Critical loss of the balance between Th17 and T regulatory cell populations in pathogenic SIV infection

PLoS Pathogens

Volumn 5, Issue 2, 2009, Pages

  Favre, David ^a   Lederer, Sharon ^b   Kanwar, Bittoo ^a   Ma, Zhong Min ^c   Proll, Sean ^b   Kasakow, Zeljka ^a   Mold, Jeff ^a   Swainson, Louise ^a   Barbour, Jason D ^a   Baskin, Carole R ^b   Palermo, Robert ^b   Pandrea, Ivona ^d   Miller, Christopher J ^c   Katze, Michael G ^b   McCune, Joseph M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17; TRANSCRIPTION FACTOR FOXP3; CYTOKINE; FORKHEAD TRANSCRIPTION FACTOR; VIRUS RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL LOSS; CELL POPULATION; CERCOPITHECIDAE; CONTROLLED STUDY; INFLAMMATION; LYMPHOID ORGAN; MACACA; MALE; MUCOSA; NONHUMAN; REGULATORY T LYMPHOCYTE; SIMIAN IMMUNODEFICIENCY VIRUS; T CELL DEPLETION; T LYMPHOCYTE ACTIVATION; TH17 CELL; VIRUS INFECTION; VIRUS LOAD; ANALYSIS OF VARIANCE; ANIMAL; CERCOPITHECUS; COLON; DNA MICROARRAY; FLOW CYTOMETRY; HELPER CELL; IMMUNOLOGY; LYMPH NODE; LYMPHOCYTE ACTIVATION; METABOLISM; MONKEY DISEASE; NONPARAMETRIC TEST; T LYMPHOCYTE SUBPOPULATION; VIROLOGY;

CERCOPITHECUS AETHIOPS; MACACA; PRIMATES; SIMIAN IMMUNODEFICIENCY VIRUS;

ANALYSIS OF VARIANCE; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CERCOPITHECUS AETHIOPS; COLON; CYTOKINES; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; INTERLEUKIN-17; LYMPH NODES; LYMPHOCYTE ACTIVATION; MACACA NEMESTRINA; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, VIRAL; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; STATISTICS, NONPARAMETRIC; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY; VIRAL LOAD;

EID: 61449115882     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000295     Document Type: Article

References (70)

