Pressure from TRIM5α contributes to control of HIV-1 replication by individuals expressing protective HLA-B alleles

Journal of Virology

Volumn 87, Issue 18, 2013, Pages 10368-10380

  Granier, Clémence ^a,b   Battivelli, Emilie ^a,b   Lécuroux, Camille ^a,c   Venet, Alain ^a,c   Lambotte, Olivier ^a,c,d   Schmitt Boulanger, Marion ^a,b   Delaugerre, Constance ^a,b,e   Molina, Jean Michel ^a,b,e   Chakrabarti, Lisa A ^f   Clavel, François ^a,b,e   Hance, Allan J ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DIDEROT   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d BICÊTRE HOSPITAL   (France)

^e SAINT LOUIS HOSPITAL   (France)

^f INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HLA B ANTIGEN; HLA B27 ANTIGEN; HLA B57 ANTIGEN; TRIPARTITE MOTIF PROTEIN 5;

ALLELE; ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; GENE; GENE EXPRESSION; GENE MUTATION; HLA B GENE; HLA B27 GENE; HLA B57 GENE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IMMUNOREGULATION; INFECTION PREVENTION; INNATE IMMUNITY; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; VIREMIA; VIRUS CAPSID; VIRUS LOAD; VIRUS RECOMBINANT; VIRUS REPLICATION;

ADULT; CARRIER PROTEINS; FEMALE; HIV INFECTIONS; HIV-1; HLA-B27 ANTIGEN; HUMANS; MALE; MIDDLE AGED; VIRAL LOAD;

EID: 84883293598     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01313-13     Document Type: Article

References (99)

1. Jin X, Bauer DE, Tuttleton SE, Lewin S, Gettie A, Blanchard J, Irwin CE, Safrit JT, Mittler J, Weinberger L, Kostrikis LG, Zhang L, Perelson AS, Ho DD. 1999. Dramatic rise in plasma viremia after CD8(+) T cell depletion in simian immunodeficiency virus-infected macaques. J. Exp. Med. 189:991-998.
2. Koup RA, Safrit JT, Cao Y, Andrews CA, McLeod G, Borkowsky W, Farthing C, Ho DD. 1994. Temporal association of cellular immune responses with the initial control of viremia in primary human immunodeficiency virus type 1 syndrome. J. Virol. 68:4650-4655.
3. Schmitz JE, Kuroda MJ, Santra S, Sasseville VG, Simon MA, Lifton MA, Racz P, Tenner-Racz K, Dalesandro M, Scallon BJ, Ghrayeb J, Forman MA, Montefiori DC, Rieber EP, Letvin NL, Reimann KA. 1999. Control of viremia in simian immunodeficiency virus infection by CD8+lymphocytes. Science 283:857-860.
4. Goonetilleke N, Liu MK, Salazar-Gonzalez JF, Ferrari G, Giorgi E, Ganusov VV, Keele BF, Learn GH, Turnbull EL, Salazar MG, Weinhold KJ, Moore S, Letvin N, Haynes BF, Cohen MS, Hraber P, Bhattacharya T, Borrow P, Perelson AS, Hahn BH, Shaw GM, Korber BT, McMichael AJ. 2009. The first T cell response to transmitted/founder virus contributes to the control of acute viremia in HIV-1 infection. J. Exp. Med. 206: 1253-1272.
5. Mudd PA, Martins MA, Ericsen AJ, Tully DC, Power KA, Bean AT, Piaskowski SM, Duan L, Seese A, Gladden AD, Weisgrau KL, Furlott JR, Kim YI, Veloso de Santana MG, Rakasz E, Capuano S, III, Wilson NA, Bonaldo MC, Galler R, Allison DB, Piatak M, Jr, Haase AT, Lifson JD, Allen TM, Watkins DI. 2012. Vaccine-induced CD8+ T cells control AIDS virus replication. Nature 491:129-133.
6. Mellors JW, Rinaldo CR, Jr, Gupta P, White RM, Todd JA, Kingsley LA. 1996. Prognosis in HIV-1 infection predicted by the quantity of virus in plasma. Science 272:1167-1170.
7. Streeck H, Jolin JS, Qi Y, Yassine-Diab B, Johnson RC, Kwon DS, Addo MM, Brumme C, Routy JP, Little S, Jessen HK, Kelleher AD, Hecht FM, Sekaly RP, Rosenberg ES, Walker BD, Carrington M, Altfeld M. 2009. Human immunodeficiency virus type 1-specific CD8+ T-cell responses during primary infection are major determinants of the viral set point and loss of CD4+ T cells. J. Virol. 83:7641-7648.
