Varicella-zoster virus infection induces autophagy in both cultured cells and human skin vesicles

Journal of Virology

Volumn 83, Issue 11, 2009, Pages 5466-5476

  Takahashi, Marie Noëlle ^a   Jackson, Wallen ^b   Laird, Donna T ^a   Culp, Timothy D ^a   Grose, Charles ^b   Haynes II, John I ^a   Benetti, Luca ^a  

^a MERCK RESEARCH LABORATORIES   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; GENE PRODUCT; PHOSPHONOACETIC ACID; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SQSTM1 PROTEIN, HUMAN; VIRUS ENVELOPE PROTEIN;

ANTIBODY TITER; ARTICLE; AUTOPHAGY; CELL CULTURE; CONTROLLED STUDY; ELECTRON MICROSCOPY; GENE EXPRESSION; GENE INDUCTION; HERPES ZOSTER; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; INNATE IMMUNITY; INOCULATION; LYSOSOME; MEMBRANE VESICLE; NONHUMAN; PHAGOSOME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN TARGETING; SKIN; STAINING; VARICELLA ZOSTER VIRUS; VIRION; VIROGENESIS; VIRUS GENE; VIRUS STRAIN; BIOPSY; CELL FREE SYSTEM; CELL LINE; CHICKENPOX; CYTOPLASM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; SKIN DISEASE; TRANSMISSION ELECTRON MICROSCOPY; VIROLOGY; VIRUS REPLICATION;

HUMAN HERPESVIRUS 3;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AUTOPHAGY; BIOPSY; CELL LINE; CELL-FREE SYSTEM; CHICKENPOX; CYTOPLASM; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRUS 3, HUMAN; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; SKIN DISEASES; VIRAL ENVELOPE PROTEINS; VIRUS REPLICATION;

EID: 66149115264     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02670-08     Document Type: Article

References (49)

