Protein disulfide isomerase-associated 6 is an ATF6-inducible ER stress response protein that protects cardiac myocytes from ischemia/reperfusion-mediated cell death

Journal of Molecular and Cellular Cardiology

Volumn 53, Issue 2, 2012, Pages 259-267

  Vekich, John A ^a   Belmont, Peter J ^a   Thuerauf, Donna J ^a   Glembotski, Christopher C ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

Author keywords

ATF6; Cardiac; ER stress; Ischemia; PDIA6; Protein disulfide isomerase

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; CCAAT BINDING FACTOR; PROTEIN DISULFIDE ISOMERASE; PROTEIN DISULFIDE ISOMERASE ASSOCIATED 6; TAMOXIFEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CATALYSIS; CELL DEATH; CELL PROTECTION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PDIA6 GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; RAT;

ACTIVATING TRANSCRIPTION FACTOR 6; ANIMALS; CELL DEATH; CHROMATIN IMMUNOPRECIPITATION; CHROMATOGRAPHY, LIQUID; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENDOPLASMIC RETICULUM STRESS; IMMUNOBLOTTING; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICRORNAS; MYOCYTES, CARDIAC; PROTEIN DISULFIDE-ISOMERASES; REAL-TIME POLYMERASE CHAIN REACTION; REPERFUSION INJURY; TANDEM MASS SPECTROMETRY;

MUS MUSCULUS;

EID: 84862838703     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2012.05.005     Document Type: Article

References (53)

