A comparison of murine leukemia viruses that escape from human and rhesus macaque TRIM5αs

Journal of Virology

Volumn 87, Issue 11, 2013, Pages 6455-6468

  Ohkura, Sadayuki ^a   Stoye, Jonathan P ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

TRIPARTITE MOTIF PROTEIN 5;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FITNESS; HUMAN; HUMAN CELL; MOLECULAR RECOGNITION; MURINE LEUKEMIA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; STRAIN DIFFERENCE; VIRUS CAPSID; VIRUS MUTANT; VIRUS MUTATION; VIRUS STRAIN;

ANIMALS; CAPSID PROTEINS; CARRIER PROTEINS; HUMANS; LEUKEMIA VIRUS, MURINE; MACACA MULATTA; MODELS, MOLECULAR; PROTEIN BINDING; RETROVIRIDAE INFECTIONS;

EID: 84878187076     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03425-12     Document Type: Article

References (50)

1. Bieniasz PD. 2004. Intrinsic immunity: a front-line defense against viral attack. Nat. Immunol. 5:1109-1115.
2. Feschotte C, Gilbert C. 2012. Endogenous viruses: insights into viral evolution and impact on host biology. Nat. Rev. Genet. 13:283-296.
3. Stoye JP. 2012. Studies of endogenous retroviruses reveal a continuing evolutionary saga. Nat. Rev. Microbiol. 10:395-406.
4. Jolicoeur P. 1979. The Fv-1 gene of the mouse and its control of murine leukemia virus replication. Curr. Top. Microbiol. Immunol. 86:67-122.
5. Lilly F. 1970. Fv-2: identification and location of a second gene governing the spleen focus response to Friend leukemia virus in mice. J. Natl. Cancer Inst. 45:163-169.
6. 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.
7. 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.
8. 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.
9. Wilson SJ, Webb BL, Ylinen LM, Verschoor E, Heeney JL, Towers GJ. 2008. Independent evolution of an antiviral TRIMCyp in rhesus macaques. Proc. Natl. Acad. Sci. U. S. A. 105:3557-3562.
10. 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.
11. 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.
12. Newman RM, Hall L, Kirmaier A, Pozzi LA, Pery E, Farzan M, O'Neil SP, Johnson W. 2008. Evolution of a TRIM5-CypA splice isoform in Old World monkeys. PLoS Pathog. 4:e1000003. doi:10.1371/journal.ppat.1000003.
13. Malfavon-Borja R, Wu LI, Emerman M, Malik HS. 2013. Birth, decay, and reconstruction of an ancient TRIMCyp gene fusion in primate genomes. Proc. Natl. Acad. Sci. U. S. A. 110:E583-E592.
14. Bishop KN, Bock M, Towers G, Stoye JP. 2001. Identification of the regions of Fv1 necessary for murine leukemia virus restriction. J. Virol. 75:5182-5188.
15. Bishop KN, Mortuza GB, Howell S, Yap MW, Stoye JP, Taylor IA. 2006. Characterization of an amino-terminal dimerization domain from retroviral restriction factor Fv1. J. Virol. 80:8225-8235.
16. Diaz-Griffero F, Qin XR, Hayashi F, Kigawa T, Finzi A, Sarnak Z, Lienlaf M, Yokoyama S, Sodroski J. 2009. A B-box 2 surface patch important for TRIM5alpha self-association, capsid binding avidity, and retrovirus restriction. J. Virol. 83:10737-10751.
17. Li X, Sodroski J. 2008. The TRIM5alpha B-box 2 domain promotes cooperative binding to the retroviral capsid by mediating higher-order self-association. J. Virol. 82:11495-11502.
