Prototype foamy virus gag nuclear localization: A novel pathway among retroviruses

Journal of Virology

Volumn 85, Issue 18, 2011, Pages 9276-9285

  Müllers, Erik ^a,b   Stirnnagel, Kristin ^a,b   Kaulfuss, Sylvia ^a,b   Lindemann, Dirk ^a,b  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; GAG PROTEIN; GLYCINE; VIRUS ENVELOPE PROTEIN; VIRUS RNA;

ARTICLE; BINDING SITE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL DIVISION; CELL NUCLEUS; CHROMATIN; CONTROLLED STUDY; DAUGHTER CELL; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; INTERPHASE; MITOSIS; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN STRUCTURE; RETROVIRUS; SIMIAN VIRUS 40; SPUMA VIRUS; VIRUS INFECTIVITY; VIRUS PARTICLE; VIRUS REPLICATION;

ACTIVE TRANSPORT, CELL NUCLEUS; BINDING SITES; CELL LINE; CELL NUCLEUS; GENE PRODUCTS, GAG; HUMANS; MICROSCOPY, FLUORESCENCE; MUTANT PROTEINS; PROTEIN SORTING SIGNALS; SPUMAVIRUS; VIRUS REPLICATION;

HUMAN SPUMARETROVIRUS; SIMIAN VIRUS 40;

EID: 80052494157     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00663-11     Document Type: Article

References (58)

