R5-SHIV induces multiple defects in T cell function during early infection of rhesus macaques including accumulation of T reg cells in lymph nodes

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Santosuosso, Michael ^a   Righi, Elda ^a   Hill, E David ^a   Leblanc, Pierre R ^a   Kodish, Brett ^a   Mylvaganam, Hari N ^a   Siddappa, Nagadenahalli B ^b   Stevceva, Liljana ^a   Hu, Shiu Lok ^c   Ghebremichael, Musie ^b   Chenine, Agnes L ^b   Hovav, Avi Hai ^d   Ruprecht, Ruth M ^b   Poznansky, Mark C ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; GLYCOPROTEIN GP 120; PROGRAMMED DEATH 1 RECEPTOR; CHEMOKINE RECEPTOR CCR5; G PROTEIN COUPLED RECEPTOR; GP120 PROTEIN, HUMAN IMMUNODEFICIENCY VIRUS 1; LEUKOCYTE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CHEMOTAXIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; EFFECTOR CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE DYSREGULATION; LENTIVIRUS INFECTION; LYMPH NODE; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; LYMPHOID TISSUE; NONHUMAN; PROTEIN ANALYSIS; REGULATORY T LYMPHOCYTE; RHESUS MONKEY; SIMIAN HUMAN IMMUNODEFICIENCY VIRUS INFECTION; T CELL DEPLETION; VIRUS STRAIN; ANIMAL; ANTIBODY SPECIFICITY; CELL DEATH; CYTOLOGY; HUMAN; IMMUNOLOGY; MACACA MULATTA; METABOLISM; MUCOSA; PHYSIOLOGY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; TIME; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS 1; MACACA MULATTA; SIMIAN-HUMAN IMMUNODEFICIENCY VIRUS;

ANIMALS; ANTIBODY SPECIFICITY; ANTIGENS, CD; CELL DEATH; CHEMOTAXIS; GENE PRODUCTS, GAG; HIV ENVELOPE PROTEIN GP120; HUMANS; LYMPH NODES; MACACA MULATTA; MUCOUS MEMBRANE; RECEPTORS, CCR5; RECEPTORS, G-PROTEIN-COUPLED; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; T-LYMPHOCYTES, REGULATORY; TIME FACTORS;

EID: 79953680488     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018465     Document Type: Article

References (58)

1. Li Q, Skinner PJ, Ha SJ, Duan L, Mattila TL, et al. (2009) Visualizing antigen-specific and infected cells in situ predicts outcomes in early viral infection. Science 323: 1726-1729.
2. Li Q, Estes JD, Schlievert PM, Duan L, Brosnahan AJ, et al. (2009) Glycerol monolaurate prevents mucosal SIV transmission. Nature 458: 1034-1038.
3. Salazar-Gonzalez JF, Salazar MG, Keele BF, Learn GH, Giorgi EE, et al. (2009) Genetic identity, biological phenotype, and evolutionary pathways of transmitted/founder viruses in acute and early HIV-1 infection. J Exp Med 206: 1273-1289.
4. Keele BF, Li H, Learn GH, Hraber P, Giorgi EE, et al. (2009) Low-dose rectal inoculation of rhesus macaques by SIVsmE660 or SIVmac251 recapitulates human mucosal infection by HIV-1. J Exp Med.
5. Munier M, Kelleher A, (2007) Acutely dysregulated, chronically disabled by the enemy within: T-cell responses to HIV-1 infection. Immunol Cell Biol 85: 6-15.
6. Cooper DA, Tindall B, Wilson EJ, Imrie AA, Penny R, (1988) Characterization of T lymphocyte responses during primary infection with human immunodeficiency virus. J Infect Dis 157: 889-896.
7. Kaufmann GR, Cunningham P, Kelleher AD, Zaunders J, Carr A, et al. (1998) Patterns of viral dynamics during primary human immunodeficiency virus type 1 infection. The Sydney Primary HIV Infection Study Group. J Infect Dis 178: 1812-1815.
