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Calcium-Handling Proteins in Diabetic Cardiomyopathy

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Diabetic Cardiomyopathy

Part of the book series: Advances in Biochemistry in Health and Disease ((ABHD,volume 9))

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Abstract

Diabetes mellitus increases the risk of cardiomyopathy independently of underlying comorbidities, and heart failure is a major cause of death in diabetic patients. The development of this distinct cardiomyopathy in both type 1 and type 2 diabetes is associated with complex and multifactorial cellular and molecular perturbations. It is widely recognized that cardiac dysfunction in chronic diabetes involves hormonal imbalance, oxidative stress, proteases activation, defects in Ca2+ cycling, and varying degrees of subcellular remodeling of organelles.

Ca2+ -handling abnormalities in diabetic cardiomyocytes have primarily been attributed to changes in the sarcolemmal Na+–Ca2+ exchanger, L-type Ca2+ channel, Na+–K+ ATPase, and Na+–H+ exchanger proteins as well as Ca2+-release channels and Ca2+-pump proteins embedded in the sarcoplasmic reticulum. Intracellular Ca2+ overload has been implicated in the impairment of excitation–contraction coupling as a result of alterations in Ca2+-entry, Ca2+-removal, Ca2+-uptake, and Ca2+-release processes in the diabetic heart. These observations are consistent with the view that defects in Ca2+-handling proteins play a critical role in the pathogenesis of cardiac dysfunction during the development of diabetic cardiomyopathy.

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References

  1. Go AS, Mozaffarian D, Roger VL et al (2013) Heart disease and stroke statistics—2013 update: a report from the American Heart Association. Circulation 127:e6–e245

    PubMed  Google Scholar 

  2. Schaffer SW (1991) Cardiomyopathy associated with noninsulin-dependent diabetes. Mol Cell Biochem 107:1–20

    CAS  PubMed  Google Scholar 

  3. Lebeche D, Davidoff AJ, Hajjar RJ (2008) Interplay between impaired calcium regulation and insulin signaling abnormalities in diabetic cardiomyopathy. Nat Clin Pract Cardiovasc Med 5:715–724

    CAS  PubMed  Google Scholar 

  4. Hayat SA, Patel B, Khattar RS, Malik RA (2004) Diabetic cardiomyopathy: mechanisms, diagnosis and treatment. Clin Sci (Lond) 107:539–557

    CAS  Google Scholar 

  5. Boudina S, Abel ED (2007) Diabetic cardiomyopathy revisited. Circulation 115:3213–3223

    PubMed  Google Scholar 

  6. Dhalla NS, Takeda N, Rodriguez-Leyva D, Elimban V (2013) Mechanisms of subcellular remodeling in heart failure due to diabetes. Heart Fail Rev. doi:10.1007/s10741-013-9385-8

    Google Scholar 

  7. Ligeti L, Szenczi O, Prestia CM et al (2006) Altered calcium handling is an early sign of streptozotocin-induced diabetic cardiomyopathy. Int J Mol Med 17:1035–1043

    CAS  PubMed  Google Scholar 

  8. Fein FS, Sonnenblick EH (1994) Diabetic cardiomyopathy. Cardiovasc Drugs Ther 8:65–73

    CAS  PubMed  Google Scholar 

  9. Op den Buijs J, Miklós Z, Van Riel NAW et al (2005) β-Adrenergic activation reveals impaired cardiac calcium handling at early stage of diabetes. Life Sci 76:1083–1098

    CAS  PubMed  Google Scholar 

  10. Hattori Y, Matsuda N, Kimura J et al (2000) Diminished function and expression of the cardiac Na+- Ca2+ exchanger in diabetic rats: implication in Ca2+ overload. J Physiol 527(Pt 1):85–94

    CAS  PubMed  Google Scholar 

  11. Ren J, Davidoff AJ (1997) Diabetes rapidly induces contractile dysfunctions in isolated ventricular myocytes. Am J Physiol 272:H148–H158

