Immune checkpoint receptors in cancer: redundant by design?

Current Opinion in Immunology

Volumn 45, Issue , 2017, Pages 37-42

  Li, Jing ^a   Ni, Ling ^a   Dong, Chen ^a  

^a Tsinghua University   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HUMAN; IMMUNOCOMPETENT CELL; IMMUNOSUPPRESSIVE TREATMENT; T LYMPHOCYTE; TUMOR CELL; TUMOR IMMUNITY; ANIMAL; CELLULAR IMMUNITY; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; NEOPLASM; PATHOLOGY;

IMMUNOGLOBULIN RECEPTOR;

ANIMALS; HUMANS; IMMUNE TOLERANCE; IMMUNITY, CELLULAR; NEOPLASMS; RECEPTORS, IMMUNOLOGIC; T-LYMPHOCYTES;

EID: 85011976409     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2017.01.001     Document Type: Review

References (51)

1. 1 Pardoll, D.M., The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 12 (2012), 252–264.
2. 2 Brunet, J.F., Denizot, F., Luciani, M.F., Roux-Dosseto, M., Suzan, M., Mattei, M.G., Golstein, P., A new member of the immunoglobulin superfamily—CTLA-4. Nature 328 (1987), 267–270.
3. 3 Tivol, E.A., Borriello, F., Schweitzer, A.N., Lynch, W.P., Bluestone, J.A., Sharpe, A.H., Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 3 (1995), 541–547.
4. 4 Gibson, H.M., Hedgcock, C.J., Aufiero, B.M., Wilson, A.J., Hafner, M.S., Tsokos, G.C., Wong, H.K., Induction of the CTLA-4 gene in human lymphocytes is dependent on NFAT binding the proximal promoter. J Immunol 179 (2007), 3831–3840.
5. 5 Zheng, Y., Josefowicz, S.Z., Kas, A., Chu, T.T., Gavin, M.A., Rudensky, A.Y., Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells. Nature 445 (2007), 936–940.
6. 6 Walunas, T.L., Bakker, C.Y., Bluestone, J.A., CTLA-4 ligation blocks CD28-dependent T cell activation. J Exp Med 183 (1996), 2541–2550.
7. 7 Collins, A.V., Brodie, D.W., Gilbert, R.J., Iaboni, A., Manso-Sancho, R., Walse, B., Stuart, D.I., van der Merwe, P.A., Davis, S.J., The interaction properties of costimulatory molecules revisited. Immunity 17 (2002), 201–210.
8. 8•• Schildberg, F.A., Klein, S.R., Freeman, G.J., Sharpe, A.H., Coinhibitory pathways in the B7-CD28 ligand-receptor family. Immunity 44 (2016), 955–972 This review summarizes the recent advances in the understanding of coinhibitory pathways in the B7-CD28 family, including CTLA-4 and PD-1 pathways.
9. 9 Jie, H.B., Schuler, P.J., Lee, S.C., Srivastava, R.M., Argiris, A., Ferrone, S., Whiteside, T.L., Ferris, R.L., CTLA-4(+) regulatory T cells increased in cetuximab-treated head and neck cancer patients suppress NK cell cytotoxicity and correlate with poor prognosis. Cancer Res 75 (2015), 2200–2210.
10. 10 Nishimura, H., Nose, M., Hiai, H., Minato, N., Honjo, T., Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 11 (1999), 141–151.
11. 11 Nishimura, H., Okazaki, T., Tanaka, Y., Nakatani, K., Hara, M., Matsumori, A., Sasayama, S., Mizoguchi, A., Hiai, H., Minato, N., et al. Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 291 (2001), 319–322.
12. 12 Austin, J.W., Lu, P., Majumder, P., Ahmed, R., Boss, J.M., STAT3, STAT4, NFATc1, and CTCF regulate PD-1 through multiple novel regulatory regions in murine T cells. J Immunol 192 (2014), 4876–4886.
