Protective HIV-specific CD8+ T cells evade T reg cell suppression

Nature Medicine

Volumn 17, Issue 8, 2011, Pages 989-995

  Elahi, Shokrollah ^a   Dinges, Warren L ^a,b   Lejarcegui, Nicholas ^a   Laing, Kerry J ^c   Collier, Ann C ^d   Koelle, David M ^c,d,e   McElrath, M Juliana ^c,d   Horton, Helen ^a,d  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b Infectious Diseases Research Institute   (United States)

^c Fred Hutchinson Cancer Research Center   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

^e BENAROYA RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ECALECTIN; EPITOPE; GRANZYME B; HLA B27 ANTIGEN; HLA B57 ANTIGEN; IMMUNOGLOBULIN; T CELL IMMUNOGLOBULIN DOMAIN AND MUCIN DOMAIN 3; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; CD8+ T LYMPHOCYTE; CELL KILLING; CLINICAL ARTICLE; DISEASE COURSE; FEMALE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MALE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SENSITIVITY ANALYSIS;

CD8-POSITIVE T-LYMPHOCYTES; CELL DEATH; EPITOPE MAPPING; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HIV INFECTIONS; HIV-1; HLA-B ANTIGENS; HLA-B27 ANTIGEN; HUMANS; MALE; MEMBRANE PROTEINS; POLYMORPHISM, SINGLE NUCLEOTIDE; RNA INTERFERENCE; RNA, SMALL INTERFERING; T-LYMPHOCYTES, REGULATORY;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 79961160736     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2422     Document Type: Article

References (41)

