The risks of targeting co-inhibitory pathways to modulate pathogen-directed T cell responses

Trends in Immunology

Volumn 34, Issue 5, 2013, Pages 193-199

  Frebel, Helge ^a   Oxenius, Annette ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; DOWN REGULATION; DRUG TARGETING; IMMUNOPATHOLOGY; INFECTION; NONHUMAN; PATHOGENESIS; REVIEW; T LYMPHOCYTE;

ANIMALS; CLINICAL TRIALS AS TOPIC; CTLA-4 ANTIGEN; DRUG EVALUATION, PRECLINICAL; HUMANS; IMMUNITY, CELLULAR; IMMUNOSUPPRESSIVE AGENTS; IMMUNOTHERAPY; INFECTION; MOLECULAR TARGETED THERAPY; PROGRAMMED CELL DEATH 1 RECEPTOR; RECEPTOR CROSS-TALK; SUPERINFECTION; T-LYMPHOCYTES;

EID: 84877130399     PISSN: 14714906     EISSN: 14714981     Source Type: Journal    
DOI: 10.1016/j.it.2012.12.002     Document Type: Review

References (81)

1. Sharpe A.H., Freeman G.J. The B7-CD28 superfamily. Nat. Rev. 2002, 2:116-126.
2. Croft M. The role of TNF superfamily members in T-cell function and diseases. Nat. Rev. 2009, 9:271-285.
3. Nishimura H., et al. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 1999, 11:141-151.
4. 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 1995, 3:541-547.
5. Peggs K.S., et al. Cell intrinsic mechanisms of T-cell inhibition and application to cancer therapy. Immunol. Rev. 2008, 224:141-165.
6. Norde W.J., et al. Co-inhibitory molecules in hematological malignancies: targets for therapeutic intervention. Blood 2012, 120:728-736.
7. Leach D.R., et al. Enhancement of antitumor immunity by CTLA-4 blockade. Science (New York, NY) 1996, 271:1734-1736.
8. Baitsch L., et al. Exhaustion of tumor-specific CD8(+) T cells in metastases from melanoma patients. J. Clin. Invest. 2011, 121:2350-2360.
9. Barber D.L., et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 2006, 439:682-687.
10. Lazar-Molnar E., et al. Programmed death-1 (PD-1)-deficient mice are extraordinarily sensitive to tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:13402-13407.
11. Bhadra R., et al. Control of Toxoplasma reactivation by rescue of dysfunctional CD8+ T-cell response via PD-1-PDL-1 blockade. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:9196-9201.
12. Lazar-Molnar E., et al. The PD-1/PD-L costimulatory pathway critically affects host resistance to the pathogenic fungus Histoplasma capsulatum. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:2658-2663.
13. Ishiwata K., et al. Costimulator B7-DC attenuates strong Th2 responses induced by Nippostrongylus brasiliensis. J. Immunol. 2010, 184:2086-2094.
14. Frebel H., et al. How chronic viral infections impact on antigen-specific T-cell responses. Eur. J. Immunol. 2011, 40:654-663.
15. Porichis F., Kaufmann D.E. Role of PD-1 in HIV pathogenesis and as target for therapy. Curr. HIV/AIDS Rep. 2012, 9:81-90.
16. Watanabe T., et al. PD-1/PD-L1 pathway and T-cell exhaustion in chronic hepatitis virus infection. J. Viral Hepat. 2010, 17:453-458.
17. Odorizzi P.M., Wherry E.J. Inhibitory receptors on lymphocytes: insights from infections. J. Immunol. 2012, 188:2957-2965.
18. Frebel H., et al. Programmed death 1 protects from fatal circulatory failure during systemic virus infection of mice. J. Exp. Med. 2012, 209:2485-2499.
19. Rowe J.H., et al. Innate IFN-gamma is essential for programmed death ligand-1-mediated T cell stimulation following Listeria monocytogenes infection. J. Immunol. 2012, 189:876-884.
20. Yamazaki T., et al. Blockade of B7-H1 on macrophages suppresses CD4+ T cell proliferation by augmenting IFN-gamma-induced nitric oxide production. J. Immunol. 2005, 175:1586-1592.
21. Lee S.J., et al. B7-H1 (programmed cell death ligand 1) is required for the development of multifunctional Th1 cells and immunity to primary, but not secondary, Salmonella infection. J. Immunol. 2010, 185:2442-2449.
22. Barber D.L., et al. CD4 T cells promote rather than control tuberculosis in the absence of PD-1-mediated inhibition. J. Immunol. 2010, 186:1598-1607.
23. Rodig N., et al. Endothelial expression of PD-L1 and PD-L2 down-regulates CD8+ T cell activation and cytolysis. Eur. J. Immunol. 2003, 33:3117-3126.
24. Lepenies B., et al. CTLA-4 blockade differentially influences the outcome of non-lethal and lethal Plasmodium yoelii infections. Microbes Infect. 2007, 9:687-694.
25. Jurado J.O., et al. Programmed death (PD)-1:PD-ligand 1/PD-ligand 2 pathway inhibits T cell effector functions during human tuberculosis. J. Immunol. 2008, 181:116-125.