13. 13 Terawaki, S., Chikuma, S., Shibayama, S., Hayashi, T., Yoshida, T., Okazaki, T., Honjo, T., IFN-alpha directly promotes programmed cell death-1 transcription and limits the duration of T cell-mediated immunity. J Immunol 186 (2011), 2772–2779.
14. 14 Yokosuka, T., Takamatsu, M., Kobayashi-Imanishi, W., Hashimoto-Tane, A., Azuma, M., Saito, T., Programmed cell death 1 forms negative costimulatory microclusters that directly inhibit T cell receptor signaling by recruiting phosphatase SHP2. J Exp Med 209 (2012), 1201–1217.
15. 15 Li, J., Jie, H.B., Lei, Y., Gildener-Leapman, N., Trivedi, S., Green, T., Kane, L.P., Ferris, R.L., PD-1/SHP-2 inhibits Tc1/Th1 phenotypic responses and the activation of T cells in the tumor microenvironment. Cancer Res 75 (2015), 508–518.
16. 16 Karunarathne, D.S., Horne-Debets, J.M., Huang, J.X., Faleiro, R., Leow, C.Y., Amante, F., Watkins, T.S., Miles, J.J., Dwyer, P.J., Stacey, K.J., et al. Programmed death-1 ligand 2-mediated regulation of the PD-L1 to PD-1 axis is essential for establishing CD4(+) T cell immunity. Immunity 45 (2016), 333–345.
17. 17 Martin-Orozco, N., Wang, Y.H., Yagita, H., Dong, C., Cutting edge: programmed death (PD) ligand-1/PD-1 interaction is required for CD8+ T cell tolerance to tissue antigens. J Immunol 177 (2006), 8291–8295.
18. 18 Zhang, Y., Chung, Y., Bishop, C., Daugherty, B., Chute, H., Holst, P., Kurahara, C., Lott, F., Sun, N., Welcher, A.A., et al. Regulation of T cell activation and tolerance by PDL2. Proc Natl Acad Sci U S A 103 (2006), 11695–11700.
19. 19 Francisco, L.M., Salinas, V.H., Brown, K.E., Vanguri, V.K., Freeman, G.J., Kuchroo, V.K., Sharpe, A.H., PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J Exp Med 206 (2009), 3015–3029.
20. 20 Tumeh, P.C., Harview, C.L., Yearley, J.H., Shintaku, I.P., Taylor, E.J., Robert, L., Chmielowski, B., Spasic, M., Henry, G., Ciobanu, V., et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 515 (2014), 568–571.
21. 21• Larkin, J., Chiarion-Sileni, V., Gonzalez, R., Grob, J.J., Cowey, C.L., Lao, C.D., Schadendorf, D., Dummer, R., Smylie, M., Rutkowski, P., et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med 373 (2015), 23–34 This article reports the combincational therapy of checkpoint blockades, anti-CTLA-4 plus anti-PD-1 in the clinical trial, revealing the non-redundant suppressive effects of CTLA-4 and PD-1 in anti-tumor immunity.
22. 22 Antonia, S.J., Gettinger, S.N., Goldman, J., Brahmer, J., Borghaei, H., Chow, L.Q., Ready, N.E., Gerber, D.E., Juergens, R., Shepherd, F., et al. ORAL01.03: CheckMate 012: safety and efficacy of first-line nivolumab and ipilimumab in advanced NSCLC: topic: medical oncology. J Thorac Oncol 11 (2016), S250–S251.
23. 23 Monney, L., Sabatos, C.A., Gaglia, J.L., Ryu, A., Waldner, H., Chernova, T., Manning, S., Greenfield, E.A., Coyle, A.J., Sobel, R.A., et al. Th1-specific cell surface protein Tim-3 regulates macrophage activation and severity of an autoimmune disease. Nature 415 (2002), 536–541.
24. 24 Sabatos, C.A., Chakravarti, S., Cha, E., Schubart, A., Sanchez-Fueyo, A., Zheng, X.X., Coyle, A.J., Strom, T.B., Freeman, G.J., Kuchroo, V.K., Interaction of Tim-3 and Tim-3 ligand regulates T helper type 1 responses and induction of peripheral tolerance. Nat Immunol 4 (2003), 1102–1110.
