Dyssynchronous (non-uniform) Ca2+ release in myocytes from streptozotocin-induced diabetic rats

Journal of Molecular and Cellular Cardiology

Volumn 42, Issue 1, 2007, Pages 234-246

  Shao, Chun Hong ^a   Rozanski, George J ^a   Patel, Kaushik P ^a   Bidasee, Keshore R ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Ca2+ sparks; Ca2+ transients; Diabetes; Dysregulation; Rat; Ryanodine receptors

Indexed keywords

CAFFEINE; CALCIUM ION; RYANODINE RECEPTOR; RYANODINE RECEPTOR 2; STREPTOZOCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CALCIUM TRANSPORT; CELL ACTIVITY; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; FUNCTIONAL PROTEOMICS; HEART ARRHYTHMIA; HEART DEATH; HEART MUSCLE CELL; INSULIN DEPENDENT DIABETES MELLITUS; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; SARCOPLASMIC RETICULUM; STREPTOZOCIN DIABETES;

ANIMALS; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; DIABETES MELLITUS, EXPERIMENTAL; MALE; MICROSCOPY, CONFOCAL; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; TACROLIMUS BINDING PROTEIN 1A; VENTRICULAR FUNCTION, LEFT;

EID: 33845657896     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2006.08.018     Document Type: Article

References (82)