1. Afonso, P. V., A. Zamborlini, A. Saib, and R. Mahieux. 2007. Centrosome and retroviruses: the dangerous liaisons. Retrovirology 4:27.
2. Bodem, J., T. Schied, R. Gabriel, M. Rammling, and A. Rethwilm. 2011. Foamy virus nuclear RNA export is distinct from that of other retroviruses. J. Virol. 85:2333-2341.
3. Bodem, J., M. Zemba, and R. M. Flügel. 1998. Nuclear localization of the functional Bel 1 transactivator but not of the gag proteins of the feline foamy virus. Virology 251:22-27.
4. Bukrinsky, M. 2004. A hard way to the nucleus. Mol. Med. 10:1-5.
5. Bukrinsky, M. I., et al. 1993. A nuclear localization signal within HIV-1 matrix protein that governs infection of non-dividing cells. Nature 365:666-669.
6. Burhans, W. C., J. E. Selegue, and N. H. Heintz. 1986. Replication intermediates formed during initiation of DNA synthesis in methotrexate-resistant CHOC 400 cells are enriched for sequences derived from a specific, amplified restriction fragment. Biochemistry 25:441-449.
7. Butterfield-Gerson, K. L., L. Z. Scheifele, E. P. Ryan, A. K. Hopper, and L. J. Parent. 2006. Importin-beta family members mediate alpharetrovirus gag nuclear entry via interactions with matrix and nucleocapsid. J. Virol. 80: 1798-1806.
8. Caron, M. C., and M. Caruso. 2005. A nuclear localization signal in the matrix of spleen necrosis virus (SNV) does not allow efficient gene transfer into quiescent cells with SNV-derived vectors. Virology 338:292-296.
9. Delelis, O., A. Zamborlini, S. Thierry, and A. Saib. 2010. Chromosomal tethering and proviral integration. Biochim. Biophys. Acta 1799:207-216.
10. Depienne, C., et al. 2000. Cellular distribution and karyophilic properties of matrix, integrase, and Vpr proteins from the human and simian immunodeficiency viruses. Exp. Cell Res. 260:387-395.
11. DuBridge, R. B., et al. 1987. Analysis of mutation in human cells by using an Epstein-Barr virus shuttle system. Mol. Cell. Biol. 7:379-387.
12. Dunn, K. C., A. E. Aotaki-Keen, F. R. Putkey, and L. M. Hjelmeland. 1996. ARPE-19, a human retinal pigment epithelial cell line with differentiated properties. Exp. Eye Res. 62:155-169.
13. Dupont, S., et al. 1999. A novel nuclear export activity in HIV-1 matrix protein required for viral replication. Nature 402:681-685.
14. Fouchier, R. A., and M. H. Malim. 1999. Nuclear import of human immunodeficiency virus type-1 preintegration complexes. Adv. Virus Res. 52:275-299.
15. Freed, E. O. 1998. HIV-1 gag proteins: diverse functions in the virus life cycle. Virology 251:1-15.
16. Garbitt-Hirst, R., S. P. Kenney, and L. J. Parent. 2009. Genetic evidence for a connection between Rous sarcoma virus gag nuclear trafficking and genomic RNA packaging. J. Virol. 83:6790-6797.
17. Gerlich, D., J. Beaudouin, M. Gebhard, J. Ellenberg, and R. Eils. 2001. Four-dimensional imaging and quantitative reconstruction to analyse complex spatiotemporal processes in live cells. Nat. Cell Biol. 3:852-855.
18. Gudleski, N., J. M. Flanagan, E. P. Ryan, M. C. Bewley, and L. J. Parent. 2010. Directionality of nucleocytoplasmic transport of the retroviral gag protein depends on sequential binding of karyopherins and viral RNA. Proc. Natl. Acad. Sci. U. S. A. 107:9358-9363.
19. Haffar, O. K., et al. 2000. Two nuclear localization signals in the HIV-1 matrix protein regulate nuclear import of the HIV-1 pre-integration complex. J. Mol. Biol. 299:359-368.
20. Heinkelein, M., et al. 2002. Improved primate foamy virus vectors and packaging constructs. J. Virol. 76:3774-3783.
21. Hooks, J. J., and C. J. Gibbs, Jr. 1975. The foamy viruses. Bacteriol. Rev. 39:169-185.
22. Imrich, H., M. Heinkelein, O. Herchenroder, and A. Rethwilm. 2000. Primate foamy virus Pol proteins are imported into the nucleus. J. Gen. Virol. 81:2941-2947.
23. Keppler, A., C. Arrivoli, L. Sironi, and J. Ellenberg. 2006. Fluorophores for live cell imaging of AGT fusion proteins across the visible spectrum. Biotechniques 41:167-170, 172, 174-175.
24. Kong, X. H., et al. 2005. The requirements and mechanism for capsid assembly and budding of bovine foamy virus. Arch. Virol. 150:1677-1684.
25. Lehmann-Che, J., et al. 2005. Protease-dependent uncoating of a complex retrovirus. J. Virol. 79:9244-9253.
26. Lindemann, D., M. Bock, M. Schweizer, and A. Rethwilm. 1997. Efficient pseudotyping of murine leukemia virus particles with chimeric human foamy virus envelope proteins. J. Virol. 71:4815-4820.
27. Lindemann, D., et al. 2001. A particle-associated glycoprotein signal peptide essential for virus maturation and infectivity. J. Virol. 75:5762-5771.
28. Lindemann, D., and A. Rethwilm. 1998. Characterization of a human foamy virus 170-kilodalton Env-Bet fusion protein generated by alternative splicing. J. Virol. 72:4088-4094.
