Hrd1 and ER-associated protein degradation, ERAD, are critical elements of the adaptive ER stress response in cardiac myocytes

Circulation Research

Volumn 117, Issue 6, 2015, Pages 536-546

  Doroudgar, Shirin ^a   Völkers, Mirko ^a,b,c   Thuerauf, Donna J ^a   Khan, Mohsin ^a,d   Mohsin, Sadia ^a,d   Respress, Jonathan L ^e   Wang, Wei ^e   Gude, Natalie ^a   Müller, Oliver J ^b   Wehrens, Xander H T ^e   Sussman, Mark A ^a   Glembotski, Christopher C ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^d TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

cardiac; endoplasmic reticulum stress; hydroxymethylglutaryl CoA reductases; myocytes; protein folding; proteolysis

Indexed keywords

ATRIAL NATRIURETIC FACTOR; BRAIN NATRIURETIC PEPTIDE; CYCLOHEXIMIDE; DITHIOTHREITOL; DNA NUCLEOTIDYLEXOTRANSFERASE; HYDROXYMETHYL GLUTARYL COENZYME A REDUCTASE DEGRADATION PROTEIN 1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; MYOSIN HEAVY CHAIN BETA; SMALL INTERFERING RNA; THAPSIGARGIN; TUNICAMYCIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; HRD1 PROTEIN, MOUSE; UBIQUITIN PROTEIN LIGASE;

ADENO ASSOCIATED VIRUS; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CELL CULTURE; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENDOPLASMIC RETICULUM STRESS; GENE OVEREXPRESSION; GENE SILENCING; HEART; HEART FUNCTION; HEART LEFT VENTRICLE ENDDIASTOLIC VOLUME; HEART LEFT VENTRICLE ENDSYSTOLIC VOLUME; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; IMMUNOBLOTTING; IN VIVO STUDY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN SYNTHESIS; TUNEL ASSAY; UBIQUITINATION; UPREGULATION; ADAPTATION; ANIMAL; BIOSYNTHESIS; CARDIAC MUSCLE CELL; METABOLISM; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; GENE KNOCKDOWN TECHNIQUES; MICE; MYOCYTES, CARDIAC; RATS; RATS, SPRAGUE-DAWLEY; UBIQUITIN-PROTEIN LIGASES;

EID: 84940552957     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.306993     Document Type: Article

References (53)

