Proteostasis and REDOX state in the heart

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 302, Issue 1, 2012, Pages

  Christians, Elisabeth S ^a   Benjamin, Ivor J ^a,b  

^a Division of Cardiology   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiac proteome; Chaperone; Glutathione; Heart disease; Nicotinamide adenine dinucleotide phosphate; Reduction oxidation state; Stress response

Indexed keywords

AMINO ACID; BORTEZOMIB; CALCIUM ION; CELASTROL; CHAPERONE; DOXORUBICIN; GLUTAREDOXIN; HEAT SHOCK PROTEIN; HYPOXIA INDUCIBLE FACTOR; MESSENGER RNA; PEROXIREDOXIN; PROTEIN DISULFIDE ISOMERASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; RESVERATROL; TEPRENONE; THIOREDOXIN; X BOX BINDING PROTEIN 1;

ANTIOXIDANT ACTIVITY; ARTICLE; CALCIUM HOMEOSTASIS; CARDIOVASCULAR DISEASE; CELL DIFFERENTIATION; CELL NUCLEUS; CELL VOLUME; CELLULAR STRESS RESPONSE; CYTOSOL; DISULFIDE BOND; ELECTRON SPIN RESONANCE; ENDOPLASMIC RETICULUM STRESS; HEART CONTRACTION; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART SIZE; HEART VENTRICLE HYPERTROPHY; HUMAN; LYSOSOME; MITOCHONDRION; MORBIDITY; MORTALITY; NITROSYLATION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CARBONYLATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEIN PROCESSING; PROTEIN SYNTHESIS; REPERFUSION INJURY; RNA TRANSLATION; SARCOMERE; STEADY STATE; TURNOVER TIME; WESTERN BLOTTING;

ANIMALS; HEART DISEASES; HOMEOSTASIS; HUMANS; MUSCLE PROTEINS; MYOCARDIAL CONTRACTION; MYOCARDIUM; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN CONFORMATION; PROTEIN FOLDING; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84255167180     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00903.2011     Document Type: Article

References (116)

1. Abel ED, Doenst T. Mitochondrial adaptations to physiological vs. pathological cardiac hypertrophy. Cardiovasc Res 90: 234-242, 2011.
2. Ago T, Liu T, Zhai P, Chen W, Li H, Molkentin JD, Vatner SF, Sadoshima J. A redox-dependent pathway for regulating class II HDACs and cardiac hypertrophy. Cell 133: 978-993, 2008.
3. Ago T, Kuroda J, Pain J, Fu C, Li H, Sadoshima J. Upregulation of Nox4 by hypertrophic stimuli promotes apoptosis and mitochondrial dysfunction in cardiac myocytes. Circ Res 106: 1253-1264, 2010.
4. Ago T, Kuroda J, Kamouchi M, Sadoshima J, Kitazono T. Pathophysiological roles of NADPH oxidase/nox family proteins in the vascular system. Circ J 75: 1791-1800, 2011.
5. Ahn SG, Thiele DJ. Redox regulation of mammalian heat shock factor 1 is essential for Hsp gene activation and protection from stress. Genes Dev 17: 516-528, 2003.
6. Ali YO, McCormack R, Darr A, Zhai RG. Nicotinamide mononucleotide adenylyltransferase is a stress response protein regulated by the heat shock factor/hypoxia-inducible factor 1a pathway. J Biol Chem 286: 19089-19099, 2011.
7. Aon MA, Cortassa S, O'Rourke B. Redox-optimized ROS balance: a unifying hypothesis. Biochim Biophys Acta 1797: 865-877, 2010.
8. Benjamin IJ, McMillan DR. Stress (heat shock) proteins: molecular chaperones in cardiovascular biology and disease. Circ Res 83: 117-132, 1998.
9. Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabe-Heider F, Walsh S, Zupicich J, Alkass K, Buchholz BA, Druid H, Jovinge S, Frisén J. Evidence for cardiomyocyte renewal in humans. Science 324: 98-102, 2009.
10. Bezstarosti K, Das S, Lamers JM, Das DK. Differential proteomic profiling to study the mechanism of cardiac pharmacological preconditioning by resveratrol. J Cell Mol Med 10: 896-907, 2006.
