Evolutionary and Functional Analysis of Old World Primate TRIM5 Reveals the Ancient Emergence of Primate Lentiviruses and Convergent Evolution Targeting a Conserved Capsid Interface

English version České info

Old World primates in Africa are reservoir hosts for more than 40 species of simian immunodeficiency viruses (SIVs), including the sources of the human immunodeficiency viruses, HIV-1 and HIV-2. To investigate the prehistoric origins of these lentiviruses, we looked for patterns of evolution in the antiviral host gene TRIM5 that would reflect selection by lentiviruses during evolution of African primates. We identified a pattern of adaptive changes unique to the TRIM5 proteins of a subset of African monkeys that suggests that the ancestors of these viruses emerged between 11–16 million years ago, and by reconstructing and comparing the function of ancestral TRIM5 proteins with extant TRIM5 proteins, we confirmed that these adaptations confer specificity for their modern descendants, the SIVs.

Vyšlo v časopise: Evolutionary and Functional Analysis of Old World Primate TRIM5 Reveals the Ancient Emergence of Primate Lentiviruses and Convergent Evolution Targeting a Conserved Capsid Interface. PLoS Pathog 11(8): e32767. doi:10.1371/journal.ppat.1005085
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1005085

Souhrn

Zdroje

1. Family—Retroviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ, editors. Virus Taxonomy. San Diego: Elsevier; 2012. p. 477–95.

2. Evans DT EJ, Desrosiers RC. Nonhuman Lentiviruses. 6th ed. Knipe DM, Howley PM, editors. Philadelphia, PA: Wolters Kluwer/Lippincott Williams & Wilkins Health; 2013. 2 volumes p.

3. Gifford RJ. Viral evolution in deep time: lentiviruses and mammals. Trends in genetics: TIG. 2012;28(2):89–100. Epub 2011/12/27. doi: 10.1016/j.tig.2011.11.003 22197521.

4. Cui J, Holmes EC. Endogenous lentiviruses in the ferret genome. J Virol. 2012;86(6):3383–5. Epub 2012/01/13. JVI.06652-11 [pii] doi: 10.1128/JVI.06652-11 22238305; PubMed Central PMCID: PMC3302300.

5. Han GZ, Worobey M. Endogenous lentiviral elements in the weasel family (Mustelidae). Mol Biol Evol. 2012;29(10):2905–8. Epub 2012/04/24. mss126 [pii] doi: 10.1093/molbev/mss126 22522310; PubMed Central PMCID: PMC3457773.

6. Keckesova Z, Ylinen LM, Towers GJ, Gifford RJ, Katzourakis A. Identification of a RELIK orthologue in the European hare (Lepus europaeus) reveals a minimum age of 12 million years for the lagomorph lentiviruses. Virology. 2009;384(1):7–11. Epub 2008/12/17. S0042-6822(08)00718-6 [pii] doi: 10.1016/j.virol.2008.10.045 19070882.

7. van der Loo W, Abrantes J, Esteves PJ. Sharing of endogenous lentiviral gene fragments among leporid lineages separated for more than 12 million years. J Virol. 2009;83(5):2386–8. Epub 2008/12/26. doi: 10.1128/JVI.01116-08 19109386; PubMed Central PMCID: PMC2643718.

8. Hron T, Fabryova H, Pa Es J, Elleder D. Endogenous lentivirus in Malayan colugo (Galeopterus variegatus), a close relative of primates. Retrovirology. 2014;11(1):84. Epub 2014/10/05. doi: 10.1186/s12977-014-0084-x 25280529; PubMed Central PMCID: PMC4198772.

9. Gifford RJ, Katzourakis A, Tristem M, Pybus OG, Winters M, Shafer RW. A transitional endogenous lentivirus from the genome of a basal primate and implications for lentivirus evolution. Proc Natl Acad Sci U S A. 2008;105(51):20362–7. Epub 2008/12/17. 0807873105 [pii] doi: 10.1073/pnas.0807873105 19075221; PubMed Central PMCID: PMC2603253.

10. Gilbert C, Maxfield DG, Goodman SM, Feschotte C. Parallel germline infiltration of a lentivirus in two Malagasy lemurs. PLoS genetics. 2009;5(3):e1000425. Epub 2009/03/21. doi: 10.1371/journal.pgen.1000425 19300488; PubMed Central PMCID: PMC2651035.

11. Apetrei C, Robertson DL, Marx PA. The history of SIVS and AIDS: epidemiology, phylogeny and biology of isolates from naturally SIV infected non-human primates (NHP) in Africa. Front Biosci. 2004;9:225–54. Epub 2004/02/10. 14766362.

