From acute ER stress to physiological roles of the unfolded protein response

Cell Death and Differentiation

Volumn 13, Issue 3, 2006, Pages 374-384

  Wu, J ^a   Kaufman, R J ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

cell; Endoplasmic reticulum (ER) stress; Hepatocyte; Lymphocyte; Osteoblast; Signal transduction; Unfolded protein response (UPR)

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INTERLEUKIN 4; LEUCINE ZIPPER PROTEIN; PROTEIN IRE1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ELF 2 ALPHA; TRANSCRIPTION FACTOR XBP1; UNCLASSIFIED DRUG;

ACUTE STRESS DISORDER; APOPTOSIS; CELL DIFFERENTIATION; CELL FUNCTION; CELL MATURATION; CELL METABOLISM; CELL SURVIVAL; DISEASE SEVERITY; ENDOPLASMIC RETICULUM; EUKARYOTIC CELL; GENETIC TRANSCRIPTION; HUMAN; LIVER CELL; NEGATIVE FEEDBACK; NONHUMAN; OSTEOBLAST; PANCREAS ISLET BETA CELL; PLASMA CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN SECRETION; PROTEIN SYNTHESIS; REVIEW; SECRETORY CELL; SIGNAL TRANSDUCTION; STRESS; SYSTEMATIC REVIEW; TRANSCRIPTION TERMINATION; TRANSLATION INITIATION;

ANIMALS; APOPTOSIS; ENDOPLASMIC RETICULUM; MICE; PROTEIN FOLDING; PROTEINS; SIGNAL TRANSDUCTION;

EUKARYOTA;

EID: 33645156429     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/sj.cdd.4401840     Document Type: Review

References (105)

