References
- Thommen DS, Schumacher TN (2018) T cell dysfunction in cancer. Cancer Cell 33, 547-562 https://doi.org/10.1016/j.ccell.2018.03.012
- Chen DS, Mellman I (2013) Oncology meets immunology: the cancer-immunity cycle. Immunity 39, 1-10 https://doi.org/10.1016/j.immuni.2013.07.012
- Ribas A, Wolchok JD (2018) Cancer immunotherapy using checkpoint blockade. Science 359, 1350-1355 https://doi.org/10.1126/science.aar4060
- Gibney GT, Weiner LM, Atkins MB (2016) Predictive biomarkers for checkpoint inhibitor-based immunotherapy. Lancet Oncol 17, e542-e551 https://doi.org/10.1016/S1470-2045(16)30406-5
- Zaretsky JM, Garcia-Diaz A, Shin DS et al (2016) Mutations associated with acquired resistance to PD-1 blockade in melanoma. N Engl J Med 375, 819-829 https://doi.org/10.1056/NEJMoa1604958
- Kong X (2018) Discovery of new immune checkpoints: family grows up. Adv Exp Med Biol 1248, 61-82 https://doi.org/10.1007/978-981-15-3266-5_4
- Rotte A, Jin JY, Lemaire V (2018) Mechanistic overview of immune checkpoints to support the rational design of their combinations in cancer immunotherapy. Ann Oncol 29, 71-83 https://doi.org/10.1093/annonc/mdx686
- Chan CJ, Andrews DM, Smyth MJ (2012) Receptors that interact with nectin and nectin-like proteins in the immunosurveillance and immunotherapy of cancer. Curr Opin Immunol 24, 246-251 https://doi.org/10.1016/j.coi.2012.01.009
- Sanchez-Correa B, Valhondo I, Hassouneh F et al (2019) DNAM-1 and the TIGIT/PVRIG/TACTILE axis: novel immune checkpoints for natural killer cell-based cancer immunotherapy. Cancers (Basel) 11, 877 https://doi.org/10.3390/cancers11060877
- Whelan S, Ophir E, Kotturi MF et al (2019) PVRIG and PVRL2 are induced in cancer and inhibit CD8(+) T-cell function. Cancer Immunol Res 7, 257-268 https://doi.org/10.1158/2326-6066.cir-18-0442
- Marin-Acevedo JA, Soyano AE, Dholaria B, Knutson KL, Lou Y (2006) Cancer immunotherapy beyond immune checkpoint inhibitors. J Hematol Oncol 11, 8 https://doi.org/10.1186/s13045-017-0552-6
- Gorvel L, Olive D (2020) Targeting the "PVR-TIGIT axis" with immune checkpoint therapies. F1000Res 9, F1000 Faculty Rev-354
- Fuchs A, Colonna M (2006) The role of NK cell recognition of nectin and nectin-like proteins in tumor immunosurveillance. Semin Cancer Biol 16, 359-366 https://doi.org/10.1016/j.semcancer.2006.07.002
- Nakanishi H, Takai Y (2004) Roles of nectins in cell adhesion, migration and polarization. Biol Chem 385, 885-892 https://doi.org/10.1515/BC.2004.116
- Zhang Q, Bi J, Zheng X et al (2018) Blockade of the checkpoint receptor TIGIT prevents NK cell exhaustion and elicits potent anti-tumor immunity. Nat Immunol 19, 723-732 https://doi.org/10.1038/s41590-018-0132-0
- Kucan Brlic P, Lenac Rovis T, Cinamon G, Tsukerman P, Mandelboim O, Jonjic S (2019) Targeting PVR (CD155) and its receptors in anti-tumor therapy. Cell Mol Immunol 16, 40-52 https://doi.org/10.1038/s41423-018-0168-y
- Nishiwada S, Sho M, Yasuda S et al (2015) Clinical significance of CD155 expression in human pancreatic cancer. Anticancer Res 35, 2287-2297
- Triki H, Charfi S, Bouzidi L et al (2019) CD155 expression in human breast cancer: clinical significance and relevance to natural killer cell infiltration. Life Sci 231, 116543 https://doi.org/10.1016/j.lfs.2019.116543
- Carlsten M, Norell H, Bryceson YT (2009) Primary human tumor cells expressing CD155 impair tumor targeting by down-regulating DNAM-1 on NK cells. J Immunol 183, 4921-4930 https://doi.org/10.4049/jimmunol.0901226
