Tear me down: Role of calpain in the development of cardiac ventricular hypertrophy

Circulation Research

Volumn 109, Issue 4, 2011, Pages 453-462

  Patterson, Cam ^a   Portbury, Andrea L ^a   Schisler, Jonathan C ^a   Willis, Monte S ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

3 integrin; calpain; calpastatin; cardiac hypertrophy; HSP90 heat shock proteins; NF B inhibition

Indexed keywords

[1 [(1 FORMYL 2 PHENYLETHYL)CARBAMOYL] 2 METHYLPROPYL]CARBAMIC ACID BENZYL ESTER; ALOXISTATIN ACID; ALPHA TROPOMYOSIN; AMYLOID PRECURSOR PROTEIN; ANGIOTENSIN II; BETA3 INTEGRIN; CALPAIN; CALPAIN 1; CALPAIN 2; CALPASTATIN; CALPEPTIN; CHROMOGRANIN B; ENDOTHELIAL NITRIC OXIDE SYNTHASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; ISOPRENALINE; NITRIC OXIDE SYNTHASE; PROTEIN KINASE B;

CELL SURVIVAL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HEART PROTECTION; HEART VENTRICLE HYPERTROPHY; HUMAN; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CALPAIN; CARDIOMEGALY; CARDIOVASCULAR AGENTS; CYSTEINE PROTEINASE INHIBITORS; DISEASE MODELS, ANIMAL; DRUG DESIGN; HEART VENTRICLES; HUMANS; SIGNAL TRANSDUCTION; VENTRICULAR REMODELING;

EID: 80051769513     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.110.239749     Document Type: Review

References (135)

1. Katz AM. Cardiomyopathy of overload: a major determinant of prognosis in congestive heart failure. N Engl J Med. 1990;322:100-110. (Pubitemid 20023868)
2. Verdecchia P, Angeli F, Borgioni C, Gattobigio R, de Simone G, Devereux RB, Porcellati C. Changes in cardiovascular risk by reduction of left ventricular mass in hypertension: a meta-analysis. Am J Hypertens. 2003;16:895-899. (Pubitemid 37315486)
3. Verdecchia P, Schillaci G, Borgioni C, Ciucci A, Gattobigio R, Zampi I, Reboldi G, Porcellati C. Prognostic significance of serial changes in left ventricular mass in essential hypertension. Circulation. 1998;97:48-54. (Pubitemid 28036154)
4. Heineke J, Molkentin JD. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol. 2006;7:589-600. (Pubitemid 44325350)
5. Magid NM, Borer JS, Young MS, Wallerson DC, DeMonteiro C. Suppression of protein degradation in progressive cardiac hypertrophy of chronic aortic regurgitation. Circulation. 1993;87:1249-1257. (Pubitemid 23110397)
6. King RK, Magid NM, Opio G, Borer JS. Protein turnover in compensated chronic aortic regurgitation. Cardiology. 1997;88:518-525. (Pubitemid 27491267)
7. Parmacek MS, Magid NM, Lesch M, Decker RS, Samarel AM. Cardiac protein synthesis and degradation during thyroxine-induced left ventricular hypertrophy. Am J Physiol. 1986;251:C727-C736.
8. Coleman PS, Parmacek MS, Lesch M, Samarel AM. Protein synthesis and degradation during regression of thyroxine-induced cardiac hypertrophy. J Mol Cell Cardiol. 1989;21:911-925. (Pubitemid 19260815)
9. Drews O, Tsukamoto O, Liem D, Streicher J, Wang Y, Ping P. Differential regulation of proteasome function in isoproterenol-induced cardiac hypertrophy. Circ Res. 2010;107:1094-1101.
10. Razeghi P, Baskin KK, Sharma S, Young ME, Stepkowski S, Essop MF, Taegtmeyer H. Atrophy, hypertrophy, and hypoxemia induce transcriptional regulators of the ubiquitin proteasome system in the rat heart. Biochem Biophys Res Commun. 2006;342:361-364. (Pubitemid 43289002)
11. Willis MS, Rojas M, Li L, Selzman CH, Tang RH, Stansfield WE, Rodriguez JE, Glass DJ, Patterson C. Muscle ring finger 1 mediates cardiac atrophy in vivo. Am J Physiol Heart Circ Physiol. 2009;296:H997-H1006.
