Alterations in myocardial contractile proteins in diabetes mellitus

Coronary Artery Disease

Volumn 7, Issue 2, 1996, Pages 124-132

  Akella, Arvind Babu ^a   Sonnenblick, Edmund H ^a   Gulati, Jag ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

calcium; length; myosin; Starking's law of the heart; troponin T

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CALCIUM; CONTRACTILE PROTEIN; MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE; REGULATOR PROTEIN; TROPONIN C; TROPONIN I; TROPONIN T;

ANIMAL EXPERIMENT; ANIMAL MODEL; CARDIOMYOPATHY; CONTROLLED STUDY; DIABETES MELLITUS; HEART MUSCLE CONTRACTILITY; NONHUMAN; PRIORITY JOURNAL; RAT; REVIEW; SARCOMERE; SODIUM CALCIUM EXCHANGE;

EID: 0030017344     PISSN: 09546928     EISSN: None     Source Type: Journal    
DOI: 10.1097/00019501-199602000-00005     Document Type: Review

References (104)

1. Dillman WH: Diabetes and thyroid-hormone-induced changes in cardiac function and their molecular basis. Ann Rev Med 1989, 40:373-394. This article together with [14] provides a succint summary of the literature on dibetes. The discussion concerning alterations in myosin is especially relevant.
2. Fein FS, Sonnenblick EH: Diabetic cardiomyopathy. Prog Cardiovasc Dis 1985, 27:255-270.
3. Silver MD, Huckell VS, Lorber M: Basement membranes of small cardiac vessels in patients with diabetic and myxedema: preliminary observations. Pathology 1977, 9:213-220.
4. Fischer VW, Barner HB, Leskiw ML: Capillary basal laminar thickness in diabetic human myocardium. Diabetes 1979, 28:713-719.
5. Factor SM, Okun EM, Minase T: Capillary microaneurysms in the human diabetic heart N Engl J Med 1980, 302:384-388.
6. Fischer VW, Barner HB, Larose LS: Pathomorphologic aspects of muscular tissue in diabetes mellitus. Hum Pathol 1984, 15:1127-1136.
7. Hamby RI, Zoneraich S, Sheran L: Diabetic cardiomyopathy. JAMA 1974, 229:1749-1754.
8. Blumenthal HT, Alex M, Goldberg S: A study of lesions internal coronary artery branches in diabetes mellitus. Arch Pathol 1960, 70:13-28
9. Clarke BF, Ewing DJ, Campbell IW: Diabetic autonomic neuropathy. Diabetologia 1979, 17:195-212.
10. Ewing DJ, Campbell IW, Clarke B: Heart rate changes in diabetes mellitus. Lancet 1981, i:183-186.
11. Weiling W, Borst C, Van Dorgen Toram MA, Van der Hofsteide JW, Van Brederode JFM, Endert E, et al.: Relationship between impaired parasympathetic and sympathetic cardiovascular control in diabetes mellitus. Diabetologia 1983, 24:422-427.
12. Lloyd-Mostyn RH, Watkins PJ: Total cardiac denervation in diabetic autonomic neuropathy. Diabetes 1976, 25:748-751.
13. Tomheh JF, Shah SD, Cryer PE: The pathogenesis of hyperadrenergic postural hypotension in diabetic patients. Am J Med 1979, 67:772-778.
14. Tahiliani AG, McNeill JH: Diabetes-induced abnormalities in the myocardium. Life Sci 1986, 38:959-974. Together with [1], this is an important review of the myosin abnormalities in diabetes.
15. Rani MA, Venkatraman BV, Jaiprakash R, Andrade C: Effect of felodopine on myocardial function and cholinergic responses in short term streptozotocin diabetes in rats, Ind J Exp Biol 1994, 32:629-632.
16. Opie L, Tansey MJ, Kennelly BM: The heart in diabetes mellitus. South Afr Med J 1979, 56:207-211.
17. Garland PG, Randle PJ, Newsholm EA: Citrate as an intermediary in the inhibition of phosphofructokinase in rat heart muscle by fatty acids ketone bodies, pyruvate, diabetes and starvation. Nature 1963, 200:169-170.
18. Rubler S, Dlugash J, Yuceoglu YZ: New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol 1972, 30:595-602.
19. Regan TJ, Lyons MM, Ahmed SS: Evidence for cardiomyopathy in familial diabetes mellitus. J Clin Invest 1977, 60:885-899.
20. Ahmed SS, Ghazanfar AJ, Narang RM, Regan TJ: Preclinical abnormality of left ventricular function in diabetes mellitus. Am Heart J 1975, 89:153-158.