1. Hazenberg MD, Hamann D, Schuitemaker H, Miedema F (2000) T cell depletion in HIV-1 infection: how CD4+ T cells go out of stock. Nat Immunol 1: 285-289.
2. McCune JM (2001) The dynamics of CD4+ T-cell depletion in HIV disease. Nature 410: 974-979.
3. Grossman Z, Meier-Schellersheim M, Sousa AE, Victorino RM, Paul WE (2002) CD4+ T-cell depletion in HIV infection: are we closer to understanding the cause? Nat Med 8: 319-323.
4. Douek DC, Picker LJ, Koup RA (2003) T cell dynamics in HIV-1 infection. Annu Rev Immunol 21: 265-304.
5. Heeney JL, Dalgleish AG, Weiss RA (2006) Origins of HIV and the evolution of resistance to AIDS. Science 313: 462-466.
6. Beer B, Denner J, Brown CR, Norley S, zur Megede J, et al. (1998) Simian immunodeficiency virus of African green monkeys is apathogenic in the newborn natural host. J Acquir Immune Defic Syndr Hum Retrovirol 18: 210-220.
7. Goldstein S, Ourmanov I, Brown CR, Plishka R, Buckler-White A, et al. (2005) Plateau levels of viremia correlate with the degree of CD4+-T-cell loss in simian immunodeficiency virus SIVagm-infected pigtailed macaques: variable pathogenicity of natural SIVagm isolates. J Virol 79: 5153-5162.
8. Lackner AA, Veazey RS (2007) Current concepts in AIDS pathogenesis: insights from the SIV/macaque model. Annu Rev Med 58: 461-476.
9. Broussard SR, Staprans SI, White R, Whitehead EM, Feinberg MB, et al. (2001) Simian immunodeficiency virus replicates to high levels in naturally infected African green monkeys without inducing immunologic or neurologic disease. J Virol 75: 2262-2275.
10. Silvestri G, Sodora DL, Koup RA, Paiardini M, O'Neil SP, et al. (2003) Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity 18: 441-452.
11. Dunham R, Pagliardini P, Gordon S, Sumpter B, Engram J, et al. (2006) The AIDS resistance of naturally SIV-infected sooty mangabeys is independent of cellular immunity to the virus. Blood 108: 209-217.
12. Wang Z, Metcalf B, Ribeiro RM, McClure H, Kaur A (2006) Th-1-type cytotoxic CD8+ T-lymphocyte responses to simian immunodeficiency virus (SIV) are a consistent feature of natural SIV infection in sooty mangabeys. J Virol 80: 2771-2783.
13. Giorgi JV, Hultin LE, McKeating JA, Johnson TD, Owens B, et al. (1999) Shorter survival in advanced human immunodeficiency virus type 1 infection is more closely associated with T lymphocyte activation than with plasma virus burden or virus chemokine coreceptor usage. J Infect Dis 179: 859-870.
14. Sousa AE, Carneiro J, Meier-Schellersheim M, Grossman Z, Victorino RM (2002) CD4 T cell depletion is linked directly to immune activation in the pathogenesis of HIV-1 and HIV-2 but only indirectly to the viral load. J Immunol 169: 3400-3406.
15. Deeks SG, Kitchen CM, Liu L, Guo H, Gascon R, et al. (2004) Immune activation set point during early HIV infection predicts subsequent CD4+ T-cell changes independent of viral load. Blood 104: 942-947.
16. Veazey RS, DeMaria M, Chalifoux LV, Shvetz DE, Pauley DR, et al. (1998) Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science 280: 427-431.
17. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, et al. (2006) Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 12: 1365-1371.
18. Pandrea IV, Gautam R, Ribeiro RM, Brenchley JM, Butler IF, et al. (2007) Acute loss of intestinal CD4+ T cells is not predictive of simian immunodeficiency virus virulence. J Immunol 179: 3035-3046.
19. Gordon SN, Klatt NR, Bosinger SE, Brenchley JM, Milush JM, et al. (2007) Severe depletion of mucosal CD4+ T cells in AIDS-free simian immunodeficiency virus-infected sooty mangabeys. J Immunol 179: 3026-3034.
20. Fauci AS (1996) Host factors and the pathogenesis of HIV-induced disease. Nature 384: 529-534.
21. Weaver CT, Harrington LE, Mangan PR, Gavrieli M, Murphy KM (2006) Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity 24: 677-688.
22. Mucida D, Park Y, Kim G, Turovskaya O, Scott I, et al. (2007) Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317: 256-260.
23. Furuzawa-Carballeda J, Vargas-Rojas MI, Cabral AR (2007) Autoimmune inflammation from the Th17 perspective. Autoimmun Rev 6: 169-175.
24. Ouyang W, Kolls JK, Zheng Y (2008) The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28: 454-467.