25. 25•• Anderson, A.C., Joller, N., Kuchroo, V.K., Lag-3, Tim-3, and TIGIT: co-inhibitory receptors with specialized functions in immune regulation. Immunity 44 (2016), 989–1004 This review summaizes the functions, signaling and roles in disease of LAG-3, Tim-3 and TIGIT.
26. 26 Zhu, C., Anderson, A.C., Schubart, A., Xiong, H., Imitola, J., Khoury, S.J., Zheng, X.X., Strom, T.B., Kuchroo, V.K., The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat Immunol 6 (2005), 1245–1252.
27. 27 Chiba, S., Baghdadi, M., Akiba, H., Yoshiyama, H., Kinoshita, I., Dosaka-Akita, H., Fujioka, Y., Ohba, Y., Gorman, J.V., Colgan, J.D., et al. Tumor-infiltrating DCs suppress nucleic acid-mediated innate immune responses through interactions between the receptor TIM-3 and the alarmin HMGB1. Nat Immunol 13 (2012), 832–842.
28. 28 Huang, Y.H., Zhu, C., Kondo, Y., Anderson, A.C., Gandhi, A., Russell, A., Dougan, S.K., Petersen, B.S., Melum, E., Pertel, T., et al. CEACAM1 regulates TIM-3-mediated tolerance and exhaustion. Nature 517 (2015), 386–390.
29. 29 Lee, J., Su, E.W., Zhu, C., Hainline, S., Phuah, J., Moroco, J.A., Smithgall, T.E., Kuchroo, V.K., Kane, L.P., Phosphotyrosine-dependent coupling of Tim-3 to T-cell receptor signaling pathways. Mol Cell Biol 31 (2011), 3963–3974.
30. 30 Rangachari, M., Zhu, C., Sakuishi, K., Xiao, S., Karman, J., Chen, A., Angin, M., Wakeham, A., Greenfield, E.A., Sobel, R.A., et al. Bat3 promotes T cell responses and autoimmunity by repressing Tim-3-mediated cell death and exhaustion. Nat Med 18 (2012), 1394–1400.
31. 31 Davidson, D., Schraven, B., Veillette, A., PAG-associated FynT regulates calcium signaling and promotes anergy in T lymphocytes. Mol Cell Biol 27 (2007), 1960–1973.
32. 32 Boivin, N., Baillargeon, J., Doss, P.M., Roy, A.P., Rangachari, M., Interferon-beta suppresses murine Th1 cell function in the absence of antigen-presenting cells. PLoS One, 10, 2015, e0124802.
33. 33 Jones, R.B., Ndhlovu, L.C., Barbour, J.D., Sheth, P.M., Jha, A.R., Long, B.R., Wong, J.C., Satkunarajah, M., Schweneker, M., Chapman, J.M., et al. Tim-3 expression defines a novel population of dysfunctional T cells with highly elevated frequencies in progressive HIV-1 infection. J Exp Med 205 (2008), 2763–2779.
34. 34 McMahan, R.H., Golden-Mason, L., Nishimura, M.I., McMahon, B.J., Kemper, M., Allen, T.M., Gretch, D.R., Rosen, H.R., Tim-3 expression on PD-1+ HCV-specific human CTLs is associated with viral persistence, and its blockade restores hepatocyte-directed in vitro cytotoxicity. J Clin Invest 120 (2010), 4546–4557.
35. 35 Wu, W., Shi, Y., Li, J., Chen, F., Chen, Z., Zheng, M., Tim-3 expression on peripheral T cell subsets correlates with disease progression in hepatitis B infection. Virol J, 8, 2011, 113.
36. 36 Sakuishi, K., Apetoh, L., Sullivan, J.M., Blazar, B.R., Kuchroo, V.K., Anderson, A.C., Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J Exp Med 207 (2010), 2187–2194.
37. 37 Sakuishi, K., Ngiow, S.F., Sullivan, J.M., Teng, M.W., Kuchroo, V.K., Smyth, M.J., Anderson, A.C., TIM3+FOXP3+ regulatory T cells are tissue-specific promoters of T-cell dysfunction in cancer. Oncoimmunology, 2, 2013, e23849.
