Cloning of mammalian Ire1 reveals diversity in the ER stress responses

EMBO Journal

Volumn 17, Issue 19, 1998, Pages 5708-5717

  Wang, Xiao Zhong ^a   Harding, Heather P ^a   Zhang, Yuhong ^a   Jolicoeur, Ethel M ^a   Kuroda, Masahiko ^a   Ron, David ^a  

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

Author keywords

Chaperones; Endoplasmic reticulum; Membrane protein; Protein folding; Protein kinase

Indexed keywords

CHAPERONE; MEMBRANE ENZYME; PROTEIN KINASE; TUNICAMYCIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL MATURATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; MAMMAL CELL; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STRESS; YEAST;

ADAPTATION, BIOLOGICAL; AMINO ACID SEQUENCE; ANIMALS; CCAAT-ENHANCER-BINDING PROTEINS; CHROMOSOME MAPPING; COS CELLS; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; GENE LIBRARY; HOMEOSTASIS; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; PROTEIN FOLDING; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; STRESS; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION FACTORS;

ANIMALIA; MAMMALIA; MURINAE;

EID: 0032190546     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.19.5708     Document Type: Article

References (50)

1. Barone, M.V., Crozat, A.Y., Tabaee, A., Philipson, L. and Ron, D. (1994) CHOP (GADD153) and its oncogenic variant, TLS-CHOP, differ in their ability to induce G1/S arrest. Genes Dev. 8, 453-464.
2. Batchvarova,N., Wang, X.-Z. and Ron, D. (1995) Inhibition of adipogenesis by the stress-induced protein CHOP (GADD153). EMBO J., 14, 4654-4661.
3. Bork, P. and Sander, C. (1993) A hybrid protein kinase-RNase in an interferon-induced pathway? FEBS Lett., 334, 149-152.
4. Carlson, S.G., Fawcett, T.W., Bartlett, J.D., Bernier, M. and Holbrook, N.J. (1993) Regulation of the C/EBP-related gene. gadd153, by glucose deprivation. Mol. Cell. Biol., 13, 4736-4744.
5. Chapman, R.E. and Walter, P. (1997) Translational attenuation mediated by an mRNA intron. Curr. Biol., 7, 850-859.
6. Clark, M.W. and Abelson, J. (1987) The subnuclear localization of tRNA ligase in yeast. J. Cell Biol., 105, 1515-1526.
7. Clay, F.J., Ernst, M.R., Trueman, J.W., Flegg, R. and Dunn, A.R. (1997) The mouse Plk gene: structural characterization, chromosomal localization and identification of a processed Plk pseudogene. Gene, 198, 329-339.
8. Cox, J.S., Chapman, R.E. 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.
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. Crozat, A.Y., Åman, R. Mandahl, N. and Ron, D. (1993) Fusion of CHOP to a novel RNA-binding protein in human myxoid liposarcoma with t (12-16) (q13;p11). Nature, 363, 640-644.
12. Dorner, A.J., Wasley, L.C. Raney, P. Haugejorden, S., Green, M. and Kaufman, R.J. (1990) The stress response in Chinese hamster ovary cells Regulation of ERp72 and protein disulfide isomerase expression and secretion. J. Biol. Chem., 265, 22029-22034.
13. Dricu, A., Carlberg, M. Wang, M. and Larsson, O. (1996) Inhibition of N-linked glycosylation using Tunicamycin causes cell death in malignant cells: role of down regulation of the Insulin-like growth factor 1 receptor in induction of apoptosis. Cancer Res., 57, 543-548.
14. Evan, G., Lewis, G., Ramsay, G. and Bishop, J. (1985) Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product Mol. Cell. Biol., 5, 3610-3616.
15. Fornace, A.J., Neibert, D.W., Hollander, M.C. Luethy, J.D., Papathanasiou, M., Fragoli, J. and Holbrook, N.J. (1989) Mammalian genes coordinately regulated by growth arrest signals and DNA-damaging agents. Mol. Cell. Biol., 9, 4196-4203.
16. Friedman, A.D. (1996) GADD153/CHOP, a DNA damage-inducible protein reduced CAAT/enhancer binding protein activities and increased apoptosis in 32D c13 myeloid cells. Cancer Res., 56, 3250-3256
17. Gething, M.J. and Sambrook, J. (1992) Protein folding in the cell. Nature, 355, 33-45.
18. Halleck, M.M., Holbrook, N.J., Skinner, J., Liu, H. and Stevens, J.L. (1997) The molecular response to reductive stress in LLC-PK1 renal epithelial cells: coordinate transcriptional regulation of gadd153 and grp78 genes by thiols. Cell Stress Chaper., 2, 31-40.
19. Kalejta, R.F., Shenk, T. and Beavis, A.J. (1997) Use of a membrane-localized green fluorescent protein allows simultaneous identification of transfected cells and cell cycle analysis by flow cytometry. Cytometry, 29, 286-291.
20. 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.
21. Kawahara, T., Yanagi, H., Yura, T. and 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, 1802-1807.
22. Kozutsumi, Y., Segal, M., Nonnington, 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.
23. Larsson, O., Carlberg, M. and Zetterberg, A. (1993) Selective killing induced by an inhibitor of N-linked glycosylation. J. Cell Sci., 106, 299-307.
24. Lee, A.S. (1987) Coordinate regulation of a set of genes by glucose and calcium ionophores in mammalian cells. Trends Biochem. Sci., 12, 20-23.
