ATF6 is a transcription factor specializing in the regulation of quality control proteins in the endoplasmic reticulum

Cell Structure and Function

Volumn 33, Issue 1, 2008, Pages 75-89

  Adachi, Yusuke ^a   Yamamoto, Keisuke ^a   Okada, Tetsuya ^a   Yoshida, Hiderou ^a   Harada, Akihiro ^b   Mori, Kazutoshi ^a  

^a KYOTO UNIVERSITY   (Japan)

^b GUNMA UNIVERSITY   (Japan)

Author keywords

Endoplasmic reticulum; Microarray analysis; Protein degradation; Protein folding; Transcription factor

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ATF6 PROTEIN, MOUSE; CHAPERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; FEMALE; GENE TARGETING; GENETIC ANALYSIS; GENOME; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN TRANSPORT; QUALITY CONTROL; ANIMAL; CATTLE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROTEIN DENATURATION; STRESS;

EUKARYOTA; MAMMALIA; METAZOA; MUS;

ACTIVATING TRANSCRIPTION FACTOR 6; ANIMALS; CATTLE; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; MICE; MOLECULAR CHAPERONES; PROTEIN DENATURATION; PROTEIN TRANSPORT; STRESS;

EID: 44449101173     PISSN: 03867196     EISSN: 13473700     Source Type: Journal    
DOI: 10.1247/csf.07044     Document Type: Article

References (75)

