Intersection of the multivesicular body pathway and lipid homeostasis in RNA replication by a positive-strand RNA virus

Journal of Virology

Volumn 85, Issue 11, 2011, Pages 5494-5503

  Wang, Xiaofeng ^a,b   Diaz, Arturo ^a   Hao, Linhui ^a   Gancarz, Brandi ^a   den Boon, Johan A ^a   Ahlquist, Paul ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID; PROTEASOME; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MGA2P; TRANSCRIPTION FACTOR SPT23P; UBIQUITIN; UNCLASSIFIED DRUG; VIRUS RNA;

ARTICLE; BRO1 GENE; CONTROLLED STUDY; DOA4 GENE; GENE; GENE CONTROL; GENE DELETION; LIPID METABOLISM; LIPOGENESIS; MOSAIC VIRUS; MULTIVESICULAR BODY; NONHUMAN; OLE1 GENE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PROCESSING; RETROVIRUS; RFU1 GENE; RNA REPLICATION; UBIQUITINATION; UBP6 GENE; UFD3 GENE; UPREGULATION; VIRION; VIRUS ENVELOPE; VIRUS GENE; VIRUS RELEASE;

BROMOVIRUS; ENDOPEPTIDASES; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; GENE DELETION; LIPID METABOLISM; MULTIVESICULAR BODIES; RNA, VIRAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN THIOLESTERASE; VIRUS REPLICATION;

BROME MOSAIC VIRUS; RNA VIRUSES;

EID: 79956061717     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02031-10     Document Type: Article

References (75)