26. Iwai Y., et al. PD-1 inhibits antiviral immunity at the effector phase in the liver. J. Exp. Med. 2003, 198:39-50.
27. Phares T.W., et al. Enhanced antiviral T cell function in the absence of B7-H1 is insufficient to prevent persistence but exacerbates axonal bystander damage during viral encephalomyelitis. J. Immunol. 2010, 185:5607-5618.
28. Mueller S.N., et al. Viral targeting of fibroblastic reticular cells contributes to immunosuppression and persistence during chronic infection. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:15430-15435.
29. Mueller S.N., et al. PD-L1 has distinct functions in hematopoietic and nonhematopoietic cells in regulating T cell responses during chronic infection in mice. J. Clin. Invest. 2010, 120:2508-2515.
30. Hafalla J.C., et al. 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.
31. Jun H., et al. B7-H1 (CD274) inhibits the development of herpetic stromal keratitis (HSK). FEBS Lett. 2005, 579:6259-6264.
32. Jacobs T., et al. Murine malaria is exacerbated by CTLA-4 blockade. J. Immunol. 2002, 169:2323-2329.
33. Good-Jacobson K.L., et al. PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells. Nat. Immunol. 2010, 11:535-542.
34. Kawamoto S., et al. The inhibitory receptor PD-1 regulates IgA selection and bacterial composition in the gut. Science (New York NY) 2012, 336:485-489.
35. Hams E., et al. Blockade of B7-H1 (programmed death ligand 1) enhances humoral immunity by positively regulating the generation of T follicular helper cells. J. Immunol. 2011, 186:5648-5655.
36. Butler N.S., et al. Therapeutic blockade of PD-L1 and LAG-3 rapidly clears established blood-stage Plasmodium infection. Nat. Immunol. 2012, 13:188-195.
37. Francisco L.M., et al. The PD-1 pathway in tolerance and autoimmunity. Immunol. Rev. 2010, 236:219-242.
38. Chen Y., et al. Programmed death (PD)-1-deficient mice are extremely sensitive to murine hepatitis virus strain-3 (MHV-3) infection. PLoS Pathog. 2011, 7:e1001347.
39. Frisancho-Kiss S., et al. Cutting edge: T cell Ig mucin-3 reduces inflammatory heart disease by increasing CTLA-4 during innate immunity. J. Immunol. 2006, 176:6411-6415.
40. Keir M.E., et al. PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 2008, 26:677-704.
41. Liang S.C., et al. PD-L1 and PD-L2 have distinct roles in regulating host immunity to cutaneous leishmaniasis. Eur. J. Immunol. 2006, 36:58-64.
42. Dulgerian L.R., et al. Programmed death ligand 2 regulates arginase induction and modifies Trypanosoma cruzi survival in macrophages during murine experimental infection. Immunology 2011, 133:29-40.
43. Wang Y., et al. Immunoregulation by tumor necrosis factor superfamily member LIGHT. Immunol. Rev. 2009, 229:232-243.
44. Cai G., Freeman G.J. The CD160, BTLA, LIGHT/HVEM pathway: a bidirectional switch regulating T-cell activation. Immunol. Rev. 2009, 229:244-258.
45. Stanley A.C., et al. Critical roles for LIGHT and its receptors in generating T cell-mediated immunity during Leishmania donovani infection. PLoS Pathog. 2011, 7:e1002279.
46. Jin H.T., et al. Cooperation of Tim-3 and PD-1 in CD8 T-cell exhaustion during chronic viral infection. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:14733-14738.
47. Hirao L.A., et al. Immune modulation through 4-1BB enhances SIV vaccine protection in non-human primates against SIVmac251 challenge. PLoS ONE 2011, 6:e24250.
48. Fisicaro P., et al. Combined blockade of programmed death-1 and activation of CD137 increase responses of human liver T cells against HBV, but not HCV. Gastroenterology 2012, 143:1576-1585.
49. Vezys V., et al. 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.
50. Vaccari M., et al. Fatal pancreatitis in simian immunodeficiency virus SIV(mac251)-infected macaques treated with 2',3'-dideoxyinosine and stavudine following cytotoxic-T-lymphocyte-associated antigen 4 and indoleamine 2,3-dioxygenase blockade. J. Virol. 2012, 86:108-113.
51. Pulko V., et al. B7-h1 expressed by activated CD8 T cells is essential for their survival. J. Immunol. 2011, 187:5606-5614.
52. Talay O., et al. B7-H1 (PD-L1) on T cells is required for T-cell-mediated conditioning of dendritic cell maturation. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:2741-2746.
53. Bryant-Hudson K.M., Carr D.J. PD-L1-expressing dendritic cells contribute to viral resistance during acute HSV-1 infection. Clin. Dev. Immunol. 2012, 2012:924619.