1. Lee A.S. The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem Sci 2001, 26:504-510.
2. Wu J., Kaufman R.J. From acute ER stress to physiological roles of the unfolded protein response. Cell Death Differ 2006, 13:374-384.
3. Glembotski C.C. Endoplasmic reticulum stress in the heart. Circ Res 2007, 101:975-984.
4. Yoshida H., Haze K., Yanagi H., Yura T., Mori K. 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 1998, 273:33741-33749.
5. Zhu C., Johansen F.E., Prywes R. Interaction of ATF6 and serum response factor. Mol Cell Biol 1997, 17:4957-4966.
6. Yamamoto K., Sato T., Matsui T., Sato M., Okada T., Yoshida H., et al. Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev Cell 2007, 13:365-376.
7. Okada T., Yoshida H., Akazawa R., Negishi M., Mori K. 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 2002, 366:585-594.
8. Belmont P.J., Tadimalla A., Chen W.J., Martindale J.J., Thuerauf D.J., Marcinko M., et al. Coordination of growth and endoplasmic reticulum stress signaling by regulator of calcineurin 1 (RCAN1), a novel ATF6-inducible gene. J Biol Chem 2008, 283:14012-14021.
9. Martindale J.J., Fernandez R., Thuerauf D., Whittaker R., Gude N., Sussman M.A., et al. Endoplasmic reticulum stress gene induction and protection from ischemia/reperfusion injury in the hearts of transgenic mice with a tamoxifen-regulated form of ATF6. Circ Res 2006, 98:1186-1193.
10. Kim I., Xu W., Reed J.C. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 2008, 7:1013-1030.
11. Belmont P.J., Chen W.J., San Pedro M.N., Thuerauf D.J., Gellings Lowe N., Gude N., et al. Roles for endoplasmic reticulum-associated degradation and the novel endoplasmic reticulum stress response gene Derlin-3 in the ischemic heart. Circ Res 2009, 106:307-316.
12. Thuerauf D.J., Marcinko M., Gude N., Rubio M., Sussman M.A., Glembotski C.C. Activation of the unfolded protein response in infarcted mouse heart and hypoxic cultured cardiac myocytes. Circ Res 2006, 99:275-282.
13. Ferrari D.M., Soling H.D. The protein disulphide-isomerase family: unravelling a string of folds. Biochem J 1999, 339(Pt 1):1-10.
14. Tu B.P., Weissman J.S. The FAD- and O(2)-dependent reaction cycle of Ero1-mediated oxidative protein folding in the endoplasmic reticulum. Mol Cell 2002, 10:983-994.
15. Doroudgar S., Thuerauf D.J., Marcinko M.C., Belmont P.J., Glembotski C.C. Ischemia activates the ATF6 branch of the endoplasmic reticulum stress response. J Biol Chem 2009, 284:29735-29745.
16. Azfer A., Niu J., Rogers L.M., Adamski F.M., Kolattukudy P.E. Activation of endoplasmic reticulum stress response during the development of ischemic heart disease. Am J Physiol Heart Circ Physiol 2006, 291:H1411-H1420.
17. Wang M., Ye R., Barron E., Baumeister P., Mao C., Luo S., et al. Essential role of the unfolded protein response regulator GRP78/BiP in protection from neuronal apoptosis. Cell Death Differ 2010, 17:488-498.
18. Toldo S., Severino A., Abbate A., Baldi A. The role of PDI as a survival factor in cardiomyocyte ischemia. Methods Enzymol 2011, 489:47-65.
19. Severino A., Campioni M., Straino S., Salloum F.N., Schmidt N., Herbrand U., et al. Identification of protein disulfide isomerase as a cardiomyocyte survival factor in ischemic cardiomyopathy. J Am Coll Cardiol 2007, 50:1029-1037.
20. Toldo S., Boccellino M., Rinaldi B., Seropian I.M., Mezzaroma E., Severino A., et al. Altered oxido-reductive state in the diabetic heart: loss of cardioprotection due to protein disulfide isomerase. Mol Med 2011, 17:1012-1021.
21. Miyamoto S., Purcell N.H., Smith J.M., Gao T., Whittaker R., Huang K., et al. PHLPP-1 negatively regulates Akt activity and survival in the heart. Circ Res 2010, 107:476-484.
22. Kim N.N., Villarreal F.J., Printz M.P., Lee A.A., Dillmann W.H. Trophic effects of angiotensin II on neonatal rat cardiac myocytes are mediated by cardiac fibroblasts. Am J Physiol 1995, 269:E426-E437.
23. Thuerauf D.J., Morrison L.E., Hoover H., Glembotski C.C. Coordination of ATF6-mediated transcription and ATF6 degradation by a domain that is shared with the viral transcription factor, VP16. J Biol Chem 2002, 277:20734-20739.
24. Shevchenko A., Wilm M., Vorm O., Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 1996, 68:850-858.
25. He T.C., Zhou S., da Costa L.T., Yu J., Kinzler K.W., Vogelstein B. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci U S A 1998, 95:2509-2514.
26. Craig R., Larkin A., Mingo A.M., Thuerauf D.J., Andrews C., McDonough P.M., et al. p38 MAPK and NF-kappa B collaborate to induce interleukin-6 gene expression and release. Evidence for a cytoprotective autocrine signaling pathway in a cardiac myocyte model system. J Biol Chem 2000, 275:23814-23824.
27. Dignam J.D., Lebovitz R.M., Roeder R.G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res 1983, 11:1475-1489.
