Intrinsic Myofilament Alterations Underlying the Decreased Contractility of Stunned Myocardium: A Consequence of Ca2+-Dependent Proteolysis?

Circulation Research

Volumn 78, Issue 3, 1996, Pages 455-465

  Gao, Wei Dong ^a   Liu, Yongge ^a   Mellgren, Ronald ^b   Marban, Eduardo ^a,c  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEDICAL COLLEGE OF OHIO   (United States)

^c Ross Building ^*  (United States)

Author keywords

Calpain I; Contractile proteins; Force Ca2+ relation; Myocardial ischemia reperfusion

Indexed keywords

CALCIUM ION; CALPAIN; CALPASTATIN; FURA 2;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; HEART MUSCLE CONTRACTILE FORCE; HEART MUSCLE CONTRACTILITY; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; MALE; MYOFILAMENT; NONHUMAN; PRIORITY JOURNAL; RAT; STUNNED HEART MUSCLE;

EID: 0030067221     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.res.78.3.455     Document Type: Article

References (50)

1. Braunwald E, Kloner RA. The stunned myocardium: prolonged, postischemic ventricular dysfunction. Circulation. 1982;66: 1146-1149.
2. 2+ transients underlie "stunning"? Circ Res. 1990;66:1268-1276.
3. Carrozza JP Jr, Bentivegna LA, Williams CP, Kuntz RE, Grossman W, Morgan JP. Decreased myofilament responsiveness in myocardial stunning follows transient calcium overload during ischemia and reperfusion. Circ Res. 1992;71:1334-1340.
4. 2+ activation of contraction as a consequence of reperfusion-induced cellular calcium overload in ferret hearts. J Clin Invest. 1987;79:950-961.
5. Kusuoka H, Marban E. Cellular mechanisms of myocardial stunning. Annu Rev Physiol. 1992;54:243-256.
6. Hofmann PA, Miller WP, Moss RL. Altered calcium sensitivity of isometric tension in myocyte-sized preparations of porcine postischemic stunned myocardium. Circ Res. 1993;72:50-56.
7. Dietrich DLL, van Leeuwen GR, Stienen GJM, Elzinga G. Stunning does not change the relation between calcium and force in skinned rat trabeculae. J Mol Cell Cardiol. 1993;25:541-549.
8. Mellgren RL, Murachi T. Intracellular Calcium-Dependent Proteolysis. Boca Raton, Fla: CRC Press Inc; 1990.
9. Mellgren RL, Carr TC. The protein inhibitor of calcium-dependent proteases: purification from bovine heart and possible mechanism of regulation. Arch Biochem Biophys. 1983;225:779-786.
10. 2+ responsiveness and altered diastolic function in intact ventricular muscle. Circ Res. 1995;76:1036-1048.
11. 2+ sensitivity in intact versus skinned rat ventricular muscle. Circ Res. 1994;74:408-415.
12. 2+] in intact rat cardiac trabeculae. J Gen Physiol. 1995;105:1-19.
13. Backx PH, ter Keurs HEDJ. Fluorescent properties of rat cardiac trabecular microinjected with fura-2 salt. Am J Physiol. 1993;72: H463-H469.
14. 2+ indicators with greatly improved fluorescent properties. J Biol Chem. 1985;260:3440-3450.
15. Martell AE, Smith RM. Critical Stability Constants, I-IV. New York, NY: Plenum Publishing Corp; 1974.
16. Pettit L, Siddiqui KF. The proton and metal complexes of adenyl-5′-yl imidodiphosphate. Biochem J. 1976;159:169-171.
17. Mellgren RL. Proteolysis of nuclear proteins by μ-calpain and m-calpain. J Biol Chem. 1991;266:13920-13924.
18. 2+-sensitive force in permeabilized myocardium and skeletal muscle. J Gen Physiol. 1990;96:1221-1245.
19. 2+ sensitivity of tension in mouse cardiac myocytes expressing skeletal troponin C. J Physiol (Lond). 1995;483:131-139.
20. Snedecor GW, Cochran WG. Statistical Methods. 8th ed. Ames, Iowa: Iowa State University Press; 1989.
21. Winer BJ. Statistical Principles in Experimental Design. 2nd ed. New York, NY: McGraw-Hill Publishing Co; 1982.
22. ter Keurs HEDJ, Rijnsburger WH, van Heuningen R, Nagelsmit MJ. Tension development and sarcomere length in rat cardiac trabeculae: evidence of length-dependent activation. Circ Res. 1980; 46:703-714.
23. Kirkels JH, van Echteld CJA, Ruigrok TJC. Intracellular magnesium during myocardial ischemia and reperfusion: possible consequences for postischemic recovery. J Mol Cell Cardiol. 1989;21: 1209-1218.
24. Murphy E, Steenbergen C, Levy LA, Raju B, London RE. Cytosolic free magnesium levels in ischemic rat heart. J Biol Chem. 1989;264; 5622-5627.
25. Fabiato A, Fabiato F. Effects of magnesium on contractile activation of skinned cardiac cells. J Physiol (Lond). 1975;249:497-517.