8. Carrington M, Walker BD. 2012. Immunogenetics of spontaneous control of HIV. Annu. Rev. Med. 63:131-145.
9. Goulder PJ, Walker BD. 2012. HIV and HLA class I: an evolving relationship. Immunity 37:426-440.
10. Dinges WL, Richardt J, Friedrich D, Jalbert E, Liu Y, Stevens CE, Maenza J, Collier AC, Geraghty DE, Smith J, Moodie Z, Mullins JI, McElrath MJ, Horton H. 2010. Virus-specific CD8+ T-cell responses better define HIV disease progression than HLA genotype. J. Virol. 84: 4461-4468.
11. Geldmacher C, Currier JR, Herrmann E, Haule A, Kuta E, McCutchan F, Njovu L, Geis S, Hoffmann O, Maboko L, Williamson C, Birx D, Meyerhans A, Cox J, Hoelscher M. 2007. CD8 T-cell recognition of multiple epitopes within specific Gag regions is associated with maintenance of a low steady-state viremia in human immunodeficiency virus type 1-seropositive patients. J. Virol. 81:2440-2448.
12. Kiepiela P, Ngumbela K, Thobakgale C, Ramduth D, Honeyborne I, Moodley E, Reddy S, de Pierres C, Mncube Z, Mkhwanazi N, Bishop K, van der Stok M, Nair K, Khan N, Crawford H, Payne R, Leslie A, Prado J, Prendergast A, Frater J, McCarthy N, Brander C, Learn GH, Nickle D, Rousseau C, Coovadia H, Mullins JI, Heckerman D, Walker BD, Goulder P. 2007. CD8+ T-cell responses to different HIV proteins have discordant associations with viral load. Nat. Med. 13:46-53.
13. Streeck H, Lichterfeld M, Alter G, Meier A, Teigen N, Yassine-Diab B, Sidhu HK, Little S, Kelleher A, Routy JP, Rosenberg ES, Sekaly RP, Walker BD, Altfeld M. 2007. Recognition of a defined region within p24 Gag by CD8+ T cells during primary human immunodeficiency virus type 1 infection in individuals expressing protective HLA class I alleles. J. Virol. 81:7725-7731.
14. Novitsky V, Gilbert P, Peter T, McLane MF, Gaolekwe S, Rybak N, Thior I, Ndung'u T, Marlink R, Lee TH, Essex M. 2003. Association between virus-specific T-cell responses and plasma viral load in human immunodeficiency virus type 1 subtype C infection. J. Virol. 77:882-890.
15. Zuniga R, Lucchetti A, Galvan P, Sanchez S, Sanchez C, Hernandez A, Sanchez H, Frahm N, Linde CH, Hewitt HS, Hildebrand W, Altfeld M, Allen TM, Walker BD, Korber BT, Leitner T, Sanchez J, Brander C. 2006. Relative dominance of Gag p24-specific cytotoxic T lymphocytes is associated with human immunodeficiency virus control. J. Virol. 80: 3122-3125.
16. Boutwell CL, Rowley CF, Essex M. 2009. Reduced viral replication capacity of human immunodeficiency virus type 1 subtype C caused by cytotoxic-T-lymphocyte escape mutations in HLA-B57 epitopes of capsid protein. J. Virol. 83:2460-2468.
17. Crawford H, Lumm W, Leslie A, Schaefer M, Boeras D, Prado JG, Tang J, Farmer P, Ndung'u T, Lakhi S, Gilmour J, Goepfert P, Walker BD, Kaslow R, Mulenga J, Allen S, Goulder PJ, Hunter E. 2009. Evolution of HLA-B*5703 HIV-1 escape mutations in HLA-B*5703-positive individuals and their transmission recipients. J. Exp. Med. 206:909-921.
18. Crawford H, Prado JG, Leslie A, Hue S, Honeyborne I, Reddy S, van der Stok M, Mncube Z, Brander C, Rousseau C, Mullins JI, Kaslow R, Goepfert P, Allen S, Hunter E, Mulenga J, Kiepiela P, Walker BD, Goulder PJ. 2007. Compensatory mutation partially restores fitness and delays reversion of escape mutation within the immunodominant HLAB* 5703-restricted Gag epitope in chronic human immunodeficiency virus type 1 infection. J. Virol. 81:8346-8351.
19. Martinez-Picado J, Prado JG, Fry EE, Pfafferott K, Leslie A, Chetty S, Thobakgale C, Honeyborne I, Crawford H, Matthews P, Pillay T, Rousseau C, Mullins JI, Brander C, Walker BD, Stuart DI, Kiepiela P, Goulder P. 2006. Fitness cost of escape mutations in p24 Gag in association with control of human immunodeficiency virus type 1. J. Virol. 80: 3617-3623.
