Interdependent IL-7 and IFN-γ signalling in T-cell controls tumour eradication by combined α-CTLA-4+α-PD-1 therapy

Nature Communications

Volumn 7, Issue , 2016, Pages

  Shi, Lewis Zhichang ^a   Fu, Tihui ^a   Guan, Baoxiang ^a   Chen, Jianfeng ^a   Blando, Jorge M ^a   Allison, James P ^a   Xiong, Liangwen ^a   Subudhi, Sumit K ^a   Gao, Jianjun ^a   Sharma, Padmanee ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; ALPHA PROGRAMMED DEATH 1 RECEPTOR; ANTINEOPLASTIC AGENT; CD8 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR ALPHA; UNCLASSIFIED DRUG; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; INTERLEUKIN 7 RECEPTOR; PROGRAMMED DEATH 1 RECEPTOR;

BIOMARKER; CANCER; CELLS AND CELL COMPONENTS; GENE; GENE EXPRESSION; IMMUNE RESPONSE; PROTEIN; TUMOR;

ANIMAL EXPERIMENT; ARTICLE; BLADDER CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CANCER SURVIVAL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DISEASE ERADICATION; FEMALE; HUMAN; IMMUNE RESPONSE; IMMUNOSUPPRESSIVE TREATMENT; LYMPHOCYTIC INFILTRATION; MALE; MONOTHERAPY; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THERAPY EFFECT; TUMOR GROWTH; TUMOR REJECTION; TUMOR VOLUME; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BLADDER TUMOR; C57BL MOUSE; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; METABOLISM; TUMOR ASSOCIATED LEUKOCYTE; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CELL LINE, TUMOR; CTLA-4 ANTIGEN; FEMALE; HUMANS; IMMUNOLOGIC MEMORY; INTERFERON-GAMMA; INTERLEUKIN-7; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MICE, INBRED BALB C; MICE, INBRED C57BL; PROGRAMMED CELL DEATH 1 RECEPTOR; RECEPTORS, INTERLEUKIN-7; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; UP-REGULATION; URINARY BLADDER NEOPLASMS;

EID: 84981357603     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms12335     Document Type: Article

References (57)

