The 8ab protein of SARS-CoV is a luminal ER membrane-associated protein and induces the activation of ATF6

Virology

Volumn 387, Issue 2, 2009, Pages 402-413

  Sung, Shu Chiun ^a   Chao, Che Yi ^c   Jeng, King Song ^a   Yang, Jyh Yuan ^d   Lai, Michael M C ^a,b  

^a INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c ASIA UNIVERSITY   (Taiwan)

^d CENTER FOR DISEASE CONTROL   (Taiwan)

Author keywords

8ab protein; ATF6; ER resident chaperones; SARS CoV; UPR

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; CALNEXIN; CALRETICULIN; DIGITONIN; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; MEMBRANE PROTEIN; PROTEIN 8AB; SAPONIN; THAPSIGARGIN; TRANSCRIPTION FACTOR ETV6; TUNICAMYCIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ARTICLE; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INDUCTION; PROTEIN SYNTHESIS; SARS CORONAVIRUS; TRANSCRIPTION INITIATION; UNFOLDED PROTEIN RESPONSE; UPREGULATION;

ACTIVATING TRANSCRIPTION FACTOR 6; AMINO ACID SEQUENCE; ANIMALS; CERCOPITHECUS AETHIOPS; ENDOPLASMIC RETICULUM; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PROTEIN TRANSPORT; SARS VIRUS; SEQUENCE ALIGNMENT; UP-REGULATION; VERO CELLS; VIRAL REGULATORY AND ACCESSORY PROTEINS;

ANIMALIA; MAMMALIA; SARS CORONAVIRUS;

EID: 64849096630     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.02.021     Document Type: Article

References (45)

