Zinc-induced cardiomyocyte relaxation in a rat model of hyperglycemia is independent of myosin isoform

Cardiovascular Diabetology

Volumn 11, Issue , 2012, Pages

  Yi, Ting ^a   Cheema, Yaser ^b   Tremble, Sarah M ^b   Bell, Stephen P ^b   Chen, Zengyi ^b   Subramanian, Meenakumari ^a   LeWinter, Martin M ^a,b   VanBuren, Peter ^a,b   Palmer, Bradley M ^a  

^a UNIVERSITY OF VERMONT   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

Cardiac; Iron; PTU; Streptozotocin; Sulfur; Type 1 diabetes

Indexed keywords

ADVANCED GLYCATION END PRODUCT; CALCIUM; CALCIUM CHANNEL L TYPE; INSULIN; LYSINE; N ACETYLGLUCOSAMINE; RYANODINE RECEPTOR; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; ZINC;

ACETYLATION; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSAY; CALCIUM METABOLISM; CALCIUM TRANSPORT; CELL FUNCTION; CONTROLLED STUDY; CYTOSOL; HEART MUSCLE CELL; HEART MUSCLE RELAXATION; HEART PACING; HYPERGLYCEMIA; MYOFILAMENT; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; RAT; SARCOMERE;

ANIMALS; BLOOD GLUCOSE; CALCIUM; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIASTOLE; GENE EXPRESSION REGULATION; HYPOTHYROIDISM; INSULIN-SECRETING CELLS; MALE; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; MYOSIN HEAVY CHAINS; NECROSIS; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, WISTAR; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOMERES; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SODIUM-CALCIUM EXCHANGER; TIME FACTORS; VENTRICULAR MYOSINS; ZINC;

EID: 84868240185     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/1475-2840-11-135     Document Type: Article

References (55)

