TRIM5 alpha Drives SIVsmm Evolution in Rhesus Macaques

PLoS Pathogens

Volumn 9, Issue 8, 2013, Pages

  Wu, Fan ^a   Kirmaier, Andrea ^b   Goeken, Robert ^a   Ourmanov, Ilnour ^a   Hall, Laura ^b   Morgan, Jennifer S ^b   Matsuda, Kenta ^a   Buckler White, Alicia ^a   Tomioka, Keiko ^a   Plishka, Ronald ^a   Whitted, Sonya ^a   Johnson, Welkin ^b   Hirsch, Vanessa M ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b BOSTON COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHYTOHEMAGGLUTININ; TRIPARTITE MOTIF PROTEIN 5; CARRIER PROTEIN;

ALLELE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; AREA UNDER THE CURVE; ARTICLE; CONTROLLED STUDY; EVOLUTION; GENE FREQUENCY; GENE MUTATION; GENOTYPE; HUMAN; HUMAN CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHYLOGENY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHESUS MONKEY; SIMIAN IMMUNODEFICIENCY VIRUS; SITE DIRECTED MUTAGENESIS; VIREMIA; VIRUS INFECTIVITY; VIRUS LOAD; VIRUS REPLICATION; ANIMAL; GENETICS; METABOLISM; MISSENSE MUTATION; MOLECULAR EVOLUTION; MOLECULAR GENETICS; PROTEIN SECONDARY STRUCTURE; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; TRANSMISSION;

ALLELES; AMINO ACID SUBSTITUTION; ANIMALS; BASE SEQUENCE; CARRIER PROTEINS; EVOLUTION, MOLECULAR; MACACA MULATTA; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PROTEIN STRUCTURE, SECONDARY; SIMIAN ACQUIRED IMMUNODEFICIENCY SYNDROME; SIMIAN IMMUNODEFICIENCY VIRUS; VIREMIA;

EID: 84883435285     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003577     Document Type: Article

References (80)

1. Hahn BH, Shaw GM, De Cock KM, Sharp PM, (2000) AIDS as a zoonosis: scientific and public health implications. Science 287: 607-614.
2. Sharp PM, Hahn BH, (2011) Origins of HIV and the AIDS pandemic. Cold Spring Harb Perspect Med 1: a006841.
3. Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, et al. (1999) Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397: 436-441.
4. Hirsch VM, Olmsted RA, Murphey-Corb M, Purcell RH, Johnson PR, (1989) An African primate lentivirus (SIVsm) closely related to HIV-2. Nature 339: 389-392.
5. Gao F, Yue L, White AT, Pappas PG, Barchue J, et al. (1992) Human infection by genetically diverse SIVSM-related HIV-2 in west Africa. Nature 358: 495-499.
6. Chen Z, Telfier P, Gettie A, Reed P, Zhang L, et al. (1996) Genetic characterization of new West African simian immunodeficiency virus SIVsm: geographic clustering of household-derived SIV strains with human immunodeficiency virus type 2 subtypes and genetically diverse viruses from a single feral sooty mangabey troop. J Virol 70: 3617-3627.
7. Jin MJ, Rogers J, Phillips-Conroy JE, Allan JS, Desrosiers RC, et al. (1994) Infection of a yellow baboon with simian immunodeficiency virus from African green monkeys: evidence for cross-species transmission in the wild. J Virol 68: 8454-8460.
8. van Rensburg EJ, Engelbrecht S, Mwenda J, Laten JD, Robson BA, et al. (1998) Simian immunodeficiency viruses (SIVs) from eastern and southern Africa: detection of a SIVagm variant from a chacma baboon. J Gen Virol 79 (Pt 7) (): 1809-1814.
9. Bailes E, Gao F, Bibollet-Ruche F, Courgnaud V, Peeters M, et al. (2003) Hybrid origin of SIV in chimpanzees. Science 300: 1713.
