Electrophysiological basis of metabolic-syndrome-induced cardiac dysfunction

Canadian Journal of Physiology and Pharmacology

Volumn 94, Issue 10, 2016, Pages 1064-1073

  Okatan, Esma N ^a   Durak, Aysegul Toy ^a   Turan, Belma ^a  

^a ANKARA UNIVERSITY   (Turkey)

Author keywords

Calcium sparks; Calcium transients; Diabetes; Heart function; High sucrose diet; Insulin resistance; SERCA

Indexed keywords

PHOSPHATASE; PHOSPHOLAMBAN; PROTEIN KINASE; RYANODINE RECEPTOR 2; SODIUM CALCIUM EXCHANGE PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRIC FIELD; ELECTROSTIMULATION; HEART DISEASE; HEART ELECTROPHYSIOLOGY; HEART MUSCLE CONTRACTILITY; HEART PAPILLARY MUSCLE; MALE; METABOLIC SYNDROME X; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SARCOPLASMIC RETICULUM; SUGAR INTAKE;

EID: 84989902351     PISSN: 00084212     EISSN: 12057541     Source Type: Journal    
DOI: 10.1139/cjpp-2015-0531     Document Type: Article

References (47)

1. Aguilera, A.A., Díaz, G.H., Barcelata, M.L., Guerrero, O.A., and Ros, R.M. 2004. Effects of fish oil on hypertension, plasma lipids, and tumor necrosis factoralpha in rats with sucrose-induced metabolic syndrome. J. Nutr. Biochem. 15(6): 350-357. doi: 10.1016/j.jnutbio.2003.12.008. PMID: 15157941.
2. Balderas-Villalobos, J., Molina-Munoz, T., Mailloux-Salinas, P., Bravo, G., Carvajal, K., and Gomez-Viquez, N.L. 2013. Oxidative stress in cardiomyocytes contributes to decreased SERCA2a activity in rats with metabolic syndrome. Am. J. Physiol. 305(9): H1344-H1353. doi: 10.1152/ajpheart.00211.2013.
3. Bassani, R.A., Bassani, J.W., and Bers, D.M. 1992. Mitochondrial and sarcolemmal Ca2+ transport reduce [Ca2+]i during caffeine contractures in rabbit cardiac myocytes. J. Physiol. (Lond.) 453: 591-608. PMID: 1464847.
4. Belke, T.W., and Pierce, W.D. 2014. Effect of sucrose availability and pre-running on the intrinsic value of wheel running as an operant and a reinforcing consequence. Behav. Processes, 103: 35-42. doi: 10.1016/j.beproc.2013.11.010.
5. Bell, D.S. 2003. Heart failure: the frequent, forgotten, and often fatal complication of diabetes. Diabetes Care, 26(8): 2433-2441. doi: 10.2337/diacare.26.8. 2433. PMID: 12882875.
6. Bouchard, R.A., and Bose, D. 1991. Influence of experimental diabetes on sarcoplasmic reticulum function in rat ventricular muscle. Am. J. Physiol. 260(2 Pt 2): H341-H354. PMID: 1996680.
7. Ceylan-Isik, A.F., Kandadi, M.R., Xu, X., Hua, Y., Chicco, A.J., Ren, J., and Nair, S. 2013. Apelin administration ameliorates high fat diet-induced cardiac hypertrophy and contractile dysfunction. J. Mol. Cell. Cardiol. 63: 4-13. doi: 10.1016/ j.yjmcc.2013.07.002. PMID: 23859766.
8. Chen, G.C., Huang, C.Y., Chang, M.Y., Chen, C.H., Chen, S.W., Huang, C.J., and Chao, P.M. 2011. Two unhealthy dietary habits featuring a high fat content and a sucrose-containing beverage intake, alone or in combination, on in- ducing metabolic syndrome in Wistar rats and C57BL/6J mice. Metabolism, 60(2): 155-164. doi: 10.1016/j.metabol.2009.12.002. PMID: 20045537.
9. Cheng, H., Lederer, W.J., and Cannell, M.B. 1993. Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science, 262(5134): 740-744. doi: 10.1126/science.8235594. PMID: 8235594.
