Activation of hepatitis B virus S promoter by a cell type-restricted IRE1-dependent pathway induced by endoplasmic reticulum stress

Molecular and Cellular Biology

Volumn 25, Issue 17, 2005, Pages 7522-7533

  Huang, Zhi Ming ^a   Tan, Thomas ^a   Yoshida, Hiderou ^b   Mori, Kazutoshi ^b   Ma, Yanjun ^c   Yen, T S Benedict ^a,d  

^a SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b KYOTO UNIVERSITY   (Japan)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MESSENGER RNA; PROTEIN IRE1; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TUNICAMYCIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL TYPE; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; ENDOPLASMIC RETICULUM; HEPATITIS B VIRUS; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRESS; SYNTHESIS; TRANSCRIPTION INITIATION;

ANIMALS; BASE SEQUENCE; CELL LINE, TUMOR; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; ENDORIBONUCLEASES; GENE EXPRESSION REGULATION, VIRAL; HEPATITIS B VIRUS; HUMANS; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; ORGAN SPECIFICITY; PROMOTER REGIONS (GENETICS); PROTEIN-SERINE-THREONINE KINASES; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TUNICAMYCIN;

HEPATITIS B VIRUS;

EID: 23844454276     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.17.7522-7533.2005     Document Type: Article

References (62)

