XBP-1 Regulates a Subset of Endoplasmic Reticulum Resident Chaperone Genes in the Unfolded Protein Response

Molecular and Cellular Biology

Volumn 23, Issue 21, 2003, Pages 7448-7459

  Lee, Ann Hwee ^a   Iwakoshi, Neal N ^a   Glimcher, Laurie H ^a,b  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE REGULATED PROTEIN 78; HEAT SHOCK PROTEIN 40; HEAT SHOCK PROTEIN 70; MEMBRANE PROTEIN; PROTEIN DISULFIDE ISOMERASE; RIBOSOME ASSOCIATED MEMBRANE PROTEIN 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ATF6ALPHA; TRANSCRIPTION FACTOR ATF6BETA; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ANIMAL CELL; ARTICLE; CELL PROTECTION; EMBRYO; ENDOPLASMIC RETICULUM; GENE CONTROL; GENE EXPRESSION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN FOLDING; SIGNAL TRANSDUCTION; STRESS; UNFOLDED PROTEIN RESPONSE; UNINDEXED SEQUENCE;

ACTIVATING TRANSCRIPTION FACTOR 6; ANIMALS; CELL LINE; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; ENZYME INHIBITORS; FIBROBLASTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEAT-SHOCK PROTEINS; HSP40 HEAT-SHOCK PROTEINS; HUMANS; MEMBRANE PROTEINS; MOLECULAR CHAPERONES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN FOLDING; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS;

ANIMALIA; MAMMALIA;

EID: 0142059951     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.21.7448-7459.2003     Document Type: Article

References (68)

