High viral burden restricts short-lived effector cell number at late times postinfection through increased natural regulatory T cell expansion

Journal of Immunology

Volumn 190, Issue 10, 2013, Pages 5020-5029

  Amoah, Samuel ^a   Holbrook, Beth C ^a   Yammani, Rama D ^a   Alexander Miller, Martha A ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; INTERLEUKIN 2; STAT5 PROTEIN; TRANSCRIPTION FACTOR T BET;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CONTROLLED STUDY; EFFECTOR CELL; FEMALE; IMMUNOMODULATION; IMMUNOREGULATION; MEMORY PRECURSOR EFFECTOR CELL; MOUSE; NONHUMAN; POXVIRUS INFECTION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SHORT LIVED EFFECTOR CELL; T LYMPHOCYTE ACTIVATION; VACCINIA VIRUS; VIRUS LOAD;

ANIMALS; B-LYMPHOCYTE SUBSETS; CASPASE 3; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL PROLIFERATION; CTLA-4 ANTIGEN; FEMALE; GLUCOCORTICOID-INDUCED TNFR-RELATED PROTEIN; INTERLEUKIN-12; INTERLEUKIN-2; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MICE; MICE, INBRED C57BL; RECEPTORS, IMMUNOLOGIC; STAT5 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, REGULATORY; VACCINIA; VACCINIA VIRUS; VIRAL LOAD;

EID: 84877830917     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200971     Document Type: Article

References (47)

