Advertisement

Intracellular Ca2+ and Insulin Action: Possible Role in the Pathogenesis of Syndrome X

  • Joseph Levy
  • James R. Sowers
Part of the Endocrinology and Metabolism book series (EAM, volume 6)

Abstract

Overwhelming evidence suggests that binding to the receptor followed by receptor autophosphorylation are the initial steps by which insulin exerts its biologic effects.1-5 However, the subsequent steps in the propagation of the signal are not clear. Indeed, since the biologic effects of insulin are many, it has been suggested that more than one second messenger may be involved in the propagation of the signal.6 Intracellular Ca2+ ([Ca2+]i) may have a significant role in this regard,5 thus explaining why abnormal [Ca2+]i homeostasis may be associated with impaired insulin action7,8 or with insulin resistance.9,10

Keywords

Insulin Resistance ATPase Activity Essential Hypertension Insulin Action Diabetic Cardiomyopathy 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Rosen OM. After insulin binds. Science 1987; 237:1452–1458.PubMedCrossRefGoogle Scholar
  2. 2.
    Ziek Y. The insulin receptor: Structure and function. Crit Rev Biochem Mol Biol 1989; 24:217–269.CrossRefGoogle Scholar
  3. 3.
    Denton RM. Search for the missing links. Nature 1990; 348:286–287.PubMedCrossRefGoogle Scholar
  4. 4.
    Khan RC, White MF, Grigorescu F, Takayama S, Häring HU, Crettaz M. The insulin receptor protein kinase. In: Czech MP, ed. Molecular Basis of Insulin Action. New York: Plenum; 1985:67–93.Google Scholar
  5. 5.
    Gherzi R, Russell DS, Taylor SI, Rosen OM. Reevaluation of the evidence that an antibody to the insulin receptor is insulinminetic without activating the protein tyrosine kinase activity of the receptor. J Biol Chem 1987; 262:16900–16905.PubMedGoogle Scholar
  6. 6.
    McDonald JM, Pershadsingh HA, Colca J. The role of calcium and calmodulin in insulin receptor function in the adipocyte. Ann NY Acad Sei 1986; 488:406–418.CrossRefGoogle Scholar
  7. 7.
    Levy J, Zemel MB, Sowers JR. Role of cellular calcium metabolism in abnormal glucose metabolism and diabetic hypertension. Am J Med 1989; 87(suppl 6A):7S–15S. PubMedCrossRefGoogle Scholar
  8. 8.
    Levy J, Gavin JR III, Hammerman MR, Avioli LV. Ca2+ + Mg2+-ATPase activity in kidney basolateral membrane in non-insulin-dependent diabetic rats: Effect of insulin. Diabetes 1986; 35:899–905.PubMedCrossRefGoogle Scholar
  9. 9.
    Draznin B. Cytosolic calcium: A new factor in insulin resistance? Diab Res Clin Pract 1991; 11:141–146.CrossRefGoogle Scholar
  10. 10.
    Levy J, Grunberger G, Karl I, Gavin JR III. Effects of food restriction and insulin treatment on (Ca2+ + Mg2+)-ATPase response to insulin in kidney basolateral membranes of non-insulin-dependent diabetic rats. Metabolism 1990; 39:25–33.PubMedCrossRefGoogle Scholar
  11. 11.
    Reaven GM. Role of insulin resistance in human disease. Diabetes 1988; 37:1595–1607.PubMedCrossRefGoogle Scholar
  12. 12.
    Zimmet P. Non-insulin-dependent (type 2) diabetes mellitus: Does it really exist? Diab Med 1989; 6:728–735.CrossRefGoogle Scholar
  13. 13.
    Carafoli E. Intracellular calcium homeostasis. Annu Rev Biochem 1987; 56:395–433.CrossRefGoogle Scholar
  14. 14.
    Carafoli E. Calcium-transporting systems of plasma membranes, with special attention to their regulation. In: Greengard P, Robison GA, Paoletti RP, eds. Advances in Cyclic Nucleotide and Protein Phosphorylation Research, Vol. 17. New York: Raven; 1984:534–549.Google Scholar
  15. 15.
    Nicholls DG. Intracellular calcium homeostasis. Br Med Bull 1986; 42:353–358.PubMedGoogle Scholar
  16. 16.
    Fleckenstein A, Frey M, Zorn J, Fleckenstein-Grum G. The role of calcium in the pathogenesis of experimental arteriosclerosis. TIPS 1987; 8:496–501.Google Scholar
  17. 17.
