Transcriptional and translational control in the mammalian unfolded protein response

Annual Review of Cell and Developmental Biology

Volumn 18, Issue , 2002, Pages 575-599

  Harding, Heather P ^a   Calfon, Marcella ^a   Urano, Fumihiko ^a   Novoa, Isabel ^a   Ron, David ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Endoplasmic reticulum; Molecular chaperones; Protein processing; Signal transduction; Translation

Indexed keywords

CELL PROTEIN; MESSENGER RNA; PROTEIN HAC1; PROTEIN IRE1; UNCLASSIFIED DRUG; CHAPERONE;

BIOSYNTHESIS; CAENORHABDITIS; CELL PROTECTION; CELL SECRETION; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; GENE INACTIVATION; METAZOON; NEGATIVE FEEDBACK; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROCESSING; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TRANSLATION REGULATION; UPREGULATION; ANIMAL; EUKARYOTIC CELL; GENETICS; HUMAN; MAMMAL; METABOLISM; REGULATOR GENE; ULTRASTRUCTURE;

CAENORHABDITIS; MAMMALIA; METAZOA;

ANIMALS; ENDOPLASMIC RETICULUM; EUKARYOTIC CELLS; GENE EXPRESSION REGULATION; GENES, REGULATOR; HUMANS; MAMMALS; MOLECULAR CHAPERONES; PROTEIN BIOSYNTHESIS; PROTEIN FOLDING; SIGNAL TRANSDUCTION;

EID: 0036437307     PISSN: 10810706     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.cellbio.18.011402.160624     Document Type: Review

References (95)