12. Pandrea I, Sodora DL, Silvestri G, Apetrei C. Into the wild: simian immunodeficiency virus (SIV) infection in natural hosts. Trends in immunology. 2008;29(9):419–28. Epub 2008/08/05. doi: 10.1016/j.it.2008.05.004 18676179; PubMed Central PMCID: PMC2840226.

13. Pandrea I, Silvestri G, Apetrei C. AIDS in african nonhuman primate hosts of SIVs: a new paradigm of SIV infection. Current HIV research. 2009;7(1):57–72. Epub 2009/01/20. 19149555.

14. Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, et al. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature. 1999;397(6718):436–41. Epub 1999/02/16. doi: 10.1038/17130 9989410.

15. Daniel MD, Letvin NL, King NW, Kannagi M, Sehgal PK, Hunt RD, et al. Isolation of T-cell tropic HTLV-III-like retrovirus from macaques. Science. 1985;228(4704):1201–4. Epub 1985/06/07. 3159089.

16. Mandell DT, Kristoff J, Gaufin T, Gautam R, Ma D, Sandler N, et al. Pathogenic Features Associated with Increased Virulence upon Simian Immunodeficiency Virus Cross-Species Transmission from Natural Hosts. J Virol. 2014. Epub 2014/04/04. doi: 10.1128/JVI.03785-13 24696477.

17. Keele BF, Jones JH, Terio KA, Estes JD, Rudicell RS, Wilson ML, et al. Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz. Nature. 2009;460(7254):515–9. Epub 2009/07/25. doi: 10.1038/nature08200 19626114; PubMed Central PMCID: PMC2872475.

18. Rudicell RS, Holland Jones J, Wroblewski EE, Learn GH, Li Y, Robertson JD, et al. Impact of simian immunodeficiency virus infection on chimpanzee population dynamics. PLoS Pathog. 2010;6(9):e1001116. Epub 2010/10/05. doi: 10.1371/journal.ppat.1001116 20886099; PubMed Central PMCID: PMC2944804.

19. Peeters M C, V. Overview of Primate Lentiviruses and Their Evolution in Non-human Primates in Africa. In: Kuiken C FB, Freed E, Hahn B, Korber B, Marx PA, McCutchan F, Mellors JW, and Wolinsky S, editor. HIV Sequence Compendium. Los Alamos, NM: Theoretical Biology and Biophysics Group, Los Alamos National Laboratory, Los Alamos, NM. LA-UR 03–3564; 2002.

20. Worobey M, Telfer P, Souquiere S, Hunter M, Coleman CA, Metzger MJ, et al. Island biogeography reveals the deep history of SIV. Science. 2010;329(5998):1487. Epub 2010/09/18. 329/5998/1487 [pii] doi: 10.1126/science.1193550 20847261.

21. Emerman M, Malik HS. Paleovirology—modern consequences of ancient viruses. PLoS Biol. 2010;8(2):e1000301. Epub 2010/02/18. doi: 10.1371/journal.pbio.1000301 20161719; PubMed Central PMCID: PMC2817711.

22. Patel MR, Emerman M, Malik HS. Paleovirology—ghosts and gifts of viruses past. Current opinion in virology. 2011;1(4):304–9. Epub 2011/10/18. doi: 10.1016/j.coviro.2011.06.007 22003379; PubMed Central PMCID: PMC3190193.

23. Malfavon-Borja R, Wu LI, Emerman M, Malik HS. Birth, decay, and reconstruction of an ancient TRIMCyp gene fusion in primate genomes. Proc Natl Acad Sci U S A. 2013. Epub 2013/01/16. 1216542110 [pii] doi: 10.1073/pnas.1216542110 23319649.

24. Compton AA, Emerman M. Convergence and Divergence in the Evolution of the APOBEC3G-Vif Interaction Reveal Ancient Origins of Simian Immunodeficiency Viruses. PLoS Pathog. 2013;9(1):e1003135. Epub 2013/01/30. doi: 10.1371/journal.ppat.1003135 PPATHOGENS-D-12-02303 [pii]. 23359341; PubMed Central PMCID: PMC3554591.

25. McCarthy KR, Schmidt AG, Kirmaier A, Wyand AL, Newman RM, Johnson WE. Gain-of-sensitivity mutations in a Trim5-resistant primary isolate of pathogenic SIV identify two independent conserved determinants of Trim5alpha specificity. PLoS Pathog. 2013;9(5):e1003352. Epub 2013/05/16. doi: 10.1371/journal.ppat.1003352 23675300; PubMed Central PMCID: PMC3649984.

26. Fregoso OI, Ahn J, Wang C, Mehrens J, Skowronski J, Emerman M. Evolutionary toggling of Vpx/Vpr specificity results in divergent recognition of the restriction factor SAMHD1. PLoS Pathog. 2013;9(7):e1003496. Epub 2013/07/23. doi: 10.1371/journal.ppat.1003496 23874202; PubMed Central PMCID: PMC3715410.

