Programmed death-1 controls T cell survival by regulating oxidative metabolism

Journal of Immunology

Volumn 194, Issue 12, 2015, Pages 5789-5800

  Tkachev, Victor ^a   Goodell, Stefanie ^a   Opipari, Anthony W ^a   Hao, Ling Yang ^b   Franchi, Luigi ^b   Glick, Gary D ^c   Ferrara, James L M ^a   Byersdorfer, Craig A ^d  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b Lycera Corporation   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ETOMOXIR; HYDROGEN PEROXIDE; PROGRAMMED DEATH 1 RECEPTOR; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REACTIVE OXYGEN METABOLITE; ANTIGEN; FATTY ACID;

AEROBIC METABOLISM; ALLOGENIC BONE MARROW TRANSPLANTATION; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; FATTY ACID OXIDATION; FEMALE; FLOW CYTOMETRY; GRAFT VERSUS HOST REACTION; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNIZATION; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; UPREGULATION; ADVERSE EFFECTS; ANIMAL; ANTAGONISTS AND INHIBITORS; BONE MARROW TRANSPLANTATION; GENE EXPRESSION; GENETICS; GRAFT VS HOST DISEASE; IMMUNOLOGY; METABOLISM; OXIDATION REDUCTION REACTION; TRANSGENIC MOUSE; XENOGRAFT;

ANIMALS; ANTIGENS; APOPTOSIS; BONE MARROW TRANSPLANTATION; CELL SURVIVAL; FATTY ACIDS; FEMALE; GENE EXPRESSION; GRAFT VS HOST DISEASE; HETEROGRAFTS; HUMANS; MICE; MICE, TRANSGENIC; OXIDATION-REDUCTION; PHENOTYPE; PROGRAMMED CELL DEATH 1 RECEPTOR; REACTIVE OXYGEN SPECIES; T-LYMPHOCYTES;

EID: 84931431126     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402180     Document Type: Article

References (68)

1. Lanzavecchia, A., and F. Sallusto. 2002. Progressive differentiation and selection of the fittest in the immune response. Nat. Rev. Immunol. 2: 982-987.
2. Chen, L., and D. B. Flies. 2013. Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat. Rev. Immunol. 13: 227-242.
3. Keir, M. E., M. J. Butte, G. J. Freeman, and A. H. Sharpe. 2008. PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 26: 677-704.
4. Barber, D. L., E. J. Wherry, D. Masopust, B. Zhu, J. P. Allison, A. H. Sharpe, G. J. Freeman, and R. Ahmed. 2006. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439: 682-687.
5. Mueller, S. N., V. K. Vanguri, S. J. Ha, E. E. West, M. E. Keir, J. N. Glickman, A. H. Sharpe, and R. Ahmed. 2010. PD-L1 has distinct functions in hematopoietic and nonhematopoietic cells in regulating T cell responses during chronic infection in mice. J. Clin. Invest. 120: 2508-2515.
6. Frebel, H., V. Nindl, R. A. Schuepbach, T. Braunschweiler, K. Richter, J. Vogel, C. A. Wagner, D. Loffing-Cueni, M. Kurrer, B. Ludewig, and A. Oxenius. 2012. Programmed death 1 protects from fatal circulatory failure during systemic virus infection of mice. J. Exp. Med. 209: 2485-2499.
7. Frebel, H., and A. Oxenius. 2013. The risks of targeting co-inhibitory pathways to modulate pathogen-directed T cell responses. Trends Immunol. 34: 193-199.
8. Wherry, E. J. 2011. T cell exhaustion. Nat. Immunol. 12: 492-499.
9. Freeman, G. J., A. J. Long, Y. Iwai, K. Bourque, T. Chernova, H. Nishimura, L. J. Fitz, N. Malenkovich, T. Okazaki, M. C. Byrne, et al. 2000. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J. Exp. Med. 192: 1027-1034.