12. Willis MS, Ike C, Li L, Wang DZ, Glass DJ, Patterson C. Muscle ring finger 1, but not muscle ring finger 2, regulates cardiac hypertrophy in vivo. Circ Res. 2007;100:456-459. (Pubitemid 46673255)
13. Li HH, Willis MS, Lockyer P, Miller N, McDonough H, Glass DJ, Patterson C. Atrogin-1 inhibits Akt-dependent cardiac hypertrophy in mice via ubiquitin-dependent coactivation of Forkhead proteins. J Clin Invest. 2007;117:3211-3223. (Pubitemid 350096979)
14. Li HH, Kedar V, Zhang C, McDonough H, Arya R, Wang DZ, Patterson C. Atrogin-1/muscle atrophy F-box inhibits calcineurin-dependent cardiac hypertrophy by participating in an SCF ubiquitin ligase complex. J Clin Invest. 2004;114:1058-1071. (Pubitemid 39578695)
15. Hedhli N, Depre C. Proteasome inhibitors and cardiac cell growth. Cardiovasc Res. 2010;85:321-329.
16. Tang M, Li J, Huang W, Su H, Liang Q, Tian Z, Horak KM, Molkentin JD, Wang X. Proteasome functional insufficiency activates the calcineurin-NFAT pathway in cardiomyocytes and promotes maladaptive remodelling of stressed mouse hearts. Cardiovasc Res. 2010;88:424-433.
17. Wildenthal K, Crie JS, Ord JM, Wakeland JR. The role of lysosomes and microtubules in cardiac protein degradation. Adv Myocardiol. 1985;5:137-144.
18. Wildenthal K, Wakeland JR, Ord JM, Stull JT. Interference with lysosomal proteolysis fails to reduce cardiac myosin degradation. Biochem Biophys Res Commun. 1980;96:793-798. (Pubitemid 11198406)
19. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev Cell. 2004;6:463-477. (Pubitemid 38456176)
20. Yitzhaki S, Huang C, Liu W, Lee Y, Gustafsson AB, Mentzer RM, Jr., Gottlieb RA. Autophagy is required for preconditioning by the adenosine A1 receptor-selective agonist CCPA. Basic Res Cardiol. 2009;104:157-167.
21. Mizushima N, Yamamoto A, Hatano M, Kobayashi Y, Kabeya Y, Suzuki K, Tokuhisa T, Ohsumi Y, Yoshimori T. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol. 2001;152:657-668.
22. Rothermel BA, Hill JA. Autophagy in load-induced heart disease. Circ Res. 2008;103:1363-1369.
23. Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol Rev. 2003;83:731-801. (Pubitemid 36828925)
24. Jackman RW, Kandarian SC. The molecular basis of skeletal muscle atrophy. Am J Physiol Cell Physiol. 2004;287:C834-C843. (Pubitemid 39238306)
25. Bukowska A, Lendeckel U, Bode-Böger SM, Goette A. Physiologic and pathophysiologic role of calpain: implications for the occurrence of atrial fibrillation. Cardiovasc Ther. 2010. Published online before print November 25, 2010. doi:10.1111/j.1755-5922.2010.00245.x. http://onlinelibrary.wiley.com/doi/ 10.1111/j.1755-5922.2010.00245.x/abstract. Accessed January 1, 2011.
26. Villa PG, Henzel WJ, Sensenbrenner M, Henderson CE, Pettmann B. Calpain inhibitors, but not caspase inhibitors, prevent actin proteolysis and DNA fragmentation during apoptosis. J Cell Sci. 1998;111(part 6):713-722. (Pubitemid 28163880)
27. Brown SB, Bailey K, Savill J. Actin is cleaved during constitutive apoptosis. Biochem J. 1997;323(part 1):233-237. (Pubitemid 27153898)
28. Vaisid T, Kosower NS, Katzav A, Chapman J, Barnoy S. Calpastatin levels affect calpain activation and calpain proteolytic activity in APP transgenic mouse model of Alzheimer's disease. Neurochem Int. 2007;51:391-397. (Pubitemid 47503460)
29. Siman R, Card JP, Davis LG. Proteolytic processing of beta-amyloid precursor by calpain I. J Neurosci. 1990;10:2400-2411.