38. 38 Koyama, S., Akbay, E.A., Li, Y.Y., Herter-Sprie, G.S., Buczkowski, K.A., Richards, W.G., Gandhi, L., Redig, A.J., Rodig, S.J., Asahina, H., et al. Adaptive resistance to therapeutic PD-1 blockade is associated with upregulation of alternative immune checkpoints. Nat Commun, 7, 2016, 10501.
39. 39 Jin, H.T., Anderson, A.C., Tan, W.G., West, E.E., Ha, S.J., Araki, K., Freeman, G.J., Kuchroo, V.K., Ahmed, R., Cooperation of Tim-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection. Proc Natl Acad Sci U S A 107 (2010), 14733–14738.
40. 40 Fourcade, J., Sun, Z., Benallaoua, M., Guillaume, P., Luescher, I.F., Sander, C., Kirkwood, J.M., Kuchroo, V., Zarour, H.M., Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD8+ T cell dysfunction in melanoma patients. J Exp Med 207 (2010), 2175–2186.
41. 41 Miyazaki, T., Dierich, A., Benoist, C., Mathis, D., Independent modes of natural killing distinguished in mice lacking Lag3. Science 272 (1996), 405–408.
42. 42 Workman, C.J., Vignali, D.A., The CD4-related molecule, LAG-3 (CD223), regulates the expansion of activated T cells. Eur J Immunol 33 (2003), 970–979.
43. 43 Huard, B., Prigent, P., Tournier, M., Bruniquel, D., Triebel, F., CD4/major histocompatibility complex class II interaction analyzed with CD4- and lymphocyte activation gene-3 (LAG-3)-Ig fusion proteins. Eur J Immunol 25 (1995), 2718–2721.
44. 44 Liu, B., Wang, M., Wang, X., Zhao, D., Liu, D., Liu, J., Chen, P.J., Yang, D., He, F., Tang, L., Liver sinusoidal endothelial cell lectin inhibits CTL-dependent virus clearance in mouse models of viral hepatitis. J Immunol 190 (2013), 4185–4195.
45. 45 Xu, F., Liu, J., Liu, D., Liu, B., Wang, M., Hu, Z., Du, X., Tang, L., He, F., LSECtin expressed on melanoma cells promotes tumor progression by inhibiting antitumor T-cell responses. Cancer Res 74 (2014), 3418–3428.
46. 46 Kouo, T., Huang, L., Pucsek, A.B., Cao, M., Solt, S., Armstrong, T., Jaffee, E., Galectin-3 shapes antitumor immune responses by suppressing CD8+ T cells via LAG-3 and inhibiting expansion of plasmacytoid dendritic cells. Cancer Immunol Res 3 (2015), 412–423.
47. 47 Workman, C.J., Dugger, K.J., Vignali, D.A., Cutting edge: molecular analysis of the negative regulatory function of lymphocyte activation gene-3. J Immunol 169 (2002), 5392–5395.
48. 48 Grosso, J.F., Kelleher, C.C., Harris, T.J., Maris, C.H., Hipkiss, E.L., De Marzo, A., Anders, R., Netto, G., Getnet, D., Bruno, T.C., et al. LAG-3 regulates CD8+ T cell accumulation and effector function in murine self- and tumor-tolerance systems. J Clin Invest 117 (2007), 3383–3392.
49. 49 Okazaki, T., Okazaki, I.M., Wang, J., Sugiura, D., Nakaki, F., Yoshida, T., Kato, Y., Fagarasan, S., Muramatsu, M., Eto, T., et al. PD-1 and LAG-3 inhibitory co-receptors act synergistically to prevent autoimmunity in mice. J Exp Med 208 (2011), 395–407.
50. 50 Blackburn, S.D., Shin, H., Haining, W.N., Zou, T., Workman, C.J., Polley, A., Betts, M.R., Freeman, G.J., Vignali, D.A., Wherry, E.J., Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat Immunol 10 (2009), 29–37.
51. 51 Woo, S.R., Turnis, M.E., Goldberg, M.V., Bankoti, J., Selby, M., Nirschl, C.J., Bettini, M.L., Gravano, D.M., Vogel, P., Liu, C.L., et al. Immune inhibitory molecules LAG-3 and PD-1 synergistically regulate T-cell function to promote tumoral immune escape. Cancer Res 72 (2012), 917–927.