1. Soltesz G. Diabetes in the young: a paediatric and epidemiological perspective. Diabetologia 46 4 (2003) 447-454
2. Couper J.J. Environmental triggers of type 1 diabetes. J. Paediatr. Child Health 37 3 (2003) 218-220
3. Akerblom H.K., Vaarala O., Hyoty H., Ilonen J., and Knip M. Environmental factors in the etiology of type 1 diabetes. Am. J. Med. Genet. 115 1 (2002) 18-29
4. Fein F.S., Kornstein L.B., Strobeck J.E., Capasso J.M., and Sonnenblick E.H. Altered myocardial mechanics in diabetic rats. Circ. Res. 47 (1980) 922-933
5. Fang Z.Y., Prins J.B., and Marwick T.H. Diabetic cardiomyopathy: evidence, mechanisms, and therapeutic implications. Endocr. Rev. 25 4 (2004) 543-567
6. Bell D.S. Diabetic cardiomyopathy. A unique entity or a complication of coronary artery disease?. Diabetes Care 18 (1995) 708-714
7. Dhalla N.S., Lui X., Panagia V., and Takeda N. Subcellular remodeling and heart dysfunction in chronic diabetes. J. Cardiovasc. Res. 40 (1998) 239-247
8. 2+ handling in ventricular myocytes isolated from diabetic rats. Am. J. Physiol. 270 5 Pt 2 (1996) H1529-H1537
9. Belke D.D., and Dillmann W.H. Altered cardiac calcium handling in diabetes. Curr. Hypertens. Rep. 6 6 (2004) 424-429
10. 2+ signaling contributes to cardiomyopathy in Type 1 diabetic rats. A. J. Physiol.: Heart Circ. Physiol. 283 (2003) H1408-H1498
11. Bers D.M. Cardiac excitation-contraction coupling. Nature 415 (2002) 198-205
12. Scoote M., and Williams A.J. The cardiac ryanodine receptor (calcium release channel): emerging role in heart failure and arrhythmia pathogenesis. Cardiovasc. Res. 56 3 (2002) 359-372
13. Eisner D.A., Choi H.S., Diaz M.E., O'Neill S.C., and Trafford A.W. Integrative analysis of calcium cycling in cardiac muscle. Circ. Res. 87 12 (2000) 1087-1094
14. Bidasee K.R., Dinçer U.D., and BeschJr H.R. Ryanodine receptor dysfunction in streptozotocin-induced diabetic rat hearts. Mol. Pharmacol. 60 (2001) 1356-1364
15. 2+ homeostasis in rat heart. Diabetes 54 11 (2005) 3082-3088
16. Bidasee K.R., Nallani K., Besch Jr. H.R., and Dincer U.D. Streptozotocin-induced diabetes increases disulfide bond formation on cardiac ryanodine receptor (RyR2). J. Pharmacol. Exp. Ther. 5 3 (2003) 989-998
17. Bidasee K.R., Nallani K., Yu Y., Cocklin R.R., Zhang Y., Wang M., et al. Chronic diabetes increases advanced-glycation end products on cardiac ryanodine receptors (RyR2). Diabetes 52 7 (2003) 1825-1836
18. Bidasee K.R., Nallani K., Henry B., Dincer U.D., and Besch Jr. H.R. Chronic diabetes alters function and expression of ryanodine receptor calcium-release channels in rat heart. Mol. Cell. Biochem. 249 1-2 (2003) 113-123
19. Bidasee K.R., Xu L., Meissner G., and Besch Jr. H.R. Diketo pyridyl ryanodine has three concentrations-dependent effects on the cardiac calcium-release channel/ryanodine receptor. J. Biol. Chem. 278 16 (2003) 14237-14248
20. Du G.G., Guo X., Khanna V.K., and MacLennan D.H. Ryanodine sensitizes the cardiac Ca(2+) release channel (ryanodine receptor isoform 2) to Ca(2+) activation and dissociates as the channel is closed by Ca(2+) depletion. Proc. Natl. Acad. Sci. U. S. A. 98 24 (2001) 13625-13630
21. Coronado R., Morrissette J., Sukhareva M., and Vaughan D.M. Structure and function of ryanodine receptors. Am. J. Physiol. 266 6 Pt 1 (1994) C1485-C1504
22. 2+ release channels and their regulation by endogenous effectors. Annu. Rev. Physiol. 56 (1994) 485-508
23. Li S., Li X., and Rozanski G.J. Regulation of glutathione in cardiac myocytes. J. Mol. Cell. Cardiol. 35 9 (2003) 1145-1152
24. 2+ waves in saponin-permeabilized rat ventricular myocytes. J. Physiol. 521 Pt 3 (1999) 575-585
25. Rozanski G.J., and Witt R.C. Acidosis masks beta-adrenergic control of cardiac L-type calcium current. J. Mol. Cell. Cardiol. 27 9 (1995) 1781-1788
26. Rozanski G.J., Xu Z., Whitney R.T., Murakami H., and Zucker I.H. Electrophysiology of rabbit ventricular myocytes following sustained rapid ventricular pacing. J. Mol. Cell. Cardiol. 29 2 (1997) 721-732
27. 2+-ATPase. Diabetes 2 (2004) 463-473
28. Casis O., Gallego M., Iriarte M., and Sanchez-Chapula J.A. Effects of diabetic cardiomyopathy on regional electrophysiologic characteristics of rat ventricle. Diabetologia 43 1 (2000) 101-199
29. Howarth F.C., Jacobson M., Shafiullah M., and Adeghate E. Long-term effects of streptozotocin-induced diabetes on the electrocardiogram, physical activity and body temperature in rats. Exp. Physiol. 90 6 (2005) 827-835
