Journal of Molecular and Cellular Cardiology
Volume 44, Issue 3 , Pages 453-459 , March 2008

The role of the unfolded protein response in the heart

Received 1 August 2007 ,Revised 14 October 2007 ,Accepted 18 October 2007.

References 

  1. Blobel G. Protein targeting. Biosci Rep. Oct 2000;20(5):303–344
  2. Wang X, Robbins J. Heart failure and protein quality control. Circ Res. Dec 8 2006;99(12):1315–1328
  3. Patterson C, Ike C, Willis PWt, Stouffer GA, Willis MS. The bitter end: the ubiquitin-proteasome system and cardiac dysfunction. Circulation. Mar 20 2007;115(11):1456–1463
  4. Drummond IA, Lee AS, Resendez E, Steinhardt RA. Depletion of intracellular calcium stores by calcium ionophore A23187 induces the genes for glucose-regulated proteins in hamster fibroblasts. J Biol Chem. Sep 15 1987;262(26):12801–12805
  5. Lee AS. Mammalian stress response: induction of the glucose-regulated protein family. Curr Opin Cell Biol. Apr 1992;4(2):267–273
  6. Shamu CE, Cox JS, Walter P. The unfolded-protein-response pathway in yeast. Trends Cell Biol. Feb 1994;4(2):56–60
  7. McMillan DR, Gething MJ, Sambrook J. The cellular response to unfolded proteins: intercompartmental signaling. Curr Opin Biotechnol. Oct 1994;5(5):540–545
  8. Kim YK, Lee AS. Transcriptional activation of the glucose-regulated protein genes and their heterologous fusion genes by beta-mercaptoethanol. Mol Cell Biol. Aug 1987;7(8):2974–2976
  9. Kozutsumi Y, Segal M, Normington K, Gething MJ, Sambrook J. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature. Mar 31 1988;332(6163):462–464
  10. Dorner AJ, Wasley LC, Raney P, Haugejorden S, Green M, Kaufman RJ. The stress response in Chinese hamster ovary cells. Regulation of ERp72 and protein disulfide isomerase expression and secretion. J Biol Chem. Dec 15 1990;265(35):22029–22034
  11. Chang SC, Wooden SK, Nakaki T, Kim YK, Lin AY, Kung L, et al. Rat gene encoding the 78-kDa glucose-regulated protein GRP78: its regulatory sequences and the effect of protein glycosylation on its expression. Proc Natl Acad Sci U S A. Feb 1987;84(3):680–684
  12. Shi Y, Vattem KM, Sood R, An J, Liang J, Stramm L, et al. Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol Cell Biol. Dec 1998;18(12):7499–7509
  13. Zhu C, Johansen FE, Prywes R. Interaction of ATF6 and serum response factor. Mol Cell Biol. Sep 1997;17(9):4957–4966
  14. 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. Dec 11 1998;273(50):33741–33749
  15. Cox JS, Shamu CE, Walter P. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell. Jun 18 1993;73(6):1197–1206
  16. Mori K, Ma W, Gething MJ, Sambrook J. A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell. Aug 27 1993;74(4):743–756
  17. Kohno K. How transmembrane proteins sense endoplasmic reticulum stress. Antioxid Redox Signal. Oct 2007;179(1):75–86
  18. Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol. Jun 2000;2(6):326–332
  19. Ma K, Vattem KM, Wek RC. Dimerization and release of molecular chaperone inhibition facilitate activation of eukaryotic initiation factor-2 kinase in response to endoplasmic reticulum stress. J Biol Chem. May 24 2002;277(21):18728–18735
  20. Shamu CE, Walter P. Oligomerization and phosphorylation of the Ire1p kinase during intracellular signaling from the endoplasmic reticulum to the nucleus. EMBO J. Jun 17 1996;15(12):3028–3039