10. Malim MH, Bieniasz PD, (2012) HIV Restriction Factors and Mechanisms of Evasion. Cold Spring Harb Perspect Med 2: a006940.
11. Stremlau M, Owens CM, Perron MJ, Kiessling M, Autissier P, et al. (2004) The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427: 848-853.
12. Ylinen LM, Keckesova Z, Webb BL, Gifford RJ, Smith TP, et al. (2006) Isolation of an active Lv1 gene from cattle indicates that tripartite motif protein-mediated innate immunity to retroviral infection is widespread among mammals. J Virol 80: 7332-7338.
13. Diehl WE, Stansell E, Kaiser SM, Emerman M, Hunter E, (2008) Identification of postentry restrictions to Mason-Pfizer monkey virus infection in New World monkey cells. J Virol 82: 11140-11151.
14. Newman RM, Hall L, Kirmaier A, Pozzi LA, Pery E, et al. (2008) Evolution of a TRIM5-CypA splice isoform in old world monkeys. PLoS Pathog 4: e1000003.
15. Schaller T, Hue S, Towers GJ, (2007) An active TRIM5 protein in rabbits indicates a common antiviral ancestor for mammalian TRIM5 proteins. J Virol 81: 11713-11721.
16. Sayah DM, Sokolskaja E, Berthoux L, Luban J, (2004) Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430: 569-573.
17. Keckesova Z, Ylinen LM, Towers GJ, (2004) The human and African green monkey TRIM5alpha genes encode Ref1 and Lv1 retroviral restriction factor activities. Proc Natl Acad Sci U S A 101: 10780-10785.
18. Sawyer SL, Wu LI, Emerman M, Malik HS, (2005) Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci U S A 102: 2832-2837.
19. Hatziioannou T, Perez-Caballero D, Yang A, Cowan S, Bieniasz PD, (2004) Retrovirus resistance factors Ref1 and Lv1 are species-specific variants of TRIM5alpha. Proc Natl Acad Sci U S A 101: 10774-10779.
20. Nisole S, Stoye JP, Saib A, (2005) TRIM family proteins: retroviral restriction and antiviral defence. Nat Rev Microbiol 3: 799-808.
21. Liao CH, Kuang YQ, Liu HL, Zheng YT, Su B, (2007) A novel fusion gene, TRIM5-Cyclophilin A in the pig-tailed macaque determines its susceptibility to HIV-1 infection. Aids 21 Suppl 8: S19-26.
22. Brennan G, Kozyrev Y, Hu SL, (2008) TRIMCyp expression in Old World primates Macaca nemestrina and Macaca fascicularis. Proc Natl Acad Sci U S A 105: 3569-3574.
23. Nisole S, Lynch C, Stoye JP, Yap MW, (2004) A Trim5-cyclophilin A fusion protein found in owl monkey kidney cells can restrict HIV-1. Proc Natl Acad Sci U S A 101: 13324-13328.
24. Virgen CA, Kratovac Z, Bieniasz PD, Hatziioannou T, (2008) Independent genesis of chimeric TRIM5-cyclophilin proteins in two primate species. Proc Natl Acad Sci U S A 105: 3563-3568.
25. Wilson SJ, Webb BL, Ylinen LM, Verschoor E, Heeney JL, et al. (2008) Independent evolution of an antiviral TRIMCyp in rhesus macaques. Proc Natl Acad Sci U S A 105: 3557-3562.
26. Perron MJ, Stremlau M, Song B, Ulm W, Mulligan RC, et al. (2004) TRIM5alpha mediates the postentry block to N-tropic murine leukemia viruses in human cells. Proc Natl Acad Sci U S A 101: 11827-11832.
27. Hatziioannou T, Cowan S, Von Schwedler UK, Sundquist WI, Bieniasz PD, (2004) Species-specific tropism determinants in the human immunodeficiency virus type 1 capsid. J Virol 78: 6005-6012.
28. Sebastian S, Luban J, (2005) TRIM5alpha selectively binds a restriction-sensitive retroviral capsid. Retrovirology 2: 40.
