Suppressive activity of regulatory T cells correlates with high CD4 + T-cell counts and low T-cell activation during chronic simian immunodeficiency virus infection

AIDS

Volumn 25, Issue 5, 2011, Pages 585-593

  Karlsson, Ingrid ^a,b   Malleret, Benoît ^a,d   Brochard, Patricia ^a,c   Delache, Benoît ^a,c   Calvo, Julien ^a   Le Grand, Roger ^a,c   Vaslin, Bruno ^a,c  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^b STATENS SERUM INSTITUT   (Denmark)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d AGENCY FOR SCIENCE   (Singapore)

Author keywords

macaque; pathogenesis; progression; regulatory T cell; simian immunodeficiency virus

Indexed keywords

CD4 ANTIGEN; INTERLEUKIN 2 RECEPTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD25+ T LYMPHOCYTE; CD4 LYMPHOCYTE COUNT; CHRONIC DISEASE; CONTROLLED STUDY; DISEASE COURSE; DISEASE MARKER; IN VITRO STUDY; LENTIVIRUS INFECTION; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MACACA; MALE; NONHUMAN; PERIPHERAL LYMPHOCYTE; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SIMIAN IMMUNODEFICIENCY VIRUS; T LYMPHOCYTE ACTIVATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; DISEASE PROGRESSION; LYMPHOCYTE ACTIVATION; MACACA FASCICULARIS; MALE; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; T-LYMPHOCYTES, REGULATORY; VIRAL LOAD;

EID: 79952442134     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0b013e3283437c7b     Document Type: Article

References (47)

1. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. 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 1995; 155:1151-1164.
2. Dieckmann D, Plottner H, Berchtold S, Berger T, Schuler G. Ex vivo isolation and characterization of CD4(R)CD25(R) T cells with regulatory properties from human blood. J Exp Med 2001; 193:1303-1310. (Pubitemid 32524780)
3. Levings MK, Sangregorio R, Sartirana C, Moschin AL, Battaglia M, Orban PC, Roncarolo MG. Human CD25RCD4R T suppressor cell clones produce transforming growth factor beta, but not interleukin 10, and are distinct from type 1 T regulatory cells. J Exp Med 2002; 196:1335-1346. (Pubitemid 35375552)
4. Weiner HL. Induction and mechanism of action of transforming growth factor-beta-secreting Th3 regulatory cells. Immunol Rev 2001; 182:207-214. (Pubitemid 33070220)
5. Baecher-Allan C, Brown JA, Freeman GJ, Hafler DA. CD4RCD25 high regulatory cells in human peripheral blood. J Immunol 2001; 167:1245-1253. (Pubitemid 32703119)
6. Belkaid Y, Rouse BT. Natural regulatory T cells in infectious disease. Nat Immunol 2005; 6:353-360. (Pubitemid 41716772)
7. Sakaguchi S, Ono M, Setoguchi R, Yagi H, Hori S, Fehervari Z, et al. Foxp3R CD25R CD4R natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 2006; 212:8-27. (Pubitemid 44116697)
8. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4RCD25R regulatory T cells. Nat Immunol 2003; 4:330-336. (Pubitemid 36432314)
9. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003; 299:1057-1061. (Pubitemid 36222930)
10. Read S, Malmstrom V, Powrie F. Cytotoxic T lymphocyteassociated antigen 4 plays an essential role in the function of CD25(R)CD4(R) regulatory cells that control intestinal inflammation. J Exp Med 2000; 192:295-302. (Pubitemid 30470312)
11. Takahashi T, Tagami T, Yamazaki S, Uede T, Shimizu J, Sakaguchi N, et al. Immunologic self-tolerance maintained by CD25(R)CD4(R) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J Exp Med 2000; 192:303-310.
12. Boasso A, Vaccari M, Nilsson J, Shearer GM, Andersson J, Cecchinato V, et al. Do regulatory T-cells play a role in AIDS pathogenesis? AIDS Rev 2006; 8:141-147. (Pubitemid 44614031)
13. 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.
14. 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. (Pubitemid 40396024)
15. 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. (Pubitemid 41003779)
16. 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. (Pubitemid 40354012)
17. Pereira LE, Villinger F, Onlamoon N, Bryan P, Cardona A, Pattanapanysat K, et al. Simian immunodeficiency virus (SIV) infection influences the level and function of regulatory T cells in SIV-infected rhesus macaques but not SIV-infected sooty mangabeys. J Virol 2007; 81:4445-4456. (Pubitemid 46668642)
18. 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.
19. Weiss L, Donkova-Petrini V, Caccavelli L, Balbo M, Carbonneil C, Levy Y. 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. (Pubitemid 39507143)
20. 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 cytomegalovirus antigens. J Virol 2004; 78:2454-2459. (Pubitemid 38228938)
21. 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. (Pubitemid 39031252)
22. Kinter AL, Horak R, Sion M, Riggin L, McNally J, Lin Y, et al. CD25R regulatory T cells isolated from HIV-infected individuals suppress the cytolytic and nonlytic antiviral activity of HIV-specific CD8RT cells in vitro. AIDS Res Hum Retroviruses 2007; 23:438-450. (Pubitemid 46608564)
23. Kinter A, McNally J, Riggin L, Jackson R, Roby G, Fauci AS. Suppression of HIV-specific T cell activity by lymph node CD25R regulatory T cells from HIV-infected individuals. Proc Natl Acad Sci USA 2007; 104:3390-3395. (Pubitemid 46364169)
24. 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. (Pubitemid 44864563)
25. Estes JD, Li Q, Reynolds MR, Wietgrefe S, Duan L, Schacker T, et al. Premature induction of an immunosuppressive regulatory T cell response during acute simian immunodeficiency virus infection. J Infect Dis 2006; 193:703-712. (Pubitemid 43271504)
26. Karlsson I, Malleret B, Brochard P, Delache B, Calvo J, Le Grand R, Vaslin B. FoxP3R CD25R CD8R T-cell induction during primary simian immunodeficiency virus infection in cynomolgus macaques correlates with low CD4R T-cell activation and high viral load. J Virol 2007; 81: 13444-13455. (Pubitemid 350247840)
27. Chase AJ, Sedaghat AR, German JR, Gama L, Zink MC, Clements JE, Siliciano RF. Severe depletion of CD4RCD25R regulatory T cells from the intestinal lamina propria but not peripheral blood or lymph nodes during acute SIV infection. J Virol 2007; 81:12748-12757. (Pubitemid 350156912)
28. Le Grand R, Clayette P, Noack O, Vaslin B, Theodoro F, Michel G, et al. An animal model for antilentiviral therapy: effect of zidovudine on viral load during acute infection after exposure of macaques to simian immunodeficiency virus. AIDS Res Hum Retroviruses 1994; 10:1279-1287. (Pubitemid 24349704)
29. Neildez O, Le Grand R, Cheret A, Caufour P, Vaslin B, Matheux F, et al. Variation in virological parameters and antibody responses in macaques after atraumatic vaginal exposure to a pathogenic primary isolate of SIVmac251. Res Virol 1998; 149:53-68. (Pubitemid 28162430)
30. Benlhassan-Chahour K, Penit C, Dioszeghy V, Vasseur F, Janvier G, Riviere Y, et al. Kinetics of lymphocyte proliferation during primary immune response in macaques infected with pathogenic simian immunodeficiency virus SIVmac251: preliminary report of the effect of early antiviral therapy. J Virol 2003; 77:12479-12493. (Pubitemid 37430645)
31. Karlsson I, Malleret B, Brochard P, Delache B, Calvo J, Le Grand R, Vaslin B. Dynamics of T-cell responses and memory T cells during primary simian immunodeficiency virus infection in cynomolgus macaques. J Virol 2007; 81:13456-13468. (Pubitemid 350247841)
32. Day CL, Kaufmann DE, Kiepiela P, Brown JA, Moodley ES, Reddy S, et al. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 2006; 443:350-354. (Pubitemid 44435155)
33. Freeman GJ, Wherry EJ, Ahmed R, Sharpe AH. Reinvigorating exhausted HIV-specific T cells via PD-1-PD-1 ligand blockade. J Exp Med 2006; 203:2223-2227. (Pubitemid 44498355)
34. Petrovas C, Casazza JP, Brenchley JM, Price DA, Gostick E, Adams WC, et al. PD-1 is a regulator of virus-specific CD8R T cell survival in HIV infection. J Exp Med 2006; 203:2281-2292. (Pubitemid 44498363)
35. 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. (Pubitemid 40489413)
36. Sumpter B, Dunham R, Gordon S, Engram J, Hennessy M, Kinter A, et al. Correlates of preserved CD4(R) T cell homeostasis during natural, nonpathogenic simian immunodeficiency virus infection of sooty mangabeys: implications for AIDS pathogenesis. J Immunol 2007; 178:1680-1691. (Pubitemid 46154640)
37. 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. (Pubitemid 29159331)
38. 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. (Pubitemid 351225605)
39. Chen Z, Zhou P, Ho DD, Landau NR, Marx PA. Genetically divergent strains of simian immunodeficiency virus use CCR5 as a coreceptor for entry. J Virol 1997; 71:2705-2714. (Pubitemid 27119907)
40. Pantaleo G, Graziosi C, Demarest JF, Butini L, Montroni M, Fox CH, et al. HIV infection is active and progressive in lymphoid tissue during the clinically latent stage of disease. Nature 1993; 362:355-358. (Pubitemid 23101310)
41. Reimann KA, Parker RA, Seaman MS, Beaudry K, Beddall M, Peterson L, et al. Pathogenicity of simian-human immunodefi-ciency virus SHIV-89.6P and SIVmac is attenuated in cynomolgus macaques and associated with early T-lymphocyte responses. J Virol 2005; 79:8878-8885. (Pubitemid 40934798)
42. Dioszeghy V, Benlhassan-Chahour K, Delache B, Dereuddre-Bosquet N, Aubenque C, Gras G, et al. Changes in soluble factor-mediated CD8R cell-derived antiviral activity in cynomolgus macaques infected with simian immunodeficiency virus SIVmac251: relationship to biological markers of progression. J Virol 2006; 80:236-245.
43. 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.
44. Lifson JD, Nowak MA, Goldstein S, Rossio JL, Kinter A, Vasquez G, et al. The extent of early viral replication is a critical determinant of the natural history of simian immunodeficiency virus infection. J Virol 1997; 71:9508-9514. (Pubitemid 27492396)
45. Watson A, Ranchalis J, Travis B, McClure J, Sutton W, Johnson PR, et al. Plasma viremia in macaques infected with simian immunodeficiency virus: plasma viral load early in infection predicts survival. J Virol 1997; 71:284-290. (Pubitemid 26412290)
46. Mellors JW, Munoz A, Giorgi JV, Margolick JB, Tassoni CJ, Gupta P, et al. Plasma viral load and CD4R lymphocytes as prognostic markers of HIV-1 infection. Ann InternMed 1997; 126:946-954. (Pubitemid 27255797)
47. Wang R, Kozhaya L, Mercer F, Khaitan A, Fujii H, Unutmaz D. Expression of GARP selectively identifies activated human FOXP3R regulatory T cells. Proc Natl Acad Sci USA 2009; 106:13439-13444.