Costimulatory and Coinhibitory Receptor Pathways in Infectious Disease

Immunity

Volumn 44, Issue 5, 2016, Pages 1052-1068

  Attanasio, John ^a   Wherry, E John ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD137 LIGAND; CYTOCHROME P450 2B4; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; OX40 LIGAND; PROGRAMMED DEATH 1 RECEPTOR;

BACTERIAL INFECTION; EXHAUSTION; GENE EXPRESSION; HUMAN; IMMUNE RESPONSE; INFECTION; NEOPLASM; NONHUMAN; PARASITOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BLOCKING; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; VACCINATION; VIRUS INFECTION; ACUTE DISEASE; ANIMAL; CHRONIC DISEASE; IMMUNOLOGY; IMMUNOMODULATION; LYMPHOCYTE ACTIVATION; METABOLISM; T LYMPHOCYTE;

ACUTE DISEASE; ANIMALS; CHRONIC DISEASE; CTLA-4 ANTIGEN; HUMANS; IMMUNOMODULATION; INFECTION; LYMPHOCYTE ACTIVATION; PROGRAMMED CELL DEATH 1 RECEPTOR; RECEPTOR CROSS-TALK; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84966762527     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.04.022     Document Type: Review

References (203)

1. Allie S.R., Zhang W., Fuse S., Usherwood E.J. Programmed death 1 regulates development of central memory CD8 T cells after acute viral infection. J. Immunol. 2011, 186:6280-6286.
2. Anderson A., Joller N., Kuchroo V. Lag-3, Tim-3, and TIGIT co-inhibitory receptors with specialized functions in immune regulation. Immunity 2016, 44:989-1004. this issue.
3. Anderson A.C., Lord G.M., Dardalhon V., Lee D.H., Sabatos-Peyton C.A., Glimcher L.H., Kuchroo V.K. T-bet, a Th1 transcription factor regulates the expression of Tim-3. Eur. J. Immunol. 2010, 40:859-866.
4. Andreasen S.O., Christensen J.E., Marker O., Thomsen A.R. Role of CD40 ligand and CD28 in induction and maintenance of antiviral CD8+ effector T cell responses. J. Immunol. 2000, 164:3689-3697.
5. Angelosanto J.M., Blackburn S.D., Crawford A., Wherry E.J. Progressive loss of memory T cell potential and commitment to exhaustion during chronic viral infection. J. Virol. 2012, 86:8161-8170.
6. Aubert R.D., Kamphorst A.O., Sarkar S., Vezys V., Ha S.J., Barber D.L., Ye L., Sharpe A.H., Freeman G.J., Ahmed R. Antigen-specific CD4 T-cell help rescues exhausted CD8 T cells during chronic viral infection. Proc. Natl. Acad. Sci. USA 2011, 108:21182-21187.
7. Autran B., Carcelain G., Combadiere B., Debre P. Therapeutic vaccines for chronic infections. Science 2004, 305:205-208.
8. Bachmann M.F., Waterhouse P., Speiser D.E., McKall-Faienza K., Mak T.W., Ohashi P.S. Normal responsiveness of CTLA-4-deficient anti-viral cytotoxic T cells. J. Immunol. 1998, 160:95-100.
9. Banerjee A., Gordon S.M., Intlekofer A.M., Paley M.A., Mooney E.C., Lindsten T., Wherry E.J., Reiner S.L. Cutting edge: The transcription factor eomesodermin enables CD8+ T cells to compete for the memory cell niche. J. Immunol. 2010, 185:4988-4992.
10. Barber D.L., Wherry E.J., Masopust D., Zhu B., Allison J.P., Sharpe A.H., Freeman G.J., Ahmed R. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 2006, 439:682-687.
11. Barber D.L., Mayer-Barber K.D., Feng C.G., Sharpe A.H., Sher A. CD4 T cells promote rather than control tuberculosis in the absence of PD-1-mediated inhibition. J. Immunol. 2011, 186:1598-1607.
12. Barnes E., Folgori A., Capone S., Swadling L., Aston S., Kurioka A., Meyer J., Huddart R., Smith K., Townsend R., et al. Novel adenovirus-based vaccines induce broad and sustained T cell responses to HCV in man. Sci. Transl. Med. 2012, 4:115ra1.
13. Barrett D.M., Singh N., Porter D.L., Grupp S.A., June C.H. Chimeric antigen receptor therapy for cancer. Annu. Rev. Med. 2014, 65:333-347.
14. Bertram E.M., Tafuri A., Shahinian A., Chan V.S., Hunziker L., Recher M., Ohashi P.S., Mak T.W., Watts T.H. Role of ICOS versus CD28 in antiviral immunity. Eur. J. Immunol. 2002, 32:3376-3385.
15. Bhadra R., Gigley J.P., Weiss L.M., Khan I.A. Control of Toxoplasma reactivation by rescue of dysfunctional CD8+ T-cell response via PD-1-PDL-1 blockade. Proc. Natl. Acad. Sci. USA 2011, 108:9196-9201.
16. Blackburn S.D., Shin H., Freeman G.J., Wherry E.J. Selective expansion of a subset of exhausted CD8 T cells by alphaPD-L1 blockade. Proc. Natl. Acad. Sci. USA 2008, 105:15016-15021.
17. 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. 2009, 10:29-37.
18. Bloch-Queyrat C., Fondanèche M.C., Chen R., Yin L., Relouzat F., Veillette A., Fischer A., Latour S. Regulation of natural cytotoxicity by the adaptor SAP and the Src-related kinase Fyn. J. Exp. Med. 2005, 202:181-192.
19. Boettler T., Cheng Y., Ehrhardt K., von Herrath M. TGF-β blockade does not improve control of an established persistent viral infection. Viral Immunol. 2012, 25:232-238.
20. Boettler T., Moeckel F., Cheng Y., Heeg M., Salek-Ardakani S., Crotty S., Croft M., von Herrath M.G. OX40 facilitates control of a persistent virus infection. PLoS Pathog. 2012, 8:e1002913.
21. Brahmamdam P., Inoue S., Unsinger J., Chang K.C., McDunn J.E., Hotchkiss R.S. Delayed administration of anti-PD-1 antibody reverses immune dysfunction and improves survival during sepsis. J. Leukoc. Biol. 2010, 88:233-240.
22. Bretscher P., Cohn M. A theory of self-nonself discrimination. Science 1970, 169:1042-1049.
23. Brooks D.G., Ha S.J., Elsaesser H., Sharpe A.H., Freeman G.J., Oldstone M.B. IL-10 and PD-L1 operate through distinct pathways to suppress T-cell activity during persistent viral infection. Proc. Natl. Acad. Sci. USA 2008, 105:20428-20433.
