Novel cardioprotective role of a small heat-shock protein, Hsp20, against ischemia/reperfusion injury

Circulation

Volumn 111, Issue 14, 2005, Pages 1792-1799

  Fan, Guo Chang ^a   Ren, Xiaoping ^a   Qian, Jiang ^a   Yuan, Qunying ^a   Nicolaou, Persoulla ^a   Wang, Yang ^a   Jones, W Keith ^a   Chu, Guoxiang ^a   Kranias, Evangelia G ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Ischemia; Myocardial infarction; Proteins; Reperfusion

Indexed keywords

CASPASE 3; HEAT SHOCK PROTEIN 20; LACTATE DEHYDROGENASE; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; ENZYME ACTIVITY; ENZYME RELEASE; HEART FUNCTION; HEART INFARCTION; HEART MUSCLE CONTRACTILITY; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PROTECTION; INTERMETHOD COMPARISON; ISOLATED HEART; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RISK ASSESSMENT; STATISTICAL SIGNIFICANCE; TRANSGENIC MOUSE; WILD TYPE;

ANIMALS; APOPTOSIS; CARDIOTONIC AGENTS; GENE THERAPY; HEART; HEAT-SHOCK PROTEINS; HSP20 HEAT-SHOCK PROTEINS; MICE; MICE, TRANSGENIC; MYOCARDIAL INFARCTION; MYOCARDIAL ISCHEMIA; PHOSPHOPROTEINS; REPERFUSION; REPERFUSION INJURY;

EID: 17144393307     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.CIR.0000160851.41872.C6     Document Type: Article

References (46)