10. Ishida, Y., Y. Agata, K. Shibahara, and T. Honjo. 1992. Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J. 11: 3887-3895.
11. Brahmer, J. R., S. S. Tykodi, L. Q. Chow, W. J. Hwu, S. L. Topalian, P. Hwu, C. G. Drake, L. H. Camacho, J. Kauh, K. Odunsi, et al. 2012. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N. Engl. J. Med. 366: 2455-2465.
12. Pardoll, D. M. 2012. Immunology beats cancer: a blueprint for successful translation. Nat. Immunol. 13: 1129-1132.
13. Topalian, S. L., F. S. Hodi, J. R. Brahmer, S. N. Gettinger, D. C. Smith, D. F. McDermott, J. D. Powderly, R. D. Carvajal, J. A. Sosman, M. B. Atkins, et al. 2012. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N. Engl. J. Med. 366: 2443-2454.
14. Iwai, Y., S. Terawaki, M. Ikegawa, T. Okazaki, and T. Honjo. 2003. PD-1 inhibits antiviral immunity at the effector phase in the liver. J. Exp. Med. 198: 39-50.
15. Phares, T. W., S. A. Stohlman, D. R. Hinton, R. Atkinson, and C. C. Bergmann. 2010. 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. 185: 5607-5618.
16. Dong, H., G. Zhu, K. Tamada, D. B. Flies, J. M. van Deursen, and L. Chen. 2004. B7-H1 determines accumulation and deletion of intrahepatic CD8(+) T lymphocytes. Immunity 20: 327-336.
17. Latchman, Y. E., S. C. Liang, Y. Wu, T. Chernova, R. A. Sobel, M. Klemm, V. K. Kuchroo, G. J. Freeman, and A. H. Sharpe. 2004. PD-L1-deficient mice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells. Proc. Natl. Acad. Sci. USA 101: 10691-10696.
18. Blazar, B. R., B. M. Carreno, A. Panoskaltsis-Mortari, L. Carter, Y. Iwai, H. Yagita, H. Nishimura, and P. A. Taylor. 2003. Blockade of programmed death-1 engagement accelerates graft-versus-host disease lethality by an IFN-gamma-dependent mechanism. J. Immunol. 171: 1272-1277.
19. Sandner, S. E., M. R. Clarkson, A. D. Salama, A. Sanchez-Fueyo, C. Domenig, A. Habicht, N. Najafian, H. Yagita, M. Azuma, L. A. Turka, and M. H. Sayegh. 2005. Role of the programmed death-1 pathway in regulation of alloimmune responses in vivo. J. Immunol. 174: 3408-3415.
20. Saha, A., K. Aoyama, P. A. Taylor, B. H. Koehn, R. G. Veenstra, A. Panoskaltsis-Mortari, D. H. Munn, W. J. Murphy, M. Azuma, H. Yagita, et al. 2013. Host programmed death ligand 1 is dominant over programmed death ligand 2 expression in regulating graft-versus-host disease lethality. Blood 122: 3062-3073.
21. Parry, R. V., J. M. Chemnitz, K. A. Frauwirth, A. R. Lanfranco, I. Braunstein, S. V. Kobayashi, P. S. Linsley, C. B. Thompson, and J. L. Riley. 2005. CTLA-4 and PD-1 receptors inhibit T-cell activation by distinct mechanisms. Mol. Cell. Biol. 25: 9543-9553.
22. Francisco, L. M., V. H. Salinas, K. E. Brown, V. K. Vanguri, G. J. Freeman, V. K. Kuchroo, and A. H. Sharpe. 2009. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J. Exp. Med. 206: 3015-3029.
23. Gatza, E., D. R. Wahl, A. W. Opipari, T. B. Sundberg, P. Reddy, C. Liu, G. D. Glick, and J. L. Ferrara. 2011. Manipulating the bioenergetics of alloreactive T cells causes their selective apoptosis and arrests graft-versus-host disease. Sci. Transl. Med. 3: ra8.