    CAS  PubMed  Google Scholar 

  12. Bai S, Sun J, Wu H et al (2012) Decrease in calcium-sensing receptor in the progress of diabetic cardiomyopathy. Diabetes Res Clin Pract 95:378–385

    CAS  PubMed  Google Scholar 

  13. Kralik P, Ye G, Metreveli N et al (2005) Cardiomyocyte dysfunction in models of type 1 and type 2 diabetes. Cardiovasc Toxicol 5:285–292

    PubMed  Google Scholar 

  14. Dhalla NS, Saini HK, Tappia PS et al (2007) Potential role and mechanisms of subcellular remodeling in cardiac dysfunction due to ischemic heart disease. J Cardiovasc Med (Hagerstown) 8:238–250

    Google Scholar 

  15. Halling DB, Aracena-Parks P, Hamilton SL (2005) Regulation of voltage-gated Ca2+ channels by calmodulin. Sci STKE 2005:re15

    PubMed  Google Scholar 

  16. Xu M, Zhou P, Xu S-M et al (2007) Intermolecular failure of L-type Ca2+ channel and ryanodine receptor signaling in hypertrophy. PLoS Biol 5:e21

    PubMed  PubMed Central  Google Scholar 

  17. Petrovic MM, Vales K, Putnikovic B et al (2008) Ryanodine receptors, voltage-gated calcium channels and their relationship with protein kinase A in the myocardium. Physiol Res 57:141–149

    CAS  PubMed  Google Scholar 

  18. Shaw RM, Colecraft HM (2013) L-type calcium channel targeting and local signalling in cardiac myocytes. Cardiovasc Res 98:177–186

    CAS  PubMed  Google Scholar 

  19. Splawski I, Timothy KW, Sharpe LM et al (2004) Ca(V)1.2 calcium channel dysfunction causes a multisystem disorder including arrhythmia and autism. Cell 119:19–31

    CAS  PubMed  Google Scholar 

  20. Shimoni Y, Firek L, Severson D, Giles W (1994) Short-term diabetes alters K+ currents in rat ventricular myocytes. Circ Res 74:620–628

    CAS  PubMed  Google Scholar 

  21. Lacombe VA, Viatchenko-Karpinski S, Terentyev D et al (2007) Mechanisms of impaired calcium handling underlying subclinical diastolic dysfunction in diabetes. Am J Physiol 293:R1787–R1797

    CAS  Google Scholar 

  22. Lengyel C, Virág L, Bíró T et al (2007) Diabetes mellitus attenuates the repolarization reserve in mammalian heart. Cardiovasc Res 73:512–520

    CAS  PubMed  Google Scholar 

  23. Lu Z, Ballou LM, Jiang Y-P et al (2011) Restoration of defective L-type Ca2+ current in cardiac myocytes of type 2 diabetic db/db mice by Akt and PKC-ι. J Cardiovasc Pharmacol 58:439–445

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Lu Z, Jiang Y-P, Xu X-H et al (2007) Decreased L-type Ca2+ current in cardiac myocytes of type 1 diabetic akita mice due to reduced phosphatidylinositol 3-kinase signaling. Diabetes 56:2780–2789

    CAS  PubMed  Google Scholar 

  25. Pereira L, Matthes J, Schuster I et al (2006) Mechanisms of [Ca2+]i transient decrease in cardiomyopathy of db/db type 2 diabetic mice. Diabetes 55:608–615

    CAS  PubMed  Google Scholar 

  26. Malhotra A, Sanghi V (1997) Regulation of contractile proteins in diabetic heart. Cardiovasc Res 34:34–40

    CAS  PubMed  Google Scholar 

  27. Sun H, Kerfant B-G, Zhao D et al (2006) Insulin-like growth factor-1 and PTEN deletion enhance cardiac L-type Ca2+ currents via increased PI3Kα/PKB signaling. Circ Res 98:1390–1397

    CAS  PubMed  Google Scholar 

  28. Gómez AM, Valdivia HH, Cheng H et al (1997) Defective excitation-contraction coupling in experimental cardiac hypertrophy and heart failure. Science 276:800–806