1. Stevens FJ and Argon Y (1999) Protein folding in the ER. Semin. Cell Dev. Biol. 10: 443-454
2. Snapp E (2005) Endoplasmic reticulum biogenesis proliferation and differentiation. In The Biogenesis of Cellular Organelles Mullins C (ed) (New York: Kluwer Academic/Plenum Publishers) pp. 63-95
3. Rutkowski DT and Kaufman RJ (2004) A trip to the ER: Coping with stress. Trends Cell Biol. 14: 20-28
4. Schroder M and Kaufman RJ (2005) The mammalian unfolded protein response. Annu. Rev. Biochem. 74: 739-789
5. Flynn GC, Pohl J, Flocco MT and Rothman JE (1991) Peptide-binding specificity of the molecular chaperone BiP. Nature 353: 726-730
6. Blond-Elguindi S, Cwirla SE, Dower WJ, Lipshutz RJ, Sprang SR, Sambrook JF and Gething MJ (1993) Affinity panning of a library of peptides displayed on bacteriophages reveals the binding specificity of BiP. Cell 75: 717-728
7. Kassenbrock CK and Kelly RB (1989) Interaction of heavy chain binding protein (BiP/GRP78) with adenine nucleotides. EMBO J. 8: 1461-1467
8. Ma K, Vattem KM and Wek RC (2002) Dimerization and release of molecular chaperone inhibition facilitate activation of eukaryotic initiation factor-2 kinase in response to endoplasmic reticulum stress. J. Biol. Chem. 277: 18728-18735
9. Shen J, Chen X, Hendershot L and Prywes R (2002) ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev. Cell 3: 99-111
10. Liu CY, Xu Z and Kaufman RJ (2003) Structure and intermolecular interactions of the luminal dimerization domain of human IRE1alpha. J. Biol. Chem. 278: 17680-17687
11. Bertolotti A, Zhang Y, Hendershot LM, Harding HP and Ron D (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell Biol. 2: 326-332
12. Domer AJ, Wasley LC and Kaufman RJ (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: 1563-1571
13. Kimata Y, Oikawa D, Shimizu Y, Ishiwata-Kimata Y and Kohno K (2004) A role for BiP as an adjustor for the endoplasmic reticulum stress-sensing protein Ire1. J. Cell Biol. 167: 445-456
14. Shen J, Snapp EL, Lippincott-Schwartz J and Prywes R (2005) Stable binding of ATF6 to BiP in the endoplasmic reticulum stress response. Mol. Cell. Biol. 25: 921-932
15. Shi Y, Vattem KM, Sood R, An J, Liang J, Stramm L and Wek RC (1998) Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol. Cell. Biol. 18: 7499-7509
16. Harding HP, Zhang Y and Ron D (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274
17. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M and Ron D (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6: 1099-1108
18. Lu PD, Harding HP and Ron D (2004) Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J. Cell Biol. 167: 27-33
19. Tirasophon W, Welihinda AA and 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: 1812-1824
20. Shen X, Ellis RE, Lee K, Liu CY, Yang K, Solomon A, Yoshida H, Morimoto R, Kumit DM, Mori K and Kaufman RJ (2001) Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell 107: 893-903
21. Yoshida H, Matsui T, Yamamoto A, Okada T and Mori K (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
22. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, Clark SG and Ron D (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415: 92-96
23. Lee K, Tirasophon W, Shen X, Michalak M, Prywes R, Okada T, Yoshida H, Mori K and Kaufman RJ (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. 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
25. Ye J, Rawson RB, Komuro R, Chen X, Dave UP, Prywes R, Brown MS and Goldstein JL (2000) ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol. Cell 6: 1355-1364
26. Yoshida H, Okada T, Haze K, Yanagi H, Yura T, Negishi M and Mori K (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
27. Harding HP, Zhang Y, Bertolotti A, Zeng H and Ron D (2000) Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5: 897-904
28. Yoshida H, Haze K, Yanagi H, Yura T and 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: 33741-33749
29. Li M, Baumeister P, Roy B, Phan T, Foti D, Luo S and Lee AS (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
30. Yoshida H, Okada T, Haze K, Yanagi H, Yura T, Negishi M and Mori K (2001) 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: 1239-1248
31. Scheuner D, Song B, McEwen E, Liu C, Laybutt R, Gillespie P, Saunders T, Bonner-Weir S and Kaufman RJ (2001) Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7: 1165-1176
32. Jousse C, Oyadomari S, Novoa I, Lu P, Zhang Y, Harding HP and Ron D (2003) Inhibition of a constitutive translation initiation factor 2alpha phosphatase, CReP, promotes survival of stressed cells. J. Cell Biol. 163: 767-775
33. Novoa I, Zeng H, Harding HP and Ron D (2001) Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J. Cell Biol. 153: 1011-1022