  21. Sidrauski C, Walter P. The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell. Sep 19 1997;90(6):1031–1039
  22. Shen J, Snapp EL, Lippincott-Schwartz J, Prywes R. Stable binding of ATF6 to BiP in the endoplasmic reticulum stress response. Mol Cell Biol. Feb 2005;25(3):921–932
  23. Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature. Jan 21 1999;397(6716):271–274
  24. Calfon M, Zeng H, Urano F, Till JH, Hubbard SR, Harding HP, et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature. Jan 3 2002;415(6867):92–96
  25. Shen J, Chen X, Hendershot L, Prywes R. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell. Jul 2002;3(1):99–111
  26. Ye J, Rawson RB, Komuro R, Chen X, Dave UP, Prywes R, et al. ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol Cell. Dec 2000;6(6):1355–1364
  27. 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. Apr 1 2001;355(Pt 1):19–28
  28. Kondo S, Murakami T, Tatsumi K, Ogata M, Kanemoto S, Otori K, et al. OASIS, a CREB/ATF-family member, modulates UPR signalling in astrocytes. Nat Cell Biol. Feb 2005;7(2):186–194
  29. Lu R, Yang P, O'Hare P, Misra V. Luman, a new member of the CREB/ATF family, binds to herpes simplex virus VP16-associated host cellular factor. Mol Cell Biol. Sep 1997;17(9):5117–5126
  30. DenBoer LM, Hardy-Smith PW, Hogan MR, Cockram GP, Audas TE, Lu R. Luman is capable of binding and activating transcription from the unfolded protein response element. Biochem Biophys Res Commun. May 27 2005;331(1):113–119
  31. Stirling J, O'Hare P. CREB4, a transmembrane bZip transcription factor and potential new substrate for regulation and cleavage by S1P. Mol Biol Cell. Jan 2006;17(1):413–426
  32. Kondo S, Saito A, Hino S, Murakami T, Ogata M, Kanemoto S, et al. BBF2H7, a novel transmembrane bZIP transcription factor, is a new type of endoplasmic reticulum stress transducer. Mol Cell Biol. Mar 2007;27(5):1716–1729
  33. Wu J, Rutkowski DT, Dubois M, Swathirajan J, Saunders T, Wang J, et al. ATF6alpha optimizes long-term endoplasmic reticulum function to protect cells from chronic stress. Dev Cell. Sep 2007;13(3):351–364
  34. Thuerauf DJ, Morrison L, Glembotski CC. Opposing roles for ATF6alpha and ATF6beta in endoplasmic reticulum stress response gene induction. J Biol Chem. May 14 2004;279(20):21078–21084
  35. Thuerauf DJ, Marcinko M, Belmont PJ, Glembotski CC. 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. Aug 3 2007;282(31):22865–22878
  36. Brodsky JL. The protective and destructive roles played by molecular chaperones during ERAD (endoplasmic-reticulum-associated degradation). Biochem J. Jun 15 2007;404(3):353–363
  37. Meusser B, Hirsch C, Jarosch E, Sommer T. ERAD: the long road to destruction. Nat Cell Biol. Aug 2005;7(8):766–772
  38. Lord JM, Roberts LM, Stirling CJ. Quality control: another player joins the ERAD cast. Curr Biol. Dec 6 2005;15(23):R963–R964
  39. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, Harding HP, et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science. Jan 28 2000;287(5453):664–666
  40. Yoneda T, Imaizumi K, Oono K, Yui D, Gomi F, Katayama T, et al. 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. Apr 27 2001;276(17):13935–13940
  41. Hacki J, Egger L, Monney L, Conus S, Rosse T, Fellay I, et al. Apoptotic crosstalk between the endoplasmic reticulum and mitochondria controlled by Bcl-2. Oncogene. May 4 2000;19(19):2286–2295
