Peroxiredoxin II regulates effector and secondary memory CD8+ T cell responses

Journal of Virology

Volumn 86, Issue 24, 2012, Pages 13629-13641

  Michalek, Ryan D ^a   Crump, Katie E ^b   Weant, Ashley E ^b   Hiltbold, Elizabeth M ^b   Juneau, Daniel G ^b   Moon, Eun Yi ^c   Yu, Dae Yeul ^d   Poole, Leslie B ^b   Grayson, Jason M ^b  

^a METABOLON INC   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

^c Sejong University   (South Korea)

^d Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN PEROXIDE; PEROXIREDOXIN 2; REACTIVE OXYGEN INTERMEDIATE; REACTIVE OXYGEN METABOLITE; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL INFECTION; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL ACTIVITY; CELL COUNT; CELL CYCLE S PHASE; CELL DEATH; CELL DIFFERENTIATION; CELL DIVISION; CELL EXPANSION; CELL FUNCTION; CELL LINE; CELL METABOLISM; CELL PROLIFERATION; CELL STIMULATION; CELL TRANSPORT; CONTROLLED STUDY; EFFECTOR CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME METABOLISM; ENZYME REGULATION; IMMUNE RESPONSE; IMMUNOPATHOLOGY; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTIC CHORIOMENINGITIS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; OXIDATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROVOCATION TEST; SPLEEN; SURVIVAL; VIRUS INFECTION;

ANIMALS; BLOTTING, WESTERN; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; IMMUNOLOGIC MEMORY; MICE; MICE, TRANSGENIC; PEROXIREDOXINS; REAL-TIME POLYMERASE CHAIN REACTION;

ANIMALIA; BACTERIA (MICROORGANISMS); MUS;

EID: 84870655394     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01559-12     Document Type: Article

References (53)