- Joller N, Hafler JP, Brynedal B et al (2011) Cutting edge: TIGIT has T cell-intrinsic inhibitory functions. J Immunol 186, 1338-1342 https://doi.org/10.4049/jimmunol.1003081
- Fuchs A, Cella M, Giurisato E, Shaw AS, Colonna M (2004) Cutting edge: CD96 (tactile) promotes NK cell-target cell adhesion by interacting with the poliovirus receptor (CD155). J Immunol 172, 3994-3998 https://doi.org/10.4049/jimmunol.172.7.3994
- Yu X, Harden K, Gonzalez LC et al (2009) The surface protein TIGIT suppresses T cell activation by promoting the generation of mature immunoregulatory dendritic cells. Nat Immunol 10, 48-57 https://doi.org/10.1038/ni.1674
- Stanietsky N, Rovis TL, Glasner A et al (2013) Mouse TIGIT inhibits NK-cell cytotoxicity upon interaction with PVR. Eur J Immunol 43, 2138-2150 https://doi.org/10.1002/eji.201243072
- Deuss FA, Watson GM, Fu Z, Rossjohn J, Berry R (2019) Structural basis for CD96 immune receptor recognition of nectin-like protein-5, CD155. Structure 27, 219-228 https://doi.org/10.1016/j.str.2018.10.023
- Okumura G, Iguchi-Manaka A, Murata R, Yamashita-Kanemaru Y, Shibuya A, Shibuya K (2020) Tumor-derived soluble CD155 inhibits DNAM-1-mediated antitumor activity of natural killer cells. J Exp Med 217, 1
- Weulersse M, Asrir A, Pichler AC et al (2020) Eomesdependent loss of the co-activating receptor CD226 restrains CD8(+) T cell anti-tumor functions and limits the efficacy of cancer immunotherapy. Immunity 53, 824-839 https://doi.org/10.1016/j.immuni.2020.09.006
- Zhu Y, Paniccia A, Schulick AC et al (2016) Identification of CD112R as a novel checkpoint for human T cells. J Exp Med 213, 167-176 https://doi.org/10.1084/jem.20150785
- Pende D, Castriconi R, Romagnani P et al (2006) Expression of the DNAM-1 ligands, nectin-2 (CD112) and poliovirus receptor (CD155), on dendritic cells: relevance for natural killer-dendritic cell interaction. Blood 107, 2030-2036 https://doi.org/10.1182/blood-2005-07-2696
- Seth S, Maier MK, Qiu Q et al (2007) The murine pan T cell marker CD96 is an adhesion receptor for CD155 and nectin-1. Biochem Biophys Res Commun 364, 959-965 https://doi.org/10.1016/j.bbrc.2007.10.102
- Satoh-Horikawa K, Nakanishi H, Takahashi K (2000) Nectin-3, a new member of immunoglobulin-like cell adhesion molecules that shows homophilic and heterophilic cell-cell adhesion activities. J Biol Chem 275, 10291-10299 https://doi.org/10.1074/jbc.275.14.10291
- Reches A, Ophir Y, Stein N et al (2020) Nectin4 is a novel TIGIT ligand which combines checkpoint inhibition and tumor specificity. J Immunother Cancer 8, e000266 https://doi.org/10.1136/jitc-2019-000266
- Harjunpaa H, Guillerey C (2020) TIGIT as an emerging immune checkpoint. Clin Exp Immunol 200, 108-119 https://doi.org/10.1111/cei.13407
- Lozano E, Dominguez-Villar M, Kuchroo V, Hafler DA (2012) The TIGIT/CD226 axis regulates human T cell function. J Immunol 188, 3869-3875 https://doi.org/10.4049/jimmunol.1103627
- Johnston RJ, Comps-Agrar L, Hackney J et al (2014) The immunoreceptor TIGIT regulates antitumor and antiviral CD8(+) T cell effector function. Cancer Cell 26, 923-937 https://doi.org/10.1016/j.ccell.2014.10.018
- Joller N, Lozano E, Burkett PR et al (2014) Treg cells expressing the coinhibitory molecule TIGIT selectively inhibit proinflammatory Th1 and Th17 cell responses. Immunity 40, 569-581 https://doi.org/10.1016/j.immuni.2014.02.012
- Kurtulus S, Sakuishi K, Ngiow SF et al (2015) TIGIT predominantly regulates the immune response via regulatory T cells. J Clin Invest 125, 4053-4062 https://doi.org/10.1172/JCI81187