26. Mellgren RL, Nettey MS, Mericle MT, Renno W, Lane RD. An improved purification procedure for calpastatin, the inhibitor protein specific for the intracellular calcium-dependent proteinases, calpains. Prep Biochem. 1988;18:183-197.
27. Kentish JC. The effects of inorganic phosphate and creatine phosphate on force production in skinned muscles from rat ventricle. J Physiol (Lond). 1986;370:585-604.
28. Orchard CH, Kentish JC. Effects of changes of pH on the contractile function of cardiac muscle. Am J Physiol. 1990;258: C967-C981.
29. Kentish JC. The inhibitory effects of monovalent ions on force development in detergent-skinned ventricular muscle from guinea-pig. J Physiol (Lond). 1984;352:353-374.
30. Zhang R, Zhao J, Mandveno A, Potter JD. Cardiac troponin I phosphorylation increases the rate of cardiac muscle relaxation. Circ Res. 1995;76:1028-1035.
31. 2+ sensitivity of tension at short sarcomere length. Circ Res. 1995;77:199-205.
32. Kentish JC, ter Keurs HEDJ, Ricciardi L, Bucx JJJ, Noble MIM. Comparison between the sarcomere length-force relations of intact and skinned trabeculae from rat right ventricle: influence of calcium concentrations on these relations. Circ Res. 1986;58: 755-768.
33. Haeberle JR, Coolican SA, Evan A, Hathaway DR. The effect of a calcium dependent protease on the ultrastructure and contractile mechanics of skinned uterine smooth muscle. J Muscle Res Cell Motil. 1985;6:347-363.
34. Croall DE, Demartino GN. Calcium-activated neutral protease (calpain) system: structure, function, and regulation. Physiol Rev. 1991;75:813-847.
35. Suzuki K, Imajoh S, Emori Y, Kawasaki H, Minami Y, Ohno S. Calcium-activated neutral protease and its endogenous inhibitor. FEBS Lett. 1987;220:271-277.
36. i of perfused hearts: critical evaluation of the 5F-BAPTA and nuclear magnetic resonance method as applied to the study of ischemia and reperfusion. Circ Res. 1990;66: 1255-1267.
37. Steenbergen C, Murphy E, Levy L, London RE. Elevation in cytosolic free calcium concentration early in myocardial ischemia in perfused rat heart. Circ Res. 1987;60:700-707.
38. Kihara Y, Grossman W, Morgan JP. Direct measurement of changes in intracellular calcium transients during hypoxia, ischemia, and reperfusion of the intact mammalian heart. Circ Res. 1989; 65:1029-1044.
39. Takahashi K. Calpain substrate specificity. In: Mellgren RL, Murachi T, eds. Intracellular Calcium-Dependent Proteolysis. Boca Raton, Fla: CRC Press Inc; 1990:56-74.
40. Hara K, Ichihara S, Suzuki K, Imahori K. Purification and characterization of a calcium-activated neutral protease from monkey cardiac muscle. J Biochem (Tokyo). 1983;93:1435-1445.
41. Toyo-oka T, Masaki T. Calcium-activated neutral protease from bovine ventricular muscle: isolation and some of its properties. J Mol Cell Carcliol. 1979;11:769-786.
42. Suzuki K. The structure of calpains and the calpain gene. In: Mellgren RL, Murachi T, eds. Intracellular Calcium-Dependent Proteolysis. Boca Raton, Fla: CRC Press Inc; 1990:26-35.
43. Atar D, Gao WD, Backx PH, Murphy AM, Marban E. Immunoblot analysis of stunned myocardium reveals structural alterations of the myofilaments predicted by modeling of cross-bridge kinetics. Circulation. 1994;90(suppl I):I-646. Abstract.
44. Gao WD Atar D, Liu Y, Murphy AM, Marban E. Degradation of troponin I in ischemic/reperfused myocardium: molecular basis of myocardial stunning? Biophys J. 1995;68:A112. Abstract.
45. Yoshida K, Sorimachi Y, Fujiwara M, Hironaka K. Calpain is implicated in rat myocardial injury after ischemia or reperfusion. Jpn Circ J. 1995;59:40-48.
46. Yoshida K, Inui M, Harada K, Saido TC, Sorimachi Y, Ishihara T, Kawashima S, Sobue K. Reperfusion of rat heart after brief ischemia induces proteolysis of calspectin (nonerythroid spectrin or fodrin) by calpain. Circ Res. 1995;77:603-610.
47. Matsumura Y, Kusuoka H, Inoue M, Hori M, Kamada T. Protective effect of the protease inhibitor leupeptin against myocardial stunning. J Cardiovasc Pharmacol. 1993;22:135-142.
48. Walker AA, Harris KD, Digerness SB, Urthaler F. MDL 28170, a calpain inhibitor, attenuates myocardial stunning. J Mol Cell Cardiol 1995;27:A8. Abstract.
49. McKee EE, Cheung JY, Rannels DE, Morgan HE. Measurement of the rate of protein synthesis and compartmentation of heart phenylalanine. J Biol Chem. 1978;253:1030-1040.
50. Martin AF. Turnover of cardiac troponin subunits: kinetic evidence for a precursor pool of troponin-I. J Biol Chem. 1981;256:964-968.