29. Linial, M. L. 1999. Foamy viruses are unconventional retroviruses. J. Virol. 73:1747-1755.
30. Linial, M. L., and S. W. Eastman. 2003. Particle assembly and genome packaging. Curr. Top. Microbiol. Immunol. 277:89-110.
31. Lo, Y. T., T. Tian, P. E. Nadeau, J. Park, and A. Mergia. 2010. The foamy virus genome remains unintegrated in the nuclei of G1/S phase-arrested cells, and integrase is critical for preintegration complex transport into the nucleus. J. Virol. 84:2832-2842.
32. Moebes, A., et al. 1997. Human foamy virus reverse transcription that occurs late in the viral replication cycle. J. Virol. 71:7305-7311.
33. Müllers, E., et al. 2011. Novel functions of prototype foamy virus Gag glycine-arginine-rich boxes in reverse transcription and particle morphogenesis. J. Virol. 85:1452-1463.
34. Nash, M. A., M. K. Meyer, G. L. Decker, and R. B. Arlinghaus. 1993. A subset of Pr65gag is nucleus associated in murine leukemia virus-infected cells. J. Virol. 67:1350-1356.
35. Patton, G. S., O. Erlwein, and M. O. McClure. 2004. Cell-cycle dependence of foamy virus vectors. J. Gen. Virol. 85:2925-2930.
36. Petit, C., et al. 2003. Targeting of incoming retroviral Gag to the centrosome involves a direct interaction with the dynein light chain 8. J. Cell Sci. 116: 3433-3442.
37. Pietschmann, T., et al. 1999. Foamy virus capsids require the cognate envelope protein for particle export. J. Virol. 73:2613-2621.
38. Pincetic, A., and J. Leis. 2009. The mechanism of budding of retroviruses from cell membranes. Adv. Virol. 2009:6239691-6239699.
39. Rasheed, S., W. A. Nelson-Rees, E. M. Toth, P. Arnstein, and M. B. Gardner. 1974. Characterization of a newly derived human sarcoma cell line (HT-1080). Cancer 33:1027-1033.
40. Renault, N., et al. 2011. A nuclear export signal within the structural Gag protein is required for prototype foamy virus replication. Retrovirology 8:6.
41. Rethwilm, A. 2003. The replication strategy of foamy viruses. Curr. Top. Microbiol. Immunol. 277:1-26.
42. Saïb, A., F. Puvion Dutilleul, M. Schmid, J. Peries, and H. de The. 1997. Nuclear targeting of incoming human foamy virus Gag proteins involves a centriolar step. J. Virol. 71:1155-1161.
43. Scheifele, L. Z., R. A. Garbitt, J. D. Rhoads, and L. J. Parent. 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.
44. Scheifele, L. Z., E. P. Ryan, and L. J. Parent. 2005. Detailed mapping of the nuclear export signal in the Rous sarcoma virus Gag protein. J. Virol. 79:8732-8741.
45. Schliephake, A. W., and A. Rethwilm. 1994. Nuclear localization of foamy virus Gag precursor protein. J. Virol. 68:4946-4954.
46. Shooter, R. A., and G. O. Gey. 1952. Studies of the mineral requirements of mammalian cells. Br. J. Exp. Pathol. 33:98-103.
47. Stange, A., D. Luftenegger, J. Reh, W. Weissenhorn, and D. Lindemann. 2008. Subviral particle release determinants of prototype foamy virus. J. Virol. 82:9858-9869.
48. Stange, A., et al. 2005. Characterization of prototype foamy virus gag late assembly domain motifs and their role in particle egress and infectivity. J. Virol. 79:5466-5476.
49. Stenbak, C. R., and M. L. Linial. 2004. Role of the C terminus of foamy virus Gag in RNA packaging and Pol expression. J. Virol. 78:9423-9430.
50. Stirnnagel, K., et al. 2010. Analysis of prototype foamy virus particle-host cell interaction with autofluorescent retroviral particles. Retrovirology 7:45.
51. Suzuki, Y., and R. Craigie. 2007. The road to chromatin-nuclear entry of retroviruses. Nat. Rev. Microbiol. 5:187-196.
52. Tobaly-Tapiero, J., et al. 2008. Chromatin tethering of incoming foamy virus by the structural Gag protein. Traffic 9:1717-1727.
53. Tobaly-Tapiero, J., et al. 2000. Isolation and characterization of an equine foamy virus. J. Virol. 74:4064-4073.
54. Trobridge, G., and D. W. Russell. 2004. Cell cycle requirements for transduction by foamy virus vectors compared to those of oncovirus and lentivirus vectors. J. Virol. 78:2327-2335.
55. Winkler, I., et al. 1997. Characterization of the genome of feline foamy virus and its proteins shows distinct features different from those of primate spumaviruses. J. Virol. 71:6727-6741.
56. Wong, L. Y., G. A. Matchett, and A. C. Wilson. 2004. Transcriptional activation by the Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen is facilitated by an N-terminal chromatin-binding motif. J. Virol. 78:10074-10085.
57. Yu, S. F., et al. 1996. The carboxyl terminus of the human foamy virus Gag protein contains separable nucleic acid binding and nuclear transport domains. J. Virol. 70:8255-8262.
58. Zhang, X. Y., et al. 2002. Lentiviral vectors for sustained transgene expression in human bone marrow-derived stromal cells. Mol. Ther. 5:555-565.