1. Aguilar, P. S., and D. de Mendoza. 2006. Control of fatty acid desaturation: a mechanism conserved from bacteria to humans. Mol. Microbiol. 62:1507-1514.
2. Ahlquist, P. 2006. Parallels among positive-strand RNA viruses, reversetranscribing viruses and double-stranded RNA viruses. Nat. Rev. Microbiol. 4:371-382.
3. Ahola, T., and P. Ahlquist. 1999. Putative RNA capping activities encoded by brome mosaic virus: methylation and covalent binding of guanylate by replicase protein 1a. J. Virol. 73:10061-10069.
4. Amerik, A., N. Sindhi, and M. Hochstrasser. 2006. A conserved late endosome-targeting signal required for Doa4 deubiquitylating enzyme function. J. Cell Biol. 175:825-835.
5. Amerik, A. Y., S. J. Li, and M. Hochstrasser. 2000. Analysis of the deubiquitinating enzymes of the yeast Saccharomyces cerevisiae. Biol. Chem. 381: 981-992.
6. Amerik, A. Y., J. Nowak, S. Swaminathan, and M. Hochstrasser. 2000. The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar proteinsorting and endocytic pathways. Mol. Biol. Cell 11:3365-3380.
7. Auld, K. L., C. R. Brown, J. M. Casolari, S. Komili, and P. A. Silver. 2006. Genomic association of the proteasome demonstrates overlapping gene regulatory activity with transcription factor substrates. Mol. Cell 21:861-871.
8. Auld, K. L., and P. A. Silver. 2006. Transcriptional regulation by the proteasome as a mechanism for cellular protein homeostasis. Cell Cycle 5:1503-1505.
9. Barajas, D., Y. Jiang, and P. D. Nagy. 2009. A unique role for the host ESCRT proteins in replication of Tomato bushy stunt virus. PLoS Pathog. 5:e1000705.
10. Bieniasz, P. D. 2009. The cell biology of HIV-1 virion genesis. Cell Host Microbe 5:550-558.
11. Calistri, A., C. Salata, C. Parolin, and G. Palu. 2009. Role of multivesicular bodies and their components in the egress of enveloped RNA viruses. Rev. Med. Virol. 19:31-45.
12. Carette, J. E., M. Stuiver, J. Van Lent, J. Wellink, and A. Van Kammen. 2000. Cowpea mosaic virus infection induces a massive proliferation of endoplasmic reticulum but not Golgi membranes and is dependent on de novo membrane synthesis. J. Virol. 74:6556-6563.
13. Castorena, K. M., K. A. Stapleford, and D. J. Miller. 2010. Complementary transcriptomic, lipidomic, and targeted functional genetic analyses in cultured Drosophila cells highlight the role of glycerophospholipid metabolism in Flock House virus RNA replication. BMC Genomics 11:183.
14. Chatellard-Causse, C., et al. 2002. Alix (ALG-2-interacting protein X), a protein involved in apoptosis, binds to endophilins and induces cytoplasmic vacuolization. J. Biol. Chem. 277:29108-29115.
15. Chen, J., and P. Ahlquist. 2000. Brome mosaic virus polymerase-like protein 2a is directed to the endoplasmic reticulum by helicase-like viral protein 1a. J. Virol. 74:4310-4318.
16. Cherry, S., et al. 2006. COPI activity coupled with fatty acid biosynthesis is required for viral replication. PLoS Pathog. 2:e102.
17. den Boon, J., A. Diaz, and Ahlquist. 2010. Cytoplasmic viral replication complexes. Cell Host Microbe 8:77-85.
18. den Boon, J. A., J. Chen, and P. Ahlquist. 2001. Identification of sequences in brome mosaic virus replicase protein 1a that mediate association with endoplasmic reticulum membranes. J. Virol. 75:12370-12381.
19. Diaz, A., X. Wang, and P. Ahlquist. 2010. Membrane-shaping host reticulon proteins play crucial roles in viral RNA replication compartment formation and function. Proc. Natl. Acad. Sci. U. S. A. 107:16291-16296.
20. Dobrosotskaya, I. Y., A. C. Seegmiller, M. S. Brown, J. L. Goldstein, and R. B. Rawson. 2002. Regulation of SREBP processing and membrane lipid production by phospholipids in Drosophila. Science 296:879-883.
21. Dupre, S., and R. Haguenauer-Tsapis. 2001. Deubiquitination step in the endocytic pathway of yeast plasma membrane proteins: crucial role of Doa4p ubiquitin isopeptidase. Mol. Cell. Biol. 21:4482-4494.
22. Finley, D., et al. 1994. Inhibition of proteolysis and cell cycle progression in a multiubiquitination-deficient yeast mutant. Mol. Cell. Biol. 14:5501-5509.
23. Guinea, R., and L. Carrasco. 1990. Phospholipid biosynthesis and poliovirus genome replication, two coupled phenomena. EMBO J. 9:2011-2016.
24. Hegemann, J. H., et al. 1999. A fast method to diagnose chromosome and plasmid loss in Saccharomyces cerevisiae strains. Yeast 15:1009-1019.