8. Mellors JW, Kingsley LA, Rinaldo CR Jr, Todd JA, Hoo BS, et al. (1995) Quantitation of HIV-1 RNA in plasma predicts outcome after seroconversion. Ann Intern Med 122: 573-579.
9. Mellors JW, Rinaldo CR Jr, Gupta P, White RM, Todd JA, et al. (1996) Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 272: 1167-1170.
10. Bachis A, Mocchetti I, (2004) The chemokine receptor CXCR4 and not the N-methyl-D-aspartate receptor mediates gp120 neurotoxicity in cerebellar granule cells. J Neurosci Res 75: 75-82.
11. Ronaldson PT, Bendayan R, (2006) HIV-1 viral envelope glycoprotein gp120 triggers an inflammatory response in cultured rat astrocytes and regulates the functional expression of P-glycoprotein. Molecular Pharmacology 70: 1087-1098.
12. Chougnet C, Gessani S, (2006) Role of gp120 in dendritic cell dysfunction in HIV infection. Journal of Leukocyte Biology 80: 994-1000.
13. Fantuzzi L, Purificato C, Donato K, Belardelli F, Gessani S, (2004) Human immunodeficiency virus type 1 gp120 induces abnormal maturation and functional alterations of dendritic cells: a novel mechanism for AIDS pathogenesis. J Virol 78: 9763-9772.
14. Shan M, Klasse PJ, Banerjee K, Dey AK, Iyer SP, et al. (2007) HIV-1 gp120 mannoses induce immunosuppressive responses from dendritic cells. PLoS Pathog 3: e169.
15. Balabanian K, Harriague J, Décrion C, Lagane B, Shorte S, et al. (2004) CXCR4-tropic HIV-1 envelope glycoprotein functions as a viral chemokine in unstimulated primary CD4+ T lymphocytes. J Immunol 173: 7150-7160.
16. 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.
17. Brainard DM, Tharp WG, Granado E, Miller N, Trocha AK, et al. (2004) Migration of antigen-specific T cells away from CXCR4-binding human immunodeficiency virus type 1 gp120. Journal of Virology 78: 5184-5193.
18. Algeciras A, Dockrell DH, Lynch DH, Paya CV, (1998) CD4 regulates susceptibility to Fas ligand- and tumor necrosis factor-mediated apoptosis. J Exp Med 187: 711-720.
19. Corbeil J, Richman DD, (1995) Productive infection and subsequent interaction of CD4-gp120 at the cellular membrane is required for HIV-induced apoptosis of CD4+ T cells. J Gen Virol 76 (Pt 3): 681-690.
20. Finkel TH, Tudor-Williams G, Banda NK, Cotton MF, Curiel T, et al. (1995) Apoptosis occurs predominantly in bystander cells and not in productively infected cells of HIV- and SIV-infected lymph nodes. Nat Med 1: 129-134.
21. Westendorp MO, Frank R, Ochsenbauer C, Stricker K, Dhein J, et al. (1995) Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature 375: 497-500.
22. Bonsignori M, Moody MA, Parks RJ, Holl TM, Kelsoe G, et al. (2009) HIV-1 envelope induces memory B cell responses that correlate with plasma antibody levels after envelope gp120 protein vaccination or HIV-1 infection. J Immunol 183: 2708-2717.
23. Moir S, Fauci A, (2009) B cells in HIV infection and disease. Nat Rev Immunol 9: 235-245.
24. Fauci AS, Johnston MI, Dieffenbach CW, Burton DR, Hammer SM, et al. (2008) HIV vaccine research: the way forward. Science 321: 530-532.
25. Fauci AS, (2008) 25 years of HIV. Nature 453: 289-290.
26. Klasse PJ, Moore J, (2004) Is there enough gp120 in the body fluids of HIV-1-infected individuals to have biologically significant effects? Virology 323: 1-8.
