Endoplasmic reticulum stress is induced and modulated by enterovirus 71

Cellular Microbiology

Volumn 12, Issue 6, 2010, Pages 796-813

  Jheng, Jia Rong ^a   Lau, Kean Seng ^a   Tang, Wen Fang ^a   Wu, Ming Sian ^a   Horng, Jim Tong ^a  

^a CHANG GUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; CALRETICULIN; EDEM PROTEIN; GLUCOSE REGULATED PROTEIN 78; INITIATION FACTOR 2ALPHA; MEMBRANE PROTEIN; MESSENGER RNA; PHOSPHOTRANSFERASE; PKR LIKE ENDOPLASMIC RETICULUM KINASE; PROTEIN IRE1; PROTEIN KINASE R; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; ATF6 PROTEIN, HUMAN; DNA BINDING PROTEIN; HEAT SHOCK PROTEIN; INITIATION FACTOR 2; MOLECULAR CHAPERONE GRP78; REGULATORY FACTOR X TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

ARTICLE; CANCER CELL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENTEROVIRUS 71; ENTEROVIRUS INFECTION; EPIGENETICS; GENE OVEREXPRESSION; GENE SILENCING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RHABDOMYOSARCOMA; RNA SPLICING; ULTRAVIOLET RADIATION; UPREGULATION; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS REPLICATION; BIOSYNTHESIS; DOWN REGULATION; ENDOPLASMIC RETICULUM; ENTEROVIRUS; GENE EXPRESSION PROFILING; HOST PATHOGEN INTERACTION; HUMAN; METABOLISM; PATHOGENICITY; PHOSPHORYLATION; TUMOR CELL LINE; VIROLOGY;

HUMAN ENTEROVIRUS 71; PICORNAVIRIDAE;

ACTIVATING TRANSCRIPTION FACTOR 6; CALRETICULIN; CELL LINE, TUMOR; DNA-BINDING PROTEINS; DOWN-REGULATION; ENDOPLASMIC RETICULUM; ENTEROVIRUS A, HUMAN; EUKARYOTIC INITIATION FACTOR-2; GENE EXPRESSION PROFILING; HEAT-SHOCK PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; PHOSPHORYLATION; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 77954144139     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01434.x     Document Type: Article

References (72)