1. Williams ML, Koch WJ. Viral-based myocardial gene therapy approaches to alter cardiac function. Annu Rev Physiol. 2004;66:49-75.
2. Bolli R, Becker L, Gross G, Mentzer R Jr, Balshaw D, Lathrop DA. Myocardial protection at a crossroads: the need for translation into clinical therapy. Circ Res. 2004;95:125-134.
3. Eefting F, Rensing B, Wigman J, Pannekoek WJ, Liu WM, Cramer MJ, Lips DJ, Doevendans PA. Role of apoptosis in reperfusion injury. Cardiovasc Res. 2004;61:414-426.
4. Kingma JG Jr. Cardiac adaptation to ischemia-reperfusion injury. Ann N Y Acad Sci. 1999;874:83-99.
5. Benjamin IJ, McMillan DR. Stress (heat shock) proteins: molecular chaperones in cardiovascular biology and disease. Circ Res. 1998;83:117-132.
6. Martin JL, Mestril R, Hilal-Dandan R, Brunton LL, Dillmann WH. Small heat shock proteins and protection against ischemic injury in cardiomyocytes. Circulation. 1997;96:4343-4348.
7. 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.
8. 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.
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. Radford NB, Fina M, Benjamin IJ, Moreadith RW, Graves KH, Zhao P, Gavva S, Wiethoff A, Sherry AD, Malloy CR, Williams RS. Cardioprotective effects of 70-kDa heat shock protein in transgenic mice. Proc Natl Acad Sci U S A. 1996;93:2339-2342.
12. 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.
13. Vander Heide RS. Increased expression of HSP27 protects canine myocytes from simulated ischemia-reperfusion injury. Am J Physiol. 2002;282:H935-H941.
14. Ray PS, Martin JL, Swanson EA, Otani H, Dillmann WH, Das DK. Transgene overexpression of alphaB crystallin confers simultaneous protection against cardiomyocyte apoptosis and necrosis during myocardial ischemia and reperfusion. FASEB J. 2001;15:393-402.
15. Morrison LE, Whittaker RJ, Klepper RE, Wawrousek EF, Glembotski CC. Roles for alphaB-crystallin and HSPB2 in protecting the myocardium from ischemia-reperfusion-induced damage in a KO mouse model. Am J Physiol. 2004;286:H847-H855.
16. Kato K, Goto S, Inaguma Y, Hasegawa K, Morishita R, Asano T. Purification and characterization of a 20-kDa protein that is highly homologous to alpha B crystallin. J Biol Chem. 1994;269:15302-15309.
17. van de Klundert FAJM, van den IJssel PRLA, Stege GJ, de Jong WW. Rat Hsp20 confers thermoresistance in a clonal survival assay, but fails to protect coexpressed luciferase in Chinese hamster ovary cells. Biochem Biophys Res Commun. 1999;254:164-168.
18. O'Connor MJ, Rembold CM. Heat-induced force suppression and HSP20 phosphorylation in swine carotid media. J Appl Physiol. 2002;93:484-488.
19. Wang Y, Xu A, Ye J, Kraegen EW, Tse CA. Cooper GJ. Alteration in phosphorylation of P20 is associated with insulin resistance. Diabetes. 2001;50:1821-1827.
20. Chu G, Egnaczyk GF, Zhao W, Jo SH, Fan GC, Maggio JE, Xiao RP, and Kranias EG. Phosphoproteome analysis of cardiomyocytes subjected to β-adrenergic stimulation: identification and characterization of a cardiac heat shock protein p20. Circ Res. 2004;94:184-193.
21. Flynn CR, Komalavilas P, Tessier D, Thresher J, Niederkofler EE, Dreiza CM, Nelson RW, Panitch A, Joshi L, Brophy CM. Transduction of biologically active motifs of the small heat shock-related protein HSP20 leads to relaxation of vascular smooth muscle. FASEB J. 2003;17:1358-1360.
22. Kozawa O, Matsuno H, Niwa M, Hatakeyama D, Oiso Y, Kato K, Uematsu T. HSP20, low-molecular-weight heat shock-related protein, acts extracellularly as a regulator of platelet functions: a novel defense mechanism. Life Sci. 2002;72:113-124.
23. Fan GC, Chu G, Mitton B, Song Q, Yuan Q, Kranias EG. Small heat-shock protein Hsp20 phosphorylation inhibits β-agonist-induced cardiac apoptosis. Circ Res. 2004;94:1474-1482.
24. Chen Z, Chua CC, Ho YS, Hamdy RC, Chua BH. Overexpression of Bcl-2 attenuates apoptosis and protects against myocardial I/R injury in transgenic mice. Am J Physiol. 2001;280:H2313-H2320.
25. Hochhauser E, Kivity S, Offen D, Maulik N, Otani H, Barhum Y, Pannet H, Shneyvays V, Shainberg A, Goldshtaub V, Tobar A, Vidne BA. Bax ablation protects against myocardial ischemia-reperfusion injury in transgenic mice. Am J Physiol. 2003;284:H2351-H2359.