    PubMed  Google Scholar 

  29. Bénitah J-P, Kerfant BG, Vassort G et al (2002) Altered communication between L-type calcium channels and ryanodine receptors in heart failure. Front Biosci 7:e263–e275

    PubMed  Google Scholar 

  30. Shao C-H, Rozanski GJ, Patel KP, Bidasee KR (2007) Dyssynchronous (non-uniform) Ca2+ release in myocytes from streptozotocin-induced diabetic rats. J Mol Cell Cardiol 42:234–246

    CAS  PubMed  Google Scholar 

  31. Eisner DA, Choi HS, Diaz ME et al (2000) Integrative analysis of calcium cycling in cardiac muscle. Circ Res 87:1087–1094

    CAS  PubMed  Google Scholar 

  32. Bers DM (2008) Calcium cycling and signaling in cardiac myocytes. Annu Rev Physiol 70:23–49

    CAS  PubMed  Google Scholar 

  33. Chattou S, Diacono J, Feuvray D (1999) Decrease in sodium-calcium exchange and calcium currents in diabetic rat ventricular myocytes. Acta Physiol Scand 166:137–144

    CAS  PubMed  Google Scholar 

  34. Wold LE, Ceylan-Isik AF, Fang CX et al (2006) Metallothionein alleviates cardiac dysfunction in streptozotocin-induced diabetes: role of Ca2+ cycling proteins, NADPH oxidase, poly(ADP-Ribose) polymerase and myosin heavy chain isozyme. Free Radic Biol Med 40:1419–1429

    CAS  PubMed  Google Scholar 

  35. Choi KM, Zhong Y, Hoit BD et al (2002) Defective intracellular Ca2+ signaling contributes to cardiomyopathy in type 1 diabetic rats. Am J Physiol Heart Circ Physiol 283:H1398–H1408

    CAS  PubMed  Google Scholar 

  36. Schaffer SW, Ballard-Croft C, Boerth S, Allo SN (1997) Mechanisms underlying depressed Na+-Ca2+ exchanger activity in the diabetic heart. Cardiovasc Res 34:129–136

    CAS  PubMed  Google Scholar 

  37. Pierce GN, Dhalla NS (1983) Sarcolemmal Na+–K+-ATPase activity in diabetic rat heart. Am J Physiol 245:C241–C247

    CAS  PubMed  Google Scholar 

  38. Kjeldsen K, Braendgaard H, Sidenius P et al (1987) Diabetes decreases Na+–K+ pump concentration in skeletal muscles, heart ventricular muscle, and peripheral nerves of rat. Diabetes 36:842–848

    CAS  PubMed  Google Scholar 

  39. Golfman L, Dixon IM, Takeda N et al (1998) Cardiac sarcolemmal Na+–Ca2+ exchange and Na+–K+ATPase activities and gene expression in alloxan-induced diabetes in rats. Mol Cell Biochem 188:91–101

    CAS  PubMed  Google Scholar 

  40. Schaffer SW, Allo S, Punna S, White T (1991) Defective response to cAMP-dependent protein kinase in non-insulin-dependent diabetic heart. Am J Physiol 261:E369–E376

    CAS  PubMed  Google Scholar 

  41. Allo SN, Lincoln TM, Wilson GL et al (1991) Non-insulin-dependent diabetes-induced defects in cardiac cellular calcium regulation. Am J Physiol 260:C1165–C1171

    CAS  PubMed  Google Scholar 

  42. Wold LE, Dutta K, Mason MM et al (2005) Impaired SERCA function contributes to cardiomyocyte dysfunction in insulin resistant rats. J Mol Cell Cardiol 39:297–307

    CAS  PubMed  Google Scholar 

  43. Belke DD, Swanson EA, Dillmann WH (2004) Decreased sarcoplasmic reticulum activity and contractility in diabetic db/db mouse heart. Diabetes 53:3201–3208

