Calpain inhibition preserves myocardial structure and function following myocardial infarction

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 297, Issue 5, 2009, Pages

  Mani, Santhosh K ^a   Balasubramanian, Sundaravadivel ^a   Zavadzkas, Juozas A ^b   Jeffords, Laura B ^b   Rivers, William T ^b   Zile, Michael R ^a,c   Mukherjee, Rupak ^b   Spinale, Francis G ^b,c   Kuppuswamy, Dhandapani ^a,c  

^a Division of Cardiology   (United States)

^b CSB 424   (United States)

^c RALPH H JOHNSON VA MEDICAL CENTER   (United States)

Author keywords

Cardiomyocytes; Cell death

Indexed keywords

CALPAIN; CALPEPTIN; CASPASE 3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ENZYME ACTIVATION; ENZYME INHIBITION; HEART EJECTION FRACTION; HEART INFARCTION; HEART MUSCLE; HEART VENTRICLE FUNCTION; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; CALPAIN; CARDIOTONIC AGENTS; CASPASE 3; CYSTEINE PROTEINASE INHIBITORS; DIPEPTIDES; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; INJECTIONS, INTRAVENOUS; INJECTIONS, SUBCUTANEOUS; MICE; MICE, INBRED C57BL; MYOCARDIAL CONTRACTION; MYOCARDIAL INFARCTION; MYOCARDIUM; STROKE VOLUME; TIME FACTORS; VENTRICULAR FUNCTION, LEFT; VENTRICULAR REMODELING;

EID: 70350482925     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00338.2009     Document Type: Article

References (58)