11. Bjelakovic G, Nikolova D, Gluud LL, Simonetti RG, Gluud C. Mortality in randomized trials of antioxidant supplements for primary and secondary prevention: systematic review and meta-analysis. JAMA 297: 842-857, 2007.
12. Boateng SY, Belin RJ, Geenen DL, Margulies KB, Martin JL, Hoshijima M, de Tombe PP, Russell B. Cardiac dysfunction and heart failure are associated with abnormalities in the subcellular distribution and amounts of oligomeric muscle LIM protein. Am J Physiol Heart Circ Physiol 292: H259-H269, 2007.
13. Boateng SY, Goldspink PH. Assembly and maintenance of the sarcomere night and day. Cardiovasc Res 77: 667-675, 2008.
14. Brady JP, Garland DL, Green DE, Tamm ER, Giblin FJ, Wawrousek EF. AlphaB-crystallin in lens development and muscle integrity: a gene knockout approach. Invest Ophthalmol Vis Sci 42: 2924-2934, 2001.
15. Brewer AC, Murray TV, Arno M, Zhang M, Anilkumar NP, Mann GE, Shah AM. Nox4 regulates Nrf2 and glutathione redox in cardio-myocytes in vivo. Free Radic Biol Med 51: 205-215, 2011.
16. Bukowska A, Schild L, Keilhoff G, Hirte D, Neumann M, Garde-mann A, Neumann KH, Rohl FW, Huth C, Goette A, Lendeckel U. Mitochondrial dysfunction and redox signaling in atrial tachyarrhythmia. Exp Biol Med (Maywood) 233: 558-574, 2008.
17. Canton M, Menazza S, Sheeran FL, Polverino de Laureto P, Di Lisa F, Pepe S. Oxidation of myofibrillar proteins in human heart failure. J Am Coll Cardiol 57: 300-309, 2011.
18. Christians ES, Benjamin IJ. The stress or heat shock (HS) response: insights from transgenic mouse models. Methods 35: 170-175, 2005.
19. Cullinan SB, Zhang D, Hannink M, Arvisais E, Kaufman RJ, Diehl JA. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol Cell Biol 23: 7198-7209, 2003.
20. De Rosa S, Cirillo P, Paglia A, Sasso L, di Palma V, Chiariello M. Reactive oxygen species and antioxidants in the pathophysiology of cardiovascular disease: does the actual knowledge justify a clinical approach? Curr Vasc Pharmacol 8: 259-275, 2010.
21. Delogu G, Signore M, Mechelli A, Famularo G. Heat shock proteins and their role in heart injury. Curr Opin Crit Care 8: 411-416, 2002.
22. Divald A, Powell SR. Proteasome mediates removal of proteins oxidized during myocardial ischemia. Free Radic Biol Med 40: 156-164, 2006.
23. Divald A, Kivity S, Wang P, Hochhauser E, Roberts B, Teichberg S, Gomes AV, Powell SR. Myocardial ischemic preconditioning preserves postischemic function of the 26S proteasome through diminished oxida-tive damage to 19S regulatory particle subunits. Circ Res 106: 1829- 1838, 2010.
24. Diviani D, Dodge-Kafka KL, Li J, Kapiloff MS. A-kinase anchoring proteins: scaffolding proteins in the heart. Am J Physiol Heart Circ Physiol 301: H1742-H1753, 2011.
25. Dorn GW 2nd, Scorrano L. Two close, too close: sarcoplasmic retic-ulum-mitochondrial crosstalk and cardiomyocyte fate. Circ Res 107: 689-699, 2010.
26. Dreiza CM, Komalavilas P, Furnish EJ, Flynn CR, Sheller MR, Smoke CC, Lopes LB, Brophy CM. The small heat shock protein, HSPB6, in muscle function and disease. Cell Stress Chaperones 15: 1-11, 2010.
27. Edwards HV, Cameron RT, Baillie GS. The emerging role of HSP20 as a multifunctional protective agent. Cell Signal 23: 1447-1454, 2011.
28. Fan GC, Ren X, Qian J, Yuan Q, Nicolaou P, Wang Y, Jones WK, Chu G, Kranias EG. Novel cardioprotective role of a small heat-shock protein, Hsp20, against ischemia/reperfusion injury. Circulation 111: 1792-1799, 2005.