1. AbuBakar, S., Chee, H.Y., Al-Kobaisi, M.F., Xiaoshan, J., Chua, K.B., and Lam, S.K. (1999) Identification of enterovirus 71 isolates from an outbreak of hand, foot and mouth disease (HFMD) with fatal cases of encephalomyelitis in Malaysia. Virus Res 61: 1-9.
2. Baltzis, D., Qu, L.K., Papadopoulou, S., Blais, J.D., Bell, J.C., Sonenberg, N., and Koromilas, A.E. (2004) Resistance to vesicular stomatitis virus infection requires a functional cross talk between the eukaryotic translation initiation factor 2alpha kinases PERK and PKR. J Virol 78: 12747-12761.
3. Beck, M.A., Chapman, N.M., McManus, B.M., Mullican, J.C., and Tracy, S. (1990) Secondary enterovirus infection in the murine model of myocarditis. Pathologic and immunologic aspects. Am J Pathol 136: 669-681.
4. Benali-Furet, N.L., Chami, M., Houel, L., De Giorgi, F., Vernejoul, F., Lagorce, D., et al. (2005) Hepatitis C virus core triggers apoptosis in liver cells by inducing ER stress and ER calcium depletion. Oncogene 24: 4921-4933.
5. Bertolotti, A., Zhang, Y., Hendershot, L.M., Harding, H.P., and Ron, D. (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2: 326-332.
6. Bienz, K., Egger, D., and Pasamontes, L. (1987) Association of polioviral proteins of the P2 genomic region with the viral replication complex and virus-induced membrane synthesis as visualized by electron microscopic immunocytochemistry and autoradiography. Virology 160: 220-226.
7. Black, T.L., Safer, B., Hovanessian, A., and Katze, M.G. (1989) The cellular 68 000-Mr protein kinase is highly autophosphorylated and activated yet significantly degraded during poliovirus infection: implications for translational regulation. J Virol 63: 2244-2251.
8. Black, T.L., Barber, G.N., and Katze, M.G. (1993) Degradation of the interferon-induced 68 000-M(r) protein kinase by poliovirus requires RNA. J Virol 67: 791-800.
9. Bolten, R., Egger, D., Gosert, R., Schaub, G., Landmann, L., and Bienz, K. (1998) Intracellular localization of poliovirus plus- and minus-strand RNA visualized by strand-specific fluorescent in situ hybridization. J Virol 72: 8578-8585.
10. Brown, B.A., Oberste, M.S., Alexander, J.P., Jr, Kennett, M.L., and Pallansch, M.A. (1999) Molecular epidemiology and evolution of enterovirus 71 strains isolated from 1970 to 1998. J Virol 73: 9969-9975.
11. Buchkovich, N.J., Maguire, T.G., Paton, A.W., Paton, J.C., and Alwine, J.C. (2009) The endoplasmic reticulum chaperone BiP/GRP78 is important in the structure and function of the HCMV assembly compartment. J Virol 83: 11421-11428.
12. Campanella, M., de Jong, A.S., Lanke, K.W., Melchers, W.J., Willems, P.H., Pinton, P., et al. (2004) The coxsackievirus 2B protein suppresses apoptotic host cell responses by manipulating intracellular Ca2+ homeostasis. J Biol Chem 279: 18440-18450.
13. Chan, S.W., and Egan, P.A. (2005) Hepatitis C virus envelope proteins regulate CHOP via induction of the unfolded protein response. FASEB J 19: 1510-1512.
14. Chao, C.C., Yam, W.C., Chen, L.K., and Lin-Chao, S. (1992) Cloning of a functional Burkitt's lymphoma polypeptidebinding protein/78 kDa glucose-regulated protein (BiP/GRP78) gene promoter by the polymerase chain reaction, and its interaction with inducible cellular factors. Biochem J 286 (Part 2): 555-559.
15. Chen, X., Shen, J., and Prywes, R. (2002) The luminal domain of ATF6 senses endoplasmic reticulum (ER) stress and causes translocation of ATF6 from the ER to the Golgi. J Biol Chem 277: 13045-13052.
16. Cheng, G., Feng, Z., and He, B. (2005) Herpes simplex virus 1 infection activates the endoplasmic reticulum resident kinase PERK and mediates eIF-2alpha dephosphorylation by the gamma(1)34.5 protein. J Virol 79: 1379-1388.
