Persistent resistance to HIV-1 infection in CD4 T cells from exposed uninfected Vietnamese individuals is mediated by entry and post-entry blocks

Retrovirology

Volumn 3, Issue , 2006, Pages

  Sáez Cirión, Asier ^a   Versmisse, Pierre ^a   Truong, Lien X ^b   Chakrabarti, Lisa A ^a   Carpentier, Wassila ^c   Barré Sinoussi, Françoise ^a   Scott Algara, Daniel ^a   Pancino, Gianfranco ^a  

^a INSTITUT PASTEUR   (France)

^b PASTEUR INSTITUTE   (Viet Nam)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR5;

ARTICLE; CD4+ T LYMPHOCYTE; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE MUTATION; HETEROZYGOSITY; HIGH RISK BEHAVIOR; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFECTION RISK; INOCULATION; INTRAVENOUS DRUG ABUSE; MALE; PERIPHERAL BLOOD MONONUCLEAR CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VIET NAM; VIRUS IMMUNITY; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS RESISTANCE;

ADULT; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; HIV INFECTIONS; HIV-1; HUMANS; IMMUNITY, INNATE; LENTIVIRUS; MALE; MIDDLE AGED; RECEPTORS, CCR6; RECEPTORS, CHEMOKINE; VIRUS INTERNALIZATION; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 33751185929     PISSN: 17424690     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-3-81     Document Type: Article

References (57)