24. Buggert M., Tauriainen J., Yamamoto T., Frederiksen J., Ivarsson M.A., Michaëlsson J., Lund O., Hejdeman B., Jansson M., Sönnerborg A., et al. T-bet and Eomes are differentially linked to the exhausted phenotype of CD8+ T cells in HIV infection. PLoS Pathog. 2014, 10:e1004251.
25. Burchill M.A., Golden-Mason L., Wind-Rotolo M., Rosen H.R. Memory re-differentiation and reduced lymphocyte activation in chronic HCV-infected patients receiving direct-acting antivirals. J. Viral Hepat. 2015, 22:983-991.
26. Butler N.S., Moebius J., Pewe L.L., Traore B., Doumbo O.K., Tygrett L.T., Waldschmidt T.J., Crompton P.D., Harty J.T. Therapeutic blockade of PD-L1 and LAG-3 rapidly clears established blood-stage Plasmodium infection. Nat. Immunol. 2012, 13:188-195.
27. Cai G., Anumanthan A., Brown J.A., Greenfield E.A., Zhu B., Freeman G.J. CD160 inhibits activation of human CD4(+) T cells through interaction with herpesvirus entry mediator. Nat Immunol. 2008, 9:176-185.
28. Callahan M.K., Postow M.A., Wolchok J.D. Targeting T Cell Co-receptors for Cancer Therapy. Immunity 2016, 44:1069-1078. this issue.
29. Cao E., Zang X., Ramagopal U.A., Mukhopadhaya A., Fedorov A., Fedorov E., Zencheck W.D., Lary J.W., Cole J.L., Deng H., et al. T cell immunoglobulin mucin-3 crystal structure reveals a galectin-9-independent ligand-binding surface. Immunity 2007, 26:311-321.
30. Carrington M., Alter G. Innate immune control of HIV. Cold Spring Harb. Perspect. Med. 2012, 2:a007070.
31. Cecchinato V., Tryniszewska E., Ma Z.M., Vaccari M., Boasso A., Tsai W.P., Petrovas C., Fuchs D., Heraud J.M., Venzon D., et al. Immune activation driven by CTLA-4 blockade augments viral replication at mucosal sites in simian immunodeficiency virus infection. J. Immunol. 2008, 180:5439-5447.
32. Chemnitz J.M., Parry R.V., Nichols K.E., June C.H., Riley J.L. SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation. J. Immunol. 2004, 173:945-954.
33. Chew G.M., Fujita T., Webb G.M., Burwitz B.J., Wu H.L., Reed J.S., Hammond K.B., Clayton K.L., Ishii N., Abdel-Mohsen M., et al. TIGIT Marks Exhausted T Cells, Correlates with Disease Progression, and Serves as a Target for Immune Restoration in HIV and SIV Infection. PLoS Pathog. 2016, 12:e1005349.
34. Chlewicki L.K., Velikovsky C.A., Balakrishnan V., Mariuzza R.A., Kumar V. Molecular basis of the dual functions of 2B4 (CD244). J. Immunol. 2008, 180:8159-8167.
35. Clouthier D.L., Zhou A.C., Watts T.H. Anti-GITR agonist therapy intrinsically enhances CD8 T cell responses to chronic lymphocytic choriomeningitis virus (LCMV), thereby circumventing LCMV-induced downregulation of costimulatory GITR ligand on APC. J. Immunol. 2014, 193:5033-5043.
36. Clouthier D.L., Zhou A.C., Wortzman M.E., Luft O., Levy G.A., Watts T.H. GITR intrinsically sustains early type 1 and late follicular helper CD4 T cell accumulation to control a chronic viral infection. PLoS Pathog. 2015, 11:e1004517.
37. Collison L.W., Workman C.J., Kuo T.T., Boyd K., Wang Y., Vignali K.M., Cross R., Sehy D., Blumberg R.S., Vignali D.A. The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature 2007, 450:566-569.
38. Crawford A., Wherry E.J. The diversity of costimulatory and inhibitory receptor pathways and the regulation of antiviral T cell responses. Curr. Opin. Immunol. 2009, 21:179-186.
39. + T cell dysfunction during chronic infection. Immunity 2014, 40:289-302.
40. Cunningham A.J., Lafferty K.J. A simple conservative explanation of the H-2 restriction of interactions between lymphocytes. Scand. J. Immunol. 1977, 6:1-6.
41. Dahan R., Sega E., Engelhardt J., Selby M., Korman A.J., Ravetch J.V. FcγRs Modulate the Anti-tumor Activity of Antibodies Targeting the PD-1/PD-L1 Axis. Cancer Cell 2015, 28:285-295.
42. Day C.L., Kaufmann D.E., Kiepiela P., Brown J.A., Moodley E.S., Reddy S., Mackey E.W., Miller J.D., Leslie A.J., DePierres C., et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 2006, 443:350-354.
43. Doering T.A., Crawford A., Angelosanto J.M., Paley M.A., Ziegler C.G., Wherry E.J. Network analysis reveals centrally connected genes and pathways involved in CD8+ T cell exhaustion versus memory. Immunity 2012, 37:1130-1144.
44. Duraiswamy J., Ibegbu C.C., Masopust D., Miller J.D., Araki K., Doho G.H., Tata P., Gupta S., Zilliox M.J., Nakaya H.I., et al. Phenotype, function, and gene expression profiles of programmed death-1(hi) CD8 T cells in healthy human adults. J. Immunol. 2011, 186:4200-4212.
45. Dyavar Shetty R., Velu V., Titanji K., Bosinger S.E., Freeman G.J., Silvestri G., Amara R.R. PD-1 blockade during chronic SIV infection reduces hyperimmune activation and microbial translocation in rhesus macaques. J. Clin. Invest. 2012, 122:1712-1716.
46. Eissmann P., Beauchamp L., Wooters J., Tilton J.C., Long E.O., Watzl C. Molecular basis for positive and negative signaling by the natural killer cell receptor 2B4 (CD244). Blood 2005, 105:4722-4729.
47. Erickson J.J., Gilchuk P., Hastings A.K., Tollefson S.J., Johnson M., Downing M.B., Boyd K.L., Johnson J.E., Kim A.S., Joyce S., Williams J.V. Viral acute lower respiratory infections impair CD8+ T cells through PD-1. J. Clin. Invest. 2012, 122:2967-2982.
48. Esch K.J., Juelsgaard R., Martinez P.A., Jones D.E., Petersen C.A. Programmed death 1-mediated T cell exhaustion during visceral leishmaniasis impairs phagocyte function. J. Immunol. 2013, 191:5542-5550.
49. Esensten J.H., Helou Y.A., Chopra G., Weiss A., Bluestone J.A. CD28 costimulation: from mechanism to therapy. Immunity 2016, 44:973-988. this issue.
