Targeted inhibition of calpain reduces myocardial hypertrophy and fibrosis in mouse models of type 1 diabetes

Diabetes

Volumn 60, Issue 11, 2011, Pages 2985-2994

  Li, Ying ^a   Ma, Jian ^a   Zhu, Huaqing ^a   Singh, Manpreet ^a   Hill, David ^a   Greer, Peter A ^b,c   Arnold, J Malcolm ^a   Abel, E Dale ^d   Peng, Tianqing ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

^c QUEEN S UNIVERSITY   (Canada)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CALPASTATIN; COLLAGEN; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MATRIX METALLOPROTEINASE; TRANSCRIPTION FACTOR NFAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME INHIBITION; FIBROBLAST; GENE EXPRESSION; HEART FUNCTION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART VENTRICLE HYPERTROPHY; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CALCIUM-BINDING PROTEINS; CALPAIN; CARDIOMYOPATHY, HYPERTROPHIC; CELL PROLIFERATION; CELLS, CULTURED; DIABETES MELLITUS, TYPE 1; DIABETIC CARDIOMYOPATHIES; DISEASE MODELS, ANIMAL; FIBROSIS; GENE EXPRESSION REGULATION; HEART; HYPERGLYCEMIA; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MOLECULAR TARGETED THERAPY; MYOCARDIUM; STREPTOZOCIN;

EID: 80755168871     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db10-1333     Document Type: Article

References (49)