27. Laguette N, Rahm N, Sobhian B, Chable-Bessia C, Munch J, Snoeck J, et al. Evolutionary and functional analyses of the interaction between the myeloid restriction factor SAMHD1 and the lentiviral Vpx protein. Cell Host Microbe. 2012;11(2):205–17. Epub 2012/02/07. doi: 10.1016/j.chom.2012.01.007 22305291; PubMed Central PMCID: PMC3595996.

28. Krupp A, McCarthy KR, Ooms M, Letko M, Morgan JS, Simon V, et al. APOBEC3G polymorphism as a selective barrier to cross-species transmission and emergence of pathogenic SIV and AIDS in a primate host. PLoS Pathog. 2013;9(10):e1003641. Epub 2013/10/08. doi: 10.1371/journal.ppat.1003641 24098115; PubMed Central PMCID: PMC3789815.

29. 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):848–53. Epub 2004/02/27. doi: 10.1038/nature02343 nature02343 [pii]. 14985764.

30. Stremlau M, Perron M, Lee M, Li Y, Song B, Javanbakht H, et al. Specific recognition and accelerated uncoating of retroviral capsids by the TRIM5alpha restriction factor. Proc Natl Acad Sci U S A. 2006;103(14):5514–9. Epub 2006/03/17. 0509996103 [pii] doi: 10.1073/pnas.0509996103 16540544; PubMed Central PMCID: PMC1459386.

31. Sebastian S, Luban J. TRIM5alpha selectively binds a restriction-sensitive retroviral capsid. Retrovirology. 2005;2:40. Epub 2005/06/22. 1742-4690-2-40 [pii] doi: 10.1186/1742-4690-2-40 15967037; PubMed Central PMCID: PMC1166576.

32. Meyerson NR, Sawyer SL. Two-stepping through time: mammals and viruses. Trends Microbiol. 2011;19(6):286–94. Epub 2011/05/03. doi: 10.1016/j.tim.2011.03.006 21531564; PubMed Central PMCID: PMC3567447.

33. Reymond A, Meroni G, Fantozzi A, Merla G, Cairo S, Luzi L, et al. The tripartite motif family identifies cell compartments. EMBO J. 2001;20(9):2140–51. Epub 2001/05/02. doi: 10.1093/emboj/20.9.2140 11331580; PubMed Central PMCID: PMC125245.

34. Borden KL, Lally JM, Martin SR, O'Reilly NJ, Etkin LD, Freemont PS. Novel topology of a zinc-binding domain from a protein involved in regulating early Xenopus development. EMBO J. 1995;14(23):5947–56. Epub 1995/12/01. 8846787; PubMed Central PMCID: PMC394714.

35. Biris N, Yang Y, Taylor AB, Tomashevski A, Guo M, Hart PJ, et al. Structure of the rhesus monkey TRIM5alpha PRYSPRY domain, the HIV capsid recognition module. Proc Natl Acad Sci U S A. 2012;109(33):13278–83. Epub 2012/08/01. 1203536109 [pii] doi: 10.1073/pnas.1203536109 22847415; PubMed Central PMCID: PMC3421187.

36. Sawyer SL, Wu LI, Emerman M, Malik HS. Positive selection of primate TRIM5alpha identifies a critical species-specific retroviral restriction domain. Proc Natl Acad Sci U S A. 2005;102(8):2832–7. Epub 2005/02/04. 0409853102 [pii] doi: 10.1073/pnas.0409853102 15689398; PubMed Central PMCID: PMC549489.

37. Yap MW, Nisole S, Stoye JP. A single amino acid change in the SPRY domain of human Trim5alpha leads to HIV-1 restriction. Curr Biol. 2005;15(1):73–8. Epub 2005/01/15. S096098220401022X [pii] doi: 10.1016/j.cub.2004.12.042 15649369.

38. Stremlau M, Perron M, Welikala S, Sodroski J. Species-specific variation in the B30.2(SPRY) domain of TRIM5alpha determines the potency of human immunodeficiency virus restriction. J Virol. 2005;79(5):3139–45. Epub 2005/02/15. 79/5/3139 [pii] doi: 10.1128/JVI.79.5.3139-3145.2005 15709033; PubMed Central PMCID: PMC548447.

39. Nakayama EE, Miyoshi H, Nagai Y, Shioda T. 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. 2005;79(14):8870–7. Epub 2005/07/05. doi: 10.1128/JVI.79.14.8870-8877.2005 15994780; PubMed Central PMCID: PMC1168783.