- Yang ZZ, Kim HJ, Wu H et al (2020) TIGIT expression is associated with T-cell suppression and exhaustion and predicts clinical outcome and anti-PD-1 response in follicular lymphoma. Clin Cancer Res 26, 5217-5231 https://doi.org/10.1158/1078-0432.ccr-20-0558
- Kong Y, Zhu L, Schell TD et al (2016) 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 https://doi.org/10.1158/1078-0432.CCR-15-2626
- Chauvin JM, Pagliano O, Fourcade J et al (2015) TIGIT and PD-1 impair tumor antigen-specific CD8(+) T cells in melanoma patients. J Clin Invest 125, 2046-2058 https://doi.org/10.1172/JCI80445
- Guillerey C, Harjunpaa H, Carrie N et al (2018) TIGIT immune checkpoint blockade restores CD8(+) T-cell immunity against multiple myeloma. Blood 132, 1689-1694 https://doi.org/10.1182/blood-2018-01-825265
- He W, Zhang H, Han F et al (2017) CD155T/TIGIT signaling regulates CD8(+) T-cell metabolism and promotes tumor progression in human gastric cancer. Cancer Res 77, 6375-6388 https://doi.org/10.1158/0008-5472.CAN-17-0381
- O'Brien SM, Klampatsa A, Thompson JC et al (2019) Function of human tumor-infiltrating lymphocytes in earlystage non-small cell lung cancer. Cancer Immunol Res 7, 896-909 https://doi.org/10.1158/2326-6066.CIR-18-0713
- Ostroumov D, Duong S, Wingerath J et al (2020) Transcriptome profiling identifies TIGIT as a marker of T cell exhaustion in liver cancer. Hepatology [Online ahead of print]
- Stalhammar G, Seregard S, Grossniklaus HE (2019) Expression of immune checkpoint receptors Indoleamine 2,3-dioxygenase and T cell Ig and ITIM domain in metastatic versus nonmetastatic choroidal melanoma. Cancer Med 8, 2784-2792 https://doi.org/10.1002/cam4.2167
- Xu D, Zhao E, Zhu C et al (2020) TIGIT and PD-1 may serve as potential prognostic biomarkers for gastric cancer. Immunobiology 225, 151915 https://doi.org/10.1016/j.imbio.2020.151915
- Wu L, Mao L, Liu JF et al (2019) Blockade of TIGIT/CD155 signaling reverses T-cell exhaustion and enhances antitumor capability in head and neck squamous cell carcinoma. Cancer Immunol Res 7, 1700-1713 https://doi.org/10.1158/2326-6066.cir-18-0725
- Lucca LE, Lerner BA, Park C et al (2020) Differential expression of the T-cell inhibitor TIGIT in glioblastoma and MS. Neurol Neuroimmunol Neuroinflamm 7, e712 https://doi.org/10.1212/nxi.0000000000000712
- Jin HS, Ko M, Choi DS et al (2020) CD226(hi)CD8(+) T cells are a prerequisite for anti-TIGIT immunotherapy. Cancer Immunol Res 8, 912-925 https://doi.org/10.1158/2326-6066.cir-19-0877
- McLane LM, Abdel-Hakeem MS, Wherry EJ (2019) CD8 T cell exhaustion during chronic viral infection and cancer. Annu Rev Immunol 37, 457-495 https://doi.org/10.1146/annurev-immunol-041015-055318
- Hashimoto M, Kamphorst AO, Im SJ et al (2018) CD8 T cell exhaustion in chronic infection and cancer: opportunities for interventions. Annu Rev Med 69, 301-318 https://doi.org/10.1146/annurev-med-012017-043208
- Tang W, Pan X, Han D et al (2019) Clinical significance of CD8(+) T cell immunoreceptor with Ig and ITIM domains(+) in locally advanced gastric cancer treated with SOX regimen after D2 gastrectomy. Oncoimmunology 8, e1593807 https://doi.org/10.1080/2162402x.2019.1593807
- Fuhrman CA, Yeh WI, Seay HR et al (2015) Divergent phenotypes of human regulatory T cells expressing the receptors TIGIT and CD226. J Immunol 195, 145-155 https://doi.org/10.4049/jimmunol.1402381