1. Bertolotti A, Ron D. 2001. Alterations in an IRE1-RNA complex in the mammalian unfolded protein response. J. Cell Sci. 114:3207-12
2. Bertolotti A, Wang X, Novoa I, Jungreis R, Schlessinger K, et al. 2001. Increased sensitivity to dextran sodium sulfate colitis in IRE1b deficient mice. J. Clin. Invest. 107:585-93
3. Bertolotti A, Zhang Y, Hendershot L, Harding H, Ron D. 2000. Dynamic interaction of BiP and the ER stress transducers in the unfolded protein response. Nat. Cell Biol. 2:326-32
4. Bork P, Sander C. 1993. A hybrid protein kinase-RNase in an interferon-induced pathway? FEBS Lett. 334:149-52
5. Brostrom CO, Brostrom MA. 1998. Regulation of translational initiation during cellular responses to stress. Prog. Nucleic Acid Res. Mol. Biol. 58:79-125
6. Brown MS, Ye J, Rawson RB, Goldstein JL. 2000. Regulated intramembrane proteolysis: A control mechanism conserved from bacteria to humans. Cell 100:391-98
7. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, et al. 2002. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415:92-96
8. Casagrande R, Stern P, Diehn M, Shamu C, Osario M, et al. 2000. Degradation of proteins from the ER of S. cerevisiae requires an intact unfolded protein response pathway. Mol. Cell 5:729-35
9. Chapman RE, Walter P. 1997. Translational attenuation mediated by an mRNA intron. Curr. Biol. 7:850-59
10. Clark MW, Abelson J. 1987. The subnuclear localization of tRNA ligase in yeast. J. Cell Biol. 105:1515-26
11. Clauss IM, Gravallese EM, Darling JM, Shapiro F, Glimcher MJ, Glimcher LH. 1993. In situ hybridization studies suggest a role for the basic region-leucine zipper protein hXBP-1 in exocrine gland and skeletal development during mouse embryogenesis. Dev. Dyn. 197:146-56
12. Cox JS, Chapman RE, Walter P. 1997. The unfolded protein response coordinates the production of endoplasmic reticulum protein and endoplasmic reticulum membrane. Mol. Biol. Cell 8:1805-14
13. Cox JS, Shamu CE, Walter P. 1993. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73:1197-206
14. Cox JS, Walter P. 1996. A novel mechanism for regulating activity of a transcription factor that controls the unfolded protein response. Cell 87:391-404
15. Culver GM, McCraith SM, Consaul SA, Stanford DR, Phizicky EM. 1997. A 2′-phosphotransferase implicated in tRNA splicing is essential in Saccharomyces cerevisiae. J. Biol. Chem. 272:13203-10
16. Delepine M, Nicolino M, Barrett T, Golamaully M, Lathrop GM, Julier C. 2000. EIF2AK3, encoding translation initiation factor 2-alpha kinase 3, is mutated in patients with Wolcott-Rallison syndrome. Nat. Genet. 25:406-9
17. Dong B, Niwa M, Walter P, Silverman RH. 2001. Basis for regulated RNA cleavage by functional analysis of RNase L and Ire1p. RNA 7:361-73
18. Dong B, Silverman RH. 1999. Alternative function of a protein kinase homology domain in 2′, 5′-oligoadenylate dependent RNase L. Nucleic Acids Res. 27:439-45
19. Dorner A, Wasley L, Kaufman R. 1992. Overexpression of GRP78 mitigates stress induction of glucose regulated proteins and blocks secretion of selective proteins in Chinese hamster ovary cells. EMBO J. 11:1563-71
20. Dorner AJ, Kaufman RJ. 1994. The levels of endoplasmic reticulum proteins and ATP affect folding and secretion of selective proteins. Biologicals 22:103-12
21. Fawcett TW, Martindale JL, Guyton KZ, Hai T, Holbrook NJ. 1999. Complexes containing activating transcription factor (ATF)/cAMP-responsive-element-binding protein (CREB) interact with the CCAAT/enhancer-binding protein (C/EBP)-ATF composite site to regulate Gadd153 expression during the stress response. Biochem. J. 339:135-41
22. Feder JH, Rossi JM, Solomon J, Solomon N, Lindquist S. 1992. The consequences of expressing hsp70 in Drosophila cells at normal temperatures. Genes Dev. 6:1402-13
23. Filipowicz W, Shatkin AJ. 1983. Origin of splice junction phosphate in tRNAs processed by HeLa cell extract. Cell 32:547-57
24. Frand AR, Cuozzo JW, Kaiser CA. 2000. Pathways for protein disulphide bond formation. Trends Cell. Biol. 10:203-10