29. Stremlau M, Perron M, Lee M, Li Y, Song B, et al. (2006) Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc Natl Acad Sci U S A 103: 5514-5519.
30. Perron MJ, Stremlau M, Lee M, Javanbakht H, Song B, et al. (2007) The human TRIM5alpha restriction factor mediates accelerated uncoating of the N-tropic murine leukemia virus capsid. J Virol 81: 2138-2148.
31. Shi J, Aiken C, (2006) Saturation of TRIM5 alpha-mediated restriction of HIV-1 infection depends on the stability of the incoming viral capsid. Virology 350: 493-500.
32. Anderson JL, Campbell EM, Wu X, Vandegraaff N, Engelman A, et al. (2006) Proteasome inhibition reveals that a functional preintegration complex intermediate can be generated during restriction by diverse TRIM5 proteins. J Virol 80: 9754-9760.
33. Zhao G, Ke D, Vu T, Ahn J, Shah VB, et al. (2011) Rhesus TRIM5alpha disrupts the HIV-1 capsid at the inter-hexamer interfaces. PLoS Pathog 7: e1002009.
34. Pertel T, Hausmann S, Morger D, Zuger S, Guerra J, et al. (2011) TRIM5 is an innate immune sensor for the retrovirus capsid lattice. Nature 472: 361-365.
35. Stremlau M, Perron M, Welikala S, Sodroski J, (2005) Species-specific variation in the B30.2(SPRY) domain of TRIM5alpha determines the potency of human immunodeficiency virus restriction. J Virol 79: 3139-3145.
36. Javanbakht H, Diaz-Griffero F, Stremlau M, Si Z, Sodroski J, (2005) The contribution of RING and B-box 2 domains to retroviral restriction mediated by monkey TRIM5alpha. J Biol Chem 280: 26933-26940.
37. Nakayama EE, Miyoshi H, Nagai Y, Shioda T, (2005) A specific region of 37 amino acid residues in the SPRY (B30.2) domain of African green monkey TRIM5alpha determines species-specific restriction of simian immunodeficiency virus SIVmac infection. J Virol 79: 8870-8877.
38. Perez-Caballero D, Hatziioannou T, Yang A, Cowan S, Bieniasz PD, (2005) Human tripartite motif 5alpha domains responsible for retrovirus restriction activity and specificity. J Virol 79: 8969-8978.
39. Yap MW, Nisole S, Stoye JP, (2005) A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-1 restriction. Curr Biol 15: 73-78.
40. Song B, Gold B, O'Huigin C, Javanbakht H, Li X, et al. (2005) The B30.2(SPRY) domain of the retroviral restriction factor TRIM5alpha exhibits lineage-specific length and sequence variation in primates. J Virol 79: 6111-6121.
41. Liu HL, Wang YQ, Liao CH, Kuang YQ, Zheng YT, et al. (2005) Adaptive evolution of primate TRIM5alpha, a gene restricting HIV-1 infection. Gene 362: 109-116.
42. Johnson WE, Sawyer SL, (2009) Molecular evolution of the antiretroviral TRIM5 gene. Immunogenetics 61: 163-176.
43. Sawyer SL, Wu LI, Akey JM, Emerman M, Malik HS, (2006) High-frequency persistence of an impaired allele of the retroviral defense gene TRIM5alpha in humans. Curr Biol 16: 95-100.
44. Javanbakht H, An P, Gold B, Petersen DC, O'Huigin C, et al. (2006) Effects of human TRIM5alpha polymorphisms on antiretroviral function and susceptibility to human immunodeficiency virus infection. Virology 354: 15-27.
45. Speelmon EC, Livingston-Rosanoff D, Li SS, Vu Q, Bui J, et al. (2006) Genetic association of the antiviral restriction factor TRIM5alpha with human immunodeficiency virus type 1 infection. J Virol 80: 2463-2471.