    CAS  PubMed  Google Scholar 

  44. Stubbs CD, Smith AD (1984) The modification of mammalian membrane polyunsaturated fatty acid composition in relation to membrane fluidity and function. Biochim Biophys Acta 779:89–137

    CAS  PubMed  Google Scholar 

  45. Vér Á, Szántó I, Bányász T et al (1997) Changes in the expression of Na+–K+-ATPase isoenzymes in the left ventricle of diabetic rat hearts: effect of insulin treatment. Diabetologia 40:1255–1262

    PubMed  Google Scholar 

  46. Dhalla NS, Liu X, Panagia V, Takeda N (1998) Subcellular remodeling and heart dysfunction in chronic diabetes. Cardiovasc Res 40:239–247

    CAS  PubMed  Google Scholar 

  47. Gerbi A, Barbey O, Raccah D et al (1997) Alteration of Na, K-ATPase isoenzymes in diabetic cardiomyopathy: effect of dietary supplementation with fish oil (n-3 fatty acids) in rats. Diabetologia 40:496–505

    CAS  PubMed  Google Scholar 

  48. Chen S, Khan ZA, Karmazyn M, Chakrabarti S (2007) Role of endothelin-1, sodium hydrogen exchanger-1 and mitogen activated protein kinase (MAPK) activation in glucose-induced cardiomyocyte hypertrophy. Diabetes Metab Res Rev 23:356–367

    PubMed  Google Scholar 

  49. Pierce GN, Ramjiawan B, Dhalla NS, Ferrari R (1990) Na+/H+exchange in cardiac sarcolemmal vesicles isolated from diabetic rats. Am J Physiol 258:H255–H261

    CAS  PubMed  Google Scholar 

  50. Le Prigent K, Lagadic-Gossmann D, Feuvray D (1997) Modulation by pH0 and intracellular Ca2+ of Na+–H+ exchange in diabetic rat isolated ventricular myocytes. Circ Res 80:253–260

    PubMed  Google Scholar 

  51. Khandoudi N, Bernard M, Cozzone P, Feuvray D (1990) Intracellular pH and role of Na+–H+ exchange during ischaemia and reperfusion of normal and diabetic rat hearts. Cardiovasc Res 24:873–878

    CAS  PubMed  Google Scholar 

  52. Darmellah A, Baetz D, Prunier F et al (2007) Enhanced activity of the myocardial Na+–H+ exchanger contributes to left ventricular hypertrophy in the Goto–Kakizaki rat model of type 2 diabetes: critical role of Akt. Diabetologia 50:1335–1344

    CAS  PubMed  Google Scholar 

  53. Jandeleit-Dahm K, Hannan KM, Farrelly CA et al (2000) Diabetes-induced vascular hypertrophy is accompanied by activation of Na+–H+ exchange and prevented by Na+–H+ exchange inhibition. Circ Res 87:1133–1140

    CAS  PubMed  Google Scholar 

  54. Kusumoto K, Haist JV, Karmazyn M (2001) Na+/H+ exchange inhibition reduces hypertrophy and heart failure after myocardial infarction in rats. Am J Physiol Heart Circ Physiol 280:H738–H745

    CAS  PubMed  Google Scholar 

  55. Baartscheer A, Hardziyenka M, Schumacher CA et al (2008) Chronic inhibition of the Na+–H+-exchanger causes regression of hypertrophy, heart failure, and ionic and electrophysiological remodelling. Br J Pharmacol 154:1266–1275

    CAS  PubMed  Google Scholar 

  56. Vial G, Dubouchaud H, Couturier K et al (2008) Na+–H+ exchange inhibition with cariporide prevents alterations of coronary endothelial function in streptozotocin-induced diabetes. Mol Cell Biochem 310:93–102

    CAS  PubMed  Google Scholar 

  57. Meissner G (2004) Molecular regulation of cardiac ryanodine receptor ion channel. Cell Calcium 35:621–628

    CAS  PubMed  Google Scholar 

  58. Bidasee KR, Dinçer ÜD, Besch HR (2001) Ryanodine receptor dysfunction in hearts of streptozotocin-induced diabetic rats. Mol Pharmacol 60:1356–1364