29. Fan GC, Zhou X, Wang X, Song G, Qian J, Nicolaou P, Chen G, Ren X, Kranias EG. Heat shock protein 20 interacting with phosphorylated Akt reduces doxorubicin-triggered oxidative stress and cardiotoxicity. Circ Res 103: 1270-1279, 2008.
30. Forkink M, Smeitink JA, Brock R, Willems PH, Koopman WJ. Detection and manipulation of mitochondrial reactive oxygen species in mammalian cells. Biochim Biophys Acta 1797: 1034-1044, 2010.
31. Gao RY, Mukhopadhyay P, Mohanraj R, Wang H, Horvath B, Yin S, Pacher P. Resveratrol attenuates azidothymidine-induced cardiotox-icity by decreasing mitochondrial reactive oxygen species generation in human cardiomyocytes. Mol Med Report 4: 151-155, 2011.
32. Gidalevitz T, Prahlad V, Morimoto RI. The stress of protein misfold-ing: from single cells to multicellular organisms. Cold Spring Harb Perspect Biol 3, pii: a009704, 2011.
33. Godoy JR, Funke M, Ackermann W, Haunhorst P, Oesteritz S, Capani F, Elsasser HP, Lillig CH. Redox atlas of the mouse. Immu-nohistochemical detection of glutaredoxin, peroxiredoxin, and thiore-doxin-family proteins in various tissues of the laboratory mouse. Biochim Biophys Acta 1810: 2-92, 2011.
34. Golenhofen N, Perng MD, Quinlan RA, Drenckhahn D. Comparison of the small heat shock proteins alphaB-crystallin, MKBP, HSP25, HSP20, and cvHSP in heart and skeletal muscle. Histochem Cell Biol 122: 415-425, 2004.
35. Groenendyk J, Sreenivasaiah PK, Kim do H, Agellon LB, Michalak M. Biology of endoplasmic reticulum stress in the heart. Circ Res 107: 1185-1197, 2010.
36. Gurusamy N, Malik G, Gorbunov NV, Das DK. Redox activation of Ref-1 potentiates cell survival following myocardial ischemia reperfu-sion injury. Free Radic Biol Med 43: 397-407, 2007.
37. Gurusamy N, Das DK. Autophagy, redox signaling, and ventricular remodeling. Antioxid Redox Signal 11: 1975-1988, 2009.
38. Haberland M, Montgomery RL, Olson EN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet 10: 32-42, 2009.
39. Haffey TA. How to avoid a heart attack: putting it all together. J Am Osteopath Assoc 110: 397-400, 2010.
40. Hartl FU, Bracher A, Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature 475: 324-332, 2011.
41. Hedhli N, Pelat M, Depre C. Protein turnover in cardiac cell growth and survival. Cardiovasc Res 68: 186-196, 2005.
42. Heineke J, Molkentin JD. Regulation of cardiac hypertrophy by intra-cellular signalling pathways. Nat Rev Mol Cell Biol 7: 589-600, 2006.
43. Huang CX, Liu Y, Xia WF, Tang YH, Huang H. Oxidative stress: a possible pathogenesis of atrial fibrillation. Med Hypotheses 72: 466-467, 2009.
44. Huang L, Min JN, Masters S, Mivechi NF, Moskophidis D. Insights into function and regulation of small heat shock protein 25 (HSPB1) in a mouse model with targeted gene disruption. Genesis 45: 487-501, 2007.
45. Jones DP, Go YM. Redox compartmentalization and cellular stress. Diabetes Obes Metab 12, Suppl 2: 116-125, 2010.
46. Kampinga HH, Henning RH, van Gelder IC, Brundel BJ. Beat shock proteins and atrial fibrillation. Cell Stress Chaperones 12: 97-100, 2007.
47. Kampinga HH, Hageman J, Vos MJ, Kubota H, Tanguay RM, Bruford EA, Cheetham ME, Chen B, Hightower LE. Guidelines for the nomenclature of the human heat shock proteins. Cell Stress Chaper-ones 14: 105-111, 2009.
48. Kanamori H, Takemura G, Goto K, Maruyama R, Ono K, Nagao K, Tsujimoto A, Ogino A, Takeyama T, Kawaguchi T, Watanabe T, Kawasaki M, Fujiwara T, Fujiwara H, Seishima M, Minatoguchi S. Autophagy limits acute myocardial infarction induced by permanent coronary artery occlusion. Am J Physiol Heart Circ Physiol 300: H2261-H2271, 2011.