1. Arthur GD, Belcastro AN. A calcium stimulated cysteine protease involved in isoproterenol induced cardiac hypertrophy. Mol Cell Biochem 176: 241-248, 1997.
2. 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 291: H1411-H1420, 2006. (Pubitemid 44343688)
3. Banik NL, Hogan EL, Jenkins MG, McDonald JK, McAlhaney WW, Sostek MB. Purification of a calcium-activated neutral proteinase from bovine brain. Neurochem Res 8: 1389-1405, 1983.
4. Carragher NO, Levkau B, Ross R, Raines EW. Degraded collagen fragments promote rapid disassembly of smooth muscle focal adhesions that correlates with cleavage of pp125(FAK), paxillin, and talin. J Cell Biol 147: 619-630, 1999. (Pubitemid 29523467)
5. Chandrashekhar Y, Narula J. Death hath a thousand doors to let out life. Circ Res 92: 710-714, 2003. (Pubitemid 36457634)
6. Chen M, Won DJ, Krajewski S, Gottlieb RA. Calpain and mitochondria in ischemia/reperfusion injury. J Biol Chem 277: 29181-29186, 2002.
7. Cleutjens JP, Creemers EE. Integration of concepts: cardiac extracellular matrix remodeling after myocardial infarction. J Card Fail 8: S344-S348, 2002. (Pubitemid 36083082)
8. Communal C, Sumandea M, de Tombe P, Narula J, Solaro RJ, Hajjar RJ. Functional consequences of caspase activation in cardiac myocytes. Proc Natl Acad Sci USA 99: 6252-6256, 2002. (Pubitemid 34493298)
9. Cooper Gt. Basic determinants of myocardial hypertrophy: a review of molecular mechanisms. Annu Rev Med 48: 13-23, 1997.
10. Creemers EE, Davis JN, Parkhurst AM, Leenders P, Dowdy KB, Hapke E, Hauet AM, Escobar PG, Cleutjens JP, Smits JF, Daemen MJ, Zile MR, Spinale FG. Deficiency of TIMP-1 exacerbates LV remodeling after myocardial infarction in mice. Am J Physiol Heart Circ Physiol 284: H364-H371, 2003. (Pubitemid 36076305)
11. Darasz KH, Underwood SR, Bayliss J, Forbat SM, Keegan J, Poole- Wilson PA, Sutton GC, Pennell D. Measurement of left ventricular volume after anterior myocardial infarction: comparison of magnetic resonance imaging, echocardiography, and radionuclide ventriculography. Int J Cardiovasc Imaging 18: 135-142, 2002. (Pubitemid 34661757)
12. Deschamps AM, Spinale FG. Matrix modulation and heart failure: new concepts question old beliefs. Curr Opin Cardiol 20: 211-216, 2005.
13. Ducharme A, Frantz S, Aikawa M, Rabkin E, Lindsey M, Rohde LE, Schoen FJ, Kelly RA, Werb Z, Libby P, Lee RT. Targeted deletion of matrix metalloproteinase-9 attenuates left ventricular enlargement and collagen accumulation after experimental myocardial infarction. J Clin Invest 106: 55-62, 2000. (Pubitemid 30437240)
14. Duguez S, Bartoli M, Richard I. Calpain 3: a key regulator of the sarcomere? FEBS J 273: 3427-3436, 2006. (Pubitemid 44086943)
15. French JP, Hamilton KL, Quindry JC, Lee Y, Upchurch PA, Powers SK. Exercise-induced protection against myocardial apoptosis and necrosis: MnSOD, calcium-handling proteins, and calpain. FASEB J 22: 2862-2871, 2008.
16. Galvez AS, Diwan A, Odley AM, Hahn HS, Osinska H, Melendez JG, Robbins J, Lynch RA, Marreez Y, Dorn GW 2nd. Cardiomyocyte degeneration with calpain deficiency reveals a critical role in protein homeostasis. Circ Res 100: 1071-1078, 2007. (Pubitemid 46598932)
17. Gao WD, Atar D, Liu Y, Perez NG, Murphy AM, Marban E. Role of troponin I proteolysis in the pathogenesis of stunned myocardium. Circ Res 80: 393-399, 1997. (Pubitemid 27093354)
18. Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol Rev 83: 731-801, 2003.
19. +-ATPase activity during early reperfusion. Cardiovasc Res 70: 364-373, 2006.
20. Janicki JS, Brower GL, Gardner JD, Forman MF, Stewart JA Jr, Murray DB, Chancey AL. Cardiac mast cell regulation of matrix metalloproteinase- related ventricular remodeling in chronic pressure or volume overload. Cardiovasc Res 69: 657-665, 2006.
21. 3 Integrin-mediated ubiquitination activates survival signaling during myocardial hypertrophy. FASEB J 23: 2759-2771, 2009.
22. Kang PM, Izumo S. Apoptosis and heart failure: a critical review of the literature. Circ Res 86: 1107-1113, 2000. (Pubitemid 30396034)