40. Perez-Caballero D, Hatziioannou T, Yang A, Cowan S, Bieniasz PD. Human tripartite motif 5alpha domains responsible for retrovirus restriction activity and specificity. J Virol. 2005;79(14):8969–78. Epub 2005/07/05. 79/14/8969 [pii] doi: 10.1128/JVI.79.14.8969-8978.2005 15994791; PubMed Central PMCID: PMC1168745.

41. 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(18):11580–7. Epub 2005/09/06. 79/18/11580 [pii] doi: 10.1128/JVI.79.18.11580-11587.2005 16140735; PubMed Central PMCID: PMC1212619.

42. Wilson SJ, Webb BL, Maplanka C, Newman RM, Verschoor EJ, Heeney JL, et al. Rhesus macaque TRIM5 alleles have divergent antiretroviral specificities. J Virol. 2008;82(14):7243–7. Epub 2008/05/16. JVI.00307-08 [pii] doi: 10.1128/JVI.00307-08 18480454; PubMed Central PMCID: PMC2446970.

43. Perron MJ, Stremlau M, Sodroski J. Two surface-exposed elements of the B30.2/SPRY domain as potency determinants of N-tropic murine leukemia virus restriction by human TRIM5alpha. J Virol. 2006;80(11):5631–6. Epub 2006/05/16. 80/11/5631 [pii] doi: 10.1128/JVI.00219-06 16699044; PubMed Central PMCID: PMC1472168.

44. Sebastian S, Grutter C, Strambio de Castillia C, Pertel T, Olivari S, Grutter MG, et al. An invariant surface patch on the TRIM5alpha PRYSPRY domain is required for retroviral restriction but dispensable for capsid binding. J Virol. 2009;83(7):3365–73. Epub 2009/01/21. JVI.00432-08 [pii] doi: 10.1128/JVI.00432-08 19153241; PubMed Central PMCID: PMC2655600.

45. Diaz-Griffero F, Kar A, Lee M, Stremlau M, Poeschla E, Sodroski J. Comparative requirements for the restriction of retrovirus infection by TRIM5alpha and TRIMCyp. Virology. 2007;369(2):400–10. Epub 2007/10/09. doi: 10.1016/j.virol.2007.08.032 17920096; PubMed Central PMCID: PMC2153441.

46. Kono K, Bozek K, Domingues FS, Shioda T, Nakayama EE. Impact of a single amino acid in the variable region 2 of the Old World monkey TRIM5alpha SPRY (B30.2) domain on anti-human immunodeficiency virus type 2 activity. Virology. 2009;388(1):160–8. Epub 2009/04/04. doi: 10.1016/j.virol.2009.03.004 19342071.

47. Nakajima T, Nakayama EE, Kaur G, Terunuma H, Mimaya JI, Ohtani H, et al. Impact of novel TRIM5alpha variants, Gly110Arg and G176del, on the anti-HIV-1 activity and the susceptibility to HIV-1 infection. AIDS. 2009;23(16):2091–100. Epub 2009/08/28. doi: 10.1097/QAD.0b013e328331567a 19710594.

48. Pham QT, Bouchard A, Grutter MG, Berthoux L. Generation of human TRIM5alpha mutants with high HIV-1 restriction activity. Gene Ther. 2010;17(7):859–71. Epub 2010/04/02. doi: 10.1038/gt.2010.40 20357830.

49. Rahm N, Yap M, Snoeck J, Zoete V, Munoz M, Radespiel U, et al. Unique spectrum of activity of prosimian TRIM5alpha against exogenous and endogenous retroviruses. J Virol. 2011;85(9):4173–83. Epub 2011/02/25. JVI.00075-11 [pii] doi: 10.1128/JVI.00075-11 21345948; PubMed Central PMCID: PMC3126249.

50. Yang Y, Brandariz-Nunez A, Fricke T, Ivanov DN, Sarnak Z, Diaz-Griffero F. Binding of the rhesus TRIM5alpha PRYSPRY domain to capsid is necessary but not sufficient for HIV-1 restriction. Virology. 2014;448:217–28. Epub 2013/12/10. doi: 10.1016/j.virol.2013.10.012 24314652; PubMed Central PMCID: PMC3900861.

51. Ohkura S, Yap MW, Sheldon T, Stoye JP. All three variable regions of the TRIM5alpha B30.2 domain can contribute to the specificity of retrovirus restriction. J Virol. 2006;80(17):8554–65. Epub 2006/08/17. 80/17/8554 [pii] doi: 10.1128/JVI.00688-06 16912305; PubMed Central PMCID: PMC1563890.

52. Javanbakht H, An P, Gold B, Petersen DC, O'Huigin C, Nelson GW, et al. Effects of human TRIM5alpha polymorphisms on antiretroviral function and susceptibility to human immunodeficiency virus infection. Virology. 2006;354(1):15–27. Epub 2006/08/05. doi: 10.1016/j.virol.2006.06.031 16887163.