34. Novoa I, Zhang Y, Zeng H, Jungreis R, Harding HP and Ron D (2003) Stress-induced gene expression requires programmed recovery from translational repression. EMBO J. 22: 1180-1187
35. Yan W, Frank CL, Korth MJ, Sopher BL, Novoa I, Ron D and Katze MG (2002) Control of PERK eIF2alpha kinase activity by the endoplasmic reticulum stress-induced molecular chaperone P58IPK. Proc. Natl. Acad. Sci. USA 99: 15920-15925
36. van Huizen R, Martindale JL, Gorospe M and Holbrook NJ (2003) P58IPK, a novel endoplasmic reticulum stress-inducible protein and potential negative regulator of eIF2alpha signaling. J. Biol. Chem. 278: 15558-15564
37. Welihinda AA, Tirasophon W, Green SR and Kaufman RJ (1998) Protein serine/threonine phosphatase Ptc2p negatively regulates the unfolded-protein response by dephosphorylating Ire1p kinase. Mol. Cell. Biol. 18: 1967-1977
38. Zong WX, Li C, Hatzivassiliou G, Lindsten T, Yu QC, Yuan J and Thompson CB (2003) Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis. J. Cell Biol. 162: 59-69
39. Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T and Korsmeyer SJ (2003) BAX and BAK regulation of endoplasmic reticulum Ca2+: A control point for apoptosis. Science 300: 135-139
40. Nakagawa T and Yuan J (2000) Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J. Cell Biol. 150: 887-894
41. Rao RV, Castro-Obregon S, Frankowski H, Schuler M, Stoka V, del Rio G, Bredesen DE and Ellerby HM (2002) Coupling endoplasmic reticulum stress to the cell death program. An Apaf-1-independent intrinsic pathway. J. Biol. Chem. 277: 21836-21842
42. Crompton M (1999) The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341 (Part 2): 233-249
43. Boya P, Cohen I, Zamzami N, Vieira HL and Kroemer G (2002) Endoplasmic reticulum stress-induced cell death requires mitochondrial membrane permeabilization. Cell Death Differ. 9: 465-467
44. McCullough KD, Martindale JL, Klotz LO, Aw TY and Holbrook NJ (2001) Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol. 21: 1249-1259
45. Ma Y, Brewer JW, Diehl JA and Hendershot LM (2002) Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol. 318: 1351-1365
46. Nishitoh H, Matsuzawa A, Tobiume K, Saegusa K, Takeda K, Inoue K, Hori S, Kakizuka A and Ichijo H (2002) ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats. Genes Dev. 16: 1345-1355
47. Yoneda T, Imaizumi K, Oono K, Yui D, Gomi F, Katayama T and Tohyama M (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: 13935-13940
48. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ, Roth KA, MacGregor GR, Thompson CB and Korsmeyer SJ (2001) Proapoptotic BAX and BAK: A requisite gateway to mitochondrial dysfunction and death. Science 292: 727-730
49. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA and Yuan J (2000) Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403: 98-103
50. Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL and Ron D (1998) CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 12: 982-995
51. Rush JS, Sweitzer T, Kent C, Decker GL and Waechter CJ (1991) Biogenesis of the endoplasmic reticulum in activated B lymphocytes: Temporal relationships between the induction of protein N-glycosylation activity and the biosynthesis of membrane protein and phospholipid. Arch. Biochem. Biophys. 284: 63-70
52. Lewis MJ, Mazzarella RA and Green M (1985) Structure and assembly of the endoplasmic reticulum. The synthesis of three major endoplasmic reticulum proteins during lipopolysaccharide-induced differentiation of murine lymphocytes. J. Biol. Chem. 260: 3050-3057
53. Wiest DL, Burkhardt JK, Hester S, Hortsch M, Meyer DI and Argon Y (1990) Membrane biogenesis during B cell differentiation: Most endoplasmic reticulum proteins are expressed coordinately. J. Cell Biol. 110: 1501-1511
54. Haas IG and Wabl M (1983) Immunoglobulin heavy chain binding protein. Nature 306: 387-389
55. Gass JN, Gifford NM and Brewer JW (2002) Activation of an unfolded protein response during differentiation of antibody-secreting B cells. J. Biol. Chem. 277: 49047-49054
56. Iwakoshi NN, Lee AH, Vallabhajosyula P, Otipoby KL, Rajewsky K and Glimcher LH (2003) Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat. Immunol. 4: 321-329
57. Fugmann SD, Lee AI, Shockett PE, Villey IJ and Schatz DG (2000) The RAG proteins and V(D)J recombination: Complexes, ends, and transposition. Annu. Rev. Immunol. 18: 495-527
58. Reimold AM, Iwakoshi NN, Manis J, Vallabhajosyula P, Szomolanyi-Tsuda E, Gravallese EM, Friend D, Grusby MJ, Alt F and Glimcher LH (2001) Plasma cell differentiation requires the transcription factor XBP-1. Nature 412: 300-307