1. Wainberg MA, Blain N, Fitz-Gibbon L: Differential susceptibility of human lymphocyte cultures to infection by HIV. Clin Exp Immunol 1987, 70(1):136-142.
2. Ciuffi A, Bleiber G, Munoz M, Martinez R, Loeuillet C, Rehr M, Fischer M, Gunthard HF, Oxenius A, Meylan P, Bonhoeffer S, Trono D, Telenti A: Entry and transcription as key determinants of differences in CD4 T-cell permissiveness to human immunodeficiency virus type 1 infection. J Virol 2004, 78(19):10747-10754.
3. Greene WC, Peterlin BM: Charting HIV's remarkable voyage through the cell: Basic science as a passport to future therapy. Nat Med 2002, 8(7):673-680.
4. Goff SP: Retrovirus restriction factors. Mol Cell 2004, 16(6):849-859.
5. Chiu YL, Soros VB, Kreisberg JF, Stopak K, Yonemoto W, Greene WC: Cellular APOBEC3G restricts HIV-1 infection in resting CD4+ T cells. Nature 2005, 435(7038):108-114.
6. Ganesh L, Burstein E, Guha-Niyogi A, Louder MK, Mascola JR, Klomp LW, Wijmenga C, Duckett CS, Nabel GJ: The gene product Murr1 restricts HIV-1 replication in resting CD4+ lymphocytes. Nature 2003, 426(6968):853-857.
7. Sawyer SL, Wu LI, Akey JM, Emerman M, Malik HS: High-frequency persistence of an impaired allele of the retroviral defense gene TRIM5alpha in humans. Curr Biol 2006, 16(1):95-100.
8. Speelmon EC, Livingston-Rosanoff D, Li SS, Vu Q, Bui J, Geraghty DE, Zhao LP, McElrath MJ: Genetic association of the antiviral restriction factor TRIM5alpha with human immunodeficiency virus type 1 infection. J Virol 2006, 80(5):2463-2471.
9. Paxton WA, Martin SR, Tse D, O'Brien TR, Skurnick J, VanDevanter NL, Padian N, Braun JF, Kotler DP, Wolinsky SM, Koup RA: Relative resistance to HIV-1 infection of CD4 lymphocytes from persons who remain uninfected despite multiple high-risk sexual exposure. Nat Med 1996, 2(4):412-417.
10. Connor RI, Paxton WA, Sheridan KE, Koup RA: Macrophages and CD4+ T lymphocytes from two multiply exposed, uninfected individuals resist infection with primary non-syncytium-inducing isolates of human immunodeficiency virus type 1. J Virol 1996, 70(12):8758-8764.
11. Truong LX, Luong TT, Scott-Algara D, Versmisse P, David A, Perez-Bercoff D, Nguyen NV, Tran HK, Cao CT, Fontanet A, Follezou JY, Theodorou I, Barre-Sinoussi F, Pancino G: CD4 cell and CD8 cell-mediated resistance to HIV-1 infection in exposed uninfected intravascular drug users in Vietnam. Aids 2003, 17(10):1425-1434.
12. Paxton WA, Liu R, Kang S, Wu L, Gingeras TR, Landau NR, Mackay CR, Koup RA: Reduced HIV-1 infectability of CD4+ lymphocytes from exposed-uninfected individuals: association with low expression of CCR5 and high production of beta-chemokines. Virology 1998, 244(1):66-73.
13. Butera ST, Pisell TL, Limpakarnjanarat K, Young NL, Hodge TW, Mastro TD, Folks TM: Production of a novel viral suppressive activity associated with resistance to infection among female sex workers exposed to HIV type 1. AIDS Res Hum Retroviruses 2001, 17(8):735-744.
14. Eyeson J, King D, Boaz MJ, Sefia E, Tomkins S, Waters A, Easterbrook PJ, Vyakarnam A: Evidence for Gag p24-specific CD4 T cells with reduced susceptibility to R5 HIV-1 infection in a UK cohort of HIV-exposed-seronegative subjects. Aids 2003, 17(16):2299-2311.
15. Liu R, Paxton WA, Choe S, Ceradini D, Martin SR, Horuk R, MacDonald ME, Stuhlmann H, Koup RA, Landau NR: Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 1996, 86(3):367-377.
16. Quillent C, Oberlin E, Braun J, Rousset D, Gonzalez-Canali G, Metais P, Montagnier L, Virelizier JL, Arenzana-Seisdedos F, Beretta A: HIV-1-resistance phenotype conferred by combination of two separate inherited mutations of CCR5 gene. Lancet 1998, 351(9095):14-18.
17. Samson M, Libert F, Doranz BJ, Rucker J, Liesnard C, Farber CM, Saragosti S, Lapoumeroulie C, Cognaux J, Forceille C, Muyldermans G, Verhofstede C, Burtonboy G, Georges M, Imai T, Rana S, Yi Y, Smyth RJ, Collman RG, Doms RW, Vassart G, Parmentier M: Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 1996, 382(6593):722-725.
18. Koning FA, Jansen CA, Dekker J, Kaslow RA, Dukers N, van Baarle D, Prins M, Schuitemaker H: Correlates of resistance to HIV-1 infection in homosexual men with high-risk sexual behaviour. Aids 2004, 18(8):1117-1126.
19. Garzino-Demo A, Moss RB, Margolick JB, Cleghorn F, Sill A, Blattner WA, Cocchi F, Carlo DJ, DeVico AL, Gallo RC: Spontaneous and antigen-induced production of HIV-inhibitory beta-chemokines are associated with AIDS-free status. Proc Natl Acad Sci U S A 1999, 96(21):11986-11991.