50. Flores M., Chew C., Tyan K., Huang W.Q., Salem A., Clynes R. FcγRIIB prevents inflammatory type I IFN production from plasmacytoid dendritic cells during a viral memory response. J. Immunol. 2015, 194:4240-4250.
51. Frebel H., Nindl V., Schuepbach R.A., Braunschweiler T., Richter K., Vogel J., Wagner C.A., Loffing-Cueni D., Kurrer M., Ludewig B., Oxenius A. Programmed death 1 protects from fatal circulatory failure during systemic virus infection of mice. J. Exp. Med. 2012, 209:2485-2499.
52. Fuller M.J., Zajac A.J. Ablation of CD8 and CD4 T cell responses by high viral loads. J. Immunol. 2003, 170:477-486.
53. Fuller M.J., Callendret B., Zhu B., Freeman G.J., Hasselschwert D.L., Satterfield W., Sharpe A.H., Dustin L.B., Rice C.M., Grakoui A., et al. Immunotherapy of chronic hepatitis C virus infection with antibodies against programmed cell death-1 (PD-1). Proc. Natl. Acad. Sci. USA 2013, 110:15001-15006.
54. Garba M.L., Pilcher C.D., Bingham A.L., Eron J., Frelinger J.A. HIV antigens can induce TGF-beta(1)-producing immunoregulatory CD8+ T cells. J. Immunol. 2002, 168:2247-2254.
55. Gardiner D., Lalezari J., Lawitz E., DiMicco M., Ghalib R., Reddy K.R., Chang K.M., Sulkowski M., Marro S.O., Anderson J., et al. A randomized, double-blind, placebo-controlled assessment of BMS-936558, a fully human monoclonal antibody to programmed death-1 (PD-1), in patients with chronic hepatitis C virus infection. PLoS ONE 2013, 8:e63818.
56. Garidou L., Heydari S., Gossa S., McGavern D.B. Therapeutic blockade of transforming growth factor beta fails to promote clearance of a persistent viral infection. J. Virol. 2012, 86:7060-7071.
57. Gerner M.Y., Heltemes-Harris L.M., Fife B.T., Mescher M.F. Cutting edge: IL-12 and type I IFN differentially program CD8 T cells for programmed death 1 re-expression levels and tumor control. J. Immunol. 2013, 191:1011-1015.
58. Greenwald R.J., Freeman G.J., Sharpe A.H. The B7 family revisited. Annu. Rev. Immunol. 2005, 23:515-548.
59. 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. 2007, 117:3383-3392.
60. Guignant C., Lepape A., Huang X., Kherouf H., Denis L., Poitevin F., Malcus C., Chéron A., Allaouchiche B., Gueyffier F., et al. Programmed death-1 levels correlate with increased mortality, nosocomial infection and immune dysfunctions in septic shock patients. Crit. Care 2011, 15:R99.
61. Ha S.J., Mueller S.N., Wherry E.J., Barber D.L., Aubert R.D., Sharpe A.H., Freeman G.J., Ahmed R. Enhancing therapeutic vaccination by blocking PD-1-mediated inhibitory signals during chronic infection. J. Exp. Med. 2008, 205:543-555.
62. Hafalla J.C., Claser C., Couper K.N., Grau G.E., Renia L., de Souza J.B., Riley E.M. The CTLA-4 and PD-1/PD-L1 inhibitory pathways independently regulate host resistance to Plasmodium-induced acute immune pathology. PLoS Pathog. 2012, 8:e1002504.
63. Hafler D.A., Kuchroo V. TIMs: central regulators of immune responses. J. Exp. Med. 2008, 205:2699-2701.
64. Hess Michelini R., Doedens A.L., Goldrath A.W., Hedrick S.M. Differentiation of CD8 memory T cells depends on Foxo1. J. Exp. Med. 2013, 210:1189-1200.
65. Hirahara K., Ghoreschi K., Yang X.P., Takahashi H., Laurence A., Vahedi G., Sciumè G., Hall A.O., Dupont C.D., Francisco L.M., et al. Interleukin-27 priming of T cells controls IL-17 production in trans via induction of the ligand PD-L1. Immunity 2012, 36:1017-1030.
66. Homann D., Dummer W., Wolfe T., Rodrigo E., Theofilopoulos A.N., Oldstone M.B., von Herrath M.G. Lack of intrinsic CTLA-4 expression has minimal effect on regulation of antiviral T-cell immunity. J. Virol. 2006, 80:270-280.
67. Hryniewicz A., Boasso A., Edghill-Smith Y., Vaccari M., Fuchs D., Venzon D., Nacsa J., Betts M.R., Tsai W.P., Heraud J.M., et al. CTLA-4 blockade decreases TGF-beta, IDO, and viral RNA expression in tissues of SIVmac251-infected macaques. Blood 2006, 108:3834-3842.
68. Huang C.T., Workman C.J., Flies D., Pan X., Marson A.L., Zhou G., Hipkiss E.L., Ravi S., Kowalski J., Levitsky H.I., et al. Role of LAG-3 in regulatory T cells. Immunity 2004, 21:503-513.
69. Huang X., Venet F., Wang Y.L., Lepape A., Yuan Z., Chen Y., Swan R., Kherouf H., Monneret G., Chung C.S., Ayala A. PD-1 expression by macrophages plays a pathologic role in altering microbial clearance and the innate inflammatory response to sepsis. Proc. Natl. Acad. Sci. USA 2009, 106:6303-6308.
70. 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 2015, 517:386-390.
71. Huard B., Tournier M., Hercend T., Triebel F., Faure F. Lymphocyte-activation gene 3/major histocompatibility complex class II interaction modulates the antigenic response of CD4+ T lymphocytes. Eur. J. Immunol. 1994, 24:3216-3221.
72. Huard B., Mastrangeli R., Prigent P., Bruniquel D., Donini S., El-Tayar N., Maigret B., Dréano M., Triebel F. Characterization of the major histocompatibility complex class II binding site on LAG-3 protein. Proc. Natl. Acad. Sci. USA 1997, 94:5744-5749.
73. Intlekofer A.M., Banerjee A., Takemoto N., Gordon S.M., Dejong C.S., Shin H., Hunter C.A., Wherry E.J., Lindsten T., Reiner S.L. Anomalous type 17 response to viral infection by CD8+ T cells lacking T-bet and eomesodermin. Science 2008, 321:408-411.
74. Isogawa M., Furuichi Y., Chisari F.V. Oscillating CD8(+) T cell effector functions after antigen recognition in the liver. Immunity 2005, 23:53-63.