1. Balch WE, Morimoto RI, Dillin A, Kelly JW, Adapting proteostasis for disease intervention. Science 2008 319 916 919. doi: 10.1126/science.1141448
2. Glembotski CC, Roles for the sarco-/endoplasmic reticulum in cardiac myocyte contraction, protein synthesis, and protein quality control. Physiology (Bethesda) 2012 27 343 350. doi: 10.1152/physiol.00034.2012
3. Gidalevitz T, Stevens F, Argon Y, Orchestration of secretory protein folding by ER chaperones. Biochim Biophys Acta 2013 1833 2410 2424. doi: 10.1016/j.bbamcr.2013.03.007
4. Amm I, Sommer T, Wolf DH, Protein quality control and elimination of protein waste: the role of the ubiquitin-proteasome system. Biochim Biophys Acta 2014 1843 182 196. doi: 10.1016/j.bbamcr.2013.06.031
5. Guerriero CJ, Brodsky JL, The delicate balance between secreted protein folding and endoplasmic reticulum-associated degradation in human physiology. Physiol Rev 2012 92 537 576. doi: 10.1152/physrev.00027.2011
6. Dickhout JG, Carlisle RE, Austin RC, Interrelationship between cardiac hypertrophy, heart failure, and chronic kidney disease: endoplasmic reticulum stress as a mediator of pathogenesis. Circ Res 2011 108 629 642. doi: 10.1161/CIRCRESAHA.110.226803
7. Minamino T, Komuro I, Kitakaze M, Endoplasmic reticulum stress as a therapeutic target in cardiovascular disease. Circ Res 2010 107 1071 1082. doi: 10.1161/CIRCRESAHA.110.227819
8. Doroudgar S, Glembotski CC, New concepts of endoplasmic reticulum function in the heart: programmed to conserve. J Mol Cell Cardiol 2013 55 85 91. doi: 10.1016/j.yjmcc.2012.10.006
9. Millott R, Dudek E, Michalak M, The endoplasmic reticulum in cardiovascular health and disease. Can J Physiol Pharmacol 2012 90 1209 1217. doi: 10.1139/y2012-058
10. Olzmann JA, Kopito RR, Christianson JC, The mammalian endoplasmic reticulum-associated degradation system. Cold Spring Harb Perspect Biol 2013 5. doi: 10.1101/cshperspect.a013185
11. Walter P, Ron D, The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011 334 1081 1086. doi: 10.1126/science.1209038
12. Brodsky JL, Cleaning up: ER-associated degradation to the rescue. Cell 2012 151 1163 1167. doi: 10.1016/j.cell.2012.11.012
13. Claessen JH, Kundrat L, Ploegh HL, Protein quality control in the ER: balancing the ubiquitin checkbook. Trends Cell Biol 2012 22 22 32. doi: 10.1016/j.tcb.2011.09.010
14. Xu C, Bailly-Maitre B, Reed JC, Endoplasmic reticulum stress: cell life and death decisions. J Clin Invest 2005 115 2656 2664. doi: 10.1172/JCI26373
15. Sano R, Reed JC, ER stress-induced cell death mechanisms. Biochim Biophys Acta 2013 1833 3460 3470. doi: 10.1016/j.bbamcr.2013.06.028
16. Zhu C, Johansen FE, Prywes R, Interaction of ATF6 and serum response factor. Mol Cell Biol 1997 17 4957 4966
17. Haze K, Yoshida H, Yanagi H, Yura T, Mori K, Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell 1999 10 3787 3799
18. Glembotski CC, Roles for ATF6 and the sarco/endoplasmic reticulum protein quality control system in the heart. J Mol Cell Cardiol 2014 71 11 15. doi: 10.1016/j.yjmcc.2013.09.018
19. Lynch JM, Maillet M, Vanhoutte D, A thrombospondin-dependent pathway for a protective ER stress response. Cell 2012 149 1257 1268. doi: 10.1016/j.cell.2012.03.050
20. Belmont PJ, Tadimalla A, Chen WJ, Martindale JJ, Thuerauf DJ, Marcinko M, Gude N, Sussman MA, Glembotski CC, 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. doi: 10.1074/jbc.M709776200
21. Hampton RY, Gardner RG, Rine J, Role of 26S proteasome and HRD genes in the degradation of 3-hydroxy-3-methylglutaryl-CoA reductase, an integral endoplasmic reticulum membrane protein. Mol Biol Cell 1996 7 2029 2044
22. Bordallo J, Plemper RK, Finger A, Wolf DH, Der3p/Hrd1p is required for endoplasmic reticulum-associated degradation of misfolded lumenal and integral membrane proteins. Mol Biol Cell 1998 9 209 222
23. Gardner RG, Swarbrick GM, Bays NW, Cronin SR, Wilhovsky S, Seelig L, Kim C, Hampton RY, Endoplasmic reticulum degradation requires lumen to cytosol signaling. Transmembrane control of Hrd1p by Hrd3p. J Cell Biol 2000 151 69 82
24. Nadav E, Shmueli A, Barr H, Gonen H, Ciechanover A, Reiss Y, A novel mammalian endoplasmic reticulum ubiquitin ligase homologous to the yeast Hrd1. Biochem Biophys Res Commun 2003 303 91 97
25. Kikkert M, Doolman R, Dai M, Avner R, Hassink G, van Voorden S, Thanedar S, Roitelman J, Chau V, Wiertz E, Human HRD1 is an E3 ubiquitin ligase involved in degradation of proteins from the endoplasmic reticulum. J Biol Chem 2004 279 3525 3534. doi: 10.1074/jbc.M307453200
26. Omura T, Kaneko M, Okuma Y, Matsubara K, Nomura Y, Endoplasmic reticulum stress and Parkinson's disease: the role of HRD1 in averting apoptosis in neurodegenerative disease. Oxid Med Cell Longev 2013 2013 239854. doi: 10.1155/2013/239854
27. Hasegawa D, Fujii R, Yagishita N, E3 ubiquitin ligase synoviolin is involved in liver fibrogenesis. PLoS One 2010 5 e13590. doi: 10.1371/journal.pone.0013590
28. Yamasaki S, Yagishita N, Nishioka K, Nakajima T, The roles of synoviolin in crosstalk between endoplasmic reticulum stress-induced apoptosis and p53 pathway. Cell Cycle 2007 6 1319 1323