53. Song B, Gold B, O'Huigin C, Javanbakht H, Li X, Stremlau M, et al. The B30.2(SPRY) domain of the retroviral restriction factor TRIM5alpha exhibits lineage-specific length and sequence variation in primates. J Virol. 2005;79(10):6111–21. Epub 2005/04/29. 79/10/6111 [pii] doi: 10.1128/JVI.79.10.6111-6121.2005 15857996; PubMed Central PMCID: PMC1091705.

54. Newman RM, Hall L, Connole M, Chen GL, Sato S, Yuste E, et al. Balancing selection and the evolution of functional polymorphism in Old World monkey TRIM5alpha. Proc Natl Acad Sci U S A. 2006;103(50):19134–9. Epub 2006/12/05. 0605838103 [pii] doi: 10.1073/pnas.0605838103 17142324; PubMed Central PMCID: PMC1679755.

55. Bininda-Emonds OR, Cardillo M, Jones KE, MacPhee RD, Beck RM, Grenyer R, et al. The delayed rise of present-day mammals. Nature. 2007;446(7135):507–12. Epub 2007/03/30. nature05634 [pii] doi: 10.1038/nature05634 17392779.

56. Perelman P, Johnson WE, Roos C, Seuanez HN, Horvath JE, Moreira MA, et al. A molecular phylogeny of living primates. PLoS genetics. 2011;7(3):e1001342. Epub 2011/03/26. doi: 10.1371/journal.pgen.1001342 21436896; PubMed Central PMCID: PMC3060065.

57. Pozzi L, Hodgson JA, Burrell AS, Sterner KN, Raaum RL, Disotell TR. Primate phylogenetic relationships and divergence dates inferred from complete mitochondrial genomes. Molecular phylogenetics and evolution. 2014;75:165–83. Epub 2014/03/04. doi: 10.1016/j.ympev.2014.02.023 24583291; PubMed Central PMCID: PMC4059600.

58. Finstermeier K, Zinner D, Brameier M, Meyer M, Kreuz E, Hofreiter M, et al. A mitogenomic phylogeny of living primates. PLoS One. 2013;8(7):e69504. Epub 2013/07/23. doi: 10.1371/journal.pone.0069504 23874967; PubMed Central PMCID: PMC3713065.

59. Newman RM, Hall L, Kirmaier A, Pozzi LA, Pery E, Farzan M, et al. Evolution of a TRIM5-CypA splice isoform in old world monkeys. PLoS Pathog. 2008;4(2):e1000003. Epub 2008/04/05. doi: 10.1371/journal.ppat.1000003 18389077; PubMed Central PMCID: PMC2279257.

60. Wilson SJ, Webb BL, Ylinen LM, Verschoor E, Heeney JL, Towers GJ. Independent evolution of an antiviral TRIMCyp in rhesus macaques. Proc Natl Acad Sci U S A. 2008;105(9):3557–62. Epub 2008/02/22. 0709003105 [pii] doi: 10.1073/pnas.0709003105 18287035; PubMed Central PMCID: PMC2265179.

61. Liao CH, Kuang YQ, Liu HL, Zheng YT, Su B. A novel fusion gene, TRIM5-Cyclophilin A in the pig-tailed macaque determines its susceptibility to HIV-1 infection. AIDS. 2007;21 Suppl 8:S19–26. Epub 2008/01/10. doi: 10.1097/01.aids.0000304692.09143.1b 00002030-200712008-00004 [pii]. 18172386.

62. Virgen CA, Kratovac Z, Bieniasz PD, Hatziioannou T. Independent genesis of chimeric TRIM5-cyclophilin proteins in two primate species. Proc Natl Acad Sci U S A. 2008;105(9):3563–8. Epub 2008/02/22. 0709258105 [pii] doi: 10.1073/pnas.0709258105 18287034; PubMed Central PMCID: PMC2265128.

63. Brennan G, Kozyrev Y, Hu SL. TRIMCyp expression in Old World primates Macaca nemestrina and Macaca fascicularis. Proc Natl Acad Sci U S A. 2008;105(9):3569–74. Epub 2008/02/22. 0709511105 [pii] doi: 10.1073/pnas.0709511105 18287033; PubMed Central PMCID: PMC2265124.

64. Ashkenazy H, Penn O, Doron-Faigenboim A, Cohen O, Cannarozzi G, Zomer O, et al. FastML: a web server for probabilistic reconstruction of ancestral sequences. Nucleic Acids Res. 2012;40(Web Server issue):W580–4. Epub 2012/06/05. doi: 10.1093/nar/gks498 22661579; PubMed Central PMCID: PMC3394241.