30. Ren J., and Davidoff A.J. Diabetes rapidly induces contractile dysfunctions in isolated ventricular myocytes. Am. J. Physiol. 272 1 Pt 2 (1997) H148-H158
31. Ren J., and Bode A.M. Altered cardiac excitation-contraction coupling in ventricular myocytes from spontaneously diabetic BB rats. Am. J. Physiol.: Heart Circ. Physiol. 279 1 (2000) H238-H244
32. Litwin S.E., Zhang D., and Bridge J.H. Dyssynchronous Ca(2+) sparks in myocytes from infarcted hearts. Circ. Res. 87 11 (2000) 1040-1047
33. Nordin C., Gilat E., and Aronson R.S. Delayed afterdepolarizations and triggered activity in ventricular muscle from rats with streptozotocin-induced diabetes. Circ. Res. 57 1 (1985) 28-34
34. Jourdon P., and Feuvray D. Calcium and potassium currents in ventricular myocytes isolated from diabetic rats. J. Physiol. 470 (1993) 411-429
35. i waves in cardiac myocytes. Am. J. Physiol. 270 1 Pt 1 (1996) C59-C148
36. Bidasee K.R., Xu L., Meissner G., and Besch Jr. H.R. Diketo pyridyl ryanodine has three concentrations-dependent effects on the cardiac calcium-release channel/ryanodine receptor. J. Biol. Chem. 278 16 (2003) 14237-14248
37. Wehrens X.H., Lehnart S.E., Reiken S.R., Deng S.X., Vest J.A., Cervantes D., et al. Protection from cardiac arrhythmia through ryanodine receptor-stabilizing protein calstabin2. Science 304 5668 (2004) 292-296
38. Reiken S., Gaburjakova M., Gaburjakova J., He Kl K.L., Prieto A., Becker E., et al. Beta-adrenergic receptor blockers restore cardiac calcium release channel (ryanodine receptor) structure and function in heart failure. Circulation 104 23 (2001) 2843-2848
39. Carter S., Colyer J., and Sitsapesan R. Maximum phosphorylation of the cardiac ryanodine receptor at serine-2809 by protein kinase a produces unique modifications to channel gating and conductance not observed at lower levels of phosphorylation. Circ. Res. 98 12 (2006) 1506-1513
40. 2+]i transient decrease in cardiomyopathy of db/db type 2 diabetic mice. Diabetes 55 3 (2006) 608-615
41. Belke D.D., Swanson E.A., and Dillmann W.H. Decreased sarcoplasmic reticulum activity and contractility in diabetic db/db mouse heart. Diabetes 53 12 (2004) 3201-3208
42. Dincer U.D., Araiza A., Knudson J.D., Shao C.H., Bidasee K.R., and Tune J.D. Dysfunction of cardiac ryanodine receptors in the metabolic syndrome. J. Mol. Cell. Cardiol. 41 1 (2006) 108-114
43. Touyz R.M., and Schiffrin E.L. Reactive oxygen species in vascular biology: implications in hypertension. Histochem. Cell Biol. 122 4 (2004) 339-352
44. Kalapos M.P. Methylglyoxal in living organisms: chemistry, biochemistry, toxicology and biological implications. Toxicol. Lett. 110 3 (1999) 145-175
45. Niwa T. 3-Deoxyglucosone: metabolism, analysis, biological activity, and clinical implication. J. Chromatogr., B, Biomed. Sci. Appl. 731 1 (1999) 23-36
46. Ulrich P. Cerami A: protein glycation, diabetes, and aging. Recent Prog. Horm. Res. 56 (2001) 1-21
47. Poole L.B., Karplus P.A., and Claiborne A. Protein sulfenic acids in redox signaling. Annu. Rev. Pharmacol. Toxicol. 44 (2004) 325-347
48. Adachi T., Weisbrod R.M., Pimentel D.R., Ying J., Sharov V.S., Schoneich C., et al. S-Glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide. Nat. Med. 10 11 (2004) 1200-1207
49. Uchida K. Role of reactive aldehyde in cardiovascular diseases. Free Radical Biol. Med. 28 12 (2000) 1685-1696
50. Thorpe S.R., and Baynes J.W. Maillard reaction products in tissue proteins: new products and new perspectives. Amino Acids 3-4 (2003) 275-281
51. Baynes J.W. Chemical modification of proteins by lipids in diabetes. Clin. Chem. Lab. Med. 41 9 (2003) 1159-1165
52. Stitt A.W., Frizzell N., and Thorpe S.R. Advanced glycation and advanced lipoxidation: possible role in initiation and progression of diabetic retinopathy. Curr. Pharm. Des. 10 27 (2004) 3349-3360
53. Aliciguzel Y., Ozen I., Aslan M., and Karayalcin U. Activities of xanthine oxidoreductase and antioxidant enzymes in different tissues of diabetic rats. J. Lab. Clin. Med. 142 3 (2003) 172-177
54. Adeghate E. Molecular and cellular basis of the aetiology and management of diabetic cardiomyopathy: a short review. Mol. Cell. Biochem. 261 1-2 (2003) 187-191
55. Taniyama Y., and Griendling K.K. Reactive oxygen species in the vasculature: molecular and cellular mechanisms. Hypertension 42 6 (2003) 1075-1081
56. Desco M.C., Asensi M., Marquez R., Martinez-Valls J., Vento M., Pallardo F.V., et al. Xanthine oxidase is involved in free radical production in type 1 diabetes: protection by allopurinol. Diabetes 51 4 (2002) 1118-1124
