Streptozotocin-induced diabetes prolongs twitch duration without affecting the energetics of isolated ventricular trabeculae

Cardiovascular Diabetology

Volumn 13, Issue 1, 2014, Pages

  Han, June Chiew ^a   Tran, Kenneth ^a   Nielsen, Poul M F ^a,b   Taberner, Andrew J ^a,b   Loiselle, Denis S ^a,b  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Cardiac efficiency; Cardiac heat production; Cardiac twitch duration; Cardiac work; STZ induced diabetes

Indexed keywords

STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE DURATION; ENERGY TRANSFER; ENTHALPY; HEART AFTERLOAD; HEART LEFT VENTRICLE; HEART WORK; HEAT; MALE; MUSCLE CONTRACTION; MUSCLE ISOMETRIC CONTRACTION; MUSCLE LENGTH; MUSCLE TWITCH; NONHUMAN; RAT; RIGIDITY; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; STRESS; THERMOGENESIS; TISSUE PREPARATION;

ANIMALS; CALORIMETRY; DIABETES MELLITUS, EXPERIMENTAL; ENERGY METABOLISM; HEART VENTRICLES; MALE; MYOCARDIAL CONTRACTION; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 84899957755     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/1475-2840-13-79     Document Type: Article

References (67)

1. Yuill KH, Tosh D, Hancox JC. Streptozotocin-induced diabetes modulates action potentials and ion channel currents from the rat atrioventricular node. Exp Physiol 2010, 95(4):508-517. 10.1113/expphysiol.2009.050286, 19946031.
2. Fein FS, Aronson RS, Nordin C, Miller-Green B, Sonnenblick EH. Altered myocardial response to ouabain in diabetic rats: mechanics and electrophysiology. J Mol Cell Cardiol 1983, 15(11):769-784. 10.1016/0022-2828(83)90336-X, 6361268.
3. Nobe S, Aomine M, Arita M, Ito S, Takaki R. Chronic diabetes mellitus prolongs action potential duration of rat ventricular muscles: circumstantial evidence for impaired Ca2+ channel. Cardiovasc Res 1990, 24(5):381-389. 10.1093/cvr/24.5.381, 2164883.
4. Jourdon P, Feuvray D. Calcium and potassium currents in ventricular myocytes isolated from diabetic rats. J Physiol 1993, 470(1):411-429. 1143925, 8308734.
5. Magyar J, Rusznák Z, Szentesi P, Szûcs G, Kovács L. Action potentials and potassium currents in rat ventricular muscle during experimental diabetes. J Mol Cell Cardiol 1992, 24(8):841-853. 10.1016/0022-2828(92)91098-P, 1433314.
6. Zhang L, Cannell MB, Phillips ARJ, Cooper GJS, Ward M-L. Altered calcium homeostasis does not explain the contractile deficit of diabetic cardiomyopathy. Diabetes 2008, 57(8):2158-2166. 10.2337/db08-0140, 2494698, 18492789.
7. Wang DW, Kiyosue T, Shigematsu S, Arita M. Abnormalities of K+ and Ca2+ currents in ventricular myocytes from rats with chronic diabetes. Am J Physiol Heart Circ Physiol 1995, 269(4):H1288-H1296.
8. Shimoni Y, Ewart HS, Severson D. Type I and II models of diabetes produce different modifications of K+ currents in rat heart: role of insulin. J Physiol 1998, 507(2):485-496. 10.1111/j.1469-7793.1998.485bt.x, 2230808, 9518707.
9. Xu Z, Patel KP, Rozanski GJ. Metabolic basis of decreased transient outward K+ current in ventricular myocytes from diabetic rats. Am J Physiol Heart Circ Physiol 1996, 271(5):H2190-H2196.
10. Qin D, Huang B, Deng L, El-Adawi H, Ganguly K, Sowers JR, El-Sherif N. Downregulation of K+ channel genes expression in type I diabetic cardiomyopathy. Biochem Biophys Res Commun 2001, 283(3):549-553. 10.1006/bbrc.2001.4825, 11341759.