24. Byersdorfer, C. A., V. Tkachev, A. W. Opipari, S. Goodell, J. Swanson, S. Sandquist, G. D. Glick, and J. L. Ferrara. 2013. Effector T cells require fatty acid metabolism during murine graft-versus-host disease. Blood 122: 3230-3237.
25. Hildeman, D. A. 2004. Regulation of T-cell apoptosis by reactive oxygen species. Free Radic. Biol. Med. 36: 1496-1504.
26. Hildeman, D. A., T. Mitchell, T. K. Teague, P. Henson, B. J. Day, J. Kappler, and P. C. Marrack. 1999. Reactive oxygen species regulate activation-induced T cell apoptosis. Immunity 10: 735-744.
27. Keir, M. E., G. J. Freeman, and A. H. Sharpe. 2007. PD-1 regulates self-reactive CD8+ T cell responses to antigen in lymph nodes and tissues. J. Immunol. 179: 5064-5070.
28. Cooke, K. R., L. Kobzik, T. R. Martin, J. Brewer, J. Delmonte, Jr., J. M. Crawford, and J. L. Ferrara. 1996. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood 88: 3230-3239.
29. Ali, N., B. Flutter, R. Sanchez Rodriguez, E. Sharif-Paghaleh, L. D. Barber, G. Lombardi, and F. O. Nestle. 2012. Xenogeneic graft-versus-host-disease in NOD-scid IL-2Rγnull mice display a T-effector memory phenotype. PLoS ONE 7: e44219.
30. King, M. A., L. Covassin, M. A. Brehm, W. Racki, T. Pearson, J. Leif, J. Laning, W. Fodor, O. Foreman, L. Burzenski, et al. 2009. Human peripheral blood leucocyte non-obese diabetic-severe combined immunodeficiency interleukin-2 receptor gamma chain gene mouse model of xenogeneic graft-versus-host-like disease and the role of host major histocompatibility complex. Clin. Exp. Immunol. 157: 104-118.
31. Dickinson, B. C., and C. J. Chang. 2008. A targetable fluorescent probe for imaging hydrogen peroxide in the mitochondria of living cells. J. Am. Chem. Soc. 130: 9638-9639.
32. Cantor, J. M., and M. H. Ginsberg. 2012. CD98 at the crossroads of adaptive immunity and cancer. J. Cell Sci. 125: 1373-1382.
33. Haynes, B. F., M. Hemler, T. Cotner, D. L. Mann, G. S. Eisenbarth, J. L. Strominger, and A. S. Fauci. 1981. Characterization of a monoclonal antibody (5E9) that defines a human cell surface antigen of cell activation. J. Immunol. 127: 347-351.
34. Lorvik, K. B., O. A. Haabeth, T. Clancy, B. Bogen, and A. Corthay. 2013. Molecular profiling of tumor-specific TH1 cells activated in vivo. OncoImmunology 2: e24383.
35. Millrud, C. R., A. Månsson Kvarnhammar, R. Uddman, S. Björnsson, K. Riesbeck, and L. O. Cardell. 2012. The activation pattern of blood leukocytes in head and neck squamous cell carcinoma is correlated to survival. PLoS ONE 7: e51120.
36. Paz Morante, M., J. Briones, E. Canto, H. Sabzevari, R. Martino, J. Sierra, J. L. Rodriguez-Sanchez, and S. Vidal. 2006. Activation-associated phenotype of CD3 T cells in acute graft-versus-host disease. Clin. Exp. Immunol. 145: 36-43.
37. Shipkova, M., and E. Wieland. 2012. Surface markers of lymphocyte activation and markers of cell proliferation. Clin. Chim. Acta 413: 1338-1349.
38. Butte, M. J., M. E. Keir, T. B. Phamduy, A. H. Sharpe, and G. J. Freeman. 2007. Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses. Immunity 27: 111-122.