1. Kaech, S. M., E. J. Wherry, and R. Ahmed. 2002. Effector and memory T-cell differentiation: implications for vaccine development. Nat. Rev. Immunol. 2: 251-262. (Pubitemid 37323225)
2. + memory T cell subsets. Proc. Natl. Acad. Sci. USA 101: 5610-5615. (Pubitemid 38481204)
3. Kaech, S. M., J. T. Tan, E. J. Wherry, B. T. Konieczny, C. D. Surh, and R. Ahmed. 2003. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4: 1191-1198. (Pubitemid 37540688)
4. Voehringer, D., C. Blaser, P. Brawand, D. H. Raulet, T. Hanke, and H. Pircher. 2001. Viral infections induce abundant numbers of senescent CD8 T cells. J. Immunol. 167: 4838-4843. (Pubitemid 33009711)
5. +) T cell fates via the graded expression of T-bet transcription factor. Immunity 27: 281-295. (Pubitemid 47284924)
6. Sarkar, S., V. Kalia, W. N. Haining, B. T. Konieczny, S. Subramaniam, and R. Ahmed. 2008. Functional and genomic profiling of effector CD8 T cell subsets with distinct memory fates. J. Exp. Med. 205: 625-640. (Pubitemid 351439309)
7. + T cells. Immunol. Rev. 211: 81-92. (Pubitemid 43882963)
8. + T cells favors terminal-effector differentiation in vivo. Immunity 32: 91-103.
9. Cui, W., N. S. Joshi, A. Jiang, and S. M. Kaech. 2009. Effects of Signal 3 during CD8 T cell priming: Bystander production of IL-12 enhances effector T cell expansion but promotes terminal differentiation. Vaccine 27: 2177-2187.
10. Pham, N. L., V. P. Badovinac, and J. T. Harty. 2009. A default pathway of memory CD8 T cell differentiation after dendritic cell immunization is deflected by encounter with inflammatory cytokines during antigen-driven proliferation. J. Immunol. 183: 2337-2348.
11. +) T cells. Eur. J. Immunol. 39: 1774-1783.
12. Cox, M. A., L. E. Harrington, and A. J. Zajac. 2011. Cytokines and the inception of CD8 T cell responses. Trends Immunol. 32: 180-186.
13. + immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J. Exp. Med. 188: 287-296. (Pubitemid 28357757)
14. Sakaguchi, S., N. Sakaguchi, M. Asano, M. Itoh, and M. Toda. 1995. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155: 1151-1164.
15. Maloy, K. J., and F. Powrie. 2001. Regulatory T cells in the control of immune pathology. Nat. Immunol. 2: 816-822.
16. + regulatory T cells in immunological tolerance to self and non-self. Nat. Immunol. 6: 345-352. (Pubitemid 41716771)
17. + T cell responses induced by direct priming and cross-priming and moderate immunodominance disparities. J. Immunol. 174: 3344-3351. (Pubitemid 40354038)
18. + T cell responses. J. Exp. Med. 198: 889-901. (Pubitemid 37152926)
19. + regulatory T cells control the severity of viral immunoinflammatory lesions. J. Immunol. 172: 4123-4132. (Pubitemid 38375224)
20. + T-cell effector differentiation by modulating IL-2 homeostasis. Proc. Natl. Acad. Sci. USA 108: 7529-7534.
21. +) T cells after infection. Nat. Immunol. 3: 619-626. (Pubitemid 34752470)
22. + T cells in response to infection is markedly efficient. Science 325: 1265-1269.
23. Whitton, J. L., N. Sheng, M. B. Oldstone, and T. A. McKee. 1993. A "string-ofbeads" vaccine, comprising linked minigenes, confers protection from lethaldose virus challenge. J. Virol. 67: 348-352. (Pubitemid 23002996)
24. Blattman, J. N., J. M. Grayson, E. J. Wherry, S. M. Kaech, K. A. Smith, and R. Ahmed. 2003. Therapeutic use of IL-2 to enhance antiviral T-cell responses in vivo. Nat. Med. 9: 540-547. (Pubitemid 36597099)
25. Lefrançois, L., and J. J. Obar. 2010. Once a killer, always a killer: from cytotoxic T cell to memory cell. Immunol. Rev. 235: 206-218.
26. Yamaguchi, T., K. Hirota, K. Nagahama, K. Ohkawa, T. Takahashi, T. Nomura, and S. Sakaguchi. 2007. Control of immune responses by antigen-specific regulatory T cells expressing the folate receptor. Immunity 27: 145-159. (Pubitemid 47089022)
27. + T cells in vivo. J. Immunol. 182: 7490-7500.
28. + regulatory T cell function. Eur. J. Immunol. 34: 2480-2488. (Pubitemid 39302805)
29. + T cell suppressor function. Eur. J. Immunol. 34: 366-376. (Pubitemid 39255947)
30. Walker, L. S., and D. M. Sansom. 2011. The emerging role of CTLA4 as a cellextrinsic regulator of T cell responses. Nat. Rev. Immunol. 11: 852-863.
31. + T cell homeostasis. J. Immunol. 181: 1806-1813.
32. + T cell effector pool size via IL-2 restriction. J. Immunol. 187: 3186-3197.
33. O'Gorman, W. E., H. Dooms, S. H. Thorne, W. F. Kuswanto, E. F. Simonds, P. O. Krutzik, G. P. Nolan, and A. K. Abbas. 2009. The initial phase of an immune response functions to activate regulatory T cells. J. Immunol. 183: 332-339.
34. Joshi, N. S., W. Cui, C. X. Dominguez, J. H. Chen, T. W. Hand, and S. M. Kaech. 2011. Increased numbers of preexisting memory CD8 T cells and decreased Tbet expression can restrain terminal differentiation of secondary effector and memory CD8 T cells. J. Immunol. 187: 4068-4076.
35. Ye, F., J. Turner, and E. Flano. 2012. Contribution of pulmonary KLRG1(high) and KLRG1(low) CD8 T cells to effector and memory responses during influenza virus infection. J. Immunol. 189: 5206-5211.
36. + T cell differentiation. J. Immunol. 187: 4967-4978.
37. + Tcell differentiation. Int. Immunol. 22: 619-625.
38. Obar, J. J., and L. Lefrançois. 2010. Early signals during CD8 T cell priming regulate the generation of central memory cells. J. Immunol. 185: 263-272.
39. Lourenço, E. V., and A. La Cava. 2011. Natural regulatory T cells in autoimmunity. Autoimmunity 44: 33-42.
40. Rouse, B. T., P. P. Sarangi, and S. Suvas. 2006. Regulatory T cells in virus infections. Immunol. Rev. 212: 272-286. (Pubitemid 44116714)
41. + regulatory T cells, which suppress HIV-specific CD4 T-cell responses in HIV-infected patients. Blood 104: 3249-3256. (Pubitemid 39507143)
42. + T cells during chronic hepatitis C virus infection. J. Virol. 79: 7860-7867. (Pubitemid 40756821)
43. +)CD25(high) regulatory T cells and programmed death-ligand 1 in chronic hepatitis B. Viral Immunol. 25: 21-28.
44. TrehanPati, N., S. Kotillil, S. S. Hissar, S. Shrivastava, A. Khanam, S. Sukriti, S. K. Mishra, and S. K. Sarin. 2011. Circulating Tregs correlate with viral load reduction in chronic HBV-treated patients with tenofovir disoproxil fumarate. J. Clin. Immunol. 31: 509-520.
45. Pipkin, M. E., J. A. Sacks, F. Cruz-Guilloty, M. G. Lichtenheld, M. J. Bevan, and A. Rao. 2010. Interleukin-2 and inflammation induce distinct transcriptional programs that promote the differentiation of effector cytolytic T cells. Immunity 32: 79-90.
46. Cheng, G., A. Yu, and T. R. Malek. 2011. T-cell tolerance and the multifunctional role of IL-2R signaling in T-regulatory cells. Immunol. Rev. 241: 63-76.
47. Benson, A., S. Murray, P. Divakar, N. Burnaevskiy, R. Pifer, J. Forman, and F. Yarovinsky. 2012. Microbial infection-induced expansion of effector T cells overcomes the suppressive effects of regulatory T cells via an IL-2 deprivation mechanism. J. Immunol. 188: 800-810.