30. Li QX, Evin G, Small DH, Multhaup G, Beyreuther K, Masters CL. Proteolytic processing of Alzheimer's disease beta A4 amyloid precursor protein in human platelets. J Biol Chem. 1995;270:14140-14147.
31. Nozaki K, Das A, Ray SK, Banik NL. Calpain inhibition attenuates intracellular changes in muscle cells in response to extracellular inflammatory stimulation. Exp Neurol. 2010;225:430-435.
32. Thomas A, El Rouby S, Reed JC, Krajewski S, Silber R, Potmesil M, Newcomb EW. Drug-induced apoptosis in B-cell chronic lymphocytic leukemia: relationship between p53 gene mutation and bcl-2/bax proteins in drug resistance. Oncogene. 1996;12:1055-1062. (Pubitemid 26104447)
33. Wood DE, Thomas A, Devi LA, Berman Y, Beavis RC, Reed JC, Newcomb EW. Bax cleavage is mediated by calpain during druginduced apoptosis. Oncogene. 1998;17:1069-1078. (Pubitemid 28444591)
34. Lakshmikuttyamma A, Selvakumar P, Sharma AR, Anderson DH, Sharma RK. In vitro proteolytic degradation of bovine brain calcineurin by m-calpain. Neurochem Res. 2004;29:1913-1921. (Pubitemid 39273655)
35. Blomgren K, Zhu C, Wang X, Karlsson JO, Leverin AL, Bahr BA, Mallard C, Hagberg H. Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia: a mechanism of "pathological apoptosis"? J Biol Chem. 2001;276:10191-10198.
36. Chowdhury I, Tharakan B, Bhat GK. Caspases: an update. Comp Biochem Physiol B Biochem Mol Biol. 2008;151:10-27.
37. 2+-ATPase. Arch Biochem Biophys. 1988;267:317-327. (Pubitemid 19001034)
38. Salamino F, Sparatore B, Melloni E, Michetti M, Viotti PL, Pontremoli S, Carafoli E. The plasma membrane calcium pump is the preferred calpain substrate within the erythrocyte. Cell Calcium. 1994;15:28-35. (Pubitemid 24038873)
39. Molinari M, Anagli J, Carafoli E. PEST sequences do not influence substrate susceptibility to calpain proteolysis. J Biol Chem. 1995;270:2032-2035.
40. McGinnis KM, Whitton MM, Gnegy ME, Wang KK. Calcium/calmodulin-dependent protein kinase IV is cleaved by caspase-3 and calpain in SH-SY5Y human neuroblastoma cells undergoing apoptosis. J Biol Chem. 1998;273:19993-20000. (Pubitemid 28377549)
41. Jariel-Encontre I, Salvat C, Steff AM, Pariat M, Acquaviva C, Furstoss O, Piechaczyk M. Complex mechanisms for c-fos and c-jun degradation. Mol Biol Rep. 1997;24:51-56. (Pubitemid 27269426)
42. Hirai S, Kawasaki H, Yaniv M, Suzuki K. Degradation of transcription factors, c-Jun. and c-Fos, by calpain. FEBS Lett. 1991;287:57-61.
43. Carillo S, Pariat M, Steff AM, Roux P, Etienne-Julan M, Lorca T, Piechaczyk M. Differential sensitivity of FOS and JUN family members to calpains. Oncogene. 1994;9:1679-1689. (Pubitemid 24163395)
44. Bhuiyan MS, Shioda N, Fukunaga K. Chronic beta-AR activationinduced calpain activation and impaired eNOS-Akt signaling mediates cardiac injury in ovariectomized female rats. Expert Opin Ther Targets. 2009;13:275-286.