54. Nishimura H., Honjo T. PD-1: an inhibitory immunoreceptor involved in peripheral tolerance. Trends Immunol. 2001, 22:265-268.
55. Berman D., et al. Blockade of cytotoxic T-lymphocyte antigen-4 by ipilimumab results in dysregulation of gastrointestinal immunity in patients with advanced melanoma. Cancer Immun. 2010, 10:11.
56. Di Giacomo A.M., et al. The emerging toxicity profiles of anti-CTLA-4 antibodies across clinical indications. Semin. Oncol. 2010, 37:499-507.
57. Brahmer J.R., et al. Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates. J. Clin. Oncol. 2010, 28:3167-3175.
58. Topalian S.L., et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 2012, 366:2443-2454.
59. Brahmer J.R., et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N. Engl. J. Med. 2012, 366:2455-2465.
60. Paterson A.M., et al. The programmed death-1 ligand 1:B7-1 pathway restrains diabetogenic effector T cells in vivo. J. Immunol. 2011, 187:1097-1105.
61. Reynoso E.D., et al. Intestinal tolerance is converted to autoimmune enteritis upon PD-1 ligand blockade. J. Immunol. 2009, 182:2102-2112.
62. Hamel K.M., et al. B7-H1 expression on non-B and non-T cells promotes distinct effects on T- and B-cell responses in autoimmune arthritis. Eur. J. Immunol. 2010, 40:3117-3127.
63. Gotsman I., et al. Proatherogenic immune responses are regulated by the PD-1/PD-L pathway in mice. J. Clin. Invest. 2007, 117:2974-2982.
64. Bu D.X., et al. Impairment of the programmed cell death-1 pathway increases atherosclerotic lesion development and inflammation. Arterioscler. Thromb. Vasc. Biol. 2011, 31:1100-1107.
65. Kroner A., et al. A PD-1 polymorphism is associated with disease progression in multiple sclerosis. Ann. Neurol. 2005, 58:50-57.
66. Salama A.D., et al. Critical role of the programmed death-1 (PD-1) pathway in regulation of experimental autoimmune encephalomyelitis. J. Exp. Med. 2003, 198:71-78.
67. Bolinger B., et al. IFN-gamma-receptor signaling ameliorates transplant vasculopathy through attenuation of CD8+ T-cell-mediated injury of vascular endothelial cells. Eur. J. Immunol. 2010, 40:733-743.
68. Chandraker A., et al. CTLA-4 is important in maintaining long-term survival of cardiac allografts. Transplantation 2005, 79:897-903.
69. Peretz Y., et al. CD160 and PD-1 co-expression on HIV-specific CD8 T cells defines a subset with advanced dysfunction. PLoS Pathog. 2012, 8:e1002840.
70. Shui J.W., et al. HVEM signalling at mucosal barriers provides host defence against pathogenic bacteria. Nature 2012, 488:222-225.
71. West E.E., et al. Tight regulation of memory CD8(+) T cells limits their effectiveness during sustained high viral load. Immunity 2011, 35:285-298.
72. Lafon M., et al. Detrimental contribution of the immuno-inhibitor B7-H1 to rabies virus encephalitis. J. Immunol. 2008, 180:7506-7515.
73. Tinoco R., et al. Cell-intrinsic transforming growth factor-beta signaling mediates virus-specific CD8+ T cell deletion and viral persistence in vivo. Immunity 2009, 31:145-157.
74. Dietze K.K., et al. Transient depletion of regulatory T cells in transgenic mice reactivates virus-specific CD8+ T cells and reduces chronic retroviral set points. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:2420-2425.
75. Brooks D.G., et al. Interleukin-10 determines viral clearance or persistence in vivo. Nat. Med. 2006, 12:1301-1309.
76. Finnefrock A.C., et al. PD-1 blockade in rhesus macaques: impact on chronic infection and prophylactic vaccination. J. Immunol. 2009, 182:980-987.
77. Ha S.J., et al. Enhancing therapeutic vaccination by blocking PD-1-mediated inhibitory signals during chronic infection. J. Exp. Med. 2008, 205:543-555.
78. Channappanavar R., et al. Blocking of PDL-1 interaction enhances primary and secondary CD8 T cell response to herpes simplex virus-1 infection. PLoS ONE 2012, 7:e39757.
79. Sehrawat S., et al. Role of Tim-3/galectin-9 inhibitory interaction in viral-induced immunopathology: shifting the balance toward regulators. J. Immunol. 2009, 182:3191-3201.
80. Duncan D.S., Miller S.D. CNS expression of B7-H1 regulates pro-inflammatory cytokine production and alters severity of Theiler's virus-induced demyelinating disease. PLoS ONE 2011, 6:e18548.
81. Peng B., et al. Enhanced upper genital tract pathologies by blocking Tim-3 and PD-L1 signaling pathways in mice intravaginally infected with Chlamydia muridarum. BMC Infect. Dis. 2011, 11:347.