Autophagosome supports coxsackievirus B3 replication in host cells

Journal of Virology

Volumn 82, Issue 18, 2008, Pages 9143-9153

  Wong, Jerry ^a   Zhang, Jingchun ^a   Si, Xiaoning ^a   Gao, Guang ^a   Mao, Ivy ^a   McManus, Bruce M ^a   Luo, Honglin ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLADENINE; AMMONIUM CHLORIDE; BAFILOMYCIN A1; BECLIN 1; BETA ACTIN; INITIATION FACTOR 2ALPHA; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; RAPAMYCIN; SMALL INTERFERING RNA;

ARTICLE; AUTOPHAGY; CELL STRAIN HEK293; CONFOCAL MICROSCOPY; CONTROLLED STUDY; COXSACKIE VIRUS B; GENE SILENCING; HELA CELL; HUMAN; HUMAN CELL; NUTRIENT LIMITATION; PHAGOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; TRANSMISSION ELECTRON MICROSCOPY; VIROGENESIS; VIRUS MYOCARDITIS; VIRUS REPLICATION; VIRUS TITRATION; WESTERN BLOTTING;

ADENINE; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CELL LINE; ENTEROVIRUS B, HUMAN; HELA CELLS; HUMANS; LYSOSOMES; MEMBRANE PROTEINS; PHAGOSOMES; RNA, SMALL INTERFERING; UBIQUITIN-ACTIVATING ENZYMES; VIRUS REPLICATION;

COXSACKIEVIRUS; PICORNAVIRIDAE; RNA VIRUSES;

EID: 50949133741     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00641-08     Document Type: Article

References (41)

