HIV-1 infection is characterized by profound depletion of CD161+ Th17 cells and gradual decline in regulatory T cells

AIDS

Volumn 24, Issue 4, 2010, Pages 491-502

  Prendergast, Andrew ^a,b   Prado, Julia G ^a   Kang, Yu Hoi ^a   Chen, Fabian ^c   Riddell, Lynn A ^d   Luzzi, Graz ^e   Goulder, Philip ^a   Klenerman, Paul ^a,b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^c ROYAL BERKSHIRE NHS FOUNDATION TRUST   (United Kingdom)

^d NORTHAMPTON GENERAL HOSPITAL   (United Kingdom)

^e WYCOMBE HOSPITAL   (United Kingdom)

Author keywords

CD161; CD4; HIV; Pathogenesis; Th17

Indexed keywords

ANTIGEN P24; CD161 ANTIGEN; CD38 ANTIGEN; HLA DR ANTIGEN; INTERLEUKIN 17; TRANSCRIPTION FACTOR FOXP3;

ANTIGEN EXPRESSION; ARTICLE; CD25+ T LYMPHOCYTE; CD3+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ISOLATION; CONTROLLED STUDY; DISEASE COURSE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; LYMPHOCYTE DEPLETION; LYMPHOCYTE SUBPOPULATION; MAJOR CLINICAL STUDY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TH17 CELL; VIRUS REPLICATION;

CD4-POSITIVE T-LYMPHOCYTES; DISEASE PROGRESSION; GASTRIC MUCOSA; HIV INFECTIONS; HIV-1; HUMANS; IMMUNITY, CELLULAR; LYMPHOCYTE ACTIVATION; PHENOTYPE; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 77649250683     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e3283344895     Document Type: Article

References (52)