    Avioli LV. Calcium, cell function and cell death. Adv Exp Med Biol 1986; 209:9–15.Google Scholar
  18. 18.
    Lidofsky SD, Xie MH, Scharschmidt BF. Na+-Ca2+ exchange in cultured rat hepatocytes: Evidence against a role in cytosolic Ca2+ regulation or signaling. Am J Physiol 1990; 259:G56–G61.PubMedGoogle Scholar
  19. 19.
    Schmitz G, Hankowitz J, Kovacs EM. Cellular processes in atherogenesis: Potential targets of Ca2+ channel blockers. Atherosclerosis 1991; 88:109–132.PubMedCrossRefGoogle Scholar
  20. 20.
    Zidek W, Vetter H. Cellular calcium metabolism in primary hypertension. Klin Wochenschr 1987; 65:155–160.PubMedCrossRefGoogle Scholar
  21. 21.
    Blaustein MP. Sodium ions, blood pressure regulation and hypertension: A reassessment of a hypothesis. Am J Physiol 1977; 232:065–073.Google Scholar
  22. 22.
    Moore RD. The case of intracellular pH in insulin action. In: Czech MP, ed. Molecular Basis of Insulin Action. New York: Plenum; 1985:145–170.Google Scholar
  23. 23.
    El-Mallakh RS. Hypertension and diabetes in obesity: A review and new ideas on the contributing role of ions. Med Hypotheses 1986; 19:44–45.CrossRefGoogle Scholar
  24. 24.
    Draznin B, Kao M, Sussman KE. Insulin and glyburide increase cytosolic free-Ca2+ concentration in isolated rat adipocytes. Diabetes 1986; 36:174–178.CrossRefGoogle Scholar
  25. 25.
    Standley PR, Zhang F, Ram JL, Zemel MB, Sowers JR. Insulin attenuates vasopressin-induced calcium transients and a voltage-dependent calcium response in rat vascular smooth muscle cells. J Clin Invest 1991; 88:1230–1236.PubMedCrossRefGoogle Scholar
  26. 26.
    Lin SH, Wallace MA, Fain JN. Regulation of Ca2+-Mg2+-ATPase activity in hepatocyte plasma membranes by vasopressin and phenylephrine. Endocrinology 1983; 113:2268–2275.PubMedCrossRefGoogle Scholar
  27. 27.
    Mine T, Kojima I, Ogato E. Calcium rather than cyclic AMP is an intracellular messenger of parathyroid hormone action on glycogen metabolism in isolated rat hepatocytes. Biochem J 1989; 258:889–894.PubMedGoogle Scholar
  28. 28.
    Rasmussen H. The messenger function of Ca2+: From PTH action to smooth muscle contraction. Bone and Mineral 1989; 5:233–248.PubMedCrossRefGoogle Scholar
  29. 29.
    Rosci NK, Stanchaert ML, Pollet RJ. The mechanism of insulin stimulation of (Na+ + K+)-ATPase transport activity in muscle. J Biol Chem 1985; 260:6206–6212.Google Scholar
  30. 30.
    Lynch CJ, Wilson PB, Blackmore PF, Exton JH. The hormone-sensitive hepatic Na+-pump. J Biol Chem 1986; 261:14551–14556.PubMedGoogle Scholar
  31. 31.
    Muallem S, Pandol SJ, Becker TG. Calcium mobilizing hormones activate the plasma membrane Ca2+ pump of pancreatic acinar cells. J Membr Biol 1988; 106:57–69.PubMedCrossRefGoogle Scholar
  32. 32.
    Blackmore PF, Augert G. The effect of hormones on cytosolic free calcium in adipocytes. Cell Calcium 1989; 10:561–567.PubMedCrossRefGoogle Scholar
  33. 33.
    Levy J, Gavin JR III, Morimoto S, Hammerman MR, Avioli LV. Hormonal regulation of (Ca2+ + Mg2+)-ATPase activity in canine renal basolateral membrane. Endocrinology 1986; 119:2405–2410.PubMedCrossRefGoogle Scholar
  34. 34.
    Hernandez H, Spencer BA, Arsenis G. 1986; Stimulation of Na+/H+ exchange by insulin (Ins) and isoproterenol (Iso) in rat adipocytes. Diabetes 1989; 38(suppl 2):182A. Abstract. Google Scholar
  35. 35.