1. Alexander, D. E., S. L. Ward, N. Mizushima, B. Levine, and D. A. Leib. 2007. Analysis of the role of autophagy in replication of herpes simplex virus in cell culture. J. Virol. 81:12128-12134.
2. Andrade, R. M., M. Wessendarp, M. J. Gubbels, B. Striepen, and C. S. Subauste. 2006. CD40 induces macrophage anti-Toxoplasma gondii activity by triggering autophagy-dependent fusion of pathogen-containing vacuoles and lysosomes. J. Clin. Invcstig. 116:2366-2377.
3. Blommaart, E. F., U. Krause, J. P. Schellens, H. Vreeling-Sindelarova, and A. J. Meijer. 1997. The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur. J. Biochem. 243:240-246.
4. Brabec-Zaruba, M., U. Berka, D. Blaas, and R. Fuchs. 2007. Induction of autophagy does not affect human rhinovirus type 2 production. J. Virol. 81:10815-10817.
5. Codogno, P., and A. J. Meijer. 2005. Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ. 12(Suppl. 2):1509-1518.
6. Esfandiarei, M., H. Luo, B. Yanagawa, A. Suarez, D. Dabiri, J. Zhang, and B. M. McManus. 2004. Protein kinase B/Akt regulates coxsackievirus B3 replication through a mechanism which is not caspase dependent. J. Virol. 78:4289-4298.
7. Espert, L., P. Codogno, and M. Biard-Piechaczyk. 2007. Involvement of autophagy in viral infections: antiviral function and subversion by viruses. J. Mol. Med. 85:811-823.
8. Gonzalez-Polo, R. A., P. Boya, A. L. Pauleau, A. Jalil, N. Larochette, S. Souquere, E. L. Eskelinen, G. Pierron, P. Saftig, and G. Kroemer. 2005. The apoptosis/autophagy paradox: autophagic vacuolization before apoptotic death. J. Cell Sci. 118:3091-3102.
9. Gutierrez, M. G., S. S. Master, S. B. Singh, G. A. Taylor, M. I. Colombo, and V. Deretic. 2004. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119:753-766.
10. Hoyer-Hansen, M., L. Bastholm, P. Szyniarowski, M. Campanella, G. Szabadkai, T. Farkas, K. Bianchi, N. Fehrenbacher, F. Elling, R. Rizzuto, I. S. Mathiasen, and M. Jaattela. 2007. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol. Cell 25:193-205.
11. Jackson, W. T., T. H. Giddings, Jr., M. P. Taylor, S. Mulinyawe, M. Rabinovitch, R. R. Kopito, and K. Kirkegaard. 2005. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 3:e156.
12. Kabeya, Y., N. Mizushima, T. Ueno, A. Yamamoto, T. Kirisako, T. Noda, E. Kominami, Y. Ohsumi, and T. Yoshimori. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19:5720-5728.
13. Kihara, A., Y. Kabeya, Y. Ohsumi, and T. Yoshimori. 2001. Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep. 2:330-335.
14. Kim, K. S., G. Hufnagel, N. M. Chapman, and S. Tracy. 2001. The group B coxsackieviruses and myocarditis. Rev. Med. Virol. 11:355-368.
15. Kirkegaard, K., M. P. Taylor, and W. T. Jackson. 2004. Cellular autophagy: surrender, avoidance and subversion by microorganisms. Nat. Rev. Microbiol. 2:301-314.
16. Klionsky, D. J. 2007. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 8:931-937.
17. Klionsky, D. J. 2005. The correct way to monitor autophagy in higher eukaryotes. Autophagy 1:65.
18. Klionsky, D. J., H. Abeliovich, P. Agostinis, D. K. Agrawal, G. Aliev, D. S. Askew, M. Baba, E. H. Baehrecke, B. A. Bahr, A. Ballabio, B. A. Bamber, D. C. Bassham, E. Bergamini, X. Bi, M. Biard-Piechaczyk, J. S. Blum, D. E. Bredesen, J. L. Brodsky, J. H. Brumell, U. T. Brunk, W. Bursch, N. Camougrand, E. Cebollero, F. Cecconi, Y. Chen, L. S. Chin, A. Choi, C. T. Chu, J. Chung, P. G. Clarke, R. S. Clark, S. G. Clarke, C. Clave, J. L. Cleveland, P. Codogno, M. I. Colombo, A. Coto-Montes, J. M. Cregg, A. M. Cuervo, J. Debnath, F. Demarchi, P. B. Dennis, P. A. Dennis, V. Deretic, R. J. Devenish, F. Di Sano, J. F. Dice, M. Difiglia, S. Dinesh-Kumar, C. W. Distelhorst, M. Djavaheri-Mergny, F. C. Dorsey, W. Droge, M. Dron, W. A. Dunn, Jr., M. Duszenko, N. T. Eissa, Z. Elazar, A. Esclatine, E. L. Eskelinen, L. Fesus, K. D. Finley, J. M. Fuentes, J. Fueyo, K. Fujisaki, B. Galliot, F. B. Gao, D. A. Gewirtz, S. B. Gibson, A. Gohla, A. L. Goldberg, R. Gonzalez, C. Gonzalez-Estevez, S. Gorski, R. A. Gottlieb, D. Haussinger, Y. W. He, K. Heidenreich, J. A. Hill, M. Hoyer-Hansen, X. Hu, W. P. Huang, A. Iwasaki, M. Jaattela, W. T. Jackson, X. Jiang, S. Jin, T. Johansen, J. U. Jung, M. Kadowaki, C. Rang, A. Kelekar, D. H. Kessel, J. A. Kiel, H. P. Kim, A. Kimchi, T. J. Kinsella, K. Kiselyov, K. Kitamoto, E. Knecht, et al. 2008. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4:151-175.