1. Bukau, B., and A. L. Horwich. 1998. The Hsp70 and Hsp60 chaperone machines. Cell 92:351-366.
2. 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.
3. Chevalier, M., H. Rhee, E. C. Elguindi, and S. Y. Blond. 2000. Interaction of murine BiP/GRP78 with the DnaJ homologue MTJ1. J. Biol. Chem. 275: 19620-19627.
4. Clauss, I. M., M. Chu, J.-L. Zhao, and L. H. Glimcher. 1996. The basic domain/leucine zipper protein hXBP-1 preferentially binds to and transactivates CRE-like sequences containing an ACGT core. Nucleic Acids Res. 24:1855-1864.
5. 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.
6. Dudek, J., J. Volkmer, C. Bies, S. Guth, A. Muller, M. Lerner, P. Feick, K. H. Schafer, E. Morgenstern, F. Hennessy, G. L. Blatch, K. Janoscheck, N. Heim, P. Scholtes, M. Frien, W. Nastainczyk, and R. Zimmermann. 2002. A novel type of co-chaperone mediates transmembrane recruitment of DnaK-like chaperones to ribosomes. EMBO J. 21:2958-2967.
7. Foti, D. M., A. Welihinda, R. J. Kaufman, and A. S. Lee. 1999. Conservation and divergence of the yeast and mammalian unfolded protein response. Activation of specific mammalian endoplasmic reticulum stress element of the grp78/BiP promoter by yeast Hac1. J. Biol. Chem. 274:30402-30409.
8. 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.
9. 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.
10. 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.
11. Haze, K., T. Okada, H. Yoshida, H. Yanagi, T. Yura, M. Negishi, and K. Mori. 2001. Identification of the G13 (cAMP-response-element-binding protein-related protein) gene product related to activating transcription factor 6 as a transcriptional activator of the mammalian unfolded protein response. Biochem. J. 355:19-28.
12. 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.
13. Hosokawa, N., I. Wada, K. Hasegawa, T. Yorihuzi, L. O. Tremblay, A. Herscovics, and K. Nagata. 2001. A novel ER alpha-mannosidase-like protein accelerates ER-associated degradation. EMBO Rep. 2:415-422.
14. Iwakoshi, N. N., A. H. Lee, P. Vallabhajosyula, K. L. Otipoby, K. Rajewsky, and L. H. Glimcher. 2003. Plasma cell differentiation and the unfolded protein response intersect the transcription factor XBP-1. Nat. Immunol. 4:321-329.
15. Katze, M. G. 1995. Regulation of the interferon-induced PKR: can viruses cope? Trends Microbiol. 3:75-78.
16. Kaufman, R. J. 2002. Orchestrating the unfolded protein response in health and disease. J. Clin. Investig. 110:1389-1398.
17. Kaufman, R. J. 1999. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13:1211-1233.
18. Kikuchi, M., E. Doi, I. Tsujimoto, T. Horibe, and Y. Tsujimoto. 2002. Functional analysis of human P5, a protein disulfide isomerase homologue. J. Biochem. 132:451-455.
19. Kokame, K., H. Kato, and T. Miyata. 2001. Identification of ERSE-II, a new cis-acting element responsible for the ATF6-dependent mammalian unfolded protein response. J. Biol. Chem. 276:9199-9205.
20. Korth, M. J., C. N. Lyons, M. Wambach, and M. G. Katze. 1996. Cloning, expression and cellular localization of the oncogenic 58-kDa inhibitor of the RNA-activated human and mouse protein kinase. Gene 170:181-188.
21. Kurisu, J., A. Honma, H. Miyajima, S. Kondo, M. Okumura, and K. Imaizumi. 2003. MDG1/ERdj4, an ER-resident DnaJ family member, suppresses cell death induced by ER stress. Genes Cells 8:189-202.
22. Lee, A. H., J. H. Hong, and Y. S. Seo. 2000. Tumor necrosis factor-alpha and interferon-gamma synergistically activate the RANTES promoter through nuclear factor κB and interferon regulatory factor 1 (IRF-1) transcription factors. Biochem. J. 350(Pt. 1):131-138.
23. 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.
24. r 68,000 from influenza virus-infected cells. Proc. Natl. Acad. Sci. USA 87:6208-6212.
25. 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.
26. Lindemann, D., E. Patriquin, S. Feng, and R. C. Mulligan. 1997. Versatile retrovirus vector systems for regulated gene expression in vitro and in vivo. Mol. Med. 3:466-476.
27. Luo, G., P. Ducy, M. D. McKee, G. J. Pinero, E. Loyer, R. R. Behringer, and G. Karsenty. 1997. Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature 386:78-81.
28. Ma, Y., and L. M. Hendershot. 2001. The unfolding tale of the unfolded protein response. Cell 107:827-830.
29. Melville, M. W., S. L. Tan, M. Wambach, J. Song, R. I. Morimoto, and M. G. Katze. 1999. The cellular inhibitor of the PKR protein kinase, P58(IPK), is an influenza virus-activated co-chaperone that modulates heat shock protein 70 activity. J. Biol. Chem. 274:3797-3803.
30. Molinari, M., V. Calanca, C. Galli, P. Lucca, and P. Paganetti. 2003. Role of EDEM in the release of misfolded glycoproteins from the calnexin cycle. Science 299:1397-1400.
31. Oda, Y., N. Hosokawa, I. Wada, and K. Nagata. 2003. EDEM as an acceptor of terminally misfolded glycoproteins released from calnexin. Science 299: 1394-1397.
32. Ohtsuka, K., and M. Hata. 2000. Mammalian HSP40/DNAJ homologs: cloning of novel cDNAs and a proposal for their classification and nomenclature. Cell Stress Chaperones 5:98-112.
33. 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.
34. 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.
