broad immune activation following combination therapy targeting human NKT cells in myeloma. Blood. 2013;121:423–430. doi:10.1182/blood-2012-06-435503.
   PubMed Web of Science ®Google Scholar
• Scheuplein F, Lamont DJ, Poynter ME, Boyson JE, Serreze D, Lundblad LK, Mashal R, Schaub R, Leite-de-Moraes M. Mouse invariant monoclonal antibody NKT14: A novel tool to manipulate iNKT cell function In Vivo. PLoS ONE. 2015;10:e0140729. doi:10.1371/journal.pone.0140729.
   PubMed Web of Science ®Google Scholar
• Singh AK, Gaur P, Das SN. Natural killer T cell anergy, co-stimulatory molecules and immunotherapeutic interventions. Hum Immunol. 2014;75:250–260. doi:10.1016/j.humimm.2013.12.004.
   PubMed Web of Science ®Google Scholar
• Escriba-Garcia L, Alvarez-Fernandez C, Tellez-Gabriel M, Sierra J, Briones J. Dendritic cells combined with tumor cells and alpha-galactosylceramide induce a potent, therapeutic and NK-cell dependent antitumor immunity in B cell lymphoma. J Transl Med. 2017;15:115. doi:10.1186/s12967-017-1219-3.
   PubMed Web of Science ®Google Scholar
• Das R, Scheuplein F, Guan P, Schaub R, Nichols KE. Cancer immunotherapeutic potential of NKTT320, a novel human invariant natural killer T-cell activating monoclonal antibody. In: Res C, editor. Proceedings of the 106th annual meeting of the American association for cancer research, 2015, Philadelphia (PA). Cancer Res; 75 (15 Suppl): Abstract 4294.
   Google Scholar
• Gebremeskel S, Lobert L, Tanner K, Walker B, Oliphant T, Clarke LE, Dellaire G, Johnston B. Natural Killer T-cell immunotherapy in combination with chemotherapy-induced immunogenic cell death targets metastatic breast cancer. Cancer Immunol Res. 2017;5:1086–1097. doi:10.1158/2326-6066.CIR-17-0229.
   PubMed Web of Science ®Google Scholar
• K TT H, Nakahara F, Matsumoto A, Kurokawa M, Ogawa S, Oda H, Hirai HCS. CD1d expression level in tumor cells is an important determinant for anti-tumor immunity by natural killer T cells. Leuk Lymphoma. 2006;47:2218–2223. doi:10.1080/10428190600682688.
   PubMed Web of Science ®Google Scholar
• Nair S, Dhodapkar MV. Natural killer T cells in cancer immunotherapy. Front Immunol. 2017;8:1178. doi:10.3389/fimmu.2017.01178.
   PubMedGoogle Scholar
• Gibbins JD, Ancelet LR, Weinkove R, Compton BJ, Painter GF, Petersen TR, Hermans IF. An autologous leukemia cell vaccine prevents murine acute leukemia relapse after cytarabine treatment. Blood. 2014;124:2953–2963. doi:10.1182/blood-2014-04-568956.
   PubMed Web of Science ®Google Scholar
• Liu K, Idoyaga J, Charalambous A, Fujii S, Bonito A, Mordoh J, Wainstok R, Bai X-F, Liu Y, Steinman RM. Innate NKT lymphocytes confer superior adaptive immunity via tumor-capturing dendritic cells. J Exp Med. 2005;202:1507–1516. doi:10.1084/jem.20050956.
   PubMed Web of Science ®Google Scholar
• Weir GM, Hrytsenko O, Stanford MM, Berinstein NL, Karkada M, Liwski RS, Mansour M. Metronomic cyclophosphamide enhances HPV16E7 peptide vaccine induced antigen-specific and cytotoxic T-cell mediated antitumor immune response. Oncoimmunology. 2014;3:e953407. doi:10.4161/21624011.2014.953407.