1. Ishida, Y., Agata, Y., Shibahara, K. & Honjo, T. Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J. 11, 3887-3895 (1992).
2. Sharma, P. & Allison, J. P. The future of immune checkpoint therapy. Science 348, 56-61 (2015).
3. Tivol, E. A., et al. Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 3, 541-547 (1995).
4. Leach, D. R., Krummel, M. F. & Allison, J. P. Enhancement of antitumor immunity by CTLA-4 blockade. Science 271, 1734-1736 (1996).
5. Hodi, F. S., et al. Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363, 711-723 (2010).
6. Robert, C., et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N. Engl. J. Med. 364, 2517-2526 (2011).
7. Hamid, O., et al. Safety and tumour responses with lambrolizumab (anti-PD-1) in melanoma. N. Engl. J. Med. 369, 134-144 (2013).
8. Robert, C., et al. Nivolumab in previously untreated melanoma without BRAF mutation. N. Engl. J. Med. 372, 320-330 (2015).
9. Curran, M. A., Montalvo, W., Yagita, H. & Allison, J. P. PD-1 and CTLA-4 combination blockade expands infiltrating T cells and reduces regulatory T and myeloid cells within B16 melanoma tumors. Proc. Natl Acad. Sci. USA 107, 4275-4280 (2010).
10. Duraiswamy, J., Kaluza, K. M., Freeman, G. J. & Coukos, G. Dual blockade of PD-1 and CTLA-4 combined with tumour vaccine effectively restores T-cell rejection function in tumors. Cancer Res. 73, 3591-3603 (2013).
11. Lussier, D. M., Johnson, J. L., Hingorani, P. & Blattman, J. N. Combination immunotherapy with alpha-CTLA-4 and alpha-PD-L1 antibody blockade prevents immune escape and leads to complete control of metastatic osteosarcoma. J. Immunother. Cancer 3, 21 (2015).
12. Larkin, J., et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N. Engl. J. Med. 373, 23-34 (2015).
13. Wolchok, J. D., et al. Nivolumab plus ipilimumab in advanced melanoma. N. Engl. J. Med. 369, 122-133 (2013).
14. Hammers, H. J., et al. Phase I study of nivolumab in combination with ipilimumab in metastatic renal cell carcinoma (mRCC). J. Clin. Oncol. 32, 5s (2014).
15. Antonia, S. J., et al. Nivolumab (anti-PD-1; BMS-936558, ONO-4538) and ipilimumab in first-line NSCLC: interim phase I results. J. Clin. Oncol. 32, 5s (2014).
16. Callahan, M. K., et al. A phase 1 study to evaluate the safety and tolerability of MEDI4736, an anti-PD-L1 antibody, in combination with tremelimumab in patients with advanced solid tumors. J. Clin. Oncol. 32, 5s (2014).
17. Carthon, B. C., et al. Preoperative CTLA-4 blockade: tolerability and immune monitoring in the setting of a presurgical clinical trial. Clin. Cancer Res. 16, 2861-2871 (2010).
18. Loskog, A., et al. Adenovirus CD40 ligand gene therapy counteracts immune escape mechanisms in the tumor microenvironment. J. Immunol. 172, 7200-7205 (2004).
19. O'Donnell, M. A., et al. The essential role of interferon-gamma during interleukin-12 therapy for murine transitional cell carcinoma of the bladder. J. Urol. 171, 1336-1342 (2004).
20. Chen, L. & Han, X. Anti-PD-1/PD-L1 therapy of human cancer: past, present, and future. J. Clin. Invest. 125, 3384-3391 (2015).
21. Summerhayes, I. C. & Franks, L. M. Effects of donor age on neoplastic transformation of adult mouse bladder epithelium in vitro. J. Natl Cancer Inst. 62, 1017-1023 (1979).
22. Hamid, O., et al. A prospective phase II trial exploring the association between tumor microenvironment biomarkers and clinical activity of ipilimumab in advanced melanoma. J. Transl. Med. 9, 204 (2011).
23. Peng, W., et al. PD-1 blockade enhances T-cell migration to tumors by elevating IFN-gamma inducible chemokines. Cancer Res. 72, 5209-5218 (2012).
24. Ribas, A., et al. Intratumoral immune cell infiltrates, FoxP3, and indoleamine 2,3-dioxygenase in patients with melanoma undergoing CTLA4 blockade. Clin. Cancer Res. 15, 390-399 (2009).
25. Simpson, T. R., et al. Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma. J. Exp. Med. 210, 1695-1710 (2013).
26. Talmadge, J. E., Meyers, K. M., Prieur, D. J. & Starkey, J. R. Role of NK cells in tumour growth and metastasis in beige mice. Nature 284, 622-624 (1980).
27. Bendelac, A., Rivera, M. N., Park, S. H. & Roark, J. H. Mouse CD1-specific NK1 T cells: development, specificity, and function. Annu. Rev. Immunol. 15, 535-562 (1997).
28. Smyth, M. J., et al. Differential tumor surveillance by natural killer (NK) and NKT cells. J. Exp. Med. 191, 661-668 (2000).
29. Lotze, M. T., Grimm, E. A., Mazumder, A., Strausser, J. L. & Rosenberg, S. A. Lysis of fresh and cultured autologous tumor by human lymphocytes cultured in T-cell growth factor. Cancer Res. 41, 4420-4425 (1981).