25. Diop OM, Gueye A, Dias-Tavares M, Kornfeld C, Faye A, et al. (2000) High levels of viral replication during primary simian immunodeficiency virus SIVagm infection are rapidly and strongly controlled in African green monkeys. J Virol 74: 7538-7547.
26. Silvestri G, Paiardini M, Pandrea I, Lederman MM, Sodora DL (2007) Understanding the benign nature of SIV infection in natural hosts. J Clin Invest 117: 3148-3154.
27. Kornfeld C, Ploquin MJ, Pandrea I, Faye A, Onanga R, et al. (2005) Antiinflammatory profiles during primary SIV infection in African green monkeys are associated with protection against AIDS. J Clin Invest 115: 1082-1091.
28. Goldstein S, Brown CR, Ourmanov I, Pandrea I, Buckler-White A, et al. (2006) Comparison of simian immunodeficiency virus SIVagmVer replication and CD4+ T-cell dynamics in vervet and sabaeus African green monkeys. J Virol 80: 4868-4877.
29. Pandrea I, Apetrei C, Dufour J, Dillon N, Barbercheck J, et al. (2006) Simian immunodeficiency virus SIVagm.sab infection of Caribbean African green monkeys: a new model for the study of SIV pathogenesis in natural hosts. J Virol 80: 4858-4867.
30. Zheng Y, Valdez PA, Danilenko DM, Hu Y, Sa SM, et al. (2008) Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med.
31. Acosta-Rodriguez EV, Rivino L, Geginat J, Jarrossay D, Gattorno M, et al. (2007) Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat Immunol 8: 639-646.
32. Lim HW, Lee J, Hillsamer P, Kim CH (2008) Human Th17 cells share major trafficking receptors with both polarized effector T cells and FOXP3+ regulatory T cells. J Immunol 180: 122-129.
33. Kolls JK, Linden A (2004) Interleukin-17 family members and inflammation. Immunity 21: 467-476.
34. Belkaid Y (2007) Regulatory T cells and infection: a dangerous necessity. Nat Rev Immunol 7: 875-888.
35. Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, et al. (2006) The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126: 1121-1133.
36. Hartigan-O'Connor DJ, Abel K, McCune JM (2007) Suppression of SIV-specific CD4+ T cells by infant but not adult macaque regulatory T cells: implications for SIV disease progression. J Exp Med 204: 2679-2692.
37. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, et al. (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441: 235-238.
38. Gavin MA, Rasmussen JP, Fontenot JD, Vasta V, Manganiello VC, et al. (2007) Foxp3-dependent programme of regulatory T-cell differentiation. Nature 445: 771-775.
39. Sakaguchi S, Powrie F (2007) Emerging challenges in regulatory T cell function and biology. Science 317: 627-629.
40. Chen X, Vodanovic-Jankovic S, Johnson B, Keller M, Komorowski R, et al. (2007) Absence of regulatory T cell control of TH1 and TH17 cells is responsible for the autoimmune-mediated pathology in chronic graft versus host disease. Blood.
41. Kinter AL, Hennessey M, Bell A, Kern S, Lin Y, et al. (2004) CD25(+)CD4(+) regulatory T cells from the peripheral blood of asymptomatic HIV-infected individuals regulate CD4(+) and CD8(+) HIV-specific T cell immune responses in vitro and are associated with favorable clinical markers of disease status. J Exp Med 200: 331-343.
42. Aandahl EM, Michaelsson J, Moretto WJ, Hecht FM, Nixon DF (2004) Human CD4+ CD25+ regulatory T cells control T-cell responses to human immunodeficiency virus and cytomegalovirus antigens. J Virol 78: 2454-2459.
43. Nilsson J, Boasso A, Velilla PA, Zhang R, Vaccari M, et al. (2006) HIV-1-driven regulatory T-cell accumulation in lymphoid tissues is associated with disease progression in HIV/AIDS. Blood 108: 3808-3817.
44. Bluestone JA, Abbas AK (2003) Natural versus adaptive regulatory T cells. Nat Rev Immunol 3: 253-257.
45. von Boehmer H (2005) Mechanisms of suppression by suppressor T cells. Nat Immunol 6: 338-344.
46. Belkaid Y, Rouse BT (2005) Natural regulatory T cells in infectious disease. Nat Immunol 6: 353-360.
47. Groux H, Torpier G, Monte D, Mouton Y, Capron A, et al. (1992) Activation-induced death by apoptosis in CD4+ T cells from human immunodeficiency virus-infected asymptomatic individuals. J Exp Med 175: 331-340.