75. Iwashiro M., Messer R.J., Peterson K.E., Stromnes I.M., Sugie T., Hasenkrug K.J. Immunosuppression by CD4+ regulatory T cells induced by chronic retroviral infection. Proc. Natl. Acad. Sci. USA 2001, 98:9226-9230.
76. 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. USA 2010, 107:14733-14738.
77. Johnston R.J., Comps-Agrar L., Hackney J., Yu X., Huseni M., Yang Y., Park S., Javinal V., Chiu H., Irving B., et al. The immunoreceptor TIGIT regulates antitumor and antiviral CD8(+) T cell effector function. Cancer Cell 2014, 26:923-937.
78. Joller N., Hafler J.P., Brynedal B., Kassam N., Spoerl S., Levin S.D., Sharpe A.H., Kuchroo V.K. Cutting edge: TIGIT has T cell-intrinsic inhibitory functions. J. Immunol. 2011, 186:1338-1342.
79. 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. 2008, 205:2763-2779.
80. Joshi N.S., Cui W., Chandele A., Lee H.K., Urso D.R., Hagman J., Gapin L., Kaech S.M. Inflammation directs a gradient of T-bet expression that specifies memory precursor and short-lived effector CD8 T cell fates. Immunity 2007, 27:281-295.
81. Kallies A., Xin A., Belz G.T., Nutt S.L. Blimp-1 transcription factor is required for the differentiation of effector CD8(+) T cells and memory responses. Immunity 2009, 31:283-295.
82. Kao C., Oestreich K.J., Paley M.A., Crawford A., Angelosanto J.M., Ali M.A., Intlekofer A.M., Boss J.M., Reiner S.L., Weinmann A.S., Wherry E.J. Transcription factor T-bet represses expression of the inhibitory receptor PD-1 and sustains virus-specific CD8+ T cell responses during chronic infection. Nat. Immunol. 2011, 12:663-671.
83. Kassu A., D'Souza M., O'Connor B.P., Kelly-McKnight E., Akkina R., Fontenot A.P., Palmer B.E. Decreased 4-1BB expression on HIV-specific CD4+ T cells is associated with sustained viral replication and reduced IL-2 production. Clin. Immunol. 2009, 132:234-245.
84. Kaufmann D.E., Kavanagh D.G., Pereyra F., Zaunders J.J., Mackey E.W., Miura T., Palmer S., Brockman M., Rathod A., Piechocka-Trocha A., et al. Upregulation of CTLA-4 by HIV-specific CD4+ T cells correlates with disease progression and defines a reversible immune dysfunction. Nat. Immunol. 2007, 8:1246-1254.
85. Keir M.E., Butte M.J., Freeman G.J., Sharpe A.H. PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 2008, 26:677-704.
86. Kennedy P.T., Sandalova E., Jo J., Gill U., Ushiro-Lumb I., Tan A.T., Naik S., Foster G.R., Bertoletti A. Preserved T-cell function in children and young adults with immune-tolerant chronic hepatitis B. Gastroenterology 2012, 143:637-645.
87. Kim M.V., Ouyang W., Liao W., Zhang M.Q., Li M.O. The transcription factor Foxo1 controls central-memory CD8+ T cell responses to infection. Immunity 2013, 39:286-297.
88. Kinter A.L., Godbout E.J., McNally J.P., Sereti I., Roby G.A., O'Shea M.A., Fauci A.S. The common gamma-chain cytokines IL-2, IL-7, IL-15, and IL-21 induce the expression of programmed death-1 and its ligands. J. Immunol. 2008, 181:6738-6746.
89. Kopf M., Ruedl C., Schmitz N., Gallimore A., Lefrang K., Ecabert B., Odermatt B., Bachmann M.F. OX40-deficient mice are defective in Th cell proliferation but are competent in generating B cell and CTL Responses after virus infection. Immunity 1999, 11:699-708.
90. Kopf M., Coyle A.J., Schmitz N., Barner M., Oxenius A., Gallimore A., Gutierrez-Ramos J.C., Bachmann M.F. Inducible costimulator protein (ICOS) controls T helper cell subset polarization after virus and parasite infection. J. Exp. Med. 2000, 192:53-61.
91. Kroy D.C., Ciuffreda D., Cooperrider J.H., Tomlinson M., Hauck G.D., Aneja J., Berger C., Wolski D., Carrington M., Wherry E.J., et al. Liver environment and HCV replication affect human T-cell phenotype and expression of inhibitory receptors. Gastroenterology 2014, 146:550-561.
92. Krummel M.F., Allison J.P. CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J. Exp. Med. 1995, 182:459-465.
93. Kuchroo V.K., Dardalhon V., Xiao S., Anderson A.C. New roles for TIM family members in immune regulation. Nat. Rev. Immunol. 2008, 8:577-580.
94. Kurachi M., Barnitz R.A., Yosef N., Odorizzi P.M., DiIorio M.A., Lemieux M.E., Yates K., Godec J., Klatt M.G., Regev A., et al. The transcription factor BATF operates as an essential differentiation checkpoint in early effector CD8+ T cells. Nat. Immunol. 2014, 15:373-383.
95. Lafferty K.J., Cunningham A.J. A new analysis of allogeneic interactions. Aust. J. Exp. Biol. Med. Sci. 1975, 53:27-42.
96. Lafon M., Mégret F., Meuth S.G., Simon O., Velandia Romero M.L., Lafage M., Chen L., Alexopoulou L., Flavell R.A., Prehaud C., Wiendl H. Detrimental contribution of the immuno-inhibitor B7-H1 to rabies virus encephalitis. J. Immunol. 2008, 180:7506-7515.
97. Langhorne J., Ndungu F.M., Sponaas A.M., Marsh K. Immunity to malaria: more questions than answers. Nat. Immunol. 2008, 9:725-732.
98. Lanier L.L. NK cell receptors. Annu. Rev. Immunol. 1998, 16:359-393.
99. Lasaro M.O., Tatsis N., Hensley S.E., Whitbeck J.C., Lin S.W., Rux J.J., Wherry E.J., Cohen G.H., Eisenberg R.J., Ertl H.C. Targeting of antigen to the herpesvirus entry mediator augments primary adaptive immune responses. Nat. Med. 2008, 14:205-212.
100. Lázár-Molnár E., Gácser A., Freeman G.J., Almo S.C., Nathenson S.G., Nosanchuk J.D. The PD-1/PD-L costimulatory pathway critically affects host resistance to the pathogenic fungus Histoplasma capsulatum. Proc. Natl. Acad. Sci. USA 2008, 105:2658-2663.
101. Lázár-Molnár E., Chen B., Sweeney K.A., Wang E.J., Liu W., Lin J., Porcelli S.A., Almo S.C., Nathenson S.G., Jacobs W.R. Programmed death-1 (PD-1)-deficient mice are extraordinarily sensitive to tuberculosis. Proc. Natl. Acad. Sci. USA 2010, 107:13402-13407.