57. Bukan N., Sancak B., Bilgihan A., Kosova F., Bugdayci G., and Altan N. The effects of the sulfonylurea glyburide on glutathione peroxidase, superoxide dismutase and catalase activities in the heart tissue of streptozotocin-induced diabetic rat. Methods Find Exp. Clin. Pharmacol. 26 7 (2004) 519-522
58. Yildirim O., and Buyukbingol Z. Effect of cobalt on the oxidative status in heart and aorta of streptozotocin-induced diabetic rats. Cell Biochem. Funct. 21 1 (2003) 27-33
59. 2+-ATPase activity in heart and liver of streptozotocin-diabetic rats: comparison with vitamin E. Biochim. Biophys. Acta 1588 1 (2002) 71-78
60. Aksoy N., Vural H., Sabuncu T., and Aksoy S. Effects of melatonin on oxidative-antioxidative status of tissues in streptozotocin-induced diabetic rats. Cell Biochem. Funct. 21 2 (2003) 121-125
61. Fiordaliso F., Bianchi R., Staszewsky L., Cuccovillo I., Doni M., Laragione T., et al. Antioxidant treatment attenuates hyperglycemia-induced cardiomyocyte death in rats. J. Mol. Cell. Cardiol. 37 5 (2004) 959-968
62. Xu L., Eu J.P., Meissner G., and Stamler J.S. Activation of the cardiac calcium release channel (ryanodine receptor) by poly-S-nitrosylation. Science 279 5348 (1998) 234-237
63. Terentyev D., Viatchenko-Karpinski S., Gyorke I., Terentyeva R., and Gyorke S. Protein phosphatases decrease sarcoplasmic reticulum calcium content by stimulating calcium release in cardiac myocytes. J. Physiol. 552 Pt 1 (2003) 109-118
64. 2+-release channel (ryanodine receptor) does not dissociate 12.6-kDa FK506-binding protein (FKBP12.6). Circ. Res. 94 4 (2004) 487-495
65. Xiao B., Jiang M.T., Zhao M., Yang D., Sutherland C., Lai F.A., et al. Characterization of a novel PKA phosphorylation site, serine-2030, reveals no PKA hyperphosphorylation of the cardiac ryanodine receptor in canine heart failure. Circ. Res. 96 8 (2005) 847-855
66. Nordquist J.E., Gokturk C., and Oreland L. Semicarbazide-sensitive amine oxidase (SSAO) gene expression in alloxan-induced diabetes in mice. Mol. Med. 8 12 (2002) 824-829
67. Garpenstrand H., Ekblom J., Backlund L.B., Oreland L., and Rosenqvist U. Elevated plasma semicarbazide-sensitive amine oxidase (SSAO) activity in Type 2 diabetes mellitus complicated by retinopathy. Diabet. Med. 16 6 (1999) 514-521
68. Boomsma F., Bhaggoe U.M., van der Houwen A.M., and van den Meiracker A.H. Plasma semicarbazide-sensitive amine oxidase in human (patho)physiology. Biochim. Biophys. Acta 1647 1-2 (2003) 48-54
69. Bers D.M. Macromolecular complexes regulating cardiac ryanodine receptor function. J. Mol. Cell. Cardiol. 37 2 (2004) 417-429
70. Rastogi S., Sentex E., Elimban V., and Dhalla N.S. Netticadan T elevated levels of protein phosphatase 1 and phosphatase 2A may contribute to cardiac dysfunction in diabetes. Biochim. Biophys. Acta 1638 3 (2003) 273-277
71. Suarez J., Belke D.D., Gloss B., Dieterle T., McDonough P.M., Kim Y.K., et al. In vivo adenoviral transfer of sorcin reverses cardiac contractile abnormalities of diabetic cardiomyopathy. Am. J. Physiol.: Heart Circ. Physiol. 286 1 (2004) H68-H75
72. Tomaselli G.F., and Zipes D.P. What causes sudden death in heart failure?. Circ. Res. 95 8 (2004) 754-763
73. 2+ release (SOICR). Proc. Natl. Acad. Sci. U. S. A. 101 35 (2004) 13062-13067
74. Tattersall R.B., and Gill G.V. Unexplained death of type-1 diabetic patients. Diabet. Med. 8 (1991) 49-58
75. Thordarsson H., and Sovik O. Dead in bed syndrome in young diabetic patients in Norway. Diabet. Med. 12 (1995) 782-787
76. Heller S.R. Abnormalities of the electrocardiogram during hypoglycaemia: the cause of the dead in bed syndrome?. Int. J. Clin. Pract., Suppl. 120 (2002) 27-32
77. 2+ overload. J. Physiol. 527 Pt 1 (2000) 85-94
78. 2+ exchanger activity in the diabetic heart. Cardiovasc. Res. 34 1 (1997) 129-136
79. 2+ exchange. Can. J. Physiol. Pharmacol. 78 1 (2000) 12-19
80. + ATPase activities and gene expression in alloxan-induced diabetes in rats. Mol. Cell. Biochem. 188 1-2 (1998) 91-101
81. Franzini-Armstrong C., Protasi F., and Tijskens P. The assembly of calcium release units in cardiac muscle. Ann. N. Y. Acad. Sci. 1047 (2005) 76-85
82. Marx S.O., Reiken S., Hisamatsu Y., Jayaraman T., Burkhoff D., Rosemblit N., et al. PKA phosphorylation dissociates FKBP12.6 from the calcium release channel (ryanodine receptor): defective regulation in failing hearts. Cell 101 4 (2000) 365-376