1. Ait-Goughoulte, M., T. Kanda, K. Meyer, J. S. Ryerse, R. B. Ray, and R. Ray. 2008. Hepatitis C virus genotype 1a growth and induction of autophagy. J. Virol. 82:2241-2249.
2. 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. (Pubitemid 350085828)
3. Bjorkoy, G., T. Lamark, A. Brech, H. Outzen, M. Perander, A. Overvatn, H. Stenmark, and T. Johansen. 2005. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J. Cell Biol. 171:603-614. (Pubitemid 41668720)
4. Carpenter, J. E., J. A. Hutchinson, W. Jackson, and C. Grose. 2008. Egress of light particles among filopodia on the surface of varicella-zoster virus-infected cells. J. Virol. 82:2821-2835.
5. Chaumorcel, M., S. Souquere, G. Pierron, P. Codogno, and A. Esclatine. 2008. Human cytomegalovirus controls a new autophagy-dependent cellular antiviral defense mechanism. Autophagy 4:46-53.
6. Chen, J. J., Z. Zhu, A. A. Gershon, and M. D. Gershon. 2004. Mannose 6-phosphate receptor dependence of varicella zoster virus infection in vitro and in the epidermis during varicella and zoster. Cell 119:915-926. (Pubitemid 40037606)
7. Cohen, J. E., S. E. Straus, and A. M. Arvin. 2007. Varicella-zoster virus replication, pathogenesis and management, p. 2773-2818. In B. N. Fields, D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology. Lippincott-Raven, Philadelphia, PA.
8. Cuervo, A. M. 2004. Autophagy: in sickness and in health. Trends Cell Biol. 14:70-77. (Pubitemid 38186640)
9. Reference deleted.
10. Reference deleted.
11. Erazo, A., M. B. Yee, N. Osterrieder, and P. R. Kinchington. 2008. Varicellazoster virus open reading frame 66 protein kinase is required for efficient viral growth in primary human corneal stromal fibroblast cells. J. Virol. 82:7653-7665.
12. 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. (Pubitemid 47077109)
13. Gershon, A. A., D. L. Sherman, Z. Zhu, C. A. Gabel, R. T. Ambron, and M. D. Gershon. 1994. Intracellular transport of newly synthesized varicellazoster virus: final envelopment in the trans-Golgi network. J. Virol. 68:6372-6390. (Pubitemid 24294888)
14. Gomi, Y., H. Sunamachi, Y. Mori, K. Nagaike, M. Takahashi, and K. Yamanishi. 2002. Comparison of the complete DNA sequences of the Oka varicella vaccine and its parental virus. J. Virol. 76:11447-11459. (Pubitemid 35231301)
15. Grose, C. 1996. Pathogenesis of infection with varicella vaccine. Infect. Dis. Clin. N. Am. 10:489-505. (Pubitemid 26285284)
16. Grose, C. 2005. Varicella vaccination of children in the United States: assessment after the first decade 1995-2005. J. Clin. Virol. 33:89-98. (Pubitemid 40725300)
17. Harson, R., and C. Grose. 1995. Egress of varicella-zoster virus from the melanoma cell: a tropism for the melanocyte. J. Virol. 69:4994-5010.
18. Hayakawa, Y., S. Torigoe, K. Shiraki, K. Yamanishi, and M. Takahashi. 1984. Biologic and biophysical markers of a live varicella vaccine strain (Oka): identification of clinical isolates from vaccine recipients. J. Infect. Dis. 149:956-963. (Pubitemid 14082160)
19. Hood, C., A. L. Cunningham, B. Slobedman, R. A. Boadle, and A. Abendroth. 2003. Varicella-zoster virus-infected human sensory neurons are resistant to apoptosis, yet human foreskin fibroblasts are susceptible: evidence for a cell-type-specific apoptotic response. J. Virol. 77:12852-12864. (Pubitemid 37430679)
20. Jones, P. C., and B. Roizman. 1979. Regulation of herpesvirus macromolecular synthesis. VIII. The transcription program consists of three phases during which both extent of transcription and accumulation of RNA in the cytoplasm are regulated. J. Virol. 31:299-314.
21. 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.
22. 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. Kang, 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.
23. Klionsky, D. J., J. M. Cregg, W. A. Dunn, Jr., S. D. Emr, Y. Sakai, I. V. Sandoval, A. Sibirny, S. Subramani, M. Thumm, M. Veenhuis, and Y. Ohsumi. 2003. A unified nomenclature for yeast autophagy-related genes. Dev. Cell 5:539-545.
24. Komatsu, M., S. Waguri, M. Koike, Y. S. Sou, T. Ueno, T. Hara, N. Mizushima, J. Iwata, J. Ezaki, S. Murata, J. Hamazaki, Y. Nishito, S. Iemura, T. Natsume, T. Yanagawa, J. Uwayama, E. Warabi, H. Yoshida, T. Ishii, A. Kobayashi, M. Yamamoto, Z. Yue, Y. Uchiyama, E. Kominami, and K. Tanaka. 2007. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131:1149-1163. (Pubitemid 350235021)
