Deletion of the inducible 70-kDa heat shock protein genes in mice impairs cardiac contractile function and calcium handling associated with hypertrophy

Circulation

Volumn 113, Issue 22, 2006, Pages 2589-2597

  Kim, Yun Kyung ^a   Suarez, Jorge ^a   Hu, Ying ^a   McDonough, Patrick M ^a   Boer, Christa ^a   Dix, David J ^b   Dillmann, Wolfgang H ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Calcium; Contractility; Hypertrophy; Ischemia; Myocytes

Indexed keywords

ALPHA ACTIN; CAFFEINE; CALCIUM ION; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN SERCA2A; RAF PROTEIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE (CALCIUM); CALCIUM; HSPA1A PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE KINASE 4; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM BINDING; CELL DAMAGE; CONTROLLED STUDY; GENE; GENE DELETION; HEART HYPERTROPHY; HEART MUSCLE CONTRACTILITY; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HSPA1A GENE; HSPA1B GENE; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SARCOPLASMIC RETICULUM; ADENOVIRUS; ANIMAL; CARDIOMEGALY; CELL CULTURE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; HEART CONTRACTION; HEART MUSCLE CELL; METABOLISM; MOUSE MUTANT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ADENOVIRIDAE; ANIMALS; CALCIUM; CALCIUM-TRANSPORTING ATPASES; CARDIOMEGALY; CELLS, CULTURED; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE DELETION; GENE EXPRESSION REGULATION; HSP70 HEAT-SHOCK PROTEINS; MALE; MAP KINASE KINASE 4; MICE; MICE, KNOCKOUT; MYOCARDIAL CONTRACTION; MYOCARDIAL ISCHEMIA; MYOCYTES, CARDIAC; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-RAF; SARCOPLASMIC RETICULUM; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SIGNAL TRANSDUCTION;

EID: 33745160393     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.105.598409     Document Type: Article

References (42)