20. Miura T, Brockman MA, Schneidewind A, Lobritz M, Pereyra F, Rathod A, Block BL, Brumme ZL, Brumme CJ, Baker B, Rothchild AC, Li B, Trocha A, Cutrell E, Frahm N, Brander C, Toth I, Arts EJ, Allen TM, Walker BD. 2009. HLA-B57/B*5801 human immunodeficiency virus type 1 elite controllers select for rare Gag variants associated with reduced viral replication capacity and strong cytotoxic T-lymphocyte [corrected] recognition. J. Virol. 83:2743-2755.
21. Schneidewind A, Brockman MA, Sidney J, Wang YE, Chen H, Suscovich TJ, Li B, Adam RI, Allgaier RL, Mothe BR, Kuntzen T, Oniangue-Ndza C, Trocha A, Yu XG, Brander C, Sette A, Walker BD, Allen TM. 2008. Structural and functional constraints limit options for cytotoxic T-lymphocyte escape in the immunodominant HLA-B27-restricted epitope in human immunodeficiency virus type 1 capsid. J. Virol. 82: 5594-5605.
22. Schneidewind A. Brockman MA, Yang R, Adam RI, Li B, Le Gall S, Rinaldo CR, Craggs SL, Allgaier RL, Power KA, Kuntzen T, Tung CS, LaBute MX, Mueller SM, Harrer T, McMichael AJ, Goulder PJ, Aiken C, Brander C, Kelleher AD, Allen TM. 2007. Escape from the dominant HLA-B27-restricted cytotoxic T-lymphocyte response in Gag is associated with a dramatic reduction in human immunodeficiency virus type 1 replication. J. Virol. 81:12382-12393.
23. Wright JK, Naidoo VL, Brumme ZL, Prince JL, Claiborne DT, Goulder PJ, Brockman MA, Hunter E, Ndung'u T. 2012. Impact of HLA-B*81-associated mutations in HIV-1 Gag on viral replication capacity. J. Virol. 86:3193-3199.
24. Almeida JR, Price DA, Papagno L, Arkoub ZA, Sauce D, Bornstein E, Asher TE, Samri A, Schnuriger A, Theodorou I, Costagliola D, Rouzioux C, Agut H, Marcelin AG, Douek D, Autran B, Appay V. 2007. Superior control of HIV-1 replication by CD8+T cells is reflected by their avidity, polyfunctionality, and clonal turnover. J. Exp. Med. 204:2473-2485.
25. Chen H, Ndhlovu ZM, Liu D, Porter LC, Fang JW, Darko S, Brockman MA, Miura T, Brumme ZL, Schneidewind A, Piechocka-Trocha A, Cesa KT, Sela J, Cung TD, Toth I, Pereyra F, Yu XG, Douek DC, Kaufmann DE, Allen TM, Walker BD. 2012. TCR clonotypes modulate the protective effect of HLA class I molecules in HIV-1 infection. Nat. Immunol. 13:691-700.
26. Dahirel V, Shekhar K, Pereyra F, Miura T, Artyomov M, Talsania S, Allen TM, Altfeld M, Carrington M, Irvine DJ, Walker BD, Chakraborty AK. 2011. Coordinate linkage of HIV evolution reveals regions of immunological vulnerability. Proc. Natl. Acad. Sci. U. S. A. 108: 11530-11535.
27. Perez CL, Larsen MV, Gustafsson R, Norstrom MM, Atlas A, Nixon DF, Nielsen M, Lund O, Karlsson AC. 2008. Broadly immunogenic HLA class I supertype-restricted elite CTL epitopes recognized in a diverse population infected with different HIV-1 subtypes. J. Immunol. 180:5092-5100.
28. Berger CT, Frahm N, Price DA, Mothe B, Ghebremichael M, Hartman KL, Henry LM, Brenchley JM, Ruff LE, Venturi V, Pereyra F, Sidney J, Sette A, Douek DC, Walker BD, Kaufmann DE, Brander C. 2011. High-functional-avidity cytotoxic T lymphocyte responses to HLA-Brestricted Gag-derived epitopes associated with relative HIV control. J. Virol. 85:9334-9345.
29. Betts MR, Nason MC, West SM, De Rosa SC, Migueles SA, Abraham J, Lederman MM, Benito JM, Goepfert PA, Connors M, Roederer M, Koup RA. 2006. HIV nonprogressors preferentially maintain highly functional HIV-specific CD8+ T cells. Blood 107:4781-4789.
