High level of susceptibility to human TRIM5α conferred by HIV-2 capsid sequences

Retrovirology

Volumn 10, Issue 1, 2013, Pages

  Takeuchi, Junko S ^a,b   Perche, Benjamin ^a,b   Migraine, Julie ^a,b   Mercier Delarue, Séverine ^c   Ponscarme, Diane ^c   Simon, François ^a,c   Clavel, François ^a,b,c   Labrosse, Béatrice ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DIDEROT   (France)

^c SAINT LOUIS HOSPITAL   (France)

Author keywords

Capsid sequences; Human TRIM5 restriction factor; Primary HIV 2 strains

Indexed keywords

CAPSID PROTEIN; TRIPARTITE MOTIF PROTEIN 5;

ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA SEQUENCE; SENSITIVITY ANALYSIS; SEQUENCE ANALYSIS; VIRUS CAPSID; VIRUS IDENTIFICATION; VIRUS INFECTIVITY; VIRUS LOAD; VIRUS STRAIN;

CAPSID PROTEINS; CARRIER PROTEINS; HIV-2; HUMANS; PROTEIN STABILITY;

CERCOCEBUS TORQUATUS ATYS; CERCOPITHECINE HERPESVIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; MIRIDAE; PRIMATES;

EID: 84877035627     PISSN: None     EISSN: 17424690     Source Type: Journal    
DOI: 10.1186/1742-4690-10-50     Document Type: Article

References (57)