49. Kavazis AN, McClung JM, Hood DA, Powers SK. Exercise induces a cardiac mitochondrial phenotype that resists apoptotic stimuli. Am J Physiol Heart Circ Physiol 294: H928-H935, 2008.
50. Ke L, Meijering RA, Hoogstra-Berends F, Mackovicova K, Vos MJ, Van Gelder IC, Henning RH, Kampinga HH, Brundel BJ. HSPB1, HSPB6, HSPB7 and HSPB8 protect against RhoA GTPase-induced remodeling in tachypaced atrial myocytes. PLoS One 6: e20395, 2011.
51. Kee HJ, Kook H. Roles and targets of class I and IIa histone deacety-lases in cardiac hypertrophy. J Biomed Biotechnol 2011: 928326, 2011.
52. Kelly FJ. Use of antioxidants in the prevention and treatment of disease. J Int Fed Clin Chem 10: 21-23, 1998.
53. Klein I, Samarel AM, Welikson R, Hong C. Heterotopic cardiac transplantation decreases the capacity for rat myocardial protein synthesis. Circ Res 68: 1100-1107, 1991.
54. Koizumi S, Gong P, Suzuki K, Murata M. Cadmium-responsive element of the human heme oxygenase-1 gene mediates heat shock factor 1-dependent transcriptional activation. J Biol Chem 282: 8715-8723, 2007.
55. Kubota Y, Iso H, Date C, Kikuchi S, Watanabe Y, Wada Y, Inaba Y, Tamakoshi A. Dietary intakes of antioxidant vitamins and mortality from cardiovascular disease: the Japan Collaborative Cohort Study (JACC) study. Stroke 42: 1665-1672, 2011.
56. Kumarapeli AR, Su H, Huang W, Tang M, Zheng H, Horak KM, Li M, Wang X. Alpha B-crystallin suppresses pressure overload cardiac hypertrophy. Circ Res 103: 1473-1482, 2008.
57. Kuramochi Y, Cote GM, Guo X, Lebrasseur NK, Cui L, Liao R, Sawyer DB. Cardiac endothelial cells regulate reactive oxygen species-induced cardiomyocyte apoptosis through neuregulin-1beta/erbB4 signaling. J Biol Chem 279: 51141-51147, 2004.
58. Li HH, Du J, Fan YN, Zhang ML, Liu DP, Li L, Lockyer P, Kang EY, Patterson C, Willis MS. The ubiquitin ligase MuRF1 protects against cardiac ischemia/reperfusion injury by its proteasome-dependent degradation of phospho-c-Jun. Am J Pathol 178: 1043-1058, 2011.
59. Lloyd-Jones DM, Wang TJ, Leip EP, Larson MG, Levy D, Vasan RS, D'Agostino RB, Massaro JM, Beiser A, Wolf PA, Benjamin EJ. Lifetime risk for development of atrial fibrillation: the Framingham Heart Study. Circulation 110: 1042-1046, 2004.
60. 2+ signaling. Int J Biochem Cell Biol 41: 1957-1971, 2009.
61. Margittai E, Sitia R. Oxidative protein folding in the secretory pathway and redox signaling across compartments and cells. Traffic 12: 1-8, 2011.
62. McLendon PM, Robbins J. Desmin-related cardiomyopathy: an unfolding story. Am J Physiol Heart Circ Physiol 301: H1220-H1228, 2011.
63. Meyer AJ, Dick TP. Fluorescent protein-based redox probes. Antioxid Redox Signal 13: 621-650, 2010.
64. Minamino T, Kitakaze M. ER stress in cardiovascular disease. J Mol Cell Cardiol 48: 1105-1110, 2010.
65. Miyata T, Takizawa S, van Ypersele de Strihou Hypoxia C. 1. Intracellular sensors for oxygen and oxidative stress: novel therapeutic targets. Am J Physiol Cell Physiol 300: C226-C231, 2011.
66. Moslehi J, Minamishima YA, Shi J, Neuberg D, Charytan DM, Padera RF, Signoretti S, Liao R, Kaelin WG. Loss of hypoxia-inducible factor prolyl hydroxylase activity in cardiomyocytes pheno-copies ischemic cardiomyopathy. Circulation 122: 1004-1016, 2010.
