CD8 down-regulation and functional impairment of SIV-specific cytotoxic T lymphocytes in lymphoid and mucosal tissues during SIV infection

Journal of Leukocyte Biology

Volumn 93, Issue 6, 2013, Pages 943-950

  Xu, Huanbin ^a   Wang, Xiaolei ^a   Lackner, Andrew A ^a   Veazey, Ronald S ^a  

^a TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

Author keywords

CD8+T cell; CTL; HIV; Immunology; Intestine

Indexed keywords

CD8 ANTIGEN; GAMMA INTERFERON; PROGRAMMED DEATH 1 RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN DETECTION; ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOKINE RESPONSE; CYTOTOXIC T LYMPHOCYTE; DISEASE COURSE; DOWN REGULATION; FLUORESCENCE ANALYSIS; IMMUNOMODULATION; IMMUNOSTIMULATION; JEJUNUM; LYMPHOCYTE PROLIFERATION; LYMPHOID TISSUE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHESUS MONKEY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; T LYMPHOCYTE SUBPOPULATION; VIRUS IMMUNITY;

CD8+ T CELL; CTL; HIV; IMMUNOLOGY; INTESTINE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; DISEASE PROGRESSION; DOWN-REGULATION; FLOW CYTOMETRY; GASTRIC MUCOSA; IMMUNOPHENOTYPING; LYMPHOID TISSUE; MACACA MULATTA; PROGRAMMED CELL DEATH 1 RECEPTOR; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; T-LYMPHOCYTES, CYTOTOXIC;

MACACA; MACACA MULATTA; SIMIAN IMMUNODEFICIENCY VIRUS;

EID: 84878385801     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.1112580     Document Type: Article

References (42)

