Endoplasmic Reticulum Stress and the Unfolded Protein Response

Clinics in Liver Disease

Volumn 13, Issue 4, 2009, Pages 581-590

  Kapoor, Ashwani ^a   Sanyal, Arun J ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

ER stress; Eukaryotic initiation factor; Fatty liver; Inflammation; Metabolic syndrome; Non alcoholic fatty liver disease; Non alcoholic steatohepatitis; Unfolded protein response

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; ADENOSINE TRIPHOSPHATE; CHAPERONE; GLUCOSE REGULATED PROTEIN; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INOSITOL REQUIRING ENZYME 1; MEMBRANE PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PKR LIKE MITOGEN ACTIVATED PROTEIN KINASE; PROTEASOME; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; UNCLASSIFIED DRUG;

APOPTOSIS; CELL FUNCTION; CELL ORGANELLE; CELLULAR DISTRIBUTION; CELLULAR STRESS RESPONSE; DISEASE COURSE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HOMEOSTASIS; HUMAN; LIVER CIRRHOSIS; NONALCOHOLIC FATTY LIVER; PHENOTYPE; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTEIN TARGETING; REVIEW;

ANIMALS; APOPTOSIS; ENDOPLASMIC RETICULUM; FATTY LIVER; HUMANS; PROTEIN FOLDING; UNFOLDED PROTEIN RESPONSE;

EID: 70349768065     PISSN: 10893261     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cld.2009.07.004     Document Type: Review

References (58)