65. Pupko T, Pe'er I, Shamir R, Graur D. A fast algorithm for joint reconstruction of ancestral amino acid sequences. Mol Biol Evol. 2000;17(6):890–6. Epub 2000/06/01. 10833195.

66. Pupko T, Pe'er I, Hasegawa M, Graur D, Friedman N. A branch-and-bound algorithm for the inference of ancestral amino-acid sequences when the replacement rate varies among sites: Application to the evolution of five gene families. Bioinformatics. 2002;18(8):1116–23. Epub 2002/08/15. 12176835.

67. Diehl WE, Stansell E, Kaiser SM, Emerman M, Hunter E. Identification of postentry restrictions to Mason-Pfizer monkey virus infection in New World monkey cells. J Virol. 2008;82(22):11140–51. Epub 2008/09/19. JVI.00269-08 [pii] doi: 10.1128/JVI.00269-08 18799582; PubMed Central PMCID: PMC2573280.

68. Song B, Javanbakht H, Perron M, Park DH, Stremlau M, Sodroski J. Retrovirus restriction by TRIM5alpha variants from Old World and New World primates. J Virol. 2005;79(7):3930–7. Epub 2005/03/16. 79/7/3930 [pii] doi: 10.1128/JVI.79.7.3930-3937.2005 15767395; PubMed Central PMCID: PMC1061569.

69. Yap MW, Nisole S, Lynch C, Stoye JP. Trim5alpha protein restricts both HIV-1 and murine leukemia virus. Proc Natl Acad Sci U S A. 2004;101(29):10786–91. Epub 2004/07/14. doi: 10.1073/pnas.0402876101 0402876101 [pii]. 15249690; PubMed Central PMCID: PMC490012.

70. Besnier C, Takeuchi Y, Towers G. Restriction of lentivirus in monkeys. Proc Natl Acad Sci U S A. 2002;99(18):11920–5. Epub 2002/08/03. doi: 10.1073/pnas.172384599 172384599 [pii]. 12154231; PubMed Central PMCID: PMC129369.

71. Mortuza GB, Haire LF, Stevens A, Smerdon SJ, Stoye JP, Taylor IA. High-resolution structure of a retroviral capsid hexameric amino-terminal domain. Nature. 2004;431(7007):481–5. Epub 2004/09/24. doi: 10.1038/nature02915 nature02915 [pii]. 15386017.

72. Mortuza GB, Goldstone DC, Pashley C, Haire LF, Palmarini M, Taylor WR, et al. Structure of the capsid amino-terminal domain from the betaretrovirus, Jaagsiekte sheep retrovirus. J Mol Biol. 2009;386(4):1179–92. Epub 2008/11/15. S0022-2836(08)01336-3 [pii] doi: 10.1016/j.jmb.2008.10.066 19007792.

73. Macek P, Chmelik J, Krizova I, Kaderavek P, Padrta P, Zidek L, et al. NMR structure of the N-terminal domain of capsid protein from the mason-pfizer monkey virus. J Mol Biol. 2009;392(1):100–14. Epub 2009/06/17. doi: 10.1016/j.jmb.2009.06.029 19527730.

74. Tang C, Ndassa Y, Summers MF. Structure of the N-terminal 283-residue fragment of the immature HIV-1 Gag polyprotein. Nat Struct Biol. 2002;9(7):537–43. Epub 2002/05/29. doi: 10.1038/nsb806 nsb806 [pii]. 12032547.

75. Cornilescu CC, Bouamr F, Yao X, Carter C, Tjandra N. Structural analysis of the N-terminal domain of the human T-cell leukemia virus capsid protein. J Mol Biol. 2001;306(4):783–97. Epub 2001/03/13. doi: 10.1006/jmbi.2000.4395 S0022-2836(00)94395-X [pii]. 11243788.

76. Kingston RL, Fitzon-Ostendorp T, Eisenmesser EZ, Schatz GW, Vogt VM, Post CB, et al. Structure and self-association of the Rous sarcoma virus capsid protein. Structure. 2000;8(6):617–28. Epub 2000/06/30. st8611 [pii]. 10873863.

77. Johnson WE, Sawyer SL. Molecular evolution of the antiretroviral TRIM5 gene. Immunogenetics. 2009;61(3):163–76. Epub 2009/02/25. doi: 10.1007/s00251-009-0358-y 19238338.

78. Ohkura S, Goldstone DC, Yap MW, Holden-Dye K, Taylor IA, Stoye JP. Novel escape mutants suggest an extensive TRIM5alpha binding site spanning the entire outer surface of the murine leukemia virus capsid protein. PLoS Pathog. 2011;7(3):e1002011. Epub 2011/04/13. doi: 10.1371/journal.ppat.1002011 21483490; PubMed Central PMCID: PMC3068999.