    CAS  PubMed  Google Scholar 

  59. Lanner JT (2012) Ryanodine receptor physiology and its role in disease. Adv Exp Med Biol 740:217–234

    CAS  PubMed  Google Scholar 

  60. Dincer UD, Araiza A, Knudson JD et al (2006) Dysfunction of cardiac ryanodine receptors in the metabolic syndrome. J Mol Cell Cardiol 41:108–114

    CAS  PubMed  Google Scholar 

  61. Netticadan T, Temsah RM, Kent A et al (2001) Depressed levels of Ca2+-cycling proteins may underlie sarcoplasmic reticulum dysfunction in the diabetic heart. Diabetes 50:2133–2138

    CAS  PubMed  Google Scholar 

  62. Lehnart SE, Mongillo M, Bellinger A et al (2008) Leaky Ca2+ release channel/ryanodine receptor 2 causes seizures and sudden cardiac death in mice. J Clin Invest 118:2230–2245

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Turan B, Vassort G (2011) Ryanodine receptor: a new therapeutic target to control diabetic cardiomyopathy. Antioxid Redox Signal 15:1847–1861

    CAS  PubMed  Google Scholar 

  64. Bidasee K, Nallani K, Henry B et al (2003) Chronic diabetes alters function and expression of ryanodine receptor calcium-release channels in rat hearts. Mol Cell Biochem 249:113–123

    CAS  PubMed  Google Scholar 

  65. Dhalla NS, Temsah RM, Netticadan T (2000) Role of oxidative stress in cardiovascular diseases. J Hypertens 18:655–673

    CAS  PubMed  Google Scholar 

  66. Bidasee KR, Nallani K, Besch HR, Dincer UD (2003) Streptozotocin-induced diabetes increases disulfide bond formation on cardiac ryanodine receptor (RyR2). J Pharmacol Exp Ther 305:989–998

    CAS  PubMed  Google Scholar 

  67. Wolff SP, Jiang ZY, Hunt JV (1991) Protein glycation and oxidative stress in diabetes mellitus and ageing. Free Radic Biol Med 10:339–352

    CAS  PubMed  Google Scholar 

  68. Hund TJ, Ziman AP, Lederer WJ, Mohler PJ (2008) The cardiac IP3 receptor: uncovering the role of “the other” calcium-release channel. J Mol Cell Cardiol 45:159–161

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Mackenzie L, Bootman MD, Laine M et al (2002) The role of inositol 1,4,5-trisphosphate receptors in Ca2+ signalling and the generation of arrhythmias in rat atrial myocytes. J Physiol 541:395–409

    CAS  PubMed  Google Scholar 

  70. Zima AV, Blatter LA (2004) Inositol-1,4,5-trisphosphate-dependent Ca2+ signalling in cat atrial excitation-contraction coupling and arrhythmias. J Physiol 555:607–615

    CAS  PubMed  Google Scholar 

  71. Fauconnier J, Lanner JT, Zhang S-J et al (2005) Insulin and inositol 1,4,5-trisphosphate trigger abnormal cytosolic Ca2+ transients and reveal mitochondrial Ca2+ handling defects in cardiomyocytes of ob/ob mice. Diabetes 54:2375–2381

    CAS  PubMed  Google Scholar 

  72. Zhou B-Q, Hu S-J, Wang G-B (2006) The analysis of ultrastructure and gene expression of sarco/endoplasmic reticulum calcium handling proteins in alloxan-induced diabetic rat myocardium. Acta Cardiol 61:21–27

    PubMed  Google Scholar 

  73. Guner S, Arioglu E, Tay A et al (2004) Diabetes decreases mRNA levels of calcium-release channels in human atrial appendage. Mol Cell Biochem 263:143–150

    CAS  PubMed  Google Scholar 

  74. Dhalla NS, Rangi S, Zieroth S, Xu Y-J (2012) Alterations in sarcoplasmic reticulum and mitochondrial functions in diabetic cardiomyopathy. Exp Clin Cardiol 17:115–120