1. Gray CC, Amrani M, Yacoub MH. Heat stress proteins and myocardial protection: experimental model or potential clinical tool? Int J Biochem Cell Biol. 1999;31:559-573.
2. Dillmann WH. Small heat shock proteins and protection against injury. Ann N Y Acad Sci. 1999;874:66-68.
3. Nollen EA, Morimoto RI. Chaperoning signaling pathways: molecular chaperones as stress-sensing 'heat shock' proteins. J Cell Sci. 2002;115:2809-2816.
4. Luft JC, Dix DJ. Hsp70 expression and function during embryogenesis. Cell Stress Chaperones. 1999;4:162-170.
5. Lee SH, Kim M, Yoon BW, Kim YJ, Ma SJ, Roh JK, Lee JS, Seo JS. Targeted hsp70.1 disruption increases infarction volume after focal cerebral ischemia in mice. Stroke. 2001;32:2905-2912.
6. Hoshida S, Kuzuya T, Fuji H, Yamashita N, Oe H, Hori M, Suzuki K, Taniguchi N, Tada M. Sublethal ischemia alters myocardial antioxidant activity in canine heart. Am J Physiol. 1993;264:H33-H39.
7. Currie RW. Effects of ischemia and perfusion temperature on the synthesis of stress-induced (heat shock) proteins in isolated and perfused rat hearts. J Mol Cell Cardiol. 1987;19:795-808.
8. Trost SU, Omens JH, Karlon WJ, Meyer M, Mestril R, Covell JW, Dillmann WH. Protection against myocardial dysfunction after a brief ischemic period in transgenic mice expressing inducible heat shock protein 70. J Clin Invest. 1998;101:855-862.
9. Marber MS, Mestril R, Chi SH, Sayen MR, Yellon DM, Dillmann WH. Overexpression of the rat inducible 70-kD heat stress protein in a transgenic mouse increases the resistance of the heart to ischemic injury. J Clin Invest. 1995;95:1446-1456.
10. Plumier JC, Ross BM, Currie RW, Angelidis CE, Kazlaris H, Kollias G, Pagoulatos GN. Transgenic mice expressing the human heat shock protein 70 have improved post-ischemic myocardial recovery. J Clin Invest. 1995;95:1854-1860.
11. Okubo S, Wildner O, Shah MR, Chelliah JC, Hess ML, Kukreja RC. Gene transfer of heat-shock protein 70 reduces infarct size in vivo after ischemia/reperfusion in the rabbit heart. Circulation. 2001;103:877-881.
12. Mestril R, Giordano FJ, Conde AG, Dillmann WH. Adenovirus-mediated gene transfer of a heat shock protein 70 (hsp 70i) protects against simulated ischemia. J Mol Cell Cardiol. 1996;28:2351-2358.
13. Hampton CR, Shimamoto A, Rothnie CL, Griscavage-Ennis J, Chong A, Dix DJ, Verrier ED, Pohlman TH. HSP70.1 and -70.3 are required for late-phase protection induced by ischemic preconditioning of mouse hearts. Am J Physiol Heart Circ Physiol. 2003;285:H866-H874.
14. Hunt CR, Dix DJ, Sharma GG, Pandita RK, Gupta A, Funk M, Pandita TK. Genomic instability and enhanced radiosensitivity in Hsp70.1- and Hsp70.3-deficient mice. Mol Cell Biol. 2004;24:899-911.
15. Dix DJ, Garges JB, Hong RL. Inhibition of hsp70-1 and hsp70-3 expression disrupts preimplantation embryogenesis and heightens embryo sensitivity to arsenic. Mol Reprod Dev. 1998;51:373-380.
16. Rockett JC, Mapp FL, Garges JB, Luft JC, Mori C, Dix DJ. Effects of hyperthermia on spermatogenesis, apoptosis, gene expression, and fertility in adult male mice. Biol Reprod. 2001;65:229-239.
17. Molkentin JD, Dorn IG II. Cytoplasmic signaling pathways that regulate cardiac hypertrophy. Annu Rev Physiol. 2001;63:391-426.
18. Sugden PH, Clerk A. Cellular mechanisms of cardiac hypertrophy. J Mol Med. 1998;76:725-746.
19. Song J, Takeda M, Morimoto RI. Bag1-Hsp70 mediates a physiological stress signalling pathway that regulates Raf-1/ERK and cell growth. Nat Cell Biol. 2001;3:276-282.
20. Gabai VL, Yaglom JA, Volloch V, Meriin AB, Force T, Koutroumanis M, Massie B, Mosser DD, Sherman MY. Hsp72-mediated suppression of c-Jun N-terminal kinase is implicated in development of tolerance to caspase-independent cell death. Mol Cell Biol. 2000;20:6826-6836.
21. Trost SU, Belke DD, Bluhm WF, Meyer M, Swanson E, Dillmann WH. Overexpression of the sarcoplasmic reticulum Ca(2+)-ATPase improves myocardial contractility in diabetic cardiomyopathy. Diabetes. 2002;51:1166-1171.
22. Brewis N, Ohst K, Fields K, Rapacciuolo A, Chou D, Bloor C, Dillmann W, Rockman H, Walter G. Dilated cardiomyopathy in transgenic mice expressing a mutant A subunit of protein phosphatase 2A. Am J Physiol Heart Circ Physiol. 2000;279:H1307-H1318.