18. Perez-Caballero D, Hatziioannou T, Yang A, Cowan S, Bieniasz PD. 2005. Human tripartite motif 5α domains responsible for retrovirus restriction activity and specificity. J. Virol. 79:8969-8978.
19. Sastri J, O'Connor C, Danielson CM, McRaven M, Perez P, Diaz-Griffero F, Campbell EM. 2010. Identification of residues within the L2 region of rhesus TRIM5alpha that are required for retroviral restriction and cytoplasmic body localization. Virology 405:259-266.
20. 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.
21. Stremlau M, Perron M, Welikala S, Sodroski J. 2005. Species-specific variation in the B30.2(SPRY) domain of TRIM5α determines the potency of human immunodeficiency virus restriction. J. Virol. 79:3139-3145.
22. 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.
23. Wu X, Anderson JL, Campbell EM, Joseph AM, Hope TJ. 2006. Proteasome inhibitors uncouple rhesus TRIM5alpha restriction of HIV-1 reverse transcription and infection. Proc. Natl. Acad. Sci. U. S. A. 103:7465-7470.
24. 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.
25. Ohkura S, Yap MW, Sheldon T, Stoye JP. 2006. All three variable regions of the TRIM5alpha B30.2 domain can contribute to the specificity of retrovirus restriction. J. Virol. 80:8554-8565.
26. Yap MW, Lindemann D, Stanke N, Reh J, Westphal D, Hanenberg H, Ohkura S, Stoye JP. 2008. Restriction of foamy viruses by primate Trim5α. J. Virol. 82:5429-5439.
27. Kozak CA, Chakraborti A. 1996. Single amino acid changes in the murine leukemia virus capsid protein gene define the target of Fv1 resistance. Virology 225:300-305.
28. Ohkura S, Goldstone DC, Yap MW, Holden-Dye K, Taylor IA, Stoye JP. 2011. Novel escape mutants suggest an extensive TRIM5alpha binding site spanning the entire outer surface of the murine leukemia virus capsid protein. PLoS Pathog. 7:e1002011. doi:10.1371/journal.ppat.1002011.
29. Yap MW, Nisole S, Lynch C, Stoye JP. 2004. Trim5alpha protein restricts both HIV-1 and murine leukemia virus. Proc. Natl. Acad. Sci. U. S. A. 101:10786-10791.
30. Bock M, Bishop KN, Towers G, Stoye JP. 2000. Use of a transient assay for studying the genetic determinants of Fv1 restriction. J. Virol. 74:7422-7430.
31. Boone LR, Myer FE, Yang DM, Ou CY, Koh CK, Roberson LE, Tennant RW, Yang WK. 1983. Reversal of Fv-1 host range by in vitro restriction endonuclease fragment exchange between molecular clones of N-tropic and B-tropic murine leukemia virus genomes. J. Virol. 48:110-119.
32. Soneoka Y, Cannon PM, Ramsdale EE, Griffiths JC, Romano G, Kingsman SM, Kingsman AJ. 1995. A transient three-plasmid expression system for the production of high titer retroviral vectors. Nucleic Acids Res. 23:628-633.
33. Dodding MP, Bock M, Yap MW, Stoye JP. 2005. Capsid processing requirements for abrogation of Fv1 and Ref1 restriction. J. Virol. 79: 10571-10577.
34. Jiang J, Ablan SD, Derebail S, Hercik K, Soheilian F, Thomas JA, Tang S, Hewlett I, Nagashima K, Gorelick RJ, Freed EO, Levin JG. 2011. The interdomain linker region of HIV-1 capsid protein is a critical determinant of proper core assembly and stability. Virology 421:253-265.
35. Perron M, Stremlau M, Sodroski J. 2006. Two surface-exposed elements of the B30.2/SPRY domain as potency determinants of N-tropic murine leukemia virus restriction by human TRIM5α. J. Virol. 80:5631-5636.