30. Vingert B, Benati D, Lambotte O, de Truchis P, Sama L, Jeannin P, Galperin M, Perez-Patrigeon S, Boufassa F, Kwok WW, Lemaitre F, Delfraissy JF, Theze J, Chakrabarti LA. 2012. HIV controllers maintain a population of highly efficient Th1 effector cells in contrast to patients treated in the long term. J. Virol. 86:10661-10674.
31. Day CL, Kaufmann DE, Kiepiela P, Brown JA, Moodley ES, Reddy S, Mackey EW, Miller JD, Leslie AJ, DePierres C, Mncube Z, Duraiswamy J, Zhu B, Eichbaum Q, Altfeld M, Wherry EJ, Coovadia HM, Goulder PJ, Klenerman P, Ahmed R, Freeman GJ, Walker BD. 2006. PD-1 expression on HIV-specific T cells is associated with T-cell exhaustion and disease progression. Nature 443:350-354.
32. Hersperger AR, Pereyra F, Nason M, Demers K, Sheth P, Shin LY, Kovacs CM, Rodriguez B, Sieg SF, Teixeira-Johnson L, Gudonis D, Goepfert PA, Lederman MM, Frank I, Makedonas G, Kaul R, Walker BD, Betts MR. 2010. Perforin expression directly ex vivo by HIV-specific CD8 T-cells is a correlate of HIV elite control. PLoS Pathog. 6:e1000917. doi:10.1371/journal.ppat.1000917.
33. Migueles SA, Laborico AC, Shupert WL, Sabbaghian MS, Rabin R, Hallahan CW, Van Baarle D, Kostense S, Miedema F, McLaughlin M, Ehler L, Metcalf J, Liu S, Connors M. 2002. HIV-specific CD8+ T cell proliferation is coupled to perforin expression and is maintained in nonprogressors. Nat. Immunol. 3:1061-1068.
34. Migueles SA, Osborne CM, Royce C, Compton AA, Joshi RP, Weeks KA, Rood JE, Berkley AM, Sacha JB, Cogliano-Shutta NA, Lloyd M, Roby G, Kwan R, McLaughlin M, Stallings S, Rehm C, O'Shea MA, Mican J, Packard BZ, Komoriya A, Palmer S, Wiegand AP, Maldarelli F, Coffin JM, Mellors JW, Hallahan CW, Follman DA, Connors M. 2008. Lytic granule loading of CD8+ T cells is required for HIV-infected cell elimination associated with immune control. Immunity 29:1009-1021.
35. Deeks SG, Walker BD. 2007. Human immunodeficiency virus controllers: mechanisms of durable virus control in the absence of antiretroviral therapy. Immunity 27:406-416.
36. Theze J, Chakrabarti LA, Vingert B, Porichis F, Kaufmann DE. 2011. HIV controllers: a multifactorial phenotype of spontaneous viral suppression. Clin. Immunol. 141:15-30.
37. Blankson JN. 2010. Control of HIV-1 replication in elite suppressors. Discov. Med. 9:261-266.
38. Battivelli E, Migraine J, Lecossier D, Yeni P, Clavel F, Hance AJ. 2011. Gag cytotoxic T lymphocyte escape mutations can increase sensitivity of HIV-1 to human TRIM5alpha, linking intrinsic and acquired immunity. J. Virol. 85:11846-11854.
39. Stremlau M, Perron M, Lee M, Li Y, Song B, Javanbakht H, Diaz-Griffero F, Anderson DJ, Sundquist WI, Sodroski J. 2006. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc. Natl. Acad. Sci. U. S. A. 103:5514-5519.
40. Kim J, Tipper C, Sodroski J. 2011. Role of the TRIM5α RING domain E3 ubiquitin ligase activity in capsid disassembly, reverse transcription blockade and restriction of simian immunodeficiency virus. J. Virol. 85:8116-8132.
41. Pertel T, Hausmann S, Morger D, Zuger S, Guerra J, Lascano J, Reinhard C, Santoni FA, Uchil PD, Chatel L, Bisiaux A, Albert ML, Strambio-De-Castillia C, Mothes W, Pizzato M, Grutter MG, Luban J. 2011. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 472:361-365.
42. Johnson WE, Sawyer SL. 2009. Molecular evolution of the antiretroviral TRIM5 gene. Immunogenetics 61:163-176.
43. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, Sodroski J. 2004. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427:848-853.
44. Battivelli E, Lecossier D, Matsuoka S, Migraine J, Clavel F, Hance AJ. 2010. Strain-specific differences in the impact of human TRIM5alpha, different TRIM5alpha alleles, and the inhibition of capsid-cyclophilin A interactions on the infectivity of HIV-1. J. Virol. 84:11010-11019.
45. Hatziioannou T, Perez-Caballero D, Cowan S, Bieniasz PD. 2005. Cyclophilin interactions with incoming human immunodeficiency virus type 1 capsids with opposing effects on infectivity in human cells. J. Virol. 79:176-183.