21. Carbonell LF, Salom MG, Garcia-Estan J, Salazar FJ, Ubeda M, Quesada T: Hemodynamic alterations in chronically conscious unrestrained diabetic rats. Am J Physiol 1987, 252:H900-H905.
22. Dowell RT, Atkins FL, Love S: Integrative nature and time course of cardiovascular alterations in the diabetic rat J Cardiovasc Pharmacol 1986, 8:406-413.
23. Airaksinen KE, Ikaheimo MJ, Linnaluoto MK, Huikuri HV, Takkunen JT: Increased left atrial size relative to left ventricular size in young women with insulin-dependent diabetes: a preclinical sign of the specific heart disease of diabetes? Diabetes Res 1987, 6:37-41.
24. Raev DC: Evolution of cardiac changes in young insulin-dependent (type 1) diabetic patients: one more piece of the puzzle of diabetic cardiomyopathy. Clin Cardiol 1993, 16:784-790.
25. Regan TJ, Ettinger PO, Khan MI, Jesrani MU, Lyons HA, Oldwurtel HA, et al.: Altered myocardial function and metabolism in chronic diabetes mellitus without ischemia in dogs. Circ Res 1974, 35:222-237.
26. Haider B, Yeh CK, Thomas G, Oldwurtel HA, Lyons MM, Regan TJ: Influence of diabetes on the myocardium and coronary arteries of rhesus monkey fed an atherogenic diet Circ Res 1981, 49:1278-1288.
27. Wu CF, Yeh CK, Oldwurtel HA, Lyons MM, Regan TJ: Does chronic insulin use affect the myocardial abnormalities of diabetes mellitus. Circulation 1977, 207 (suppl III):III55-III61.
28. Pelouch V, Dixon IM, Golfman L, Beamish RE, Dhalla NS: Role of extracellular matrix proteins in heart function. Mol Cell Biochem 1993, 129:101-120.
29. Pierce GN, Beamish RE, Dhalla NS: Heart Dysfunction in Diabetes. Boca Raton, Florida: CRC Press; 1988.
30. Fein FS, Kornstein LB, Strobeck JE, Capasso JM, Sonnenblick EH: Altered myocardial mechanics in diabetic rats. Circ Res 1980, 47:922-933, This is the first article in an important series of studies by these authors reporting mechanical abnormalities in isolated cardiac muscle. Their later studies [32] included measurements of biochemical parameters as well and the two together provided a conceptual understanding of myocardial dysfunction up to thai time.
31. Penpargkul S, Schaible T, Yiptinosi T, Scheuer J: The effect of diabetes on performance and metabolism of rat hearts. Circ Res 1980, 47:911-921.
32. Fein FS, Malhotra A, Miller-Green B, Scheuer J, Sonnenblick EH: Diabetic cardiomyopathy in rats: mechanical and biochemical response to different insulin doses. Am J Physiol 1984, 247:H817-H823.
33. Dillman WH: Diabetes mellitus induces changes in cardiac myosin in the rat Diabetes 1980, 29:579-582.
34. Ganguly PK, Pierce GN, Dhalla KS, Dhalla NS: Defective sarcoplasmic reticular calcium transport in diabetic cardiomyopathy. Am J Physiol 1983, 244:E528-E535.
35. Heyliger CE, Prakash A, McNeill JH: Alterations in cardiac sarcolemmal Ca pump activity during diabetes mellitus. Am J Physiol 1987, 252:H540-H544.
36. Penpargkul S, Fein FS, Sonnenblick EH, Scheuer J: Depressed cardiac sarcoplasmic reticular function from diabetic rats. J Mol Cell Cardiol 1981, 13:303-309.
37. Lopashuk 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. Car J Physiol Pharmacol 1983, 61:439-448.
38. Pitts B, Tate CA, Van Winkle B, Wood JM, Entman ML: Palmitylcarnitine inhibition of the calcium pump in cardiac sarcoplasmic reticulum: a possible role In myocardial ischemia. Life Sci 1978, 23:391-402.
39. Rupp H, Elimban V, Dhalla NS: Modification of myosin isozymes and SR Ca(2+)-pump ATPase of the diabetic rat heart by lipid-lowering interventions. Mol Cell Biochem 1994, 132:69-80.
40. Pierce GN, Dhalla NS: Sarcotemmal Na-K-ATPase activity in diabetic rat heart Am J Physiol 1983, 245:C241-C247.
41. Onji T, Liu M-S: Effects of alloxan-diabetes on the sodium-potassium adenosine triphosphatase enzyme system in dog hearts. Biochem Biophys Res Commun 1980, 96:387-397,
42. Bassani BA, Bassani JW, Bers D: Relaxation in ferret ventricular myocytes: unusual interplay among calcium transport systems. J Physiol 1994, 476:295-308.