1. Schmitz, J. E., Kuroda, M. J., Santra, S., Sasseville, V. G., Simon, M. A., Lifton, M. A., Racz, P., Tenner-Racz, K., Dalesandro, M., Scallon, B. J., Ghrayeb, J., Forman, M. A., Montefiori, D. C., Rieber, E. P., Letvin, N. L., Reimann, K. A. (1999) Control of viremia in simian immunodeficiency virus infection by CD8+ lymphocytes. Science 283, 857-860
2. Koup, R. A., Safrit, J. T., Cao, Y., Andrews, C. A., McLeod, G., Borkowsky, W., Farthing, C., Ho, D. D. (1994) Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 68, 4650-4655
3. Kuroda, M. J., Schmitz, J. E., Seth, A., Veazey, R. S., Nickerson, C. E., Lifton, M. A., Dailey, P. J., Forman, M. A., Racz, P., Tenner-Racz, K., Letvin, N. L. (2000) Simian immunodeficiency virus-specific cytotoxic T lymphocytes and cell-associated viral RNA levels in distinct lymphoid compartments of SIVmac-infected rhesus monkeys. Blood 96, 1474-1479
4. Schmitz, J. E., Kuroda, M. J., Veazey, R. S., Seth, A., Taylor, W. M., Nickerson, C. E., Lifton, M. A., Dailey, P. J., Forman, M. A., Racz, P., Tenner-Racz, K., Letvin, N. L. (2000) Simian immunodeficiency virus (SIV)-specific CTL are present in large numbers in livers of SIV-infected rhesus monkeys. J. Immunol. 164, 6015-6019
5. Borrow, P., Lewicki, H., Wei, X., Horwitz, M. S., Peffer, N., Meyers, H., Nelson, J. A., Gairin, J. E., Hahn, B. H., Oldstone, M. B., Shaw, G. M. (1997) Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat. Med. 3, 205-211
6. Veazey, R. S., Gauduin, M. C., Mansfield, K. G., Tham, I. C., Altman, J. D., Lifson, J. D., Lackner, A. A., Johnson, R. P. (2001) Emergence and kinetics of simian immunodeficiency virus-specific CD8(+) T cells in the intestines of macaques during primary infection. J. Virol. 75, 10515-10519
7. Luescher, I. F., Vivier, E., Layer, A., Mahiou, J., Godeau, F., Malissen, B., Romero, P. (1995) CD8 modulation of T-cell antigen receptor-ligand interactions on living cytotoxic T lymphocytes. Nature 373, 353-356
8. Valitutti, S., Muller, S., Dessing, M., Lanzavecchia, A. (1996) Different responses are elicited in cytotoxic T lymphocytes by different levels of T cell receptor occupancy. J. Exp. Med. 183, 1917-1921
9. Daniels, M. A., Jameson, S. C. (2000) Critical role for CD8 in T cell receptor binding and activation by peptide/major histocompatibility complex multimers. J. Exp. Med. 191, 335-346
10. Holler, P. D., Kranz, D. M. (2003) Quantitative analysis of the contribution of TCR/pepMHC affinity and CD8 to T cell activation. Immunity 18, 255-264
11. Xiao, Z., Mescher, M. F., Jameson, S. C. (2007) Detuning CD8 T cells: down-regulation of CD8 expression, tetramer binding, and response during CTL activation. J. Exp. Med. 204, 2667-2677
12. Apte, S. H., Baz, A., Groves, P., Kelso, A., Kienzle, N. (2008) Interferon-+ and interleukin-4 reciprocally regulate CD8 expression in CD8+ T cells. Proc. Natl. Acad. Sci. USA 105, 17475-17480
13. Schmitz, J. E., Forman, M. A., Lifton, M. A., Concepcion, O., Reimann K. A., Jr., Crumpacker, C. S., Daley, J. F., Gelman, R. S., Letvin, N. L. (1998) Expression of the CD8[1]-heterodimer on CD8(+) T lymphocytes in peripheral blood lymphocytes of human immunodeficiency virus-and human immunodeficiency virus+ individuals. Blood 92, 198-206
14. Maile, R., Siler, C. A., Kerry, S. E., Midkiff, K. E., Collins, E. J., Frelinger, J. A. (2005) Peripheral "CD8 tuning" dynamically modulates the size and responsiveness of an antigen-specific T cell pool in vivo. J. Immunol. 174, 619-627
15. Kizaki, T., Kobayashi, S., Ogasawara, K., Day, N. K., Good, R. A., Onoe, K. (1991) Immune suppression induced by protoscoleces of Echinococcus multilocularis in mice. Evidence for the presence of CD8dull suppressor cells in spleens of mice intraperitoneally infected with E. multilocularis. J. Immunol. 147, 1659-1666
16. Vogel, T. U., Allen, T. M., Altman, J. D., Watkins, D. I. (2001) Functional impairment of simian immunodeficiency virus-specific CD8+ T cells during the chronic phase of infection. J. Virol. 75, 2458-2461
17. Goepfert, P. A., Bansal, A., Edwards, B. H., Ritter G. D., Jr., Tellez, I., McPherson, S. A., Sabbaj, S., Mulligan, M. J. (2000) A significant number of human immunodeficiency virus epitope-specific cytotoxic T lymphocytes detected by tetramer binding do not produce + interferon. J. Virol. 74, 10249-10255
18. Kostense, S., Vandenberghe, K., Joling, J., Van Baarle, D., Nanlohy, N., Manting, E., Miedema, F. (2002) Persistent numbers of tetramer+ CD8(+) T cells, but loss of interferon-++ HIV-specific T cells during progression to AIDS. Blood 99, 2505-2511
19. Shankar, P., Russo, M., Harnisch, B., Patterson, M., Skolnik, P., Lieberman, J. (2000) Impaired function of circulating HIV-specific CD8(+) T cells in chronic human immunodeficiency virus infection. Blood 96, 3094-3101
20. Lakhashe, S. K., Velu, V., Sciaranghella, G., Siddappa, N. B., Dipasquale, J. M., Hemashettar, G., Yoon, J. K., Rasmussen, R. A., Yang, F., Lee, S. J., Montefiori, D. C., Novembre, F. J., Villinger, F., Amara, R. R., Kahn, M., Hu, S. L., Li, S., Li, Z., Frankel, F. R., Robert-Guroff, M., Johnson, W. E., Lieberman, J., Ruprecht, R. M. (2011) Prime-boost vaccination with heterologous live vectors encoding SIV gag and multimeric HIV-1 gp160 protein: efficacy against repeated mucosal R5 clade C SHIV challenges. Vaccine 29, 5611-5622
21. Jiang, S., Rasmussen, R. A., Nolan, K. M., Frankel, F. R., Lieberman, J., McClure, H. M., Williams, K. M., Babu, U. S., Raybourne, R. B., Strobert, E., Ruprecht, R. M. (2007) Live attenuated Listeria monocytogenes expressing HIV Gag: immunogenicity in rhesus monkeys. Vaccine 25, 7470-7479