67. Nag AC. Study of non-muscle cells of the adult mammalian heart: a fine structural analysis and distribution. Cytobios 28: 41-61, 1980.
68. Ooie T, Takahashi N, Saikawa T, Nawata T, Arikawa M, Yamanaka K, Hara M, Shimada T, Sakata T. Single oral dose of geranylgerany-lacetone induces heat-shock protein 72 and renders protection against ischemia/reperfusion injury in rat heart. Circulation 104: 1837-1843, 2001.
69. Osburn WO, Kensler TW. Nrf2 signaling: an adaptive response pathway for protection against environmental toxic insults. Mutat Res 659: 31-39, 2008.
70. Padrao AI, Ferreira RM, Vitorino R, Alves RM, Neuparth MJ, Duarte JA, Amado F. OXPHOS susceptibility to oxidative modifica-tions: the role of heart mitochondrial subcellular location. Biochim Biophys Acta 1807: 1106-1113, 2011.
71. Papageorgopoulos C, Caldwell K, Schweingrubber H, Neese RA, Shackleton CH, Hellerstein M. Measuring synthesis rates of muscle creatine kinase and myosin with stable isotopes and mass spectrometry. Anal Biochem 309: 1-10, 2002.
72. Patterson C, Portbury AL, Schisler JC, Willis MS. Tear me down: role of calpain in the development of cardiac ventricular hypertrophy. Circ Res 109: 453-462, 2011.
73. Peng W, Zhang Y, Zheng M, Cheng H, Zhu W, Cao CM, Xiao RP. Cardioprotection by CaMKII-deltaB is mediated by phosphorylation of heat shock factor 1 and subsequent expression of inducible heat shock protein 70. Circ Res 106: 102-110, 2010.
74. Portbury AL, Willis MS, Patterson C. Tearin' up my heart: proteolysis in the cardiac sarcomere. J Biol Chem 286: 9929-9934, 2011.
75. Powell SR. The ubiquitin-proteasome system in cardiac physiology and pathology. Am J Physiol Heart Circ Physiol 291: H1-H19, 2006.
76. Preville X, Salvemini F, Giraud S, Chaufour S, Paul C, Stepien G, Ursini MV, Arrigo AP. Mammalian small stress proteins protect against oxidative stress through their ability to increase glucose-6-phosphate dehydrogenase activity and by maintaining optimal cellular detoxifying machinery. Exp Cell Res 247: 61-78, 1999.
77. Rajasekaran NS, Connell P, Christians ES, Yan LJ, Taylor RP, Orosz A, Zhang XQ, Stevenson TJ, Peshock RM, Leopold JA, Barry WH, Loscalzo J, Odelberg SJ, Benjamin IJ. Human alpha B-crystallin mutation causes oxido-reductive stress and protein aggregation cardio-myopathy in mice. Cell 130: 427-439, 2007.
78. Rajasekaran NS, Varadharaj S, Khanderao GD, Davidson CJ, Kan-nan S, Firpo MA, Zweier JL, Benjamin IJ. Sustained activation of nuclear erythroid 2-related factor 2/antioxidant response element signaling promotes reductive stress in the human mutant protein aggregation cardiomyopathy in mice. Antioxid Redox Signal 14: 957-971, 2011.
79. Ranek MJ, Wang X. Activation of the ubiquitin-proteasome system in doxorubicin cardiomyopathy. Curr Hypertens Rep 11: 389-395, 2009.
80. Razeghi P, Sharma S, Ying J, Li YP, Stepkowski S, Reid MB, Taegtmeyer H. Atrophic remodeling of the heart in vivo simultaneously activates pathways of protein synthesis and degradation. Circulation 108: 2536-2541, 2003.
81. Richardson PG, Sonneveld P, Schuster MW, Irwin D, Stadtmauer EA, Facon T, Harousseau JL, Ben-Yehuda D, Lonial S, Goldschmidt H, Reece D, San-Miguel JF, Bladé J, Boccadoro M, Cavenagh J, Dalton WS, Boral AL, Esseltine DL, Porter JB, Schenkein D, Anderson KC. Bortezomib or high-dose dexamethasone for relapsed multiple myeloma. N Engl J Med 352: 2487-2498, 2005.