43. Bouchard RA, Clark RB, Giles WL: Role of sodium-calcium exchange in activation of contraction in rat ventricle. J Physiol 1993, 472:391-413,
44. Negretti N, O'Neill SC, Eisner DA: The relative contributions of different intracellular and sarcolemmal systems to relaxations in rat ventricular myocytes. Cardiovasc Res 1993, 27:1826-1830.
45. Harrison SM, McCall E, Boyett MR: The relationship between contraction and intracellular sodium in rat and guinea-pig ventricular myocytes. J Physiol 1992, 449:517-550.
46. Weir WG: Intracellular calcium during excitation-contraction coupling in mammalian ventricle. Med Sci Sports Exercise 1991, 23:1149-1156.
47. O'Neill SC, Valdeolmillos M, Lamont C, Douso P, Eisner DA: The contribution of Na-Ca exchange to relaxation in mammalian cardiac muscle. Ann NY Acad Sci 1991, 639:444-452.
48. Jenkins RL, G MH, Digerness S, Parrish SW, Ong RL: Adenine nucleotide metabolism in hearts of diabetic rats: comparisons to diaphragm, liver, and kidney. Diabetes 1988, 37:629-636.
49. Su CY, Payne M, Strauss AW, Dillamn WH: Selective reduction of creatine kinase subunit mRNAs in striated muscles of diabetic rats. Am J Physiol 1992, 263:E310-316,
50. Lymn RW, Taylor EW: Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 1971, 10:4617-4624,
51. Payment I, Holden HM, Whittaker M, Yohn CB, Lorenz M, Holmes KC, et al.: Structure of the actin-myosin complex and its implications for muscle contraction. Science 1993, 261:58-65.
52. Huxley A: Reflections on Muscle. Princeton, New Jersey: Princeton University Press; 1980.
53. Brenner B: Muscle mechanics and biochemical kinetics. In Molecular Mechanisms in Muscle Contraction: Edited by Squire JM, Boca Raton, Florida: CRC Press; 1990:77-150.
54. Cooke R: The mechanism of muscle contraction. CRC Crit Rev Biochem 1986, 21:53-118.
55. Gulati J, Babu A: Contraction kinetics of intact and skinned frog muscle fibers and degree of activation. J Gen Physiol 1985, 86:479-500.
56. Barrieux A, Neeley WE, Dillmann WH: Diabetes-induced alterations in the transcriptional activity of specific messenger ribonucleic acids from rat hearts. Circ Res 1985, 57:296-303.
57. Shanker R, Neeley WE, Dillmann WH: Rapid effects of insulin on the in vitro translational activity of specific mRNAs in the diabetic rat heart Am J Physiol 1986, 250:E355-E363.
58. Jefferson LS: Role of insulin in the protein synthesis. Diabetes 1980, 29:487-496.
59. Williams IH, Chua BHL, Sahms RH, Siehl D, Morgan HE: Effects of diabetes on protein turnover in cardiac muscle. Am j Physiol 1980, 239:E178-E185.
60. Hoh JFY, McGrath PA, Hale PT: Electrophoretic analysis of multiple forms of rat cardiac myosin: effects of hypophysectomy and thyroxine replacement J Mol Cell Cardiol 1977, 10:1053-1076. The pyrophospahate gels used to analyze cardiac myosin provided a technical breakthrough into the study of myosin isoformic shifts during cardiomyopathy.
61. Mercadier JJ, Lompre AM, Wisnewsky JL, Samuel J, Bercovici B, Swynghedauw B, et al.: Myosin isoenzymic changes in several models of rat cardiac hypertrophy. Circ Res 1981, 49:525-532.
62. Malhotra A, Penpargkul P, Fein F, Sonnenblick EH, Scheuer J: The effect of streptozotocin-induced diabetes in rats on cardiac contractile proteins. Circ Res 1981, 49:1243-1250.
63. Akella AB, Ding X-L, Cheng R, Gulati J: Diminished Ca sensitivity of skinned cardiac muscle contractility coincident with troponin T-band shifts in the diabetic rat Circ Res 1995, 76:600-606. This was the first report of troponin T alterations in diabetes. Many of the recent findings discussed in the present review were taken from this paper which contains further details.
64. Hofmann PA, Menon V, Gannaway KF: Effects of diabetes on isometric tension as a function of Ca and pH in rat cardiac myocytes. Am J Physiol 1995, 269:H1656-H1663.