25. Gonzalez TN, Sidrauski C, Dorfler S, Walter P. 1999. Mechanism of non-spliceosomal mRNA splicing in the unfolded protein response pathway. EMBO J. 18:3119-32
26. Hampton RY. 2002. Proteolyis and sterol regulation. Annu. Rev. Cell Dev. Biol. 18:345-78
27. Han AP, Yu C, Lu L, Fujiwara Y, Browne C, et al. 2001. Heme-regulated eIF2alpha kinase (HRI) is required for translational regulation and survival of erythroid precursors in iron deficiency. EMBO J. 20:6909-18
28. Harding H, Novoa I, Zhang Y, Zeng H, Wek RC, et al. 2000a. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6:1099-108
29. Harding H, Zeng H, Zhang Y, Jungreis R, Chung P, et al. 2001. Diabetes mellitus and excocrine pancreatic dysfunction in Perk-/- mice reveals a role for translational control in survival of secretory cells. Mol. Cell 7:1153-63
30. Harding H, Zhang Y, Bertolotti A, Zeng H, Ron D. 2000b. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5:897-904
31. Harding H, Zhang Y, Ron D. 1999. Translation and protein folding are coupled by an endoplasmic reticulum resident kinase. Nature 397:271-74
32. Harding HP, Novoa I, Bertolotti A, Zeng H, Zhang A, et al. 2001. Translational regulation in the cellular response to biosynthetic load on the endoplasmic reticulum. Cold Spring Harbor Symp. Quant. Biol. 66:499-508
33. Haze K, Yoshida H, Yanagi H, Yura T, 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 10:3787-99
34. He B, Gross M, Roizman B. 1997. The gamma(1)34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1alpha to dephosphorylate the alpha subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNA-activated protein kinase. Proc. Natl. Acad. Sci. USA 94:843-48
35. He B, Gross M, Roizman B. 1998. The gamma134.5 protein of herpes simplex virus 1 has the structural and functional attributes of a protein phosphatase 1 regulatory subunit and is present in a high molecular weight complex with the enzyme in infected cells. J. Biol. Chem. 273:20737-43
36. Hendershot L, Ting J, Lee A. 1988. Identity of the immunoglobulin heavy-chain-binding protein with the 78,000 dalton glucose-regulated protein and the role of posttranslational modifications in its binding function. Mol. Cell. Biol. 8:4250-56
37. Hinnebusch A. 1996. Translational control of GCN4: Gene-specific regulation by phosphorylation of eIF2. In Translational Control, ed. J Hershey, M Mathews, N Sonenberg, pp. 199-244. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press
38. Hinnebusch AG. 1997. Translational regulation of yeast GCN4. A window on factors that control initiator-tRNA binding to the ribosome. J. Biol. Chem. 272:21661-64
39. Hinnebusch AG. 2000. Mechanism and regulation of initiator methionyl-tRNA binding to ribosomes. In Translational Control of Gene Expression, ed. N Sonenberg, JWB Hershey, MB Mathews, pp. 185-243. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press
40. Kaufman RJ. 1999. Stress signaling from the lumen of the endoplasmic reticulum: Coordination of gene transcriptional and translational controls. Genes Dev. 13:1211-33
41. Kawahara T, Yanagi H, Yura T, 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 8:1845-62
42. Kawahara T, Yanagi H, Yura T, Mori K. 1998. Unconventional splicing of HAC1/ERN4 mRNA required for the unfolded protein response. Sequence-specific and non-sequential cleavage of the splice sites. J. Biol. Chem. 273:1802-7
43. Kohno K, Normington K, Sambrook J, Gething MJ, Mori K. 1993. The promoter region of the yeast KAR2 (BiP) gene contains a regulatory domain that responds to the presence of unfolded proteins in the endoplasmic reticulum. Mol. Cell Biol. 13:877-90
44. Kozutsumi Y, Normington K, Press E, Slaughter C, Sambrook J, Gething MJ. 1989. Identification of immunoglobulin heavy chain binding protein as glucose-regulated protein 78 on the basis of amino acid sequence, immunological cross-reactivity, and functional activity. J. Cell Sci. Suppl. 11:115-37
45. Kozutsumi Y, Segal M, Normington K, Gething MJ, Sambrook J. 1988. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature 332:462-64
46. Laitusis AL, Brostrom MA, Brostrom CO. 1999. The dynamic role of GRP78/BiP in the coordination of mRNA translation with protein processing. J. Biol. Chem. 274:486-93
