Rab5 and class III phosphoinositide 3-kinase Vps34 are involved in hepatitis C virus NS4B-induced autophagy

Journal of Virology

Volumn 85, Issue 20, 2011, Pages 10561-10571

  Su, Wen Chi ^a   Chao, Ti Chun ^a,b   Huang, Yih Leh ^a   Weng, Shih Che ^a   Jeng, King Song ^a   Lai, Michael M C ^a,c  

^a INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^b NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 4E BINDING PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; NONSTRUCTURAL PROTEIN 4B; PHOSPHATIDYLINOSITOL 3 KINASE; RAB PROTEIN; S6 KINASE;

AMINO ACID SEQUENCE; ARTICLE; AUTOPHAGY; CELL VACUOLE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; GENE OVEREXPRESSION; GENE SILENCING; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

AUTOPHAGY; CELL LINE; CLASS III PHOSPHATIDYLINOSITOL 3-KINASES; GENE SILENCING; HEPACIVIRUS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOPRECIPITATION; MUTANT PROTEINS; PROTEIN BINDING; RAB5 GTP-BINDING PROTEINS; VIRAL NONSTRUCTURAL PROTEINS;

HEPATITIS C VIRUS;

EID: 80054978956     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00173-11     Document Type: Article

References (51)

1. Ait-Goughoulte, M., et al. 2008. Hepatitis C virus genotype 1a growth and induction of autophagy. J. Virol. 82:2241-2249.
2. Aligo, J., S. Jia, D. Manna, and K. V. Konan. 2009. Formation and function of hepatitis C virus replication complexes require residues in the carboxyterminal domain of NS4B protein. Virology 393:68-83.
3. Benali-Furet, N. L., et al. 2005. Hepatitis C virus core triggers apoptosis in liver cells by inducing ER stress and ER calcium depletion. Oncogene 24: 4921-4933.
4. Berkova, Z., et al. 2006. Rotavirus NSP4 induces a novel vesicular compartment regulated by calcium and associated with viroplasms. J. Virol. 80:6061-6071.
5. Chan, S. W., and P. A. Egan. 2005. Hepatitis C virus envelope proteins regulate CHOP via induction of the unfolded protein response. FASEB J. 19:1510-1512.
6. Chen, Y. C., et al. 2010. Polo-like kinase 1 is involved in hepatitis C virus replication by hyperphosphorylating NS5A. J. Virol. 84:7983-7993.
7. Cherra, S. J., III, et al. 2010. Regulation of the autophagy protein LC3 by phosphorylation. J. Cell Biol. 190:533-539.
8. Christoforidis, S., et al. 1999. Phosphatidylinositol-3-OH kinases are Rab5 effectors. Nat. Cell Biol. 1:249-252.
9. Deretic, V. 2008. Autophagosome and phagosome. Methods Mol. Biol. 445: 1-10.
10. Dreux, M., P. Gastaminza, S. F. Wieland, and F. V. Chisari. 2009. The autophagy machinery is required to initiate hepatitis C virus replication. Proc. Natl. Acad. Sci. U. S. A. 106:14046-14051.
11. Egger, D., et al. 2002. Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J. Virol. 76:5974-5984.
12. Eskelinen, E. L. 2005. Maturation of autophagic vacuoles in mammalian cells. Autophagy 1:1-10.
13. Funderburk, S. F., Q. J. Wang, and Z. Yue. 2010. The Beclin 1-VPS34 complex-at the crossroads of autophagy and beyond. Trends Cell Biol. 20:355-362.
14. Gannage, M., et al. 2009. Matrix protein 2 of influenza A virus blocks autophagosome fusion with lysosomes. Cell Host Microbe 6:367-380.
15. Gong, G., G. Waris, R. Tanveer, and A. Siddiqui. 2001. Human hepatitis C virus NS5A protein alters intracellular calcium levels, induces oxidative stress, and activates STAT-3 and NF-kappa B. Proc. Natl. Acad. Sci. U. S. A. 98:9599-9604.
16. Gosert, R., et al. 2003. Identification of the hepatitis C virus RNA replication complex in Huh-7 cells harboring subgenomic replicons. J. Virol. 77:5487-5492.
17. Gouttenoire, J., et al. 2009. Identification of a novel determinant for membrane association in hepatitis C virus nonstructural protein 4B. J. Virol. 83:6257-6268.
18. Gouttenoire, J., R. Montserret, A. Kennel, F. Penin, and D. Moradpour. 2009. An amphipathic alpha-helix at the C terminus of hepatitis C virus nonstructural protein 4B mediates membrane association. J. Virol. 83: 11378-11384.
19. Grosshans, B. L., D. Ortiz, and P. Novick. 2006. Rabs and their effectors: achieving specificity in membrane traffic. Proc. Natl. Acad. Sci. U. S. A. 103:11821-11827.
20. Howard, C. R. 2002. Hepatitis C virus: clades and properties. J. Gastroenterol. Hepatol. 17(Suppl.):S468-S470.