10. Choi, K.M., Zhong, Y., Hoit, B.D., Grupp, I.L., Hahn, H., Dilly, K.W., Guatimosim, S., Lederer, W.J., and Matlib, M.A. 2002. Defective intracellular Ca(2+) signaling contributes to cardiomyopathy in Type 1 diabetic rats. Am. J. Physiol. 283(4): H1398-H1408. doi: 10.1152/ajpheart.00313.2002.
11. Curran, J., Hinton, M.J., Ríos, E., Bers, D.M., and Shannon, T.R. 2007. Betaadrenergic enhancement of sarcoplasmic reticulum calcium leak in cardiac myocytes is mediated by calcium/calmodulin-dependent protein kinase. Circ. Res. 100(3): 391-398. doi: 10.1161/01.RES.0000258172.74570.e6. PMID: 17234966.
12. Davidoff, A.J., Mason, M.M., Davidson, M.B., Carmody, M.W., Hintz, K.K., Wold, L.E., Podolin, D.A., and Ren, J. 2004. Sucrose-induced cardiomyocyte dysfunction is both preventable and reversible with clinically relevant treatments. Am. J. Physiol. 286(5): E718-E724. doi: 10.1152/ajpendo.00358.2003.
13. Dinh, W., Lankisch, M., Nickl, W., Gies, M., Scheyer, D., Kramer, F., Scheffold, T., Krahns, T., Sause, A., and Futh, R. 2011. Metabolic syndrome with or without diabetes contributes to left ventricular diastolic dysfunction. Acta Cardiol. 66(2): 167-174. PMID: 21591574.
14. Dutta, K., Podolin, D.A., Davidson, M.B., and Davidoff, A.J. 2001. Cardiomyocyte dysfunction in sucrose-fed rats is associated with insulin resistance. Diabetes, 50(5): 1186-1192. doi: 10.2337/diabetes.50.5.1186. PMID: 11334425.
15. Dutta, K., Carmody, M.W., Cala, S.E., and Davidoff, A.J. 2002. Depressed PKA activity contributes to impaired SERCA function and is linked to the pathogenesis of glucose-induced cardiomyopathy. J. Mol. Cell. Cardiol. 34(8): 985-996. doi: 10.1006/jmcc.2002.2035. PMID: 12234768.
16. Eisner, D.A., Díaz, M.E., O’Neill, S.C., and Trafford, A.W. 2000. The ryanodine receptor: cause or consequence of diabetic heart failure? J. Mol. Cell. Cardiol. 32(7): 1377-1378. doi: 10.1006/jmcc.2000.1163. PMID: 10861137.
17. Fauconnier, J., Lacampagne, A., Rauzier, J.M., Fontanaud, P., Frapier, J.M., Sejersted, O.M., Vassort, G., and Richard, S. 2005. Frequency-dependent and proarrhythmogenic effects of FK-506 in rat ventricular cells. Am. J. Physiol. 288(2): H778-H786. doi: 10.1152/ajpheart.00542.2004.
18. Fontes-Carvalho, R., Ladeiras-Lopes, R., Bettencourt, P., Leite-Moreira, A., and Azevedo, A. 2015. Diastolic dysfunction in the diabetic continuum: association with insulin resistance, metabolic syndrome and type 2 diabetes. Cardiovasc. Diabetol. 14: 4. doi: 10.1186/s12933-014-0168-x. PMID: 25582424.
19. Ganguly, P.K., Pierce, G.N., Dhalla, K.S., and Dhalla, N.S. 1983. Defective sarcoplasmic reticular calcium transport in diabetic cardiomyopathy. Am. J. Physiol. 244(6): E528-E535. PMID: 6134470.
20. Grundy, S.M., Hansen, B., Smith, S.C., Jr., Cleeman, J.I., Kahn, R.A., American Heart, A., National Heart, L., Blood, I., and American Diabetes, A. 2004. Clinical management of metabolic syndrome: report of the American Heart Association/National Heart, Lung, and Blood Institute/American Diabetes Association conference on scientific issues related to management. Artheroscler. Thromb.Vasc. Biol. 24(2): e19-e24. doi: 10.1161/01.ATV.0000112379.88385. 67.