65. Anderson PAW, Malouf NN, Oakeley AE, Pagani ED, Allen PD: troponin T isoform expression in humans: a comparison among normal and failing adult heart, fetal heart, and adult and fetal skeletal muscle. Cire Res 1991, 69:1226-1233. This important study related troponin T alterations to heart failure.
66. Theirfelder L, Watkins H, Macrae C, Lamas R, McKenna W, Vosberg H-P, et al.: Alpha-tropomyosin and cardiac troponin T mutations cause familial cardiomyopathy: a disease of the sarcomere. Cell 1994, 77:701-712. Genetic analysis indicated point mutations in the thin filament proteins and suggested that these mutations were cntical in causing heart failure in humans.
67. Gulati J, Akella AB, Nikolic SD, Stare V, Siri F: Shifts in contractile regulatory protein subunits troponin T and troponin I in cardiac hypertrophy. Biochem Biophys Res Commun 1994, 202:384-390. The first report of troponin T changes in an experimental heart failure model, the guinea pig with aortic constriction, indicated that troponin T shifts accompanied the resultant hypertrophy and that an even more drastic troponin T change occured in extreme heart failure.
68. Watkins H, McKenna WJ, Theirfelder L, Suk HJ, Anan R, O'Donoghue A, et al.: Mutations in the genes for cardiac troponin T and alpha-tropomyosin in hypertrophic cardiomyopathy. N Engl J Med 1995, 332:1058-1064.
69. Elstein E: The molecular genetics of hypertrophic cardiomyopathy. Curr Opin Cardiol 1995, 10:293-298.
70. Mayer NJ, Rubin SA: The molecular and cellular biology of heart failure Curr Opin Cardiol 1995, 10:238-245.
71. Anderson PAW: The molecular genetics of cardiovascular disease. Curr Opin Cardiol 1995, 10:33-43.
72. Pope B, Hoh JFY, Weeds A: The ATPase activities of rat cardiac myosin isoenzymes. FEBS Lett 1980, 118:205-208.
73. Sata M, Sugiura S, Yamashita H, Momomura S, Serizawa T: Dynamic interaction between cardiac myosin isoforms modifies velocity of actomyosin sliding in vitro. Circ Res 1993, 73:696-704.
74. Harris DE, Work SS, Wright RK, Alpert NR, Warshaw DM: Smooth, cardiac and skeletal muscle myosin force and motion generation assessed by cross-bridge mechanical interactions in vitro. J Musc Res Cell Motil 1994, 15:11-19.
75. Swynghedauw B: Developmental and functional adaptations of contractile proteins in cardiac and skeletal muscles. Physiol Rev 1986, 66:710-771.
76. Pagani ED, Julian FJ: Rabbit papillary muscle myosin isozymes and the velocity of muscle shortening. Circ Res 1984, 54:586-594
77. Matsuoka R, Beisel KW, Furutani M, Arai S, Takao A: Complete sequence of human cardiac alpha-myosin heavy chain gene and amino acid comparison to other myosins based on structural and functional differences. Am J Med Genet 1991, 41:537-547.
78. Epp TA, Dixon IM, Wang HY, Sole MJ, Liew CC: Structural organization of the human cardiac alpha-myosin heavy chain gene. Genomics 1993, 18:505-509.
79. Jandreski MA, Liew CC: Construction of a human ventricular cDNA library and characterization of a beta myosin heavy chain cDNA clone. Hum Genet 1987, 76:47-53.
80. Diederich KW, Eisele I, Ried T, Jaenicke T, Lichter P, Vosberg HP: Isolation and characterization of the complete human beta-myosin heavy chain gene. Hum Genet 1989, 81:214-220
81. Van den Berg MH, Meijer H, Geraedts JP: A trinucleotide repeat combination polymorphism in the cardiac alpha myosin heavy chain (MYH6) gene. Hum Genet 1995, 95:723-724.
82. Wang R, Sole MJ, Cukerman E, Liew CC: Characterization and nucleotide sequence of the cardiac alpha-myosin heavy chain gene from Syrian hamster. J Mol Cell Cardiol 1994, 29:1155-1165.
83. McNally EM, Kraft R, Bravo-Zender M, Taylor DA, Leinwand LA: Full-length rat alpha and beta cardiac myosin heavy chain sequences. Comparisons suggest molecular basis for functional differences. J Mol Biol 1989, 210:665-671.
84. Pierce GN, Dhalla NS: Cardiac myofibrillar ATpase activity in diabetic rats. J Mol Cell Cardiol 1981, 13:1063-1069.