25. Hitchcock, A. L., et al. 2001. The conserved npl4 protein complex mediates proteasome-dependent membrane-bound transcription factor activation. Mol. Biol. Cell 12:3226-3241.
26. Hoppe, T., et al. 2000. Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 102:577-586.
27. Hurley, J. H., and S. D. Emr. 2006. The ESCRT complexes: structure and mechanism of a membrane-trafficking network. Annu. Rev. Biophys. Biomol. Struct. 35:277-298.
28. Janda, M., and P. Ahlquist. 1998. Brome mosaic virus RNA replication protein 1a dramatically increases in vivo stability but not translation of viral genomic RNA3. Proc. Natl. Acad. Sci. U. S. A. 95:2227-2232.
29. Janda, M., and P. Ahlquist. 1993. RNA-dependent replication, transcription, and persistence of brome mosaic virus RNA replicons in S. cerevisiae. Cell 72:961-970.
30. Johnson, E. S., P. C. Ma, I. M. Ota, and A. Varshavsky. 1995. A proteolytic pathway that recognizes ubiquitin as a degradation signal. J. Biol. Chem. 270:17442-17456.
31. Kao, C. C., and P. Ahlquist. 1992. Identification of the domains required for direct interaction of the helicase-like and polymerase-like RNA replication proteins of brome mosaic virus. J. Virol. 66:7293-7302.
32. Kapadia, S. B., and F. V. Chisari. 2005. Hepatitis C virus RNA replication is regulated by host geranylgeranylation and fatty acids. Proc. Natl. Acad. Sci. U. S. A. 102:2561-2566.
33. Katzmann, D. J., G. Odorizzi, and S. D. Emr. 2002. Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3:893-905.
34. Kimura, Y., et al. 2009. An inhibitor of a deubiquitinating enzyme regulates ubiquitin homeostasis. Cell 137:549-559.
35. Kong, F., K. Sivakumaran, and C. Kao. 1999. The N-terminal half of the brome mosaic virus 1a protein has RNA capping-associated activities: specificity for GTP and S-adenosylmethionine. Virology 259:200-210.
36. Kopek, B. G., G. Perkins, D. J. Miller, M. H. Ellisman, and P. Ahlquist. 2007. Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle. PLoS Biol. 5:e220.
37. Krol, M. A., et al. 1999. RNA-controlled polymorphism in the in vivo assembly of 180-subunit and 120-subunit virions from a single capsid protein. Proc. Natl. Acad. Sci. U. S. A. 96:13650-13655.
38. Kushner, D. B., et al. 2003. Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. Proc. Natl. Acad. Sci. U. S. A. 100:15764-15769.
39. Lee, W. M., and P. Ahlquist. 2003. Membrane synthesis, specific lipid requirements, and localized lipid composition changes associated with a positive-strand RNA virus RNA replication protein. J. Virol. 77:12819-12828.
40. Lee, W. M., M. Ishikawa, and P. Ahlquist. 2001. Mutation of host Δ9 fatty acid desaturase inhibits brome mosaic virus RNA replication between template recognition and RNA synthesis. J. Virol. 75:2097-2106.
41. Leggett, D. S., et al. 2002. Multiple associated proteins regulate proteasome structure and function. Mol. Cell 10:495-507.
42. Liu, L., et al. 2009. An amphipathic alpha-helix controls multiple roles of brome mosaic virus protein 1a in RNA replication complex assembly and function. PLoS Pathog. 5:e1000351.
43. Losko, S., F. Kopp, A. Kranz, and R. Kolling. 2001. Uptake of the ATPbinding cassette (ABC) transporter Ste6 into the yeast vacuole is blocked in the doa4 mutant. Mol. Biol. Cell 12:1047-1059.
44. Luhtala, N., and G. Odorizzi. 2004. Bro1 coordinates deubiquitination in the multivesicular body pathway by recruiting Doa4 to endosomes. J. Cell Biol. 166:717-729.
45. Martin-Serrano, J., D. Perez-Caballero, and P. D. Bieniasz. 2004. Contextdependent effects of L domains and ubiquitination on viral budding. J. Virol. 78:5554-5563.
46. Matsuo, H., et al. 2004. Role of LBPA and Alix in multivesicular liposome formation and endosome organization. Science 303:531-534.
47. Miller, S., and J. Krijnse-Locker. 2008. Modification of intracellular membrane structures for virus replication. Nat. Rev. Microbiol. 6:363-374.
48. Morita, E., and W. I. Sundquist. 2004. Retrovirus budding. Annu. Rev. Cell Dev. Biol. 20:395-425.
49. Nikko, E., and B. Andre. 2007. Split-ubiquitin two-hybrid assay to analyze protein-protein interactions at the endosome: application to Saccharomyces cerevisiae Bro1 interacting with ESCRT complexes, the Doa4 ubiquitin hydrolase, and the Rsp5 ubiquitin ligase. Eukaryot. Cell 6:1266-1277.
50. Papa, F. R., A. Y. Amerik, and M. Hochstrasser. 1999. Interaction of the Doa4 deubiquitinating enzyme with the yeast 26S proteasome. Mol. Biol. Cell 10:741-756.