102. Lee K.M., McNerney M.E., Stepp S.E., Mathew P.A., Schatzle J.D., Bennett M., Kumar V. 2B4 acts as a non-major histocompatibility complex binding inhibitory receptor on mouse natural killer cells. J. Exp. Med. 2004, 199:1245-1254.
103. Lenschow D.J., Walunas T.L., Bluestone J.A. CD28/B7 system of T cell costimulation. Annu. Rev. Immunol. 1996, 14:233-258.
104. Liang S.C., Latchman Y.E., Buhlmann J.E., Tomczak M.F., Horwitz B.H., Freeman G.J., Sharpe A.H. Regulation of PD-1, PD-L1, and PD-L2 expression during normal and autoimmune responses. Eur. J. Immunol. 2003, 33:2706-2716.
105. Linsley P.S., Ledbetter J.A. The role of the CD28 receptor during T cell responses to antigen. Annu. Rev. Immunol. 1993, 11:191-212.
106. Lu P., Youngblood B.A., Austin J.W., Mohammed A.U., Butler R., Ahmed R., Boss J.M. Blimp-1 represses CD8 T cell expression of PD-1 using a feed-forward transcriptional circuit during acute viral infection. J. Exp. Med. 2014, 211:515-527.
107. + T cells. Immunity 2015, 42:265-278.
108. Matter M., Odermatt B., Yagita H., Nuoffer J.M., Ochsenbein A.F. Elimination of chronic viral infection by blocking CD27 signaling. J. Exp. Med. 2006, 203:2145-2155.
109. McMahon C.W., Zajac A.J., Jamieson A.M., Corral L., Hammer G.E., Ahmed R., Raulet D.H. Viral and bacterial infections induce expression of multiple NK cell receptors in responding CD8(+) T cells. J. Immunol. 2002, 169:1444-1452.
110. McNally B., Ye F., Willette M., Flaño E. Local blockade of epithelial PDL-1 in the airways enhances T cell function and viral clearance during influenza virus infection. J. Virol. 2013, 87:12916-12924.
111. McNerney M.E., Lee K.M., Kumar V. 2B4 (CD244) is a non-MHC binding receptor with multiple functions on natural killer cells and CD8+ T cells. Mol. Immunol. 2005, 42:489-494.
112. Miura K. Progress and prospects for blood-stage malaria vaccines. Expert Rev. Vaccines 2016, 1-17.
113. Moir S., Ho J., Malaspina A., Wang W., DiPoto A.C., O'Shea M.A., Roby G., Kottilil S., Arthos J., Proschan M.A., et al. Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J. Exp. Med. 2008, 205:1797-1805.
114. Mooney J.M., Klem J., Wülfing C., Mijares L.A., Schwartzberg P.L., Bennett M., Schatzle J.D. The murine NK receptor 2B4 (CD244) exhibits inhibitory function independent of signaling lymphocytic activation molecule-associated protein expression. J. Immunol. 2004, 173:3953-3961.
115. Moskophidis D., Lechner F., Pircher H., Zinkernagel R.M. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature 1993, 362:758-761.
116. Muhammad A., Schiller H.B., Forster F., Eckerstorfer P., Geyeregger R., Leksa V., Zlabinger G.J., Sibilia M., Sonnleitner A., Paster W., Stockinger H. Sequential cooperation of CD2 and CD48 in the buildup of the early TCR signalosome. J. Immunol. 2009, 182:7672-7680.
117. Murphy T.L., Tussiwand R., Murphy K.M. Specificity through cooperation: BATF-IRF interactions control immune-regulatory networks. Nat. Rev. Immunol. 2013, 13:499-509.
118. Nakamoto N., Cho H., Shaked A., Olthoff K., Valiga M.E., Kaminski M., Gostick E., Price D.A., Freeman G.J., Wherry E.J., Chang K.M. Synergistic reversal of intrahepatic HCV-specific CD8 T cell exhaustion by combined PD-1/CTLA-4 blockade. PLoS Pathog. 2009, 5:e1000313.
119. Odorizzi P.M., Wherry E.J. Inhibitory receptors on lymphocytes: insights from infections. J. Immunol. 2012, 188:2957-2965.
120. Oestreich K.J., Yoon H., Ahmed R., Boss J.M. NFATc1 regulates PD-1 expression upon T cell activation. J. Immunol. 2008, 181:4832-4839.
121. 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. 2011, 208:395-407.
122. Orr M.T., Lanier L.L. Inhibitory Ly49 receptors on mouse natural killer cells. Curr. Top. Microbiol. Immunol. 2011, 350:67-87.
123. Paley M.A., Kroy D.C., Odorizzi P.M., Johnnidis J.B., Dolfi D.V., Barnett B.E., Bikoff E.K., Robertson E.J., Lauer G.M., Reiner S.L., Wherry E.J. Progenitor and terminal subsets of CD8+ T cells cooperate to contain chronic viral infection. Science 2012, 338:1220-1225.
124. Paley M.A., Gordon S.M., Bikoff E.K., Robertson E.J., Wherry E.J., Reiner S.L. Technical Advance: Fluorescent reporter reveals insights into eomesodermin biology in cytotoxic lymphocytes. J. Leukoc. Biol. 2013, 93:307-315.
125. Parry R.V., Chemnitz J.M., Frauwirth K.A., Lanfranco A.R., Braunstein I., Kobayashi S.V., Linsley P.S., Thompson C.B., Riley J.L. CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol. Cell. Biol. 2005, 25:9543-9553.
126. Pascutti M.F., Geerman S., Slot E., van Gisbergen K.P., Boon L., Arens R., van Lier R.A., Wolkers M.C., Nolte M.A. Enhanced CD8 T cell responses through GITR-mediated costimulation resolve chronic viral infection. PLoS Pathog. 2015, 11:e1004675.
127. Patsoukis N., Brown J., Petkova V., Liu F., Li L., Boussiotis V.A. Selective effects of PD-1 on Akt and Ras pathways regulate molecular components of the cell cycle and inhibit T cell proliferation. Sci. Signal. 2012, 5:ra46.
128. Pearce E.L., Mullen A.C., Martins G.A., Krawczyk C.M., Hutchins A.S., Zediak V.P., Banica M., DiCioccio C.B., Gross D.A., Mao C.A., et al. Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science 2003, 302:1041-1043.
129. Penaloza-MacMaster P., Kamphorst A.O., Wieland A., Araki K., Iyer S.S., West E.E., O'Mara L., Yang S., Konieczny B.T., Sharpe A.H., et al. Interplay between regulatory T cells and PD-1 in modulating T cell exhaustion and viral control during chronic LCMV infection. J. Exp. Med. 2014, 211:1905-1918.