11. 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.
12. Zhang L, Ward M-L, Phillips A, Zhang S, Kennedy J, Barry B, Cannell M, Cooper G. Protection of the heart by treatment with a divalent-copper-selective chelator reveals a novel mechanism underlying cardiomyopathy in diabetic rats. Cardiovasc Diabetol 2013, 12(1):123. 3848860, 23981320.
13. Kotsanas G, Delbridge LMD, Wendt IR. Stimulus interval-dependent differences in Ca2+ transients and contractile responses of diabetic rat cardiomyocytes. Cardiovasc Res 2000, 46(3):450-462. 10.1016/S0008-6363(00)00062-6, 10912456.
14. Golfman L, Dixon IMC, Takeda N, Lukas A, Dakshinamurti K, Dhalla NS. Cardiac sarcolemmal Na+-Ca2+ exchange and Na+-K+ ATPase activities and gene expression in alloxan-induced diabetes in rats. Mol Cell Biochem 1998, 188(1-2):91-101.
15. Kato K, Chapman DC, Rupp H, Lukas A, Dhalla NS. Alterations of heart function and Na+-K+-ATPase activity by etomoxir in diabetic rats. J Appl Physiol 1999, 86(3):812-818.
16. Pierce GN, Dhalla NS. Sarcolemmal Na+-K+-ATPase activity in diabetic rat heart. Am J Physiol Cell Physiol 1983, 245(14):C241-C247.
17. Penpargkul S, Fein F, Sonnenblick EH, Scheuer J. Depressed cardiac sarcoplasmic reticular function from diabetic rats. J Mol Cell Cardiol 1981, 13(3):303-309. 10.1016/0022-2828(81)90318-7, 6115064.
18. Ganguly PK, Pierce GN, Dhalla KS, Dhalla NS. Defective sarcoplasmic reticular calcium transport in diabetic cardiomyopathy. Am J Physiol Endocrinol Metab 1983, 244(6):E528-E535.
19. Lopaschuk GD, Katz S, McNeill JH. The effect of alloxan- and streptozotocin-induced diabetes on calcium transport in rat cardiac sarcoplasmic reticulum. The possible involvement of long chain acylcarnitines. Can J Physiol Pharmacol 1983, 61(5):439-448. 10.1139/y83-068, 6883199.
20. Rupp H, Elimban V, Dhalla NS. Modification of myosin isozymes and SR Ca2+-pump ATPase of the diabetic rat heart by lipid-lowering interventions. Mol Cell Biochem 1994, 132(1):69-80. 10.1007/BF00925676, 8078510.
21. Zarain-Herzberg A, Yano K, Elimban V, Dhalla NS. Cardiac sarcoplasmic reticulum Ca2+-ATPase expression in streptozotocin-induced diabetic rat heart. Biochem Biophys Res Commun 1994, 203(1):113-120. 10.1006/bbrc.1994.2156, 8074644.
22. Zhao X-Y, Hu S-J, Li J, Mou Y, Chen B-P, Xia Q. Decreased cardiac sarcoplasmic reticulum Ca2+-ATPase activity contributes to cardiac dysfunction in streptozotocin-induced diabetic rats. J Physiol Biochem 2006, 62(1):1-8. 10.1007/BF03165800, 16909926.
23. Pierce GN, Dhalla NS. Cardiac myofibrillar ATPase activity in diabetic rats. J Mol Cell Cardiol 1981, 13(12):1063-1069. 10.1016/0022-2828(81)90296-0, 6120242.
24. Malhotra A, Penpargkul S, Fein FS, Sonnenblick EH, Scheuer J. The effect of streptozotocin-induced diabetes in rats on cardiac contractile proteins. Circ Res 1981, 49(6):1243-1250. 10.1161/01.RES.49.6.1243, 6458419.
25. Malhotra A, Lopez MC, Nakouzi A. Troponin subunits contribute to altered myosin ATPase activity in diabetic cardiomyopathy. Mol Cell Biochem 1995, 151(2):165-172. 10.1007/BF01322339, 8569762.