30. Shankaran, V., et al. IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. Nature 410, 1107-1111 (2001).
31. Wang, A., et al. The stoichiometric production of IL-2 and IFN-gamma mRNA defines memory T cells that can self-renew after adoptive transfer in humans. Sci. Transl. Med. 4, 149ra120 (2012).
32. Gubin, M. M., et al. Checkpoint blockade cancer immunotherapy targets tumour-specific mutant antigens. Nature 515, 577-581 (2014).
33. Walzer, T., Arpin, C., Beloeil, L. & Marvel, J. Differential in vivo persistence of two subsets of memory phenotype CD8 T cells defined by CD44 and CD122 expression levels. J. Immunol. 168, 2704-2711 (2002).
34. Kaech, S. M., et al. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4, 1191-1198 (2003).
35. Kondrack, R. M., et al. Interleukin 7 regulates the survival and generation of memory CD4 cells. J. Exp. Med. 198, 1797-1806 (2003).
36. Surh, C. D. & Sprent, J. Homeostasis of naive and memory T cells. Immunity 29, 848-862 (2008).
37. Das, R., et al. Combination therapy with anti-CTLA-4 and anti-PD-1 leads to distinct immunologic changes in vivo. J. Immunol. 194, 950-959 (2015).
38. Topalian, S. L., Drake, C. G. & Pardoll, D. M. Targeting the PD-1/B7-H1 (PD-L1) pathway to activate anti-tumor immunity. Curr. Opin. Immunol. 24, 207-212 (2012).
39. Perna, S. K., et al. Interleukin-7 mediates selective expansion of tumorredirected cytotoxic T lymphocytes (CTLs) without enhancement of regulatory T-cell inhibition. Clin. Cancer Res. 20, 131-139 (2014).
40. Andersson, A., et al. IL-7 promotes CXCR3 ligand-dependent T cell antitumor reactivity in lung cancer. J. Immunol. 182, 6951-6958 (2009).
41. Heninger, A. K., et al. IL-7 abrogates suppressive activity of human CD4+CD25+FOXP3+ regulatory T cells and allows expansion of alloreactive and autoreactive T cells. J. Immunol. 189, 5649-5658 (2012).
42. Pellegrini, M., et al. Adjuvant IL-7 antagonizes multiple cellular and molecular inhibitory networks to enhance immunotherapies. Nat. Med. 15, 528-536 (2009).
43. Sportes, C., et al. Administration of rhIL-7 in humans increases in vivo TCR repertoire diversity by preferential expansion of naive T cell subsets. J. Exp. Med. 205, 1701-1714 (2008).
44. Rosenberg, S. A., et al. IL-7 administration to humans leads to expansion of CD8+ and CD4+ cells but a relative decrease of CD4+ T-regulatory cells. J. Immunother. 29, 313-319 (2006).
45. Topalian, S. L., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 366, 2443-2454 (2012).
46. Johnson, C. B., et al. Effector CD8+ T-cell Engraftment and Antitumor Immunity in Lymphodepleted Hosts Is IL7Ralpha Dependent. Cancer Immunol. Res. 3, 1364-1374 (2015).
47. Bulliard, Y., et al. Activating Fc gamma receptors contribute to the antitumor activities of immunoregulatory receptor-targeting antibodies. J. Exp. Med. 210, 1685-1693 (2013).
48. Simpson, T. R., Quezada, S. A. & Allison, J. P. Regulation of CD4 T cell activation and effector function by inducible costimulator (ICOS). Curr. Opin. Immunol. 22, 326-332 (2010).
49. Oshima, S., et al. Interferon regulatory factor 1 (IRF-1) and IRF-2 distinctively up-regulate gene expression and production of interleukin-7 in human intestinal epithelial cells. Mol. Cell. Biol. 24, 6298-6310 (2004).
50. Belyaev, N. N., et al. Induction of an IL7-R(+)c-Kit(hi) myelolymphoid progenitor critically dependent on IFN-gamma signaling during acute malaria. Nat. Immunol. 11, 477-485 (2010).
51. Colpitts, S. L., Dalton, N. M. & Scott, P. IL-7 receptor expression provides the potential for long-term survival of both CD62Lhigh central memory T cells and Th1 effector cells during Leishmania major infection. J. Immunol. 182, 5702-5711 (2009).
52. Mangsbo, S. M., et al. Enhanced tumor eradication by combining CTLA-4 or PD-1 blockade with CpG therapy. J. Immunother. 33, 225-235 (2010).
53. Powles, T., et al. MPDL3280A (anti-PD-L1) treatment leads to clinical activity in metastatic bladder cancer. Nature 515, 558-562 (2014).
54. Shi, L. Z., et al. Inhibitory role of the transcription repressor Gfi1 in the generation of thymus-derived regulatory T cells. Proc. Natl Acad. Sci. USA 110, E3198-E3205 (2013).
55. Herbst, R. S., et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 515, 563-567 (2014).
56. Tumeh, P. C., et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 515, 568-571 (2014).
57. Twyman-Saint Victor, C., et al. Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature 520, 373-377 (2015).