1. Regan TJ, Lyons MM, Ahmed SS, Levinson GE, Oldewurtel HA, Ahmad MR, Haider B. Evidence for cardiomyopathy in familial diabetes mellitus. J Clin Invest 1977, 60(4):884-899. 372437, 893679.
2. Diamant M, Lamb HJ, Groeneveld Y, Endert EL, Smit JW, Bax JJ, Romijn JA, de Roos A, Radder JK. Diastolic dysfunction is associated with altered myocardial metabolism in asymptomatic normotensive patients with well-controlled type 2 diabetes mellitus. J Am Coll Cardiol 2003, 42(2):328-335. 10.1016/S0735-1097(03)00625-9, 12875772.
3. Scognamiglio R, Avogaro A, Negut C, Piccolotto R, Vigili De Kreutzenberg S, Tiengo A. Early myocardial dysfunction in the diabetic heart: current research and clinical applications. Am J Cardiol 2004, 93(8A):17A-20A.
4. Fang ZY, Prins JB, Marwick TH. Diabetic cardiomyopathy: evidence, mechanisms, and therapeutic implications. Endocr Rev 2004, 25(4):543-567. 10.1210/er.2003-0012, 15294881.
5. Davidoff AJ, Pinault FM, Rodgers RL. Ventricular relaxation of diabetic spontaneously hypertensive rat. Hypertension 1990, 15(6 Pt 1):643-651.
6. Boudina S, Abel ED. Diabetic cardiomyopathy revisited. Circulation 2007, 115(25):3213-3223. 10.1161/CIRCULATIONAHA.106.679597, 17592090.
7. Bugger H, Abel ED. Mitochondria in the diabetic heart. Cardiovascular research 2010, 88(2):229-240. 10.1093/cvr/cvq239, 2952534, 20639213.
8. Fein FS, Kornstein LB, Strobeck JE, Capasso JM, Sonnenblick EH. Altered myocardial mechanics in diabetic rats. Circ Res 1980, 47(6):922-933. 10.1161/01.RES.47.6.922, 7438339.
9. Zola BE, Miller B, Stiles GL, Rao PS, Sonnenblick EH, Fein FS. Heart rate control in diabetic rabbits: blunted response to isoproterenol. Am J Physiol 1988, 255(5 Pt 1):E636-641.
10. Lacombe VA, Viatchenko-Karpinski S, Terentyev D, Sridhar A, Emani S, Bonagura JD, Feldman DS, Gyorke S, Carnes CA. Mechanisms of impaired calcium handling underlying subclinical diastolic dysfunction in diabetes. Am J Physiol Regul Integr Comp Physiol 2007, 293(5):R1787-1797. 10.1152/ajpregu.00059.2007, 2413069, 17761517.
11. Zhang L, Cannell MB, Phillips AR, Cooper GJ, Ward ML. Altered calcium homeostasis does not explain the contractile deficit of diabetic cardiomyopathy. Diabetes 2008, 57(8):2158-2166. 10.2337/db08-0140, 2494698, 18492789.
12. Suarez J, Scott B, Dillmann WH. Conditional increase in SERCA2a protein is able to reverse contractile dysfunction and abnormal calcium flux in established diabetic cardiomyopathy. Am J Physiol Regul Integr Comp Physiol 2008, 295(5):R1439-1445. 10.1152/ajpregu.00736.2007, 2584853, 18799637.
13. Shao CH, Rozanski GJ, Patel KP, Bidasee KR. Dyssynchronous (non-uniform) Ca2+ release in myocytes from streptozotocin-induced diabetic rats. Journal of molecular and cellular cardiology 2007, 42(1):234-246. 10.1016/j.yjmcc.2006.08.018, 17027851.
14. Tian C, Shao CH, Moore CJ, Kutty S, Walseth T, DeSouza C, Bidasee KR. Gain of function of cardiac ryanodine receptor in a rat model of type 1 diabetes. Cardiovascular research 2011, 91(2):300-309. 10.1093/cvr/cvr076, 3125072, 21421556.
15. Yaras N, Ugur M, Ozdemir S, Gurdal H, Purali N, Lacampagne A, Vassort G, Turan B. Effects of diabetes on ryanodine receptor Ca release channel (RyR2) and Ca2+ homeostasis in rat heart. Diabetes 2005, 54(11):3082-3088. 10.2337/diabetes.54.11.3082, 16249429.
16. Shen X, Zheng S, Thongboonkerd V, Xu M, Pierce WM, Klein JB, Epstein PN. Cardiac mitochondrial damage and biogenesis in a chronic model of type 1 diabetes. Am J Physiol Endocrinol Metab 2004, 287(5):E896-905. 10.1152/ajpendo.00047.2004, 15280150.
17. Wang J, Song Y, Elsherif L, Song Z, Zhou G, Prabhu SD, Saari JT, Cai L. Cardiac metallothionein induction plays the major role in the prevention of diabetic cardiomyopathy by zinc supplementation. Circulation 2006, 113(4):544-554. 10.1161/CIRCULATIONAHA.105.537894, 16432057.
18. Liang Q, Carlson EC, Donthi RV, Kralik PM, Shen X, Epstein PN. Overexpression of metallothionein reduces diabetic cardiomyopathy. Diabetes 2002, 51(1):174-181.