59. Zhang K, Wong HN, Song B, Miller CN, Scheuner D and Kaufman RJ (2005) The unfolded protein response sensor IRE1alpha is required at 2 distinct steps in B cell lymphopoiesis. J. Clin. Invest. 115: 268-281
60. van Anken E, Romijn EP, Maggioni C, Mezghrani A, Sitia R, Braakman I and Heck AJ (2003) Sequential waves of functionally related proteins are expressed when B cells prepare for antibody secretion. Immunity 18: 243-253
61. Liu CY, Schroder M and 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: 24881-24885
62. Gunn KE, Gifford NM, Mori K and Brewer JW (2004) A role for the unfolded protein response in optimizing antibody secretion. Mol. Immunol. 41: 919-927
63. Lee AH, Iwakoshi NN and Glimcher LH (2003) XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 23: 7448-7459
64. Shaffer AL, Shapiro-Shelef M, Iwakoshi NN, Lee AH, Qian SB, Zhao H, Yu X, Yang L, Tan BK, Rosenwald A, Hurt EM, Petroulakis E, Sonenberg N, Yewdell JW, Calame K, Glimcher LH and Staudt LM (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
65. Sriburi R, Jackowski S, Mori K and Brewer JW (2004) XBP1: A link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J. Cell Biol. 167: 35-41
66. Lingohr MK, Buettner R and Rhodes CJ (2002) Pancreatic beta-cell growth and survival - a role in obesity-linked type 2 diabetes? Trends Mol. Med. 8: 375-384
67. Lowell BB and Shulman GI (2005) Mitochondrial dysfunction and type 2 diabetes. Science 307: 384-387
68. Lo D, Burkly LC, Widera G, Cowing C, Flavell RA, Palmiter RD and Brinster RL (1988) Diabetes and tolerance in transgenic mice expressing class II MHC molecules in pancreatic beta cells. Cell 53: 159-168
69. Wang J, Takeuchi T, Tanaka S, Kubo SK, Kayo T, Lu D, Takata K, Koizumi A and Izumi T (1999) A mutation in the insulin 2 gene induces diabetes with severe pancreatic beta-cell dysfunction in the Mody mouse. J. Clin. Invest. 103: 27-37
70. Leroux L, Desbois P, Lamotte L, Duvillie B, Cordonnier N, Jackerott M, Jami J, Bucchini D and Joshi RL (2001) Compensatory responses in mice carrying a null mutation for Ins1 or Ins2. Diabetes 50 (Suppl 1): S150-S153
71. Oyadomari S, Koizumi A, Takeda K, Gotoh T, Akira S, Araki E and Mori M (2002) Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J. Clin. Invest. 109: 525-532
72. Oyadomari S, Takeda K, Takiguchi M, Gotoh T, Matsumoto M, Wada I, Akira S, Araki E and Mori M (2001) Nitric oxide-induced apoptosis in pancreatic beta cells is mediated by the endoplasmic reticulum stress pathway. Proc. Natl. Acad. Sci. USA 98: 10845-10850
73. Chan NN, Vallance P and Colhoun HM (2000) Nitric oxide and vascular responses in Type I diabetes. Diabetologia 43: 137-147
74. Delepine M, Nicolino M, Barrett T, Golamaully M, Lathrop GM and Julier C (2000) EIF2AK3, encoding translation initiation factor 2-alpha kinase 3, is mutated in patients with Wolcott-Rallison syndrome. Nat. Genet. 25: 406-409
75. Harding HP, Zeng H, Zhang Y, Jungries R, Chung P, Plesken H, Sabatini DD and Ron D (2001) Diabetes mellitus and exocrine pancreatic dysfunction in perk-/- mice reveals a role for translational control in secretory cell survival. Mol. Cell 7: 1153-1163
76. Berlanga JJ, Santoyo J and De Haro C (1999) Characterization of a mammalian homolog of the GCN2 eukaryotic initiation factor 2alpha kinase. Eur. J. Biochem. 265: 754-762
77. Sood R, Porter AC, Olsen DA, Cavener DR and Wek RC (2000) A mammalian homologue of GCN2 protein kinase important for translational control by phosphorylation of eukaryotic initiation factor-2alpha. Genetics 154: 787-801
78. Scarim AL, Amush M, Blair LA, Concepcion J, Heitmeier MR, Scheuner D, Kaufman RJ, Ryerse J, Buller RM and Corbett JA (2001) Mechanisms of beta-cell death in response to double-stranded (ds) RNA and interferon-gamma: DsRNA-dependent protein kinase apoptosis and nitric oxide-dependent necrosis. Am. J. Pathol. 159: 273-283
79. Scheuner D, Mierde DV, Song B, Flamez D, Creemers JW, Tsukamoto K, Ribick M, Schuit FC and Kaufman RJ (2005) Control of mRNA translation preserves endoplasmic reticulum function in beta cells and maintains glucose homeostasis. Nat. Med. 11: 757-764
80. Ladiges WC, Knoblaugh SE, Morton JF, Korth MJ, Sopher BL, Baskin CR, MacAuley A, Goodman AG, LeBoeuf RC and Katze MG (2005) Pancreatic beta-cell failure and diabetes in mice with a deletion mutation of the endoplasmic reticulum molecular chaperone gene P58IPK. Diabetes 54: 1074-1081
81. Marciniak SJ, Yun CY, Oyadomari S, Novoa I, Zhang Y, Jungreis R, Nagata K, Harding HP and Ron D (2004) CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 18: 3066-3077