    Gupta MP, Makino N, Khatter K, Dhalla NS. Stimulation of Na+-Ca2+ exchange in heart sarcolemma by insulin. Life Sei 1986;39:1077–1083.CrossRefGoogle Scholar
  36. 36.
    Davis FB, Davis PJ, Blas SD, Schoenl M. Action of long-chain fatty acids in vitro on Ca2+-stimulatable, Mg2+-dependent ATPase activity in human red cell membranes. Biochem J 1987; 248:511–516.PubMedGoogle Scholar
  37. 37.
    Hoeing M, Lee RJ, Ferguson DC. Glucose inhibits the high-affinity (Ca2+ + Mg2+)-ATPase in the plasma membrane of a glucose-responsive insulinoma. Biochim Biophys Acta 1990; 1022:333–338.CrossRefGoogle Scholar
  38. 38.
    Obando MA, Marin R, Proverbio T, Proverbio F. High sodium diet and Na+ stimulated ATPase activities in basolateral plasma membranes from rat kidney proximal tubular cells. Biochem Pharmacol 1987; 36:7–11.PubMedCrossRefGoogle Scholar
  39. 39.
    Smallwood JI, Gugi B, Rasmussen H. Modulation of erythrocyte Ca2+ pump activity by protein kinase C. J Biol Chem 1988; 263:2195–2202.PubMedGoogle Scholar
  40. 40.
    Neyses L, Reinlib L, Carafoli E. Phosphorylation of the Ca2+-pumping ATPase of heart sarcolemma and erythrocyte plasma membrane by the cAMP-dependent protein kinase. J Biol Chem 1985; 260:10283–10287.PubMedGoogle Scholar
  41. 41.
    Carafoli E. The calcium pumping ATPase of the plasma membrane. Annu Rev Physiol 1991; 53:531–547.PubMedCrossRefGoogle Scholar
  42. 42.
    Niggli V, Adunyah ES, Carafoli E. Acidic phospholipids, unsaturated fatty acids, and limited proteolysis mimic the effect of calmodulin on the purified erythrocyte Ca2+-ATPase. J Biol Chem 1981; 256:395–401.PubMedGoogle Scholar
  43. 43.
    Froud RJ, East JM, Jones OT, Lee AG. Effects of lipids and long-chain alkyl derivatives on the activity of (Ca2+ -I- Mg2+)-ATPase. Biochemistry 1986; 25:7544–7552.PubMedCrossRefGoogle Scholar
  44. 44.
    Levy J, Suzuki Y, Avioli LV, Grunberger G, Gavin JR III. Plasma membrane phospholipid content in non-insulin-dependent streptozotocin-diabetic rats-effect of insulin. Diabetologia 1988; 31:315–321.PubMedGoogle Scholar
  45. 45.
    Warren GB, Hously MD, Metcalfe JC, Birdsall NJM. Cholestrol is excluded from the phospholipid annulus surrounding an active calcium transport protein. Nature 1975; 255:684–687.PubMedCrossRefGoogle Scholar
  46. 46.
    Bennett JP, Smith GA, Hously MD, Hesketh TR, Metcalfe JC, Warren GB. The phospholipid headgroup specificity of an ATP-dependent calcium pump. Biochim Biophys Acta 1978; 513:310–320.PubMedCrossRefGoogle Scholar
  47. 47.
    Ortego A, Mas-Oliva J. Direct regulatory effect of cholestrol on the calmodulin stimulated calcium pump of cardiac sarcolemma. Biochem Biophys Res Commun 1986; 139:868–874.CrossRefGoogle Scholar
  48. 48.
    Pershadsingh HA, McDonald JM. Hormone receptor coupling and the molecular mechanism of insulin action in the adipocyte: A paradign for Ca2+ homeostasis in the initiation of the insulin induced metabolic cascade. Cell Calcium 1984; 5:111–130.PubMedCrossRefGoogle Scholar
  49. 49.
    Klip A, Li G, Logan WJ. Role of calcium ions in insulin action on hexose transport in L6 muscle cells. Am J Physiol 1984; 24:E297–E304.Google Scholar
  50. 50.
    Vydelingum N, Kissebah AH, Wynn V. The role of calcium in insulin action. V. Importance of cyclic guanosine 3′5′ monophosphate and calcium ions in insulin stimulation of lipoprotein lipase activity and portein synthesis in adipose tissue. Horm Metab Res 1978; 10:38–46. PubMedCrossRefGoogle Scholar
  51. 51.