45. Murayama A, Fukai F, Murachi T. Action of calpain on the basic estrogen receptor molecule of porcine uterus. J Biochem. 1984;95:1697-1704. (Pubitemid 14122384)
46. Shiba E, Kim S, Fujitani M, Kambayashi JI, Kawamura I, Tsujimoto S, Shimomura K, Tanji Y, Taguchi T, Kimoto Y, Izukura M, Takai SI. Possible involvement of calpain in the growth of estrogen receptor positive breast cancer cells. Anticancer Res. 1996;16:773-777. (Pubitemid 26182008)
47. Yuan Y, Dopheide SM, Ivanidis C, Salem HH, Jackson SP. Calpain regulation of cytoskeletal signaling complexes in von Willebrand factorstimulated platelets: distinct roles for glycoprotein Ib-V-IX and glycoprotein IIb-IIIa (integrin αIIbβ3) in von Willebrand factor-induced signal transduction. J Biol Chem. 1997;272:21847-21854. (Pubitemid 27382801)
48. Cooray P, Yuan Y, Schoenwaelder SM, Mitchell CA, Salem HH, Jackson SP. Focal adhesion kinase (pp125FAK) cleavage and regulation by calpain. Biochem J. 1996;318(part 1):41-47.
49. Greenwood AF, Jope RS. Brain G-protein proteolysis by calpain: enhancement by lithium. Brain Res. 1994;636:320-326. (Pubitemid 24044649)
50. Han Y, Weinman S, Boldogh I, Walker RK, Brasier AR. Tumor necrosis factor-alpha-inducible IkappaBalpha proteolysis mediated by cytosolic m-calpain: a mechanism parallel to the ubiquitin-proteasome pathway for nuclear factor-κb activation. J Biol Chem. 1999;274:787-794.
51. Lin YC, Brown K, Siebenlist U. Activation of NF-kappa B requires proteolysis of the inhibitor I kappa B-alpha: signal-induced phosphorylation of I kappa B-alpha alone does not release active NF-kappa B. Proc Natl Acad Sci USA. 1995;92:552-556.
52. Pfaff M, Du X, Ginsberg MH. Calpain cleavage of integrin beta cytoplasmic domains. FEBS Lett. 1999;460:17-22. (Pubitemid 29479236)
53. Meredith J, Jr., Mu Z, Saido T, Du X. Cleavage of the cytoplasmic domain of the integrin beta3 subunit during endothelial cell apoptosis. J Biol Chem. 1998;273:19525-19531. (Pubitemid 28367004)
54. Xi X, Flevaris P, Stojanovic A, Chishti A, Phillips DR, Lam SC, Du X. Tyrosine phosphorylation of the integrin beta 3 subunit regulates beta 3 cleavage by calpain. J Biol Chem. 2006;281:29426-29430. (Pubitemid 44536949)
55. 2+ channels. Biochem Biophys Res Commun. 2007;364:372-377. (Pubitemid 47633423)
56. Hao LY, Kameyama A, Kuroki S, Takano J, Takano E, Maki M, Kameyama M. Calpastatin domain L is involved in the regulation of L-type Ca2+ channels in guinea pig cardiac myocytes. Biochem Biophys Res Commun. 2000;279:756-761. (Pubitemid 32042853)
57. 2+ channel: partial restoration of channel activity in cell-free patches by calpastatin. Pflugers Arch. 1998;435:344-349. (Pubitemid 28066224)
58. Hell JW, Westenbroek RE, Breeze LJ, Wang KK, Chavkin C, Catterall WA. N-methyl-D-aspartate receptor-induced proteolytic conversion of postsynaptic class C L-type calcium channels in hippocampal neurons. Proc Natl Acad Sci USA. 1996;93:3362-3367. (Pubitemid 26125625)
59. De Jongh KS, Colvin AA, Wang KK, Catterall WA. Differential proteolysis of the full-length form of the L-type calcium channel alpha 1 subunit by calpain. J Neurochem. 1994;63:1558-1564. (Pubitemid 24299547)
60. Kubbutat MH, Vousden KH. Proteolytic cleavage of human p53 by calpain: a potential regulator of protein stability. Mol Cell Biol. 1997;17:460-468. (Pubitemid 26425636)
61. Pariat M, Carillo S, Molinari M, Salvat C, Debussche L, Bracco L, Milner J, Piechaczyk M. Proteolysis by calpains: a possible contribution to degradation of p53. Mol Cell Biol. 1997;17:2806-2815. (Pubitemid 27175164)
62. Banno Y, Nakashima S, Hachiya T, Nozawa Y. Endogenous cleavage of phospholipase C-beta 3 by agonist-induced activation of calpain in human platelets. J Biol Chem. 1995;270:4318-4324.
