Human endogenous retrovirus K gag coassembles with HIV-1 gag and reduces the release efficiency and infectivity of HIV-1

Journal of Virology

Volumn 86, Issue 20, 2012, Pages 11194-11208

  Monde, Kazuaki ^a,b   Contreras Galindo, Rafael ^a   Kaplan, Mark H ^a   Markovitz, David M ^a   Ono, Akira ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b KUMAMOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GAG PROTEIN; PROTEINASE;

ARTICLE; CELL MEMBRANE; CELL NUCLEUS; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOPRECIPITATION; INTRACELLULAR TRANSPORT; MYRISTYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEFECT; PROTEIN DEPLETION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN RNA BINDING; PROTEIN SECRETION; PROTEIN TRANSPORT; RETROVIRUS; RETROVIRUS K; VIRION; VIRUS INFECTIVITY; VIRUS NUCLEOCAPSID;

CELL LINE, TUMOR; CELL MEMBRANE; ENDOGENOUS RETROVIRUSES; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GENE PRODUCTS, GAG; HELA CELLS; HIV-1; HUMANS; PROTEIN TRANSPORT; RETROVIRIDAE PROTEINS; VIRUS RELEASE; VIRUS REPLICATION;

HUMAN ENDOGENOUS RETROVIRUS K; HUMAN ENDOGENOUS RETROVIRUSES; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84869105185     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00301-12     Document Type: Article

References (55)