46. Keckesova Z, Ylinen LM, Towers GJ. 2006. Cyclophilin A renders human immunodeficiency virus type 1 sensitive to Old World monkey but not human TRIM5 alpha antiviral activity. J. Virol. 80:4683-4690.
47. Sokolskaja E, Berthoux L, Luban J. 2006. Cyclophilin A and TRIM5alpha independently regulate human immunodeficiency virus type 1 infectivity in human cells. J. Virol. 80:2855-2862.
48. Stremlau M, Song B, Javanbakht H, Perron M, Sodroski J. 2006. Cyclophilin A: an auxiliary but not necessary cofactor for TRIM5alpha restriction of HIV-1. Virology 351:112-120.
49. Letvin NL, Rao SS, Montefiori DC, Seaman MS, Sun Y, Lim SY, Yeh WW, Asmal M, Gelman RS, Shen L, Whitney JB, Seoighe C, Lacerda M, Keating S, Norris PJ, Hudgens MG, Gilbert PB, Buzby AP, Mach LV, Zhang J, Balachandran H, Shaw GM, Schmidt SD, Todd JP, Dodson A, Mascola JR, Nabel GJ. 2011. Immune and genetic correlates of vaccine protection against mucosal infection by SIV in monkeys. Sci. Transl. Med. 3:81ra36.
50. Lim SY, Chan T, Gelman RS, Whitney JB, O'Brien KL, Barouch DH, Goldstein DB, Haynes BF, Letvin NL. 2010. Contributions of Mamu-A*01 status and TRIM5 allele expression, but not CCL3L copy number variation, to the control of SIVmac251 replication in Indian-origin rhesus monkeys. PLoS Genet. 6:e1000997. doi:10.1371/journal.pgen.1000997.
51. Lim SY, Rogers T, Chan T, Whitney JB, Kim J, Sodroski J, Letvin NL. 2010. TRIM5alpha modulates immunodeficiency virus control in rhesus monkeys. PLoS Pathog. 6:e1000738. doi:10.1371/journal.ppat.1000738.
52. Rogers TF, Lim SY, Sundsvold TJ, Chan T, Hsu A, Letvin NL. 2010. Variability in a dominant block to SIV early reverse transcription in rhesus monkey cells predicts in vivo viral replication and time to death. Virol. J. 7:79.
53. Jordan M, Wurm F. 2004. Transfection of adherent and suspended cells by calcium phosphate. Methods 33:136-143.
54. Matsuoka S, Dam E, Lecossier D, Clavel F, Hance AJ. 2009. Modulation of HIV-1 infectivity and cyclophilin A-dependence by Gag sequence and target cell type. Retrovirology 6:21.
55. Nora T, Bouchonnet F, Labrosse B, Charpentier C, Mammano F, Clavel F, Hance AJ. 2008. Functional diversity of HIV-1 envelope proteins expressed by contemporaneous plasma viruses. Retrovirology 5:23.
56. Lacabaratz-Porret C, Urrutia A, Doisne JM, Goujard C, Deveau C, Dalod M, Meyer L, Rouzioux C, Delfraissy JF, Venet A, Sinet M. 2003. Impact of antiretroviral therapy and changes in virus load on human immunodeficiency virus (HIV)-specific T cell responses in primary HIV infection. J. Infect. Dis. 187:748-757.
57. Matthews PC, Leslie AJ, Katzourakis A, Crawford H, Payne R, Prendergast A, Power K, Kelleher AD, Klenerman P, Carlson J, Heckerman D, Ndung'u T, Walker BD, Allen TM, Pybus OG, Goulder PJ. 2009. HLA footprints on human immunodeficiency virus type 1 are associated with interclade polymorphisms and intraclade phylogenetic clustering. J. Virol. 83:4605-4615.
58. McMichael A, Klenerman P. 2002. HIV/AIDS. HLA leaves its footprints on HIV. Science 296:1410-1411.
59. Descamps D, Chaix ML, Montes B, Pakianather S, Charpentier C, Storto A, Barin F, Dos Santos G, Krivine A, Delaugerre C, Izopet J, Marcelin AG, Maillard A, Morand-Joubert L, Pallier C, Plantier JC, Tamalet C, Cottalorda J, Desbois D, Calvez V, Brun-Vezinet F, Masquelier B, Costagliola D. 2010. Increasing prevalence of transmitted drug resistance mutations and non-B subtype circulation in antiretroviralnaive chronically HIV-infected patients from 2001 to 2006/2007 in France. J. Antimicrob. Chemother. 65:2620-2627.