1. Calfon, M., H. Zeng, F. Urano, J. H. Till, S. R. Hubbard, H. P. Harding, S. G. Clark, and D. Ron. 2002. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415:92-96.
2. Cox, J. S., C. E. Shamu, and P. Walter. 1993. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73:1197-1206.
3. Cox, J. S., and P. Walter. 1996. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87: 391-404.
4. Flores, E. R., K. Y. Tsai, D. Crowley, S. Sengupta, A. Yang, F. McKeon, and T. Jacks. 2002. p63 and p73 are required for p53-dependent apoptosis in response to DNA damage. Nature 416:560-564.
5. Ghoshal, K., S. Majumder, Q. Zhu, J. Hunzeker, J. Datta, M. Shah, J. F. Sheridan, and S. T. Jacob. 2001. Influenza virus infection induces metallothionein gene expression in the mouse liver and lung by overlapping but distinct molecular mechanisms. Mol. Cell. Biol. 21:8301-8317.
6. Gorman, C. 1985. High efficiency gene transfer into mammalian cells. In D. M. Glover (ed.), DNA cloning, vol. 2. IRL Press, Oxford, England.
7. Gorski, K., M. Carneiro, and U. Schibler. 1986. Tissue-specific in vitro transcription from the mouse albumin promoter. Cell 47:767-776.
8. Guidotti, L. G., B. Matzke, H. Schaller, and F. V. Chisari. 1995. High-level hepatitis B virus replication in transgenic mice. J. Virol. 69:6158-6169.
9. Harding, H. P., M. Calfon, F. Urano, I. Novoa, and D. Ron. 2002. Transcriptional and translational control in the mammalian unfolded protein response. Annu. Rev. Cell Dev. Biol. 18:575-599.
10. Harding, H. P., I. Novoa, Y. Zhang, H. Zeng, R. Wek, M. Schapira, and D. Ron. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6:1099-1108.
11. Harding, H. P., Y. Zhang, and D. Ron. 1999. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271-274.
12. Harding, H. P., Y. Zhang, H. Zeng, I. Novoa, P. D. Lu, M. Calfon, N. Sadri, C. Yun, B. Popko, R. Paules, D. F. Stojdl, J. C. Bell, T. Hettmann, J. M. Leiden, and D. Ron. 2003. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11:619-633.
13. Haze, K., H. Yoshida, H. Yanagi, T. Yura, and K. Mori. 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.
14. Huang, Z. M., and T. S. Yen. 1993. Dysregulated surface gene expression from disrupted hepatitis B virus genomes. J. Virol. 67:7032-7040.
15. Kawahara, T., H. Yanagi, T. Yura, and K. Mori. 1997. Endoplasmic reticulum stress-induced mRNA splicing permits synthesis of transcription factor Hac1p/Ern4p that activates the unfolded protein response. Mol. Biol. Cell 8:1845-1862.
16. Keller, E. T., C. Chang, and W. B. Ershler. 1996. Inhibition of NFκB activity through maintenance of IκBα levels contributes to dihydrotestosterone-mediated repression of the interleukin-6 promoter. J. Biol. Chem. 271: 26267-26275.
17. Kondo, S., T. Murakami, K. Tatsumi, M. Ogata, S. Kanemoto, K. Otori, K. Iseki, A. Wanaka, and K. Imaizumi. 2005. OASIS, a CREB/ATF-family member, modulates UPR signalling in astrocytes. Nat. Cell Biol. 7:186-194.
18. Lee, A. H., N. N. Iwakoshi, and L. H. Glimcher. 2003. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 23:7448-7459.
19. Lee, K., W. Tirasophon, X. Shen, M. Michalak, R. Prywes, T. Okada, H. Yoshida, K. Mori, and R. J. Kaufman. 2002. IRE1-mediated unconventional mRNA splicing and S2P-mediated ATF6 cleavage merge to regulate XBP1 in signaling the unfolded protein response. Genes Dev. 16:452-466.
20. Li, M., P. Baumeister, B. Roy, T. Phan, D. Foti, S. Luo, and A. S. Lee. 2000. 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. 20:5096-5106.
21. 2+-ATPase inhibitor thapsigargin. J. Biol. Chem. 268:12003-12009.
22. Liu, C. Y., M. Schroder, and R. J. Kaufman. 2000. Ligand-independent dimerization activates the stress response kinases IRE1 and PERK in the lumen of the endoplasmic reticulum. J. Biol. Chem. 275:24881-24885.
23. Lu, C. C., M. Chen, J. H. Ou, and T. S. Yen. 1995. Key role of a CCAAT element in regulating hepatitis B virus surface protein expression. Virology 206:1155-1158.
24. Lu, C. C., and T. S. Yen. 1996. Activation of the hepatitis B virus S promoter by transcription factor NF-Y via a CCAAT element. Virology 225:387-394.
25. Ma, Y., J. W. Brewer, J. A. Diehl, and L. M. Hendershot. 2002. Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol. 318:1351-1365.
26. Ma, Y., and L. M. Hendershot. 2003. Delineation of a negative feedback regulatory loop that controls protein translation during endoplasmic reticulum stress. J. Biol. Chem. 278:34864-34873.
27. Ma, Y., and L. M. Hendershot. 2001. The unfolding tale of the unfolded protein response. Cell 107:827-830.
28. +/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74:743-756.
29. Mori, K., N. Ogawa, T. Kawahara, H. Yanagi, and T. Yura. 2000. mRNA splicing-mediated C-terminal replacement of transcription factor Hac1p is required for efficient activation of the unfolded protein response. Proc. Natl. Acad. Sci. USA 97:4660-4665.
30. Newman, J. R., and A. E. Keating. 2003. Comprehensive identification of human bZIP interactions with coiled-coil arrays. Science 300:2097-2101.
31. Ng, D. T., E. D. Spear, and P. Walter. 2000. The unfolded protein response regulates multiple aspects of secretory and membrane protein biogenesis and endoplasmic reticulum quality control. J. Cell Biol. 150:77-88.