130. Petrovas C., Casazza J.P., Brenchley J.M., Price D.A., Gostick E., Adams W.C., Precopio M.L., Schacker T., Roederer M., Douek D.C., Koup R.A. PD-1 is a regulator of virus-specific CD8+ T cell survival in HIV infection. J. Exp. Med. 2006, 203:2281-2292.
131. Porichis F., Hart M.G., Zupkosky J., Barblu L., Kwon D.S., McMullen A., Brennan T., Ahmed R., Freeman G.J., Kavanagh D.G., Kaufmann D.E. Differential impact of PD-1 and/or interleukin-10 blockade on HIV-1-specific CD4 T cell and antigen-presenting cell functions. J. Virol. 2014, 88:2508-2518.
132. Quigley M., Pereyra F., Nilsson B., Porichis F., Fonseca C., Eichbaum Q., Julg B., Jesneck J.L., Brosnahan K., Imam S., et al. Transcriptional analysis of HIV-specific CD8+ T cells shows that PD-1 inhibits T cell function by upregulating BATF. Nat. Med. 2010, 16:1147-1151.
133. 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. 2012, 18:1394-1400.
134. Raué H.P., Slifka M.K. Pivotal advance: CTLA-4+ T cells exhibit normal antiviral functions during acute viral infection. J. Leukoc. Biol. 2007, 81:1165-1175.
135. Ravetch J.V., Lanier L.L. Immune inhibitory receptors. Science 2000, 290:84-89.
136. Raziorrouh B., Schraut W., Gerlach T., Nowack D., Grüner N.H., Ulsenheimer A., Zachoval R., Wächtler M., Spannagl M., Haas J., et al. The immunoregulatory role of CD244 in chronic hepatitis B infection and its inhibitory potential on virus-specific CD8+ T-cell function. Hepatology 2010, 52:1934-1947.
137. Richter K., Agnellini P., Oxenius A. On the role of the inhibitory receptor LAG-3 in acute and chronic LCMV infection. Int. Immunol. 2010, 22:13-23.
138. Riley J.L. PD-1 signaling in primary T cells. Immunol. Rev. 2009, 229:114-125.
139. Rowe J.H., Johanns T.M., Ertelt J.M., Way S.S. PDL-1 blockade impedes T cell expansion and protective immunity primed by attenuated Listeria monocytogenes. J. Immunol. 2008, 180:7553-7557.
140. Rutishauser R.L., Martins G.A., Kalachikov S., Chandele A., Parish I.A., Meffre E., Jacob J., Calame K., Kaech S.M. Transcriptional repressor Blimp-1 promotes CD8(+) T cell terminal differentiation and represses the acquisition of central memory T cell properties. Immunity 2009, 31:296-308.
141. Schildberg F.A., Klein S.R., Freeman G.J., Sharpe A.H. Coinhibitory Pathways in the B7-CD28 Ligand-Receptor Family. Immunity 2016, 44:955-972. this issue.
142. Schurich A., Khanna P., Lopes A.R., Han K.J., Peppa D., Micco L., Nebbia G., Kennedy P.T., Geretti A.M., Dusheiko G., Maini M.K. Role of the coinhibitory receptor cytotoxic T lymphocyte antigen-4 on apoptosis-Prone CD8 T cells in persistent hepatitis B virus infection. Hepatology 2011, 53:1494-1503.
143. Scott P., Hunter C.A. Dendritic cells and immunity to leishmaniasis and toxoplasmosis. Curr. Opin. Immunol. 2002, 14:466-470.
144. Seo S.K., Jeong H.Y., Park S.G., Lee S.W., Choi I.W., Chen L., Choi I. Blockade of endogenous B7-H1 suppresses antibacterial protection after primary Listeria monocytogenes infection. Immunology 2008, 123:90-99.
145. Seung E., Dudek T.E., Allen T.M., Freeman G.J., Luster A.D., Tager A.M. PD-1 blockade in chronically HIV-1-infected humanized mice suppresses viral loads. PLoS ONE 2013, 8:e77780.
146. Sharpe A.H., Abbas A.K. T-cell costimulation--biology, therapeutic potential, and challenges. N. Engl. J. Med. 2006, 355:973-975.
147. Shin H., Blackburn S.D., Intlekofer A.M., Kao C., Angelosanto J.M., Reiner S.L., Wherry E.J. A Role for the Transcriptional Repressor Blimp-1 in CD8(+) T Cell Exhaustion during Chronic Viral Infection. Immunity 2009, 31:309-320.
148. Shuford W.W., Klussman K., Tritchler D.D., Loo D.T., Chalupny J., Siadak A.W., Brown T.J., Emswiler J., Raecho H., Larsen C.P., et al. 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. 1997, 186:47-55.
149. Snelgrove R.J., Goulding J., Didierlaurent A.M., Lyonga D., Vekaria S., Edwards L., Gwyer E., Sedgwick J.D., Barclay A.N., Hussell T. A critical function for CD200 in lung immune homeostasis and the severity of influenza infection. Nat. Immunol. 2008, 9:1074-1083.
150. Song A., Tang X., Harms K.M., Croft M. OX40 and Bcl-xL promote the persistence of CD8 T cells to recall tumor-associated antigen. J. Immunol. 2005, 175:3534-3541.
151. Song J., So T., Croft M. Activation of NF-kappaB1 by OX40 contributes to antigen-driven T cell expansion and survival. J. Immunol. 2008, 180:7240-7248.
152. Stanietsky N., Simic H., Arapovic J., Toporik A., Levy O., Novik A., Levine Z., Beiman M., Dassa L., Achdout H., et al. The interaction of TIGIT with PVR and PVRL2 inhibits human NK cell cytotoxicity. Proc. Natl. Acad. Sci. USA 2009, 106:17858-17863.
153. Staron M.M., Gray S.M., Marshall H.D., Parish I.A., Chen J.H., Perry C.J., Cui G., Li M.O., Kaech S.M. The transcription factor FoxO1 sustains expression of the inhibitory receptor PD-1 and survival of antiviral CD8(+) T cells during chronic infection. Immunity 2014, 41:802-814.
154. Stiles K.M., Whitbeck J.C., Lou H., Cohen G.H., Eisenberg R.J., Krummenacher C. Herpes simplex virus glycoprotein D interferes with binding of herpesvirus entry mediator to its ligands through downregulation and direct competition. J. Virol. 2010, 84:11646-11660.
155. Suresh M., Whitmire J.K., Harrington L.E., Larsen C.P., Pearson T.C., Altman J.D., Ahmed R. Role of CD28-B7 interactions in generation and maintenance of CD8 T cell memory. J. Immunol. 2001, 167:5565-5573.
