Blockade of the checkpoint receptor TIGIT prevents NK cell exhaustion and elicits potent anti-tumor immunity

Nature Immunology

Volumn 19, Issue 7, 2018, Pages 723-732

  Zhang, Qing ^a,b   Bi, Jiacheng ^b,c   Zheng, Xiaodong ^b   Chen, Yongyan ^b   Wang, Hua ^d   Wu, Wenyong ^d   Wang, Zhengguang ^d   Wu, Qiang ^d   Peng, Hui ^b   Wei, Haiming ^a,b   Sun, Rui ^a,b   Tian, Zhigang ^a,b  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c SHENZHEN INSTITUTES OF ADVANCED TECHNOLOGY   (China)

^d ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC MONOCLONAL ANTIBODY; CHECKPOINT RECEPTOR TIGIT; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; IMMUNOGLOBULIN RECEPTOR; PROGRAMMED DEATH 1 LIGAND 1; UNCLASSIFIED DRUG; T CELL IG AND ITIM DOMAIN PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CANCER GROWTH; CELLULAR IMMUNITY; COLON CANCER; CONTROLLED STUDY; EXHAUSTION; HUMAN; IMMUNORECEPTOR TYROSINE BASED INHIBITION MOTIF; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; TUMOR IMMUNITY; ADAPTIVE IMMUNITY; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; C57BL MOUSE; CELL LINE; COLON TUMOR; EXPERIMENTAL MELANOMA; EXPERIMENTAL NEOPLASM; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; METABOLISM; NONOBESE DIABETIC MOUSE; SCID MOUSE; TUMOR ASSOCIATED LEUKOCYTE;

ADAPTIVE IMMUNITY; ANIMALS; CELL LINE; COLONIC NEOPLASMS; HUMANS; IMMUNOLOGIC MEMORY; KILLER CELLS, NATURAL; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA, EXPERIMENTAL; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; NEOPLASMS, EXPERIMENTAL; RECEPTORS, IMMUNOLOGIC;

EID: 85048669393     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/s41590-018-0132-0     Document Type: Article

References (39)