1. Luban J. Cyclophilin A, TRIM5, and resistance to human immunodeficiency virus type 1 infection. J Virol 2007, 81:1054-1061. 10.1128/JVI.01519-06, 1797489, 16956947.
2. 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, 427:848-853. 10.1038/nature02343, 14985764.
3. Towers GJ. The control of viral infection by tripartite motif proteins and cyclophilin A. Retrovirology 2007, 4:40. 10.1186/1742-4690-4-40, 1906832, 17565686.
4. Pertel T, Hausmann S, Morger D, Zuger S, Guerra J, Lascano J, Reinhard C, Santoni FA, Uchil PD, Chatel L, et al. TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 2011, 472:361-365. 10.1038/nature09976, 3081621, 21512573.
5. Stremlau M, Perron M, Lee M, Li Y, Song B, Javanbakht H, Diaz-Griffero F, Anderson DJ, Sundquist WI, Sodroski J. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc Natl Acad Sci USA 2006, 103:5514-5519. 10.1073/pnas.0509996103, 1459386, 16540544.
6. Kaiser SM, Malik HS, Emerman M. Restriction of an extinct retrovirus by the human TRIM5alpha antiviral protein. Science 2007, 316:1756-1758. 10.1126/science.1140579, 17588933.
7. Newman RM, Johnson WE. A brief history of TRIM5alpha. AIDS Rev 2007, 9:114-125.
8. Hatziioannou T, Perez-Caballero D, Cowan S, Bieniasz PD. Cyclophilin interactions with incoming human immunodeficiency virus type 1 capsids with opposing effects on infectivity in human cells. J Virol 2005, 79:176-183. 10.1128/JVI.79.1.176-183.2005, 538701, 15596813.
9. Keckesova Z, Ylinen LM, Towers GJ. Cyclophilin A renders human immunodeficiency virus type 1 sensitive to Old World monkey but not human TRIM5 alpha antiviral activity. J Virol 2006, 80:4683-4690. 10.1128/JVI.80.10.4683-4690.2006, 1472055, 16641261.
10. Sokolskaja E, Berthoux L, Luban J. Cyclophilin A and TRIM5alpha independently regulate human immunodeficiency virus type 1 infectivity in human cells. J Virol 2006, 80:2855-2862. 10.1128/JVI.80.6.2855-2862.2006, 1395419, 16501094.
11. Stremlau M, Song B, Javanbakht H, Perron M, Sodroski J. Cyclophilin A: an auxiliary but not necessary cofactor for TRIM5alpha restriction of HIV-1. Virology 2006, 351:112-120. 10.1016/j.virol.2006.03.015, 16643975.
12. Battivelli E, Lecossier D, Matsuoka S, Migraine J, Clavel F, Hance AJ. 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 2010, 84:11010-11019. 10.1128/JVI.00758-10, 2953162, 20702630.
13. Battivelli E, Migraine J, Lecossier D, Yeni P, Clavel F, Hance AJ. Gag cytotoxic T lymphocyte escape mutations can increase sensitivity of HIV-1 to human TRIM5alpha, linking intrinsic and acquired immunity. J Virol 2011, 85:11846-11854. 10.1128/JVI.05201-11, 3209307, 21917976.
14. Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, Cummins LB, Arthur LO, Peeters M, Shaw GM, et al. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 1999, 397:436-441. 10.1038/17130, 9989410.
15. Ortiz M, Bleiber G, Martinez R, Kaessmann H, Telenti A. Patterns of evolution of host proteins involved in retroviral pathogenesis. Retrovirology 2006, 3:11. 10.1186/1742-4690-3-11, 1409793, 16460575.
16. Cagliani R, Fumagalli M, Biasin M, Piacentini L, Riva S, Pozzoli U, Bonaglia MC, Bresolin N, Clerici M, Sironi M. Long-term balancing selection maintains trans-specific polymorphisms in the human TRIM5 gene. Hum Genet 2010, 128:577-588. 10.1007/s00439-010-0884-6, 20811909.
17. de Silva TI, Cotten M, Rowland-Jones SL. HIV-2: the forgotten AIDS virus. Trends Microbiol 2008, 16:588-595. 10.1016/j.tim.2008.09.003, 18964021.
18. Lemey P, Pybus OG, Wang B, Saksena NK, Salemi M, Vandamme AM. Tracing the origin and history of the HIV-2 epidemic. Proc Natl Acad Sci USA 2003, 100:6588-6592. 10.1073/pnas.0936469100, 164491, 12743376.
19. Campbell-Yesufu OT, Gandhi RT. Update on human immunodeficiency virus (HIV)-2 infection. Clin Infect Dis 2011, 52:780-787. 10.1093/cid/ciq248, 3106263, 21367732.
20. Andersson S, Norrgren H, da Silva Z, Biague A, Bamba S, Kwok S, Christopherson C, Biberfeld G, Albert J. Plasma viral load in HIV-1 and HIV-2 singly and dually infected individuals in Guinea-Bissau, West Africa: significantly lower plasma virus set point in HIV-2 infection than in HIV-1 infection. Arch Intern Med 2000, 160:3286-3293. 10.1001/archinte.160.21.3286, 11088091.
21. Popper SJ, Sarr AD, Travers KU, Gueye-Ndiaye A, Mboup S, Essex ME, Kanki PJ. Lower human immunodeficiency virus (HIV) type 2 viral load reflects the difference in pathogenicity of HIV-1 and HIV-2. J Infect Dis 1999, 180:1116-1121. 10.1086/315010, 10479138.
22. Pandrea I, Silvestri G, Onanga R, Veazey RS, Marx PA, Hirsch V, Apetrei C. Simian immunodeficiency viruses replication dynamics in African non-human primate hosts: common patterns and species-specific differences. J Med Primatol 2006, 35:194-201. 10.1111/j.1600-0684.2006.00168.x, 16872282.