17. Ciccaglione, A.R., Costantino, A., Tritarelli, E., Marcantonio, C., Equestre, M., Marziliano, N., and Rapicetta, M. (2005) Activation of endoplasmic reticulum stress response by hepatitis C virus proteins. Arch Virol 150: 1339-1356.
18. Dignam, J.D., Lebovitz, R.M., and Roeder, R.G. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 11: 1475-1489.
19. Ding, W., Albrecht, B., Luo, R., Zhang, W., Stanley, J.R., Newbound, G.C., and Lairmore, M.D. (2001) Endoplasmic reticulum and cis-Golgi localization of human T-lymphotropic virus type 1 p12(I): association with calreticulin and calnexin. J Virol 75: 7672-7682.
20. Doedens, J.R., and Kirkegaard, K. (1995) Inhibition of cellular protein secretion by poliovirus proteins 2B and 3A. EMBO J 14: 894-907.
21. Dorner, A.J., Wasley, L.C., and Kaufman, R.J. (1992) Overexpression of GRP78 mitigates stress induction of glucose regulated proteins and blocks secretion of selective proteins in Chinese hamster ovary cells. EMBO J 11: 1563-1571.
22. Durose, J.B., Tam, A.B., and Niwa, M. (2006) Intrinsic capacities of molecular sensors of the unfolded protein response to sense alternate forms of endoplasmic reticulum stress. Mol Biol Cell 17: 3095-3107.
23. Egger, D., Teterina, N., Ehrenfeld, E., and Bienz, K. (2000) Formation of the poliovirus replication complex requires coupled viral translation, vesicle production, and viral RNA synthesis. J Virol 74: 6570-6580.
24. Gao, B., Adhikari, R., Howarth, M., Nakamura, K., Gold, M.C., Hill, A.B., et al. (2002) Assembly and antigenpresenting function of MHC class I molecules in cells lacking the ER chaperone calreticulin. Immunity 16: 99-109.
25. Goodman, A.G., Smith, J.A., Balachandran, S., Perwitasari, O., Proll, S.C., Thomas, M.J., et al. (2007) The cellular protein P58IPK regulates influenza virus mRNA translation and replication through a PKR-mediated mechanism. J Virol 81: 2221-2230.
26. Harding, H.P., Zhang, Y., Bertolotti, A., Zeng, H., and Ron, D. (2000) Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 5: 897-904.
27. Haze, K., Yoshida, H., Yanagi, H., Yura, T., and Mori, K. (1999) Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 10: 3787-3799.
28. Hirota, M., Kitagaki, M., Itagaki, H., and Aiba, S. (2006) Quantitative measurement of spliced XBP1 mRNA as an indicator of endoplasmic reticulum stress. J Toxicol Sci 31: 149-156.
29. Isler, J.A., Skalet, A.H., and Alwine, J.C. (2005) Human cytomegalovirus infection activates and regulates the unfolded protein response. J Virol 79: 6890-6899.
30. Iwawaki, T., Akai, R., Kohno, K., and Miura, M. (2004) A transgenic mouse model for monitoring endoplasmic reticulum stress. Nat Med 10: 98-102.
31. Jindadamrongwech, S., Thepparit, C., and Smith, D.R. (2004) Identification of GRP 78 (BiP) as a liver cell expressed receptor element for dengue virus serotype 2. Arch Virol 149: 915-927.
32. de Jong, A.S., Visch, H.J., de Mattia, F., van Dommelen, M.M., Swarts, H.G., Luyten, T., et al. (2006) The coxsackievirus 2B protein increases efflux of ions from the endoplasmic reticulum and Golgi, thereby inhibiting protein trafficking through the Golgi. J Biol Chem 281: 14144-14150.
33. Kaufmann, Y., Goldstein, E., and Penman, S. (1976) Poliovirus-induced inhibition of polypeptide initiation in vitro on native polyribosomes. Proc Natl Acad Sci USA 73: 1834-1838.
34. Kepp, O., Senovilla, L., Galluzzi, L., Panaretakis, T., Tesniere, A., Schlemmer, F., et al. (2009) Viral subversion of immunogenic cell death. Cell Cycle 8: 860-869.
