Luman/CREB3 induces transcription of the endoplasmic reticulum (ER) stress response protein herp through an ER stress response element

Molecular and Cellular Biology

Volumn 26, Issue 21, 2006, Pages 7999-8010

  Liang, Genqing ^a   Audas, Timothy E ^a   Li, Yu ^a   Cockram, Gregory P ^a   Dean, J Doug ^a,c   Martyn, Amanda C ^a   Kokame, Koichi ^b   Lu, Rui ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

^c UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; CELL PROTEIN; DNA BINDING PROTEIN; MEMBRANE PROTEIN; MUTANT PROTEIN; PROTEIN HERP; PROTEIN XBP1; SMALL INTERFERING RNA; THAPSIGARGIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LUMAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA BINDING; DNA RESPONSIVE ELEMENT; DNA SEQUENCE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS RESPONSE ELEMENT II; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE MUTATION; GENE OVEREXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STRESS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS;

ANIMALS; CELL LINE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; HUMANS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXIDATIVE STRESS; PROMOTER REGIONS (GENETICS); PROTEIN-SERINE-THREONINE KINASES; RESPONSE ELEMENTS; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC;

EID: 33750350899     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01046-06     Document Type: Article

References (66)

1. Brown, M. S., and J. L. Goldstein. 1997. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89:331-340.
2. Brown, M. S., J. Ye, R. B. Rawson, and J. L. Goldstein. 2000. Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 100:391-398.
3. 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.
4. 2+ homeostasis and mitochondrial function during endoplasmic reticulum stress. J. Biol. Chem. 279:28733-28743.
5. Chen, X., J. Shen, and R. Prywes. 2002. The luminal domain of ATF6 senses endoplasmic reticulum (ER) stress and causes translocation of ATF6 from the ER to the Golgi. J. Biol. Chem. 277:13045-13052.
6. DenBoer, L. M., P. W. Hardy-Smith, M. R. Hogan, G. P. Cockram, T. E. Audas, and R. Lu. 2005. Luman is capable of binding and activating transcription from the unfolded protein response element. Biochem. Biophys. Res. Commun. 331:113-119.
7. Freiman, R. N., and W. Herr. 1997. Viral mimicry: common mode of association with HCF by VP16 and the cellular protein LZIP. Genes Dev. 11:3122-3137.
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, A. Bertolotti, H. Zeng, and D. Ron. 2000. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5:897-904.
10. 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.
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. Hori, O., F. Ichinoda, A. Yamaguchi, T. Tamatani, M. Taniguchi, Y. Koyama, T. Katayama, M. Tohyama, D. M. Stern, K. Ozawa, Y. Kitao, and S. Ogawa. 2004. Role of Herp in the endoplasmic reticulum stress response. Genes Cells 9:457-469.
14. Ikeda, J., S. Kaneda, K. Kuwabara, S. Ogawa, T. Kobayashi, M. Matsumoto, T. Yura, and H. Yanagi. 1997. Cloning and expression of cDNA encoding the human 150 kDa oxygen-regulated protein, ORP150. Biochem. Biophys. Res. Commun. 230:94-99.
15. Jiang, H. Y., S. A. Wek, B. C. McGrath, D. Lu, T. Hai, H. P. Harding, X. Wang, D. Ron, D. R. Cavener, and R. C. Wek. 2004. Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol. Cell. Biol. 24:1365-1377.
16. Kaneko, M., M. Ishiguro, Y. Niinuma, M. Uesugi, and Y. Nomura. 2002. Human HRD1 protects against ER stress-induced apoptosis through ER-associated degradation. FEBS Lett. 532:147-152.
17. Kokame, K., K. L. Agarwala, H. Kato, and T. Miyata. 2000. Herp, a new ubiquitin-like membrane protein induced by endoplasmic reticulum stress. J. Biol. Chem. 275:32846-32853.
18. 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.
19. 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.
20. Kopito, R. R. 1997. ER quality control: the cytoplasmic connection. Cell 88:427-430.
21. Kristie, T. M., and P. A. Sharp. 1993. Purification of the cellular C1 factor required for the stable recognition of the Oct-1 homeodomain by the herpes simplex virus alpha trans-induction factor (VP16). J. Biol. Chem. 268:6525-6534.
22. 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.
23. 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.
24. Lu, P. D., H. P. Harding, and D. Ron. 2004. Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J. Cell Biol. 167:27-33.
25. Lu, R., and V. Misra. 2000. Potential role for luman, the cellular homologue of herpes simplex virus VP16 (alpha gene trans-inducing factor), in herpesvirus latency. J. Virol. 74:934-943.
26. Lu, R., and V. Misra. 2000. Zhangfei: a second cellular protein interacts with herpes simplex virus accessory factor HCF in a manner similar to Luman and VP16. Nucleic Acids Res. 28:2446-2454.
27. Lu, R., P. Yang, P. O'Hare, and V. Misra. 1997. Luman, a new member of the CREB/ATF family, binds to herpes simplex virus VP16-associated host cellular factor. Mol. Cell. Biol. 17:5117-5126.
28. Lu, R., P. Yang, S. Padmakumar, and V. Misra. 1998. The herpesvirus transactivator VP16 mimics a human basic domain leucine zipper protein, luman, in its interaction with HCF. J. Virol. 72:6291-6297.
29. 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.
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. Mori, K. 2003. Frame switch splicing and regulated intramembrane proteolysis: key words to understand the unfolded protein response. Traffic 4:519-528.