85. Dillman WH: Influence of thyroid hormone administration on myosin ATPase activity and myosin isoenzyme distribution in the heart of diabetic rats. Metabolism 1982, 31:199-204.
86. Pollack PS, Malhotra A, Fein FS, Scheuer J: Effects of diabetes on cardiac contractile proteins in rabbits and reversal with insulin. Am J Physiol 1986, 251 :H448-H454.
87. Fein FS, Miller-Green B, Sonnenblick EH: Altered myocardial mechanics in diabetic rabbits. Am J Physiol 1985, 248:H729-H736.
88. Sternthal E, Like AA, Sarantis K, Braverman LE: Lymphocytic thyroiditls in the BB/W rat A new model of autoimmune endocrinopathy. Diabetes 1981, 30:1058-1061.
89. Malhotra A, Mordes JP, McDermott ML, Schaible TB: Abnormal cardiac biochemistry in spontaneously diabetic BB/W rat Am J Physiol 1985, 249:H1051-H1055.
90. Rodrigues B, McNeill JH: Cardiac dysfunction in isolated perfused hearts from spontaneously diabetic BB rats. Can J Physiol Pharmacol 1990, 68:514-518.
91. Fein FS, Strobeck JE, Malhotra A, Scheuer J, Sonnenblick EH: Reversibility of diabetic cardiomyopathy with insulin in rats. Circ Res 1981, 49:1251-1261.
92. Cagliero E, Barrieux A, Lehman C, Dillmann WH: Diabetes-induced changes of proteins synthesized by adult cardiac myocytes are partially reversed by insulin. J Mol Cell Cardiol 1988, 20:427-434.
93. Geister-Lowrance AAT, Kass S, Tonigawa G, Vosberg H-P, Seidman JG, Seidman CE: A molecular basis for familial hypertrophic cardiomyopathy: a beta cardiac myosin heavy gene missense mutation. Cell 1990, 62:999-1006.
94. Cuda G, Fananapazir L, Zhu W, Sellers JR, Epstein ND: Skeletal muscle expression and abnormal function of beta-myosin in hypertrophic cardiomyopathy. J Clin Invest 1993, 91:2861-2865.
95. Farah CS, Reinach FC: The troponin complex and regulation of muscle contraction. FASEB J 1995, 9:755-767.
96. Ding X-L, Akella AB, Gulati J: Contributions of troponin I and troponin C to the acidic pH-induced depression of contractile Ca sensitivity in cardiotrabeculae. Biochemistry 1995, 34: 2309-2316.
97. Breitbart RE, Nguyen HT, Medtord RM, Mahdavi V, Nadal-Ginard B: Intricate combinatorial patterns of exon splicing generate multiple regulated troponin T isoforms from a single gene. Cell 1985, 41:67-82.
98. Briggs MM, Schachat F: Origin of fetal troponin T: developmentally regulated splicing of a new exon in the fast troponin T gene. Dev Biol 1993, 158:503-509.
99. Tobacman LS, Lee R: Isolation and functional comparison of bovine cardiac troponin T isoforms. J Biol Chem 1987, 262:4059-4064.
100. Risnik VV, Verin AD, Gusev NB: Comparison of the structure of two cardiac troponin T isoforms. Biochem J 1985, 225:549-552.
101. Hibberd MG, Jewell BR: Calcium and length dependent force production in rat ventricular muscle. J Physiol 1978, 329: 527-540. This study established an important conceptual link between sarcomere length-dependent alterations in Ca sensitivity of permeabilized cardiac muscle and Starling's law of the heart.
102. Gulati J: The molecular biology of the length-tension relationship. In Molecular Mechanism of Muscle Contraction. Edited by Sugi H, Pollack GH. Tokyo: Plenum Publishing; 1993:593-602. These authors extended the concepts of Hibberd and Jewell [101] and, furthermore tried to develop a molecular basis for the mechanism underlying the Starling mechanism. They proposed that troponin C has a central role as a length sensor, and this has now become important with the discovery that troponin T alterations in cardiomyopathy also modify the length-dependency of Ca sensitivity by acting on the troponin C moiety.
103. Wang WP, Fuchs F: Osmotic compression of skinned cardiac and skeletal muscle bundles. Effects on force generation, Ca sensitivity and Ca binding. J Mol Cell Cardiol 1995, 27:1235-1244.
104. Watkins HC, Seidman CE, Seidman JG, Feng HS, Sweeney HL: Expression and functional assessment of wild type and a hypertrophic cardiomyopathy mutant cardiac troponin T in quail myotubules [abstract]. Circulation 1995, 92:1-233.