51. Papa, F. R., and M. Hochstrasser. 1993. The yeast DOA4 gene encodes a deubiquitinating enzyme related to a product of the human tre-2 oncogene. Nature 366:313-319.
52. Perez, L., R. Guinea, and L. Carrasco. 1991. Synthesis of Semliki Forest virus RNA requires continuous lipid synthesis. Virology 183:74-82.
53. Piper, R. C., and D. J. Katzmann. 2007. Biogenesis and function of multivesicular bodies. Annu. Rev. Cell Dev. Biol. 23:519-547.
54. Piwko, W., and S. Jentsch. 2006. Proteasome-mediated protein processing by bidirectional degradation initiated from an internal site. Nat. Struct. Mol. Biol. 13:691-697.
55. Rape, M., et al. 2001. Mobilization of processed, membrane-tethered SPT23 transcription factor by CDC48(UFD1/NPL4), a ubiquitin-selective chaperone. Cell 107:667-677.
56. Rape, M., and S. Jentsch. 2004. Productive RUPture: activation of transcription factors by proteasomal processing. Biochim. Biophys. Acta 1695:209-213.
57. Restrepo-Hartwig, M., and P. Ahlquist. 1999. Brome mosaic virus RNA replication proteins 1a and 2a colocalize and 1a independently localizes on the yeast endoplasmic reticulum. J. Virol. 73:10303-10309.
58. Restrepo-Hartwig, M. A., and P. Ahlquist. 1996. Brome mosaic virus helicase-and polymerase-like proteins colocalize on the endoplasmic reticulum at sites of viral RNA synthesis. J. Virol. 70:8908-8916.
59. Richter, C., M. West, and G. Odorizzi. 2007. Dual mechanisms specify Doa4-mediated deubiquitination at multivesicular bodies. EMBO J. 26: 2454-2464.
60. Row, P. E., I. A. Prior, J. McCullough, M. J. Clague, and S. Urbe. 2006. The ubiquitin isopeptidase UBPY regulates endosomal ubiquitin dynamics and is essential for receptor down-regulation. J. Biol. Chem. 281:12618-12624.
61. Rumpf, S., and S. Jentsch. 2006. Functional division of substrate processing cofactors of the ubiquitin-selective Cdc48 chaperone. Mol. Cell 21:261-269.
62. Salonen, A., T. Ahola, and L. Kaariainen. 2005. Viral RNA replication in association with cellular membranes. Curr. Top. Microbiol. Immunol. 285: 139-173.
63. Schwartz, M., et al. 2002. A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol. Cell 9:505-514.
64. Sharma, M., Z. Sasvari, and P. D. Nagy. 2010. Inhibition of sterol biosynthesis reduces tombusvirus replication in yeast and plants. J. Virol. 84:2270-2281.
65. Shcherbik, N., T. Zoladek, J. T. Nickels, and D. S. Haines. 2003. Rsp5p is required for ER bound Mga2p120 polyubiquitination and release of the processed/tethered transactivator Mga2p90. Curr. Biol. 13:1227-1233.
66. Stapleford, K. A., D. Rapaport, and D. J. Miller. 2009. Mitochondrionenriched anionic phospholipids facilitate Flock House virus RNA polymerase membrane association. J. Virol. 83:4498-4507.
67. Stukey, J. E., V. M. McDonough, and C. E. Martin. 1989. Isolation and characterization of OLE1, a gene affecting fatty acid desaturation from Saccharomyces cerevisiae. J. Biol. Chem. 264:16537-16544.
68. Sullivan, M. L., and P. Ahlquist. 1999. A brome mosaic virus intergenic RNA3 replication signal functions with viral replication protein 1a to dramatically stabilize RNA in vivo. J. Virol. 73:2622-2632.
69. Swaminathan, S., A. Y. Amerik, and M. Hochstrasser. 1999. The Doa4 deubiquitinating enzyme is required for ubiquitin homeostasis in yeast. Mol. Biol. Cell 10:2583-2594.
70. Wang, X., and P. Ahlquist. 2008. Brome mosaic virus (Bromoviridae), p. 381-386. In B. W. J. Mahy and M. H. V. van Regenmortel (ed.), Encyclopedia of virology, 3rd ed. Academic Press, New York, NY.
71. Wang, X., et al. 2005. Brome mosaic virus 1a nucleoside triphosphatase/helicase domain plays crucial roles in recruiting RNA replication templates. J. Virol. 79:13747-13758.
72. Wu, S. X., P. Ahlquist, and P. Kaesberg. 1992. Active complete in vitro replication of nodavirus RNA requires glycerophospholipid. Proc. Natl. Acad. Sci. U. S. A. 89:11136-11140.
73. Ye, J. 2007. Reliance of host cholesterol metabolic pathways for the life cycle of hepatitis C virus. PLoS Pathog. 3:e108.
74. Ye, J., et al. 2003. Disruption of hepatitis C virus RNA replication through inhibition of host protein geranylgeranylation. Proc. Natl. Acad. Sci. U. S. A. 100:15865-15870.
75. Zhang, S., Y. Skalsky, and D. J. Garfinkel. 1999. MGA2 or SPT23 is required for transcription of the delta9 fatty acid desaturase gene, OLE1, and nuclear membrane integrity in Saccharomyces cerevisiae. Genetics 151:473-483.