32. Nogalska, A., W. K. Engel, J. McFerrin, K. Kokame, H. Komano, and V. Askanas. 2006. Homocysteine-induced endoplasmic reticulum protein (Herp) is up-regulated in sporadic inclusion-body myositis and in endoplasmic reticulum stress-induced cultured human muscle fibers. J. Neurochem. 96:1491-1499.
33. Oda, Y., T. Okada, H. Yoshida, R. J. Kaufman, K. Nagata, and K. Mori. 2006. Derlin-2 and Derlin-3 are regulated by the mammalian unfolded protein response and are required for ER-associated degradation. J. Cell Biol. 172:383-393.
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. Plemper, R. K., and D. H. Wolf. 1999. Retrograde protein translocation: ERADication of secretory proteins in health and disease. Trends Biochem. Sci. 24:266-270.
36. Raggo, C., N. Rapin, J. Stirling, P. Gobeil, E. Smith-Windsor, P. O'Hare, and V. Misra. 2002. Luman, the cellular counterpart of herpes simplex virus VP16, is processed by regulated intramembrane proteolysis. Mol. Cell. Biol. 22:5639-5649.
37. Rao, R. V., A. Peel, A. Logvinova, G. del Rio, E. Hermel, T. Yokota, P. C. Goldsmith, L. M. Ellerby, H. M. Ellerby, and D. E. Bredesen. 2002. Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperone GRP78. FEBS Lett. 514:122-128.
38. Reddy, R. K., C. H. Mao, P. Baumeister, R. C. Austin, R. J. Kaufman, and A. S. Lee. 2003. Endoplasmic reticulum chaperone protein GRP78 protects cells from apoptosis induced by topoisomerase inhibitors. Role of ATP binding site in suppression of caspase-7 activation. J. Biol. Chem. 278:20915-20924.
39. Ron, D. 2002. Translational control in the endoplasmic reticulum stress response. J. Clin. Investig. 110:1383-1388.
40. 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.
41. Rutkowski, D. T., and R. J. Kaufman. 2004. A trip to the ER: coping with stress. Trends Cell Biol. 14:20-28.
42. Sai, X., Y. Kawamura, K. Kokame, H. Yamaguchi, H. Shiraishi, R. Suzuki, T. Suzuki, M. Kawaichi, T. Miyata, T. Kitamura, B. De Strooper, K. Yanagisawa, and H. Komano. 2002. Endoplasmic reticulum stress-inducible protein, Herp, enhances presenilin-mediated generation of amyloid beta-protein. J. Biol. Chem. 277:12915-12920.
43. Sai, X., K. Kokame, H. Shiraishi, Y. Kawamura, T. Miyata, K. Yanagisawa, and H. Komano. 2003. The ubiquitin-like domain of Herp is involved in Herp degradation, but not necessary for its enhancement of amyloid beta-protein generation. FEBS Lett. 553:151-156.
44. Schroder, M., and R. J. Kaufman. 2005. The mammalian unfolded protein response. Annu. Rev. Biochem. 74:739-789.
45. Schulze, A., S. Standera, E. Buerger, M. Kikkert, S. van Voorden, E. Wiertz, F. Koning, P. M. Kloetzel, and M. Seeger. 2005. The ubiquitin-domain protein HERP forms a complex with components of the endoplasmic reticulum associated degradation pathway. J. Mol. Biol. 354:1021-1027.
46. Shang, J., and M. A. Lehrman. 2004. biscordance of UPR signaling by ATF6 and Ire1p-XBP1 with levels of target transcripts. Biochem. Biophys. Res. Commun. 317:390-396.
47. 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.
48. Shen, J., and R. Prywes. 2005. ER stress signaling by regulated proteolysis of ATF6. Methods 35:382-389.
49. Shen, J., E. L. Snapp, J. Lippincott-Schwartz, and R. Prywes. 2005. Stable binding of ATF6 to BiP in the endoplasmic reticulum stress response. Mol. Cell. Biol. 25:921-932.
50. 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.
51. Shen, X., K. Zhang, and R. J. Kaufman. 2004. The unfolded protein response: a stress signaling pathway of the endoplasmic reticulum. J. Chem. Neuroanat. 28:79-92.
52. Shi, Y., J. An, J. Liang, S. E. Hayes, G. E. Sandusky, L. E. Stramm, and N. N. Yang. 1999. Characterization of a mutant pancreatic eIF-2α kinase, PEK, and co-localization with somatostatin in islet delta cells. J. Biol. Chem. 274:5723-5730.
53. Stirling, J., and P. O'Hare. 2005. CREB4, a transmembrane bZip transcription factor and potential new substrate for regulation and cleavage by S1P. Mol. Biol. Cell 17:413-426.
54. Tusher, V. G., R. Tibshirani, and G. Chu. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98:5116-5121.
55. van Laar, T., T. Schouten, E. Hoogervorst, M. van Eck, A. J. van der Eb, and C. Terleth. 2000. The novel MMS-inducible gene Mif1/KIAA0025 is a target of the unfolded protein response pathway. FEBS Lett. 469:123-131.
56. 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.
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. Wilson, A. C., K. LaMarco, M. G. Peterson, and W. Herr. 1993. The VP16 accessory protein HCF is a family of polypeptides processed from a large precursor protein. Cell 74:115-125.
59. 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.
60. 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.
61. 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. (Erratum, 274:2592, 1999.)
62. 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.
63. 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.
64. 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.
65. 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.
66. Zhou, Q. P., T. N. Le, X. Qiu, V. Spencer, J. de Melo, G. Du, M. Plews, M. Fonseca, J. M. Sun, J. R. Davie, and D. D. Eisenstat. 2004. Identification of a direct Dlx homeodomain target in the developing mouse forebrain and retina by optimization of chromatin immunoprecipitation. Nucleic Acids Res. 32:884-892.