79. Ohkura S, Stoye JP. A comparison of murine leukemia viruses that escape from human and rhesus macaque TRIM5alphas. J Virol. 2013;87(11):6455–68. Epub 2013/03/29. doi: 10.1128/JVI.03425-12 23536686; PubMed Central PMCID: PMC3648092.

80. Goldschmidt V, Ciuffi A, Ortiz M, Brawand D, Munoz M, Kaessmann H, et al. Antiretroviral activity of ancestral TRIM5alpha. J Virol. 2008;82(5):2089–96. Epub 2007/12/14. doi: 10.1128/JVI.01828-07 18077724; PubMed Central PMCID: PMC2258955.

81. Lim ES, Malik HS, Emerman M. Ancient adaptive evolution of tetherin shaped the functions of Vpu and Nef in human immunodeficiency virus and primate lentiviruses. J Virol. 2010;84(14):7124–34. Epub 2010/05/07. doi: 10.1128/JVI.00468-10 20444900; PubMed Central PMCID: PMC2898239.

82. Sauter D, Vogl M, Kirchhoff F. Ancient origin of a deletion in human BST2/Tetherin that confers protection against viral zoonoses. Human mutation. 2011;32(11):1243–5. Epub 2011/07/29. doi: 10.1002/humu.21571 21796732.

83. Franke EK, Yuan HE, Luban J. Specific incorporation of cyclophilin A into HIV-1 virions. Nature. 1994;372(6504):359–62. Epub 1994/11/24. doi: 10.1038/372359a0 7969494.

84. Gamble TR, Vajdos FF, Yoo S, Worthylake DK, Houseweart M, Sundquist WI, et al. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell. 1996;87(7):1285–94. Epub 1996/12/27. S0092-8674(00)81823-1 [pii]. 8980234.

85. Schaller T, Ocwieja KE, Rasaiyaah J, Price AJ, Brady TL, Roth SL, et al. HIV-1 capsid-cyclophilin interactions determine nuclear import pathway, integration targeting and replication efficiency. PLoS Pathog. 2011;7(12):e1002439. Epub 2011/12/17. doi: 10.1371/journal.ppat.1002439 PPATHOGENS-D-11-01130 [pii]. 22174692; PubMed Central PMCID: PMC3234246.

86. Price AJ, Fletcher AJ, Schaller T, Elliott T, Lee K, Kewalramani VN, et al. CPSF6 Defines a Conserved Capsid Interface that Modulates HIV-1 Replication. PLoS Pathog. 2012;8(8):e1002896. Epub 2012/09/08. doi: 10.1371/journal.ppat.1002896 PPATHOGENS-D-12-00429 [pii]. 22956906; PubMed Central PMCID: PMC3431306.

87. Matreyek KA, Yucel SS, Li X, Engelman A. Nucleoporin NUP153 phenylalanine-glycine motifs engage a common binding pocket within the HIV-1 capsid protein to mediate lentiviral infectivity. PLoS Pathog. 2013;9(10):e1003693. Epub 2013/10/17. doi: 10.1371/journal.ppat.1003693 24130490; PubMed Central PMCID: PMC3795039.

88. Price AJ, Jacques DA, McEwan WA, Fletcher AJ, Essig S, Chin JW, et al. Host cofactors and pharmacologic ligands share an essential interface in HIV-1 capsid that is lost upon disassembly. PLoS Pathog. 2014;10(10):e1004459. Epub 2014/10/31. doi: 10.1371/journal.ppat.1004459 25356722; PubMed Central PMCID: PMC4214760.

89. Bhattacharya A, Alam SL, Fricke T, Zadrozny K, Sedzicki J, Taylor AB, et al. Structural basis of HIV-1 capsid recognition by PF74 and CPSF6. Proc Natl Acad Sci U S A. 2014;111(52):18625–30. Epub 2014/12/19. doi: 10.1073/pnas.1419945112 25518861; PubMed Central PMCID: PMC4284599.

90. Meehan AM, Saenz DT, Guevera R, Morrison JH, Peretz M, Fadel HJ, et al. A cyclophilin homology domain-independent role for Nup358 in HIV-1 infection. PLoS Pathog. 2014;10(2):e1003969. Epub 2014/03/04. doi: 10.1371/journal.ppat.1003969 24586169; PubMed Central PMCID: PMC3930637.

91. Mamede JI, Sitbon M, Battini JL, Courgnaud V. Heterogeneous susceptibility of circulating SIV isolate capsids to HIV-interacting factors. Retrovirology. 2013;10:77. Epub 2013/07/26. doi: 10.1186/1742-4690-10-77 23883001; PubMed Central PMCID: PMC3751554.