  42. Hetz C, Bernasconi P, Fisher J, Lee AH, Bassik MC, Antonsson B, et al. Proapoptotic BAX and BAK modulate the unfolded protein response by a direct interaction with IRE1alpha. Science. Apr 28 2006;312(5773):572–576
  43. 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. Nov 1999;10(11):3787–3799
  44. Wang Y, Shen J, Arenzana N, Tirasophon W, Kaufman RJ, Prywes R. Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response. J Biol Chem. Sep 1 2000;275(35):27013–27020
  45. Thuerauf DJ, Hoover H, Meller J, Hernandez J, Su L, Andrews C, et al. Sarco/endoplasmic reticulum calcium ATPase-2 expression is regulated by ATF6 during the endoplasmic reticulum stress response: intracellular signaling of calcium stress in a cardiac myocyte model system. J Biol Chem. Dec 21 2001;276(51):48309–48317
  46. Rao RV, Peel A, Logvinova A, del Rio G, Hermel E, Yokota T, et al. Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperone GRP78. FEBS Lett. Mar 13 2002;514(2–3):122–128
  47. Shiu RP, Pouyssegur J, Pastan I. Glucose depletion accounts for the induction of two transformation-sensitive membrane proteins in Rous sarcoma virus-transformed chick embryo fibroblasts. Proc Natl Acad Sci U S A. Sep 1977;74(9):3840–3844
  48. Welch WJ, Garrels JI, Thomas GP, Lin JJ, Feramisco JR. Biochemical characterization of the mammalian stress proteins and identification of two stress proteins as glucose- and Ca2+-ionophore-regulated proteins. J Biol Chem. Jun 10 1983;258(11):7102–7111
  49. Gorlach A, Klappa P, Kietzmann T. The endoplasmic reticulum: folding, calcium homeostasis, signaling, and redox control. Antioxid Redox Signal. Sep–Oct 2006;8(9–10):1391–1418
  50. Paschen W. Endoplasmic reticulum dysfunction in brain pathology: critical role of protein synthesis. Curr Neurovasc Res. Apr 2004;1(2):173–181
  51. Hayashi T, Saito A, Okuno S, Ferrand-Drake M, Chan PH. Induction of GRP78 by ischemic preconditioning reduces endoplasmic reticulum stress and prevents delayed neuronal cell death. J Cereb Blood Flow Metab. Aug 2003;23(8):949–961
  52. Vikman P, Edvinsson L. Gene expression profiling in the human middle cerebral artery after cerebral ischemia. Eur J Neurol. Dec 2006;13(12):1324–1332
  53. Bi M, Naczki C, Koritzinsky M, Fels D, Blais J, Hu N, et al. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J. Oct 5 2005;24(19):3470–3481
  54. Koumenis C. ER stress, hypoxia tolerance and tumor progression. Curr Mol Med. Feb 2006;6(1):55–69
  55. Feldman DE, Chauhan V, Koong AC. The unfolded protein response: a novel component of the hypoxic stress response in tumors. Mol Cancer Res. Nov 2005;3(11):597–605
  56. 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. Aug 4 2006;99(3):275–282
  57. Qi X, Vallentin A, Churchill E, Mochly-Rosen D. deltaPKC participates in the endoplasmic reticulum stress-induced response in cultured cardiac myocytes and ischemic heart. J Mol Cell Cardiol. Oct 2007;43(4):420–428
  58. Azfer A, Niu J, Rogers LM, Adamski FM, Kolattukudy PE. Activation of endoplasmic reticulum stress response during the development of ischemic heart disease. Am J Physiol Heart Circ Physiol. Sep 2006;291(3):H1411–H1420
  59. Severino A, Campioni M, Straino S, Salloum FN, Schmidt N, Herbrand U, et al. Identification of protein disulfide isomerase as a cardiomyocyte survival factor in ischemic cardiomyopathy. J Am Coll Cardiol. Sep 11 2007;50(11):1029–1037