    PubMed  PubMed Central  Google Scholar 

  75. Dutta K, Carmody MW, Cala SE, Davidoff AJ (2002) Depressed PKA activity contributes to impaired SERCA function and is linked to the pathogenesis of glucose-induced cardiomyopathy. J Mol Cell Cardiol 34:985–996

    CAS  PubMed  Google Scholar 

  76. Davidoff AJ, Davidson MB, Carmody MW et al (2004) Diabetic cardiomyocyte dysfunction and myocyte insulin resistance: role of glucose-induced PKC activity. Mol Cell Biochem 262:155–163

    CAS  PubMed  Google Scholar 

  77. Zhong Y, Ahmed S, Grupp IL, Matlib MA (2001) Altered SR protein expression associated with contractile dysfunction in diabetic rat hearts. Am J Physiol Heart Circ Physiol 281:H1137–H1147

    CAS  PubMed  Google Scholar 

  78. Bidasee KR, Nallani K, Yu Y et al (2003) Chronic diabetes increases advanced glycation end products on cardiac ryanodine receptors/calcium-release channels. Diabetes 52:1825–1836

    CAS  PubMed  Google Scholar 

  79. Bidasee KR, Zhang Y, Shao CH et al (2004) Diabetes increases formation of advanced glycation end products on sarco(endo)plasmic reticulum Ca2+-ATPase. Diabetes 53:463–473

    CAS  PubMed  Google Scholar 

  80. Abe T, Ohga Y, Tabayashi N et al (2002) Left ventricular diastolic dysfunction in type 2 diabetes mellitus model rats. Am J Physiol Heart Circ Physiol 282:H138–H148

    CAS  PubMed  Google Scholar 

  81. Fredersdorf S, Thumann C, Zimmermann WH et al (2012) Increased myocardial SERCA expression in early type 2 diabetes mellitus is insulin dependent: in vivo and in vitro data. Cardiovasc Diabetol 11:57

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Trost SU, Belke DD, Bluhm WF et al (2002) Overexpression of the sarcoplasmic reticulum Ca2+-ATPase improves myocardial contractility in diabetic cardiomyopathy. Diabetes 51:1166–1171

    CAS  PubMed  Google Scholar 

  83. Vetter R, Rehfeld U, Reissfelder C et al (2002) Transgenic overexpression of the sarcoplasmic reticulum Ca2+ ATPase improves reticular Ca2+ handling in normal and diabetic rat hearts. FASEB J 16:1657–1659

    CAS  PubMed  Google Scholar 

  84. Golfman L, Dixon IC, Takeda N et al (1999) Differential changes in cardiac myofibrillar and sarcoplasmic reticular gene expression in alloxan-induced diabetes. Mol Cell Biochem 200:15–25

    CAS  PubMed  Google Scholar 

  85. Cai L, Kang YJ (2001) Oxidative stress and diabetic cardiomyopathy: a brief review. Cardiovasc Toxicol 1:181–193

    CAS  PubMed  Google Scholar 

  86. Boudina S, Abel ED (2006) Mitochondrial uncoupling: a key contributor to reduced cardiac efficiency in diabetes. Physiology (Bethesda) 21:250–258

    CAS  Google Scholar 

  87. An D, Rodrigues B (2006) Role of changes in cardiac metabolism in development of diabetic cardiomyopathy. Am J Physiol Heart Circ Physiol 291:H1489–H1506

    CAS  PubMed  Google Scholar 

  88. Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552: 335–344

    CAS  PubMed  Google Scholar 

  89. Chen Y, Saari JT, Kang YJ (1994) Weak antioxidant defenses make the heart a target for damage in copper-deficient rats. Free Radic Biol Med 17:529–536

    CAS  PubMed  Google Scholar 

  90. Yan SD, Schmidt AM, Anderson GM et al (1994) Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J Biol Chem 269:9889–9897