1. Boudina S, Abel ED. Diabetic cardiomyopathy revisited. Circulation 2007;115:3213-3223 (Pubitemid 47012236)
2. Di Filippo C, Marfella R, Cuzzocrea S, et al. Hyperglycemia in streptozotocin-induced diabetic rat increases infarct size associated with low levels of myocardial HO-1 during ischemia/reperfusion. Diabetes 2005;54:803-810 (Pubitemid 40322085)
3. Greer JJ, Ware DP, Lefer DJ. Myocardial infarction and heart failure in the db/db diabetic mouse. Am J Physiol Heart Circ Physiol 2006;290:H146-H153
4. Schramm TK, Gislason GH, Køber L, et al. Diabetes patients requiring glucose-lowering therapy and nondiabetics with a prior myocardial infarction carry the same cardiovascular risk: a population study of 3.3 million people. Circulation 2008;117:1945-1954 (Pubitemid 351543470)
5. Fang ZY, Prins JB, Marwick TH. Diabetic cardiomyopathy: evidence, mechanisms, and therapeutic implications. Endocr Rev 2004;25:543-567 (Pubitemid 39096070)
6. Poornima IG, Parikh P, Shannon RP. Diabetic cardiomyopathy: the search for a unifying hypothesis. Circ Res 2006;98:596-605
7. Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol Rev 2003;83:731-801 (Pubitemid 36828925)
8. Hanna RA, Campbell RL, Davies PL. Calcium-bound structure of calpain and its mechanism of inhibition by calpastatin. Nature 2008;456:409-412
9. Suzuki K, Hata S, Kawabata Y, Sorimachi H. Structure, activation, and biology of calpain. Diabetes 2004;53(Suppl. 1):S12-S18 (Pubitemid 38168687)
10. Arthur JS, Elce JS, Hegadorn C, Williams K, Greer PA. Disruption of the murine calpain small subunit gene, Capn4: calpain is essential for embryonic development but not for cell growth and division. Mol Cell Biol 2000;20:4474-4481 (Pubitemid 30346642)
11. Peltier J, Bellocq A, Perez J, et al. Calpain activation and secretion promote glomerular injury in experimental glomerulonephritis: evidence from calpastatin-transgenic mice. J Am Soc Nephrol 2006;17:3415-3423 (Pubitemid 44865284)
12. 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
13. 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
14. Li Y, Li Y, Feng Q, Arnold M, Peng T. Calpain activation contributes to hyperglycaemia-induced apoptosis in cardiomyocytes. Cardiovasc Res 2009;84:100-110
15. Chen M, Won DJ, Krajewski S, Gottlieb RA. Calpain and mitochondria in ischemia/reperfusion injury. J Biol Chem 2002;277:29181-29186
16. Khalil PN, Neuhof C, Huss R, et al. Calpain inhibition reduces infarct size and improves global hemodynamics and left ventricular contractility in a porcine myocardial ischemia/reperfusion model. Eur J Pharmacol 2005;528:124-131 (Pubitemid 41773662)
17. Mani SK, Balasubramanian S, Zavadzkas JA, et al. Calpain inhibition preserves myocardial structure and function following myocardial infarction. Am J Physiol Heart Circ Physiol 2009;297:H1744-H1751
18. Wilkins BJ, Dai YS, Bueno OF, et al. Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res 2004;94:110-118 (Pubitemid 38064105)
19. Bourajjaj M, Armand AS, da Costa Martins PA, et al. NFATc2 is a necessary mediator of calcineurin-dependent cardiac hypertrophy and heart failure. J Biol Chem 2008;283:22295-22303
20. 2+ signal integrators. Proc Natl Acad Sci USA 2008;105:2859-2864
21. Yang D, Ma S, Tan Y, et al. 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
22. Tan Y, Dourdin N, Wu C, De Veyra T, Elce JS, Greer PA. Conditional disruption of ubiquitous calpains in the mouse. Genesis 2006;44:297-303
23. Abel ED, Kaulbach HC, Tian R, et al. Cardiac hypertrophy with preserved contractile function after selective deletion of GLUT4 from the heart. J Clin Invest 1999;104:1703-1714 (Pubitemid 30053187)
24. Bashey RI, Donnelly M, Insinga F, Jimenez SA. Growth properties and biochemical characterization of collagens synthesized by adult rat heart fibroblasts in culture. J Mol Cell Cardiol 1992;24:691-700
25. Li J, Zhu H, Shen E, Wan L, Arnold JM, Peng T. Deficiency of rac1 blocks NADPH oxidase activation, inhibits endoplasmic reticulum stress, and reduces myocardial remodeling in a mouse model of type 1 diabetes. Diabetes 2010;59:2033-2042
26. Dourdin N, Bhatt AK, Dutt P, et al. Reduced cell migration and disruption of the actin cytoskeleton in calpain-deficient embryonic fibroblasts. J Biol Chem 2001;276:48382-48388
27. Peng T, Lu X, Lei M, Moe GW, Feng Q. Inhibition of p38 MAPK decreases myocardial TNF-alpha expression and improves myocardial function and survival in endotoxemia. Cardiovasc Res 2003;59:893-900 (Pubitemid 38366245)
28. Peng T, Zhang T, Lu X, Feng Q. JNK1/c-fos inhibits cardiomyocyte TNF-alpha expression via a negative crosstalk with ERK and p38 MAPK in endotoxaemia. Cardiovasc Res 2009;81:733-741
29. van Rooij E, Doevendans PA, de Theije CC, Babiker FA, Molkentin JD, de Windt LJ. Requirement of nuclear factor of activated T-cells in calcineurin-mediated cardiomyocyte hypertrophy. J Biol Chem 2002;277:48617-48626 (Pubitemid 35470824)
30. Li Y, Ha T, Gao X, et al. NF-kappaB activation is required for the development of cardiac hypertrophy in vivo. Am J Physiol Heart Circ Physiol 2004;287:H1712-H1720 (Pubitemid 39313278)
31. Wilkins BJ, Dai YS, Bueno OF, et al. Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res 2004;94:110-118 (Pubitemid 38064105)
32. Zelarayan L, Renger A, Noack C, et al. NF-kappaB activation is required for adaptive cardiac hypertrophy. Cardiovasc Res 2009;84:416-424
33. Chen F, Lu Y, Kuhn DC, et al. Calpain contributes to silica-induced I kappa B-alpha degradation and nuclear factor-kappa B activation. Arch Biochem Biophys 1997;342:383-388 (Pubitemid 27251261)
34. Asbun J, Villarreal FJ. The pathogenesis of myocardial fibrosis in the setting of diabetic cardiomyopathy. J Am Coll Cardiol 2006;47:693-700 (Pubitemid 43243087)
35. Wilson EM, Spinale FG. Myocardial remodelling and matrix metalloproteinases in heart failure: turmoil within the interstitium. Ann Med 2001;33:623-634 (Pubitemid 34081500)
36. Taegtmeyer H, McNulty P, Young ME. Adaptation and maladaptation of the heart in diabetes: Part I: general concepts. Circulation 2002;105:1727-1733 (Pubitemid 34298619)
37. McKinsey TA, Kass DA. Small-molecule therapies for cardiac hypertrophy: moving beneath the cell surface. Nat Rev Drug Discov 2007;6:617-635 (Pubitemid 47207749)
38. Letavernier E, Perez J, Bellocq A, et al. 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)
39. Gupta S, Young D, Maitra RK, et al. Prevention of cardiac hypertrophy and heart failure by silencing of NF-kappaB. J Mol Biol 2008;375:637-649
40. Van der Heiden K, Cuhlmann S, Luong A, Zakkar M, Evans PC. Role of nuclear factor kappaB in cardiovascular health and disease. Clin Sci (Lond) 2010;118:593-605
41. Heidrich FM, Ehrlich BE. Calcium, calpains, and cardiac hypertrophy: a new link. Circ Res 2009;104:e19-e20
42. Takeda N, Manabe I, Uchino Y, et al. Cardiac fibroblasts are essential for the adaptive response of the murine heart to pressure overload. J Clin Invest 2010;120:254-265
43. Hamid T, Guo SZ, Kingery JR, Xiang X, Dawn B, Prabhu SD. Cardiomyocyte NF-kappaB p65 promotes adverse remodeling, apoptosis and endoplasmic reticulum stress in heart failure. Cardiovasc Res 2011;89:129-138
44. Onai Y, Suzuki J, Maejima Y, et al. Inhibition of NF-kappaB improves left ventricular remodeling and cardiac dysfunction after myocardial infarction. Am J Physiol Heart Circ Physiol 2007;292:H530-H538 (Pubitemid 46105217)
45. Petrov VV, Fagard RH, Lijnen PJ. Stimulation of collagen production by transforming growth factor-beta1 during differentiation of cardiac fibroblasts to myofibroblasts. Hypertension 2002;39:258-263 (Pubitemid 34165225)
46. Camp TM, Tyagi SC, Senior RM, Hayden MR, Tyagi SC. Gelatinase B(MMP-9) an apoptotic factor in diabetic transgenic mice. Diabetologia 2003;46:1438-1445 (Pubitemid 37297215)
47. Westermann D, Rutschow S, Jäger S, et al. Contributions of inflammation and cardiac matrix metalloproteinase activity to cardiac failure in diabetic cardiomyopathy: the role of angiotensin type 1 receptor antagonism. Diabetes 2007;56:641-646 (Pubitemid 46348458)
48. Yaras N, Sariahmetoglu M, Bilginoglu A, et al. Protective action of doxycycline against diabetic cardiomyopathy in rats. Br J Pharmacol 2008;155:1174-1184
49. Moshal KS, Singh M, Sen U, et al. Homocysteine-mediated activation and mitochondrial translocation of calpain regulates MMP-9 in MVEC. Am J Physiol Heart Circ Physiol 2006;291:H2825-H2835 (Pubitemid 44904083)