- Duan X, Liu J, Cui J et al (2019) Expression of TIGIT/CD155 and correlations with clinical pathological features in human hepatocellular carcinoma. Mol Med Rep 20, 3773-3781
- Fourcade J, Sun Z, Chauvin JM et al (2018) CD226 opposes TIGIT to disrupt Tregs in melanoma. JCI Insight 3, e121157 https://doi.org/10.1172/jci.insight.121157
- Dixon KO, Schorer M, Nevin J et al (2018) Functional anti-TIGIT antibodies regulate development of autoimmunity and antitumor immunity. J Immunol 200, 3000-3007 https://doi.org/10.4049/jimmunol.1700407
- Chiu DK, Yuen VW, Wing-Sum Cheu J et al (2020) Hepatocellular carcinoma cells up-regulate PVRL1, stabilizing poliovirus receptor and inhibiting the cytotoxic T-cell response via TIGIT to mediate tumor resistance to PD1 inhibitors in mice. Gastroenterology 159, 609-623 https://doi.org/10.1053/j.gastro.2020.03.074
- Lee BR, Chae S, Moon J et al (2020) Combination of PD-L1 and PVR determines sensitivity to PD-1 blockade. JCI Insight 5, e128633 https://doi.org/10.1172/jci.insight.128633
- Jin HS, Choi DS, Ko M et al (2019) Extracellular pH modulating injectable gel for enhancing immune checkpoint inhibitor therapy. J Control Release 315, 65-75 https://doi.org/10.1016/j.jconrel.2019.10.041
- Hung AL, Maxwell R, Theodros D et al (2018) TIGIT and PD-1 dual checkpoint blockade enhances antitumor immunity and survival in GBM. Oncoimmunology 7, e1466769 https://doi.org/10.1080/2162402x.2018.1466769
- Grapin M, Richard C, Limagne E et al (2019) Optimized fractionated radiotherapy with anti-PD-L1 and anti-TIGIT: a promising new combination. J Immunother Cancer 7, 160 https://doi.org/10.1186/s40425-019-0634-9
- Wang B, Zhang W, Jankovic V et al (2018) Combination cancer immunotherapy targeting PD-1 and GITR can rescue CD8(+) T cell dysfunction and maintain memory phenotype. Sci Immunol 3, eaat7061 https://doi.org/10.1126/sciimmunol.aat7061
- Liu S, Zhang H, Li M et al (2013) Recruitment of Grb2 and SHIP1 by the ITT-like motif of TIGIT suppresses granule polarization and cytotoxicity of NK cells. Cell Death Differ 20, 456-464 https://doi.org/10.1038/cdd.2012.141
- Shibuya K, Lanier LL, Phillips JH (1999) Physical and functional association of LFA-1 with DNAM-1 adhesion molecule. Immunity 11, 615-623 https://doi.org/10.1016/S1074-7613(00)80136-3
- Enqvist M, Ask EH, Forslund E et al (2015) Coordinated expression of DNAM-1 and LFA-1 in educated NK cells. J Immunol 194, 4518-4527 https://doi.org/10.4049/jimmunol.1401972
- Shibuya A, Campbell D, Hannum C et al (1996) DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity 4, 573-581 https://doi.org/10.1016/S1074-7613(00)70060-4
- Iguchi-Manaka A, Kai H, Yamashita Y et al (2008) Accelerated tumor growth in mice deficient in DNAM-1 receptor. J Exp Med 205, 2959-2964 https://doi.org/10.1084/jem.20081611
- Sanchez-Correa B, Gayoso I, Bergua JM et al (2012) Decreased expression of DNAM-1 on NK cells from acute myeloid leukemia patients. Immunol Cell Biol 90, 109-115 https://doi.org/10.1038/icb.2011.15
- Minnie SA, Kuns RD, Gartlan KH et al (2018) Myeloma escape after stem cell transplantation is a consequence of T-cell exhaustion and is prevented by TIGIT blockade. Blood 132, 1675-1688
- Jin Z, Lan T, Zhao Y et al (2020) Higher TIGIT(+)CD226(-) gammadelta T cells in patients with acute myeloid leukemia. Immunol Invest 1-11 [Online ahead of print]
- Gilfillan S, Chan CJ, Cella M et al (2008) DNAM-1 promotes activation of cytotoxic lymphocytes by nonprofessional antigen-presenting cells and tumors. J Exp Med 205, 2965-2973 https://doi.org/10.1084/jem.20081752