1. Anfinsen C.B. Principles that govern the folding of protein chains. Science 181 (1973) 223-230
2. Shamu C.E., Cox J.S., and Walter P. The unfolded-protein-response pathway in yeast. Trends Cell Biol 4 (Feb 1994) 56-60
3. Brostrom M.A., Prostko C.R., Gmitter D., et al. Independent signaling of grp78 gene transcription and phosphorylation of eukaryotic initiator factor 2 alpha by the stressed endoplasmic reticulum. J Biol Chem 270 (1995) 4127-4132
4. Feng B., Yao P.M., Li Y., et al. The endoplasmic reticulum is the site of cholesterol-induced cytotoxicity in macrophages. Nat Cell Biol 5 (2003) 781-792
5. Gomez E., Powell M.L., Bevington A., et al. A decrease in cellular energy status stimulates PERK-dependent eIF2alpha phosphorylation and regulates protein synthesis in pancreatic beta-cells. Biochem J 410 (2008) 485-493
6. Su H.L., Liao C.L., and Lin Y.L. Japanese encephalitis virus infection initiates endoplasmic reticulum stress and an unfolded protein response. J Virol 76 (2002) 4162-4171
7. Yacoub Wasef S.Z., Robinson K.A., Berkaw M.N., et al. Glucose, dexamethasone, and the unfolded protein response regulate TRB3 mRNA expression in 3T3-L1 adipocytes and L6 myotubes. Am J Physiol Endocrinol Metab 291 (2006) E1274-E1280
8. Bertolotti A., Zhang Y., Hendershot L.M., et al. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2 (2000) 326-332
9. Liu C.Y., Schroder M., and Kaufman R.J. Ligand-independent dimerization activates the stress response kinases IRE1 and PERK in the lumen of the endoplasmic reticulum. J Biol Chem 275 (2000) 24881-24885
10. Harding H.P., Zhang Y., Bertolotti A., et al. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 5 (2000) 897-904
11. Scheuner D., Song B., McEwen E., et al. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 7 (2001) 1165-1176
12. Hinnebusch A.G. The eIF-2 alpha kinases: regulators of protein synthesis in starvation and stress. Semin Cell Biol 5 (1994) 417-426
13. Novoa I., Zeng H., Harding H.P., et al. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J Cell Biol 153 (2001) 1011-1022
14. van Huizen R., Martindale J.L., Gorospe M., et al. P58IPK, a novel endoplasmic reticulum stress-inducible protein and potential negative regulator of eIF2alpha signaling. J Biol Chem 278 (2003) 15558-15564
15. Dinkova-Kostova A.T., Holtzclaw W.D., Cole R.N., et al. Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc Natl Acad Sci U S A 99 (2002) 11908-11913
16. Cullinan S.B., Zhang D., Hannink M., et al. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol Cell Biol 23 (2003) 7198-7209
17. Haze K., Okada T., Yoshida H., et al. 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 (2001) 19-28
18. Yoshida H., Okada T., Haze K., et al. 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 (2000) 6755-6767
19. Ye J., Rawson R.B., Komuro R., et al. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell 6 (2000) 1355-1364
20. Yoshida H., Matsui T., Yamamoto A., et al. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107 (2001) 881-891
21. Wang X.Z., Harding H.P., Zhang Y., et al. Cloning of mammalian Ire1 reveals diversity in the ER stress responses. EMBO J 17 (1998) 5708-5717
22. Yoshida H. Unconventional splicing of XBP-1 mRNA in the unfolded protein response. Antioxid Redox Signal 9 (2007) 2323-2333
23. Kostova Z., Tsai Y.C., and Weissman A.M. Ubiquitin ligases, critical mediators of endoplasmic reticulum-associated degradation. Semin Cell Dev Biol 18 6 (2007) 770-779
24. Lippincott-Schwartz J., Bonifacino J.S., Yuan L.C., et al. Degradation from the endoplasmic reticulum: disposing of newly synthesized proteins. Cell 54 (1988) 209-220
25. Hirao K., Natsuka Y., Tamura T., et al. EDEM3, a soluble EDEM homolog, enhances glycoprotein endoplasmic reticulum-associated degradation and mannose trimming. J Biol Chem 281 (2006) 9650-9658
26. Hosokawa N., Tremblay L.O., You Z., et al. Enhancement of endoplasmic reticulum (ER) degradation of misfolded Null Hong Kong alpha1-antitrypsin by human ER mannosidase I. J Biol Chem 278 (2003) 26287-26294
27. Mast S.W., Diekman K., Karaveg K., et al. Human EDEM2, a novel homolog of family 47 glycosidases, is involved in ER-associated degradation of glycoproteins. Glycobiology 15 (2005) 421-436
28. Urano F., Wang X., Bertolotti A., et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287 (2000) 664-666
29. Adler V., Schaffer A., Kim J., et al. UV irradiation and heat shock mediate JNK activation via alternate pathways. J Biol Chem 270 (1995) 26071-26077
30. Wang X.Z., Kuroda M., Sok J., et al. Identification of novel stress-induced genes downstream of chop. EMBO J 17 (1998) 3619-3630
31. Yan W., Frank C.L., Korth M.J., et al. Control of PERK eIF2alpha kinase activity by the endoplasmic reticulum stress-induced molecular chaperone P58IPK. Proc Natl Acad Sci U S A 99 (2002) 15920-15925
32. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell 103 (2000) 239-252
33. Morishima N., Nakanishi K., Takenouchi H., et al. An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J Biol Chem 277 (2002) 34287-34294
34. Nakagawa T., Zhu H., Morishima N., et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403 (2000) 98-103
35. Wang D., Wei Y., and Pagliassotti M.J. Saturated fatty acids promote endoplasmic reticulum stress and liver injury in rats with hepatic steatosis. Endocrinology 147 (2006) 943-951
36. Schattenberg J.M., Singh R., Wang Y., et al. JNK1 but not JNK2 promotes the development of steatohepatitis in mice. Hepatology 43 (2006) 163-172
37. Ji C., Shinohara M., Kuhlenkamp J., et al. Mechanisms of protection by the betaine-homocysteine methyltransferase/betaine system in HepG2 cells and primary mouse hepatocytes. Hepatology 46 (2007) 1586-1596
38. Puri P., Baillie R.A., Wiest M.M., et al. A lipidomic analysis of nonalcoholic fatty liver disease. Hepatology 46 (2007) 1081-1090
39. Sanyal A.J., Campbell-Sargent C., Mirshahi F., et al. Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities. Gastroenterology 120 (2001) 1183-1192
40. Seki S., Kitada T., and Sakaguchi H. Clinicopathological significance of oxidative cellular damage in non-alcoholic fatty liver diseases. Hepatol Res 33 (2005) 132-134
41. Puri P., Mirshahi F., Cheung O., et al. Activation and dysregulation of the unfolded protein response in nonalcoholic fatty liver disease. Gastroenterology 134 (2008) 568-576
42. Donnelly K.L., Smith C.I., Schwarzenberg S.J., et al. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J Clin Invest 115 (2005) 1343-1351
43. Diraison F., Moulin P., and Beylot M. Contribution of hepatic de novo lipogenesis and reesterification of plasma non esterified fatty acids to plasma triglyceride synthesis during nonalcoholic fatty liver disease. Diabetes Metab 29 (2003) 478-485
44. Brown M.S., and Goldstein J.L. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89 (1997) 331-340
45. Schultz J.R., Tu H., Luk A., et al. Role of LXRs in control of lipogenesis. Genes Dev 14 (2000) 2831-2838
46. Shimomura I., Bashmakov Y., and Horton J.D. Increased levels of nuclear SREBP-1c associated with fatty livers in two mouse models of diabetes mellitus. J Biol Chem 274 (1999) 30028-30032
47. Horton J.D., Shah N.A., Warrington J.A., et al. Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes. Proc Natl Acad Sci U S A 100 (2003) 12027-12032
48. Lange Y., and Steck T.L. Cholesterol homeostasis and the escape tendency (activity) of plasma membrane cholesterol. Prog Lipid Res 47 (2008) 319-332
49. Lee A.H., Scapa E.F., Cohen D.E., et al. Regulation of hepatic lipogenesis by the transcription factor XBP1. Science 320 (2008) 1492-1496
50. Devries-Seimon T., Li Y., Yao P.M., et al. Cholesterol-induced macrophage apoptosis requires ER stress pathways and engagement of the type A scavenger receptor. J Cell Biol 171 (2005) 61-73
51. Feldstein A.E., Canbay A., Angulo P., et al. Hepatocyte apoptosis and fas expression are prominent features of human nonalcoholic steatohepatitis. Gastroenterology 125 (2003) 437-443
52. Ribeiro P.S., Cortez-Pinto H., Sola S., et al. Hepatocyte apoptosis, expression of death receptors, and activation of NF-kappaB in the liver of nonalcoholic and alcoholic steatohepatitis patients. Am J Gastroenterol 99 (2004) 1708-17017
53. Weston C.R., and Davis R.J. The JNK signal transduction pathway. Curr Opin Cell Biol 19 (2007) 142-149
54. Matsukawa J., Matsuzawa A., Takeda K., et al. The ASK1-MAP kinase cascades in mammalian stress response. J Biochem 136 (2004) 261-265
55. Aguirre V., Werner E.D., Giraud J., et al. Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J Biol Chem 277 (2002) 1531-1537
56. White M.F. Insulin signaling in health and disease. Science 302 (2003) 1710-1711
57. Marra F. Hepatic stellate cells and the regulation of liver inflammation. J Hepatol 31 (1999) 1120-1130
58. Stumptner C., Fuchsbichler A., Lehner M., et al. Sequence of events in the assembly of Mallory body components in mouse liver: clues to the pathogenesis and significance of Mallory body formation. J Hepatol 34 (2001) 665-675