23. Kawada T, Masui F, Kumagai H, Koshimizu M, Nakazawa M, Toyo-Oka T. A novel paradigm for therapeutic basis of advanced heart failure-assessment by gene therapy. Pharmacol Ther 107: 31-43, 2005. (Pubitemid 40800407)
24. Khalil PN, Neuhof C, Huss R, Pollhammer M, Khalil MN, Neuhof H, Fritz H, Siebeck M. Calpain inhibition reduces infarct size and improves global hemodynamics and left ventricular contractility in a porcine myocardial ischemia/reperfusion model. Eur J Pharmacol 528: 124-131, 2005. (Pubitemid 41773662)
25. Kim KA, Lee YA, Shin MH. Calpain-dependent calpastatin cleavage regulates caspase-3 activation during apoptosis of Jurkat T cells induced by Entamoeba histolytica. Int J Parasitol 37: 1209-1219, 2007.
26. Krijnen PA, Nijmeijer R, Meijer CJ, Visser CA, Hack CE, Niessen HW. Apoptosis in myocardial ischaemia and infarction. J Clin Pathol 55: 801-811, 2002.
27. Kunapuli S, Rosanio S, Schwarz ER. "How do cardiomyocytes die?" Apoptosis and autophagic cell death in cardiac myocytes. J Card Fail 12: 381-391, 2006. (Pubitemid 43817581)
28. Lindsey ML, Escobar GP, Mukherjee R, Goshorn DK, Sheats NJ, Bruce JA, Mains IM, Hendrick JK, Hewett KW, Gourdie RG, Matrisian LM, Spinale FG. Matrix metalloproteinase-7 affects connexin-43 levels, electrical conduction, and survival after myocardial infarction. Circulation 113: 2919-2928, 2006. (Pubitemid 44297233)
29. Majno G, Joris I. Apoptosis, oncosis, necrosis. An overview of cell death. Am J Pathol 146: 3-15, 1995.
30. Mani SK, Shiraishi H, Balasubramanian S, Yamane K, Chellaiah M, Cooper G, Banik N, Zile MR, Kuppuswamy D. In vivo administration of calpeptin attenuates calpain activation and cardiomyocyte loss in pressure-overloaded feline myocardium. Am J Physiol Heart Circ Physiol 295: H314-H326, 2008.
31. Marwick TH. Techniques for comprehensive two dimensional echocardiographic assessment of left ventricular systolic function. Heart 89, Suppl 3: iii2-iii8, 2003.
32. Melloni E, Averna M, Salamino F, Sparatore B, Minafra R, Pontremoli S. Acyl-CoA-binding protein is a potent m-calpain activator. J Biol Chem 275: 82-86, 2000. (Pubitemid 30038956)
33. Mukherjee R, Mingoia JT, Bruce JA, Austin JS, Stroud RE, Escobar GP, McClister DM Jr, Allen CM, Alfonso-Jaume MA, Fini ME, Lovett DH, Spinale FG. Selective spatiotemporal induction of matrix metalloproteinase-2 and matrix metalloproteinase-9 transcription after myocardial infarction. Am J Physiol Heart Circ Physiol 291: H2216-H2228, 2006. (Pubitemid 44776648)
34. Mukherjee R, Parkhurst AM, Mingoia JT, Sweterlitsch SE, Leiser JS, Escobar GP, Spinale FG, Saul JP. Myocardial remodeling after discrete radiofrequency injury: effects of tissue inhibitor of matrix metalloproteinase- 1 gene deletion. Am J Physiol Heart Circ Physiol 286: H1242-H1247, 2004. (Pubitemid 38381130)
35. Mullenheim J, Ebel D, Frassdorf J, Preckel B, Thamer V, Schlack W. Isoflurane preconditions myocardium against infarction via release of free radicals. Anesthesiology 96: 934-940, 2002. (Pubitemid 34266688)
36. Nakagawa T, Yuan J. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J Cell Biol 150: 887-894, 2000. (Pubitemid 30663424)
37. Okada K, Minamino T, Tsukamoto Y, Liao Y, Tsukamoto O, Takashima S, Hirata A, Fujita M, Nagamachi Y, Nakatani T, Yutani C, Ozawa K, Ogawa S, Tomoike H, Hori M, Kitakaze M. Prolonged endoplasmic reticulum stress in hypertrophic and failing heart after aortic constriction: possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis. Circulation 110: 705-712, 2004. (Pubitemid 39056270)
38. Rodriguez-Sinovas A, Abdallah Y, Piper HM, Garcia-Dorado D. Reperfusion injury as a therapeutic challenge in patients with acute myocardial infarction. Heart Fail Rev 12: 207-216, 2007. (Pubitemid 350176694)
39. Saitoh T, Nakajima T, Takahashi T, Kawahara K. Changes in cardiovascular function on treatment of inhibitors of apoptotic signal transduction pathways in left ventricular remodeling after myocardial infarction. Cardiovasc Pathol 15: 130-138, 2006. (Pubitemid 43669068)
40. Sandmann S, Prenzel F, Shaw L, Schauer R, Unger T. Activity profile of calpains I and II in chronically infarcted rat myocardium-influence of the calpain inhibitor CAL 9961. Br J Pharmacol 135: 1951-1958, 2002.