1. Abate C, Patel L, Rauscher FJ III, Curran T. 1990. Redox regulation of fos and jun DNA-binding activity in vitro. Science 249:1157-1161.
2. Ahmed R, Salmi A, Butler LD, Chiller JM, Oldstone MB. 1984. Selection of genetic variants of lymphocytic choriomeningitis virus in spleens of persistently infected mice. Role in suppression of cytotoxic T lymphocyte response and viral persistence. J. Exp. Med. 160:521-540.
3. Alexander-Miller MA. 2005. High-avidity CD8+T cells: optimal soldiers in the war against viruses and tumors. Immunol. Res. 31:13-24.
4. Barber DL, et al. 2006. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439:682-687.
5. Blackburn SD, et al. 2009. Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat. Immunol. 10:29-37.
6. Case AJ, et al. 2011. Elevated mitochondrial superoxide disrupts normal T cell development, impairing adaptive immune responses to an influenza challenge. Free Radic. Biol. Med. 50:448-458.
7. Cayota A, Vuillier F, Gonzalez G, Dighiero G. 1996. In vitro antioxidant recoverstreatment recovers proliferative responses of anergic CD4+ lymphocytes from human immunodeficiency virus-infected individuals. Blood 87:4746-4753.
8. Chae HZ, Kim HJ, Kang SW, Rhee SG. 1999. Characterization of three isoforms of mammalian peroxiredoxin that reduce peroxides in the presence of thioredoxin. Diabetes Res. Clin. Pract. 45:101-112.
9. Chaudhri G, Clark IA, Hunt NH, Cowden WB, Ceredig R. 1986. Effect of antioxidants on primary alloantigen-induced T cell activation and proliferation. J. Immunol. 137:2646-2652.
10. Choi MH, et al. 2005. Regulation of PDGF signalling and vascular remodelling by peroxiredoxin II. Nature 435:347-353.
11. Chung YM, Yoo YD, Park JK, Kim YT, Kim HJ. 2001. Increased expression of peroxiredoxin II confers resistance to cisplatin. Anticancer Res. 21:1129-1133.
12. Cui W, Kaech SM. 2010. Generation of effector CD8+ T cells and their conversion to memory T cells. Immunol. Rev. 236:151-166.
13. Das R, Ponnappan S, Ponnappan U. 2007. Redox regulation of the proteasome in T lymphocytes during aging. Free Radic. Biol. Med. 42:541-551.
14. Devadas S, Zaritskaya L, Rhee SG, Oberley L, Williams MS. 2002. Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation: selective regulation of mitogen-activated protein kinase activation and fas ligand expression. J. Exp. Med. 195:59-70.
15. Gopalakrishna R, Gundimeda U, Schiffman JE, McNeill TH. 2008. A direct redox regulation of protein kinase C isoenzymes mediates oxidantinduced neuritogenesis in PC12 cells. J. Biol. Chem. 283:14430-14444.
16. Grayson JM, Harrington LE, Lanier JG, Wherry EJ, Ahmed R. 2002. Differential sensitivity of naive and memory CD8+T cells to apoptosis in vivo. J. Immunol. 169:3760-3770.
17. Grayson JM, Zajac AJ, Altman JD, Ahmed R. 2000. Cutting edge: increased expression of Bcl-2 in antigen-specific memory CD8+T cells. J. Immunol. 164:3950-3954.
18. Hockenbery DM, Oltvai ZN, Yin XM, Milliman CL, Korsmeyer SJ. 1993. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75:241-251.
19. Ichii H, et al. 2002. Role for Bcl-6 in the generation and maintenance of memory CD8+ T cells. Nat. Immunol. 3:558-563.
20. Imboden JB, Weiss A. 1987. The T-cell antigen receptor regulates sustained increases in cytoplasmic free Ca2+ through extracellular Ca2+ influx and ongoing intracellular Ca2+mobilization. Biochem. J. 247:695-700.
21. Intlekofer AM, et al. 2005. Effector and memory CD8+ T cell fate coupled by T-bet and eomesodermin. Nat. Immunol. 6:1236-1244.
22. Jabbari A, Harty JT. 2006. Secondary memory CD8+ T cells are more protective but slower to acquire a central-memory phenotype. J. Exp. Med. 203:919-932.
23. Jonsson TJ, Johnson LC, Lowther WT. 2008. Structure of the sulphiredoxin-peroxiredoxin complex reveals an essential repair embrace. Nature 451:98-101.
24. Joshi NS, et al. 2007. Inflammation directs memory precursor and shortlived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 27:281-295.
25. Kusmartsev S, Nefedova Y, Yoder D, Gabrilovich DI. 2004. Antigenspecific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J. Immunol. 172:989-999.
26. Kwon J, et al. 2005. Receptor-stimulated oxidation of SHP-2 promotes T-cell adhesion through SLP-76-ADAP. EMBO J. 24:2331-2341.
27. Laniewski NG, Grayson JM. 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.
28. Lee TH, et al. 2003. Peroxiredoxin II is essential for sustaining life span of erythrocytes in mice. Blood 101:5033-5038.
29. Low FM, Hampton MB, Peskin AV, Winterbourn CC. 2007. Peroxiredoxin 2 functions as a noncatalytic scavenger of low-level hydrogen peroxidez in the erythrocyte. Blood 109:2611-2617.
30. Matthews JR, Wakasugi N, Virelizier JL, Yodoi J, Hay RT. 1992. Thioredoxin regulates the DNA binding activity of NF-kappa B by reduction of a disulphide bond involving cysteine 62. Nucleic Acids Res. 20:3821-3830.
31. May JM, de Haen C. 1979. Insulin-stimulated intracellular hydrogen peroxide production in rat epididymal fat cells. J. Biol. Chem. 254:2214-2220.
32. Meng TC, Buckley DA, Galic S, Tiganis T, Tonks NK. 2004. Regulation of insulin signaling through reversible oxidation of the protein-tyrosine phosphatases TC45 and PTP1B. J. Biol. Chem. 279:37716-37725.
33. Michalek RD, et al. 2007. The requirement of reversible cysteine sulfenic acid formation for T cell activation and function. J. Immunol. 179:6456-6467.
34. Moon EY, et al. 2006. T lymphocytes and dendritic cells are activated by the deletion of peroxiredoxin II (Prx II) gene. Immunol. Lett. 102:184-190.
35. Murali-Krishna K, Ahmed R. 2000. Cutting edge: naive T cells masquerading as memory cells. J. Immunol. 165:1733-1737.
36. Murali-Krishna K, et al. 1998. Counting antigen-specific CD8 T cells: a ofreevaluation of bystander activation during viral infection. Immunity 8:177-187.
37. Mustelin T, Coggeshall KM, Isakov N, Altman A. 1990. T cell antigen receptor-mediated activation of phospholipase C requires tyrosine phosphorylation. Science 247:1584-1587.
38. Nishi T, et al. 2002. Spatial redox regulation of a critical cysteine residue of NF-kappa B in vivo. J. Biol. Chem. 277:44548-44556.
39. Pearce EL, et al. 2009. Enhancing CD8 T-cell memory by modulating fatty acid metabolism. Nature 460:103-107.
40. Perl A, Gergely P, Jr, Banki K. 2004. Mitochondrial dysfunction in T cells of patients with systemic lupus erythematosus. Int. Rev. Immunol. 23:293-313.
41. Piganelli JD, et al. 2002. A metalloporphyrin-based superoxide dismutase mimic inhibits adoptive transfer of autoimmune diabetes by a diabetogenic T-cell clone. Diabetes 51:347-355.
42. Rutishauser RL, et al. 2009. Transcriptional repressor Blimp-1 promotes CD8(+) T cell terminal differentiation and represses the acquisition of central memory T cell properties. Immunity 31:296-308.
43. Shlomai J. 2010. Redox control of protein-DNA interactions: from molecular mechanisms to significance in signal transduction, gene expression, and DNA replication. Antioxid. Redox Signal. 13:1429-1476.
44. Tebo AE, et al. 2005. Rapid recruitment of virus-specific CD8 T cells restructures immunodominance during protective secondary responses. J. Virol. 79:12703-12713.
45. Wherry EJ. 2011. T cell exhaustion. Nat. Immunol. 12:492-499.
46. Wood ZA, Poole LB, Karplus PA. 2003. Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300:650-653.
47. Wood ZA, Schroder E, Robin Harris J, Poole LB. 2003. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28:32-40.
48. Xanthoudakis S, Curran T. 1992. Identification and characterization of Ref-1, a nuclear protein that facilitates AP-1 DNA-binding activity. EMBO J. 11:653-665.
49. Yang CS, et al. 2007. Roles of peroxiredoxin II in the regulation of proinflammatory responses to LPS and protection against endotoxininduced lethal shock. J. Exp. Med. 204:583-594.
50. Yang CY, et al. 2011. The transcriptional regulators Id2 and Id3 control the formation of distinct memory CD8(+) T cell subsets. Nat. Immunol. 12:1221-1229.
51. Yi JS, Holbrook BC, Michalek RD, Laniewski NG, Grayson JM. 2006. Electron transport complex I is required for CD8+ T cell function. J. Immunol. 177:852-862.
52. Zenewicz LA, Foulds KE, Jiang J, Fan X, Shen H. 2002. Nonsecreted bacterial proteins induce recall CD8 T cell responses but do not serve as protective antigens. J. Immunol. 169:5805-5812.
53. Zhang N, Bevan MJ. 2011. CD8(+) T cells: foot soldiers of the immune system. Immunity 35:161-168.