1. Acosta-Alvear, D., Zhou, Y., Blais, A., Tsikitis, M., Lents, N.H., Arias, C., Lennon, C.J., Kluger, Y., and Dynlacht, B.D. 2007. XBP1 controls diverse cell type- and condition-specific transcriptional regulatory networks. Mol. Cell, 27: 53-66.
2. Allan, B.B., Moyer, B.D., and Balch, W.E. 2000. Rab1 recruitment of p115 into a cis-SNARE complex: programming budding COPII vesicles for fusion. Science, 289: 444-448.
3. Barbosa-Tessmann, I.P., Chen, C., Zhong, C., Siu, F., Schuster, S.M., Nick, H.S., and Kilberg, M.S. 2000. Activation of the human asparagine synthetase gene by the amino acid response and the endoplasmic reticulum stress response pathways occurs by common genomic elements. J. Biol. Chem., 275: 26976-26985.
4. Bernales, S., Papa, F.R., and Walter, P. 2006. Intracellular signaling by the unfolded protein response. Annu. Rev. Cell Dev. Biol., 22: 487-508.
5. Bernstein, H.D., Poritz, M.A., Strub, K., Hoben, P.J., Brenner, S., and Walter, P. 1989. Model for signal sequence recognition from amino-acid sequence of 54K subunit of signal recognition particle. Nature, 340: 482-486.
6. Bertolotti, A., Wang, X., Novoa, I., Jungreis, R., Schlessinger, K., Cho, J.H., West, A.B., and Ron, D. 2001. Increased sensitivity to dextran sodium sulfate colitis in IRE1beta-deficient mice. J. Clin. Invest., 107: 585-593.
7. Bukau, B., Weissman, J., and Horwich, A. 2006. Molecular chaperones and protein quality control. Cell, 125: 443-451.
8. Calfon, M., Zeng, H., Urano, F., Till, J.H., Hubbard, S.R., Harding, H.P., Clark, S.G., and Ron, D. 2002. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature, 415: 92-96.
9. Cox, J.S., Shamu, C.E., and Walter, P. 1993. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell, 73: 1197-1206.
10. Cox, J.S. and Walter, P. 1996. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell, 87: 391-404.
11. Fukuda, S., Sumii, M., Masuda, Y., Takahashi, M., Koike, N., Teishima, J., Yasumoto, H., Itamoto, T., Asahara, T., Dohi, K., and Kamiya, K. 2001. Murine and human SDF2L1 is an endoplasmic reticulum stress-inducible gene and encodes a new member of the Pmt/rt protein family. Biochem. Biophys. Res. Commun., 280: 407-414.
12. Harding, H.P., Novoa, I.I., Zhang, Y., Zeng, H., Wek, R., Schapira, M., and Ron, D. 2000a. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell, 6: 1099-1108.
13. Harding, H.P., Zhang, Y., Bertolotti, A., Zeng, H., and Ron, D. 2000b. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell, 5: 897-904.
14. Haze, K., Okada, T., Yoshida, H., Yanagi, H., Yura, T., Negishi, M., and Mori, K. 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.
15. Haze, K., Yoshida, H., Yanagi, H., Yura, T., and Mori, K. 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.
16. Hjelmqvist, L., Tuson, M., Marfany, G., Herrero, E., Balcells, S., and Gonzalez-Duarte, R. 2002. ORMDL proteins are a conserved new family of endoplasmic reticulum membrane proteins. Genome Biol., 3: 1-16.
17. Hollien, J. and Weissman, J.S. 2006. Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science, 313: 104-107.
18. Hori, O., Miyazaki, M., Tamatani, T., Ozawa, K., Takano, K., Okabe, M., Ikawa, M., Hartmann, E., Mai, P., Stern, D.M., Kitao, Y., and Ogawa, S. 2006. Deletion of SERP1/RAMP4, a component of the endoplasmic reticulum (ER) translocation sites, leads to ER stress. Mol. Cell. Biol., 26: 4257-4267.
19. 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.
20. Kawaguchi, S. and Ng, D.T. 2007. SnapShot: ER-associated protein degradation pathways. Cell, 129: 1230.
21. Kawahara, T., Yanagi, H., Yura, T., and Mori, K. 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.
22. Kondo, S., Murakami, T., Tatsumi, K., Ogata, M., Kanemoto, S., Otori, K., Iseki, K., Wanaka, A., and Imaizumi, K. 2005. OASIS, a CREB/ATF-family member, modulates UPR signalling in astrocytes. Nat. Cell Biol., 7: 186-194.
23. Kozutsumi, Y., Segal, M., Normington, K., Gething, M.J., and Sambrook, J. 1988. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature, 332: 462-464.
24. Lee, A.H., Iwakoshi, N.N., and Glimcher, L.H. 2003. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol., 23: 7448-7459.
25. Lee, K., Tirasophon, W., Shen, X., Michalak, M., Prywes, R., Okada, T., Yoshida, H., Mori, K., and Kaufman, R.J. 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.
26. Lilley, B.N. and Ploegh, H.L. 2004. A membrane protein required for dislocation of misfolded proteins from the ER. Nature, 429: 834-840.
27. Ma, Y., Brewer, J.W., Diehl, J.A., and Hendershot, L.M. 2002. Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol., 318: 1351-1365.