47. Li WW, Sistonen L, Morimoto RI, Lee AS. 1994. Stress induction of the mammalian GRP78/BiP protein gene: In vivo genomic footprinting and identification of p70CORE from human nuclear extract as a DNA-binding component specific to the stress regulatory element. Mol. Cell Biol. 14:5533-46
48. Liu CY, Schroder M, Kaufman RJ. 2000. Ligand-independent dimerization activates the stress-response kinases IRE1 and PERK in the lumen of the endoplasmic reticulum. J. Biol. Chem. 275:44881-85
49. Macejak DG, Sarnow P. 1990. Translational regulation of the immunoglobulin heavy-chain binding protein mRNA. Enzyme 44:310-19
50. Masaki T, Yoshida M, Noguchi S. 1999. Targeted disruption of CRE-binding factor TREB5 gene leads to cellular necrosis in cardiac myocytes at the embryonic stage. Biochem. Biophys. Res. Commun. 261:350-56
51. Mori K. 2000. Tripartite management of unfolded proteins in the endoplasmic reticulum. Cell 101:451-54
52. Mori K, Kawahara T, Yoshida H, Yanagi H, 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 1:803-17
53. Mori K, Ma W, Gething MJ, Sambrook J. 1993. A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74:743-56
54. Mori K, Ogawa N, Kawahara T, Yanagi H, Yura T. 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 97:4660-65
55. Mori K, Sant A, Kohno K, Normington K, Gething MJ, Sambrook JF. 1992. A 22 bp cis-acting element is necessary and sufficient for the induction of the yeast KAR2 (BiP) gene by unfolded proteins. EMBO J. 11:2583-93
56. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, et al. 2000. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403:98-103
57. Nikawa J, Yamashita S. 1992. IRE1 encodes a putative protein kinase containing a membrane-spanning domain and is required for inositol phototrophy in Saccharomyces cerevisiae. Mol. Microbiol. 6:1441-46
58. Nishikura K, De Robertis EM. 1981. RNA processing in microinjected Xenopus oocytes. Sequential addition of base modifications in the spliced transfer RNA. J. Mol. Biol. 145:405-20
59. Niwa M, Sidrauski C, Kaufman RJ, Walter P. 1999. A role for presenilin-1 in nuclear accumulation of Ire1 fragments and induction of the mammalian unfolded protein response. Cell 99:691-702
60. Novoa I, Zeng H, Harding H, Ron D. 2001. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. J. Cell Biol. 153:1011-22
61. Okamura K, Kimata Y, Higashio H, Tsuru A, Kohno K. 2000. Dissociation of Kar2p/BiP from an ER sensory molecule, Ire1p, triggers the unfolded protein response in yeast. Biochem. Biophys. Res. Commun. 279:445-50
62. Parker R, Phan T, Baumeister P, Roy B, Cheriyath V, et al. 2001. Identification of TFII-I as the endoplasmic reticulum stress response element binding factor ERSF: Its autoregulation by stress and interaction with ATF6. Mol. Cell. Biol. 21:3220-33
63. Patil C, Walter P. 2001. Intracellular signaling from the endoplasmic reticulum to the nucleus: The unfolded protein response in yeast and mammals. Curr. Opin. Cell Biol. 13:349-55
64. Reimold AM, Etkin A, Clauss I, Perkins A, Friend DS, et al. 2000. An essential role in liver development for transcription factor XBP-1. Genes Dev. 14:152-57
65. Reimold AM, Iwakoshi NN, Manis J, Vallabhajosyula P, Szomolanyi-Tsuda E, et al. 2001. Plasma cell differentiation requires the transcription factor XBP-1. Nature 412:300-7
66. Roy B, Lee AS. 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. 27:1437-43
67. Ruegsegger U, Leber JH, Walter P. 2001. Block of HAC1 mRNA translation by long-range base pairing is released by cytoplasmic splicing upon induction of the unfolded protein response. Cell 107:103-14
68. Sato N, Urano F, Leem J, Kim S, Li M, et al. 2000. Upregulation of BiP and CHOP by the unfolded-protein response is independent of Presenilin expression. Nat. Cell Biol. 2:863-70
69. Scheuner D, Song B, McEwen E, Gillespie P, Saunders T, et al. 2001. Translational control is required for the unfolded protein response and in-vivo glucose homeostasis. Mol. Cell 7:1165-76
70. Shamu CE, Walter P. 1996. Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. EMBO J. 15:3028-39