26. Yamashita N, Baxter GF, Yellon DM. Exercise directly enhances myocardial tolerance to ischaemia-reperfusion injury in the rat through a protein kinase C mediated mechanism. Heart. 2001;85:331-336.
27. Oldenburg O, Qin Q, Krieg T, Yang XM, Philipp S, Critz SD, Cohen MV, Downey JM. Bradykinin induces mitochondrial ROS generation via NO, cGMP, PKG, and mitoKATP channel opening and leads to cardioprotection. Am J Physiol. 2004;286:H468-H476.
28. Ren X, Wang Y, Jones WK. TNF-α is required for late ischemic preconditioning but not for remote preconditioning of trauma. J Surg Res. 2004;121:120-129.
29. Gupta S, Knowlton AA. Cytosolic heat shock protein 60, hypoxia, and apoptosis. Circulation. 2002;10:2727-2733.
30. Zhao ZQ, Vinten-Johansen J. Myocardial apoptosis and ischemic preconditioning. Cardiovasc Res. 2002;55:438-455.
31. Yet SF, Tian R, Layne MD, Wang ZY, Maemura K, Solovyeva M, Ith B, Melo LG, Zhang L, Ingwall JS, Dzau VJ, Lee ME, Perrella MA. Cardiac-specific expression of heme oxygenase-1 protects against ischemia and reperfusion injury in transgenic mice. Circ Res. 2001;89:168-173.
32. Verschuure P, Croes Y, van den IJssel PR, Quinlan RA, de Jong WW, Boelens WC. Translocation of small heat shock proteins to the actin cytoskeleton upon proteasomal inhibition. J Mol Cell Cardiol. 2002;34:117-128.
33. Baghelai K, Graham LJ, Wechsler AS, Jakoi ER. Phenylephrine induces delayed cardioprotection against necrosis without amelioration of stunning. Ann Thorac Surg. 1999;68:1219-1224.
34. Guttenplan N, Lee C, Frishman WH. Inhibition of myocardial apoptosis as a therapeutic target in cardiovascular disease prevention: focus on caspase inhibition. Heart Dis. 2001;3:313-318.
35. Chapman JG, Magee WP, Stukenbrok HA, Beckius GE, Milici AJ, Tracey WR. A novel nonpeptidic caspase-3/7 inhibitor, (S)-(+)-5-[1-(2- methoxymethylpyrrolidinyl) sulfonyl]isatin reduces myocardial ischemic injury. Eur J Pharmacol. 2002;456:59-68.
36. Condorelli G, Roncarati R, Ross J Jr, Pisani A, Stassi G, Todaro M, Trocha S, Drusco A, Gu Y, Russo MA, Frati G, Jones SP, Lefer DJ, Napoli C, Croce CM. Heart-targeted overexpression of caspase3 in mice increases infarct size and depresses cardiac function. Proc Natl Acad Sci U S A. 2001;98:9977-9982.
37. Kirchhoff SR, Gupta S, Knowlton AA. Cytosolic heat shock protein 60, apoptosis, and myocardial injury. Circulation. 2002;105:2899-2904.
38. Shan YX, Liu TJ, Su HF, Samsamshariat A, Mestril R, Wang PH. Hsp10 and Hsp60 modulate Bcl-2 family and mitochondria apoptosis signaling induced by doxorubicin in cardiac muscle cells. J Mol Cell Cardiol. 2003;35:1135-1143.
39. Mao YW, Liu JP, Xiang H, Li DW. Human alphaA- and alphaB-crystallins bind to Bax and Bcl-X(S) to sequester their translocation during staurosporine-induced apoptosis. Cell Death Differ. 2004;11:512-526.
40. Jaattela M, Wissing D, Kokholm K, Kallunki T, Egeblad M. Hsp70 exerts its anti-apoptotic function downstream of caspase-3-like proteases. EMBO J. 1998;17:6124-6134.
41. Beere HM, Wolf BB, Cain K, Mosser DD, Mahboubi A, Kuwana T, Tailor P, Morimoto RI, Cohen GM, Green DR. Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat Cell Biol. 2000;2:469-475.
42. Saleh A, Srinivasula SM, Balkir L, Robbins PD, Alnemri ES. Negative regulation of the Apaf-1 apoptosome by Hsp70. Nat Cell Biol. 2000;2:476-483.
43. Bruey JM, Ducasse C, Bonniaud P, Ravagnan L, Susin SA, Diaz-Latoud C, Gurbuxani S, Arrigo AP, Kroemer G, Solary E, Garrido C. Hsp27 negatively regulates cell death by interacting with cytochrome c. Nat Cell Biol. 2000;2:645-652.
44. Garrido C, Bruey JM, Fromentin A, Hammann A, Arrigo AP, Solary E. HSP27 inhibits cytochrome c-dependent activation of procaspase-9. FASEB J. 1999;13:2061-2070.
45. Tessier DJ, Komalavilas P, Panitch A, Joshi L, Brophy CM. The small heat shock protein (HSP) 20 is dynamically associated with the actin cross-linking protein actinin. J Surg Res. 2003;111:152-157.
46. Bluhm WF, Martin JL, Mestril R, Dillmann WH. Specific heat shock proteins protect microtubules during simulated ischemia in cardiac myocytes. Am J Physiol. 1998;275:H2243-H2249.