23. Suarez J, Gloss B, Belke DD, Hu Y, Scott B, Dieterle T, Kim YK, Valencik ML, McDonald JA, Dillmann WH. Doxycycline inducible expression of SERCA2a improves calcium handling and reverts cardiac dysfunction in pressure overload-induced cardiac hypertrophy. Am J Physiol Heart Circ Physiol. 2004;287:H2164-H2172.
24. Mestril R, Chi SH, Sayen MR, Dillmann WH. Isolation of a novel inducible rat heat-shock protein (HSP70) gene and its expression during ischaemia/hypoxia and heat shock. Biochem J. 1994;298(Pt 3):561-569.
25. Shannon TR, Ginsburg KS, Bers DM. Quantitative assessment of the SR Ca2+ leak-load relationship. Circ Res. 2002;91:594-600.
26. Bluhm WF, Kranias EG, Dillmann WH, Meyer M. Phospholamban: a major determinant of the cardiac force-frequency relationship. Am J Physiol Heart Circ Physiol. 2000;278:H249-H255.
27. Bers DM. SR Ca loading in cardiac muscle preparations based on rapid-cooling contractures. Am J Physiol. 1989;256:C109-C120.
28. Ho PD, Zechner DK, He H, Dillmann WH, Glembotski CC, McDonough PM. The Raf-MEK-ERK cascade represents a common pathway for alteration of intracellular calcium by Ras and protein kinase C in cardiac myocytes. J Biol Chem. 1998;273:21730-21735.
29. Andrews C, Ho PD, Dillmann WH, Glembotski CC, McDonough PM. The MKK6-p38 MAPK pathway prolongs the cardiac contractile calcium transient, downregulates SERCA2, and activates NF-AT. Cardiovasc Res. 2003;59:46-56.
30. Nakano M, Mann DL, Knowlton AA. Blocking the endogenous increase in HSP 72 increases susceptibility to hypoxia and reoxygenation in isolated adult feline cardiocytes. Circulation. 1997;95:1523-1531.
31. Das DK, Engelman RM, Kimura Y. Molecular adaptation of cellular defenses following preconditioning of the heart by repeated ischaemia. Cardiovasc Res. 1993;27:578-584.
32. Currie RW, Tanguay RM. Analysis of RNA for transcripts for catalase and SP71 in rat hearts after in vivo hyperthermia. Biochem Cell Biol. 1991;69:375-382.
33. Liu X, Engelman RM, Moraru II, Rousou JA, Flack JE III, Deaton DW, Maulik N, Das DK. Heat shock: a new approach for myocardial preservation in cardiac surgery. Circulation. 1992;86:II-358-II-63.
34. Cook SA, Sugden PH, Clerk A. Activation of c-Jun N-terminal kinases and p38-mitogen-activated protein kinases in human heart failure secondary to ischaemic heart disease. J Mol Cell Cardiol. 1999;31:1429-1434.
35. Choukroun G, Hajjar R, Fry S, del Monte F, Haq S, Guerrero JL, Picard M, Rosenzweig A, Force T. Regulation of cardiac hypertrophy in vivo by the stress-activated protein kinases/c-Jun NH(2)-terminal kinases. J Clin Invest. 1999;104:391-398.
36. Choukroun G, Hajjar R, Kyriakis JM, Bonventre JV, Rosenzweig A, Force T. Role of the stress-activated protein kinases in endothelin-induced cardiomyocyte hypertrophy. J Clin Invest. 1998;102:1311-1320.
37. Zechner D, Thuerauf DJ, Hanford DS, McDonough PM, Glembotski CC. A role for the p38 mitogen-activated protein kinase pathway in myocardial cell growth, sarcomeric organization, and cardiac-specific gene expression. J Cell Biol. 1997;139:115-127.
38. Adams JW, Sah VP, Henderson SA, Brown JH. Tyrosine kinase and c-Jun NH2-terminal kinase mediate hypertrophic responses to prostaglandin F2alpha in cultured neonatal rat ventricular myocytes. Circ Res. 1998;83:167-178.
39. Wang Y, Su B, Sah VP, Brown JH, Han J, Chien KR. Cardiac hypertrophy induced by mitogen-activated protein kinase kinase 7, a specific activator for c-Jun NH2-terminal kinase in ventricular muscle cells. J Biol Chem. 1998;273:5423-5426.
40. Ramirez MT, Sah VP, Zhao XL, Hunter JJ, Chien KR, Brown JH. The MEKK-JNK pathway is stimulated by alpha1-adrenergic receptor and ras activation and is associated with in vitro and in vivo cardiac hypertrophy. J Biol Chem. 1997;272:14057-14061.
41. Wang Y, Huang S, Sah VP, Ross J Jr, Brown JH, Han J, Chien KR. Cardiac muscle cell hypertrophy and apoptosis induced by distinct members of the p38 mitogen-activated protein kinase family. J Biol Chem. 1998;273:2161-2168.
42. Gaia G, Comini L, Pasini E, Tomelleri G, Agnoletti L, Ferrari R. Heat shock protein 72 in cardiac and skeletal muscles during hypertension. Mol Cell Biochem. 1995;146:1-6.