156. Talay O., Shen C.H., Chen L., Chen J. B7-H1 (PD-L1) on T cells is required for T-cell-mediated conditioning of dendritic cell maturation. Proc. Natl. Acad. Sci. USA 2009, 106:2741-2746.
157. Tan J.T., Whitmire J.K., Ahmed R., Pearson T.C., Larsen C.P. 4-1BB ligand, a member of the TNF family, is important for the generation of antiviral CD8 T cell responses. J. Immunol. 1999, 163:4859-4868.
158. Teijaro J.R., Ng C., Lee A.M., Sullivan B.M., Sheehan K.C., Welch M., Schreiber R.D., de la Torre J.C., Oldstone M.B. Persistent LCMV infection is controlled by blockade of type I interferon signaling. Science 2013, 340:207-211.
159. Tinoco R., Alcalde V., Yang Y., Sauer K., Zuniga E.I. Cell-intrinsic transforming growth factor-beta signaling mediates virus-specific CD8+ T cell deletion and viral persistence in vivo. Immunity 2009, 31:145-157.
160. Topalian S.L., Hodi F.S., Brahmer J.R., Gettinger S.N., Smith D.C., McDermott D.F., Powderly J.D., Carvajal R.D., Sosman J.A., Atkins M.B., et al. Safety, Activity, and Immune Correlates of Anti-PD-1 Antibody in Cancer. N Engl J Med. 2012, 366:2443-2454.
161. Trautmann L., Janbazian L., Chomont N., Said E.A., Gimmig S., Bessette B., Boulassel M.R., Delwart E., Sepulveda H., Balderas R.S., et al. Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction. Nat. Med. 2006, 12:1198-1202.
162. Triebel F. LAG-3: a regulator of T-cell and DC responses and its use in therapeutic vaccination. Trends Immunol. 2003, 24:619-622.
163. Triebel F., Jitsukawa S., Baixeras E., Roman-Roman S., Genevee C., Viegas-Pequignot E., Hercend T. LAG-3, a novel lymphocyte activation gene closely related to CD4. J. Exp. Med. 1990, 171:1393-1405.
164. Velu V., Titanji K., Zhu B., Husain S., Pladevega A., Lai L., Vanderford T.H., Chennareddi L., Silvestri G., Freeman G.J., et al. Enhancing SIV-specific immunity in vivo by PD-1 blockade. Nature 2009, 458:206-210.
165. Vezys V., Penaloza-Macmaster P., Barber D.L., Ha S.J., Konieczny B., Freeman G.J., Mittler R.S., Ahmed R. 4-1BB Signaling Synergizes with Programmed Death Ligand 1 Blockade To Augment CD8 T Cell Responses during Chronic Viral Infection. J Immunol. 2011, 187:1634-1642.
166. Vinetz J.M., Kumar S., Good M.F., Fowlkes B.J., Berzofsky J.A., Miller L.H. Adoptive transfer of CD8+ T cells from immune animals does not transfer immunity to blood stage Plasmodium yoelii malaria. J. Immunol. 1990, 144:1069-1074.
167. Virgin H.W., Wherry E.J., Ahmed R. Redefining chronic viral infection. Cell 2009, 138:30-50.
168. Walker L.S., Gulbranson-Judge A., Flynn S., Brocker T., Raykundalia C., Goodall M., Förster R., Lipp M., Lane P. Compromised OX40 function in CD28-deficient mice is linked with failure to develop CXC chemokine receptor 5-positive CD4 cells and germinal centers. J. Exp. Med. 1999, 190:1115-1122.
169. Walunas T.L., Lenschow D.J., Bakker C.Y., Linsley P.S., Freeman G.J., Green J.M., Thompson C.B., Bluestone J.A. CTLA-4 can function as a negative regulator of T cell activation. Immunity 1994, 1:405-413.
170. Wang C., McPherson A.J., Jones R.B., Kawamura K.S., Lin G.H., Lang P.A., Ambagala T., Pellegrini M., Calzascia T., Aidarus N., et al. Loss of the signaling adaptor TRAF1 causes CD8+ T cell dysregulation during human and murine chronic infection. J. Exp. Med. 2012, 209:77-91.
171. Ward-Kavanagh L.K., Lin W.W., Šedý J.R., Ware C.F. The TNF Receptor Superfamily in Co-stimulating and Co-inhibitory Responses. Immunity 2016, 44:1005-1019. this issue.
172. Watts T.H. TNF/TNFR family members in costimulation of T cell responses. Annu. Rev. Immunol. 2005, 23:23-68.
173. Wei F., Zhong S., Ma Z., Kong H., Medvec A., Ahmed R., Freeman G.J., Krogsgaard M., Riley J.L. Strength of PD-1 signaling differentially affects T-cell effector functions. Proc. Natl. Acad. Sci. USA 2013, 110:E2480-E2489.
174. Weiss G.E., Crompton P.D., Li S., Walsh L.A., Moir S., Traore B., Kayentao K., Ongoiba A., Doumbo O.K., Pierce S.K. Atypical memory B cells are greatly expanded in individuals living in a malaria-endemic area. J. Immunol. 2009, 183:2176-2182.
175. West E.E., Youngblood B., Tan W.G., Jin H.T., Araki K., Alexe G., Konieczny B.T., Calpe S., Freeman G.J., Terhorst C., et al. Tight regulation of memory CD8(+) T cells limits their effectiveness during sustained high viral load. Immunity 2011, 35:285-298.
176. West E.E., Jin H.T., Rasheed A.U., Penaloza-Macmaster P., Ha S.J., Tan W.G., Youngblood B., Freeman G.J., Smith K.A., Ahmed R. PD-L1 blockade synergizes with IL-2 therapy in reinvigorating exhausted T cells. J. Clin. Invest. 2013, 123:2604-2615.
177. Wherry E.J., Blattman J.N., Murali-Krishna K., van der Most R., Ahmed R. Viral persistence alters CD8 T-cell immunodominance and tissue distribution and results in distinct stages of functional impairment. J. Virol. 2003, 77:4911-4927.
178. Wherry E.J., Ha S.J., Kaech S.M., Haining W.N., Sarkar S., Kalia V., Subramaniam S., Blattman J.N., Barber D.L., Ahmed R. Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 2007, 27:670-684.
179. Whitmire J.K., Flavell R.A., Grewal I.S., Larsen C.P., Pearson T.C., Ahmed R. CD40-CD40 ligand costimulation is required for generating antiviral CD4 T cell responses but is dispensable for CD8 T cell responses. J. Immunol. 1999, 163:3194-3201.