19. Song Y, Wang J, Li Y, Du Y, Arteel GE, Saari JT, Kang YJ, Cai L. Cardiac metallothionein synthesis in streptozotocin-induced diabetic mice, and its protection against diabetes-induced cardiac injury. Am J Pathol 2005, 167(1):17-26. 10.1016/S0002-9440(10)62949-5, 1603431, 15972948.
20. Wold LE, Ceylan-Isik AF, Fang CX, Yang X, Li SY, Sreejayan N, Privratsky JR, Ren J. 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 radical biology & medicine 2006, 40(8):1419-1429. 10.1016/j.freeradbiomed.2005.12.009, 23238816.
21. Powell SR, Aiuto L, Hall D, Tortolani AJ. Zinc supplementation enhances the effectiveness of St. Thomas' Hospital No. 2 cardioplegic solution in an in vitro model of hypothermic cardiac arrest. J Thorac Cardiovasc Surg 1995, 110(6):1642-1648. 10.1016/S0022-5223(95)70025-0, 8523874.
22. Powell SR, Nelson RL, Finnerty J, Alexander D, Pottanat G, Kooker K, Schiff RJ, Moyse J, Teichberg S, Tortolani AJ. Zinc-bis-histidinate preserves cardiac function in a porcine model of cardioplegic arrest. Ann Thorac Surg 1997, 64(1):73-80. 10.1016/S0003-4975(97)00300-7, 9236338.
23. Atar D, Backx PH, Appel MM, Gao WD, Marban E. Excitation-transcription coupling mediated by zinc influx through voltage-dependent calcium channels. J Biol Chem 1995, 270(6):2473-2477. 10.1074/jbc.270.6.2473, 7852308.
24. Turan B. Zinc-induced changes in ionic currents of cardiomyocytes. Biol Trace Elem Res 2003, 94(1):49-60. 10.1385/BTER:94:1:49, 12907827.
25. Tuncay E, Bilginoglu A, Sozmen NN, Zeydanli EN, Ugur M, Vassort G, Turan B. Intracellular free zinc during cardiac excitation-contraction cycle: calcium and redox dependencies. Cardiovascular research 2010, 89(3):634-642.
26. Davidoff AJ, Rodgers RL. Insulin, thyroid hormone, and heart function of diabetic spontaneously hypertensive rat. Hypertension 1990, 15(6 Pt 1):633-642.
27. Dillmann WH. Diabetes mellitus induces changes in cardiac myosin of the rat. Diabetes 1980, 29(7):579-582.
28. Joseph T, Coirault C, Dubourg O, Lecarpentier Y. Changes in crossbridge mechanical properties in diabetic rat cardiomyopathy. Basic Res Cardiol 2005, 100(3):231-239. 10.1007/s00395-005-0512-5, 15645163.
29. Rundell VL, Manaves V, Martin AF, de Tombe PP. Impact of beta-myosin heavy chain isoform expression on cross-bridge cycling kinetics. Am J Physiol Heart Circ Physiol 2005, 288(2):H896-903.
30. Fitzsimons DP, Patel JR, Moss RL. Role of myosin heavy chain composition in kinetics of force development and relaxation in rat myocardium. J Physiol 1998, 513(Pt 1):171-183. 2231272, 9782168.
31. Herron TJ, Korte FS, McDonald KS. Loaded shortening and power output in cardiac myocytes are dependent on myosin heavy chain isoform expression. Am J Physiol Heart Circ Physiol 2001, 281(3):H1217-1222.
32. Korte FS, Herron TJ, Rovetto MJ, McDonald KS. Power output is linearly related to MyHC content in rat skinned myocytes and isolated working hearts. Am J Physiol Heart Circ Physiol 2005, 289(2):H801-812. 10.1152/ajpheart.01227.2004, 15792987.
33. Godt RE, Lindley BD. Influence of temperature upon contractile activation and isometric force production in mechanically skinned muscle fibers of the frog. J Gen Physiol 1982, 80(2):279-297. 10.1085/jgp.80.2.279, 2228673, 6981684.
34. Palmer BM, Fishbaugher DE, Schmitt JP, Wang Y, Alpert NR, Seidman CE, Seidman JG, VanBuren P, Maughan DW. Differential cross-bridge kinetics of FHC myosin mutations R403Q and R453C in heterozygous mouse myocardium. Am J Physiol Heart Circ Physiol 2004, 287(1):H91-99. 10.1152/ajpheart.01015.2003, 15001446.
35. Noguchi T, Hunlich M, Camp PC, Begin KJ, El-Zaru M, Patten R, Leavitt BJ, Ittleman FP, Alpert NR, LeWinter MM, et al. Thin-filament-based modulation of contractile performance in human heart failure. Circulation 2004, 110(8):982-987. 10.1161/01.CIR.0000139334.43109.F9, 15302786.
36. VanBuren P, Alix SL, Gorga JA, Begin KJ, LeWinter MM, Alpert NR. Cardiac troponin T isoforms demonstrate similar effects on mechanical performance in a regulated contractile system. Am J Physiol Heart Circ Physiol 2002, 282(5):H1665-1671.
37. Palmer BM, Chen Z, Lachapelle RR, Hendley ED, LeWinter MM. Cardiomyocyte function associated with hyperactivity and/or hypertension in genetic models of LV hypertrophy. Am J Physiol Heart Circ Physiol 2006, 290(1):H463-473.