25. Lenny, N. and Green, M. (1991) Regulation of endoplasmic reticulum stress proteins in COS cells transfected with immunoglobulin μ heavy chain cDNA. J. Biol. Chem., 266, 20532-20537.
26. Little, E. and Lee, A.S. (1995) Generation of a mammalian cell line deficient in glucose-regulated protein stress induction through targeted ribozyme driven by a stress-inducible promoter. J. Biol. Chem., 270, 9526-9534.
27. Little, E., Ramakrishnan, M., Roy, B., Gazit, G. and Lee, A.S. (1994) The glucose-regulated proteins (GRP78 and GRP94): functions, gene regulation and applications. Crit. Rev. Eukaryot. Gene Expr., 4, 1-18.
28. Morf, K., Ma, W., Gething, M.J. and 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, 743-756.
29. 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.
30. Morris, J.A., Dorner, A.J., Edwards, C.A., Hendershot, L.M. and Kaufman, R.J. (1997) Immunoglobulin binding protein (BiP) function is required to protect cells from endoplasmic reticulum stress but is not required for the secretion of selective proteins. J. Biol. Chem., 272, 4327-4334.
31. Nakashima, T., Sekiguchi, T., Kuraoka, A., Fukushima, K., Shibata, Y., Komiyama, S. and Nishimoto, T. (1993) Molecular cloning of a human cDNA encoding a novel protein, DAD1, whose defect causes apoptotic cell death in hamster BHK21 cells. Mol. Cell. Biol., 13, 6367-6374.
32. Nikawa, J., Akiyoshi, M., Hirata, S. and Fukuda, T. (1996) Saccharomyces cerevisiae IRE2/HAC1 is involved in IRE1-mediated KAR2 expression. Nucleic Acids Res., 24, 4222-1226.
33. Pérez-Sala, D. and Mollinedo, F. (1995) Inhibition of N-linked glycosylation induces early apoptosis in human promyelocytic HL-60 cells. J. Cell Physiol., 163, 523-531.
34. Price, B. and Calderwood, S. (1992) Gadd45 and Gadd153 messenger RNA levels are increased during hypoxia and after exposure of cells to agents which elevate the levels of glucose-regulated proteins. Cancer Res., 52, 3814-3817.
35. Rahhitts, T.H., Forster, A., Larson, R. and Nathan, P. (1993) Fusion of the dominant negative transcription regulator CHOP with a novel gene FUS by translocation t (12;16) in malignant liposarcoma. Nature Genet., 4, 175-180.
36. Ron, D. and Habener, J.F. (1992) CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant negative inhibitor of gene transcription. Genes Dev., 6, 439-153.
37. Sadowski, I. and Ptashne, M. (1989) A vector for expressing GAL4 (1-147) fusions in mammalian cells. Nucleic Acids Res., 17, 7539.
38. Sánchez, L. Hughes, R., Mayer, B., Yee, K., Woodget, J., Avruch, J., Kyriakis, J. and Zon, L. (1994) Role of SAPK/ERK kinase-1 in the stress-activated pathway regulating transcription factor c-Jun. Nature, 372, 794-797.
39. Shamu, C.E. and Walter, P. (1996) Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. EMBO J., 15, 3028-3039.
40. Sidrauski, C. and Walter, P. (1997) The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell, 90, 1031-1039.
41. Sidrauski, C., Cox, J.S. and Walter, P. (1996) tRNA ligase is required for regulated mRNA splicing in the unfolded protein response. Cell, 87, 405-413.
42. Silberstein, S., Collins, P., Kelleher, D. and Gilmore, R. (1995) The essential OST2 gene encodes the 16-kD subunit of the yeast oligosaccharyltransferase, a highly conserved protein expressed in diverse eukaryotic organisms. J. Cell Biol., 131, 371-383.
43. Silver, P.A., Keegan, L.P. and Ptashine, M. (1984) Amino terminus of the yeast GAL4 gene product is sufficient for nuclear localization. Proc. Natl Acad. Sci. USA, 81, 5951-5955.
44. Squinto, S.P., Aldrich, T.H., Lindsay, R.M., Morrissey, D.M., Panayotatos, N., Bianco, S.M., Furth, M.E. and Yancopoulos, G.D. (1990) Identification of functional receptors for ciliary neurotrophic factor on neuronal cell lines and primary neurons. Neuron, 5, 757-766.
45. Tirasophon, W., Welihinda, A.A. and Kaufman, R.J. (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.
46. Wang, X.-Z., Lawson, B., Brewer, J., Zinszner, H., Sanjay, A., Mi, L., Boorstein, R., Kreibich, G., Hendershot, L. and Ron, D. (1996) Signals from the stressed endoplasmic reticulum induce C/EBP homologous protein (CHOP/GADD153). Mol. Cell. Biol., 16, 4273-4280.
47. Wang, X.-Z., Kuroda, M. Sok, J., Batchvarova, N., Kimmel, R., Chung, P., Zinszner, H. and Ron, D. (1998) Identification of novel stress-induced genes downstream of chop. EMBO J., 17, 3619-3630.
48. Welihinda, A.A. and Kaufman, R.J. (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.
49. Welihinda, A.A., Tirasophon, W., Green, S.R. and Kaufman, R.J. (1998) Protein serine/threonine phosphatase Ptc2p negatively regulates the unfolded-protein response by dephosphorylating Ire1p kinase. Mol. Cell. Biol., 18, 1967-1977.
50. Zinszner, H., Kuroda, M., Wang, X., Batchvarova, N., Lightfoot, R.T., Remotti, H., Stevens, J.L. 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.