28. Yoshida H., Okada T., Haze K., Yanagi H., Yura T., Negishi M., 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 2000, 20:6755-6767.
29. Lee A.S., Bell J., Ting J. Biochemical characterization of the 94- and 78-kilodalton glucose-regulated proteins in hamster fibroblasts. J Biol Chem 1984, 259:4616-4621.
30. Munro S., Pelham H.R. A C-terminal signal prevents secretion of luminal ER proteins. Cell 1987, 48:899-907.
31. Kang H.S., Welch W.J. Characterization and purification of the 94-kD glucose-regulated protein. J Biol Chem 1991, 266:5643-5649.
32. Vaux D., Tooze J., Fuller S. Identification by anti-idiotype antibodies of an intracellular membrane protein that recognizes a mammalian endoplasmic reticulum retention signal. Nature 1990, 345:495-502.
33. Tadimalla A., Belmont P.J., Thuerauf D.J., Glassy M.S., Martindale J.J., Gude N., et al. Mesencephalic astrocyte-derived neurotrophic factor is an ischemia-inducible secreted endoplasmic reticulum stress response protein in the heart. Circ Res 2008, 103:1249-1258.
34. Wooden S.K., Li L.J., Navarro D., Qadri I., Pereira L., Lee A.S. Transactivation of the grp78 promoter by malfolded proteins, glycosylation block, and calcium ionophore is mediated through a proximal region containing a CCAAT motif which interacts with CTF/NF-I. Mol Cell Biol 1991, 11:5612-5623.
35. Zhang Y., Chen B., Li Y., Chen J., Lou G., Chen M., et al. Transcriptional regulation of the human PNRC promoter by NFY in HepG2 cells. J Biochem 2008, 143:675-683.
36. Thuerauf D.J., Morrison L., Glembotski C.C. Opposing roles for ATF6alpha and ATF6beta in endoplasmic reticulum stress response gene induction. J Biol Chem 2004, 279:21078-21084.
37. Haze K., Okada T., Yoshida H., Yanagi H., Yura T., Negishi M., 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 2001, 355:19-28.
38. Li M., Baumeister P., Roy B., Phan T., Foti D., Luo S., et al. 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 2000, 20:5096-5106.
39. Thuerauf D.J., Marcinko M., Belmont P.J., Glembotski C.C. Effects of the isoform-specific characteristics of ATF6 alpha and ATF6 beta on endoplasmic reticulum stress response gene expression and cell viability. J Biol Chem 2007, 282:22865-22878.
40. Liu X.M., Peyton K.J., Ensenat D., Wang H., Schafer A.I., Alam J., et al. Endoplasmic reticulum stress stimulates heme oxygenase-1 gene expression in vascular smooth muscle. Role in cell survival. J Biol Chem 2005, 280:872-877.
41. Doroudgar S., Glembotski C.C. The cardiokine story unfolds: ischemic stress-induced protein secretion in the heart. Trends Mol Med 2011, 17:207-214.
42. Bulleid N.J., Ellgaard L. Multiple ways to make disulfides. Trends Biochem Sci 2011, 36:485-492.
43. Kozlov G., Maattanen P., Thomas D.Y., Gehring K. A structural overview of the PDI family of proteins. FEBS J 2010, 277:3924-3936.
44. Hatahet F., Ruddock L.W. Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid Redox Signal 2009, 11:2807-2850.
45. Su A.I., Cooke M.P., Ching K.A., Hakak Y., Walker J.R., Wiltshire T., et al. Large-scale analysis of the human and mouse transcriptomes. Proc Natl Acad Sci U S A 2002, 99:4465-4470.
46. Hatahet F., Ruddock L.W. Substrate recognition by the protein disulfide isomerases. FEBS J 2007, 274:5223-5234.
47. Sorensen B.S., Horsman M.R., Vorum H., Honore B., Overgaard J., Alsner J. Proteins upregulated by mild and severe hypoxia in squamous cell carcinomas in vitro identified by proteomics. Radiother Oncol 2009, 92:443-449.
48. Krajewska M., Xu L., Xu W., Krajewski S., Kress C.L., Cui J., et al. Endoplasmic reticulum protein BI-1 modulates unfolded protein response signaling and protects against stroke and traumatic brain injury. Brain Res 2011, 1370:227-237.
49. Jordan P.A., Stevens J.M., Hubbard G.P., Barrett N.E., Sage T., Authi K.S., et al. A role for the thiol isomerase protein ERP5 in platelet function. Blood 2005, 105:1500-1507.
50. Mellgren R.L. A plasma membrane wound proteome: reversible externalization of intracellular proteins following reparable mechanical damage. J Biol Chem 2010, 285:36597-36607.
51. Kaiser B.K., Yim D., Chow I.T., Gonzalez S., Dai Z., Mann H.H., et al. Disulphide-isomerase-enabled shedding of tumour-associated NKG2D ligands. Nature 2007, 447:482-486.
52. Kimura T., Horibe T., Sakamoto C., Shitara Y., Fujiwara F., Komiya T., et al. Evidence for mitochondrial localization of P5, a member of the protein disulphide isomerase family. J Biochem 2008, 144:187-196.
53. Chin K.T., Kang G., Qu J., Gardner L.B., Coetzee W.A., Zito E., et al. The sarcoplasmic reticulum luminal thiol oxidase ERO1 regulates cardiomyocyte excitation-coupled calcium release and response to hemodynamic load. FASEB J 2011, 25:2583-2591.