    Hope-Gill HR. The effect of calcium on purified human adipose tissue “I” form glycogen synthase: A possible mechanism of hormonal regulation. Horm Metab Res 1976; 8:321–322.PubMedCrossRefGoogle Scholar
  52. 52.
    Van de Werve G. Ca2+, a newly discovered regulatory of liver microsomal glucose 6-phosphatase activity. Diabetes 1989; 38(suppl 2):42A. Abstract. Google Scholar
  53. 53.
    Ochs R. Does calcium regulate pyruvate kinase? TIBS 1988; 13:2–3.Google Scholar
  54. 54.
    Lawrence JC Jr, Larner J. Effect of insulin, methoxamine, and calcium on glycogen synthase in rat adipocytes. Mol Pharmacol 1978; 14:1079–1091.PubMedGoogle Scholar
  55. 55.
    Bonne D, Belhadu O, Cohen P. Modulation by calcium on the insulin action and of the insulin-like effect of ocytocin on isolated rat adipocytes. Eur J Biochem 1977; 75:101–105.PubMedCrossRefGoogle Scholar
  56. 56.
    Clausen T, Elbrink J, Martin BR. Insulin controlling calcium distribution in muscle and fat cell. Acta Endocrinol (Copenhagen) 1974; 77(suppl 191):137–143.Google Scholar
  57. 57.
    Saggerson ED, Sooranna SR, Evans CJ. Insulin-like actions of nickel and other transtion-metal ions in rat fat-cells. Biochem J 1976; 154:349–357.PubMedGoogle Scholar
  58. 58.
    Kissebah AH, Tulloch BR, Vydelingum N, Hope-Gill H, Clarke P, Fraser TR. The role of calcium in insulin action. II. Effects of insulin and procaine hydrochloride on lipolysis. Horm Metab Res 1974; 6:357–364. PubMedCrossRefGoogle Scholar
  59. 59.
    Pierce GN, Kutryk MJB, Dhalla NS. Alterations in Ca2+ binding by and composition of the cardiac sarcolemmal membrane in chronic diabetes. Pro Natl Acad Sei USA 1983; 80:5412–5416.CrossRefGoogle Scholar
  60. 60.
    Clausen T. The role of calcium in the activation of the glucose transport system. Cell Calcium 1980; 1:311–325.CrossRefGoogle Scholar
  61. 61.
    Pershadsingh HA, McDonald JM. Direct addition of insulin inhibits a high affinity Ca2+-ATPase in isolated adipocyte plasma membranes. Nature 1979; 281:495–497.PubMedCrossRefGoogle Scholar
  62. 62.
    Wong ECC, Sacks DB, Laurino JP, McDonnald JM. Characteristics of calmodulin phosphorylation by the insulin receptor kinase. Endocronology 1988; 123:1830–1836.CrossRefGoogle Scholar
  63. 63.
    Sandra A, Fyler DJ. Effects of liposome-adipocyte interaction on calcium binding and insulin action. Endoc Res Commun 1982; 9:107–120.CrossRefGoogle Scholar
  64. 64.
    Pershadsigh HA, Shade DL, Delfert DM, Macdonald JM. Chelation of intracellular calcium blocks insulin action in the adipocyte. Proc Natl Acad Sei USA 1987; 84:1025–1029.CrossRefGoogle Scholar
  65. 65.
    Levy J, Gavin JR III, Morimoto S, Hammerman MR, Avioli LV. Hormonal regulation of (Ca2+ + Mg2+)-ATPase activity in canine renal basolateral membrane. Endocrinology 1986; 119:2405–2410.PubMedCrossRefGoogle Scholar
  66. 66.
    Gavin JR III, Lowry M, Levy J. (Ca2+ + Mg2+)-ATPase activity is stimulated by insulin in canine and rat fat membranes. Diabetes 1987; 36(suppl 1):50A. Abstract. Google Scholar
  67. 67.
    Gupta MP, Makino N, Khatter K, Dahalla NS. Stimulation of Na+-Ca2+ exchange in heart sarcolemma by insulin. Life Sei 1986; 39:1077–1083.CrossRefGoogle Scholar
  68. 68.
    Hope-Gill HF, Nanada V. Stimulation of calcium ATPase by insulin, glucagon, cyclic AMP and cyclic GMP in triton-X 100 extracts of purified rat liver plasma membrane. Horm Metab Res 1979; 11:698–700.PubMedCrossRefGoogle Scholar
  69. 69.
    Zierler K. Insulin’s block of slow Ca2+ conduction requires hydrolyzable GTP. Clin Res 1989; 37.610A. Abstract. Google Scholar
  70. 70.