36. Maillard PV, Reynard S, Serhan F, Turelli P, Trono D. 2007. Interfering residues narrow the spectrum of MLV restriction by human TRIM5alpha. PLoS Pathog. 3:e200. doi:10.1371/journal.ppat.0030200.
37. Ganser-Pornillos BK, Chandrasekaran V, Pornillos O, Sodroski JG, Sundquist WI, Yeager M. 2011. Hexagonal assembly of a restricting TRIM5a protein. Proc. Natl. Acad. Sci. U. S. A. 108:534-539.
38. Miyamoto T, Yokoyama M, Kono K, Shioda T, Sato H, Nakayama EE. 2011. A single amino acid of human immunodeficiency virus type 2 capsid protein affects conformation of two external loops and viral sensitivity to TRIM5a. PLoS One 6:e22779. doi:10.1371/journal.pone.0022779.
39. Song H, Nakayama EE, Yokoyama M, Sato H, Levy JA, Shioda T. 2007. A single amino acid of the human immunodeficiency virus type 2 capsid affects its replication in the presence of cynomolgus monkey and human TRIM5αs. J. Virol. 81:7280-7285.
40. Kuroishi A, Saito A, Shingai Y, Shioda T, Nomaguchi M, Adachi A, Akari H, Nakayama EE. 2009. Modification of a loop sequence between alpha-helices 6 and 7 of virus capsid (CA) protein in a human immunodeficiency virus type 1 (HIV-1) derivative that has simian immunodeficiency virus (SIVmac239) vif and CA α-helices 4 and 5 loop improves replication in cynomolgus monkey cells. Retrovirology 6:70. doi:10.1186 /1742-4690-6-70.
41. Pacheco B, Finzi A, Stremlau M, Sodroski J. 2010. Adaptation of HIV-1 to cells expressing rhesus monkey TRIM5a. Virology 408:204-212.
42. Kono K, Song H, Yokoyama M, Sato H, Shioda T, Nakayama EE. 2010. Multiple sites in the N-terminal half of simian immunodeficiency virus capsid protein contribute to evasion from rhesus monkey TRIM5alphamediated restriction. Retrovirology 7:72. doi:10.1186/1742-4690-7-72.
43. Biris N, Yang Y, Taylor AB, Tomashevski A, Guo M, Hart PJ, Diaz-Griffero F, Ivanov DN. 2012. Structure of the rhesus monkey TRIM5alpha PRYSPRY domain, the HIV capsid recognition module. Proc. Natl. Acad. Sci. U. S. A. 109:13278-13283.
44. Yang H, Ji X, Zhao G, Ning J, Zhao Q, Aiken C, Gronenborn AM, Zhang P, Xiong Y. 2012. Structural insight into HIV-1 capsid recognition by rhesus TRIM5alpha. Proc. Natl. Acad. Sci. U. S. A. 109:18372-18377.
45. Stevens A, Bock M, Ellis S, LeTissier P, Bishop KN, Yap MW, Taylor W, Stoye JP. 2004. Retroviral capsid determinants of Fv1 NB-and NRtropism. J. Virol. 78:9592-9598.
46. Auerbach MR, Shu C, Kaplan A, Singh IR. 2003. Functional characterization of a portion of the Moloney murine leukemia gag gene by genetic footprinting. Proc. Natl. Acad. Sci. U. S. A. 100:11678-11683.
47. Towers G, Bock M, Martin S, Takeuchi Y, Stoye JP, Danos O. 2000. A conserved mechanism of retrovirus restriction in mammals. Proc. Natl. Acad. Sci. U. S. A. 97:12295-12299.
48. Newman RM, Hall L, Connole M, Chen G-L, Sato S, Yuste E, Diehl W, Hunter E, Kaur A, Miller GM, Johnson WE. 2006. Balancing selection and the evolution of functional polymorphism in Old World monkey TRIM5a. Proc. Natl. Acad. Sci. U. S. A. 103:19134-19139.
49. 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.
50. Li X, Yeung DF, Fiegen AM, Sodroski J. 2011. Determinants of the higher order association of the restriction factor TRIM5alpha and other tripartite motif (TRIM) proteins. J. Biol. Chem. 286:27959-27970.