28. Mizobuchi, N., Hoseki, J., Kubota, H., Toyokuni, S., Nozaki, J. , Naitoh, M., Koizumi, A., and Nagata, K. 2007. ARMET is a soluble ER protein induced by the unfolded protein response via ERSE-II element. Cell Struct. Funct., 32: 41-50.
29. Mori, K. 2000. Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell, 101: 451-454.
30. Mori, K. 2003. Frame switch splicing and regulated intramembrane proteolysis: key words to understand the unfolded protein response. Traffic, 4: 519-528.
31. Mori, K., Kawahara, T., Yoshida, H., Yanagi, H., and Yura, T. 1996. Signalling from endoplasmic reticulum to nucleus: transcription factor with a basic-leucine zipper motif is required for the unfolded protein-response pathway. Genes Cells, 1: 803-817.
32. +/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell, 74: 743-756.
33. Mori, K., Ogawa, N., Kawahara, T., Yanagi, H., and Yura, T. 1998. Palindrome with spacer of one nucleotide is characteristic of the cis-acting unfolded protein-response element in Saccharomyces cerevisiae. J. Biol. Chem., 273: 9912-9920.
34. Nadanaka, S., Yoshida, H., Kano, F., Murata, M., and Mori, K. 2004. Activation of mammalian unfolded protein response is compatible with the quality control system operating in the endoplasmic reticulum. Mol. Biol. Cell, 15: 2537-2548.
35. Nagamori, I., Yabuta, N., Fujii, T., Tanaka, H., Yomogida, K., Nishimune, Y., and Nojima, H. 2005. Tisp40, a spermatid specific bZip transcription factor, functions by binding to the unfolded protein response element via the Rip pathway. Genes Cells, 10: 575-594.
36. Nehls, S., Snapp, E.L., Cole, N.B., Zaal, K.J., Kenworthy, A.K., Roberts, T.H., Ellenberg, J., Presley, J.F., Siggia, E., and Lippincott-Schwartz, J. 2000. Dynamics and retention of misfolded proteins in native ER membranes. Nat. Cell Biol., 2: 288-295.
37. Novoa, I., Zeng, H., Harding, H.P., and Ron, D. 2001. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. J. Cell Biol., 153: 1011-1022.
38. Oda, Y., Okada, T., Yoshida, H., Kaufman, R.J., Nagata, K., and Mori, K. 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.
39. Okada, T., Yoshida, H., Akazawa, R., Negishi, M., and Mori, K. 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.
40. Ortiz, J.A., Castillo, M., del Toro, E.D., Mulet, J., Gerber, S., Valor, L.M., Sala, S., Sala, F., Gutierrez, L.M., and Criado, M. 2005. The cysteine-rich with EGF-like domains 2 (CRELD2) protein interacts with the large cytoplasmic domain of human neuronal nicotinic acetylcholine receptor alpha4 and beta2 subunits. J. Neurochem., 95: 1585-1596.
41. Otterson, G.A., Flynn, G.C., Kratzke, R.A., Coxon, A., Johnston, P.G., and Kaye, F.J. 1994. Stch encodes the 'ATPase core' of a microsomal stress 70 protein. EMBO J., 13: 1216-1225.
42. Paccaud, J.P., Reith, W., Carpentier, J.L., Ravazzola, M., Amherdt, M., Schekman, R., and Orci, L. 1996. Cloning and functional characterization of mammalian homologues of the COPII component Sec23. Mol. Biol. Cell, 7: 1535-1546.
43. Raggo, C., Rapin, N., Stirling, J., Gobeil, P., Smith-Windsor, E., O'Hare, P., and Misra, V. 2002. Luman, the cellular counterpart of herpes simplex virus VP16, is processed by regulated intramembrane proteolysis. Mol. Cell. Biol., 22: 5639-5649.
44. Ron, D. 2002. Translational control in the endoplasmic reticulum stress response. J. Clin. Invest., 110: 1383-1388.
45. Ron, D. and Walter, P. 2007. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol., 8: 519-529.
46. Rutkowski, D.T., Kang, S.W., Goodman, A.G., Garrison, J.L., Taunton, J., Katze, M.G., Kaufman, R.J., and Hegde, R.S. 2007. The role of p58IPK in protecting the stressed endoplasmic reticulum. Mol. Biol. Cell, 18: 3681-3691.
47. Sambrook, J., Fritsch, E.F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
48. Scheuner, D., Song, B., McEwen, E., Liu, C., Laybutt, R., Gillespie, P., Saunders, T., Bonner-Weir, S., and Kaufman, R.J. 2001. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell, 7: 1165-1176.
49. Schroder, M. and Kaufman, R.J. 2005. The mammalian unfolded protein response. Annu. Rev. Biochem., 74: 739-789.
50. Shaffer, A.L., Shapiro-Shelef, M., Iwakoshi, N.N., Lee, A.H., Qian, S.B., Zhao, H., Yu, X., Yang, L., Tan, B.K., Rosenwald, A., Hurt, E.M., Petroulakis, E., Sonenberg, N., Yewdell, J.W., Calame, K., Glimcher, L.H., and Staudt, L.M. 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.
51. Shen, J., Chen, X., Hendershot, L., and Prywes, R. 2002a. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev. Cell, 3: 99-111.