92. Goldstone DC, Walker PA, Calder LJ, Coombs PJ, Kirkpatrick J, Ball NJ, et al. Structural studies of postentry restriction factors reveal antiparallel dimers that enable avid binding to the HIV-1 capsid lattice. Proc Natl Acad Sci U S A. 2014;111(26):9609–14. Epub 2014/07/01. doi: 10.1073/pnas.1402448111 24979782.

93. Sanchez JG, Okreglicka K, Chandrasekaran V, Welker JM, Sundquist WI, Pornillos O. The tripartite motif coiled-coil is an elongated antiparallel hairpin dimer. Proc Natl Acad Sci U S A. 2014;111(7):2494–9. Epub 2014/02/20. doi: 10.1073/pnas.1318962111 24550273; PubMed Central PMCID: PMC3932864.

94. Yang H, Ji X, Zhao G, Ning J, Zhao Q, Aiken C, et al. Structural insight into HIV-1 capsid recognition by rhesus TRIM5alpha. Proc Natl Acad Sci U S A. 2012. Epub 2012/10/24. 1210903109 [pii] doi: 10.1073/pnas.1210903109 23091002.

95. Zhang H, Zhou Y, Alcock C, Kiefer T, Monie D, Siliciano J, et al. Novel single-cell-level phenotypic assay for residual drug susceptibility and reduced replication capacity of drug-resistant human immunodeficiency virus type 1. J Virol. 2004;78(4):1718–29. Epub 2004/01/30. 14747537; PubMed Central PMCID: PMC369469.

96. Kirmaier A, Wu F, Newman RM, Hall LR, Morgan JS, O'Connor S, et al. TRIM5 suppresses cross-species transmission of a primate immunodeficiency virus and selects for emergence of resistant variants in the new species. PLoS Biol. 2010;8(8). Epub 2010/09/03. doi: 10.1371/journal.pbio.1000462 20808775; PubMed Central PMCID: PMC2927514.

97. Chen CM, Smith DM, Peters MA, Samson ME, Zitz J, Tabin CJ, et al. Production and design of more effective avian replication-incompetent retroviral vectors. Developmental biology. 1999;214(2):370–84. Epub 1999/10/20. doi: 10.1006/dbio.1999.9432 10525341.

98. Patel M, Giddings AM, Sechelski J, Olsen JC. High efficiency gene transfer to airways of mice using influenza hemagglutinin pseudotyped lentiviral vectors. The journal of gene medicine. 2013;15(1):51–62. Epub 2013/01/16. doi: 10.1002/jgm.2695 23319179.

99. McKay T, Patel M, Pickles RJ, Johnson LG, Olsen JC. Influenza M2 envelope protein augments avian influenza hemagglutinin pseudotyping of lentiviral vectors. Gene Ther. 2006;13(8):715–24. Epub 2006/01/07. doi: 10.1038/sj.gt.3302715 16397505.

100. Loewen N, Barraza R, Whitwam T, Saenz DT, Kemler I, Poeschla EM. FIV Vectors. Methods Mol Biol. 2003;229:251–71. Epub 2003/06/26. doi: 10.1385/1-59259-393-3:251 12824636.

101. Khare PD, Loewen N, Teo W, Barraza RA, Saenz DT, Johnson DH, et al. Durable, safe, multi-gene lentiviral vector expression in feline trabecular meshwork. Mol Ther. 2008;16(1):97–106. Epub 2007/10/04. doi: 10.1038/sj.mt.6300318 17912236.

102. Kratovac Z, Virgen CA, Bibollet-Ruche F, Hahn BH, Bieniasz PD, Hatziioannou T. Primate lentivirus capsid sensitivity to TRIM5 proteins. J Virol. 2008;82(13):6772–7. Epub 2008/04/18. doi: 10.1128/JVI.00410-08 18417575; PubMed Central PMCID: PMC2447065.

103. Owens CM, Yang PC, Gottlinger H, Sodroski J. Human and simian immunodeficiency virus capsid proteins are major viral determinants of early, postentry replication blocks in simian cells. J Virol. 2003;77(1):726–31. Epub 2002/12/13. 12477877; PubMed Central PMCID: PMC140632.

104. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59(3):307–21. Epub 2010/06/09. doi: 10.1093/sysbio/syq010 20525638.

105. Varthakavi V, Browning PJ, Spearman P. Human immunodeficiency virus replication in a primary effusion lymphoma cell line stimulates lytic-phase replication of Kaposi's sarcoma-associated herpesvirus. J Virol. 1999;73(12):10329–38. Epub 1999/11/13. 10559351; PubMed Central PMCID: PMC113088.