23. Silvestri G, Sodora DL, Koup RA, Paiardini M, O'Neil SP, McClure HM, Staprans SI, Feinberg MB. Nonpathogenic SIV infection of sooty mangabeys is characterized by limited bystander immunopathology despite chronic high-level viremia. Immunity 2003, 18:441-452. 10.1016/S1074-7613(03)00060-8, 12648460.
24. Apetrei C, Gautam R, Sumpter B, Carter AC, Gaufin T, Staprans SI, Else J, Barnes M, Cao R, Garg S, et al. Virus subtype-specific features of natural simian immunodeficiency virus SIVsmm infection in sooty mangabeys. J Virol 2007, 81:7913-7923. 10.1128/JVI.00281-07, 1951324, 17507488.
25. Jaffar S, Grant AD, Whitworth J, Smith PG, Whittle H. The natural history of HIV-1 and HIV-2 infections in adults in Africa: a literature review. Bull World Health Organ 2004, 82:462-469. 2622848, 15356940.
26. Shanmugam V, Switzer WM, Nkengasong JN, Garcia-Lerma G, Green TA, Ekpini E, Sassan-Morokro M, Antunes F, Manshino K, Soriano V, et al. Lower HIV-2 plasma viral loads may explain differences between the natural histories of HIV-1 and HIV-2 infections. J Acquir Immune Defic Syndr 2000, 24:257-263.
27. MacNeil A, Sarr AD, Sankale JL, Meloni ST, Mboup S, Kanki P. Direct evidence of lower viral replication rates in vivo in human immunodeficiency virus type 2 (HIV-2) infection than in HIV-1 infection. J Virol 2007, 81:5325-5330. 10.1128/JVI.02625-06, 1900238, 17329334.
28. Kashyap B, Gautam H, Chadha S, Bhalla P. Delayed progression and inefficient transmission of HIV-2. Southeast Asian J Trop Med Public Health 2010, 41:570-573.
29. Gottlieb GS, Hawes SE, Agne HD, Stern JE, Critchlow CW, Kiviat NB, Sow PS. Lower levels of HIV RNA in semen in HIV-2 compared with HIV-1 infection: implications for differences in transmission. AIDS 2006, 20:895-900. 10.1097/01.aids.0000218554.59531.80, 16549974.
30. De Cock KM, Adjorlolo G, Ekpini E, Sibailly T, Kouadio J, Maran M, Brattegaard K, Vetter KM, Doorly R, Gayle HD. Epidemiology and transmission of HIV-2. Why there is no HIV-2 pandemic. JAMA 1993, 270:2083-2086. 10.1001/jama.1993.03510170073033, 8147962.
31. da Silva ZJ, Oliveira I, Andersen A, Dias F, Rodrigues A, Holmgren B, Andersson S, Aaby P. Changes in prevalence and incidence of HIV-1, HIV-2 and dual infections in urban areas of Bissau, Guinea-Bissau: is HIV-2 disappearing?. AIDS 2008, 22:1195-1202. 10.1097/QAD.0b013e328300a33d, 18525265.
32. O'Donovan D, Ariyoshi K, Milligan P, Ota M, Yamuah L, Sarge-Njie R, Whittle H. Maternal plasma viral RNA levels determine marked differences in mother-to-child transmission rates of HIV-1 and HIV-2 in The Gambia. MRC/Gambia Government/University College London Medical School working group on mother-child transmission of HIV. AIDS 2000, 14:441-448. 10.1097/00002030-200003100-00019, 10770548.
33. Burgard M, Jasseron C, Matheron S, Damond F, Hamrene K, Blanche S, Faye A, Rouzioux C, Warszawski J, Mandelbro L. Mother-to-child transmission of HIV-2 infection from 1986 to 2007 in the ANRS French Perinatal Cohort EPF-CO1. Clin Infect Dis 2010, 51:833-843. 10.1086/656284, 20804413.
34. Damond F, Descamps D, Farfara I, Telles JN, Puyeo S, Campa P, Lepretre A, Matheron S, Brun-Vezinet F, Simon F. Quantification of proviral load of human immunodeficiency virus type 2 subtypes A and B using real-time PCR. J Clin Microbiol 2001, 39:4264-4268. 10.1128/JCM.39.12.4264-4268.2001, 88534, 11724830.
35. Damond F, Worobey M, Campa P, Farfara I, Colin G, Matheron S, Brun-Vezinet F, Robertson DL, Simon F. Identification of a highly divergent HIV type 2 and proposal for a change in HIV type 2 classification. AIDS Res Hum Retroviruses 2004, 20:666-672. 10.1089/0889222041217392, 15242544.
36. Gao F, Yue L, Robertson DL, Hill SC, Hui H, Biggar RJ, Neequaye AE, Whelan TM, Ho DD, Shaw GM, et al. Genetic diversity of human immunodeficiency virus type 2: evidence for distinct sequence subtypes with differences in virus biology. J Virol 1994, 68:7433-7447. 237186, 7933127.
37. Gao F, Yue L, White AT, Pappas PG, Barchue J, Hanson AP, Greene BM, Sharp PM, Shaw GM, Hahn BH. Human infection by genetically diverse SIVSM-related HIV-2 in west Africa. Nature 1992, 358:495-499. 10.1038/358495a0, 1641038.
38. Ylinen LM, Keckesova Z, Wilson SJ, Ranasinghe S, Towers GJ. Differential restriction of human immunodeficiency virus type 2 and simian immunodeficiency virus SIVmac by TRIM5alpha alleles. J Virol 2005, 79:11580-11587. 10.1128/JVI.79.18.11580-11587.2005, 1212619, 16140735.
39. Zhang F, Hatziioannou T, Perez-Caballero D, Derse D, Bieniasz PD. Antiretroviral potential of human tripartite motif-5 and related proteins. Virology 2006, 353:396-409. 10.1016/j.virol.2006.05.035, 16828831.