1. 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 18 (2006) 9279-9287
2. Chen X., Shen J., and Prywes R. 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 15 (2002) 13045-13052
3. Chinese S.M.E.C. Molecular evolution of the SARS coronavirus during the course of the SARS epidemic in China. Science 303 5664 (2004) 1666-1669
4. de Haan C.A., Masters P.S., Shen X., Weiss S., and Rottier P.J. The group-specific murine coronavirus genes are not essential, but their deletion, by reverse genetics, is attenuating in the natural host. Virology 296 1 (2002) 177-189
5. Guan Y., Zheng B.J., He Y.Q., Liu X.L., Zhuang Z.X., Cheung C.L., Luo S.W., Li P.H., Zhang L.J., Guan Y.J., Butt K.M., Wong K.L., Chan K.W., Lim W., Shortridge K.F., Yuen K.Y., Peiris J.S., and Poon L.L. Isolation and characterization of viruses related to the SARS coronavirus from animals in Southern China. Science 302 5643 (2003) 276-278
6. Harding H.P., Zhang Y., Bertolotti A., Zeng H., and Ron D. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5 5 (2000) 897-904
7. Haze K., Yoshida H., Yanagi H., Yura T., and Mori K. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell 10 11 (1999) 3787-3799
8. He B. Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ. 13 3 (2006) 393-403
9. Ivashkina N., Wolk B., Lohmann V., Bartenschlager R., Blum H.E., Penin F., and Moradpour D. The hepatitis C virus RNA-dependent RNA polymerase membrane insertion sequence is a transmembrane segment. J. Virol. 76 24 (2002) 13088-13093
10. Keng C.T., Choi Y.W., Welkers M.R., Chan D.Z., Shen S., Gee Lim S., Hong W., and Tan Y.J. The human severe acute respiratory syndrome coronavirus (SARS-CoV) 8b protein is distinct from its counterpart in animal SARS-CoV and down-regulates the expression of the envelope protein in infected cells. Virology 354 1 (2006) 132-142
11. Lee K., Tirasophon W., Shen X., Michalak M., Prywes R., Okada T., Yoshida H., Mori K., and Kaufman R.J. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev. 16 4 (2002) 452-466
12. Li M., Baumeister P., Roy B., Phan T., Foti D., Luo S., and Lee A.S. ATF6 as a transcription activator of the endoplasmic reticulum stress element: thapsigargin stress-induced changes and synergistic interactions with NF-Y and YY1. Mol. Cell. Biol. 20 14 (2000) 5096-5106
13. Liberman E., Fong Y.L., Selby M.J., Choo Q.L., Cousens L., Houghton M., and Yen T.S. Activation of the grp78 and grp94 promoters by hepatitis C virus E2 envelope protein. J. Virol. 73 5 (1999) 3718-3722
14. Lundin M., Monne M., Widell A., Von Heijne G., and Persson M.A. Topology of the membrane-associated hepatitis C virus protein NS4B. J. Virol. 77 9 (2003) 5428-5438
15. Marra M.A., Jones S.J., Astell C.R., Holt R.A., Brooks-Wilson A., Butterfield Y.S., Khattra J., Asano J.K., Barber S.A., Chan S.Y., Cloutier A., Coughlin S.M., Freeman D., Girn N., Griffith O.L., Leach S.R., Mayo M., McDonald H., Montgomery S.B., Pandoh P.K., Petrescu A.S., Robertson A.G., Schein J.E., Siddiqui A., Smailus D.E., Stott J.M., Yang G.S., Plummer F., Andonov A., Artsob H., Bastien N., Bernard K., Booth T.F., Bowness D., Czub M., Drebot M., Fernando L., Flick R., Garbutt M., Gray M., Grolla A., Jones S., Feldmann H., Meyers A., Kabani A., Li Y., Normand S., Stroher U., Tipples G.A., Tyler S., Vogrig R., Ward D., Watson B., Brunham R.C., Krajden M., Petric M., Skowronski D.M., Upton C., and Roper R.L. The genome sequence of the SARS-associated coronavirus. Science 300 5624 (2003) 1399-1404
16. McCullough K.D., Martindale J.L., Klotz L.O., Aw T.Y., and Holbrook N.J. Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol. 21 4 (2001) 1249-1259
17. Oostra M., de Haan C.A., and Rottier P.J. The 29-nucleotide deletion present in human but not in animal severe acute respiratory syndrome coronaviruses disrupts the functional expression of open reading frame 8. J. Virol. 81 24 (2007) 13876-13888
18. Oyadomari S., and Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 11 4 (2004) 381-389
19. Pavio N., Romano P.R., Graczyk T.M., Feinstone S.M., and Taylor D.R. Protein synthesis and endoplasmic reticulum stress can be modulated by the hepatitis C virus envelope protein E2 through the eukaryotic initiation factor 2alpha kinase PERK. J. Virol. 77 6 (2003) 3578-3585
20. Peiris J.S., Chu C.M., Cheng V.C., Chan K.S., Hung I.F., Poon L.L., Law K.I., Tang B.S., Hon T.Y., Chan C.S., Chan K.H., Ng J.S., Zheng B.J., Ng W.L., Lai R.W., Guan Y., and Yuen K.Y. Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: a prospective study. Lancet 361 9371 (2003) 1767-1772
