The immunity-related GTPase Irgm3 relieves endoplasmic reticulum stress response during coxsackievirus B3 infection via a PI3K/Akt dependent pathway

Cellular Microbiology

Volumn 14, Issue 1, 2012, Pages 133-146

  Liu, Zhen ^a   Zhang, Huifang M ^a   Yuan, Ji ^a   Ye, Xin ^a   Taylor, Gregory A ^b,c   Yang, Decheng ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b DURHAM VA MEDICAL CENTER   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ACTIVATING TRANSCRIPTION FACTOR 6; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; GUANOSINE TRIPHOSPHATASE; INITIATION FACTOR 2ALPHA; IRGM3 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; STRESS ACTIVATED PROTEIN KINASE; TUNICAMYCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; COXSACKIE VIRUS INFECTION; COXSACKIEVIRUS B3 INFECTION; ENDOPLASMIC RETICULUM STRESS; FIBROBLAST; GENE EXPRESSION; GENETIC TRANSFECTION; HELA CELL; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION;

ACTIVATING TRANSCRIPTION FACTOR 6; APOPTOSIS; CHROMONES; EIF-2 KINASE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENTEROVIRUS B, HUMAN; ENTEROVIRUS INFECTIONS; EUKARYOTIC INITIATION FACTOR-2; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GTP-BINDING PROTEINS; HELA CELLS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE SIGNALING SYSTEM; MORPHOLINES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN PHOSPHATASE 1; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTOR CHOP;

COXSACKIEVIRUS;

EID: 83655167092     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2011.01708.x     Document Type: Article

References (55)