35. Kohno, K., Normington, K., Sambrook, J., Gething, M.J., and Mori, K. (1993) The promoter region of the yeast KAR2 (BiP) gene contains a regulatory domain that responds to the presence of unfolded proteins in the endoplasmic reticulum. Mol Cell Biol 13: 877-890.
36. Lee, A.H., Iwakoshi, N.N., and Glimcher, L.H. (2003) XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol 23: 7448-7459.
37. Lee, E.S., Yoon, C.H., Kim, Y.S., and Bae, Y.S. (2007) The double-strand RNA-dependent protein kinase PKR plays a significant role in a sustained ER stress-induced apoptosis. FEBS Lett 581: 4325-4332.
38. Leibowitz, R., and Penman, S. (1971) Regulation of protein synthesis in HeLa cells. 3. Inhibition during poliovirus infection. J Virol 8: 661-668.
39. Liberman, E., Fong, Y.L., Selby, M.J., Choo, Q.L., Cousens, L., Houghton, M., and Yen, T.S. (1999) Activation of the grp78 and grp94 promoters by hepatitis C virus E2 envelope protein. J Virol 73: 3718-3722.
40. Limjindaporn, T.,Wongwiwat,W., Noisakran, S., Srisawat, C., Netsawang, J., Puttikhunt, C., et al. (2009) Interaction of dengue virus envelope protein with endoplasmic reticulumresident chaperones facilitates dengue virus production. Biochem Biophys Res Commun 379: 196-200.
41. Lin, J.Y., Shih, S.R., Pan, M., Li, C., Lue, C.F., Stollar, V., and Li, M.L. (2009) hnRNP A1 interacts with the 5( untranslated regions of enterovirus 71 and Sindbis virus RNA and is required for viral replication. J Virol 83: 6106-6114.
42. Medigeshi, G.R., Lancaster, A.M., Hirsch, A.J., Briese, T., Lipkin, W.I., Defilippis, V., et al. (2007) West Nile virus infection activates the unfolded protein response, leading to CHOP induction and apoptosis. J Virol 81: 10849-10860.
43. Onuki, R., Bando, Y., Suyama, E., Katayama, T., Kawasaki, H., Baba, T., et al. (2004) An RNA-dependent protein kinase is involved in tunicamycin-induced apoptosis and Alzheimer's disease. EMBO J 23: 959-968.
44. Pieren, M., Galli, C., Denzel, A., and Molinari, M. (2005) The use of calnexin and calreticulin by cellular and viral glycoproteins. J Biol Chem 280: 28265-28271.
45. Prostko, C.R., Dholakia, J.N., Brostrom, M.A., and Brostrom, C.O. (1995) Activation of the double-stranded RNAregulated protein kinase by depletion of endoplasmic reticular calcium stores. J Biol Chem 270: 6211-6215.
46. Ransone, L.J., and Dasgupta, A. (1987) Activation of doublestranded RNA-activated protein kinase in HeLa cells after poliovirus infection does not result in increased phosphorylation of eucaryotic initiation factor-2. J Virol 61: 1781-1787.
47. Rose, J.K., Trachsel, H., Leong, K., and Baltimore, D. (1978) Inhibition of translation by poliovirus: inactivation of a specific initiation factor. Proc Natl Acad Sci USA 75: 2732-2736.
48. Rust, R.C., Landmann, L., Gosert, R., Tang, B.L., Hong, W., Hauri, H.P., et al. (2001) Cellular COPII proteins are involved in production of the vesicles that form the poliovirus replication complex. J Virol 75: 9808-9818.
49. Schlegel, A., Giddings, T.H., Jr, Ladinsky, M.S., and Kirkegaard, K. (1996) Cellular origin and ultrastructure of membranes induced during poliovirus infection. J Virol 70: 6576-6588.
50. Shen, J., and Prywes, R. (2005) ER stress signaling by regulated proteolysis of ATF6. Methods 35: 382-389.
51. Shen, J., Chen, X., Hendershot, L., and Prywes, R. (2002) ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 3: 99-111.
52. Srivastava, S.P., Davies, M.V., and Kaufman, R.J. (1995) Calcium depletion from the endoplasmic reticulum activates the double-stranded RNA-dependent protein kinase (PKR) to inhibit protein synthesis. J Biol Chem 270: 16619-16624.
53. Su, H.L., Liao, C.L., and Lin, Y.L. (2002) Japanese encephalitis virus infection initiates endoplasmic reticulum stress and an unfolded protein response. J Virol 76: 4162-4171.