46. Goldschmidt V, Bleiber G, May M, Martinez R, Ortiz M, et al. (2006) Role of common human TRIM5alpha variants in HIV-1 disease progression. Retrovirology 3: 54.
47. Newman RM, Hall L, Connole M, Chen GL, Sato S, et al. (2006) Balancing selection and the evolution of functional polymorphism in Old World monkey TRIM5alpha. Proc Natl Acad Sci U S A 103: 19134-19139.
48. Wilson SJ, Webb BL, Maplanka C, Newman RM, Verschoor EJ, et al. (2008) Rhesus macaque TRIM5 alleles have divergent antiretroviral specificities. J Virol 82: 7243-7247.
49. Kirmaier A, Wu F, Newman RM, Hall LR, Morgan JS, et al. (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.
50. Lim SY, Rogers T, Chan T, Whitney JB, Kim J, et al. (2010) TRIM5alpha Modulates Immunodeficiency Virus Control in Rhesus Monkeys. PLoS Pathog 6: e1000738.
51. Hirsch V, Adger-Johnson D, Campbell B, Goldstein S, Brown C, et al. (1997) A molecularly cloned, pathogenic, neutralization-resistant simian immunodeficiency virus, SIVsmE543-3. J Virol 71: 1608-1620.
52. Goldstein S, Brown CR, Dehghani H, Lifson JD, Hirsch VM, (2000) Intrinsic susceptibility of rhesus macaque peripheral CD4(+) T cells to simian immunodeficiency virus in vitro is predictive of in vivo viral replication. J Virol 74: 9388-9395.
53. Rud EW, Cranage M, Yon J, Quirk J, Ogilvie L, et al. (1994) Molecular and biological characterization of simian immunodeficiency virus macaque strain 32H proviral clones containing nef size variants. J Gen Virol 75 (Pt 3) (): 529-543.
54. Wu F, Ourmanov I, Kuwata T, Goeken R, Brown CR, et al. (2012) Sequential evolution and escape from neutralization of simian immunodeficiency virus SIVsmE660 clones in rhesus macaques. J Virol 86: 8835-8847.
55. Hunt RD, Blake BJ, Chalifoux LV, Sehgal PK, King NW, et al. (1983) Transmission of naturally occurring lymphoma in macaque monkeys. Proc Natl Acad Sci U S A 80: 5085-5089.
56. Novembre FJ, Hirsch VM, McClure HM, Fultz PN, Johnson PR, (1992) SIV from stump-tailed macaques: molecular characterization of a highly transmissible primate lentivirus. Virology 186: 783-787.
57. Khan AS, Galvin TA, Lowenstine LJ, Jennings MB, Gardner MB, et al. (1991) A highly divergent simian immunodeficiency virus (SIVstm) recovered from stored stump-tailed macaque tissues. J Virol 65: 7061-7065.
58. Marthas ML, Banapour B, Sutjipto S, Siegel ME, Marx PA, et al. (1989) Rhesus macaques inoculated with molecularly cloned simian immunodeficiency virus. J Med Primatol 18: 311-319.
59. Kestler H, Kodama T, Ringler D, Marthas M, Pedersen N, et al. (1990) Induction of AIDS in rhesus monkeys by molecularly cloned simian immunodeficiency virus. Science 248: 1109-1112.
60. Chakrabarti L, Guyader M, Alizon M, Daniel MD, Desrosiers RC, et al. (1987) Sequence of simian immunodeficiency virus from macaque and its relationship to other human and simian retroviruses. Nature 328: 543-547.
61. Dewhurst S, Embretson JE, Anderson DC, Mullins JI, Fultz PN, (1990) Sequence analysis and acute pathogenicity of molecularly cloned SIVSMM-PBj14. Nature 345: 636-640.
62. Benveniste RE, Arthur LO, Tsai CC, Sowder R, Copeland TD, et al. (1986) Isolation of a lentivirus from a macaque with lymphoma: comparison with HTLV-III/LAV and other lentiviruses. J Virol 60: 483-490.