60. Fleury H, Recordon-Pinson P, Caumont A, Faure M, Roques P, Plantier JC, Couturier E, Dormont D, Masquelier B, Simon F. 2003. HIV type 1 diversity in France, 1999-2001: molecular characterization of non-B HIV type 1 subtypes and potential impact on susceptibility to antiretroviral drugs. AIDS Res. Hum. Retroviruses 19:41-47.
61. Brockman M.A. Schneidewind A, Lahaie M, Schmidt A, Miura T, Desouza I, Ryvkin F, Derdeyn CA, Allen S, Hunter E, Mulenga J, Goepfert PA, Walker BD, Allen TM. 2007. Escape and compensation from early HLA-B57-mediated cytotoxic T-lymphocyte pressure on human immunodeficiency virus type 1 Gag alter capsid interactions with cyclophilin A. J. Virol. 81:12608-12618.
62. Leslie AJ, Pfafferott KJ, Chetty P, Draenert R, Addo MM, Feeney M, Tang Y, Holmes EC, Allen T, Prado JG, Altfeld M, Brander C, Dixon C, Ramduth D, Jeena P, Thomas SA, St. John A, Roach TA, Kupfer B, Luzzi G, Edwards A, Taylor G, Lyall H, Tudor-Williams G, Novelli V, Martinez-Picado J, Kiepiela P, Walker BD, Goulder PJ. 2004. HIV evolution: CTL escape mutation and reversion after transmission. Nat. Med. 10:282-289.
63. Altfeld M, Addo MM, Rosenberg ES, Hecht FM, Lee PK, Vogel M, Yu XG, Draenert R, Johnston MN, Strick D, Allen TM, Feeney ME, Kahn JO, Sekaly RP, Levy JA, Rockstroh JK, Goulder PJ, Walker BD. 2003. Influence of HLA-B57 on clinical presentation and viral control during acute HIV-1 infection. AIDS 17:2581-2591.
64. Altfeld M, Kalife ET, Qi Y, Streeck H, Lichterfeld M, Johnston MN, Burgett N, Swartz ME, Yang A, Alter G, Yu XG, Meier A, Rockstroh JK, Allen TM, Jessen H, Rosenberg ES, Carrington M, Walker BD. 2006. HLA alleles associated with delayed progression to AIDS contribute strongly to the initial CD8(+) T cell response against HIV-1. PLoS Med. 3:e403. doi:10.1371/journal.pmed.0030403.
65. Schneidewind A, Tang Y, Brockman MA, Ryland EG, Dunkley-Thompson J, Steel-Duncan JC, St. John MA, Conrad JA, Kalams SA, Noel F, Allen TM, Christie CD, Feeney ME. 2009. Maternal transmission of human immunodeficiency virus escape mutations subverts HLA-B57 immunodominance but facilitates viral control in the haploidentical infant. J. Virol. 83:8616-8627.
66. Ladell K, Hashimoto M, Iglesias MC, Wilmann PG, McLaren JE, Gras S, Chikata T, Kuse N, Fastenackels S, Gostick E, Bridgeman JS, Venturi V, Arkoub ZA, Agut H, van Bockel DJ, Almeida JR, Douek DC, Meyer L, Venet A, Takiguchi M, Rossjohn J, Price DA, Appay V. 2013. A molecular basis for the control of preimmune escape variants by HIVspecific CD8(+) T cells. Immunity 38:425-436.
67. Kelleher AD, Long C, Holmes EC, Allen RL, Wilson J, Conlon C, Workman C, Shaunak S, Olson K, Goulder P, Brander C, Ogg G, Sullivan JS, Dyer W, Jones I, McMichael AJ, Rowland-Jones S, Phillips RE. 2001. Clustered mutations in HIV-1 Gag are consistently required for escape from HLA-B27-restricted cytotoxic T lymphocyte responses. J. Exp. Med. 193:375-386.
68. Schneidewind A, Brumme ZL, Brumme CJ, Power KA, Reyor LL, O'Sullivan K, Gladden A, Hempel U, Kuntzen T, Wang YE, Oniangue-Ndza C, Jessen H, Markowitz M, Rosenberg ES, Sekaly RP, Kelleher AD, Walker BD, Allen TM. 2009. Transmission and long-term stability of compensated CD8 escape mutations. J. Virol. 83:3993-3997.
69. Streeck H, Li B, Poon AF, Schneidewind A, Gladden AD, Power KA, Daskalakis D, Bazner S, Zuniga R, Brander C, Rosenberg ES, Frost SD, Altfeld M, Allen TM. 2008. Immune-driven recombination and loss of control after HIV superinfection. J. Exp. Med. 205:1789-1796.