19. Klionsky, D. J., and S. D. Emr. 2000. Autophagy as a regulated pathway of cellular degradation. Science 290:1717-1721.
20. Komatsu, M., S. Waguri, T. Ueno, J. Iwata, S. Murata, I. Tanida, J. Ezaki, N. Mizushima, Y. Ohsumi, Y. Uchiyama, E. Kominami, K. Tanaka, and T. Chiba. 2005. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169:425-434.
21. Kouroku, Y., E. Fujita, I. Tanida, T. Ueno, A. Isoai, H. Kumagai, S. Ogawa, R. J. Kaufman, E. Kominami, and T. Momoi. 2007. ER stress (PERK/ eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ. 14: 230-239.
22. Levine, B. 2003. Autophagy in development, tumor suppression, and innate immunity. Harvey Lect. 99:47-76.
23. Levine, B., and G. Kroemer. 2008. Autophagy in the pathogenesis of disease. Cell 132:27-42.
24. Mizushima, N. 2004. Methods for monitoring autophagy. Int. J. Biochem. Cell. Biol. 36:2491-2502.
25. Mizushima, N., Y. Ohsumi, and T. Yoshimori. 2002. Autophagosome formation in mammalian cells. Cell Struct. Funct. 27:421-429.
26. Mohr, I. 2004. Neutralizing innate host defenses to control viral translation in HSV-1 infected cells. Int. Rev. Immunol. 23:199-220.
27. Ogawa, M., T. Yoshimori, T. Suzuki, H. Sagara, N. Mizushima, and C. Sasakawa. 2005. Escape of intracellular Shigella from autophagy. Science 307:727-731.
28. Ohsumi, Y. 2001. Molecular dissection of autophagy: two ubiquitin-like systems. Nat. Rev. Mol. Cell Biol. 2:211-216.
29. Petiot, A., E. Ogier-Denis, E. F. Blommaart, A. J. Meijer, and P. Codogno. 2000. Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 275:992-998.
30. Pilipenko, E. V., S. V. Maslova, A. N. Sinyakov, and V. I. Agol. 1992. Towards identification of cis-acting elements involved in the replication of enterovirus and rhinovirus RNAs: a proposal for the existence of tRNA-like terminal structures. Nucleic Acids Res. 20:1739-1745.
31. Prentice, E., W. G. Jerome, T. Yoshimori, N. Mizushima, and M. R. Denison. 2004. Coronavirus replication complex formation utilizes components of cellular autophagy. J. Biol. Chem. 279:10136-10141.
32. Schmid, D., and C. Munz. 2007. Innate and adaptive immunity through autophagy. Immunity 27:11-21.
33. Seglen, P. O., and P. B. Gordon. 1982. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. USA 79:1889-1892.
34. Si, X., Y. Wang, J. Wong, J. Zhang, B. M. McManus, and H. Luo. 2007. Dysregulation of the ubiquitin-proteasome system by curcumin suppresses coxsackievirus B3 replication. J. Virol. 81:3142-3150.
35. Suzuki, K., T. Kirisako, Y. Kamada, N. Mizushima, T. Noda, and Y. Ohsumi. 2001. The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. EMBO J. 20:5971-5981.
36. Talloczy, Z., W. Jiang, H. W. T. Virgin, D. A. Leib, D. Scheuner, R. J. Kaufman, E. L. Eskelinen, and B. Levine. 2002. Regulation of starvation-and virus-induced autophagy by the eIF2alpha kinase signaling pathway. Proc. Natl. Acad. Sci. USA 99:190-195.
37. Tanaka, Y., G. Guhde, A. Suter, E. L. Eskelinen, D. Hartmann, R. Lullmann-Rauch, P. M. Janssen, J. Blanz, K. von Figura, and P. Saftig. 2000. Accumulation of autophagic vacuoles and cardiomyopathy in LAMP-2-deficient mice. Nature 406:902-906.
38. Wileman, T. 2006. Aggresomes and autophagy generate sites for virus replication. Science 312:875-878.
39. Zeng, X., J. H. Overmeyer, and W. A. Maltese. 2006. Functional specificity of the mammalian Beclin-Vps34 PI 3-kinase complex in macroautophagy versus endocytosis and lysosomal enzyme trafficking. J. Cell Sci. 119:259-270.
40. Zhao, Z., L. B. Thackray, B. C. Miller, T. M. Lynn, M. M. Becker, E. Ward, N. N. Mizushima, M. R. Denison, and H. W. T. Virgin. 2007. Coronavirus replication does not require the autophagy gene ATG5. Autophagy 3:581-585.
41. Zhou, B., N. Boudreau, C. Coulber, J. Hammarback, and M. Rabinovitch. 1997. Microtubule-associated protein 1 light chain 3 is a fibronectin mRNA-binding protein linked to mRNA translation in lamb vascular smooth muscle cells. J. Clin. Investig. 100:3070-3082.