35. Reimold, A. M., N. N. Iwakoshi, J. Manis, P. Vallabhajosyula, E. Szomolanyi-Tsuda, E. M. Gravallese, D. Friend, M. J. Grusby, F. Alt, and L. H. Glimcher. 2001. Plasma cell differentiation requires transcription factor XBP-1. Nature 412:300-307.
36. Reimold, A. M., P. D. Ponath, Y. S. Li, R. R. Hardy, C. S. David, J. L. Strominger, and L. H. Glimcher. 1996. Transcription factor B-cell lineage-specific activator protein regulates the gene for human X-box binding protein 1. J. Exp. Med. 183:393-401.
37. Roy, B., and A. S. Lee. 1999. The mammalian endoplasmic reticulum stress response element consists of an evolutionarily conserved tripartite structure and interacts with a novel stress-inducible complex. Nucleic Acids Res. 27:1437-1443.
38. 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.
39. Samuel, C. E. 1993. The eIF-2 alpha protein kinases, regulators of translation in eukaryotes from yeasts to humans. J. Biol. Chem. 268:7603-7606.
40. Scheuner, D., B. Song, E. McEwen, C. Liu, R. Laybutt, P. Gillespie, T. Saunders, S. Bonner-Weir, and R. J. Kaufman. 2001. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7:1165-1176.
41. Schmid, D., A. Baici, H. Gehring, and P. Christen. 1994. Kinetics of molecular chaperone action. Science 263:971-973.
42. Schroder, K., B. Martoglio, M. Hofmann, C. Holscher, E. Hartmann, S. Prehn, T. A. Rapoport, and B. Dobberstein. 1999. Control of glycosylation of MHC class II-associated invariant chain by translocon-associated RAMP4. EMBO J. 18:4804-4815.
43. Shamu, C. E., and P. Walter. 1996. Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. EMBO J. 15:3028-3039.
44. 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.
45. 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 Caenorhabditis elegans development. Cell 107:893-903.
46. Shen, Y., L. Meunier, and L. M. Hendershot. 2003. Identification and characterization of a novel endoplasmic reticulum (ER) DnaJ homologue, which stimulates ATPase activity of BiP in vitro and is induced by ER stress. J. Biol. Chem. 277:15947-15956.
47. 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.
48. Sidrauski, C., J. S. Cox, and P. Walter. 1996. tRNA ligase is required for regulated mRNA splicing in the unfolded protein response. Cell 87:405-413.
49. Skowronski, J., C. Jolicoeur, S. Alpert, and D. Hanahan. 1990. Determinants of the B-cell response against a transgenic autoantigen. Proc. Natl. Acad. Sci. USA 87:7487-7491.
50. Sui, G., C. Soohoo, B. Affar el, F. Gay, Y. Shi, and W. C. Forrester. 2002. A DNA vector-based RNAi technology to suppress gene expression in mammalian cells. Proc. Natl. Acad. Sci. USA 99:5515-5520.
51. Tirasophon, W., K. Lee, B. Callaghan, A. Welihinda, and R. J. Kaufman. 2000. The endoribonuclease activity of mammalian IRE1 autoregulates its mRNA and is required for the unfolded protein response. Genes Dev. 14:2725-2736.
52. 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.
53. Travers, K. J., C. K. Patil, L. Wodicka, D. J. Lockhart, J. S. Weissman, and P. Walter. 2000. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101:249-258.
54. Ubeda, M., and J. F. Habener. 2000. CHOP gene expression in response to endoplasmic-reticular stress requires NFY interaction with different domains of a conserved DNA-binding element. Nucleic Acids Res. 28:4987-4997.
55. Urano, F., A. Bertolotti, and D. Ron. 2000. IRE1 and efferent signaling from the endoplasmic reticulum. J. Cell Sci. 113:3697-3702.
56. Wang, L., and B. Dobberstein. 1999. Oligomeric complexes involved in translocation of proteins across the membrane of the endoplasmic reticulum. FEBS Lett. 457:316-322.
57. 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.
58. Welihinda, A. A., and R. J. Kaufman. 1996. The unfolded protein response pathway in Saccharomyces cerevisiae: oligomerization and trans-phosphorylation of Ire1p (Ern1p) are required for kinase activation. J. Biol. Chem. 271:18181-18187.
59. Yamaguchi, A., O. Hori, D. M. Stern, E. Hartmann, S. Ogawa, and M. Tohyama. 1999. Stress-associated endoplasmic reticulum protein 1 (SERP1)/ ribosome-associated membrane protein 4 (RAMP4) stabilizes membrane proteins during stress and facilitates subsequent glycosylation. J. Cell Biol. 147:1195-1204.
60. Yan, W., C. L. Frank, M. J. Korth, B. L. Sopher, I. Novoa, D. Ron, and M. G. Katze. 2002. Control of PERK eIF2α kinase activity by the endoplasmic reticulum stress-induced molecular chaperone P58IPK. Proc. Natl. Acad. Sci. USA 99:15920-15925.
61. 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.
62. 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.
63. 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.
64. 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.
65. 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.
66. Yoshida, H., T. Okada, K. Haze, H. Yanagi, T. Yura, M. Negishi, and K. Mori. 2001. Endoplasmic reticulum stress-induced formation of transcription factor complex ERSF including NF-Y (CBF) and activating transcription factors 6α and 6β that activates the mammalian unfolded protein response. Mol. Cell. Biol. 21:1239-1248.
67. Yu, M., R. H. Haslam, and D. B. Haslam. 2000. HEDJ, an Hsp40 cochaperone localized to the endoplasmic reticulum of human cells. J. Biol. Chem. 275:24984-24992.
68. Zhu, C., F. E. Johansen, and R. Prywes. 1997. Interaction of ATF6 and serum response factor. Mol. Cell. Biol. 17:4957-4966.