- Chan CJ, Martinet L, Gilfillan S et al (2014) The receptors CD96 and CD226 oppose each other in the regulation of natural killer cell functions. Nat Immunol 15, 431-438 https://doi.org/10.1038/ni.2850
- Lakshmikanth T, Burke S, Ali TH et al (2009) NCRs and DNAM-1 mediate NK cell recognition and lysis of human and mouse melanoma cell lines in vitro and in vivo. J Clin Invest 119, 1251-1263 https://doi.org/10.1172/JCI36022
- Zhang Z, Wu N, Lu Y, Davidson D, Colonna M, Veillette A (2015) DNAM-1 controls NK cell activation via an ITT-like motif. J Exp Med 212, 2165-2182 https://doi.org/10.1084/jem.20150792
- Braun M, Aguilera AR, Sundarrajan A et al (2020) CD155 on tumor cells drives resistance to immunotherapy by inducing the degradation of the activating receptor CD226 in CD8(+) T cells. Immunity 53, 805-823 https://doi.org/10.1016/j.immuni.2020.09.010
- Georgiev H, Ravens I, Papadogianni G, Bernhardt G (2018) Coming of age: CD96 emerges as modulator of immune responses. Front Immunol 9, 1072 https://doi.org/10.3389/fimmu.2018.01072
- Lepletier A, Lutzky VP, Mittal D et al (2019) The immune checkpoint CD96 defines a distinct lymphocyte phenotype and is highly expressed on tumor-infiltrating T cells. Immunol Cell Biol 97, 152-164 https://doi.org/10.1111/imcb.12205
- Mittal D, Lepletier A, Madore J et al (2019) CD96 is an immune checkpoint that regulates CD8(+) T-cell antitumor function. Cancer Immunol Res 7, 559-571 https://doi.org/10.1158/2326-6066.CIR-18-0637
- Sun H, Huang Q, Huang M et al (2019) Human CD96 correlates to natural killer cell exhaustion and predicts the prognosis of human hepatocellular carcinoma. Hepatology 70, 168-183 https://doi.org/10.1002/hep.30347
- Peng YP, Xi CH, Zhu Y et al (2016) Altered expression of CD226 and CD96 on natural killer cells in patients with pancreatic cancer. Oncotarget 7, 66586-66594 https://doi.org/10.18632/oncotarget.11953
- Blake SJ, Stannard K, Liu J et al (2016) Suppression of metastases using a new lymphocyte checkpoint target for cancer immunotherapy. Cancer Discov 6, 446-459 https://doi.org/10.1158/2159-8290.CD-15-0944
- Chiang EY, de Almeida PE, de Almeida Nagata DE et al (2020) CD96 functions as a co-stimulatory receptor to enhance CD8(+) T cell activation and effector responses. Eur J Immunol 50, 891-902 https://doi.org/10.1002/eji.201948405
- Meyer D, Seth S, Albrecht J et al (2009) CD96 interaction with CD155 via its first Ig-like domain is modulated by alternative splicing or mutations in distal Ig-like domains. J Biol Chem 284, 2235-2244 https://doi.org/10.1074/jbc.M807698200
- Chambers CA (2001) The expanding world of co-stimulation: the two-signal model revisited. Trends Immunol 22, 217-223 https://doi.org/10.1016/S1471-4906(01)01868-3
- Roman Aguilera A, Lutzky VP, Mittal D et al (2018) CD96 targeted antibodies need not block CD96-CD155 interactions to promote NK cell anti-metastatic activity. Oncoimmunology 7, e1424677 https://doi.org/10.1080/2162402X.2018.1424677
- Murter B, Pan X, Ophir E et al (2019) Mouse PVRIG has CD8(+) T cell-specific coinhibitory functions and dampens antitumor immunity. Cancer Immunol Res 7, 244-256 https://doi.org/10.1158/2326-6066.cir-18-0460
- Xu F, Sunderland A, Zhou Y, Schulick RD, Edil BH, Zhu Y (2017) Blockade of CD112R and TIGIT signaling sensitizes human natural killer cell functions. Cancer Immunol Immunother 66, 1367-1375 https://doi.org/10.1007/s00262-017-2031-x