82. Reimold AM, Etkin A, Clauss I, Perkins A, Friend DS, Zhang J, Horton HF, Scott A, Orkin SH, Byrne MC, Grusby MJ and Glimcher LH (2000) An essential role in liver development for transcription factor XBP-1. Genes Dev. 14: 152-157
83. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, Tuncman G, Gorgun C, Glimcher LH and Hotamisligil GS (2004) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306: 457-461
84. Nakatani Y, Kaneto H, Kawamori D, Yoshiuchi K, Hatazaki M, Matsuoka TA, Ozawa K, Ogawa S, Hori M, Yamasaki Y and Matsuhisa M (2005) Involvement of endoplasmic reticulum stress in insulin resistance and diabetes. J. Biol. Chem. 280: 847-851
85. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP and Ron D (2000) Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287: 664-666
86. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, Maeda K, Karin M and Hotamisligil GS (2002) A central role for JNK in obesity and insulin resistance. Nature 420: 333-336
87. Gu F, Nguyen DT, Stuible M, Dube N, Tremblay ML and Chevet E (2004) Protein-tyrosine phosphatase 1B potentiates IRE1 signaling during endoplasmic reticulum stress. J. Biol. Chem. 279: 49689-49693
88. Frangioni JV, Beahm PH, Shifrin V, Jost CA and Neel BG (1992) The nontransmembrane tyrosine phosphatase PTP-1B localizes to the endoplasmic reticulum via its 35 amino acid C-terminal sequence. Cell 68: 545-560
89. Cheng A, Dube N, Gu F and Tremblay ML (2002) Coordinated action of protein tyrosine phosphatases in insulin signal transduction. Eur. J. Biochem. 269: 1050-1059
90. Zeng L, Lu M, Mori K, Luo S, Lee AS, Zhu Y and Shyy JY (2004) ATF6 modulates SREBP2-mediated lipogenesis. Embo. J. 23: 950-958
91. Shen X, Ellis RE, Sakaki K and Kaufman RJ (2005) Genetic interactions due to constitutive and inducible gene regulation mediated by the unfolded protein response in C. elegans. PLoS. Genet. 1: E37
92. Zhang K, Shen X, Wu J, Sakaki K, Saunders T, Rutkowski DT, Back SH and Kaufman RJ (2006) Endoplasmic reticulum stress activates S1P- and S2P-mediated cleavage of CREBH to induce the acute phase response. Cell, in press
93. Rudnick DA and Perlmutter DH (2005) Alpha-1-antitrypsin deficiency: A new paradigm for hepatocellular carcinoma in genetic liver disease. Hepatology 42: 514-521
94. Wu Y, Whitman I, Molmenti E, Moore K, Hippenmeyer P and Perlmutter DH (1994) A lag in intracellular degradation of mutant alpha 1-antitrypsin correlates with the liver disease phenotype in homozygous PiZZ alpha 1-antitrypsin deficiency. Proc. Natl. Acad. Sci. USA 91: 9014-9018
95. Yang X, Matsuda K, Bialek P, Jacquot S, Masuoka HC, Schinke T, Li L, Brancorsini S, Sassone-Corsi P, Townes TM, Hanauer A and Karsenty G (2004) ATF4 is a substrate of RSK2 and an essential regulator of osteoblast biology; implication for Coffin-Lowry syndrome. Cell 117: 387-398
96. Yang X and Karsenty G (2004) ATF4, the osteoblast accumulation of which is determined post-translationally, can induce osteoblast-specific gene expression in non-osteoblastic cells. J. Biol. Chem. 279: 47109-47114
97. Zhang P, McGrath B, Li S, Frank A, Zambito F, Reinert J, Gannon M, Ma K, McNaughton K and Cavener DR (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: 3864-3874
98. Lamande SR and Bateman JF (1999) Procollagen folding and assembly: The role of endoplasmic reticulum enzymes and molecular chaperones. Semin. Cell Dev. Biol. 10: 455-464
99. Kubota K, Lee DH, Tsuchiya M, Young CS, Everett ET, Martinez-Mier EA, Snead ML, Nguyen L, Urano F and Bartlett JD (2005) Fluoride induces ER stress in ameloblasts responsible for dental enamel formation. J. Biol. Chem. 280: 23194-23202
100. Cox JS, Chapman RE and Walter P (1997) The unfolded protein response coordinates the production of endoplasmic reticulum protein and endoplasmic reticulum membrane. Mol. Biol. Cell 8: 1805-1814
101. Kawahara T, Yanagi H, Yura T and Mori K (1997) Endoplasmic reticulum stress-induced mRNA splicing permits synthesis of transcription factor Hac1p/Em4p that activates the unfolded protein response. Mol. Biol. Cell 8: 1845-1862
102. DenBoer LM, Hardy-Smith PW, Hogan MR, Cockram GP, Audas TE and Lu R (2005) Luman is capable of binding and activating transcription from the unfolded protein response element. Biochem. Biophys. Res. Commun. 331: 113-119
103. 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
104. Omori Y, Imai J, Watanabe M, Komatsu T, Suzuki Y, Kataoka K, Watanabe S, Tanigami A and Sugano S (2001) CREB-H: A novel mammalian transcription factor belonging to the CREB/ATF family and functioning via the box-B element with a liver-specific expression. Nucleic. Acids Res. 29: 2154-2162
105. 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