32. Okada, T., H. Yoshida, R. Akazawa, M. Negishi, and K. Mori. 2002. 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. 366:585-594.
33. Ono, S. J., H. C. Liou, R. Davidon, J. L. Strominger, and L. H. Glimcher. 1991. Human X-box-binding protein 1 is required for the transcription of a subset of human class II major histocompatibility genes and forms a heterodimer with c-fos. Proc. Natl. Acad. Sci. USA 88:4309-4312.
34. Patil, C., and P. Walter. 2001. Intracellular signaling from the endoplasmic reticulum to the nucleus: the unfolded protein response in yeast and mammals. Curr. Opin. Cell Biol. 13:349-355.
35. Reimold, A. M., A. Etkin, I. Clauss, A. Perkins, D. S. Friend, J. Zhang, H. F. Horton, A. Scott, S. H. Orkin, M. C. Byrne, M. J. Grusby, and L. H. Glimcher. 2000. An essential role in liver development for transcription factor XBP-1. Genes Dev. 14:152-157.
36. Roy, B., and A. S. Lee. 1999. The mammalian endoplasmic reticulum stress response element consists of an evolutionary conserved tripartite structure and interacts with a novel stress-inducible complex. Nucleic Acids Res. 27:1437-1443.
37. Ruegsegger, U., J. H. Leber, and P. Walter. 2001. Block of HAC1 mRNA translation by long-range base pairing is released by cytoplasmic splicing upon induction of the unfolded protein response. Cell 107:103-114.
38. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
39. Shaffer, A. L., M. Shapiro-Shelef, N. N. Iwakoshi, A. H. Lee, S. B. Qian, H. Zhao, X. Yu, L. Yang, B. K. Tan, A. Rosenwald, E. M. Hurt, E. Petroulakis, N. Sonenberg, J. W. Yewdell, K. Calame, L. H. Glimcher, and L. M. Staudt. 2004. XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 21:81-93.
40. Shen, J., X. Chen, L. Hendershot, and R. Prywes. 2002. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev. Cell 3:99-111.
41. Shen, X., R. E. Ellis, K. Lee, C. Y. Liu, K. Yang, A. Solomon, H. Yoshida, R. Morimoto, D. M. Kurnit, K. Mori, and R. J. Kaufman. 2001. Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107:893-903.
42. Shi, Y., K. M. Vattem, R. Sood, J. An, J. Liang, L. Stramm, and R. C. Wek. 1998. Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol. Cell. Biol. 18:7499-7509.
43. Sidrauski, C., and P. Walter. 1997. The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90:1031-1039.
44. Tardif, K. D., K. Mori, R. J. Kaufman, and A. Siddiqui. 2004. Hepatitis C virus suppresses the IRE1-XBP1 pathway of the unfolded protein response. J. Biol. Chem. 279:17158-17164.
45. Tirasophon, W., A. A. Welihinda, and R. J. Kaufman. 1998. A stress response pathway from the endoplasmic reticulum to the nucleus requires a novel bifunctional protein kinase/endoribonuclease (Ire1p) in mammalian cells. Genes Dev. 12:1812-1824.
46. Urano, F., X. Wang, A. Bertolotti, Y. Zhang, P. Chung, H. P. Harding, and D. Ron. 2000. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287:664-666.
47. Vattem, K. M., and R. C. Wek. 2004. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl. Acad. Sci. USA 101:11269-11274.
48. Wagner, E. J., and M. A. Garcia-Blanco. 2002. RNAi-mediated PTB depletion leads to enhanced exon definition. Mol. Cell 10:943-949.
49. Wang, X. Z., H. P. Harding, Y. Zhang, E. M. Jolicoeur, M. Kuroda, and D. Ron. 1998. Cloning of mammalian Ire1 reveals diversity in the ER stress responses. EMBO J. 17:5708-5717.
50. Wang, Y., J. Shen, N. Arenzana, W. Tirasophon, R. J. Kaufman, and R. Prywes. 2000. Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response. J. Biol. Chem. 275:27013-27020.
51. Xu, Z., V. Bruss, and T. S. Yen. 1997. Formation of intracellular particles by hepatitis B virus large surface protein. J. Virol. 71:5487-5494.
52. Xu, Z., G. Jensen, and T. S. Yen. 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.
53. Xu, Z., T. S. Yen, L. Wu, C. R. Madden, W. Tan, B. L. Slagle, and J. H. Ou. 2002. Enhancement of hepatitis B virus replication by its X protein in transgenic mice. J. Virol. 76:2579-2584.
54. Yamamoto, K., H. Yoshida, K. Kokame, R. J. Kaufman, and K. Mori. 2004. Differential contributions of ATF6 and XBP1 to the activation of endoplasmic reticulum stress-responsive cis-acting elements ERSE, UPRE and ERSE-II. J. Biochem. (Tokyo) 136:343-350.
55. Ye, J., R. B. Rawson, R. Komuro, X. Chen, U. P. Dave, R. Prywes, M. S. Brown, and J. L. Goldstein. 2000. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol. Cell 6:1355-1364.
56. Yen, T. S. 1993. Regulation of hepatitis B virus gene expression. Semin. Virol. 4:33-42.
57. Yoshida, H., K. Haze, H. Yanagi, T. Yura, and K. Mori. 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.
58. Yoshida, H., T. Matsui, N. Hosokawa, R. J. Kaufman, K. Nagata, and K. Mori. 2003. A time-dependent phase shift in the mammalian unfolded protein response. Dev. Cell 4:265-271.
59. Yoshida, H., T. Matsui, A. Yamamoto, T. Okada, and K. Mori. 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.
60. Yoshida, H., T. Okada, K. Haze, H. Yanagi, T. Yura, M. Negishi, and K. Mori. 2000. 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. 20:6755-6767.
61. Zhang, K., and R. J. Kaufman. 2004. Signaling the unfolded protein response from the endoplasmic reticulum. J. Biol. Chem. 279:25935-25938.
62. Zinszner, H., M. Kuroda, X. Wang, N. Batchvarova, R. T. Lightfoot, H. Remotti, J. L. Stevens, and D. Ron. 1998. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12:982-995.