A human coronavirus OC43 variant harboring persistence-associated mutations in the S glycoprotein differentially induces the unfolded protein response in human neurons as compared to wild-type virus

Virology

Volumn 395, Issue 2, 2009, Pages 255-267

  Favreau, Dominique J ^a   Desforges, Marc ^a   St Jean, Julien R ^a   Talbot, Pierre J ^a  

^a INRS INSTITUT ARMAND FRAPPIER   (Canada)

Author keywords

Apoptosis; HCoV OC43; Human Coronavirus OC43; Neurons; Unfolded Protein Response

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; ARGININE; CASPASE 3; HISTIDINE; INITIATION FACTOR 2ALPHA; PROTEIN IRE1; S GLYCOPROTEIN; TYROSINE; UNCLASSIFIED DRUG; VIRUS PROTEIN; X BOX BINDING PROTEIN 1;

ARTICLE; CONTROLLED STUDY; CORONAVIRUS; CYTOTOXICITY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; NERVE CELL; NERVE CELL NECROSIS; NEUROPATHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PERSISTENT VIRUS INFECTION; POINT MUTATION; PRIORITY JOURNAL; VIRUS CELL INTERACTION; VIRUS MUTANT; VIRUS MUTATION; VIRUS PARTICLE; VIRUS PATHOGENESIS; VIRUS VIRULENCE; WILD TYPE;

ANIMALS; ANTIGENS, DIFFERENTIATION; CELL CYCLE PROTEINS; CELL LINE; CORONAVIRIDAE; DNA-BINDING PROTEINS; ENDORIBONUCLEASES; GENE EXPRESSION REGULATION; HUMANS; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; MUTATION; NEURONS; PROTEIN-SERINE-THREONINE KINASES; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE; VIRAL ENVELOPE PROTEINS;

CORONAVIRUS; MUS;

EID: 70450224459     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.09.026     Document Type: Article

References (58)