20. Furci L, Scarlatti G, Burastero S, Tambussi G, Colognesi C, Quillent C, Longhi R, Loverro P, Borgonovo B, Gaffi D, Carrow E, Malnati M, Lusso P, Siccardi AG, Lazzarin A, Beretta A: Antigen-driven C-C chemokine-mediated HIV-1 suppression by CD4(+) T cells from exposed uninfected individuals expressing the wild-type CCR-5 allele. J Exp Med 1997, 186(3):455-460.
21. Stranford SA, Skurnick J, Louria D, Osmond D, Chang SY, Sninsky J, Ferrari G, Weinhold K, Lindquist C, Levy JA: Lack of infection in HIV-exposed individuals is associated with a strong CD8(+) cell noncytotoxic anti-HIV response. Proc Natl Acad Sci U S A 1999, 96(3):1030-1035.
22. John R, Arango-Jaramillo S, Finny GJ, Schwartz DH: Risk associated HIV-1 cross-clade resistance of whole peripheral blood mononuclear cells from exposed uninfected individuals with wild-type CCR5. J Acquir Immune Defic Syndr 2004, 35(1):1-8.
23. Kaul R, Rowland-Jones SL, Kimani J, Dong T, Yang HB, Kiama P, Rostron T, Njagi E, Bwayo JJ, MacDonald KS, McMichael AJ, Plummer FA: Late seroconversion in HIV-resistant Nairobi prostitutes despite pre-existing HIV-specific CD8+ responses. J Clin Invest 2001, 107(3):341-349.
24. Capoulade-Metay C, Ma L, Truong LX, Dudoit Y, Versmisse P, Nguyen NV, Nguyen M, Scott-Algara D, Barre-Sinoussi F, Debre P, Bismuth G, Pancino G, Theodorou I: New CCR5 variants associated with reduced HIV coreceptor function in southeast Asia. Aids 2004, 18(17):2243-2252.
25. Magierowska M, Lepage V, Lien TX, Lan NT, Guillotel M, Issafras H, Reynes JM, Fleury HJ, Chi NH, Follezou JY, Debre P, Theodorou I, Barre-Sinoussi F: Novel variant of the CCR5 gene in a Vietnamese population. Microbes Infect 1999, 1(2):123-124.
26. Blanpain C, Lee B, Vakili J, Doranz BJ, Govaerts C, Migeotte I, Sharron M, Dupriez V, Vassart G, Doms RW, Parmentier M: Extracellular cysteines of CCR5 are required for chemokine binding, but dispensable for HIV-1 coreceptor activity. J Biol Chem 1999, 274(27):18902-18908.
27. Aiken C: Pseudotyping human immunodeficiency virus type 1 (HIV-1) by the glycoprotein of vesicular stomatitis virus targets HIV-1 entry to an endocytic pathway and suppresses both the requirement for Nef and the sensitivity to cyclosporin A. J Virol 1997, 71(8):5871-5877.
28. Lin YL, Mettling C, Portales P, Reant B, Clot J, Corbeau P: G-protein signaling triggered by R5 human immunodeficiency virus type 1 increases virus replication efficiency in primary T lymphocytes. J Virol 2005, 79(12):7938-7941.
29. Misse D, Gajardo J, Oblet C, Religa A, Riquet N, Mathieu D, Yssel H, Veas F: Soluble HIV-1 gp120 enhances HIV-1 replication in non-dividing CD4+ T cells, mediated via cell signaling and Tat cofactor overexpression. Aids 2005, 19(9):897-905.
30. Balabanian K, Harriague J, Decrion C, Lagane B, Shorte S, Baleux F, Virelizier JL, Arenzana-Seisdedos F, Chakrabarti LA: CXCR4-tropic HIV-1 envelope glycoprotein functions as a viral chemokine in unstimulated primary CD4+ T lymphocytes. J Immunol 2004, 173(12):7150-7160.
31. Baba M, Nishimura O, Kanzaki N, Okamoto M, Sawada H, Iizawa Y, Shiraishi M, Aramaki Y, Okonogi K, Ogawa Y, Meguro K, Fujino M: A small-molecule, nonpeptide CCR5 antagonist with highly potent and selective anti-HIV-1 activity. Proc Natl Acad Sci U S A 1999, 96(10):5698-5703.
32. Sharpless NE, O'Brien WA, Verdin E, Kufta CV, Chen IS, Dubois-Dalcq M: Human immunodeficiency virus type 1 tropism for brain microglial cells is determined by a region of the env glycoprotein that also controls macrophage tropism. J Virol 1992, 66(4):2588-2593.
33. Westervelt P, Trowbridge DB, Epstein LG, Blumberg BM, Li Y, Hahn BH, Shaw GM, Price RW, Ratner L: Macrophage tropism determinants of human immunodeficiency virus type 1 in vivo. J Virol 1992, 66(4):2577-2582.
34. Chanel C, Staropoli I, Baleux F, Amara A, Valenzuela-Fernandez A, Virelizier JL, Arenzana-Seisdedos F, Altmeyer R: Low levels of coreceptor CCR5 are sufficient to permit HIV envelope-mediated fusion with resting CD4 T cells. Aids 2002, 16(17):2337-2340.
35. Wu L, Paxton WA, Kassam N, Ruffing N, Rottman JB, Sullivan N, Choe H, Sodroski J, Newman W, Koup RA, Mackay CR: CCR5 levels and expression pattern correlate with infectability by macrophage-tropic HIV-1, in vitro. J Exp Med 1997, 185(9):1681-1691.
36. Kim A, Pettoello-Mantovani M, Goldstein H: Decreased susceptibility of peripheral blood mononuclear cells from individuals heterozygous for a mutant CCR5 allele to HIV infection. J Acquir Immune Defic Syndr Hum Retrovirol 1998, 19(2):145-149.