21. Peiris J.S., Lai S.T., Poon L.L., Guan Y., Yam L.Y., Lim W., Nicholls J., Yee W.K., Yan W.W., Cheung M.T., Cheng V.C., Chan K.H., Tsang D.N., Yung R.W., Ng T.K., and Yuen K.Y. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet 361 9366 (2003) 1319-1325
22. Rota P.A., Oberste M.S., Monroe S.S., Nix W.A., Campagnoli R., Icenogle J.P., Penaranda S., Bankamp B., Maher K., Chen M.H., Tong S., Tamin A., Lowe L., Frace M., DeRisi J.L., Chen Q., Wang D., Erdman D.D., Peret T.C., Burns C., Ksiazek T.G., Rollin P.E., Sanchez A., Liffick S., Holloway B., Limor J., McCaustland K., Olsen-Rasmussen M., Fouchier R., Gunther S., Osterhaus A.D., Drosten C., Pallansch M.A., Anderson L.J., and Bellini W.J. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 300 5624 (2003) 1394-1399
23. Rutkowski D.T., and Kaufman R.J. A trip to the ER: coping with stress. Trends Cell. Biol. 14 1 (2004) 20-28
24. Sarma J.D., Scheen E., Seo S.H., Koval M., and Weiss S.R. Enhanced green fluorescent protein expression may be used to monitor murine coronavirus spread in vitro and in the mouse central nervous system. J. Neurovirol. 8 5 (2002) 381-391
25. Schroder M., and Kaufman R.J. The mammalian unfolded protein response. Annu. Rev. Biochem. 74 (2005) 739-789
26. Shen J., Chen X., Hendershot L., and Prywes R. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev. Cell 3 1 (2002) 99-111
27. Shen J., and Prywes R. ER stress signaling by regulated proteolysis of ATF6. Methods 35 4 (2005) 382-389
28. Shen J., Snapp E.L., Lippincott-Schwartz J., and Prywes R. Stable binding of ATF6 to BiP in the endoplasmic reticulum stress response. Mol. Cell. Biol. 25 3 (2005) 921-932
29. Shen Y., and Hendershot L.M. ERdj3, a stress-inducible endoplasmic reticulum DnaJ homologue, serves as a cofactor for BiP's interactions with unfolded substrates. Mol. Biol. Cell. 16 1 (2005) 40-50
30. Sola I., Alonso S., Zuniga S., Balasch M., Plana-Duran J., and Enjuanes L. Engineering the transmissible gastroenteritis virus genome as an expression vector inducing lactogenic immunity. J. Virol. 77 7 (2003) 4357-4369
31. Stadler K., Masignani V., Eickmann M., Becker S., Abrignani S., Klenk H.D., and Rappuoli R. SARS-beginning to understand a new virus. Nat. Rev. Microbiol. 1 3 (2003) 209-218
32. Tan Y.J., Lim S.G., and Hong W. Understanding the accessory viral proteins unique to the severe acute respiratory syndrome (SARS) coronavirus. Antiviral. Res. 72 2 (2006) 78-88
33. Tardif K.D., Mori K., Kaufman R.J., and Siddiqui A. Hepatitis C virus suppresses the IRE1-XBP1 pathway of the unfolded protein response. J. Biol. Chem. 279 17 (2004) 17158-17164
34. 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 15 (2002) 7453-7459
35. Tardif K.D., Waris G., and Siddiqui A. Hepatitis C virus, ER stress, and oxidative stress. Trends Microbiol. 13 4 (2005) 159-163
36. 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 5453 (2000) 664-666
37. Wang X.Z., Harding H.P., Zhang Y., Jolicoeur E.M., Kuroda M., and Ron D. Cloning of mammalian Ire1 reveals diversity in the ER stress responses. Embo J. 17 19 (1998) 5708-5717
38. Wang Y., Shen J., Arenzana N., Tirasophon W., Kaufman R.J., and Prywes R. Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response. J. Biol. Chem. 275 35 (2000) 27013-27020
39. Ye J., Rawson R.B., Komuro R., Chen X., Dave U.P., Prywes R., Brown M.S., and Goldstein J.L. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol. Cell 6 6 (2000) 1355-1364
40. Yoshida H., Haze K., Yanagi H., Yura T., and Mori K. 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 50 (1998) 33741-33749
41. Yoshida H., Matsui T., Hosokawa N., Kaufman R.J., Nagata K., and Mori K. A time-dependent phase shift in the mammalian unfolded protein response. Dev. Cell 4 2 (2003) 265-271
42. 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 7 (2001) 881-891
43. Yoshida H., Okada T., Haze K., Yanagi H., Yura T., Negishi M., and Mori K. ATF6 activated by proteolysis binds in the presence of NF-Y (CBF) directly to the cis-acting element responsible for the mammalian unfolded protein response. Mol. Cell. Biol. 20 18 (2000) 6755-6767
44. Yount B., Roberts R.S., Sims A.C., Deming D., Frieman M.B., Sparks J., Denison M.R., Davis N., and Baric R.S. Severe acute respiratory syndrome coronavirus group-specific open reading frames encode nonessential functions for replication in cell cultures and mice. J. Virol. 79 23 (2005) 14909-14922
45. 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 7 (1998) 982-995