1. Antony J.M., Ellestad K.K., Hammond R., Imaizumi K., Mallet F., Warren K.G., and Power C. The human endogenous retrovirus envelope glycoprotein, syncytin-1, regulates neuroinflammation and its receptor expression in multiple sclerosis: a role for endoplasmic reticulum chaperones in astrocytes. J. Immunol. 179 (2007) 1210-1224
2. Arbour N., Côté G., Lachance C., Tardieu M., Cashman N.R., and Talbot P.J. Acute and persistent infection of human neural cell lines by human coronavirus OC43. J. Virol. 73 (1999) 3338-3350
3. Arbour N., Day R., Newcombe J., and Talbot P.J. Neuroinvasion by human respiratory coronaviruses. J. Virol. 74 (2000) 8913-8921
4. Bechill J., Chen Z., Brewer J.W., and Baker S.C. Coronavirus infection modulates the unfolded protein response and mediates sustained translational repression. J. Virol. 82 (2008) 4492-4501
5. Bonavia A., Arbour N., Yong V.W., and Talbot P.J. Infection of primary cultures of human neural cells by human coronaviruses 229E and OC43. J. Virol. 71 (1997) 800-806
6. Buchmeier M.J., Dalziel R.G., Koolen M.J., and Lampert P.W. Molecular determinants of CNS virulence of MHV-4. Adv. Exp. Med. Biol. 218 (1987) 287-295
7. Chan C.P., Siu K.L., Chin K.T., Yuen K.Y., Zheng B., and Jin D.Y. Modulation of the unfolded protein response by the severe acute respiratory syndrome coronavirus spike protein. J. Virol. 80 (2006) 9279-9287
8. Cheng G., Feng Z., and He B. 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 (2005) 1379-1388
9. Cory A.H., Owen T.C., Barltrop J.A., and Cory J.G. Use of an aqueous soluble tetrazolium/formazan assay for cell growth assays in culture. Cancer Commun. 3 (1991) 207-212
10. Gu J., Gong E., Zhang B., Zheng J., Gao Z., Zhong Y., Zou W., Zhan J., Wang S., Xie Z., Zhuang H., Wu B., Zhong H., Shao H., Fang W., Gao D., Pei F., Li X., He Z., Xu D., Shi X., Anderson V.M., and Leong A.S. Multiple organ infection and the pathogenesis of SARS. J. Exp. Med. 202 (2005) 415-424
11. Haneda M., Xiao H., Hasegawa T., Kimura Y., Nakashima I., and Isobe K. Regulation of mouse GADD34 gene transcription after DNA damaging agent methylmethane sulfonate. Gene 336 (2004) 139-146
12. Harding H.P., Novoa I., Zhang Y., Zeng H., Wek R., Schapira M., and Ron D. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6 (2000) 1099-1108
13. Hill D.P., and Robertson K.A. Differentiation of LA-N-5 neuroblastoma cells into cholinergic neurons: methods for differentiation, immunohistochemistry and reporter gene introduction. Brain Res. Brain Res. Protoc. 2 (1998) 183-190
14. Hirota M., Kitagaki M., Itagaki H., and Aiba S. Quantitative measurement of spliced XBP1 mRNA as an indicator of endoplasmic reticulum stress. J. Toxicol. Sci. 31 (2006) 149-156
15. Imai Y., Soda M., and Takahashi R. Parkin suppresses unfolded protein stress-induced cell death through its E3 ubiquitin-protein ligase activity. J. Biol. Chem. 275 (2000) 35661-35664
16. Imaizumi K., Miyoshi K., Katayama T., Yoneda T., Taniguchi M., Kudo T., and Tohyama M. The unfolded protein response and Alzheimer's disease. Biochim. Biophys. Acta 1536 (2001) 85-96
17. Isler J.A., Maguire T.G., and Alwine J.C. Production of infectious human cytomegalovirus virions is inhibited by drugs that disrupt calcium homeostasis in the endoplasmic reticulum. J. Virol. 79 (2005) 15388-15397
18. Jacomy H., and Talbot P.J. Vacuolating encephalitis in mice infected by human coronavirus OC43. Virology 315 (2003) 20-33
19. Jacomy H., Fragoso G., Almazan G., Mushynski W.E., and Talbot P.J. Human coronavirus OC43 infection induces chronic encephalitis leading to disabilities in BALB/C mice. Virology 349 (2006) 335-346
20. Jiang H.Y., Wek S.A., McGrath B.C., Lu D., Hai T., Harding H.P., Wang X., Ron D., Cavener D.R., and Wek R.C. Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol. Cell Biol. 24 (2004) 1365-1377
21. Kim T.Y., Kim E., Yoon S.K., and Yoon J.B. Herp enhances ER-associated protein degradation by recruiting ubiquilins. Biochem. Biophys. Res. Commun. 369 (2008) 741-746
22. Lee A.H., Iwakoshi N.N., and Glimcher L.H. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell Biol. 23 (2003) 7448-7459
23. Lindholm D., Wootz H., and Korhonen L. ER stress and neurodegenerative diseases. Cell Death Differ 13 (2006) 385-392
24. Livak K.J., and Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (2001) 402-408
25. Matsumoto M., Minami M., Takeda K., Sakao Y., and Akira S. Ectopic expression of CHOP (GADD153) induces apoptosis in M1 myeloblastic leukemia cells. FEBS Lett. 395 (1996) 143-147
26. Medigeshi G.R., Lancaster A.M., Hirsch A.J., Briese T., Lipkin W.I., Defilippis V., Fruh K., Mason P.W., Nikolich-Zugich J., and Nelson J.A. West Nile virus infection activates the unfolded protein response, leading to CHOP induction and apoptosis. J. Virol. 81 (2007) 10849-10860
27. Mounir S., and Talbot P.J. Sequence analysis of the membrane protein gene of human coronavirus OC43 and evidence for O-glycosylation. J. Gen. Virol. 73 (1992) 2731-2736
28. Netland J., Meyerholz D.K., Moore S., Cassell M., and Perlman S. Severe acute respiratory syndrome coronavirus infection causes neuronal death in the absence of encephalitis in mice transgenic for human ACE2. J. Virol. 82 (2008) 7264-7275
29. Novoa I., Zeng H., Harding H.P., and Ron D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J. Cell Biol. 153 (2001) 1011-1022
30. Okada T., Yoshida H., Akazawa R., Negishi M., and Mori K. Distinct roles of activating transcription factor 6 (ATF6) and double-stranded RNA-activated protein kinase-like endoplasmic reticulum kinase (PERK) in transcription during the mammalian unfolded protein response. Biochem. J. 366 (2002) 585-594