63. Park D, Jhon DY, Lee CW, Ryu SH, Rhee SG. Removal of the carboxylterminal region of phospholipase C-beta 1 by calpain abolishes activation by G alpha q. J Biol Chem. 1993;268:3710-3714. (Pubitemid 23071018)
64. Zimmerman UJ, Wang M, Nelson JB, Ekwunife FS, Liu L. Secretagogue-induced proteolysis of cAMP-dependent protein kinase in intact rat alveolar epithelial type II cells. Biochim Biophys Acta. 1996;1311:117-123.
65. Kishimoto A, Mikawa K, Hashimoto K, Yasuda I, Tanaka S, Tominaga M, Kuroda T, Nishizuka Y. Limited proteolysis of protein kinase C subspecies by calcium-dependent neutral protease (calpain). J Biol Chem. 1989;264:4088-4092. (Pubitemid 19072301)
66. Dwyer LD, Miller AC, Parks AL, Jaken S, Malkinson AM. Calpaininduced downregulation of activated protein kinase C-alpha affects lung epithelial cell morphology. Am J Physiol. 1994;266:L569-L576.
67. Shea TB, Beermann ML, Griffin WR, Leli U. Degradation of protein kinase C alpha and its free catalytic subunit, protein kinase M, in intact human neuroblastoma cells and under cell-free conditions: evidence that PKM is degraded by mM calpain-mediated proteolysis at a faster rate than PKC. FEBS Lett. 1994;350:223-229.
68. 2+ release channel. J Membr Biol. 1998;161:33-43. (Pubitemid 28046337)
69. Johnson GV. Tau phosphorylation and proteolysis: insights and perspectives. J Alzheimers Dis. 2006;9:243-250. (Pubitemid 44253316)
70. Xie HQ, Johnson GV. Calcineurin inhibition prevents calpain-mediated proteolysis of tau in differentiated PC12 cells. J Neurosci Res. 1998;53:153-164. (Pubitemid 28300121)
71. Kemp CM, Sensky PL, Bardsley RG, Buttery PJ, Parr T. Tenderness: an enzymatic view. Meat Sci. 2010;84:248-256.
72. Jiang ST. Contribution of muscle proteinases to meat tenderization. Proc Natl Sci Counc Repub China B. 1998;22:97-107.
73. 2+-dependent proteases (calpains) in post mortem proteolysis and meat tenderness. Biochimie. 1992;74:239-245.
74. Shiraha H, Glading A, Chou J, Jia Z, Wells A. Activation of m-calpain (calpain II) by epidermal growth factor is limited by protein kinase A phosphorylation of m-calpain. Mol Cell Biol. 2002;22:2716-2727. (Pubitemid 34262992)
75. 2+-dependent proteinases and their inhibitor in normal, fasted, and denervated rat skeletal muscle. Anat Rec. 1992;232:60-77.
76. Dayton WR, Schollmeyer JV. Immunocytochemical localization of a calcium-activated protease in skeletal muscle cells. Exp Cell Res. 1981;136:423-433. (Pubitemid 12150891)
77. Azanza JL, Raymond J, Robin JM, Cottin P, Ducastaing A. Purification and some physico-chemical and enzymic properties of a calcium ionactivated neutral proteinase from rabbit skeletal muscle. Biochem J. 1979;183:339-347.
78. Mohrhauser DA, Underwood KR, Weaver AD. In vitro degradation of bovine myofibrils is caused by μ-calpain, not caspase-3. J Anim Sci. 2011;89:798-808.