21. Guo, J.Z., Gong, Y.C., Zhang, J.L., Qing, Y.W., Dai, Q.Y., Wang, Y.C., Gao, X., and Ni, Y.F. 2005. [A clinical intervention study among 463 essential hypertensive patients with metabolic syndrome]. Zhonghua xin xue guan bing za zhi, 33(2): 132-136. PMID: 15924807.
22. Hansen, B.C. 1999. The metabolic syndrome X. Ann. N.Y. Acad. Sci. 892: 1-24. doi: 10.1111/j.1749-6632.1999.tb07782.x. PMID: 10842649.
23. Hintz, K.K., Aberle, N.S., and Ren, J. 2003. Insulin resistance induces hyperleptinemia, cardiac contractile dysfunction but not cardiac leptin resistance in ventricular myocytes. Int. J. Obesity Related Metab. Dis. 27(10): 1196-1203. doi: 10.1038/sj.ijo.0802389.
24. Kassi, E., Pervanidou, P., Kaltsas, G., and Chrousos, G. 2011. Metabolic syndrome: definitions and controversies. BMC Med. 9: 48. doi: 10.1186/1741-7015-9-48. PMID: 21542944.
25. Kim, J.K., Ju, Y.S., Moon, S.J., Song, Y.R., Kim, H.J., and Kim, S.G. 2013. High pulse pressure and metabolic syndrome are associated with proteinuria in young adult women. BMC Nephrol. 14: 45. doi: 10.1186/1471-2369-14-45. PMID: 23433013.
26. Lee, T.C., and McDonald, E.G. 2015. Clinician Understanding of Cholesterol Treatment Guidelines. JAMA, 313(23): 2381-2382. doi: 10.1001/jama.2015.5519. PMID: 26080349.
27. Lempiäinen, P., Mykkänen, L., Pyörälä, K., Laakso, M., and Kuusisto, J. 1999. Insulin resistance syndrome predicts coronary heart disease events in elderly nondiabetic men. Circulation, 100(2): 123-128. doi: 10.1161/01.CIR.100.2.123. PMID: 10402440.
28. Li, S.Y., Yang, X., Ceylan-Isik, A.F., Du, M., Sreejayan, N., and Ren, J. 2006. Cardiac contractile dysfunction in Lep/Lep obesity is accompanied by NADPH oxidase activation, oxidative modification of sarco(endo)plasmic reticulum Ca2+-ATPase and myosin heavy chain isozyme switch. Diabetologia, 49(6): 1434-1446. doi: 10.1007/s00125-006-0229-0. PMID: 16612592.
29. Lopez-Jaramillo, P., Lopez-Lopez, J., Lopez-Lopez, C., and Rodriguez-Alvarez, M.I. 2014. The goal of blood pressure in the hypertensive patient with diabetes is defined: now the challenge is go from recommendations to practice. Diabetol. Metab. Syndr. 6(1): 31. doi: 10.1186/1758-5996-6-31. PMID: 24594121.
30. Malhotra, A., Penpargkul, S., Fein, F.S., Sonnenblick, E.H., and Scheuer, J. 1981. The effect of streptozotocin-induced diabetes in rats on cardiac contractile proteins. Circ. Res. 49(6): 1243-1250. doi: 10.1161/01.RES.49.6.1243. PMID: 6458419.
31. Matsuzawa, Y., Funahashi, T., and Nakamura, T. 2011. The concept of metabolic syndrome: contribution of visceral fat accumulation and its molecular mechanism. J. Atheroscler. Thromb. 18(8): 629-639. doi: 10.5551/jat.7922. PMID: 21737960.
32. Mellor, K.M., Wendt, I.R., Ritchie, R.H., and Delbridge, L.M. 2012. Fructose diet treatment in mice induces fundamental disturbance of cardiomyocyte Ca2+ handling and myofilament responsiveness. Am. J. Physiol. 302(4): H964-H972. doi: 10.1152/ajpheart.00797.2011.
33. Misra, T., Gilchrist, J.S., Russell, J.C., and Pierce, G.N. 1999. Cardiac myofibrillar and sarcoplasmic reticulum function are not depressed in insulin-resistant JCR: LA-cp rats. The Am. J. Physiol. 276(6 Pt 2): H1811-H1817. PMID: 10362658.
34. Okatan, E.N., K.S., Gokturk, H, Can, B, and Turan, B. 2015a. High-carbohydrate diet-induced myocardial remodelling in rats. Curr. Res. Cardiol. 2(1): 5-10.