22. Xu, H., Wang, X., Pahar, B., Moroney-Rasmussen, T., Alvarez, X., Lackner, A. A., Veazey, R. S. (2010) Increased B7-H1 expression on dendritic cells correlates with programmed death 1 expression on T cells in simian immunodeficiency virus-infected macaques and may contribute to T cell dysfunction and disease progression. J. Immunol. 185, 7340-7348
23. Kuroda, M. J., Schmitz, J. E., Barouch, D. H., Craiu, A., Allen, T. M., Sette, A., Watkins, D. I., Forman, M. A., Letvin, N. L. (1998) Analysis of Gag-specific cytotoxic T lymphocytes in simian immunodeficiency virusinfected rhesus monkeys by cell staining with a tetrameric major histocompatibility complex class I-peptide complex. J. Exp. Med. 187, 1373-1381
24. Vanderford, T. H., Bleckwehl, C., Engram, J. C., Dunham, R. M., Klatt, N. R., Feinberg, M. B., Garber, D. A., Betts, M. R., Silvestri, G. (2011) Viral CTL escape mutants are generated in lymph nodes and subsequently become fixed in plasma and rectal mucosa during acute SIV infection of macaques. PLoS Pathog. 7, e1002048
25. Barber, D. L., Wherry, E. J., Masopust, D., Zhu, B., Allison, J. P., Sharpe, A. H., Freeman, G. J., Ahmed, R. (2006) Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439, 682-687
26. 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. (2007) Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity 27, 670-684
27. Petrovas, C., Price, D. A., Mattapallil, J., Ambrozak, D. R., Geldmacher, C., Cecchinato, V., Vaccari, M., Tryniszewska, E., Gostick, E., Roederer, M., Douek, D. C., Morgan, S. H., Davis, S. J., Franchini, G., Koup, R. A. (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
28. 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. (2009) Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat. Immunol. 10, 29-37
29. Kaur, A., Hale, C. L., Ramanujan, S., Jain, R. K., Johnson, R. P. (2000) Differential dynamics of CD4(+) and CD8(+) T-lymphocyte proliferation and activation in acute simian immunodeficiency virus infection. J. Virol. 74, 8413-8424
30. Sacha, J. B., Chung, C., Rakasz, E. G., Spencer, S. P., Jonas, A. K., Bean, A. T., Lee, W., Burwitz, B. J., Stephany, J. J., Loffredo, J. T., Allison, D. B., Adnan, S., Hoji, A., Wilson, N. A., Friedrich, T. C., Lifson, J. D., Yang, O. O., Watkins, D. I. (2007) Gag-specific CD8+ T lymphocytes recognize infected cells before AIDS-virus integration and viral protein expression. J. Immunol. 178, 2746-2754
31. Drake III D. R., Ream, R. M., Lawrence, C. W., Braciale, T. J. (2005) Transient loss of MHC class I tetramer binding after CD8+ T cell activation reflects altered T cell effector function. J. Immunol. 175, 1507-1515
32. Xu, H., Wang, X., Morici, L. A., Pahar, B., Veazey, R. S. (2011) Early divergent host responses in SHIVsf162P3 and SIVmac251 infected macaques correlate with control of viremia. PLoS One 6, e17965
33. Murayama, Y., Amano, A., Mukai, R., Shibata, H., Matsunaga, S., Takahashi, H., Yoshikawa, Y., Hayami, M., Noguchi, A. (1997) CD4 and CD8 expressions in African green monkey helper T lymphocytes: implication for resistance to SIV infection. Int. Immunol. 9, 843-851
34. Beaumier, C. M., Harris, L. D., Goldstein, S., Klatt, N. R., Whitted, S., McGinty, J., Apetrei, C., Pandrea, I., Hirsch, V. M., Brenchley, J. M. (2009) CD4 downregulation by memory CD4+ T cells in vivo renders African green monkeys resistant to progressive SIVagm infection. Nat. Med. 15, 879-885
35. Murayama, Y., Mukai, R., Inoue-Murayama, M., Yoshikawa, Y. (1999) An African green monkey lacking peripheral CD4 lymphocytes that retains helper T cell activity and coexists with SIVagm. Clin. Exp. Immunol. 117, 504-512
36. Veazey, R. S., Lifson, J. D., Schmitz, J. E., Kuroda, M. J., Piatak Jr., M., Pandrea, I., Purcell, J., Bohm, R., Blanchard, J., Williams, K. C., Lackner, A. A. (2003) Dynamics of simian immunodeficiency virus-specific cytotoxic T-cell responses in tissues. J. Med. Primatol. 32, 194-200
37. Tjernlund, A., Zhu, J., Laing, K., Diem, K., McDonald, D., Vazquez, J., Cao, J., Ohlen, C., McElrath, M. J., Picker, L. J., Corey, L. (2010) In situ detection of Gag-specific CD8+ cells in the GI tract of SIV infected Rhesus macaques. Retrovirology 7, 12
38. Hong, J. J., Reynolds, M. R., Mattila, T. L., Hage, A., Watkins, D. I., Miller, C. J., Skinner, P. J. (2009) Localized populations of CD8 MHC class I tetramer SIV-specific T cells in lymphoid follicles and genital epithelium. PLoS One 4, e4131
39. Feldmann, J., Leligdowicz, A., Jaye, A., Dong, T., Whittle, H., Rowland-Jones, S. L. (2009) Downregulation of the T-cell receptor by human immunodeficiency virus type 2 Nef does not protect against disease progression. J. Virol. 83, 12968-12972
40. Shin, H., Wherry, E. J. (2007) CD8 T cell dysfunction during chronic viral infection. Curr. Opin. Immunol. 19, 408-415
41. Velu, V., Kannanganat, S., Ibegbu, C., Chennareddi, L., Villinger, F., Freeman, G. J., Ahmed, R., Amara, R. R. (2007) Elevated expression levels of inhibitory receptor programmed death 1 on simian immunodeficiency virus-specific CD8 T cells during chronic infection but not after vaccination. J. Virol. 81, 5819-5828
42. Gallimore, A., Cranage, M., Cook, N., Almond, N., Bootman, J., Rud, E., Silvera, P., Dennis, M., Corcoran, T., Stott, J.(1995) Early suppression of SIV replication by CD8+ nef-specific cytotoxic T cells in vaccinated macaques. Nat. Med. 1, 1167-1173.