    Hernandez H, Spencer BA, Arsenis G. Stimulation Na+/H+ exchange by insulin (Ins) and isoproterenol (Iso) in rat adipocytes. Diabetes 1989; 38(suppl 2):182A. Abstract. Google Scholar
  71. 71.
    Levy J, Suzuki Y, Avioli LV, Grunberger G, Gavin JR III. Plasma membrane phospholipid content in non-insulin-dependent streptozotocin-diabetic rats-effect of insulin. Diabetologia 1988; 31:315–321.PubMedGoogle Scholar
  72. 72.
    Levy J, Rempinski D. Insulin phosphorylates the membrane (Ca2+ + Mg2+)-ATPase in kidney basolateral membranes. Clin Res 1991; 39(3):698A. Abstract. Google Scholar
  73. 73.
    Levy J, Rempinski D. Inhibition of insulin bioeffects in adipocytes by monoclonal antibodies to the membrane (Ca2+ -I- Mg2+)-adenosine triphosphatase. Endocrinology Proceeding 74th Annual Meeting. San Antonio, TX: Endocrinology Society 1992; 22. Abstract.Google Scholar
  74. 74.
    Levy J, Avioli LV, Roberts ML, Gavin JR III. (Na+ + K+)-ATPase activity in kidney basolateral membranes of noninsulin dependent diabetic rats. Biochem Biophys Res Commun 1986; 139:1313–1319.PubMedCrossRefGoogle Scholar
  75. 75.
    Rosic NK, Standaert ML, Pollst RJ. The mechanism of insulin stimulation of (Na+ + K+)-ATPase transport activity in muscle. J Biol Chem 1985; 260:6206–6212.PubMedGoogle Scholar
  76. 76.
    DeLuise MA, Harker M. Insulin stimulation of Na+ + K+ pump in clonal rat osteosarcoma cells. Diabetes 1988; 37:33–37.CrossRefGoogle Scholar
  77. 77.
    Draznin B, Sussman K, Kao M, Lewis D, Sherman N. The existence of an optimal range of cytosolic free calcium for insulin-stimulated glucose transport in rat adipocytes. J Biol Chem 1987; 262:14385–14388.PubMedGoogle Scholar
  78. 78.
    Levy J, Rempinski D. A hormone specific defect in insulin regulation of the membrane (Ca2+ + Mg2+)-ATPase in obesity. Clin Res 1989; 37:455. Abstract. Google Scholar
  79. 79.
    Draznin B, Sussman KE, Ekel RH, Kao M, Yost T, Shermann NA. Possible role of cytosolic free calcium concentrations in mediating insulin resistance of obesity and hyperinsulinemia. J Clin Invest 1988; 28:1848–1852.CrossRefGoogle Scholar
  80. 80.
    Levy J, Grunberger G, Karl I, Gavin JR III. Effects of food restriction and insulin treatment on (Ca2+ -I- Mg2+)-ATPase response to insulin in kidney basolateral membranes of noninsulin-dependent-diabetic rats. Metabolism 1990; 39:25–33.PubMedCrossRefGoogle Scholar
  81. 81.
    Karl IE, Gavin JR III, Levy J. Effect of insulin on glucose utilization in epitrochleasis muscle of rats with streptozotocin-induced NIDDM. Diabetes 1990; 39:1106–1115.PubMedCrossRefGoogle Scholar
  82. 82.
    Carnie JA, Smith DG, Marvis-Vavayannis M. Effects of insulin on lipolysis and lipogenesis in adipocytes from genetically obese (ob/ob) mice. Biochem J 1979; 184:107–112.PubMedGoogle Scholar
  83. 83.
    Draznin B. Intracellular calcium, insulin secretion and action. Am J Med 1988; 85(suppl 5A):44–58. PubMedCrossRefGoogle Scholar
  84. 84.
    Begum N, Sussman KE, Draznin B. High level of cytosolic free calcium inhibit dephosphorylation of insulin receptor and glycogen synthase. Cell Calcium 1991; 12:423–430.PubMedCrossRefGoogle Scholar
  85. 85.
    Allo SN, Lincoln TM, Wilson GL, Green FJ, Watanabe AM, Schaffer SW. Non-insulin-dependent diabetes-induced defects in cardiac cellular calcium regulation. Am J Physiol 1991; 260:C1165–C1171.PubMedGoogle Scholar
  86. 86.