70. Feeney ME, Tang Y, Roosevelt KA, Leslie AJ, McIntosh K, Karthas N, Walker BD, Goulder PJ. 2004. Immune escape precedes breakthrough human immunodeficiency virus type 1 viremia and broadening of the cytotoxic T-lymphocyte response in an HLA-B27-positive long-termnonprogressing child. J. Virol. 78:8927-8930.
71. Goulder PJ, Phillips RE, Colbert RA, McAdam S, Ogg G, Nowak MA, Giangrande P, Luzzi G, Morgan B, Edwards A, McMichael AJ, Rowland-Jones S. 1997. Late escape from an immunodominant cytotoxic T-lymphocyte response associated with progression to AIDS. Nat. Med. 3:212-217.
72. Bailey JR, Williams TM, Siliciano RF, Blankson JN. 2006. Maintenance of viral suppression in HIV-1-infected HLA-B*57+ elite suppressors despite CTL escape mutations. J. Exp. Med. 203:1357-1369.
73. Durand CM, O'Connell KA, Apuzzo LG, Langan SJ, Imteyaz H, Ahonkhai AA, Ceccato CM, Williams TM, Margolick JB, Blankson JN. 2010. HIV-1 Gag evolution in recently infected human leukocyte antigen-B*57 patients with low-level viremia. AIDS 24:2405-2408.
74. O'Connell KA, Brennan TP, Bailey JR, Ray SC, Siliciano RF, Blankson JN. 2010. Control of HIV-1 in elite suppressors despite ongoing replication and evolution in plasma virus. J. Virol. 84:7018-7028.
75. Migueles SA, Laborico AC, Imamichi H, Shupert WL, Royce C, McLaughlin M, Ehler L, Metcalf J, Liu S, Hallahan CW, Connors M. 2003. The differential ability of HLA B*5701+long-term nonprogressors and progressors to restrict human immunodeficiency virus replication is not caused by loss of recognition of autologous viral Gag sequences. J. Virol. 77:6889-6898.
76. Kirmaier A, Wu F, Newman RM, Hall LR, Morgan JS, O'Connor S, Marx PA, Meythaler M, Goldstein S, Buckler-White A, Kaur A, Hirsch VM, Johnson WE. 2010. TRIM5 suppresses cross-species transmission of a primate immunodeficiency virus and selects for emergence of resistant variants in the new species. PLoS Biol. 8:e1000462. doi:10.1371/journal .pbio.1000462.
77. Barbour JD, Hecht FM, Wrin T, Segal MR, Ramstead CA, Liegler TJ, Busch MP, Petropoulos CJ, Hellmann NS, Kahn JO, Grant RM. 2004. Higher CD4+ T cell counts associated with low viral pol replication capacity among treatment-naive adults in early HIV-1 infection. J. Infect. Dis. 190:251-256.
78. Deeks SG, Wrin T, Liegler T, Hoh R, Hayden M, Barbour JD, Hellmann NS, Petropoulos CJ, McCune JM, Hellerstein MK, Grant RM. 2001. Virologic and immunologic consequences of discontinuing combination antiretroviral-drug therapy in HIV-infected patients with detectable viremia. N. Engl. J. Med. 344:472-480.
79. Nijhuis M, Deeks S, Boucher C. 2001. Implications of antiretroviral resistance on viral fitness. Curr. Opin. Infect. Dis. 14:23-28.
80. Norstrom MM, Buggert M, Tauriainen J, Hartogensis W, Prosperi MC, Wallet MA, Hecht FM, Salemi M, Karlsson AC. 2012. Combination of immune and viral factors distinguishes low-risk versus high-risk HIV-1 disease progression in HLA-B*5701 subjects. J. Virol. 86:9802-9816.
81. Feeney ME, Tang Y, Pfafferott K, Roosevelt KA, Draenert R, Trocha A, Yu XG, Verrill C, Allen T, Moore C, Mallal S, Burchett S, McIntosh K, Pelton SI, St. John MA, Hazra R, Klenerman P, Altfeld M, Walker BD, Goulder PJ. 2005. HIV-1 viral escape in infancy followed by emergence of a variant-specific CTL response. J. Immunol. 174:7524-7530.
82. von Schwedler UK, Stray KM, Garrus JE, Sundquist WI. 2003. Functional surfaces of the human immunodeficiency virus type 1 capsid protein. J. Virol. 77:5439-5450.
83. Rahm N, Gfeller D, Snoeck J, Martinez R, McLaren PJ, Ortiz M, Ciuffi A, Telenti A. 2013. Susceptibility and adaptation to human TRIM5alpha alleles at positive selected sites in HIV-1 capsid. Virology 441:162-170.