71. Shen X, Ellis RE, Lee K, Liu C-Y, Yang K, et al. 2001. Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107:893-903
72. Shi Y, An J, Liang J, Hayes SE, Sandusky GE, et al. 1999. Characterization of a mutant pancreatic eIF-2alpha kinase, PEK, and colocalization with somatostatin in islet delta cells. J. Biol. Chem. 274:5723-30
73. Shi Y, Vattem KM, Sood R, An J, Liang J, et al. 1998. Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol. Cell Biol. 18:7499-509.
74. Sidrauski C, Cox JS, Walter P. 1996. tRNA ligase is required for regulated mRNA splicing in the unfolded protein response. Cell 87:405-13
75. Sidrauski C, Walter P. 1997. The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90:1031-39
76. Spinelli SL, Kierzek R, Turner DH, Phizicky EM. 1999. Transient ADP-ribosylation of a 2′-phosphate implicated in its removal from ligated tRNA during splicing in yeast. J. Biol. Chem. 274:2637-44
77. Stewart FJ, Carson DJ, Thomas PS, Humphreys M, Thornton C, Nevin NC. 1996. Wolcott-Rallison syndrome associated with congenital malformations and a mosaic deletion 15q 11-12. Clin. Genet. 49:152-55
78. Tan S, Somia N, Maher P, Schubert D. 2001. Regulation of antioxidant metabolism by translation initiation factor 2alpha. J. Cell Biol. 152:997-1006
79. Thornton CM, Carson DJ, Stewart FJ. 1997. Autopsy findings in the Wolcott-Rallison syndrome. Pediatr. Pathol. Lab. Med. 17:487-96
80. Tiedge M, Lortz S, Drinkgern J, Lenzen S. 1997. Relation between antioxidant enzyme gene expression and antioxidative defense status of insulin-producing cells. Diabetes 46:1733-42
81. Tirasophon W, Lee K, Callaghan B, Welihinda A, Kaufman RJ. 2000. The endoribonuclease activity of mammalian IRE1 autoregulates its mRNA and is required for the unfolded protein response. Genes Dev. 14:2725-36
82. Tirasophon W, Welihinda AA, Kaufman RJ. 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. 12:1812-24
83. Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P. 2000. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101:249-58
84. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, et al. 2000. Coupling of stress in the endoplasmic reticulum to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287:664-66
85. Wang XZ, Harding HP, Zhang Y, Jolicoeur EM, Kuroda M, Ron D. 1998. Cloning of mammalian Ire1 reveals diversity in the ER stress responses. EMBO J. 17:5708-17
86. Welihinda AA, Tirasophon W, Green SR, Kaufman RJ. 1998. Protein serine/threonine phosphatase Ptc2p negatively regulates the unfolded-protein response by dephosphorylating Ire1p kinase. Mol. Cell. Biol. 18:1967-77
87. Welihinda AA, Tirasophon W, Kaufman RJ. 2000. The transcriptional co-activator ADA5 is required for HAC1 mRNA processing in vivo. J. Biol. Chem. 275:3377-81
88. Wolcott C, Rallison M. 1972. Infancy-onset diabetes mellitus and multiple epiphyseal dysplasia. J. Pediatr. 80:292-97
89. Ye J, Rawson RB, Komuro R, Chen X, Dave UP, et al. 2000. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol. Cell 6:1355-64
90. Yoneda T, Imaizumi K, Oono K, Yui D, Gomi F, et al. 2001. Activation of caspase-12, an endoplastic reticulum (ER) resident caspase, through tumor necrosis factor receptor-associated factor 2-dependent mechanism in response to the ER stress. J. Biol. Chem. 276:13935-40
91. Yoshida H, Haze K, Yanagi H, Yura T, Mori K. 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. 273:33741-49
92. Yoshida H, Matsui T, Yamamoto A, Okada T, 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 107:881-91
93. Yoshida H, Okada T, Haze K, Yanagi H, Yura T, et al. 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. 20:6755-67
94. Yoshida H, Okada T, Haze K, Yanagi H, Yura T, et al. 2001b. Endoplasmic reticulum stress-induced formation of transcription factor complex ERSF including NF-Y (CBF) and activating transcription factors 6alpha and 6beta that activates the mammalian unfolded protein response. Mol. Cell. Biol. 21:1239-48
95. Zhang P, McGrath B, Li S, Frank A, Zarnbito F, et al. 2002. The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol. Cell Biol. 22:3864-74