38. Palmer BM, Moore RL. Excitation wavelengths for fura 2 provide a linear relationship between [Ca(2+)] and fluorescence ratio. Am J Physiol Cell Physiol 2000, 279(4):C1278-1284.
39. Reiser PJ, Kline WO. Electrophoretic separation and quantitation of cardiac myosin heavy chain isoforms in eight mammalian species. Am J Physiol 1998, 274(3 Pt 2):H1048-1053.
40. Kay AR. Detecting and minimizing zinc contamination in physiological solutions. BMC Physiol 2004, 4:4. 10.1186/1472-6793-4-4, 395835, 15113426.
41. Fredersdorf S, Thumann C, Zimmermann WH, Vetter R, Graf T, Luchner A, Riegger GA, Schunkert H, Eschenhagen T, Weil J. Increased myocardial SERCA expression in early type 2 diabetes mellitus is insulin dependent: In vivo and in vitro data. Cardiovascular diabetology 2012, 11:57. 10.1186/1475-2840-11-57, 3447673, 22621761.
42. Thackeray JT, Radziuk J, Harper ME, Suuronen EJ, Ascah KJ, Beanlands RS, Dasilva JN. Sympathetic nervous dysregulation in the absence of systolic left ventricular dysfunction in a rat model of insulin resistance with hyperglycemia. Cardiovascular diabetology 2011, 10:75. 10.1186/1475-2840-10-75, 3170183, 21831292.
43. Fulop N, Marchase RB, Chatham JC. Role of protein O-linked N-acetyl-glucosamine in mediating cell function and survival in the cardiovascular system. Cardiovascular research 2007, 73(2):288-297. 10.1016/j.cardiores.2006.07.018, 2848961, 16970929.
44. Nass N, Bartling B, Navarrete Santos A, Scheubel RJ, Borgermann J, Silber RE, Simm A. Advanced glycation end products, diabetes and ageing. Zeitschrift fur Gerontologie und Geriatrie 2007, 40(5):349-356. 10.1007/s00391-007-0484-9, 17943238.
45. Samant SA, Courson DS, Sundaresan NR, Pillai VB, Tan M, Zhao Y, Shroff SG, Rock RS, Gupta MP. HDAC3-dependent reversible lysine acetylation of cardiac myosin heavy chain isoforms modulates their enzymatic and motor activity. J Biol Chem 2011, 286(7):5567-5577. 10.1074/jbc.M110.163865, 3037670, 21177250.
46. Andrews GK. Cellular zinc sensors: MTF-1 regulation of gene expression. Biometals 2001, 14(3-4):223-237.
47. Gunther V, Lindert U, Schaffner W. The taste of heavy metals: gene regulation by MTF-1. Biochimica et biophysica acta 2012, 1823(9):1416-1425. 10.1016/j.bbamcr.2012.01.005, 22289350.
48. Guo L, Lichten LA, Ryu MS, Liuzzi JP, Wang F, Cousins RJ. STAT5-glucocorticoid receptor interaction and MTF-1 regulate the expression of ZnT2 (Slc30a2) in pancreatic acinar cells. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(7):2818-2823. 10.1073/pnas.0914941107, 2840329, 20133611.
49. Kumar SD, Vijaya M, Samy RP, Dheen ST, Ren M, Watt F, Kang YJ. Bay BH. Tay SS: Zinc supplementation prevents cardiomyocyte apoptosis and congenital heart defects in embryos of diabetic mice. Free radical biology & medicine;. 2012, 53(8):1595-1606.
50. Lichtlen P, Wang Y, Belser T, Georgiev O, Certa U, Sack R, Schaffner W. Target gene search for the metal-responsive transcription factor MTF-1. Nucleic acids research 2001, 29(7):1514-1523. 10.1093/nar/29.7.1514, 31279, 11266553.
51. Foster M, Samman S. Zinc and redox signaling: perturbations associated with cardiovascular disease and diabetes mellitus. Antioxidants & redox signaling 2010, 13(10):1549-1573. 10.1089/ars.2010.3111, 23257932.
52. Singh J, Chonkar A, Bracken N, Adeghate E, Latt Z, Hussain M. Effect of streptozotocin-induced type 1 diabetes mellitus on contraction, calcium transient, and cation contents in the isolated rat heart. Ann N Y Acad Sci 2006, 1084:178-190. 10.1196/annals.1372.028, 17151301.
53. Nakagawa M, Kobayashi S, Kimura I, Kimura M. Diabetic state-induced modification of Ca, Mg, Fe and Zn content of skeletal, cardiac and smooth muscles. Endocrinol Jpn 1989, 36(6):795-807. 10.1507/endocrj1954.36.795, 2633909.
54. Maret W. Zinc and sulfur: a critical biological partnership. Biochemistry 2004, 43(12):3301-3309. 10.1021/bi036340p, 15035601.
55. Soinio M, Marniemi J, Laakso M, Pyorala K, Lehto S, Ronnemaa T. Serum zinc level and coronary heart disease events in patients with type 2 diabetes. Diabetes care 2007, 30(3):523-528. 10.2337/dc06-1682, 17327315.