26. Dillmann WH. Diabetes mellitus induces changes in cardiac myosin of the rat. Diabetes 1980, 29(7):579-582. 10.2337/diab.29.7.579, 6445843.
27. Garber DW, Neely JR. Decreased myocardial function and myosin ATPase in hearts from diabetic rats. Am J Physiol Heart Circ Physiol 1983, 244(4):H586-H591.
28. Fein FS, Strobeck JE, Malhotra A, Scheuer J, Sonnenblick EH. Reversibility of diabetic cardiomyopathy with insulin in rats. Circ Res 1981, 49(6):1251-1261. 10.1161/01.RES.49.6.1251, 7030513.
29. Aragno M, Mastrocola R, Ghe C, Arnoletti E, Bassino E, Alloatti G, Muccioli G. Obestatin induced recovery of myocardial dysfunction in type 1 diabetic rats: underlying mechanisms. Cardiovasc Diabetol 2012, 11(1):129. 3537569, 23066908.
30. Takeda N, Nakamura I, Hatanaka T, Ohkubo T, Nagano M. Myocardial mechanical and myosin isoenzyme alterations in streptozotocin-diabetic rats. Jpn Heart J 1988, 29(4):455-463. 10.1536/ihj.29.455, 2846906.
31. Choi KM, Zhong Y, Hoit BD, Grupp IL, Hahn H, Dilly KW, Guatimosim S, Lederer WJ, Matlib MA. Defective intracellular Ca2+ signaling contributes to cardiomyopathy in Type 1 diabetic rats. Am J Physiol Heart Circ Physiol 2002, 283(4):H1398-H1408.
32. MacDonald JR, Oellermann M, Rynbeck S, Chang G, Ruggiero K, Cooper GJS, Hickey AJR. Transmural differences in respiratory capacity across the rat left ventricle in health, aging, and streptozotocin-induced diabetes mellitus: evidence that mitochondrial dysfunction begins in the subepicardium. Am J Physiol Cell Physiol 2011, 300(2):C246-C255. 10.1152/ajpcell.00294.2010, 21084644.
33. Zhong Y, Ahmed S, Grupp IL, Matlib MA. Altered SR protein expression associated with contractile dysfunction in diabetic rat hearts. Am J Physiol Heart Circ Physiol 2001, 281(3):H1137-H1147.
34. Cameron NE, Cotter MA, Robertson S. Contractile properties of cardiac papillary muscle in streptozotocin-diabetic rats and the effects of aldose reductase inhibition. Diabetologia 1989, 32(6):365-370. 10.1007/BF00277260, 2503412.
35. Brown RA, Anthony MJ, Petrovski P, Ren J. The influence of gender, diabetes, and acetaldehyde on the intrinsic contractile properties of isolated rat myocardium. Cardiovasc Toxicol 2001, 1(1):35-42. 10.1385/CT:1:1:35, 12213995.
36. 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.
37. Lagadic-Gossmann D, Feuvray D. Decreased sensitivity of contraction to changes of intracellular pH in papillary muscle from diabetic rat hearts. J Physiol 1990, 422(1):481-497. 1190144, 2352189.
38. Kain V, Kumar S, Sitasawad S. Azelnidipine prevents cardiac dysfunction in streptozotocin-diabetic rats by reducing intracellular calcium accumulation, oxidative stress and apoptosis. Cardiovasc Diabetol 2011, 10(1):97. 3234183, 22054019.
39. Ren J, Davidoff AJ. Diabetes rapidly induces contractile dysfunctions in isolated ventricular myocytes. Am J Physiol Heart Circ Physiol 1997, 272(1):H148-H158.
40. Rösen P, Windeck P, Zimmer HG, Frenzel H, Bürrig KF, Reinauer H. Myocardial performance and metabolism in non-ketotic, diabetic rat hearts: myocardial function and metabolism in vivo and in the isolated perfused heart under the influence of insulin and octanoate. Basic Res Cardiol 1986, 81(6):620-635. 10.1007/BF02005186, 3545178.