1. Lanier, L. L. NK cell recognition. Annu. Rev. Immunol. 23, 225-274 (2005).
2. Zhang, Q. F. et al. Liver-infiltrating CD11b-CD27- NK subsets account for NK-cell dysfunction in patients with hepatocellular carcinoma and are associated with tumor progression. Cell. Mol. Immunol. 14, 819-829 (2017).
3. Long, E. O., Kim, H. S., Liu, D., Peterson, M. E. &Rajagopalan, S. Controlling natural killer cell responses: integration of signals for activation and inhibition. Annu. Rev. Immunol. 31, 227-258 (2013).
4. Chen, L. &Flies, D. B. Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat. Rev. Immunol. 13, 227-242 (2013).
5. Pardoll, D. M. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 12, 252-264 (2012).
6. Zou, W., Wolchok, J. D. &Chen, L. PD-L1 (B7-H1) and PD-1 pathway blockade for cancer therapy: mechanisms, response biomarkers, and combinations. Sci. Transl. Med. 8, 328rv4 (2016).
7. Sharma, P. &Allison, J. P. Immune checkpoint targeting in cancer therapy: toward combination strategies with curative potential. Cell 161, 205-214 (2015).
8. Yu, X. et al. The surface protein TIGIT suppresses T cell activation by promoting the generation of mature immunoregulatory dendritic cells. Nat. Immunol. 10, 48-57 (2009).
9. Stanietsky, N. et al. The interaction of TIGIT with PVR and PVRL2 inhibits human NK cell cytotoxicity. Proc. Natl. Acad. Sci. USA 106, 17858-17863 (2009).
10. Bi, J. et al. T-cell Ig and ITIM domain regulates natural killer cell activation in murine acute viral hepatitis. Hepatology 59, 1715-1725 (2014).
11. Bi, J. et al. TIGIT safeguards liver regeneration through regulating natural killer cell-hepatocyte crosstalk. Hepatology 60, 1389-1398 (2014).
12. Joller, N. et al. Treg cells expressing the coinhibitory molecule TIGIT selectively inhibit proinflammatory Th1 and Th17 cell responses. Immunity 40, 569-581 (2014).
13. Johnston, R. J. et al. The immunoreceptor TIGIT regulates antitumor and antiviral CD8+ T cell effector function. Cancer Cell 26, 923-937 (2014).
14. Chauvin, J. M. et al. TIGIT and PD-1 impair tumor antigen-specific CD8+ T cells in melanoma patients. J. Clin. Invest. 125, 2046-2058 (2015).
15. Kong, Y. et al. T-cell immunoglobulin and ITIM domain (TIGIT) associates with CD8+ T cell exhaustion and poor clinical outcome in AML patients. Clin. Cancer Res. 22, 3057-3066 (2016).
16. Shibuya, A. et al. DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity 4, 573-581 (1996).
17. Chan, C. J. et al. The receptors CD96 and CD226 oppose each other in the regulation of natural killer cell functions. Nat. Immunol. 15, 431-438 (2014).
18. Kurtulus, S. et al. TIGIT predominantly regulates the immune response via regulatory T cells. J. Clin. Invest. 125, 4053-4062 (2015).
19. van Elsas, A., Hurwitz, A. A. &Allison, J. P. Combination immunotherapy of B16 melanoma using anti-cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) and granulocyte/macrophage colony-stimulating factor (GM-CSF)-producing vaccines induces rejection of subcutaneous and metastatic tumors accompanied by autoimmune depigmentation. J. Exp. Med. 190, 355-366 (1999).
20. Yang, Y. F. et al. Enhanced induction of antitumor T-cell responses by cytotoxic T lymphocyte-associated molecule-4 blockade: the effect is manifested only at the restricted tumor-bearing stages. Cancer Res. 57, 4036-4041 (1997).
21. Quezada, S. A., Peggs, K. S., Curran, M. A. &Allison, J. P. CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells. J. Clin. Invest. 116, 1935-1945 (2006).
22. Li, B. et al. Anti-programmed death-1 synergizes with granulocyte macrophage colony-stimulating factor-secreting tumor cell immunotherapy providing therapeutic benefit to mice with established tumors. Clin. Cancer Res. 15, 1623-1634 (2009).
23. Curran, M. A. &Allison, J. P. Tumor vaccines expressing flt3 ligand synergize with ctla-4 blockade to reject preimplanted tumors. Cancer Res. 69, 7747-7755 (2009).
24. 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).
25. Ngiow, S. F. et al. Anti-TIM3 antibody promotes T cell IFN-γ-mediated antitumor immunity and suppresses established tumors. Cancer Res. 71, 3540-3551 (2011).
26. Dong, J., McPherson, C. M. &Stambrook, P. J. Flt-3 ligand: a potent dendritic cell stimulator and novel antitumor agent. Cancer Biol. Ther. 1, 486-489 (2002).
27. Hou, S. et al. Eradication of hepatoma and colon cancer in mice with Flt3L gene therapy in combination with 5-FU. Cancer Immunol. Immunother. 56, 1605-1613 (2007).
28. Salmon, H. et al. Expansion and activation of CD103+ dendritic cell progenitors at the tumor site enhances tumor responses to therapeutic PD-L1 and BRAF inhibition. Immunity 44, 924-938 (2016).
29. Zou, W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat. Rev. Cancer 5, 263-274 (2005).
30. Nagamura-Inoue, T., Mori, Y., Yizhou, Z., Watanabe, N. &Takahashi, T. A. Differential expansion of umbilical cord blood mononuclear cell-derived natural killer cells dependent on the dose of interleukin-15 with Flt3L. Exp. Hematol. 32, 202-209 (2004).
31. Lin, S. J., Yang, M. H., Chao, H. C., Kuo, M. L. &Huang, J. L. Effect of interleukin-15 and Flt3-ligand on natural killer cell expansion and activation: umbilical cord vs. adult peripheral blood mononuclear cells. Pediatr. Allergy Immunol. 11, 168-174 (2000).
32. Stanietsky, N. et al. Mouse TIGIT inhibits NK-cell cytotoxicity upon interaction with PVR. Eur. J. Immunol. 43, 2138-2150 (2013).
33. Gur, C. et al. Binding of the Fap2 protein of Fusobacterium nucleatum to human inhibitory receptor TIGIT protects tumors from immune cell attack. Immunity 42, 344-355 (2015).
34. Segal, N. H. et al. A phase I dose escalation and cohort expansion study of lirilumab (anti-KIR; BMS-986015) in combination with nivolumab (anti-PD-1; BMS-936558, ONO-4538) in advanced solid tumors. ASCO Annual Meeting Proc. 2014, TPS3115 (2014).
35. Zheng, M., Sun, R., Wei, H. &Tian, Z. NK cells help induce anti-hepatitis B virus CD8+ T cell immunity in mice. J. Immunol. 196, 4122-4131 (2016).
36. Liu, Y. et al. Uncompromised NK cell activation is essential for virus-specific CTL activity during acute influenza virus infection. Cell. Mol. Immunol. https://doi.org/10.1038/cmi.2017.10 (2017).
37. Twyman-Saint Victor, C. et al. Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature 520, 373-377 (2015).
38. Yang, X. et al. Targeting the tumor microenvironment with interferon-β bridges innate and adaptive immune responses. Cancer Cell 25, 37-48 (2014).
39. Hou, X. et al. CD205-TLR9-IL-12 axis contributes to CpG-induced oversensitive liver injury in HBsAg transgenic mice by promoting the interaction of NKT cells with Kupffer cells. Cell. Mol. Immunol. 14, 675-684 (2017).