21. Hoyer-Hansen, M., et al. 2007. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol. Cell 25:193-205.
22. Jackson, W. T., et al. 2005. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 3:e156.
23. Jager, S., et al. 2004. Role for Rab7 in maturation of late autophagic vacuoles. J. Cell Sci. 117:4837-4848.
24. Jung, C. H., S. H. Ro, J. Cao, N. M. Otto, and D. H. Kim. 2010. mTOR regulation of autophagy. FEBS Lett. 584:1287-1295.
25. Kabeya, Y., et al. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19:5720-5728.
26. Ke, P. Y., and S. S. Chen. 2011. Activation of the unfolded protein response and autophagy after hepatitis C virus infection suppresses innate antiviral immunity in vitro. J. Clin. Invest. 121:37-56.
27. Komatsu, M., et al. 2005. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169:425-434.
28. Kudchodkar, S. B., and B. Levine. 2009. Viruses and autophagy. Rev. Med. Virol. 19:359-378.
29. Lai, C. K., K. S. Jeng, K. Machida, and M. M. Lai. 2010. Hepatitis C virus egress and release depend on endosomal trafficking of core protein. J. Virol. 84:11590-11598.
30. Lee, H. K., and A. Iwasaki. 2008. Autophagy and antiviral immunity. Curr. Opin. Immunol. 20:23-29.
31. Levine, B., and D. J. Klionsky. 2004. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 6:463-477.
32. Li, L., et al. 2010. Regulation of mTORC1 by the Rab and Arf GTPases. J. Biol. Chem. 285:19705-19709.
33. Li, S., et al. 2009. Hepatitis C virus NS4B induces unfolded protein response and endoplasmic reticulum overload response-dependent NF-kappaB activation. Virology 391:257-264.
34. Lin, L. T., P. W. Dawson, and C. D. Richardson. 2010. Viral interactions with macroautophagy: a double-edged sword. Virology 402:1-10.
35. Lohmann, V., J. O. Koch, and R. Bartenschlager. 1996. Processing pathways of the hepatitis C virus proteins. J. Hepatol. 24:11-19.
36. Manna, D., et al. 2010. Endocytic Rab proteins are required for hepatitis C virus replication complex formation. Virology 398:21-37.
37. Meijer, A. J., and P. Codogno. 2006. Signalling and autophagy regulation in health, aging and disease. Mol. Aspects Med. 27:411-425.
38. Mizushima, N., and T. Yoshimori. 2007. How to interpret LC3 immunoblotting. Autophagy 3:542-545.
39. Moradpour, D., F. Penin, and C. M. Rice. 2007. Replication of hepatitis C virus. Nat. Rev. Microbiol. 5:453-463.
40. Pattingre, S., L. Espert, M. Biard-Piechaczyk, and P. Codogno. 2008. Regulation of macroautophagy by mTOR and Beclin 1 complexes. Biochimie 90:313-323.
41. Ravikumar, B., S. Imarisio, S. Sarkar, C. J. O'Kane, and D. C. Rubinsztein. 2008. Rab5 modulates aggregation and toxicity of mutant huntingtin through macroautophagy in cell and fly models of Huntington disease. J. Cell Sci. 121:1649-1660.
42. Simonsen, A., and S. A. Tooze. 2009. Coordination of membrane events during autophagy by multiple class III PI3-kinase complexes. J. Cell Biol. 186:773-782.
43. Sir, D., et al. 2008. Induction of incomplete autophagic response by hepatitis C virus via the unfolded protein response. Hepatology 48:1054-1061.
44. Sir, D., et al. 2010. The early autophagic pathway is activated by hepatitis B virus and required for viral DNA replication. Proc. Natl. Acad. Sci. U. S. A. 107:4383-4388.
45. Stenmark, H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10:513-525.
46. Stone, M., S. Jia, W. D. Heo, T. Meyer, and K. V. Konan. 2007. Participation of Rab5, an early endosome protein, in hepatitis C virus RNA replication machinery. J. Virol. 81:4551-4563.
47. Tanida, I., et al. 2009. Knockdown of autophagy-related gene decreases the production of infectious hepatitis C virus particles. Autophagy 5:937-945.
48. Villano, S. A., D. Vlahov, K. E. Nelson, S. Cohn, and D. L. Thomas. 1999. Persistence of viremia and the importance of long-term follow-up after acute hepatitis C infection. Hepatology 29:908-914.
49. Vitale, G., et al. 1995. The GDP/GTP cycle of Rab5 in the regulation of endocytotic membrane traffic. Cold Spring Harb. Symp. Quant. Biol. 60:211-220.
50. Zheng, Y., et al. 2005. Hepatitis C virus non-structural protein NS4B can modulate an unfolded protein response. J. Microbiol. 43:529-536.
51. Zhong, J., et al. 2005. Robust hepatitis C virus infection in vitro. Proc. Natl. Acad. Sci. U. S. A. 102:9294-9299.