41. Boudina S, Bugger H, Sena S, O'Neill BT, Zaha VG, Ilkun O, Wright JJ, Mazumder PK, Palfreyman E, Tidwell TJ, Theobald H, Khalimonchuk O, Wayment B, Sheng X, Rodnick KJ, Centini R, Chen D, Litwin SE, Weimer BE, Abel ED. Contribution of impaired myocardial insulin signaling to mitochondrial dysfunction and oxidative stress in the heart. Circulation 2009, 119(9):1272-1283. 10.1161/CIRCULATIONAHA.108.792101, 2739097, 19237663.
42. Radovits T, Korkmaz S, Loganathan S, Barnucz E, Bömicke T, Arif R, Karck M, Szabó G. Comparative investigation of the left ventricular pressure-volume relationship in rat models of type 1 and type 2 diabetes mellitus. Am J Physiol Heart Circ Physiol 2009, 297(1):H125-H133. 10.1152/ajpheart.00165.2009, 19429826.
43. Joffe II, Travers KE, Perreault-Micale CL, Hampton T, Katz SE, Morgan JP, Douglas PS. Abnormal cardiac function in the streptozotocin-induced, non-insulin-dependent diabetic rat: noninvasive assessment with doppler echocardiography and contribution of the nitric oxide pathway. J Am Coll Cardiol 1999, 34(7):2111-2119. 10.1016/S0735-1097(99)00436-2, 10588232.
44. Litwin SE, Raya TE, Anderson PG, Daugherty S, Goldman S. Abnormal cardiac function in the streptozotocin-diabetic rat. Changes in active and passive properties of the left ventricle. J Clin Invest 1990, 86(2):481-488. 10.1172/JCI114734, 296750, 2200804.
45. Penpargkul S, Schaible T, Yipintsoi T, Scheuer J. The effect of diabetes on performance and metabolism of rat hearts. Circ Res 1980, 47(6):911-921. 10.1161/01.RES.47.6.911, 7002345.
46. Shiels H, O'Connell A, Qureshi MA, Howarth FC, White E, Calaghan S. Stable microtubules contribute to cardiac dysfunction in the streptozotocin-induced model of type 1 diabetes in the rat. Mol Cell Biochem 2007, 294(1-2):173-180.
47. Bracken NK, Woodall AJ, Howarth FC, Singh J. Voltage-dependence of contraction in streptozotocin-induced diabetic myocytes. Mol Cell Biochem 2004, 261(1):235-243.
48. Schlack W, Preckel B, Stunneck D, Thämer V. Effects of halothane, enflurane, isoflurane, sevoflurane and desflurane on myocardial reperfusion injury in the isolated rat heart. Br J Anaesth 1998, 81(6):913-919. 10.1093/bja/81.6.913, 10211019.
49. Howarth FC, Qureshi A, Singh J. Effects of acidosis on ventricular myocyte shortening and intracellular Ca2+ in streptozotocin-induced diabetic rats. Mol Cell Biochem 2004, 261(1):227-233.
50. Han J-C, Goo S, Barrett CJ, Mellor KM, Taberner AJ, Loiselle DS. The afterload-dependent peak efficiency of the isolated working rat heart is unaffected by streptozotocin-induced diabetes. Cardiovasc Diabetol 2014, 13(1):4. 3916799, 24387738.
51. Taberner AJ, Han J-C, Loiselle DS, Nielsen PMF. An innovative work-loop calorimeter for in vitro measurement of the mechanics and energetics of working cardiac trabeculae. J Appl Physiol 2011, 111:1798-1803. 10.1152/japplphysiol.00752.2011, 21903883.
52. Han J-C, Taberner AJ, Nielsen PMF, Loiselle DS. Interventricular comparison of the energetics of contraction of trabeculae carneae isolated from the rat heart. J Physiol 2013, 591(3):701-717. 10.1113/jphysiol.2012.242719, 3577548, 23184511.