25. Reference deleted.
26. Ku, B., J. S. Woo, C. Liang, K. H. Lee, H. S. Hong, X. E., K. S. Kim, J. U. Jung, and B. H. Oh. 2008. Structural and biochemical bases for the inhibition of autophagy and apoptosis by viral BCL-2 of murine gamma-herpesvirus 68. PLoS Pathog. 4:e25.
27. Lee, D. Y., and B. Sugden. 2008. The latent membrane protein 1 oncogene modifies B-cell physiology by regulating autophagy. Oncogene 27:2833-2842.
28. Levine, B. 2005. Eating oneself and uninvited guests: autophagy-related pathways in cellular defense. Cell 120:159-162. (Pubitemid 40174758)
29. Liang, X. H., L. K. Kleeman, H. H. Jiang, G. Gordon, J. E. Goldman, G. Berry, B. Herman, and B. Levine. 1998. Protection against fatal Sindbis virus encephalitis by beclin, a novel Bcl-2-interacting protein. J. Virol. 72:8586-8596. (Pubitemid 28471796)
30. Liu, Y., M. Schiff, K. Czymmek, Z. Talloczy, B. Levine, and S. P. Dinesh-Kumar. 2005. Autophagy regulates programmed cell death during the plant innate immune response. Cell 121:567-577. (Pubitemid 40720010)
31. Reference deleted.
32. May, D. C., M. R. Miller, and F. Rapp. 1977. The effect of phosphonoacetic acid on the in vitro replication of varicella-zoster virus. Intervirology 8:83-91. (Pubitemid 8068971)
33. Mizushima, N., and T. Yoshimori. 2007. How to interpret LC3 immunoblotting. Autophagy 3:542-545. (Pubitemid 350060049)
34. Orvedahl, A., D. Alexander, Z. Talloczy, Q. Sun, Y. Wei, W. Zhang, D. Burns, D. A. Leib, and B. Levine. 2007. HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 1:23-35. (Pubitemid 46506007)
35. Pattingre, S., A. Tassa, X. Qu, R. Garuti, X. H. Liang, N. Mizushima, M. Packer, M. D. Schneider, and B. Levine. 2005. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122:927-939. (Pubitemid 41345209)
36. Peake, M. L., P. Nystrom, and L. I. Pizer. 1982. Herpesvirus glycoprotein synthesis and insertion into plasma membranes. J. Virol. 42:678-690.
37. Peters, G. A., S. D. Tyler, C. Grose, A. Severini, M. J. Gray, C. Upton, and G. A. Tipples. 2006. A full-genome phylogenetic analysis of varicella-zoster virus reveals a novel origin of replication-based genotyping scheme and evidence of recombination between major circulating clades. J. Virol. 80:9850-9860. (Pubitemid 44435659)
38. Rapp, F., and D. Vanderslice. 1964. Spread of zoster virus in human embryonic lung cells and the inhibitory effect of lododeoxyuridine. Virology 22:321-330.
39. Reggiori, F., and D. J. Klionsky. 2002. Autophagy in the eukaryotic cell. Eukaryot. Cell 1:11-21.
40. Shintani, T., and D. J. Klionsky. 2004. Autophagy in health and disease: a double-edged sword. Science 306:990-995. (Pubitemid 39482894)
41. Storlie, J., J. E. Carpenter, W. Jackson, and C. Grose. 2008. Discordant varicella-zoster virus glycoprotein C expression and localization between cultured cells and human skin vesicles. Virology 382:171-181.
42. Storlie, J., W. Jackson, J. Hutchinson, and C. Grose. 2006. Delayed biosynthesis of varicella-zoster virus glycoprotein C: upregulation by hexamethylene bisacetamide and retinoic acid treatment of infected cells. J. Virol. 80:9544-9556. (Pubitemid 44435630)
43. Takahashi, M. 1986. Clinical overview of varicella vaccine: development and early studies. Pediatrics 78:736-741. (Pubitemid 16007076)
44. Takahashi, M. 1984. Development and characterization of a live varicella vaccine (Oka strain). Biken J. 27:31-36. (Pubitemid 15167918)
45. Tanida, I., N. Minematsu-Ikeguchi, T. Ueno, and E. Kominami. 2005. Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 1:84-91.
46. Tanida, I., T. Ueno, and E. Kominami. 2004. LC3 conjugation system in mammalian autophagy. Int. J. Biochem. Cell Biol. 36:2503-2518. (Pubitemid 39119762)
47. Tillieux, S. L., W. S. Halsey, E. S. Thomas, J. J. Voycik, G. M. Sathe, and V. Vassilev. 2008. Complete DNA sequences of two Oka strain varicella-zoster virus genomes. J. Virol. 82:11023-11044.
48. Wang, Z. H., M. D. Gershon, O. Lungu, Z. Zhu, S. Mallory, A. M. Arvin, and A. A. Gershon. 2001. Essential role played by the C-terminal domain of glycoprotein I in envelopment of varicella-zoster virus in the trans-Golgi network: interactions of glycoproteins with tegument. J. Virol. 75:323-340.
49. Weigle, K. A., and C. Grose. 1983. Common expression of varicella-zoster viral glycoprotein antigens in vitro and in chickenpox and zoster vesicles. J. Infect. Dis. 148:630-638.