82. Riva A, Tandler B, Loffredo F, Vazquez E, Hoppel C. Structural differences in two biochemically defined populations of cardiac mitochondria. Am J Physiol Heart Circ Physiol 289: H868-H872, 2005.
83. Sanbe A, Daicho T, Mizutani R, Endo T, Miyauchi N, Yamauchi J, Tanonaka K, Glabe C, Tanoue A. Protective effect of geranylgerany-lacetone via enhancement of HSPB8 induction in desmin-related cardio-myopathy. PLoS One 4: e5351, 2009.
84. Santos CX, Anilkumar N, Zhang M, Brewer AC, Shah AM. Redox signaling in cardiac myocytes. Free Radic Biol Med 50: 777-793, 2011.
85. Semenza GL. Hydroxylation of HIF-1: oxygen sensing at the molecular level. Physiology 19: 176-182, 2004.
86. Seo WY, Goh AR, Ju SM, Song HY, Kwon DJ, Jun JG, Kim BC, Choi SY, Park J. Celastrol induces expression of heme oxygenase-1 through ROS/Nrf2/ARE signaling in the HaCaT cells. Biochem Biophys Res Commun 407: 535-540, 2011.
87. Shirley RL, Palting F, Easley JF, Carpenter JW, Koger M. Water, phosphorus, calcium, ash and protein in heart, liver and muscel of Hereford, Brehman and Hereford-Brehman cross-bred cattle. J Anim Sci 22: 393-395, 1963.
88. Sirker A, Zhang M, Shah AM. NADPH oxidases in cardiovascular disease: insights from in vivo models and clinical studies. Basic Res Cardiol 106: 735-747, 2011.
89. Smoliga JM, Baur JA, Hausenblas HA. Resveratrol and health-a comprehensive review of human clinical trials. Mol Nutr Food Res 55: 1129-1141 2011.
90. Stěrba M, Popelová O, Lenčo J, Fučíková A, Brc ̌áková E, Mazurová Y, Jirkovský E, Simu °nek T, Adamcová M, Mic ̌uda S, Stulík J, Geršl V. Proteomic insights into chronic anthracycline cardiotoxicity. J Mol Cell Cardiol 50: 849-862, 2011.
91. Sumandea MP, Steinberg SF. Redox signaling and cardiac sarcomeres. J Biol Chem 286: 9921-9927, 2011.
92. Tanaka K, Tsutsumi S, Arai Y, Hoshino T, Suzuki K, Takaki E, Ito T, Takeuchi K, Nakai A, Mizushima T. Genetic evidence for a protective role of heat shock factor 1 against irritant-induced gastric lesions. Mol Pharmacol 71: 985-993, 2007.
93. Taylor RP, Benjamin IJ. Small heat shock proteins: a new classification scheme in mammals. J Mol Cell Cardiol 38: 433-444, 2005.
94. Trinklein ND, Murray JI, Hartman SJ, Botstein D, Myers RM. The role of heat shock transcription factor 1 in the genome-wide regulation of the mammalian heat shock response. Mol Biol Cell 15: 1254-1261, 2004.
95. Turakhia S, Venkatakrishnan CD, Dunsmore K, Wong H, Kup-pusamy P, Zweier JL, Ilangovan G. Doxorubicin-induced cardiotox-icity: direct correlation of cardiac fibroblast and H9c2 cell survival and aconitase activity with heat shock protein 27. Am J Physiol Heart Circ Physiol 293: H3111-H3121, 2007.
96. Uversky VN, Dunker AK. Understanding protein non-folding. Biochim Biophys Acta 1804: 1231-1264, 2010.
97. Vedam K, Nishijima Y, Druhan LJ, Khan M, Moldovan NI, Zweier JL, Ilangovan G. Role of heat shock factor-1 activation in the doxoru-bicin-induced heart failure in mice. Am J Physiol Heart Circ Physiol 298: H1832-H1841, 2010.
98. Vliegen HW, van der Laarse A, Cornelisse CJ, Eulderink F. Myo-cardial changes in pressure overload-induced left ventricular hypertrophy. A study on tissue composition, polyploidization and multinucle-ation. Eur Heart J 12: 488-494, 1991.
99. Vos MJ, Kanon B, Kampinga HH. HSPB7 is a SC35 speckle resident small heat shock protein. Biochim Biophys Acta 1793: 1343-1353, 2009.