27. Stevceva L, Yoon V, Carville A, Pacheco B, Santosuosso M, et al. (2008) The Efficacy of T Cell-Mediated Immune Responses Is Reduced by the Envelope Protein of the Chimeric HIV-1/SIV-KB9 Virus In Vivo. J Immunol 181: 5510-5521.
28. Popovic M, Tenner-Racz K, Pelser C, Stellbrink HJ, van Lunzen J, et al. (2005) Persistence of HIV-1 structural proteins and glycoproteins in lymph nodes of patients under highly active antiretroviral therapy. Proc Natl Acad Sci USA 102: 14807-14812.
29. Santosuosso M, Righi E, Lindstrom V, Leblanc PR, Poznansky MC, (2009) HIV-1 envelope protein gp120 is present at high concentrations in secondary lymphoid organs of individuals with chronic HIV-1 infection. J Infect Dis 200: 1050-1053.
30. Musey LK, Krieger JN, Hughes JP, Schacker TW, Corey L, et al. (1999) Early and persistent human immunodeficiency virus type 1 (HIV-1)-specific T helper dysfunction in blood and lymph nodes following acute HIV-1 infection. J Infect Dis 180: 278-284.
31. Song RJ, Chenine AL, Rasmussen RA, Ruprecht CR, Mirshahidi S, et al. (2006) Molecularly cloned SHIV-1157ipd3N4: a highly replication- competent, mucosally transmissible R5 simian-human immunodeficiency virus encoding HIV clade C Env. Journal of Virology 80: 8729-8738.
32. Humbert M, Rasmussen RA, Song R, Ong H, Sharma P, et al. (2008) SHIV-1157i and passaged progeny viruses encoding R5 HIV-1 clade C env cause AIDS in rhesus monkeys. Retrovirology 5: 94.
33. Poznansky MC, Olszak IT, Foxall R, Evans RH, Luster AD, et al. (2000) Active movement of T cells away from a chemokine. Nat Med 6: 543-548.
34. Baba M, Nishimura O, Kanzaki N, Okamoto M, Sawada H, et al. (1999) A small-molecule, nonpeptide CCR5 antagonist with highly potent and selective anti-HIV-1 activity. Proc Natl Acad Sci U S A 96: 5698-5703.
35. Chenine AL, Siddappa NB, Kramer VG, Sciaranghella G, Rasmussen RA, et al. (2010) Relative transmissibility of an R5 clade C simian-human immunodeficiency virus across different mucosae in macaques parallels the relative risks of sexual HIV-1 transmission in humans via different routes. J Infect Dis 201: 1155-1163.
36. Chertova E, Bess JW Jr, Crise BJ, Sowder RC II, Schaden TM, et al. (2002) Envelope glycoprotein incorporation, not shedding of surface envelope glycoprotein (gp120/SU), Is the primary determinant of SU content of purified human immunodeficiency virus type 1 and simian immunodeficiency virus. Journal of Virology 76: 5315-5325.
37. Accornero P, Radrizzani M, Carè A, Mattia G, Chiodoni C, et al. (1998) HIV/gp120 and PMA/ionomycin induced apoptosis but not activation induced cell death require PKC for Fas-L upregulation. FEBS Letters 436: 461-465.
38. Day C, Kaufmann D, Kiepiela P, Brown J, Moodley E, et al. (2006) PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 443: 350-354.
39. Petrovas C, Casazza JP, Brenchley JM, Price DA, Gostick E, et al. (2006) PD-1 is a regulator of virus-specific CD8+ T cell survival in HIV infection. J Exp Med 203: 2281-2292.
40. Trautmann L, Janbazian L, Chomont N, Said E, Gimmig S, et al. (2006) Upregulation of PD-1 expression on HIV-specific CD8+ T cells leads to reversible immune dysfunction. Nat Med 12: 1198-1202.