41. Sanges D, Marigo V. Cross-talk between two apoptotic pathways activated by endoplasmic reticulum stress: differential contribution of caspase-12 and AIF. Apoptosis 11: 1629-1641, 2006. (Pubitemid 44253679)
42. 2-mediated ERK and calpain activation play a critical role in cell adhesion and motility via focal adhesion kinase signaling: identification of a novel signaling pathway. J Biol Chem 281: 8497-8510, 2006.
43. Singh RB, Chohan PK, Dhalla NS, Netticadan T. The sarcoplasmic reticulum proteins are targets for calpain action in the ischemic-reperfused heart. J Mol Cell Cardiol 37: 101-110, 2004. (Pubitemid 38900533)
44. Singh RB, Dandekar SP, Elimban V, Gupta SK, Dhalla NS. Role of proteases in the pathophysiology of cardiac disease. Mol Cell Biochem 263: 241-256, 2004. (Pubitemid 39256162)
45. Sorimachi H, Imajoh-Ohmi S, Emori Y, Kawasaki H, Ohno S, Minami Y, Suzuki K. Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m- and μ-types. Specific expression of the mRNA in skeletal muscle. J Biol Chem 264: 20106-20111, 1989. (Pubitemid 20008132)
46. Sutton MG, Sharpe N. Left ventricular remodeling after myocardial infarction: pathophysiology and therapy. Circulation 101: 2981-2988, 2000. (Pubitemid 30415891)
47. Takahashi M, Tanonaka K, Yoshida H, Koshimizu M, Daicho T, Oikawa R, Takeo S. Possible involvement of calpain activation in pathogenesis of chronic heart failure after acute myocardial infarction. J Cardiovasc Pharmacol 47: 413-421, 2006. (Pubitemid 44309695)
48. Tan Y, Dourdin N, Wu C, De Veyra T, Elce JS, Greer PA. Ubiquitous calpains promote caspase-12 and JNK activation during endoplasmic reticulum stress-induced apoptosis. J Biol Chem 281: 16016-16024, 2006. (Pubitemid 43848495)
49. Tan Y, Wu C, De Veyra T, Greer PA. Ubiquitous calpains promote both apoptosis and survival signals in response to different cell death stimuli. J Biol Chem 281: 17689-17698, 2006. (Pubitemid 44035567)
50. Toth A, Nickson P, Mandl A, Bannister ML, Toth K, Erhardt P. Endoplasmic reticulum stress as a novel therapeutic target in heart diseases. Cardiovasc Hematol Disord Drug Targets 7: 205-218, 2007. (Pubitemid 47496578)
51. von Wnuck Lipinski K, Keul P, Ferri N, Lucke S, Heusch G, Fischer JW, Levkau B. Integrin-mediated transcriptional activation of inhibitor of apoptosis proteins protects smooth muscle cells against apoptosis induced by degraded collagen. Circ Res 98: 1490-1497, 2006. (Pubitemid 44297071)
52. von Wnuck Lipinski K, Keul P, Lucke S, Heusch G, Wohlschlaeger J, Baba HA, Levkau B. Degraded collagen induces calpain-mediated apoptosis and destruction of the X-chromosome-linked inhibitor of apoptosis (xIAP) in human vascular smooth muscle cells. Cardiovasc Res 69: 697-705, 2006. (Pubitemid 43139732)
53. Wadhawan V, Karim ZA, Mukhopadhyay S, Gupta R, Dikshit M, Dash D. Platelet storage under in vitro condition is associated with calcium-dependent apoptosis-like lesions and novel reorganization in platelet cytoskeleton. Arch Biochem Biophys 422: 183-190, 2004. (Pubitemid 38169365)
54. Wang KK. Calpain and caspase: can you tell the difference? Trends Neurosci 23: 20-26, 2000. [Erratum. Trends Neurosci (Feb): 59, 2000.]
55. Wencker D, Chandra M, Nguyen K, Miao W, Garantziotis S, Factor SM, Shirani J, Armstrong RC, Kitsis RN. A mechanistic role for cardiac myocyte apoptosis in heart failure. J Clin Invest 111: 1497-1504, 2003. (Pubitemid 38063282)
56. Wu HY, Tomizawa K, Matsui H. Calpain-calcineurin signaling in the pathogenesis of calcium-dependent disorder. Acta Med Okayama 61: 123-137, 2007. (Pubitemid 47052599)
57. Yarbrough WM, Mukherjee R, Escobar GP, Sample JA, McLean JE, Dowdy KB, Hendrick JW, Gibson WC, Hardin AE, Mingoia JT, White PC, Stiko A, Armstrong RC, Crawford FA, Spinale FG. Pharmacologic inhibition of intracellular caspases after myocardial infarction attenuates left ventricular remodeling: a potentially novel pathway. J Thorac Cardiovasc Surg 126: 1892-1899, 2003.
58. Yoshida K. Pursuing enigmas on ischemic heart disease and sudden cardiac death. Leg Med (Tokyo) 11: 51-58, 2008.