52. Shen, X., Ellis, R.E., Lee, K., Liu, C.Y., Yang, K., Solomon, A., Yoshida, H., Morimoto, R., Kurnit, D.M., Mori, K., and Kaufman, R.J. 2001. Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell, 107: 893-903.
53. Shen, X., Ellis, R.E., Sakaki, K., and Kaufman, R.J. 2005. Genetic interactions due to constitutive and inducible gene regulation mediated by the unfolded protein response in C. elegans. PLoS Genet., 1: 355-368.
54. Shen, Y. and Hendershot, L.M. 2005. ERdj3, a stress-inducible endoplasmic reticulum DnaJ homologue, serves as a cofactor for BiP's interactions with unfolded substrates. Mol. Biol. Cell, 16: 40-50.
55. Shen, Y., Meunier, L., and Hendershot, L.M. 2002b. 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.
56. Shiu, R.P., Pouyssegur, J., and Pastan, I. 1977. Glucose depletion accounts for the induction of two transformation-sensitive membrane proteins in Rous sarcoma virus-transformed chick embryo fibroblasts. Proc. Natl. Acad. Sci. USA, 74: 3840-3844.
57. Silverman, R.H. and Williams, B.R. 1999. Translational control perks up. Nature, 397: 208-210.
58. Sitia, R. and Braakman, I. 2003. Quality control in the endoplasmic reticulum protein factory. Nature, 426: 891-894.
59. Sriburi, R., Bommiasamy, H., Buldak, G.L., Robbins, G.R., Frank, M., Jackowski, S., and Brewer, J.W. 2007. Coordinate regulation of phospholipid biosynthesis and secretory pathway gene expression in XBP-1(S)-induced endoplasmic reticulum biogenesis. J. Biol. Chem., 282: 7024-7034.
60. 2+ channels. J. Cell Biol., 175: 901-911.
61. Thuerauf, D.J., Hoover, H., Meller, J., Hernandez, J., Su, L., Andrews, C., Dillmann, W.H., McDonough, P.M., and Glembotski, C.C. 2001. Sarco/endoplasmic reticulum calcium ATPase-2 expression is regulated by ATF6 during the endoplasmic reticulum stress response: Intracellular signaling of calcium stress in a cardiac myocyte model system. J. Biol. Chem., 276: 48309-48317.
62. Travers, K.J., Patil, C.K., Wodicka, L., Lockhart, D.J., Weissman, J.S., and Walter, P. 2000. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell, 101: 249-258.
63. Wasmeier, C., Romao, M., Plowright, L., Bennett, D.C., Raposo, G., and Seabra, M.C. 2006. Rab38 and Rab32 control post-Golgi trafficking of melanogenic enzymes. J. Cell Biol., 175: 271-281.
64. Watanabe, R., Kinoshita, T., Masaki, R., Yamamoto, A., Takeda, J., and Inoue, N. 1996. PIG-A and PIG-H, which participate in glycosyl- phosphatidylinositol anchor biosynthesis, form a protein complex in the endoplasmic reticulum. J. Biol. Chem., 271: 26868-26875.
65. Wu, J., Rutkowski, D.T., Dubois, M., Swathirajan, J., Saunders, T., Wang, J., Song, B., Yau, G.D., and Kaufman, R.J. 2007. ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev. Cell, 13: 351-364.
66. Yamamoto, K., Sato, T., Matsui, T., Sato, M., Okada, T., Yoshida, H., Harada, A., and Mori, K. 2007. Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev. Cell, 13: 365-376.
67. Ye, J., Rawson, R.B., Komuro, R., Chen, X., Dave, U.P., Prywes, R., Brown, M.S., and Goldstein, J.L. 2000. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol. Cell, 6: 1355-1364.
68. Ye, Y., Meyer, H.H., and Rapoport, T.A. 2001. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature, 414: 652-656.
69. Ye, Y., Shibata, Y., Yun, C., Ron, D., and Rapoport, T.A. 2004. A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol. Nature, 429: 841-847.
70. Yoshida, H., Matsui, T., Hosokawa, N., Kaufman, R.J., Nagata, K., and Mori, K. 2003. A time-dependent phase shift in the mammalian unfolded protein response. Dev. Cell, 4: 265-271.
71. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T., and Mori, K. 2001a. 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.
72. Yoshida, H., Okada, T., Haze, K., Yanagi, H., Yura, T., and Mori, K. 2000. ATF6 activated by proteolysis directly binds in the presence of NF-Y (CBF) to the cis-acting element responsible for the mammalian unfolded protein response. Mol. Cell Biol., 20: 6755-6767.
73. Yoshida, H., Okada, T., Haze, K., Yanagi, H., Yura, T., Negishi, M., and Mori, K. 2001b. 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.
74. Zhang, K., Shen, X., Wu, J., Sakaki, K., Saunders, T., Rutkowski, D.T., Back, S.H., and Kaufman, R.J. 2006. Endoplasmic reticulum stress activates cleavage of CREBH to induce a systemic inflammatory response. Cell, 124: 587-599.
75. Zhang, T., Wong, S.H., Tang, B.L., Xu, Y., Peter, F., Subramaniam, V.N., and Hong, W. 1997. The mammalian protein (rbet1) homologous to yeast Bet1p is primarily associated with the pre-Golgi intermediate compartment and is involved in vesicular transport from the endoplasmic reticulum to the Golgi apparatus. J. Cell Biol., 139: 1157-1168.