1. McMichael, A.J. & Rowland-Jones, S.L. Cellular immune responses to HIV. Nature 410, 980-987 (2001). (Pubitemid 32335849)
2. Kaslow, R.A. et al. Influence of combinations of human major histocompatibility complex genes on the course of HIV-1 infection. Nat. Med. 2, 405-411 (1996). (Pubitemid 26193012)
3. Carrington, M. et al. HLA and HIV-1: heterozygote advantage and B*35-Cw*04 disadvantage. Science 283, 1748-1752 (1999).
4. Carrington, M. & O'Brien, S.J. The influence of HLA genotype on AIDS. Annu. Rev. Med. 54, 535-551 (2003). (Pubitemid 37386411)
5. Dinges, W.L. et al. Virus-specific CD8+ T cell responses better define HIV disease progression than HLA genotype. J. Virol. 84, 4461-4468 (2010).
6. Migueles, S.A. et al. HIV-specific CD8+ T cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nat. Immunol. 3, 1061-1068 (2002). (Pubitemid 35363659)
7. Lichterfeld, M. et al. Loss of HIV-1-specific CD8+ T cell proliferation after acute HIV-1 infection and restoration by vaccine-induced HIV-1-specific CD4+ T cells. J. Exp. Med. 200, 701-712 (2004). (Pubitemid 39299457)
8. Horton, H. et al. Preservation of T cell proliferation restricted by protective HLA alleles is critical for immune control of HIV-1 infection. J. Immunol. 177, 7406-7415 (2006). (Pubitemid 44715111)
9. Vila, J., Isaacs, J.D. & Anderson, A.E. Regulatory T cells and autoimmunity. Curr. Opin. Hematol. 16, 274-279 (2009).
10. Galgani, M., Di Giacomo, A., Matarese, G. & La Cava, A. The Yin and Yang of CD4+ regulatory T cells in autoimmunity and cancer. Curr. Med. Chem. 16, 4626-4631 (2009).
11. Zhu, C. et al. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat. Immunol. 6, 1245-1252 (2005). (Pubitemid 43045636)
12. Koguchi, K. et al. Dysregulated T cell expression of TIM3 in multiple sclerosis. J. Exp. Med. 203, 1413-1418 (2006). (Pubitemid 43877603)
13. Li, X.C. & Turka, L.A. An update on regulatory T cells in transplant tolerance and rejection. Nat. Rev. Nephrol. 6, 577-583 (2010).
14. Jones, R.B. et al. Tim-3 expression defines a novel population of dysfunctional T cells with highly elevated frequencies in progressive HIV-1 infection. J. Exp. Med. 205, 2763-2779 (2008).
15. Neumann-Haefelin, C. et al. Dominant influence of an HLA-B27 restricted CD8+ T cell response in mediating HCV clearance and evolution. Hepatology 43, 563-572 (2006).
16. Mathieu, A. et al. The interplay between the geographic distribution of HLA-B27 alleles and their role in infectious and autoimmune diseases: a unifying hypothesis. Autoimmun. Rev. 8, 420-425 (2009).
17. Henseler, T. Genetics of psoriasis. Arch. Dermatol. Res. 290, 463-476 (1998). (Pubitemid 28468389)
18. Migueles, S.A. & Connors, M. Frequency and function of HIV-specific CD8(+) T cells. Immunol. Lett. 79, 141-150 (2001). (Pubitemid 32938219)
19. Migueles, S.A. et al. Lytic granule loading of CD8+ T cells is required for HIV-infected cell elimination associated with immune control. Immunity 29, 1009-1021 (2008).
20. Wang, F. et al. Tim-3-Galectin-9 pathway involves the suppression induced by CD4+CD25+ regulatory T cells. Immunobiology 214, 342-349 (2009).
21. Francisco, L.M., Sage, P.T. & Sharpe, A.H. The PD-1 pathway in tolerance and autoimmunity. Immunol. Rev. 236, 219-242 (2010).
22. Sabatos, C.A. et al. Interaction of Tim-3 and Tim-3 ligand regulates T helper type 1 responses and induction of peripheral tolerance. Nat. Immunol. 4, 1102-1110 (2003). (Pubitemid 37428038)
23. Barber, D.L. et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439, 682-687 (2006). (Pubitemid 43237609)
24. Sakuishi, K. et al. Targeting Tim-3 and PD-1 pathways to reverse T cell exhaustion and restore anti-tumor immunity. J. Exp. Med. 207, 2187-2194 (2010).
25. Wehler, T.C. et al. Rapid identification and sorting of viable virus-reactive CD4+ and CD8+ T cells based on antigen-triggered CD137 expression. J. Immunol. Methods 339, 23-37 (2008).
26. Chabot, S. et al. Regulation of galectin-9 expression and release in Jurkat T cell line cells. Glycobiology 12, 111-118 (2002). (Pubitemid 34428934)
27. Ashley, C.W. & Baecher-Allan, C. Cutting Edge: Responder T cells regulate human DR+ effector regulatory T cell activity via granzyme B. J. Immunol. 183, 4843-4847 (2009).
28. Andersson, J. et al. The prevalence of regulatory T cells in lymphoid tissue is correlated with viral load in HIV-infected patients. J. Immunol. 174, 3143-3147 (2005). (Pubitemid 40354012)
29. Nilsson, J. et al. HIV-1-driven regulatory T-cell accumulation in lymphoid tissues is associated with disease progression in HIV/AIDS. Blood 108, 3808-3817 (2006). (Pubitemid 44864563)
30. Tsunemi, S. et al. Relationship of CD4+CD25+ regulatory T cells to immune status in HIV-infected patients. AIDS 19, 879-886 (2005). (Pubitemid 40834930)
31. Eggena, M.P. et al. Depletion of regulatory T cells in HIV infection is associated with immune activation. J. Immunol. 174, 4407-4414 (2005). (Pubitemid 40396024)
32. Abrams, D. et al. Interleukin-2 therapy in patients with HIV infection. N. Engl. J. Med. 361, 1548-1559 (2009).
33. Weiss, L. et al. In vivo expansion of naive and activated CD4+CD25+FOXP3+ regulatory T cell populations in interleukin-2-treated HIV patients. Proc. Natl. Acad. Sci. USA 107, 10632-10637 (2010).
34. Almeida, J.R. et al. Superior control of HIV-1 replication by CD8+ T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J. Exp. Med. 204, 2473-2485 (2007). (Pubitemid 47529331)
35. Antoniou, A.N., Ford, S., Taurog, J.D., Butcher, G.W. & Powis, S.J. Formation of HLA-B27 homodimers and their relationship to assembly kinetics. J. Biol. Chem. 279, 8895-8902 (2004). (Pubitemid 38295950)
36. Xing, S. et al. Increased turnover of FoxP3high regulatory T cells is associated with hyperactivation and disease progression of chronic HIV-1 infection. J. Acquir. Immune Defic. Syndr. 54, 455-462 (2010).
37. Sabbagh, L. et al. The selective increase in caspase-3 expression in effector but not memory T cells allows susceptibility to apoptosis. J. Immunol. 173, 5425-5433 (2004). (Pubitemid 39392126)
38. Feng, B.J. et al. Multiple Loci within the major histocompatibility complex confer risk of psoriasis. PLoS Genet. 5, e1000606 (2009).
39. Laing, K.J. et al. Diversity in CD8+ T cell function and epitope breadth among persons with genital herpes. J. Clin. Immunol. 30, 703-722 (2010).
40. Horton, H. et al. Induction of human immunodeficiency virus type 1 (HIV-1)-specific T-cell responses in HIV vaccine trial participants who subsequently acquire HIV-1 infection. J. Virol. 80, 9779-9788 (2006). (Pubitemid 44435652)
41. Horton, H. et al. Optimization and validation of an 8-color intracellular cytokine staining (ICS) assay to quantify antigen-specific T cells induced by vaccination. J. Immunol. Methods 323, 39-54 (2007). (Pubitemid 46722712)