29. Neutzner A, Neutzner M, Benischke AS, Ryu SW, Frank S, Youle RJ, Karbowski M, A systematic search for endoplasmic reticulum (ER) membrane-associated RING finger proteins identifies Nixin/ZNRF4 as a regulator of calnexin stability and ER homeostasis. J Biol Chem 2011 286 8633 8643. doi: 10.1074/jbc.M110.197459
30. Yu H, Kaung G, Kobayashi S, Kopito RR, Cytosolic degradation of T-cell receptor alpha chains by the proteasome. J Biol Chem 1997 272 20800 20804
31. Olden K, Pratt RM, Jaworski C, Yamada KM, Evidence for role of glycoprotein carbohydrates in membrane transport: specific inhibition by tunicamycin. Proc Natl Acad Sci USA 1979 76 791 795
32. Thastrup O, Cullen PJ, Drøbak BK, Hanley MR, Dawson AP, Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc Natl Acad Sci USA 1990 87 2466 2470
33. Jämsä E, Simonen M, Makarow M, Selective retention of secretory proteins in the yeast endoplasmic reticulum by treatment of cells with a reducing agent. Yeast 1994 10 355 370. doi: 10.1002/yea.320100308
34. Ishikura S, Weissman AM, Bonifacino JS, Serine residues in the cytosolic tail of the T-cell antigen receptor alpha-chain mediate ubiquitination and endoplasmic reticulum-associated degradation of the unassembled protein. J Biol Chem 2010 285 23916 23924. doi: 10.1074/jbc.M110.127936
35. Boecker W, Bernecker OY, Wu JC, Zhu X, Sawa T, Grazette L, Rosenzweig A, del Monte F, Schmidt U, Hajjar RJ, Cardiac-specific gene expression facilitated by an enhanced myosin light chain promoter. Mol Imaging 2004 3 69 75. doi: 10.1162/1535350041464847
36. Müller OJ, Leuchs B, Pleger ST, Grimm D, Franz WM, Katus HA, Kleinschmidt JA, Improved cardiac gene transfer by transcriptional and transductional targeting of adeno-associated viral vectors. Cardiovasc Res 2006 70 70 78. doi: 10.1016/j.cardiores.2005.12.017
37. Völkers M, Konstandin MH, Doroudgar S, Toko H, Quijada P, Din S, Joyo A, Ornelas L, Samse K, Thuerauf DJ, Gude N, Glembotski CC, Sussman MA, Mechanistic target of rapamycin complex 2 protects the heart from ischemic damage. Circulation 2013 128 2132 2144. doi: 10.1161/CIRCULATIONAHA.113.003638
38. Völkers M, Toko H, Doroudgar S, Din S, Quijada P, Joyo AY, Ornelas L, Joyo E, Thuerauf DJ, Konstandin MH, Gude N, Glembotski CC, Sussman MA, Pathological hypertrophy amelioration by PRAS40-mediated inhibition of mTORC1. Proc Natl Acad Sci USA 2013 110 12661 12666. doi: 10.1073/pnas.1301455110
39. Minamino T, Kitakaze M, ER stress in cardiovascular disease. J Mol Cell Cardiol 2010 48 1105 1110. doi: 10.1016/j.yjmcc.2009.10.026
40. Christians ES, Mustafi SB, Benjamin IJ, Chaperones and cardiac misfolding protein diseases. Curr Protein Pept Sci 2014 15 189 204
41. Sandri M, Robbins J, Proteotoxicity: an underappreciated pathology in cardiac disease. J Mol Cell Cardiol 2014 71 3 10. doi: 10.1016/j.yjmcc.2013.12.015
42. Wang X, Robbins J, Proteasomal and lysosomal protein degradation and heart disease. J Mol Cell Cardiol 2014 71 16 24. doi: 10.1016/j.yjmcc.2013.11.006
43. Okada K, Minamino T, Tsukamoto Y, Prolonged endoplasmic reticulum stress in hypertrophic and failing heart after aortic constriction: possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis. Circulation 2004 110 705 712. doi: 10.1161/01.CIR.0000137836.95625.D4
44. Kim SK, Kim YK, Lee AS, Expression of the glucose-regulated proteins (GRP94 and GRP78) in differentiated and undifferentiated mouse embryonic cells and the use of the GRP78 promoter as an expression system in embryonic cells. Differentiation 1990 42 153 159
45. Barnes JA, Smoak IW, Immunolocalization and heart levels of GRP94 in the mouse during post-implantation development. Anat Embryol (Berl) 1997 196 335 341
46. Barnes JA, Smoak IW, Glucose-regulated protein 78 (GRP78) is elevated in embryonic mouse heart and induced following hypoglycemic stress. Anat Embryol (Berl) 2000 202 67 74
47. Mesaeli N, Nakamura K, Zvaritch E, Dickie P, Dziak E, Krause KH, Opas M, MacLennan DH, Michalak M, Calreticulin is essential for cardiac development. J Cell Biol 1999 144 857 868
48. Luo S, Mao C, Lee B, Lee AS, GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Mol Cell Biol 2006 26 5688 5697. doi: 10.1128/MCB.00779-06
49. Yang Y, Liu B, Dai J, Srivastava PK, Zammit DJ, Lefrançois L, Li Z, Heat shock protein gp96 is a master chaperone for toll-like receptors and is important in the innate function of macrophages. Immunity 2007 26 215 226. doi: 10.1016/j.immuni.2006.12.005
50. Amano T, Yamasaki S, Yagishita N, Synoviolin/Hrd1, an E3 ubiquitin ligase, as a novel pathogenic factor for arthropathy. Genes Dev 2003 17 2436 2449. doi: 10.1101/gad.1096603
51. Martindale JJ, Fernandez R, Thuerauf D, Whittaker R, Gude N, Sussman MA, Glembotski CC, 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. doi: 10.1161/01.RES.0000220643.65941.8d
52. Thuerauf DJ, Marcinko M, Gude N, Rubio M, Sussman MA, Glembotski CC, Activation of the unfolded protein response in infarcted mouse heart and hypoxic cultured cardiac myocytes. Circ Res 2006 99 275 282. doi: 10.1161/01.RES.0000233317.70421.03
53. Wang ZV, Deng Y, Gao N, Spliced X-box binding protein 1 couples the unfolded protein response to hexosamine biosynthetic pathway. Cell 2014 156 1179 1192. doi: 10.1016/j.cell.2014.01.014