40. Clavel F, Guyader M, Guetard D, Salle M, Montagnier L, Alizon M. Molecular cloning and polymorphism of the human immune deficiency virus type 2. Nature 1986, 324:691-695. 10.1038/324691a0, 3025743.
41. Song H, Nakayama EE, Yokoyama M, Sato H, Levy JA, Shioda T. A single amino acid of the human immunodeficiency virus type 2 capsid affects its replication in the presence of cynomolgus monkey and human TRIM5alphas. J Virol 2007, 81:7280-7285. 10.1128/JVI.00406-07, 1933286, 17475650.
42. Onyango CO, Leligdowicz A, Yokoyama M, Sato H, Song H, Nakayama EE, Shioda T, de Silva T, Townend J, Jaye A, et al. HIV-2 capsids distinguish high and low virus load patients in a West African community cohort. Vaccine 2010, 28(Suppl 2):B60-67.
43. Nora T, Bouchonnet F, Labrosse B, Charpentier C, Mammano F, Clavel F, Hance AJ. Functional diversity of HIV-1 envelope proteins expressed by contemporaneous plasma viruses. Retrovirology 2008, 5:23. 10.1186/1742-4690-5-23, 2270869, 18312646.
44. Matsuoka S, Dam E, Lecossier D, Clavel F, Hance AJ. Modulation of HIV-1 infectivity and cyclophilin A-dependence by Gag sequence and target cell type. Retrovirology 2009, 6:21. 10.1186/1742-4690-6-21, 2653016, 19254360.
45. Chatterji U, Bobardt MD, Stanfield R, Ptak RG, Pallansch LA, Ward PA, Jones MJ, Stoddart CA, Scalfaro P, Dumont JM, et al. Naturally occurring capsid substitutions render HIV-1 cyclophilin A independent in human cells and TRIM-cyclophilin-resistant in Owl monkey cells. J Biol Chem 2005, 280:40293-40300. 10.1074/jbc.M506314200, 16199531.
46. Ptak RG, Gallay PA, Jochmans D, Halestrap AP, Ruegg UT, Pallansch LA, Bobardt MD, de Bethune MP, Neyts J, De Clercq E, et al. Inhibition of human immunodeficiency virus type 1 replication in human cells by Debio-025, a novel cyclophilin binding agent. Antimicrob Agents Chemother 2008, 52:1302-1317. 10.1128/AAC.01324-07, 2292519, 18212100.
47. Kawamura M, Sakai H, Adachi A. Human immunodeficiency virus Vpx is required for the early phase of replication in peripheral blood mononuclear cells. Microbiol Immunol 1994, 38:871-878.
48. Ibe S, Yokomaku Y, Shiino T, Tanaka R, Hattori J, Fujisaki S, Iwatani Y, Mamiya N, Utsumi M, Kato S, et al. HIV-2 CRF01_AB: first circulating recombinant form of HIV-2. J Acquir Immune Defic Syndr 2010, 54:241-247. 10.1097/QAI.0b013e3181dc98c1, 20502347.
49. Shibata R, Miura T, Hayami M, Ogawa K, Sakai H, Kiyomasu T, Ishimoto A, Adachi A. Mutational analysis of the human immunodeficiency virus type 2 (HIV-2) genome in relation to HIV-1 and simian immunodeficiency virus SIV (AGM). J Virol 1990, 64:742-747. 249168, 2296082.
50. Ryan-Graham MA, Peden KW. Both virus and host components are important for the manifestation of a Nef- phenotype in HIV-1 and HIV-2. Virology 1995, 213:158-168. 10.1006/viro.1995.1556, 7483259.
51. Chen Z, Luckay A, Sodora DL, Telfer P, Reed P, Gettie A, Kanu JM, Sadek RF, Yee J, Ho DD, et al. Human immunodeficiency virus type 2 (HIV-2) seroprevalence and characterization of a distinct HIV-2 genetic subtype from the natural range of simian immunodeficiency virus-infected sooty mangabeys. J Virol 1997, 71:3953-3960. 191547, 9094672.
52. Brennan CA, Yamaguchi J, Vallari AS, Hickman RK, Devare SG. Genetic variation in human immunodeficiency virus type 2: identification of a unique variant from human plasma. AIDS Res Hum Retroviruses 1997, 13:401-404. 10.1089/aid.1997.13.401, 9075481.
53. Novembre FJ, Johnson PR, Lewis MG, Anderson DC, Klumpp S, McClure HM, Hirsch VM. Multiple viral determinants contribute to pathogenicity of the acutely lethal simian immunodeficiency virus SIVsmmPBj variant. J Virol 1993, 67:2466-2474. 237565, 8474153.
54. Sugimoto C, Watanabe S, Naruse T, Kajiwara E, Shiino T, Umano N, Ueda K, Sato H, Ohgimoto S, Hirsch V, et al. Protection of macaques with diverse MHC genotypes against a heterologous SIV by vaccination with a deglycosylated live-attenuated SIV. PLoS One 2010, 5:e11678. 10.1371/journal.pone.0011678, 2907403, 20652030.
55. Hirsch V, Adger-Johnson D, Campbell B, Goldstein S, Brown C, Elkins WR, Montefiori DC. A molecularly cloned, pathogenic, neutralization-resistant simian immunodeficiency virus, SIVsmE543-3. J Virol 1997, 71:1608-1620. 191219, 8995688.
56. Hirsch VM, Olmsted RA, Murphey-Corb M, Purcell RH, Johnson PR. An African primate lentivirus (SIVsm) closely related to HIV-2. Nature 1989, 339:389-392. 10.1038/339389a0, 2786147.
57. Kestler H, Kodama T, Ringler D, Marthas M, Pedersen N, Lackner A, Regier D, Sehgal P, Daniel M, King N, et al. Induction of AIDS in rhesus monkeys by molecularly cloned simian immunodeficiency virus. Science 1990, 248:1109-1112. 10.1126/science.2160735, 2160735.