63. Kimata JT, Mozaffarian A, Overbaugh J, (1998) A lymph node-derived cytopathic simian immunodeficiency virus Mne variant replicates in nonstimulated peripheral blood mononuclear cells. J Virol 72: 245-256.
64. Kimata JT, Overbaugh J, (1997) The cytopathicity of a simian immunodeficiency virus Mne variant is determined by mutations in Gag and Env. J Virol 71: 7629-7639.
65. Hirsch VM, Johnson PR, (1994) Pathogenic diversity of simian immunodeficiency viruses. Virus Res 32: 183-203.
66. Apetrei C, Kaur A, Lerche NW, Metzger M, Pandrea I, et al. (2005) Molecular epidemiology of simian immunodeficiency virus SIVsm in U.S. primate centers unravels the origin of SIVmac and SIVstm. J Virol 79: 8991-9005.
67. Hirsch VM, Lifson JD, (2000) Simian immunodeficiency virus infection of monkeys as a model system for the study of AIDS pathogenesis, treatment, and prevention. Adv Pharmacol 49: 437-477.
68. Hirsch V, Adger-Johnson D, Campbell B, Goldstein S, Brown CR, et al. (1997) A molecularly cloned, pathogenic, neutralization-resistant simian immunodeficiency virus, SIVsmE543-3. J Virol 71: 1608-1620.
69. Daniel MD, Letvin NL, King NW, Kannagi M, Sehgal PK, et al. (1985) Isolation of T-cell tropic HTLV-III-like retrovirus from macaques. Science 228: 1201-1204.
70. Compton AA, Hirsch VM, Emerman M, (2012) The host restriction factor APOBEC3G and retroviral Vif protein coevolve due to ongoing genetic conflict. Cell Host Microbe 11: 91-98.
71. Compton AA, Emerman M, (2013) Convergence and divergence in the evolution of the APOBEC3G-Vif interaction reveal ancient origins of simian immunodeficiency viruses. PLoS Pathog 9: e1003135.
72. Kirchhoff F, (2010) Immune evasion and counteraction of restriction factors by HIV-1 and other primate lentiviruses. Cell Host Microbe 8: 55-67.
73. Gotz N, Sauter D, Usmani SM, Fritz JV, Goffinet C, et al. (2012) Reacquisition of Nef-mediated tetherin antagonism in a single in vivo passage of HIV-1 through its original chimpanzee host. Cell Host Microbe 12: 373-380.
74. Kuiken C, Foley B, Leitner T, Apetrei C, Hahn B, et al. (2012) HIV Sequence Compendium 2012. Los Alamos National Laboratory, Theoretical Biology and Biophysics, Los Alamos, New Mexico.
75. van Manen D, Rits MA, Beugeling C, van Dort K, Schuitemaker H, et al. (2008) The effect of Trim5 polymorphisms on the clinical course of HIV-1 infection. PLoS Pathog 4: e18.
76. Korber B, Muldoon M, Theiler J, Gao F, Gupta R, et al. (2000) Timing the ancestor of the HIV-1 pandemic strains. Science 288: 1789-1796.
77. Battivelli E, Migraine J, Lecossier D, Yeni P, Clavel F, et al. (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.
78. Reynolds MR, Sacha JB, Weiler AM, Borchardt GJ, Glidden CE, et al. (2011) The TRIM5{alpha} genotype of rhesus macaques affects acquisition of simian immunodeficiency virus SIVsmE660 infection after repeated limiting-dose intrarectal challenge. J Virol 85: 9637-9640.
79. Yeh WW, Rao SS, Lim SY, Zhang J, Hraber PT, et al. (2011) The TRIM5 gene modulates penile mucosal acquisition of simian immunodeficiency virus in rhesus monkeys. J Virol 85: 10389-10398.
80. Reed LJ, Muench H, (1938) A simple method of estimating fifty percent endpoints. The American Journal of Hygiene 27: 493-497.