54. Tang, W.F., Yang, S.Y., Wu, B.W., Jheng, J.R., Chen, Y.L., Shih, C.H., et al. (2007) Reticulon 3 binds the 2C protein of enterovirus 71 and is required for viral replication. J Biol Chem 282: 5888-5898.
55. Tardif, K.D., Mori, K., and Siddiqui, A. (2002) Hepatitis C virus subgenomic replicons induce endoplasmic reticulum stress activating an intracellular signaling pathway. J Virol 76: 7453-7459.
56. Tardif, K.D., Mori, K., Kaufman, R.J., and Siddiqui, A. (2004) Hepatitis C virus suppresses the IRE1-XBP1 pathway of the unfolded protein response. J Biol Chem 279: 17158-17164.
57. Tardif, K.D., Waris, G., and Siddiqui, A. (2005) Hepatitis C virus, ER stress, and oxidative stress. Trends Microbiol 13: 159-163.
58. Triantafilou, K., Fradelizi, D., Wilson, K., and Triantafilou, M. (2002) GRP78, a coreceptor for coxsackievirus A9, interacts with major histocompatibility complex class I molecules which mediate virus internalization. J Virol 76: 633-643.
59. Wang, X.Z., Lawson, B., Brewer, J.W., Zinszner, H., Sanjay, A., Mi, L.J., et al. (1996) Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol Cell Biol 16: 4273-4280.
60. Wong, W.R., Chen, Y.Y., Yang, S.M., Chen, Y.L., and Horng, J.T. (2005) Phosphorylation of PI3K/Akt and MAPK/ERK in an early entry step of enterovirus 71. Life Sci 78: 82-90.
61. Wooden, S.K., Li, L.J., Navarro, D., Qadri, I., Pereira, L., and Lee, A.S. (1991) Transactivation of the grp78 promoter by malfolded proteins, glycosylation block, and calcium ionophore is mediated through a proximal region containing a CCAAT motif which interacts with CTF/NF-I. Mol Cell Biol 11: 5612-5623.
62. Wu, B.W., Pan, T.L., Leu, Y.L., Chang, Y.K., Tai, P.J., Lin, K.H., and Horng, J.T. (2007) Antiviral effects of Salvia miltiorrhiza (Danshen) against enterovirus 71. Am J Chin Med 35: 153-168.
63. Xu, Z., Jensen, G., and Yen, T.S. (1997) Activation of hepatitis B virus S promoter by the viral large surface protein via induction of stress in the endoplasmic reticulum. J Virol 71: 7387-7392.
64. Yamamoto, K., Yoshida, H., Kokame, K., Kaufman, R.J., and Mori, K. (2004) Differential contributions of ATF6 and XBP1 to the activation of endoplasmic reticulum stressresponsive cis-acting elements ERSE, UPRE and ERSE-II. J Biochem (Tokyo) 136: 343-350.
65. Ye, J., Rawson, R.B., Komuro, R., Chen, X., Dave, U.P., Prywes, R., et al. (2000) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6: 1355-1364.
66. Yoshida, H., Haze, K., Yanagi, H., Yura, T., and Mori, K. (1998) Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. Involvement of basic leucine zipper transcription factors. J Biol Chem 273: 33741-33749.
67. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T., and Mori, K. (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107: 881-891.
68. Yoshida, H., Matsui, T., Hosokawa, N., Kaufman, R.J., Nagata, K., and Mori, K. (2003) A time-dependent phase shift in the mammalian unfolded protein response. Dev Cell 4: 265-271.
69. Yoshida, H., Oku, M., Suzuki, M., and Mori, K. (2006) pXBP1(U) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(S) in mammalian ER stress response. J Cell Biol 172: 565-575.
70. Yu, C.Y., Hsu, Y.W., Liao, C.L., and Lin, Y.L. (2006) Flavivirus infection activates the XBP1 pathway of the unfolded protein response to cope with endoplasmic reticulum stress. J Virol 80: 11868-11880.
71. Zhu, C., Johansen, F.E., and Prywes, R. (1997) Interaction of ATF6 and serum response factor. Mol Cell Biol 17: 4957-4966.
72. Zhu, J., and Newkirk, M.M. (1994) Viral induction of the human autoantigen calreticulin. Clin Invest Med 17: 196-205.