35. Okatan, E.N., Tuncay, E., Hafez, G., and Turan, B. 2015b. Profiling of cardiac beta-adrenoceptor subtypes in the cardiac left ventricle of rats with metabolic syndrome: Comparison with streptozotocin-induced diabetic rats. Can. J. Physiol. Pharmacol. 93(7): 517-525. doi: 10.1139/cjpp-2014-0507. PMID: 25994289.
36. Ozdemir, S., Ugur, M., Gurdal, H., and Turan, B. 2005. Treatment with AT1 receptor blocker restores diabetes-induced alterations in intracellular Ca(2+) transients and contractile function of rat myocardium. Arch. Biochem. Biophys. 435(1): 166-174. doi: 10.1016/j.abb.2004.11.027. PMID: 15680918.
37. Panchal, S.K., and Brown, L. 2011. Rodent models for metabolic syndrome research. J. Biomed. Biotechnol. 2011: 351982. doi: 10.1155/2011/351982. PMID: 21253582.
38. Schannwell, C.M., Schneppenheim, M., Perings, S., Plehn, G., and Strauer, B.E. 2002. Left ventricular diastolic dysfunction as an early manifestation of diabetic cardiomyopathy. Cardiology, 98(1-2): 33-39. doi: 10.1159/000064682. PMID: 12373045.
39. Streja, D. 2004. Metabolic syndrome and other factors associated with increased risk of diabetes. Clin. Cornerstone, 6(S3): S14-S29. PMID: 15707266.
40. Suh, S., and Lee, M.K. 2014. Metabolic syndrome and cardiovascular diseases in Korea. J. Atherscler. Thromb. 21(S1): S31-S35. PMID: 24452115.
41. Tang, W.H., Cheng, W.T., Kravtsov, G.M., Tong, X.Y., Hou, X.Y., Chung, S.K., and Chung, S.S. 2010. Cardiac contractile dysfunction during acute hyperglycemia due to impairment of SERCA by polyol pathway-mediated oxidative stress. Am. J. Physiol.: Cell. Physiol. 299(3): C643-C653. doi: 10.1152/ajpcell. 00137.2010.
42. Turan, B., Fliss, H., and Desilets, M. 1997. Oxidants increase intracellular free Zn2+ concentration in rabbit ventricular myocytes. Am. J. Physiol. 272(5 Pt 2): H2095-H2106. PMID: 9176274.
43. Vasanji, Z., Cantor, E.J., Juric, D., Moyen, M., and Netticadan, T. 2006. Alterations in cardiac contractile performance and sarcoplasmic reticulum function in sucrose-fed rats is associated with insulin resistance. Am. J. Physiol.: Cell. Physiol. 291(4): C772-C780. doi: 10.1152/ajpcell.00086.2005.
44. Wehrens, X.H., and Marks, A.R. 2003. Altered function and regulation of cardiac ryanodine receptors in cardiac disease. Trends Biochem. Sci. 28(12): 671-678. doi: 10.1016/j.tibs.2003.10.003. PMID: 14659699.
45. Wold, L.E., Dutta, K., Mason, M.M., Ren, J., Cala, S.E., Schwanke, M.L., and Davidoff, A.J. 2005. Impaired SERCA function contributes to cardiomyocyte dysfunction in insulin resistant rats. J. Mol. Cell. Cardiol. 39(2): 297-307. doi: 10.1016/j.yjmcc.2005.03.014. PMID: 15878173.
46. Xi, S., Yin, W., Wang, Z., Kusunoki, M., Lian, X., Koike, T., Fan, J., and Zhang, Q. 2004. A minipig model of high-fat/high-sucrose diet-induced diabetes and atherosclerosis. Int. J. Exp. Pathol. 85(4): 223-231. doi: 10.1111/j.0959-9673. 2004.00394.x. PMID: 15312127.
47. Yaras, N., Ugur, M., Ozdemir, S., Gurdal, H., Purali, N., Lacampagne, A., Vassort, G., and Turan, B. 2005. Effects of diabetes on ryanodine receptor Ca release channel (RyR2) and Ca2+ homeostasis in rat heart. Diabetes, 54(11): 3082-3088. doi: 10.2337/diabetes.54.11.3082. PMID: 16249429.