  60. Terai K, Hiramoto Y, Masaki M, Sugiyama S, Kuroda T, Hori M, et al. AMP-activated protein kinase protects cardiomyocytes against hypoxic injury through attenuation of endoplasmic reticulum stress. Mol Cell Biol. Nov 2005;25(21):9554–9575
  61. Szegezdi E, Duffy A, O'Mahoney ME, Logue SE, Mylotte LA, O'Brien T, et al. ER stress contributes to ischemia-induced cardiomyocyte apoptosis. Biochem Biophys Res Commun. Nov 3 2006;349(4):1406–1411
  62. Martindale JJ, Fernandez R, Thuerauf D, Whittaker R, Gude N, Sussman MA, 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. May 12 2006;98(9):1186–1193
  63. Shintani-Ishida K, Nakajima M, Uemura K, Yoshida K. Ischemic preconditioning protects cardiomyocytes against ischemic injury by inducing GRP78. Biochem Biophys Res Commun. Jul 14 2006;345(4):1600–1605
  64. Zhang PL, Lun M, Teng J, Huang J, Blasick TM, Yin L, et al. Preinduced molecular chaperones in the endoplasmic reticulum protect cardiomyocytes from lethal injury. Ann Clin Lab Sci. Autumn 2004;34(4):449–457
  65. Vitadello M, Penzo D, Petronilli V, Michieli G, Gomirato S, Menabo R, et al. Overexpression of the stress protein Grp94 reduces cardiomyocyte necrosis due to calcium overload and simulated ischemia. FASEB J. May 2003;17(8):923–925
  66. Takagi H, Matsui Y, Sadoshima J. The role of autophagy in mediating cell survival and death during ischemia and reperfusion in the heart. Antioxid Redox Signal. Sep 2007;9(9):1373–1381
  67. Nickson P, Toth A, Erhardt P. PUMA is critical for neonatal cardiomyocyte apoptosis induced by endoplasmic reticulum stress. Cardiovasc Res. Jan 1 2007;73(1):48–56
  68. Toth A, Jeffers JR, Nickson P, Min JY, Morgan JP, Zambetti GP, et al. Targeted deletion of Puma attenuates cardiomyocyte death and improves cardiac function during ischemia–reperfusion. Am J Physiol Heart Circ Physiol. Jul 2006;291(1):H52–H60
  69. Rutkowski DT, Arnold SM, Miller CN, Wu J, Li J, Gunnison KM, et al. Adaptation to ER stress is mediated by differential stabilities of pro-survival and pro-apoptotic mRNAs and proteins. PLoS Biol. Nov 2006;4(11):e374
  70. Okada K, Minamino T, Tsukamoto Y, Liao Y, Tsukamoto O, Takashima S, et al. Prolonged endoplasmic reticulum stress in hypertrophic and failing heart after aortic constriction: possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis. Circulation. Aug 10 2004;110(6):705–712
  71. Hamada H, Suzuki M, Yuasa S, Mimura N, Shinozuka N, Takada Y, et al. Dilated cardiomyopathy caused by aberrant endoplasmic reticulum quality control in mutant KDEL receptor transgenic mice. Mol Cell Biol. Sep 2004;24(18):8007–8017
  72. Barnes JA, Smoak IW. Glucose-regulated protein 78 (GRP78) is elevated in embryonic mouse heart and induced following hypoglycemic stress. Anat Embryol (Berl). Jul 2000;202(1):67–74
  73. Mao C, Tai WC, Bai Y, Poizat C, Lee AS. In vivo regulation of Grp78/BiP transcription in the embryonic heart: role of the endoplasmic reticulum stress response element and GATA-4. J Biol Chem. Mar 31 2006;281(13):8877–8887
  74. Masaki T, Yoshida M, Noguchi S. Targeted disruption of CRE-binding factor TREB5 gene leads to cellular necrosis in cardiac myocytes at the embryonic stage. Biochem Biophys Res Commun. Aug 2 1999;261(2):350–356

PII: S0022-2828(07)01283-7

doi: 10.1016/j.yjmcc.2007.10.017

Journal of Molecular and Cellular Cardiology
Volume 44, Issue 3 , Pages 453-459 , March 2008

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