100. Westerheide SD, Bosman JD, Mbadugha BN, Kawahara TL, Matsu- moto G, Kim S, Gu W, Devlin JP, Silverman RB, Morimoto RI. Celastrols as inducers of the heat shock response and cytoprotection. J Biol Chem 279: 56053-56060, 2004.
101. Willis MS, Schisler JC, Portbury AL, Patterson C. Build it up-Tear it down: protein quality control in the cardiac sarcomere. Cardiovasc Res 81: 439-448, 2009.
102. Willis MS, Patterson C. Hold me tight: role of the heat shock protein family of chaperones in cardiac disease. Circulation 122: 1740 -1751, 2010.
103. Willis MS, Townley-Tilson WH, Kang EY, Homeister JW, Patterson C. Sent to destroy: the ubiquitin proteasome system regulates cell signaling and protein quality control in cardiovascular development and disease. Circ Res 106: 463-478, 2010.
104. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, Batalov S, Hodge CL, Haase J, Janes J, Huss JW 3rd, Su AI. BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 10: R130, 2009.
105. Wu JM, Hsieh TC. Resveratrol: a cardioprotective substance. Ann NY Acad Sci 1215: 16-21, 2011.
106. Yeh ET, Bickford CL. Cardiovascular complications of cancer therapy: incidence, pathogenesis, diagnosis, and management. J Am Coll Cardiol 53: 2231-2247, 2009.
107. Yu X, Tao W, Jiang F, Li C, Lin J, Liu C. Celastrol attenuates hypertension-induced inflammation and oxidative stress in vascular smooth muscle cells via induction of heme oxygenase-1. Am J Hypertens 23: 895-903, 2010.
108. Yuan H, Perry CN, Huang C, Iwai-Kanai E, Carreira RS, Glem-botski CC, Gottlieb RA. LPS-induced autophagy is mediated by oxi-dative signaling in cardiomyocytes and is associated with cytoprotection. Am J Physiol Heart Circ Physiol 296: H470-H479, 2009.
109. Zak R. Development and proliferative capacity of cardiac muscle cells. Circ Res 35, Suppl II: 17-26, 1974.
110. Zhang C, Xu Z, He XR, Michael LH, Patterson C. CHIP, a cochap-erone/ubiquitin ligase that regulates protein quality control, is required for maximal cardioprotection after myocardial infarction in mice. Am J Physiol Heart Circ Physiol 288: H2836-H2842, 2005.
111. Zhang X, Min X, Li C, Benjamin IJ, Qian B, Zhang X, Ding Z, Gao X, Yao Y, Ma Y, Cheng Y, Liu L. Involvement of reductive stress in the cardiomyopathy in transgenic mice with cardiac-specific overexpression of heat shock protein 27. Hypertension 55: 1412-1417, 2010.
112. Zhang YW, Shi J, Li YJ, Wei L. Cardiomyocyte death in doxorubicin-induced cardiotoxicity. Arch Immunol Ther Exp (Warsz) 57: 435-445, 2009.
113. Zito E, Melo EP, Yang Y, Wahlander A, Neubert TA, Ron D. Oxidative protein folding by an endoplasmic reticulum-localized perox-iredoxin. Mol Cell 40: 787-797, 2010.
114. Zou Y, Zhu W, Sakamoto M, Qin Y, Akazawa H, Toko H, Mizukami M, Takeda N, Minamino T, Takano H, Nagai T, Nakai A, Komuro I. Heat shock transcription factor 1 protects cardiomyocytes from isch-emia/reperfusion injury. Circulation 108: 3024-3030, 2003.
115. Zou Y, Li J, Ma H, Jiang H, Yuan J, Gong H, Liang Y, Guan A, Wu J, Li L, Zhou N, Niu Y, Sun A, Nakai A, Wang P, Takano H, Komuro I, Ge J. Heat shock transcription factor 1 protects heart after pressure overload through promoting myocardial angiogenesis in male mice. J Mol Cell Cardiol 51: 821-829 2011.
116. Zweier JL, Flaherty JT, Weisfeldt ML. Direct measurement of free radical generation following reperfusion of ischemic myocardium. Proc Natl Acad Sci USA 84: 1404-1407, 1987.