48. Meyaard L, Otto SA, Jonker RR, Mijnster MJ, Keet RP, et al. (1992) Programmed death of T cells in HIV-1 infection. Science 257: 217-219.
49. Munn DH, Sharma MD, Lee JR, Jhaver KG, Johnson TS, et al. (2002) Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science 297: 1867-1870.
50. Toscano MA, Bianco GA, Ilarregui JM, Croci DO, Correale J, et al. (2007) Differential glycosylation of TH1, TH2 and TH-17 effector cells selectively regulates susceptibility to cell death. Nat Immunol 8: 825-834.
51. Garin MI, Chu CC, Golshayan D, Cernuda-Morollon E, Wait R, et al. (2007) Galectin-1: a key effector of regulation mediated by CD4+CD25+ T cells. Blood 109: 2058-2065.
52. Banda NK, Bernier J, Kurahara DK, Kurrle R, Haigwood N, et al. (1992) Crosslinking CD4 by human immunodeficiency virus gp120 primes T cells for activation-induced apoptosis. J Exp Med 176: 1099-1106.
53. Herbeuval JP, Grivel JC, Boasso A, Hardy AW, Chougnet C, et al. (2005) CD4+ T-cell death induced by infectious and noninfectious HIV-1: role of type 1 interferon-dependent, TRAIL/DR5-mediated apoptosis. Blood 106: 3524-3531.
54. Boasso A, Herbeuval JP, Hardy AW, Anderson SA, Dolan MJ, et al. (2007) HIV inhibits CD4+ T-cell proliferation by inducing indoleamine 2,3-dioxygenase in plasmacytoid dendritic cells. Blood 109: 3351-3359.
55. Ye P, Garvey PB, Zhang P, Nelson S, Bagby G, et al. (2001) Interleukin-17 and lung host defense against Klebsiella pneumoniae infection. Am J Respir Cell Mol Biol 25: 335-340.
56. Mangan PR, Harrington LE, O'Quinn DB, Helms WS, Bullard DC, et al. (2006) Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441: 231-234.
57. Kleinschek MA, Muller U, Brodie SJ, Stenzel W, Kohler G, et al. (2006) IL-23 enhances the inflammatory cell response in Cryptococcus neoformans infection and induces a cytokine pattern distinct from IL-12. J Immunol 176: 1098-1106.
58. Higgins SC, Jarnicki AG, Lavelle EC, Mills KH (2006) TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J Immunol 177: 7980-7989.
59. Khader SA, Bell GK, Pearl JE, Fountain JJ, Rangel-Moreno J, et al. (2007) IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat Immunol 8: 369-377.
60. Scriba TJ, Kalsdorf B, Abrahams DA, Isaacs F, Hofmeister J, et al. (2008) Distinct, specific IL-17- and IL-22-producing CD4+ T cell subsets contribute to the human anti-mycobacterial immune response. J Immunol 180: 1962-1970.
61. Rice L, Orlow D, Ceonzo K, Stahl GL, Tzianabos AO, et al. (2005) CpG oligodeoxynucleotide protection in polymicrobial sepsis is dependent on interleukin-17. J Infect Dis 191: 1368-1376.
62. Raffatellu M, Santos RL, Verhoeven DE, George MD, Wilson RP, et al. (2008) Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat Med 14: 421-428.
63. Cecchinato V, Trindade CJ, Laurence A, Heraud JM, Brenchley JM, et al. (2008) Altered balance between Th17 and Th1 cells at mucosal sites predicts AIDS progression in simian immunodeficiency virus-infected macaques. Mucosal Immunology 1: 279-288.
64. Brenchley JM, Paiardini M, Knox KS, Asher AI, Cervasi B, et al. (2008) Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 112: 2826-2835.
65. van Beelen AJ, Zelinkova Z, Taanman-Kueter EW, Muller FJ, Hommes DW, et al. (2007) Stimulation of the Intracellular Bacterial Sensor NOD2 Programs Dendritic Cells to Promote Interleukin-17 Production in Human Memory T Cells. Immunity.
66. Denning TL, Wang YC, Patel SR, Williams IR, Pulendran B (2007) Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol 8: 1086-1094.
67. LeibundGut-Landmann S, Gross O, Robinson MJ, Osorio F, Slack EC, et al. (2007) Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat Immunol 8: 630-638.
68. Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F (2007) Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol 8: 942-949.
69. Grossman Z, Meier-Schellersheim M, Paul WE, Picker LJ (2006) Pathogenesis of HIV infection: what the virus spares is as important as what it destroys. Nat Med 12: 289-295.
70. Mandl JN, Barry AP, Vanderford TH, Kozyr N, Chavan R, et al. (2008) Divergent TLR7 and TLR9 signaling and type I interferon production distinguish pathogenic and nonpathogenic AIDS virus infections. Nat Med 14: 1077-1087.