1. Ako-Adjei D, Johnson MC, Vogt VM. 2005. The retroviral capsid domain dictates virion size, morphology, and coassembly of gag into viruslike particles. J. Virol. 79:13463-13472.
2. Arien KK, et al. 2005. The replicative fitness of primary human immunodeficiency virus type 1 (HIV-1) group M, HIV-1 group O, and HIV-2 isolates. J. Virol. 79:8979-8990.
3. Bailes E, et al. 2003. Hybrid origin of SIV in chimpanzees. Science 300: 1713.
4. Balasubramaniam M, Freed EO. 2011. New insights into HIV assembly and trafficking. Physiology (Bethesda) 26:236-251.
5. Bannert N, Kurth R. 2004. Retroelements and the human genome: new perspectives on an old relation. Proc. Natl. Acad. Sci. U. S. A. 101(Suppl. 2):14572-14579.
6. Beimforde N, Hanke K, Ammar I, Kurth R, Bannert N. 2008. Molecular cloning and functional characterization of the human endogenous retrovirus K113. Virology 371:216-225.
7. Bennett RP, Wills JW. 1999. Conditions for copackaging Rous sarcoma virus and murine leukemia virus Gag proteins during retroviral budding. J. Virol. 73:2045-2051.
8. Boller K, Frank H, Lower J, Lower R, Kurth R. 1983. Structural organization of unique retrovirus-like particles budding from human teratocarcinoma cell lines. J. Gen. Virol. 64:2549-2559.
9. Boller K, et al. 2008. Human endogenous retrovirus HERV-K113 is capable of producing intact viral particles. J. Gen. Virol. 89:567-572.
10. Boyko V, et al. 2006. Coassembly and complementation of Gag proteins from HIV-1 and HIV-2, two distinct human pathogens. Mol. Cell 23:281-287.
11. Chen J, Pathak VK, Peng W, Hu WS. 2008. Capsid proteins from human immunodeficiency virus type 1 and simian immunodeficiency virus SIVmac can coassemble into mature cores of infectious viruses. J. Virol. 82:8253-8261.
12. Colicelli J, Goff SP. 1988. Sequence and spacing requirements of a retrovirus integration site. J. Mol. Biol. 199:47-59.
13. Contreras-Galindo R, Almodovar-Camacho S, Gonzalez-Ramirez S, Lorenzo E, Yamamura Y. 2007. Comparative longitudinal studies of HERV-K and HIV-1 RNA titers in HIV-1-infected patients receiving successful versus unsuccessful highly active antiretroviral therapy. AIDS Res. Hum. Retroviruses 23:1083-1086.
14. Contreras-Galindo R, et al. 2006. A new real-time-RT-PCR for quantitation of human endogenous retroviruses type K (HERV-K) RNA load in plasma samples: increased HERV-K RNA titers in HIV-1 patients with HAART non-suppressive regimens. J. Virol. Methods 136:51-57.
15. Contreras-Galindo R, et al. 2012. Characterization of human endogenous retroviral elements in the blood of HIV-1-infected individuals. J. Virol. 86:262-276.
16. Contreras-Galindo R, Kaplan MH, Markovitz DM, Lorenzo E, Yamamura Y. 2006. Detection of HERV-K(HML-2) viral RNA in plasma of HIV type 1-infected individuals. AIDS Res. Hum. Retroviruses 22:979-984.
17. Contreras-Galindo R, Lopez P, Velez R, Yamamura Y. 2007. HIV-1 infection increases the expression of human endogenous retroviruses type K (HERV-K) in vitro. AIDS Res. Hum. Retroviruses 23:116-122.
18. Dewannieux M, et al. 2006. Identification of an infectious progenitor for the multiple-copy HERV-K human endogenous retroelements. Genome Res. 16:1548-1556.
19. Garrison KE, et al. 2007. T cell responses to human endogenous retroviruses in HIV-1 infection. PLoS Pathog. 3:e165. doi:10.1371/journal.ppat.0030165.
20. Garrus JE, et al. 2001. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107:55-65.
21. George M, et al. 2011. Identification of the protease cleavage sites in a reconstituted Gag polyprotein of an HERV-K(HML-2) element. Retrovirology 8:30.
22. Gervaix A, et al. 1997. A new reporter cell line to monitor HIV infection and drug susceptibility in vitro. Proc. Natl. Acad. Sci. U. S. A. 94:4653-4658.
23. Gonzalez-Hernandez MJ, et al. 2012. Expression of human endogenous retrovirus type-K (HML-2) is activated by the Tat protein of HIV-1. J. Virol. 86:7790-7805
24. Gottlieb GS, et al. 2003. Molecular epidemiology of dual HIV-1/HIV-2 seropositive adults from Senegal, West Africa. AIDS Res. Hum. Retroviruses 19:575-584.
25. Gottlinger HG, Dorfman T, Sodroski JG, Haseltine WA. 1991. Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release. Proc. Natl. Acad. Sci. U. S. A. 88:3195-3199.
26. Heslin DJ, et al. 2009. A single amino acid substitution in a segment of the CA protein within Gag that has similarity to human immunodeficiency virus type 1 blocks infectivity of a human endogenous retrovirus K provirus in the human genome. J. Virol. 83:1105-1114.
27. Hogue IB, Hoppe A, Ono A. 2009. Quantitative fluorescence resonance energy transfer microscopy analysis of the human immunodeficiency virus type 1 Gag-Gag interaction: relative contributions of the CA and NC domains and membrane binding. J. Virol. 83:7322-7336.