79. 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. 1997;80:393-399. (Pubitemid 27093354)
80. 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. 2002;135:1951-1958. (Pubitemid 34478307)
81. Galvez AS, Diwan A, Odley AM, Hahn HS, Osinska H, Melendez JG, Robbins J, Lynch RA, Marreez Y, Dorn GW, II. Cardiomyocyte degeneration with calpain deficiency reveals a critical role in protein homeostasis. Circ Res. 2007;100:1071-1078. (Pubitemid 46598932)
82. Dargelos E, Poussard S, Brule C, Daury L, Cottin P. Calcium-dependent proteolytic system and muscle dysfunctions: a possible role of calpains in sarcopenia. Biochimie. 2008;90:359-368. (Pubitemid 351172567)
83. Suzuki K, Hata S, Kawabata Y, Sorimachi H. Structure, activation, and biology of calpain. Diabetes. 2004;53(SUPPL 1):S12-S18. (Pubitemid 38168687)
84. Sato K, Kawashima S. Calpain function in the modulation of signal transduction molecules. Biol Chem. 2001;382:743-751. (Pubitemid 32631711)
85. Huang Y, Wang KK. The calpain family and human disease. Trends Mol Med. 2001;7:355-362. (Pubitemid 32735021)
86. Carafoli E, Molinari M. Calpain: a protease in search of a function? Biochem Biophys Res Commun. 1998;247:193-203. (Pubitemid 28420799)
87. Sorimachi H, Ishiura S, Suzuki K. Structure and physiological function of calpains. Biochem J. 1997;328(part 3):721-732. (Pubitemid 28005767)
88. Singh RB, Dandekar SP, Elimban V, Gupta SK, Dhalla NS. Role of proteases in the pathophysiology of cardiac disease. Mol Cell Biochem. 2004;263:241-256. (Pubitemid 39256162)
89. Hernando V, Inserte J, Sartorio CL, Parra VM, Poncelas-Nozal M, Garcia-Dorado D. Calpain translocation and activation as pharmacological targets during myocardial ischemia/reperfusion. J Mol Cell Cardiol. 2010;49:271-279.
90. Iwamoto H, Miura T, Okamura T, Shirakawa K, Iwatate M, Kawamura S, Tatsuno H, Ikeda Y, Matsuzaki M. Calpain inhibitor-1 reduces infarct size and DNA fragmentation of myocardium in ischemic/reperfused rat heart. J Cardiovasc Pharmacol. 1999;33:580-586. (Pubitemid 29164821)
91. Ke L, Qi XY, Dijkhuis AJ, Chartier D, Nattel S, Henning RH, Kampinga HH, Brundel BJ. Calpain mediates cardiac troponin degradation and contractile dysfunction in atrial fibrillation. J Mol Cell Cardiol. 2008;45:685-693.
92. McDonough JL, Arrell DK, Van Eyk JE. Troponin I degradation and covalent complex formation accompanies myocardial ischemia/reperfusion injury. Circ Res. 1999;84:9-20. (Pubitemid 29074876)
93. Van Eyk JE, Powers F, Law W, Larue C, Hodges RS, Solaro RJ. Breakdown and release of myofilament proteins during ischemia and ischemia/reperfusion in rat hearts: identification of degradation products and effects on the pCa-force relation. Circ Res. 1998;82:261-271. (Pubitemid 28080109)
94. 2+-dependent proteolysis? Circ Res. 1996;78:455-465.
95. Inserte J, Barrabes JA, Hernando V, Garcia-Dorado D. Orphan targets for reperfusion injury. Cardiovasc Res. 2009;83:169-178.
96. Chen M, Won DJ, Krajewski S, Gottlieb RA. Calpain and mitochondria in ischemia/reperfusion injury. J Biol Chem. 2002;277:29181-29186.
97. Yang D, Ma S, Tan Y, Li D, Tang B, Zhang X, Sun M, Yang Y. Increased expression of calpain and elevated activity of calcineurin in the myocardium of patients with congestive heart failure. Int J Mol Med. 2010;26:159-164.
98. Razeghi P, Volpini KC, Wang ME, Youker KA, Stepkowski S, Taegtmeyer H. Mechanical unloading of the heart activates the calpain system. J Mol Cell Cardiol. 2007;42:449-452. (Pubitemid 46156947)
99. Frey N, Olson EN. Cardiac hypertrophy: the good, the bad, and the ugly. Annu Rev Physiol. 2003;65:45-79. (Pubitemid 38249147)
100. Molkentin JD, Robbins J. With great power comes great responsibility: using mouse genetics to study cardiac hypertrophy and failure. J Mol Cell Cardiol. 2009;46:130-136.