84. Sewram S, Singh R, Kormuth E, Werner L, Mlisana K, Karim SS, Ndung'u T. 2009. Human TRIM5alpha expression levels and reduced susceptibility to HIV-1 infection. J. Infect. Dis. 199:1657-1663.
85. Cagliani R, Fumagalli M, Biasin M, Piacentini L, Riva S, Pozzoli U, Bonaglia MC, Bresolin N, Clerici M, Sironi M. 2010. Long-term balancing selection maintains trans-specific polymorphisms in the human TRIM5 gene. Hum. Genet. 128:577-588.
86. Carthagena L, Parise MC, Ringeard M, Chelbi-Alix MK, Hazan U, Nisole S. 2008. Implication of TRIM alpha and TRIMCyp in interferoninduced anti-retroviral restriction activities. Retrovirology 5:59.
87. Sakuma R, Mael AA, Ikeda Y. 2007. Alpha interferon enhances TRIM5alpha-mediated antiviral activities in human and rhesus monkey cells. J. Virol. 81:10201-10206.
88. Battivelli E, Migraine J, Lecossier D, Matsuoka S, Perez-Bercoff D, Saragosti S, Clavel F, Hance AJ. 2011. Modulation of TRIM5alpha activity in human cells by alternatively spliced TRIM5 isoforms. J. Virol. 85:7828-7835.
89. Goldschmidt V, Bleiber G, May M, Martinez R, Ortiz M, Telenti A. 2006. Role of common human TRIM5alpha variants in HIV-1 disease progression. Retrovirology 3:54.
90. Javanbakht H, An P, Gold B, Petersen DC, O'Huigin C, Nelson GW, O'Brien SJ, Kirk GD, Detels R, Buchbinder S, Donfield S, Shulenin S, Song B, Perron MJ, Stremlau M, Sodroski J, Dean M, Winkler C. 2006. Effects of human TRIM5alpha polymorphisms on antiretroviral function and susceptibility to human immunodeficiency virus infection. Virology 354:15-27.
91. Liu FL, Qiu YQ, Li H, Kuang YQ, Tang X, Cao G, Tang NL, Zheng YT. 2011. An HIV-1 resistance polymorphism in TRIM5alpha gene among Chinese intravenous drug users. J. Acquir. Immune Defic. Syndr. 56:306-311.
92. Nakajima T, Nakayama EE, Kaur G, Terunuma H, Mimaya JI, Ohtani H, Mehra N, Shioda T, Kimura A. 2009. Impact of novel TRIM5alpha variants, Gly110Arg and G176del, on the anti-HIV-1 activity and the susceptibility to HIV-1 infection. AIDS 23:2091-2100.
93. Nakayama EE, Carpentier W, Costagliola D, Shioda T, Iwamoto A, Debre P, Yoshimura K, Autran B, Matsushita S, Theodorou I. 2007. Wild type and H43Y variant of human TRIM5alpha show similar antihuman immunodeficiency virus type 1 activity both in vivo and in vitro. Immunogenetics 59:511-515.
94. Price H, Lacap P, Tuff J, Wachihi C, Kimani J, Ball TB, Luo M, Plummer FA. 2010. A TRIM5alpha exon 2 polymorphism is associated with protection from HIV-1 infection in the Pumwani sex worker cohort. AIDS 24:1813-1821.
95. Sawyer SL, Wu LI, Akey JM, Emerman M, Malik HS. 2006. Highfrequency persistence of an impaired allele of the retroviral defense gene TRIM5alpha in humans. Curr. Biol. 16:95-100.
96. Speelmon EC, Livingston-Rosanoff D, Li SS, Vu Q, Bui J, Geraghty DE, Zhao LP, McElrath MJ. 2006. Genetic association of the antiviral restriction factor TRIM5alpha with human immunodeficiency virus type 1 infection. J. Virol. 80:2463-2471.
97. van Manen D, Rits MA, Beugeling C, van Dort K, Schuitemaker H, Kootstra NA. 2008. The effect of Trim5 polymorphisms on the clinical course of HIV-1 infection. PLoS Pathog. 4:e18. doi:10.1371/journal.ppat .0040018.
98. Saez-Cirion A, Hamimi C, Bergamaschi A, David A, Versmisse P, Melard A, Boufassa F, Barre-Sinoussi F, Lambotte O, Rouzioux C, Pancino G. 2011. Restriction of HIV-1 replication in macrophages and CD4+ T cells from HIV controllers. Blood 118:955-964.
99. Watts JM, Dang KK, Gorelick RJ, Leonard CW, Bess JW, Jr, Swanstrom R, Burch CL, Weeks KM. 2009. Architecture and secondary structure of an entire HIV-1 RNA genome. Nature 460:711-716.