1. Alwine, J.C. (2008) Modulation of host cell stress responses by human cytomegalovirus. Curr Top Microbiol Immunol 325: 263-279.
2. Averous, J., Bruhat, A., Jousse, C., Carraro, V., Thiel, G., and Fafournoux, P. (2004) Induction of CHOP expression by amino acid limitation requires both ATF4 expression and ATF2 phosphorylation. J Biol Chem 279: 5288-5297.
3. 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.
4. Bekpen, C., Hunn, J.P., Rohde, C., Parvanova, I., Guethlein, L., Dunn, D.M., etal. (2005) The interferon-inducible p47 (IRG) GTPases in vertebrates: loss of the cell autonomous resistance mechanism in the human lineage. Genome Biol 6: R92.
5. Bienz, K., Egger, D., Troxler, M., and Pasamontes, L. (1990) Structural organization of poliovirus RNA replication is mediated by viral proteins of the P2 genomic region. J Virol 64: 1156-1163.
6. Boyce, M., and Yuan, J. (2006) Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ 13: 363-373.
7. Braakman, I., and van Anken, E. (2000) Folding of viral envelope glycoproteins in the endoplasmic reticulum. Traffic 1: 533-539.
8. 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.
9. Doedens, J.R., Giddings, T.H., Jr, and Kirkegaard, K. (1997) Inhibition of endoplasmic reticulum-to-Golgi traffic by poliovirus protein 3A: genetic and ultrastructural analysis. J Virol 71: 9054-9064.
10. Du, K., Herzig, S., Kulkarni, R.N., and Montminy, M. (2003) TRB3: a tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Science 300: 1574-1577.
11. Duriez, P.J., and Shah, G.M. (1997) Cleavage of poly(ADP-ribose) polymerase: a sensitive parameter to study cell death. Biochem Cell Biol 75: 337-349.
12. Egger, D., and Bienz, K. (2005) Intracellular location and translocation of silent and active poliovirus replication complexes. J Gen Virol 86: 707-718.
13. Halonen, S.K., Taylor, G.A., and Weiss, L.M. (2001) Gamma interferon-induced inhibition of Toxoplasma gondii in astrocytes is mediated by IGTP. Infect Immun 69: 5573-5576.
14. Harding, H.P., Zhang, Y., and Ron, D. (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274.
15. He, B. (2006) Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ 13: 393-403.
16. Hu, P., Han, Z., Couvillon, A.D., and Exton, J.H. (2004) Critical role of endogenous Akt/IAPs and MEK1/ERK pathways in counteracting endoplasmic reticulum stress-induced cell death. J Biol Chem 279: 49420-49429.
17. Huang, Z.M., Tan, T., Yoshida, H., Mori, K., Ma, Y., and Yen, T.S. (2005) Activation of hepatitis B virus S promoter by a cell type-restricted IRE1-dependent pathway induced by endoplasmic reticulum stress. Mol Cell Biol 25: 7522-7533.
18. Jordan, R., Wang, L., Graczyk, T.M., Block, T.M., and Romano, P.R. (2002) Replication of a cytopathic strain of bovine viral diarrhea virus activates PERK and induces endoplasmic reticulum stress-mediated apoptosis of MDBK cells. J Virol 76: 9588-9599.
19. Kim, I., Shu, C.W., Xu, W., Shiau, C.W., Grant, D., Vasile, S., etal. (2009) Chemical biology investigation of cell death pathways activated by endoplasmic reticulum stress reveals cytoprotective modulators of ASK1. J Biol Chem 284: 1593-1603.
20. Knowlton, K.U. (2008) CVB infection and mechanisms of viral cardiomyopathy. Curr Top Microbiol Immunol 323: 315-335.
21. van Kuppeveld, F.J., Hoenderop, J.G., Smeets, R.L., Willems, P.H., Dijkman, H.B., Galama, J.M., and Melchers, W.J. (1997) Coxsackievirus protein 2B modifies endoplasmic reticulum membrane and plasma membrane permeability and facilitates virus release. EMBO J 16: 3519-3532.
22. Li, B., Gao, B., Ye, L., Han, X., Wang, W., Kong, L., etal. (2007) Hepatitis B virus X protein (HBx) activates ATF6 and IRE1-XBP1 pathways of unfolded protein response. Virus Res 124: 44-49.
23. Lin, W., Bailey, S.L., Ho, H., Harding, H.P., Ron, D., Miller, S.D., and Popko, B. (2007) The integrated stress response prevents demyelination by protecting oligodendrocytes against immune-mediated damage. J Clin Invest 117: 448-456.
24. Lin, J.H., Walter, P., and Yen, T.S. (2008a) Endoplasmic reticulum stress in disease pathogenesis. Annu Rev Pathol 3: 399-425.
25. Lin, W., Kunkler, P.E., Harding, H.P., Ron, D., Kraig, R.P., and Popko, B. (2008b) Enhanced integrated stress response promotes myelinating oligodendrocyte survival in response to interferon-gamma. Am J Pathol 173: 1508-1517.
26. Liu, Z., Zhang, H.M., Yuan, J., Lim, T., Sall, A., Taylor, G.A., and Yang, D. (2008) Focal adhesion kinase mediates the interferon-gamma-inducible GTPase-induced phosphatidylinositol 3-kinase/Akt survival pathway and further initiates a positive feedback loop of NF-kappaB activation. Cell Microbiol 10: 1787-1800.
27. Marciniak, S.J., and Ron, D. (2006) Endoplasmic reticulum stress signaling in disease. Physiol Rev 86: 1133-1149.