53. Han J-C, Taberner AJ, Nielsen PMF, Kirton RS, Ward M-L, Loiselle DS. Energetics of stress production in isolated cardiac trabeculae from the rat. Am J Physiol Heart Circ Physiol 2010, 299:H1382-H1394. 10.1152/ajpheart.00454.2010, 20729397.
54. Han J-C, Tran K, Taberner AJ, Nickerson DP, Kirton RS, Nielsen PMF, Ward M-L, Nash MP, Crampin EJ, Loiselle DS. Myocardial twitch duration and the dependence of oxygen consumption on pressure-volume area: experiments and modelling. J Physiol 2012, 590(18):4603-4622. 10.1113/jphysiol.2012.228965, 3477760, 22570375.
55. de Tombe PP, ter Keurs HEDJ. Force and velocity of sarcomere shortening in trabeculae from rat heart. Effects of temperature. Circ Res 1990, 66:1239-1254. 10.1161/01.RES.66.5.1239, 2335024.
56. Littell RC, Miliken GA, Stroup WW, Wolfinger RD, Schabenberger O. SAS for mixed models 2006, Cary, NC: SAS Institute Inc, 2.
57. Noda N, Hayashi H, Satoh H, Terada H, Hirano M, Kobayashi A, Yamazaki N. Ca2+ transients and cell shortening in diabetic rat ventricular myocytes. Jpn Circ J 1993, 57(5):449-457. 10.1253/jcj.57.449, 8510315.
58. Op Den Buijs J, Ligeti L, Ivanics T, Miklós Z, Van Der Vusse GJ, Van Riel NAW. Mathematical modelling of the calcium-left ventricular pressure relationship in the intact diabetic rat heart. Acta Physiol 2008, 193(3):205-217.
59. Metzger JM, Wahr PA, Michele DE, Albayya F, Westfall MV. Effects of myosin heavy chain isoform switching on Ca2+-activated tension development in single adult cardiac myocytes. Circ Res 1999, 84(11):1310-1317. 10.1161/01.RES.84.11.1310, 10364569.
60. Barclay JK, Gibbs CL, Loiselle DS. Stress as an index of metabolic cost in papillary muscle of the cat. Basic Res Cardiol 1979, 74:594-603. 10.1007/BF01907501, 548022.
61. Gibbs CL, Gibson WR. Effect of alterations in the stimulus rate upon energy output, tension development and tension-time integral of cardiac muscle in rabbits. Circ Res 1970, XXVII:611-618.
62. Goo S, Pham T, Han J-C, Nielsen P, Taberner A, Hickey A, Loiselle D. Multiscale measurement of cardiac energetics. Clin Exp Pharmacol Physiol 2013, 40(9):671-681. 10.1111/1440-1681.12139, 23745944.
63. Rundell VLM, Geenen DL, Buttrick PM, de Tombe PP. Depressed cardiac tension cost in experimental diabetes is due to altered myosin heavy chain isoform expression. Am J Physiol Heart Circ Physiol 2004, 287(1):H408-H413. 10.1152/ajpheart.00049.2004, 15001437.
64. Holubarsch C, Goulette RP, Litten RZ, Martin BJ, Mulieri LA, Alpert NR. The economy of isometric force development, myosin isoenzyme pattern and myofibrillar ATPase activity in normal and hypothyroid rat myocardium. Circ Res 1985, 56(1):78-86. 10.1161/01.RES.56.1.78, 3155672.
65. Holubarsch C, Litten RZ, Mulieri LA, Alpert NR. Energetic changes of myocardium as an adaptation to chronic hemodynamic overload and thyroid gland activity. Basic Res Cardiol 1985, 80(6):582-593. 10.1007/BF01907857, 4091775.
66. Siri FM, Malhotra A, Factor SM, Sonnenblick EH, Fein FS. Prolonged ejection duration helps to maintain pump performance of the renal-hypertensive-diabetic rat heart: correlations between isolated papillary muscle function and ventricular performance in situ. Cardiovasc Res 1997, 34(1):230-240. 10.1016/S0008-6363(96)00239-8, 9217895.
67. 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.