   PubMed Web of Science ®Google Scholar
• Salem ML, Kadima AN, El-Naggar SA, Rubinstein MP, Chen Y, Gillanders WE, Cole DJ. Defining the ability of cyclophosphamide preconditioning to enhance the antigen-specific CD8+ T-cell response to peptide vaccination: creation of a beneficial host microenvironment involving type I IFNs and myeloid cells. J Immunother. 2007;30:40–53. doi:10.1097/01.cji.0000211311.28739.e3.
   PubMed Web of Science ®Google Scholar
• Vacchelli E, Aranda F, Eggermont A, Galon J, Sautes-Fridman C, Cremer I, Zitvogel L, Kroemer G, Galluzzi L. Trial Watch: chemotherapy with immunogenic cell death inducers. Oncoimmunology. 2014;3:e27878. doi:10.4161/onci.27878.
   PubMed Web of Science ®Google Scholar
• Sauter B, Albert ML, Francisco L, Larsson M, Somersan S, Bhardwaj N. Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J Exp Med. 2000;191:423–434.
   PubMed Web of Science ®Google Scholar
• Le DT, Jaffee EM. Regulatory T-cell modulation using cyclophosphamide in vaccine approaches: a current perspective. Cancer Res. 2012;72:3439–3444. doi:10.1158/0008-5472.CAN-11-3912.
   PubMed Web of Science ®Google Scholar
• Mattarollo SR, Kenna T, Nieda M, Nicol AJ. Chemotherapy pretreatment sensitizes solid tumor-derived cell lines to V alpha 24+ NKT cell-mediated cytotoxicity. Int J Cancer. 2006;119:1630–1637. doi:10.1002/ijc.22019.
   PubMed Web of Science ®Google Scholar
• Fallarini S, Paoletti T, Orsi Battaglini N, Lombardi G. Invariant NKT cells increase drug-induced osteosarcoma cell death. Br J Pharmacol. 2012;167:1533–1549. doi:10.1111/j.1476-5381.2012.02108.x.
   PubMed Web of Science ®Google Scholar
• Shankaran V, Ikeda H, Bruce AT, White JM, Swanson PE, Old LJ, Schreiber RD. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature. 2001;410:1107–1111. doi:10.1038/35074122.
   PubMed Web of Science ®Google Scholar
• Kaplan DH, Shankaran V, Dighe AS, Stockert E, Aguet M, Old LJ, Schreiber RD. Demonstration of an interferon gamma-dependent tumor surveillance system in immunocompetent mice. Proc Natl Acad Sci USA. 1998;95:7556–7561.
   PubMed Web of Science ®Google Scholar
• Curtsinger JM, Agarwal P, Lins DC, Mescher MF. Autocrine IFN-gamma promotes naive CD8 T cell differentiation and synergizes with IFN-alpha to stimulate strong function. J Immunol. 2012;189:659–668. doi:10.4049/jimmunol.1102727.
   PubMed Web of Science ®Google Scholar
• Haabeth OA, Lorvik KB, Hammarstrom C, Donaldson IM, Haraldsen G, Bogen B, Corthay A. Inflammation driven by tumour-specific Th1 cells protects against B-cell cancer. Nat Commun. 2011;2:240. doi:10.1038/ncomms1239.
   PubMed Web of Science ®Google Scholar
• Corthay A, Skovseth DK, Lundin KU, Rosjo E, Omholt H, Hofgaard PO, Haraldsen G, Bogen B. Primary antitumor immune response mediated by CD4+ T cells. Immunity. 2005;22:371–383. doi:10.1016/j.immuni.2005.02.003.
   PubMed Web of Science ®Google Scholar
• Fulda S, Debatin KM. IFNgamma sensitizes for apoptosis by upregulating caspase-8 expression through the Stat1 pathway. Oncogene. 2002;21:2295–2308. doi:10.1038/sj.onc.1205255.
   PubMed Web of Science ®Google Scholar
• Beatty G, Paterson Y. IFN-gamma-dependent inhibition of tumor angiogenesis by tumor-infiltrating CD4+ T cells requires tumor responsiveness to IFN-gamma. J Immunol. 2001;166:2276–2282.
   PubMed Web of Science ®Google Scholar