Focusing and sustaining the antitumor CTL effector killer response by agonist anti-CD137 mAb

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 24, 2015, Pages 7551-7556

  Weigelin, Bettina ^a   Bolaños, Elixabet ^b   Teijeira, Alvaro ^b   Martinez Forero, Ivan ^b   Labiano, Sara ^b   Azpilikueta, Arantza ^b   Morales Kastresana, Aizea ^b   Quetglas, José I ^b   Wagena, Esther ^a   Sánchez Paulete, Alfonso Rodríguez ^b   Chen, Lieping ^c   Friedl, Peter ^a   Melero, Ignacio ^b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF NAVARRA   (Spain)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Adoptive T cell therapy; CD137; Costimulation; Cytotoxic T lymphocyte; Immunotherapy

Indexed keywords

ANTINEOPLASTIC AGENT; CD137 ANTIGEN; CD137 MONOCLONAL ANTIBODY; EOMESODERMIN; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; AVIAN PROTEIN; EOMES PROTEIN, MOUSE; OVALBUMIN; T BOX TRANSCRIPTION FACTOR;

ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; CANCER IMMUNOTHERAPY; CELL FUNCTION; CELL KILLING; CELL THERAPY; CELL TRANSFER; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DISEASE ERADICATION; EFFECTOR CELL; MICROSCOPY; MOUSE; NEOPLASM; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STIMULATION; TARGET CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL; TUMOR MICROENVIRONMENT; TUMOR REJECTION; ANIMAL; C57BL MOUSE; DEFICIENCY; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; MALE; MELANOMA, EXPERIMENTAL; METABOLISM; MULTIMODALITY CANCER THERAPY; PATHOLOGY; PROCEDURES; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD137; AVIAN PROTEINS; CELL LINE, TUMOR; COMBINED MODALITY THERAPY; IMMUNOTHERAPY, ADOPTIVE; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; OVALBUMIN; T-BOX DOMAIN PROTEINS; T-LYMPHOCYTES, CYTOTOXIC; TUMOR MICROENVIRONMENT;

EID: 84935919398     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1506357112     Document Type: Article

References (41)