    CAS  PubMed  Google Scholar 

  91. Müller AL, Dhalla NS (2012) Role of various proteases in cardiac remodeling and progression of heart failure. Heart Fail Rev 17:395–409

    PubMed  Google Scholar 

  92. Dhalla NS, Rangi S, Babick AP et al (2012) Cardiac remodeling and subcellular defects in heart failure due to myocardial infarction and aging. Heart Fail Rev 17:671–681

    PubMed  Google Scholar 

  93. Clark RJ, McDonough PM, Swanson E et al (2003) Diabetes and the accompanying hyperglycemia impairs cardiomyocyte calcium cycling through increased nuclear O-GlcNAcylation. J Biol Chem 278:44230–44237

    CAS  PubMed  Google Scholar 

  94. Belin RJ, Sumandea MP, Allen EJ et al (2007) Augmented protein kinase C-induced myofilament protein phosphorylation contributes to myofilament dysfunction in experimental congestive heart failure. Circ Res 101:195–204

    CAS  PubMed  Google Scholar 

  95. Shimoni Y, Liu X-F (2003) Role of PKC in autocrine regulation of rat ventricular K+ currents by angiotensin and endothelin. Am J Physiol Heart Circ Physiol 284:H1168–H1181

    CAS  PubMed  Google Scholar 

  96. Rupp H, Elimban V, Dhalla NS (1989) Diabetes-like action of intermittent fasting on sarcoplasmic reticulum Ca2+ pump ATPase and myosin isoenzymes can be prevented by sucrose. Biochem Biophys Res Commun 164:319–325

    CAS  PubMed  Google Scholar 

  97. Dillmann WH (1982) Influence of thyroid hormone administration on myosin ATPase activity and myosin isoenzyme distribution in the heart of diabetic rats. Metabolism 31:199–204

    CAS  PubMed  Google Scholar 

  98. Afzal N, Pierce GN, Elimban V et al (1989) Influence of verapamil on some subcellular defects in diabetic cardiomyopathy. Am J Physiol 256:E453–E458

    CAS  PubMed  Google Scholar 

  99. Dillmann WH (1980) Diabetes mellitus induces changes in cardiac myosin of the rat. Diabetes 29:579–582

    CAS  PubMed  Google Scholar 

  100. Yu JZ, Rodrigues B, McNeill JH (1997) Intracellular calcium levels are unchanged in the diabetic heart. Cardiovasc Res 34:91–98

    CAS  PubMed  Google Scholar 

  101. Pierce GN, Russell JC (1997) Regulation of intracellular Ca2+ in the heart during diabetes. Cardiovasc Res 34:41–47

    CAS  PubMed  Google Scholar 

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Acknowledgments

 This work was supported by the St. Boniface Hospital Research Foundation, and A.F.P. Pinto was supported by the National Council for Scientific and Technological Development (CNPq), Brazil.

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Authors and Affiliations

  1. Institute of Cardiovascular Sciences and Department of Physiology, University of Manitoba, St. Boniface Hospital Research, Winnipeg, MB, R2H 2A6, Canada

    Vijayan Elimban, Adriana Frota P. Pinto & Naranjan S. Dhalla

  2. Institute of Cardiovascular Sciences, St. Boniface Hospital Research, 351 Tache Avenue, Winnipeg, MB, R2H 2A6, Canada

    Vijayan Elimban

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  1. Vijayan Elimban
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  2. Adriana Frota P. Pinto
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Correspondence to Vijayan Elimban .

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  1. Department of Biophysics, University of Ankara, Ankara, Ankara, Turkey

    Belma Turan

  2. St. Boniface Hosp. Research, Univ. of Ma Institute of Cardiovascular Sciences, Winnipeg, Manitoba, Canada

    Naranjan S. Dhalla

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Elimban, V., Pinto, A.F.P., Dhalla, N.S. (2014). Calcium-Handling Proteins in Diabetic Cardiomyopathy. In: Turan, B., Dhalla, N. (eds) Diabetic Cardiomyopathy. Advances in Biochemistry in Health and Disease, vol 9. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-9317-4_17

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