101. Sugden PH, Fuller SJ, Weiss SC, Clerk A. Glycogen synthase kinase 3 (GSK3) in the heart: a point of integration in hypertrophic signalling and a therapeutic target? A critical analysis. Br J Pharmacol. 2008;153(suppl 1):S137-S153. (Pubitemid 351341012)
102. Van der Heiden K, Cuhlmann S, Luong le A, Zakkar M, Evans PC. Role of nuclear factor kappaB in cardiovascular health and disease. Clin Sci (Lond). 2010;118:593-605.
103. Wilkins BJ, Dai YS, Bueno OF, Parsons SA, Xu J, Plank DM, Jones F, Kimball TR, Molkentin JD. Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res. 2004;94:110-118. (Pubitemid 38064105)
104. Letavernier E, Perez J, Bellocq A, Mesnard L, de Castro Keller A, Haymann JP, Baud L. Targeting the calpain/calpastatin system as a new strategy to prevent cardiovascular remodeling in angiotensin II-induced hypertension. Circ Res. 2008;102:720-728. (Pubitemid 351457854)
105. Shumway SD, Maki M, Miyamoto S. The PEST domain of IκBα is necessary and sufficient for in vitro degradation by μ-calpain. J Biol Chem. 1999;274:30874-30881. (Pubitemid 129576835)
106. Freund C, Schmidt-Ullrich R, Baurand A, Dunger S, Schneider W, Loser P, El-Jamali A, Dietz R, Scheidereit C, Bergmann MW. Requirement of nuclear factor-κB in angiotensin II-and isoproterenolinduced cardiac hypertrophy in vivo. Circulation. 2005;111:2319-2325. (Pubitemid 40647067)
107. Rouet-Benzineb P, Gontero B, Dreyfus P, Lafuma C. Angiotensin II induces nuclear factor-kappa B activation in cultured neonatal rat cardiomyocytes through protein kinase C signaling pathway. J Mol Cell Cardiol. 2000;32:1767-1778.
108. Wilkins BJ, De Windt LJ, Bueno OF, Braz JC, Glascock BJ, Kimball TF, Molkentin JD. Targeted disruption of NFATc3, but not NFATc4, reveals an intrinsic defect in calcineurin-mediated cardiac hypertrophic growth. Mol Cell Biol. 2002;22:7603-7613.
109. Burkard N, Becher J, Heindl C, Neyses L, Schuh K, Ritter O. Targeted proteolysis sustains calcineurin activation. Circulation. 2005;111:1045-1053. (Pubitemid 40354524)
110. Heidrich FM, Zhang K, Estrada M, Huang Y, Giordano FJ, Ehrlich BE. Chromogranin B regulates calcium signaling, nuclear factor kappaB activity, and brain natriuretic peptide production in cardiomyocytes. Circ Res. 2008;102:1230-1238.
111. Heidrich FM, Ehrlich BE. Calcium, calpains, and cardiac hypertrophy: a new link. Circ Res. 2009;104:e19-20.
112. Cowan BR, Young AA. Left ventricular hypertrophy and renin-angiotensin system blockade. Curr Hypertens Rep. 2009;11:167-172.
113. Barry SP, Townsend PA. What causes a broken heart: molecular insights into heart failure. Int Rev Cell Mol Biol. 2010;284:113-179.
114. Iizuka K, Kawaguchi H, Yasuda H. Calpain is activated by betaadrenergic receptor stimulation under hypoxic myocardial cell injury. Jpn Circ J. 1991;55:1086-1093.
115. Averna M, Stifanese R, De Tullio R, Passalacqua M, Salamino F, Pontremoli S, Melloni E. Functional role of HSP90 complexes with endothelial nitric-oxide synthase (eNOS) and calpain on nitric oxide generation in endothelial cells. J Biol Chem. 2008;283:29069-29076.
116. Smith IJ, Dodd SL. Calpain activation causes a proteasome-dependent increase in protein degradation and inhibits the Akt signalling pathway in rat diaphragm muscle. Exp Physiol. 2007;92:561-573. (Pubitemid 46608406)
117. Bellocq A, Doublier S, Suberville S, Perez J, Escoubet B, Fouqueray B, Puyol DR, Baud L. Somatostatin increases glucocorticoid binding and signaling in macrophages by blocking the calpain-specific cleavage of Hsp 90. J Biol Chem. 1999;274:36891-36896.