1. Restifo NP, Dudley ME, Rosenberg SA (2012) Adoptive immunotherapy for cancer: Harnessing the T cell response. Nat Rev Immunol 12(4):269-281.
2. Darcy PK, Neeson P, Yong CS, Kershaw MH (2014) Manipulating immune cells for adoptive immunotherapy of cancer. Curr Opin Immunol 27:46-52.
3. Kalos M, et al. (2011) T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci Transl Med 3(95):95ra73.
4. Porter DL, Levine BL, Kalos M, Bagg A, June CH (2011) Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 365(8):725-733.
5. Milone MC, et al. (2009) Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol Ther 17(8):1453-1464.
6. Pollok KE, et al. (1993) Inducible T cell antigen 4-1BB. Analysis of expression and function. J Immunol 150(3):771-781.
7. Melero I, Johnston JV, Shufford WW, Mittler RS, Chen L (1998) NK1.1 cells express 4-1BB (CDw137) costimulatory molecule and are required for tumor immunity elicited by anti-4-1BB monoclonal antibodies. Cell Immunol 190(2):167-172.
8. Melero I, Hirschhorn-Cymerman D, Morales-Kastresana A, Sanmamed MF, Wolchok JD (2013) Agonist antibodies to TNFR molecules that costimulate T and NK cells. Clin Cancer Res 19(5):1044-1053.
9. Wortzman ME, Clouthier DL, McPherson AJ, Lin GH, Watts TH (2013) The contextual role of TNFR family members in CD8(+) T-cell control of viral infections. Immunol Rev 255(1):125-148.
10. May KF, Jr, Chen L, Zheng P, Liu Y (2002) Anti-4-1BB monoclonal antibody enhances rejection of large tumor burden by promoting survival but not clonal expansion of tumor-specific CD8+ T cells. Cancer Res 62(12):3459-3465.
11. Melero I, et al. (1997) Monoclonal antibodies against the 4-1BB T-cell activation molecule eradicate established tumors. Nat Med 3(6):682-685.
12. Kohrt HE, et al. (2011) CD137 stimulation enhances the antilymphoma activity of anti-CD20 antibodies. Blood 117(8):2423-2432.
13. Kohrt HE, et al. (2012) Stimulation of natural killer cells with a CD137-specific antibody enhances trastuzumab efficacy in xenotransplant models of breast cancer. J Clin Invest 122(3):1066-1075.
14. Kohrt HE, et al. (2014) Targeting CD137 enhances the efficacy of cetuximab. J Clin Invest 124(6):2668-2682.
15. Wilcox RA, et al. (2002) Cutting edge: Expression of functional CD137 receptor by dendritic cells. J Immunol 168(9):4262-4267.
16. Palazón A, et al. (2011) Agonist anti-CD137 mAb act on tumor endothelial cells to enhance recruitment of activated T lymphocytes. Cancer Res 71(3):801-811.
17. Zhang X, et al. (2010) CD137 promotes proliferation and survival of human B cells. J Immunol 184(2):787-795.
18. Lee SW, et al. (2008) Identification of regulatory functions for 4-1BB and 4-1BBL in myelopoiesis and the development of dendritic cells. Nat Immunol 9(8):917-926.
19. Lin GH, et al. (2012) Contribution of 4-1BBL on radioresistant cells in providing survival signals through 4-1BB expressed on CD8+ memory T cells in the bone marrow. Eur J Immunol 42(11):2861-2874.
20. Bellone M, et al. (2000) Relevance of the tumor antigen in the validation of three vaccination strategies for melanoma. J Immunol 165(5):2651-2656.
21. Quetglas JI, et al. (2012) Immunotherapeutic synergy between anti-CD137 mAb and intratumoral administration of a cytopathic Semliki Forest virus encoding IL-12. Mol Ther 20(9):1664-1675.
22. Shuford WW, et al. (1997) 4-1BB costimulatory signals preferentially induce CD8+ T cell proliferation and lead to the amplification in vivo of cytotoxic T cell responses. J Exp Med 186(1):47-55.
23. Kaech SM, Cui W (2012) Transcriptional control of effector and memory CD8+ T cell differentiation. Nat Rev Immunol 12(11):749-761.
24. Qui HZ, et al. (2011) CD134 plus CD137 dual costimulation induces Eomesodermin in CD4 T cells to program cytotoxic Th1 differentiation. J Immunol 187(7):3555-3564.
25. Curran MA, et al. (2013) Systemic 4-1BB activation induces a novel T cell phenotype driven by high expression of Eomesodermin. J Exp Med 210(4):743-755.
26. Pearce EL, et al. (2003) Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science 302(5647):1041-1043.
27. McLane LM, et al. (2013) Differential localization of T-bet and Eomes in CD8 T cell memory populations. J Immunol 190(7):3207-3215.
28. Li G, et al. (2013) T-Bet and Eomes Regulate the Balance between the Effector/Central Memory T Cells versus Memory Stem Like T Cells. PLoS ONE 8(6):e67401.
29. Boissonnas A, Fetler L, Zeelenberg IS, Hugues S, Amigorena S (2007) In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. JExpMed204(2):345-356.
30. Rabinovich GA, Gabrilovich D, Sotomayor EM (2007) Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol 25:267-296.
31. Hurtado JC, Kim YJ, Kwon BS (1997) Signals through 4-1BB are costimulatory to previously activated splenic T cells and inhibit activation-induced cell death. J Immunol 158(6):2600-2609.
32. Lin GH, et al. (2010) Evaluating the cellular targets of anti-4-1BB agonist antibody during immunotherapy of a pre-established tumor in mice. PLoS ONE 5(6):e11003.
33. Morales-Kastresana A, et al. (2013) Combined immunostimulatory monoclonal antibodies extend survival in an aggressive transgenic hepatocellular carcinoma mouse model. Clin Cancer Res 19(22):6151-6162.
34. Melero I, Murillo O, Dubrot J, Hervás-Stubbs S, Perez-Gracia JL (2008) Multi-layered action mechanisms of CD137 (4-1BB)-targeted immunotherapies. Trends Pharmacol Sci 29(8):383-390.
35. Morales-Kastresana A, et al. (2013) Essential complicity of perforin-granzyme and FAS-L mechanisms to achieve tumor rejection following treatment with anti-CD137 mAb. J Immunother Cancer 1:3.
36. Breart B, Lemaître F, Celli S, Bousso P (2008) Two-photon imaging of intratumoral CD8+ T cell cytotoxic activity during adoptive T cell therapy in mice. J Clin Invest 118(4):1390-1397.
37. Palazón A, et al. (2012) The HIF-1α hypoxia response in tumor-infiltrating T lymphocytes induces functional CD137 (4-1BB) for immunotherapy. Cancer Discov 2(7):608-623.
38. Wolfl M, et al. (2007) Activation-induced expression of CD137 permits detection, isolation, and expansion of the full repertoire of CD8+ T cells responding to antigen without requiring knowledge of epitope specificities. Blood 110(1):201-210.
39. Hernandez-Chacon JA, et al. (2011) Costimulation through the CD137/4-1BB pathway protects human melanoma tumor-infiltrating lymphocytes from activation-induced cell death and enhances antitumor effector function. J Immunother 34(3):236-250.
40. Chacon JA, et al. (2013) Co-stimulation through 4-1BB/CD137 improves the expansion and function of CD8(+) melanoma tumor-infiltrating lymphocytes for adoptive T-cell therapy. PLoS ONE 8(4):e60031.
41. Hendriks J, et al. (2005) During viral infection of the respiratory tract, CD27, 4-1BB, and OX40 collectively determine formation of CD8+ memory T cells and their capacity for secondary expansion. J Immunol 175(3):1665-1676.