1. Brenchley JM, Schacker TW, Ruff LE, Price DA, Taylor JH, Beilman GJ, et al. CD4R T cell depletion during all stages of HIV disease occurs predominantly in the gastrointestinal tract. J Exp Med 2004; 200:749-759.
2. Guadalupe M, Reay E, Sankaran S, Prindiville T, Flamm J, McNeil A, Dandekar S. Severe CD4R T-cell depletion in gut lymphoid tissue during primary human immunodeficiency virus type 1 infection and substantial delay in restoration following highly active antiretroviral therapy. J Virol 2003; 77:11708-11717.
3. Mehandru S, Poles MA, Tenner-Racz K, Horowitz A, Hurley A, Hogan C, et al. Primary HIV-1 infection is associated with preferential depletion of CD4R T lymphocytes from effector sites in the gastrointestinal tract. J Exp Med 2004; 200:761-770.
4. Deeks SG, Kitchen CM, Liu L, Guo H, Gascon R, Narvaez AB, et al. Immune activation set point during early HIV infection predicts subsequent CD4R T-cell changes independent of viral load. Blood 2004; 104:942-947.
5. Giorgi JV, Hultin LE, McKeating JA, Johnson TD, Owens B, Jacobson LP, et al. 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 1999; 179:859-870.
6. Brenchley JM, Price DA, Schacker TW, Asher TE, Silvestri G, Rao S, et al. Microbial translocation is a cause of systemic immune activation in chronic HIV infection. Nat Med 2006; 12:1365-1371.
7. Mosmann TR, Coffman RL. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol 1989; 7:145-173.
8. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immu-nologic 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 1995; 155:1151-1164.
9. Thornton AM, Shevach EM. CD4RCD25R immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med 1998; 188:287-296.
10. Bettelli E, Korn T, Oukka M, Kuchroo VK. Induction and effector functions of T(H)17 cells. Nature 2008; 453:1051-1057.
11. Baecher-Allan C, Brown JA, Freeman GJ, Hafler DA. CD4RCD25high regulatory cells in human peripheral blood. J Immunol 2001; 167:1245-1253.
12. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4RCD25R regulatory T cells. Nat Immunol 2003; 4:330-336.
13. Acosta-Rodriguez EV, Rivino L, Geginat J, Jarrossay D, Gattorno M, Lanzavecchia A, et al. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat Immunol 2007; 8:639-646.
14. Annunziato F, Cosmi L, Santarlasci V, Maggi L, Liotta F, Mazzinghi B, et al. Phenotypic and functional features of human Th17 cells. J Exp Med 2007; 204:1849-1861.
15. Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, Lafaille JJ, et al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17R T helper cells. Cell 2006; 126:1121-1133.
16. Wilson NJ, Boniface K, Chan JR, McKenzie BS, Blumenschein WM, Mattson JD, et al. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol 2007; 8:950-957.
17. Cosmi L, De Palma R, Santarlasci V, Maggi L, Capone M, Frosali F, et al. Human interleukin 17-producing cells originate from a CD161RCD4R T cell precursor. J Exp Med 2008; 205:1903-1916.
18. Kleinschek MA, Boniface K, Sadekova S, Grein J, Murphy EE, Turner SP, et al. Circulating and gut-resident human Th17 cells express CD161 and promote intestinal inflammation. J Exp Med 2009; 206:525-534.
19. Brenchley JM, Paiardini M, Knox KS, Asher AI, Cervasi B, Asher TE, et al. Differential Th17 CD4 T-cell depletion in pathogenic and nonpathogenic lentiviral infections. Blood 2008; 112: 2826-2835.
20. Favre D, Lederer S, Kanwar B, Ma ZM, Proll S, Kasakow Z, et al. Critical loss of the balance between Th17 and T regulatory cell populations in pathogenic SIV infection. PLoS Pathog 2009; 5:e1000295.
21. Aandahl EM, Michaelsson J, Moretto WJ, Hecht FM, Nixon DF. Human CD4R CD25R regulatory T cells control T-cell responses to human immunodeficiency virus and cytomegalo-virus antigens. J Virol 2004; 78:2454-2459.
22. Andersson J, Boasso A, Nilsson J, Zhang R, Shire NJ, Lindback S, et al. The prevalence of regulatory T cells in lymphoid tissue is correlated with viral load in HIV-infected patients. J Immunol 2005; 174:3143-3147.
23. Cao W, Jamieson BD, Hultin LE, Hultin PM, Detels R. Regulatory T cell expansion and immune activation during untreated HIV type 1 infection are associated with disease progression. AIDS Res Hum Retroviruses 2009; 25:183-191.
24. Epple HJ, Loddenkemper C, Kunkel D, Troger H, Maul J, Moos V, et al. Mucosal but not peripheral FOXP3R regulatory T cells are highly increased in untreated HIV infection and normalize after suppressive HAART. Blood 2006; 108:3072-3078.
25. Nilsson J, Boasso A, Velilla PA, Zhang R, Vaccari M, Franchini G, et al. HIV-1-driven regulatory T-cell accumulation in lymphoid tissues is associated with disease progression in HIV/AIDS. Blood 2006; 108:3808-3817.
26. Weiss L, Donkova-Petrini V, Caccavelli L, Balbo M, Carbonneil C, LevyY.Human immunodeficiency virus-driven expansion of CD4RCD25R regulatory T cells, which suppress HIV-specific CD4 T-cell responses in HIV-infected patients. Blood 2004; 104:3249-3256.
27. Apoil PA, Puissant B, Roubinet F, Abbal M, Massip P, Blancher A. FOXP3 mRNA levels are decreased in peripheral blood CD4R lymphocytes from HIV-positive patients. J Acquir Immune Defic Syndr 2005; 39:381-385.