37. Venkatesan S, Petrovic A, Van Ryk DI, Locati M, Weissman D, Murphy PM: Reduced cell surface expression of CCR5 in CCR5Delta 32 heterozygotes is mediated by gene dosage, rather than by receptor sequestration. J Biol Chem 2002, 277(3):2287-2301.
38. Benkirane M, Jin DY, Chun RF, Koup RA, Jeang KT: Mechanism of transdominant inhibition of CCR5-mediated HIV-1 infection by ccr5delta32. J Biol Chem 1997, 272(49):30603-30606.
39. Chelli M, Alizon M: Determinants of the trans-dominant negative effect of truncated forms of the CCR5 chemokine receptor. J Biol Chem 2001, 276(50):46975-46982.
40. Cocchi F, DeVico AL, Garzino-Demo A, Arya SK, Gallo RC, Lusso P: Identification of RANTES, MIP-1 alpha, and MIP-1 beta as the major HIV-suppressive factors produced by CD8+ T cells. Science 1995, 270(5243):1811-1815.
41. Nguyen DH, Taub D: Cholesterol is essential for macrophage inflammatory protein 1 beta binding and conformational integrity of CC chemokine receptor 5. Blood 2002, 99(12):4298-4306.
42. Venkatesan S, Rose JJ, Lodge R, Murphy PM, Foley JF: Distinct mechanisms of agonist-induced endocytosis for human chemokine receptors CCR5 and CXCR4. Mol Biol Cell 2003, 14(8):3305-3324.
43. Mariani R, Chen D, Schrofelbauer B, Navarro F, Konig R, Bollman B, Munk C, Nymark-McMahon H, Landau NR: Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 2003, 114(1):21-31.
44. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J: The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 2004, 427(6977):848-853.
45. Hatziioannou T, Perez-Caballero D, Yang A, Cowan S, Bieniasz PD: Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha. Proc Natl Acad Sci U S A 2004, 101(29):10774-10779.
46. Ray N, Doms RW: HIV-1 coreceptors and their inhibitors. Curr Top Microbiol Immunol 2006, 303:97-120.
47. Kulkarni PS, Butera ST, Duerr AC: Resistance to HIV-1 infection: lessons learned from studies of highly exposed persistently seronegative (HEPS) individuals. AIDS Rev 2003, 5(2):87-103.
48. Scott-Algara D, Truong LX, Versmisse P, David A, Luong TT, Nguyen NV, Theodorou I, Barre-Sinoussi F, Pancino G: Cutting edge: increased NK cell activity in HIV-1-exposed but uninfected Vietnamese intravascular drug users. J Immunol 2003, 171(11):5663-5667.
49. Zhu T, Mo H, Wang N, Nam DS, Cao Y, Koup RA, Ho DD: Genotypic and phenotypic characterization of HIV-1 patients with primary infection. Science 1993, 261(5125):1179-1181.
50. van't Wout AB, Kootstra NA, Mulder-Kampinga GA, Albrecht-van Lent N, Scherpbier HJ, Veenstra J, Boer K, Coutinho RA, Miedema F, Schuitemaker H: Macrophage-tropic variants initiate human immunodeficiency virus type 1 infection after sexual, parenteral, and vertical transmission. J Clin Invest 1994, 94(5):2060-2067.
51. Pantaleo G, Graziosi C, Butini L, Pizzo PA, Schnittman SM, Kotler DP, Fauci AS: Lymphoid organs function as major reservoirs for human immunodeficiency virus. Proc Natl Acad Sci U S A 1991, 88(21):9838-9842.
52. Veazey RS, Marx PA, Lackner AA: The mucosal immune system: primary target for HIV infection and AIDS. Trends Immunol 2001, 22(11):626-633.
53. Follezou JY, Lan NY, Lien TX, Lafon ME, Tram LT, Hung PV, Aknine X, Lowenstein W, Ngai NV, Theodorou I, Delfraissy JF, Debre P, Fleury HJ, Barre-Sinoussi F, Chi NH: Clinical and biological characteristics of human immunodeficiency virus-infected and uninfected intravascular drug users in Ho Chi Minh City, Vietnam. Am J Trop Med Hyg 1999, 61(3):420-424.
54. Connor RI, Chen BK, Choe S, Landau NR: Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes. Virology 1995, 206(2):935-944.
55. O'Doherty U, Swiggard WJ, Malim MH: Human immunodeficiency virus type 1 spinoculation enhances infection through virus binding. J Virol 2000, 74(21):10074-10080.
56. Rouet F, Ekouevi DK, Chaix ML, Burgard M, Inwoley A, Tony TD, Danel C, Anglaret X, Leroy V, Msellati P, Dabis F, Rouzioux C: Transfer and evaluation of an automated, low-cost real-time reverse transcription-PCR test for diagnosis and monitoring of human immunodeficiency virus type 1 infection in a West African resource-limited setting. J Clin Microbiol 2005, 43(6):2709-2717.
57. Folks TM, Powell D, Lightfoote M, Koenig S, Fauci AS, Benn S, Rabson A, Daugherty D, Gendelman HE, Hoggan MD, et al.: Biological and biochemical characterization of a cloned Leu-3- cell surviving infection with the acquired immune deficiency syndrome retrovirus. J Exp Med 1986, 164(1):280-290.