118. Minami Y, Kimura Y, Kawasaki H, Suzuki K, Yahara I. The carboxyterminal region of mammalian HSP90 is required for its dimerization and function in vivo. Mol Cell Biol. 1994;14:1459-1464. (Pubitemid 24036596)
119. Sato S, Fujita N, Tsuruo T. Modulation of Akt kinase activity by binding to Hsp90. Proc Natl Acad Sci USA. 2000;97:10832-10837.
120. Garcia-Cardena G, Fan R, Shah V, Sorrentino R, Cirino G, Papapetropoulos A, Sessa WC. Dynamic activation of endothelial nitric oxide synthase by Hsp90. Nature. 1998;392:821-824. (Pubitemid 28225323)
121. Johnston RK, Balasubramanian S, Kasiganesan H, Baicu CF, Zile MR, Kuppuswamy D. Beta3 integrin-mediated ubiquitination activates survival signaling during myocardial hypertrophy. FASEB J. 2009;23:2759-2771.
122. Brancaccio M, Hirsch E, Notte A, Selvetella G, Lembo G, Tarone G. Integrin signalling: the tug-of-war in heart hypertrophy. Cardiovasc Res. 2006;70:422-433.
123. Suryakumar G, Kasiganesan H, Balasubramanian S, Kuppuswamy D. Lack of beta3 integrin signaling contributes to calpain-mediated myocardial cell loss in pressure-overloaded myocardium. J Cardiovasc Pharmacol. 2010;55:567-573.
124. Li Y, Arnold JM, Pampillo M, Babwah AV, Peng T. Taurine prevents cardiomyocyte death by inhibiting NADPH oxidase-mediated calpain activation. Free Radic Biol Med. 2009;46:51-61.
125. Franchini KG, Clemente CF, Marin TM. Focal adhesion kinase signaling in cardiac hypertrophy and failure. Braz J Med Biol Res. 2009;42:44-52.
126. Lal H, Verma SK, Foster DM, Golden HB, Reneau JC, Watson LE, Singh H, Dostal DE. Integrins and proximal signaling mechanisms in cardiovascular disease. Front Biosci. 2009;14:2307-2334.
127. Sandmann S, Yu M, Unger T. Transcriptional and translational regulation of calpain in the rat heart after myocardial infarction: effects of AT (1) and AT (2) receptor antagonists and ACE inhibitor. Br J Pharmacol. 2001;132:767-777. (Pubitemid 32165193)
128. Sorimachi Y, Harada K, Saido TC, Ono T, Kawashima S, Yoshida K. Downregulation of calpastatin in rat heart after brief ischemia and reperfusion. J Biochem. 1997;122:743-748. (Pubitemid 27474943)
129. 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. 2006;47:413-421. (Pubitemid 44309695)
130. Li X, Li Y, Shan L, Shen E, Chen R, Peng T. Over-expression of calpastatin inhibits calpain activation and attenuates myocardial dysfunction during endotoxaemia. Cardiovasc Res. 2009;83:72-79.
131. Maekawa A, Lee JK, Nagaya T, Kamiya K, Yasui K, Horiba M, Miwa K, Uzzaman M, Maki M, Ueda Y, Kodama I. Overexpression of calpastatin by gene transfer prevents troponin I degradation and ameliorates contractile dysfunction in rat hearts subjected to ischemia/reperfusion. J Mol Cell Cardiol. 2003;35:1277-1284. (Pubitemid 37163534)
132. 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. 2008;295:H314-H326.
133. Greyson CR, Schwartz GG, Lu L, Ye S, Helmke S, Xu Y, Ahmad H. Calpain inhibition attenuates right ventricular contractile dysfunction after acute pressure overload. J Mol Cell Cardiol. 2008;44:59-68.
134. Arthur GD, Belcastro AN. A calcium stimulated cysteine protease involved in isoproterenol induced cardiac hypertrophy. Mol Cell Biochem. 1997;176:241-248. (Pubitemid 27491489)
135. Pietsch M, Chua KC, Abell AD. Calpains: attractive targets for the development of synthetic inhibitors. Curr Top Med Chem. 2010;10:270-293.