41. Barber D, Wherry EJ, Masopust D, Zhu B, Allison J, et al. (2006) Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439: 682-687.
42. Velu V, Titanji K, Zhu B, Husain S, Pladevega A, et al. (2009) Enhancing SIV-specific immunity in vivo by PD-1 blockade. Nature 458: 206-210.
43. Belkaid Y, (2007) Regulatory T cells and infection: a dangerous necessity. Nat Rev Immunol 7: 875-888.
44. Haeryfar SM, DiPaolo RJ, Tscharke DC, Bennink JR, Yewdell JW, (2005) Regulatory T cells suppress CD8+ T cell responses induced by direct priming and cross-priming and moderate immunodominance disparities. J Immunol 174: 3344-3351.
45. Moore AC, Gallimore A, Draper SJ, Watkins KR, Gilbert SC, et al. (2005) Anti-CD25 antibody enhancement of vaccine-induced immunogenicity: increased durable cellular immunity with reduced immunodominance. J Immunol 175: 7264-7273.
46. Moir S, Ho J, Malaspina A, Wang W, DiPoto AC, et al. (2008) Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J Exp Med 205: 1797-1805.
47. Hovav AH, Santosuosso M, Bivas-Benita M, Plair A, Cheng A, et al. (2009) X4 human immunodeficiency virus type 1 gp120 down-modulates expression and immunogenicity of codelivered antigens. J Virol 83: 10941-10950.
48. Biancotto A, Grivel JC, Iglehart SJ, Vanpouille C, Lisco A, et al. (2007) Abnormal activation and cytokine spectra in lymph nodes of people chronically infected with HIV-1. Blood 109: 4272-4279.
49. Krathwohl MD, Schacker TW, Anderson JL, (2006) Abnormal presence of semimature dendritic cells that induce regulatory T cells in HIV-infected subjects. J Infect Dis 193: 494-504.
50. Wang XZ, Stepp SE, Brehm MA, Chen HD, Selin LK, et al. (2003) Virus-specific CD8 T cells in peripheral tissues are more resistant to apoptosis than those in lymphoid organs. Immunity 18: 631-642.
51. Antons AK, Wang R, Oswald-Richter K, Tseng M, Arendt CW, et al. (2008) Naive precursors of human regulatory T cells require FoxP3 for suppression and are susceptible to HIV infection. J Immunol 180: 764-773.
52. Epple HJ, Loddenkemper C, Kunkel D, Tröger H, Maul J, et al. (2006) Mucosal but not peripheral FOXP3+ regulatory T cells are highly increased in untreated HIV infection and normalize after suppressive HAART. Blood 108: 3072-3078.
53. Ji J, Cloyd MW, (2009) HIV-1 binding to CD4 on CD4+CD25+ regulatory T cells enhances their suppressive function and induces them to home to, and accumulate in, peripheral and mucosal lymphoid tissues: an additional mechanism of immunosuppression. Int Immunol 21: 283-294.
54. Kinter A, Mcnally J, Riggin L, Jackson R, Roby G, et al. (2007) Suppression of HIV-specific T cell activity by lymph node CD25+ regulatory T cells from HIV-infected individuals. Proc Natl Acad Sci USA 104: 3390-3395.
55. 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.
56. Dunham R, Cervasi B, Brenchley JM, Albrecht H, Weintrob A, et al. (2008) CD127 and CD25 expression defines CD4+ T cell subsets that are differentially depleted during HIV infection. J Immunol 180: 5582-5592.
57. Hu H, Fernando K, Ni H, Weissman D, (2008) HIV envelope suppresses CD4+ T cell activation independent of T regulatory cells. J Immunol 180: 5593-5600.
58. Becker C, Taube C, Bopp T, Michel K, Kubach J, et al. (2009) Protection from graft-versus-host disease by HIV-1 envelope protein gp120-mediated activation of human CD4+CD25+ regulatory T cells. Blood 114: 1263-1269.