180. Wieland A., Shashidharamurthy R., Kamphorst A.O., Han J.H., Aubert R.D., Choudhury B.P., Stowell S.R., Lee J., Punkosdy G.A., Shlomchik M.J., et al. Antibody effector functions mediated by Fcγ-receptors are compromised during persistent viral infection. Immunity 2015, 42:367-378.
181. Wilson E.H., Harris T.H., Mrass P., John B., Tait E.D., Wu G.F., Pepper M., Wherry E.J., Dzierzinski F., Roos D., et al. Behavior of parasite-specific effector CD8+ T cells in the brain and visualization of a kinesis-associated system of reticular fibers. Immunity 2009, 30:300-311.
182. Wilson E.B., Yamada D.H., Elsaesser H., Herskovitz J., Deng J., Cheng G., Aronow B.J., Karp C.L., Brooks D.G. Blockade of chronic type I interferon signaling to control persistent LCMV infection. Science 2013, 340:202-207.
183. Wolchok J.D., Kluger H., Callahan M.K., Postow M.A., Rizvi N.A., Lesokhin A.M., Segal N.H., Ariyan C.E., Gordon R.A., Reed K., et al. Nivolumab plus ipilimumab in advanced melanoma. N. Engl. J. Med. 2013, 369:122-133.
184. 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. 2012, 72:917-927.
185. Workman C.J., Vignali D.A. Negative regulation of T cell homeostasis by lymphocyte activation gene-3 (CD223). J. Immunol. 2005, 174:688-695.
186. Workman C.J., Cauley L.S., Kim I.J., Blackman M.A., Woodland D.L., Vignali D.A. Lymphocyte activation gene-3 (CD223) regulates the size of the expanding T cell population following antigen activation in vivo. J. Immunol. 2004, 172:5450-5455.
187. Wu B., Huang B., Chen Y., Li S., Yan J., Zheng H., Huang S., Shen J., Lun Z.R., Wang Y., et al. Upregulated expression of Tim-3 involved in the process of toxoplasmic encephalitis in mouse model. Parasitol. Res. 2013, 112:2511-2521.
188. Xu D., Fu H.H., Obar J.J., Park J.J., Tamada K., Yagita H., Lefrançois L. A potential new pathway for PD-L1 costimulation of the CD8-T cell response to Listeria monocytogenes infection. PLoS ONE 2013, 8:e56539.
189. Yamada D.H., Elsaesser H., Lux A., Timmerman J.M., Morrison S.L., de la Torre J.C., Nimmerjahn F., Brooks D.G. Suppression of Fcγ-receptor-mediated antibody effector function during persistent viral infection. Immunity 2015, 42:379-390.
190. Yamazaki T., Akiba H., Iwai H., Matsuda H., Aoki M., Tanno Y., Shin T., Tsuchiya H., Pardoll D.M., Okumura K., et al. Expression of programmed death 1 ligands by murine T cells and APC. J. Immunol. 2002, 169:5538-5545.
191. Yokosuka T., Kobayashi W., Takamatsu M., Sakata-Sogawa K., Zeng H., Hashimoto-Tane A., Yagita H., Tokunaga M., Saito T. Spatiotemporal basis of CTLA-4 costimulatory molecule-mediated negative regulation of T cell activation. Immunity 2010, 33:326-339.
192. 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. 2012, 209:1201-1217.
193. Youngblood B., Oestreich K.J., Ha S.J., Duraiswamy J., Akondy R.S., West E.E., Wei Z., Lu P., Austin J.W., Riley J.L., et al. Chronic virus infection enforces demethylation of the locus that encodes PD-1 in antigen-specific CD8(+) T cells. Immunity 2011, 35:400-412.
194. Youngblood B., Noto A., Porichis F., Akondy R.S., Ndhlovu Z.M., Austin J.W., Bordi R., Procopio F.A., Miura T., Allen T.M., et al. Cutting edge: Prolonged exposure to HIV reinforces a poised epigenetic program for PD-1 expression in virus-specific CD8 T cells. J. Immunol. 2013, 191:540-544.
195. Yu Q., Yue F.Y., Gu X.X., Schwartz H., Kovacs C.M., Ostrowski M.A. OX40 ligation of CD4+ T cells enhances virus-specific CD8+ T cell memory responses independently of IL-2 and CD4+ T regulatory cell inhibition. J. Immunol. 2006, 176:2486-2495.
196. Yu X., Harden K., Gonzalez L.C., Francesco M., Chiang E., Irving B., Tom I., Ivelja S., Refino C.J., Clark H., et al. The surface protein TIGIT suppresses T cell activation by promoting the generation of mature immunoregulatory dendritic cells. Nat. Immunol. 2009, 10:48-57.
197. Zajac A.J., Blattman J.N., Murali-Krishna K., Sourdive D.J., Suresh M., Altman J.D., Ahmed R. Viral immune evasion due to persistence of activated T cells without effector function. J. Exp. Med. 1998, 188:2205-2213.
198. Zander R.A., Obeng-Adjei N., Guthmiller J.J., Kulu D.I., Li J., Ongoiba A., Traore B., Crompton P.D., Butler N.S. PD-1 Co-inhibitory and OX40 Co-stimulatory Crosstalk Regulates Helper T Cell Differentiation and Anti-Plasmodium Humoral Immunity. Cell Host Microbe 2015, 17:628-641.
199. Zehn D., Wherry E.J. Immune Memory and Exhaustion: Clinically Relevant Lessons from the LCMV Model. Adv. Exp. Med. Biol. 2015, 850:137-152.
200. Zhang Z., Zhang J.Y., Wherry E.J., Jin B., Xu B., Zou Z.S., Zhang S.Y., Li B.S., Wang H.F., Wu H., et al. Dynamic programmed death 1 expression by virus-specific CD8 T cells correlates with the outcome of acute hepatitis B. Gastroenterology 2008, 134:1938-1949. 1949 e1931-1933.
201. Zhang Y., Zhou Y., Lou J., Li J., Bo L., Zhu K., Wan X., Deng X., Cai Z. PD-L1 blockade improves survival in experimental sepsis by inhibiting lymphocyte apoptosis and reversing monocyte dysfunction. Crit. Care 2010, 14:R220.
202. Zhou X., Yu S., Zhao D.M., Harty J.T., Badovinac V.P., Xue H.H. Differentiation and persistence of memory CD8(+) T cells depend on T cell factor 1. Immunity 2010, 33:229-240.
203. Zhu C., Sakuishi K., Xiao S., Sun Z., Zaghouani S., Gu G., Wang C., Tan D.J., Wu C., Rangachari M., et al. An IL-27/NFIL3 signalling axis drives Tim-3 and IL-10 expression and T-cell dysfunction. Nat. Commun. 2015, 6:6072.