31. Olivari S., Cali T., Salo K.E., Paganetti P., Ruddock L.W., and Molinari M. EDEM1 regulates ER-associated degradation by accelerating de-mannosylation of folding-defective polypeptides and by inhibiting their covalent aggregation. Biochem. Biophys. Res. Commun. 349 (2006) 1278-1284
32. Paschen W. Dependence of vital cell function on endoplasmic reticulum calcium levels: implications for the mechanisms underlying neuronal cell injury in different pathological states. Cell. Calcium 29 (2001) 1-11
33. Paschen W. Endoplasmic reticulum: a primary target in various acute disorders and degenerative diseases of the brain. Cell. Calcium 34 (2003) 365-383
34. Phillips J.J., Chua M.M., Lavi E., and Weiss S.R. Pathogenesis of chimeric MHV4/MHV-A59 recombinant viruses: the murine coronavirus spike protein is a major determinant of neurovirulence. J. Virol. 73 (1999) 7752-7760
35. Pleasure S.J., and Lee V.M. NTera 2 cells: a human cell line which displays characteristics expected of a human committed neuronal progenitor cell. J. Neurosci. Res. 35 (1993) 585-602
36. Ron D., and Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev., Mol. Cell. Biol. 8 (2007) 519-529
37. Roth-Cross J.K., Martinez-Sobrido L., Scott E.P., Garcia-Sastre A., and Weiss S.R. Inhibition of the alpha/beta interferon response by mouse hepatitis virus at multiple levels. J. Virol. 81 (2007) 7189-7199
38. Saeed A.I., Sharov V., White J., Li J., Liang W., Bhagabati N., Braisted J., Klapa M., Currier T., Thiagarajan M., Sturn A., Snuffin M., Rezantsev A., Popov D., Ryltsov A., Kostukovich E., Borisovsky I., Liu Z., Vinsavich A., Trush V., and Quackenbush J. TM4: a free, open-source system for microarray data management and analysis. BioTechniques 34 (2003) 374-378
39. Shi Y., Vattem K.M., Sood R., An J., Liang J., Stramm L., and Wek R.C. Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol. Cell. Biol. 18 (1998) 7499-7509
40. St-Jean J.R., Desforges M., Almazan F., Jacomy H., Enjuanes L., and Talbot P.J. Recovery of a neurovirulent human coronavirus OC43 from an infectious cDNA clone. J. Virol. 80 (2006) 3670-3674
41. Sung S.C., Chao C.Y., Jeng K.S., Yang J.Y., and Lai M.M. The 8ab protein of SARS-CoV is a luminal ER membrane-associated protein and induces the activation of ATF6. Virology 387 (2009) 402-413
42. Talbot P.J., Jacomy H., and Desforges M. Pathogenesis of human coronaviruses other than severe acute respiratory syndrome coronavirus. In: Perlman S., Gallagher T., and Snijder E.J. (Eds). Nidoviruses (2008), ASM Press, Washington, D.C. 313-324
43. Tardif K.D., Mori K., and Siddiqui A. Hepatitis C virus subgenomic replicons induce endoplasmic reticulum stress activating an intracellular signaling pathway. J. Virol. 76 (2002) 7453-7459
44. Tirasophon W., Welihinda A.A., and Kaufman R.J. A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes Dev. 12 (1998) 1812-1824
45. Tirasophon W., Lee K., Callaghan B., Welihinda A., and Kaufman R.J. The endoribonuclease activity of mammalian IRE1 autoregulates its mRNA and is required for the unfolded protein response. Genes Dev. 14 (2000) 2725-2736
46. Tseng G.C., Oh M.K., Rohlin L., Liao J.C., and Wong W.H. Issues in cDNA microarray analysis: quality filtering, channel normalization, models of variations and assessment of gene effects. Nucleic Acids Res. 29 (2001) 2549-2557
47. Umareddy I., Pluquet O., Wang Q.Y., Vasudevan S.G., Chevet E., and Gu F. Dengue virus serotype infection specifies the activation of the unfolded protein response. Virol. J. 4 (2007) 91
48. Urano F., Wang X., Bertolotti A., Zhang Y., Chung P., Harding H.P., and Ron D. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287 (2000) 664-666
49. van Huizen R., Martindale J.L., Gorospe M., and Holbrook N.J. P58IPK, a novel endoplasmic reticulum stress-inducible protein and potential negative regulator of eIF2alpha signaling. J. Biol. Chem. 278 (2003) 15558-15564
50. Versteeg G.A., van de Nes P.S., Bredenbeek P.J., and Spaan W.J. The coronavirus spike protein induces endoplasmic reticulum stress and upregulation of intracellular chemokine mRNA concentrations. J. Virol. 81 (2007) 10981-10990
51. Williams B.L., and Lipkin W.I. Endoplasmic reticulum stress and neurodegeneration in rats neonatally infected with Borna disease virus. J. Virol. 80 (2006) 8613-8626
52. Xuan B., Qian Z., Torigoi E., and Yu D. Human cytomegalovirus protein pUL38 induces ATF4 expression, inhibits persistent JNK phosphorylation, and suppresses endoplasmic reticulum stress-induced cell death. J. Virol. 83 (2009) 3463-3474
53. Yamamoto K., Yoshida H., Kokame K., Kaufman R.J., and Mori K. Differential contributions of ATF6 and XBP1 to the activation of endoplasmic reticulum stress-responsive cis-acting elements ERSE, UPRE and ERSE-II. J. Biochem. 136 (2004) 343-350
54. Yeh E.A., Collins A., Cohen M.E., Duffner P.K., and Faden H. Detection of coronavirus in the central nervous system of a child with acute disseminated encephalomyelitis. Pediatrics 113 (2004) e73-e76
55. Yoshida H., Matsui T., Yamamoto A., Okada T., and Mori K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107 (2001) 881-891
56. Yu C.Y., Hsu Y.W., Liao C.L., and Lin Y.L. Flavivirus infection activates the XBP1 pathway of the unfolded protein response to cope with endoplasmic reticulum stress. J. Virol. 80 (2006) 11868-11880
57. Zhu B., Xu F., and Baba Y. An evaluation of linear RNA amplification in cDNA microarray gene expression analysis. Mol. Genet. Metab. 87 (2006) 71-79
58. Zinszner H., Kuroda M., Wang X., Batchvarova N., Lightfoot R.T., Remotti H., Stevens J.L., and Ron D. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12 (1998) 982-995