39. Balaban, R. S., S. Nemoto, and T. Finkel. 2005. Mitochondria, oxidants, and aging. Cell 120: 483-495.
40. Okazaki, T., S. Chikuma, Y. Iwai, S. Fagarasan, and T. Honjo. 2013. A rheostat for immune responses: the unique properties of PD-1 and their advantages for clinical application. Nat. Immunol. 14: 1212-1218.
41. Day, B. J., I. Fridovich, and J. D. Crapo. 1997. Manganic porphyrins possess catalase activity and protect endothelial cells against hydrogen peroxide-mediated injury. Arch. Biochem. Biophys. 347: 256-262.
42. Patel, M. 1998. Inhibition of neuronal apoptosis by a metalloporphyrin superoxide dismutase mimic. J. Neurochem. 71: 1068-1074.
43. Laniewski, N. G., and J. M. Grayson. 2004. Antioxidant treatment reduces expansion and contraction of antigen-specific CD8+ T cells during primary but not secondary viral infection. J. Virol. 78: 11246-11257.
44. Wherry, E. J., S. J. Ha, S. M. Kaech, W. N. Haining, S. Sarkar, V. Kalia, S. Subramaniam, J. N. Blattman, D. L. Barber, and R. Ahmed. 2007. Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 27: 670-684.
45. Blatt, N. B., A. E. Boitano, C. A. Lyssiotis, A. W. Opipari, Jr., and G. D. Glick. 2008. Bz-423 superoxide signals apoptosis via selective activation of JNK, Bak, and Bax. Free Radic. Biol. Med. 45: 1232-1242.
46. Sundberg, T. B., L. Swenson, D. R. Wahl, A. W. Opipari, Jr., and G. D. Glick. 2009. Apoptotic signaling activated by modulation of the F0F1-ATPase: implications for selective killing of autoimmune lymphocytes. J. Pharmacol. Exp. Ther. 331: 437-444.
47. Petrovas, C., D. A. Price, J. Mattapallil, D. R. Ambrozak, C. Geldmacher, V. Cecchinato, M. Vaccari, E. Tryniszewska, E. Gostick, M. Roederer, et al. 2007. SIV-specific CD8+ T cells express high levels of PD1 and cytokines but have impaired proliferative capacity in acute and chronic SIVmac251 infection. Blood 110: 928-936.
48. Zelinskyy, G., L. Myers, K. K. Dietze, K. Gibbert, M. Roggendorf, J. Liu, M. Lu, A. R. Kraft, V. Teichgräber, K. J. Hasenkrug, and U. Dittmer. 2011. Virus-specific CD8+ T cells upregulate programmed death-1 expression during acute friend retrovirus infection but are highly cytotoxic and control virus replication. J. Immunol. 187: 3730-3737.
49. Taylor, P. A., A. Panoskaltsis-Mortari, G. J. Freeman, A. H. Sharpe, R. J. Noelle, A. Y. Rudensky, T. W. Mak, J. S. Serody, and B. R. Blazar. 2005. Targeting of inducible costimulator (ICOS) expressed on alloreactive T cells down-regulates graft-versus-host disease (GVHD) and facilitates engraftment of allogeneic bone marrow (BM). Blood 105: 3372-3380.
50. Watanabe, S., S. Ogawa, Y. Hara, K. Tanabe, H. Toma, and R. Abe. 2006. Expression level of costimulatory receptor ICOS is critical for determining the polarization of helper T cell function. Transpl. Immunol. 15: 255-263.
51. Byersdorfer, C. A. 2014. The role of fatty acid oxidation in the metabolic reprograming of activated t-cells. Front. Immunol. 5: 641.
52. Nishimura, H., M. Nose, H. Hiai, N. Minato, and T. Honjo. 1999. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 11: 141-151.
53. Nishimura, H., T. Okazaki, Y. Tanaka, K. Nakatani, M. Hara, A. Matsumori, S. Sasayama, A. Mizoguchi, H. Hiai, N. Minato, and T. Honjo. 2001. Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 291: 319-322.