28. Chase AJ, Yang HC, Zhang H, Blankson JN, Siliciano RF. Preservation of FoxP3R regulatory T cells in the peripheral blood of human immunodeficiency virus type 1-infected elite suppressors correlates with low CD4R T-cell activation. J Virol 2008; 82:8307-8315.
29. Eggena MP, Barugahare B, Jones N, Okello M, Mutalya S, Kityo C, et al. Depletion of regulatory T cells in HIV infection is associated with immune activation. J Immunol 2005; 174: 4407-4414.
30. Jiao Y, Fu J, Xing S, Fu B, Zhang Z, Shi M, et al. The decrease of regulatory T cells correlates with excessive activation and apoptosis of CD8(R) T cells in HIV-1-infected typical progres-sors, but not in long-term nonprogressors. Immunology 2008; 128:e366-e375.
31. Kinter AL, Hennessey M, Bell A, Kern S, Lin Y, Daucher M, et al. CD25(R)CD4(R) regulatory T cells from the peripheral blood of asymptomatic HIV-infected individuals regulate CD4(R) and CD8(R) HIV-specific T cell immune responses in vitro and are associated with favorable clinical markers of disease status. J Exp Med 2004; 200:331-343.
32. Ndhlovu LC, Loo CP, Spotts G, Nixon DF, Hecht FM. FOXP3 expressing CD127lo CD4R T cells inversely correlate with CD38R CD8R T cell activation levels in primary HIV-1 infection. J Leukoc Biol 2008; 83:254-262.
33. Goulder PJ, Brander C, Annamalai K, Mngqundaniso N, Govender U, Tang Y, et al. Differential narrow focusing of immunodominant human immunodeficiency virus gag-specific cytotoxic T-lymphocyte responses in infected African and caucasoid adults and children. J Virol 2000; 74:5679-5690.
34. Lim HW, Lee J, Hillsamer P, Kim CH. Human Th17 cells share major trafficking receptors with both polarized effector T cells and FOXP3R regulatoryTcells. JImmunol 2008; 180:122-129.
35. Douek DC, Picker LJ, Koup RA. T cell dynamics in HIV-1 infection. Annu Rev Immunol 2003; 21:265-304.
36. Maek ANW, Buranapraditkun S, Klaewsongkram J, Ruxrung-tham K. Increased interleukin-17 production both in helper T cell subset Th17 and CD4-negative T cells in human immunodeficiency virus infection. Viral Immunol 2007; 20:66-75.
37. Redd AD, Dabitao D, Bream JH, Charvat B, Laeyendecker O, Kiwanuka N, et al. Microbial translocation, the innate cytokine response, and HIV-1 disease progression in Africa. Proc Natl Acad Sci USA 2009; 106:6718-6723.
38. Rowan AG, Fletcher JM, Ryan EJ, Moran B, Hegarty JE, O'Farrelly C, Mills KH. Hepatitis C virus-specific Th17 cells are suppressed by virus-induced TGF-beta. J Immunol 2008; 181:4485-4494.
39. Yue FY, MerchantA,Kovacs CM, LoutfyM, PersadD,Ostrowski MA. Virus-specific interleukin-17-producing CD4R T cells are detectable in early human immunodeficiency virus type 1 infection. J Virol 2008; 82:6767-6771.
40. Ndhlovu LC, Chapman JM, Jha AR, Snyder-Cappione JE, Pagan M, Leal FE, et al. Suppression of HIV-1 plasma viral load below detection preserves IL-17 producing T cells in HIV-1 infection. AIDS 2008; 22:990-992.
41. Roark CL, Simonian PL, Fontenot AP, Born WK, O'Brien RL. gd T cells: an important source of IL-17. Curr Opin Immunol 2008; 20:353-357.
42. Fenoglio D, Poggi A, Catellani S, Battaglia F, Ferrera A, Setti M, et al. V{delta}1 T lymphocytes producing IFN{gamma} and IL-17 are expanded in HIV-1 infected patients and respond to Candida albicans. Blood 2009; 113:6611-6618.
43. Casetti R, Agrati C, Wallace M, Sacchi A, Martini F, Martino A, et al. Cutting edge: TGV-beta1 and IL-15 induce FOXP3R gammadelta regulatory T cells in the presence of antigen stimulation. J Immunol 2009; 183:3574-3577.
44. Egan PJ, Carding SR. Downmodulation of the inflammatory response to bacterial infection by gammadelta T cells cytotoxic for activated macrophages. J Exp Med 2000; 191:2145-2158.
45. Lahn M, Kanehiro A, Takeda K, Joetham A, Schwarze J, Kohler G, et al. Negative regulation of airway responsiveness that is dependent on gammadelta T cells and independent of alpha-beta T cells. Nat Med 1999; 5:1150-1156.
46. Hamada H, Garcia-Hernandez Mde L, Reome JB, Misra SK, Strutt TM, McKinstry KK, et al. Tc17, a unique subset of CD8 T cells that can protect against lethal influenza challenge. J Immunol 2009; 182:3469-3481.
47. Kondo T, Takata H, Matsuki F, Takiguchi M. Cutting edge: phenotypic characterization and differentiation of human CD8R T cells producing IL-17. J Immunol 2009; 182:1794-1798.
48. Kornfeld C, Ploquin MJ, Pandrea I, Faye A, Onanga R, Apetrei C, et al. Antiinflammatory profiles during primary SIV infection in African green monkeys are associated with protection against AIDS. J Clin Invest 2005; 115:1082-1091.
49. Oswald-Richter K, Grill SM, Shariat N, Leelawong M, Sundrud MS, Haas DW, Unutmaz D. HIV infection of naturally occurring and genetically reprogrammed human regulatory T-cells. PLoS Biol 2004; 2:E198.
50. de St Groth BF, Landay AL. Regulatory T cells in HIV infection: pathogenic or protective participants in the immune response? AIDS 2008; 22:671-683.
51. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006; 441:235-238.
52. Carlson MJ, West ML, Coghill JM, Panoskaltsis-Mortari A, Blazar BR, Serody JS. In vitro-differentiated TH17 cells mediate lethal acute graft-versus-host disease with severe cutaneous and pulmonary pathologic manifestations. Blood 2009; 113: 1365-1374.