28. Marciniak, S.J., Yun, C.Y., Oyadomari, S., Novoa, I., Zhang, Y., Jungreis, R., etal. (2004) CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev 18: 3066-3077.
29. Nakagawa, T., Zhu, H., Morishima, N., Li, E., Xu, J., Yankner, B.A., and Yuan, J. (2000) Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403: 98-103.
30. Netherton, C.L., Parsley, J.C., and Wileman, T. (2004) African swine fever virus inhibits induction of the stress-induced proapoptotic transcription factor CHOP/GADD153. J Virol 78: 10825-10828.
31. Ohoka, N., Yoshii, S., Hattori, T., Onozaki, K., and Hayashi, H. (2005) TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J 24: 1243-1255.
32. Rasheva, V.I., and Domingos, P.M. (2009) Cellular responses to endoplasmic reticulum stress and apoptosis. Apoptosis 14: 996-1007.
33. Schroder, M. (2008) Endoplasmic reticulum stress responses. Cell Mol Life Sci 65: 862-894.
34. Singh, S.B., Davis, A.S., Taylor, G.A., and Deretic, V. (2006) Human IRGM induces autophagy to eliminate intracellular mycobacteria. Science 313: 1438-1441.
35. Smith, J.A., Schmechel, S.C., Raghavan, A., Abelson, M., Reilly, C., Katze, M.G., etal. (2006) Reovirus induces and benefits from an integrated cellular stress response. J Virol 80: 2019-2033.
36. 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.
37. Suhy, D.A., Giddings, T.H., Jr, and Kirkegaard, K. (2000) Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles. J Virol 74: 8953-8965.
38. Szegezdi, E., Logue, S.E., Gorman, A.M., and Samali, A. (2006) Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Rep 7: 880-885.
39. Tajiri, S., Oyadomari, S., Yano, S., Morioka, M., Gotoh, T., Hamada, J.I., etal. (2004) Ischemia-induced neuronal cell death is mediated by the endoplasmic reticulum stress pathway involving CHOP. Cell Death Differ 11: 403-415.
40. Tam, P.E. (2006) Coxsackievirus myocarditis: interplay between virus and host in the pathogenesis of heart disease. Viral Immunol 19: 133-146.
41. 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.
42. 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.
43. Taylor, G.A., Stauber, R., Rulong, S., Hudson, E., Pei, V., Pavlakis, G.N., etal. (1997) The inducibly expressed GTPase localizes to the endoplasmic reticulum, independently of GTP binding. J Biol Chem 272: 10639-10645.
44. Taylor, G.A., Collazo, C.M., Yap, G.S., Nguyen, K., Gregorio, T.A., Taylor, L.S., etal. (2000) Pathogen-specific loss of host resistance in mice lacking the IFN-gamma-inducible gene IGTP. Proc Natl Acad Sci USA 97: 751-755.
45. Taylor, G.A., Feng, C.G., and Sher, A. (2004) p47 GTPases: regulators of immunity to intracellular pathogens. Nat Rev Immunol 4: 100-109.
46. Trono, D., Pelletier, J., Sonenberg, N., and Baltimore, D. (1988) Translation in mammalian cells of a gene linked to the poliovirus 5′ noncoding region. Science 241: 445-448.
47. Urano, F., Wang, X., Bertolotti, A., Zhang, Y., Chung, P., Harding, H.P., and Ron, D. (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287: 664-666.
48. Wang, H., Kouri, G., and Wollheim, C.B. (2005) ER stress and SREBP-1 activation are implicated in beta-cell glucolipotoxicity. J Cell Sci 118: 3905-3915.
49. Yang, D., Wilson, J.E., Anderson, D.R., Bohunek, L., Cordeiro, C., Kandolf, R., and McManus, B.M. (1997) In vitro mutational and inhibitory analysis of the cis-acting translational elements within the 5′ untranslated region of coxsackievirus B3: potential targets for antiviral action of antisense oligomers. Virology 228: 63-73.
50. Yang, D., Yu, J., Luo, Z., Carthy, C.M., Wilson, J.E., Liu, Z., and McManus, B.M. (1999) Viral myocarditis: identification of five differentially expressed genes in coxsackievirus B3-infected mouse heart. Circ Res 84: 704-712.
51. Yoshida, H. (2007) ER stress and diseases. FEBS J 274: 630-658.
52. 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.
53. Zhang, H.M., Yuan, J., Cheung, P., Luo, H., Yanagawa, B., Chau, D., etal. (2003) Overexpression of interferon-gamma-inducible GTPase inhibits coxsackievirus B3-induced apoptosis through the activation of the phosphatidylinositol 3-kinase/Akt pathway and inhibition of viral replication. J Biol Chem 278: 33011-33019.
54. Zhang, H.M., Ye, X., Su, Y., Yuan, J., Liu, Z., Stein, D.A., and Yang, D. (2010) Coxsackievirus B3 infection activates the unfolded protein response and induces apoptosis through downregulation of p58IPK and activation of CHOP and SREBP1. J Virol 84: 8446-8459.
55. Zhou, H., Gurley, E.C., Jarujaron, S., Ding, H., Fang, Y., Xu, Z., etal. (2006) HIV protease inhibitors activate the unfolded protein response and disrupt lipid metabolism in primary hepatocytes. Am J Physiol Gastrointest Liver Physiol 291: G1071-G1080.