28. Huang M, Orenstein JM, Martin MA, Freed EO. 1995. p6Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease. J. Virol. 69:6810-6818.
29. Jern P, Coffin JM. 2008. Effects of retroviruses on host genome function. Annu. Rev. Genet. 42:709-732.
30. Jolicoeur P, Baltimore D. 1976. Effect of Fv-1 gene product on proviral DNA formation and integration in cells infected with murine leukemia viruses. Proc. Natl. Acad. Sci. U. S. A. 73:2236-2240.
31. Kannangai R, et al. 2003. HIV-2 subtype circulating in India (south). J. Acquir. Immune Defic. Syndr. 33:219-222.
32. Kraus B, Boller K, Reuter A, Schnierle BS. 2011. Characterization of the human endogenous retrovirus K Gag protein: identification of protease cleavage sites. Retrovirology 8:21.
33. Kuhelj R, et al. 2001. Inhibition of human endogenous retrovirus-K10 protease in cell-free and cell-based assays. J. Biol. Chem. 276:16674-16682.
34. Kutluay SB, Bieniasz PD. 2010. Analysis of the initiating events in HIV-1 particle assembly and genome packaging. PLoS Pathog. 6:e1001200. doi: 10.1371/journal.ppat.1001200.
35. Lander ES, et al. 2001. Initial sequencing and analysis of the human genome. Nature 409:860-921.
36. Lee SK, Boyko V, Hu WS. 2007. Capsid is an important determinant for functional complementation of murine leukemia virus and spleen necrosis virus Gag proteins. Virology 360:388-397.
37. Lee YN, Bieniasz PD. 2007. Reconstitution of an infectious human endogenous retrovirus. PLoS Pathog. 3:e10. doi:10.1371/journal.ppat.0030010.
38. Lefebvre G, et al. 2011. Analysis of HIV-1 expression level and sense of transcription by high-throughput sequencing of the infected cell. J. Virol. 85:6205-6211.
39. Li F, Chen C, Puffer BA, Montelaro RC. 2002. Functional replacement and positional dependence of homologous and heterologous L domains in equine infectious anemia virus replication. J. Virol. 76:1569-1577.
40. Li SK, et al. Detection and identification of plasma bacterial and viral elements in HIV/AIDS patients in comparison to healthy adults. Clin. Microbiol. Infect. doi:10.1111/j.1469-0691.2011.03690.x.
41. Lower R, Lower J, Kurth R. 1996. The viruses in all of us: characteristics and biological significance of human endogenous retrovirus sequences. Proc. Natl. Acad. Sci. U. S. A. 93:5177-5184.
42. Martin-Serrano J, Perez-Caballero D, Bieniasz PD. 2004. Contextdependent effects of L domains and ubiquitination on viral budding. J. Virol. 78:5554-5563.
43. Ono A, Freed EO. 1999. Binding of human immunodeficiency virus type 1 Gag to membrane: role of the matrix amino terminus. J. Virol. 73:4136-4144.
44. Ono A, Waheed AA, Joshi A, Freed EO. 2005. Association of human immunodeficiency virus type 1 gag with membrane does not require highly basic sequences in the nucleocapsid: use of a novel Gag multimerization assay. J. Virol. 79:14131-14140.
45. Ott DE, et al. 2003. Elimination of protease activity restores efficient virion production to a human immunodeficiency virus type 1 nucleocapsid deletion mutant. J. Virol. 77:5547-5556.
46. Parent LJ, et al. 1995. Positionally independent and exchangeable late budding functions of the Rous sarcoma virus and human immunodeficiency virus Gag proteins. J. Virol. 69:5455-5460.
47. Salemi M, et al. 2003. Mosaic genomes of the six major primate lentivirus lineages revealed by phylogenetic analyses. J. Virol. 77:7202-7213.
48. Scheifele LZ, Garbitt RA, Rhoads JD, Parent LJ. 2002. Nuclear entry and CRM1-dependent nuclear export of the Rous sarcoma virus Gag polyprotein. Proc. Natl. Acad. Sci. U. S. A. 99:3944-3949.
49. SenGupta D, et al. 2011. Strong human endogenous retrovirus-specific T cell responses are associated with control of HIV-1 in chronic infection. J. Virol. 85:6977-6985.
50. Sveda MM, Soeiro R. 1976. Host restriction of Friend leukemia virus: synthesis and integration of the provirus. Proc. Natl. Acad. Sci. U. S. A. 73:2356-2360.
51. Tandon R, et al. 2011. Identification of human endogenous retrovirusspecific T cell responses in vertically HIV-1-infected subjects. J. Virol. 85:11526-11531.
52. Turner G, et al. 2001. Insertional polymorphisms of full-length endogenous retroviruses in humans. Curr. Biol. 11:1531-1535.
53. Venter JC, et al. 2001. The sequence of the human genome. Science 291:1304-1351.
54. Vogetseder W, Dumfahrt A, Mayersbach P, Schonitzer D, Dierich MP. 1993. Antibodies in human sera recognizing a recombinant outer membrane protein encoded by the envelope gene of the human endogenous retrovirus K. AIDS Res. Hum. Retroviruses 9:687-694.
55. Willey RL, et al. 1988. In vitro mutagenesis identifies a region within the envelope gene of the human immunodeficiency virus that is critical for infectivity. J. Virol. 62:139-147.