54. Jackson, S. H., S. Devadas, J. Kwon, L. A. Pinto, and M. S. Williams. 2004. T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation. Nat. Immunol. 5: 818-827.
55. Purushothaman, D., and A. Sarin. 2009. Cytokine-dependent regulation of NADPH oxidase activity and the consequences for activated T cell homeostasis. J. Exp. Med. 206: 1515-1523.
56. Kwon, J., K. E. Shatynski, H. Chen, S. Morand, X. de Deken, F. Miot, T. L. Leto, and M. S. Williams. 2010. The nonphagocytic NADPH oxidase Duox1 mediates a positive feedback loop during T cell receptor signaling. Sci. Signal. 3: ra59.
57. Perl, A., P. Gergely, Jr., F. Puskas, and K. Banki. 2002. Metabolic switches of T-cell activation and apoptosis. Antioxid. Redox Signal. 4: 427-443.
58. Sena, L. A., S. Li, A. Jairaman, M. Prakriya, T. Ezponda, D. A. Hildeman, C. R. Wang, P. T. Schumacker, J. D. Licht, H. Perlman, et al. 2013. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity 38: 225-236.
59. Kamiński, M. M., S. W. Sauer, M. Kamiński, S. Opp, T. Ruppert, P. Grigaravičius, P. Grudnik, H. J. Gröne, P. H. Krammer, and K. Gülow. 2012. T cell activation is driven by an ADP-dependent glucokinase linking enhanced glycolysis with mitochondrial reactive oxygen species generation. Cell Reports 2: 1300-1315.
60. Kaminski, M., M. Kiessling, D. Süss, P. H. Krammer, and K. Gülow. 2007. Novel role for mitochondria: protein kinase Ctheta-dependent oxidative signaling organelles in activation-induced T-cell death. Mol. Cell. Biol. 27:3625-3639.
61. Hildeman, D. A., T. Mitchell, B. Aronow, S. Wojciechowski, J. Kappler, and P. Marrack. 2003. Control of Bcl-2 expression by reactive oxygen species. Proc. Natl. Acad. Sci. USA 100: 15035-15040.
62. Dong, H., S. E. Strome, D. R. Salomao, H. Tamura, F. Hirano, D. B. Flies, P. C. Roche, J. Lu, G. Zhu, K. Tamada, et al. 2002. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med. 8: 793-800.
63. Tome, M. E., D. B. Johnson, B. K. Samulitis, R. T. Dorr, and M. M. Briehl. 2006. Glucose 6-phosphate dehydrogenase overexpression models glucose deprivation and sensitizes lymphoma cells to apoptosis. Antioxid. Redox Signal. 8: 1315-1327.
64. Phillips, D. C., K. J. Woollard, and H. R. Griffiths. 2003. The anti-inflammatory actions of methotrexate are critically dependent upon the production of reactive oxygen species. Br. J. Pharmacol. 138: 501-511.
65. Zamzami, N., P. Marchetti, M. Castedo, D. Decaudin, A. Macho, T. Hirsch, S. A. Susin, P. X. Petit, B. Mignotte, and G. Kroemer. 1995. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182: 367-377.
66. Lassègue, B., and K. K. Griendling. 2007. Mycophenolic acid is a new Nox2 inhibitor. Hypertension 49: 25-26.
67. Honeychurch, J., W. Alduaij, M. Azizyan, E. J. Cheadle, H. Pelicano, A. Ivanov, P. Huang, M. S. Cragg, and T. M. Illidge. 2012. Antibody-induced nonapoptotic cell death in human lymphoma and leukemia cells is mediated through a novel reactive oxygen species-dependent pathway. Blood 119: 3523-3533.
68. Sa, G., T. Das, C. Moon, C. M. Hilston, P. A. Rayman, B. I. Rini, C. S. Tannenbaum, and J. H. Finke. 2009. GD3, an overexpressed tumor-derived ganglioside, mediates the apoptosis of activated but not resting T cells. Cancer Res. 69: 3095-3104.