    Heijnis JB, Mathy MJ, Van Zwieten PA. Effects of various calcium antagonists in isolated perfused hearts from diabetic and age-matched control rats. J Cardiovasc Pharmacol 1991; 17:983–989.PubMedCrossRefGoogle Scholar
  87. 87.
    Borda E, Pascual J, Wald M, Sterin-Borda L. Hypersensitivity to calcium associated with an increased sarcolemmal Ca2+-ATPase activity in diabetic rat heart. Can J Cardiol 1988; 4:97–101.PubMedGoogle Scholar
  88. 88.
    Ganguly PK, Pierce GN, Dhalla KS, Dhalla SN. Defective sarcoplasmic reticular calcium transport in diabetic cardiomyopathy. Am J Physiol 1983; 244:E528–E535.PubMedGoogle Scholar
  89. 89.
    Makino N, Dhalla KS, Elimban V, Dhalla NS. Sarcolemmal Ca2+ transport in streptozotocin-induced diabetic cardiomyopathy in rats. Am J Physiol 1987; 253:E202–E207.PubMedGoogle Scholar
  90. 90.
    Russ M, Reinaver H, Eckel J. Diabetes-induced decrease in the mRNA coding for sarcoplasmic reticulum Ca2+-ATPase in adult rat cardiomyocytes. Biochem Biophys Res Comm 1991; 178:905–912.CrossRefGoogle Scholar
  91. 91.
    Black SC, Katz S, NcNeill H. Cardiac performance and plasma lipids of omega-3 fatty acid-treated streptozocin-induced diabetic rats. Diabetes 1989; 38:969–974.PubMedCrossRefGoogle Scholar
  92. 92.
    Nobe S, Aomine M, Artia M, Ito S, Takaki R. Chronic diabetes mellitus prolongs potential duration of rat ventricular muscles: Circumstantial evidence for impaired Ca2+ channel. Cardiovasc Res 1990; 24:381–389.PubMedCrossRefGoogle Scholar
  93. 93.
    Pierce GN, Dhalla NS. Cardiac myofibrillar ATPase activity in diabetic rats. J Mol Cell Cardiol 1981; 13:1063–1069.PubMedCrossRefGoogle Scholar
  94. 94.
    Afzal N, Ganguly PK, Dhalla KS, Pierce GN, Singal PK, Dhalla NS. Beneficial effects of verapamil in diabetic cardiomyopathy. Diabetes 1988; 37:936–942.PubMedCrossRefGoogle Scholar
  95. 95.
    Nagase N, Tamura Y, Kobayashi S, Saito K, Saito M, Niki T, Chikamori K, Mori H. Myocardial disorders of hereditarily diabetic KK mice. J Mol Cell Cardiol 1981; 13(suppl 2):70. Abstract. CrossRefGoogle Scholar
  96. 96.
    Dhalla NS, Pierce GN, Innes IR, Beamish RE. Pathogenesis of cardiac dysfunction in diabetes mellitus. Can J Cardiol 1985; 1:263–281.PubMedGoogle Scholar
  97. 97.
    Ohara T, Sussman KE, Draznin B. Effect of diabetes on cytosolic free Ca2+ and Na+-K+-ATPase in rat aorta. Diabetes 1991; 40:1560–1563.PubMedCrossRefGoogle Scholar
  98. 98.
    Agrawal KD, McNeill JH. Vascular responses to agonists in rat mesenteric artery from diabetic rats. Can J Physiol Pharmacol 1987; 65:1484–1490.PubMedCrossRefGoogle Scholar
  99. 99.
    Piper GM, Gross GJ. Diabetes enhances vasoreactivity to calcium entry blockers. Artery 1989; 16:263–271.Google Scholar
  100. 100.
    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; 36:795–807.PubMedGoogle Scholar
  101. 101.
    Kobayashi S, Fujihara M, Hoshino N, Kimura I, Kimura M. Diabetic state-induced activation of calcium-activated neutral proteinase in mouse skeletal muscle. Endocrinol Jpn 1989; 36:833–844.PubMedGoogle Scholar
  102. 102.
    Taira Y, Hata T, Ganguly PK, Elimban V, Dhalla S. Increased sarcolemmal Ca2+ transport activity in skeletal muscle of diabetic rats. Am J Physiol 1991; 260:E626–E632.PubMedGoogle Scholar
  103. 103.
    Ganguly PK, Mathur S, Gupta MP, Beamish RE, Dhalla NS. Calcium pump activity of sarcoplasmic reticulum in diabetic rat skeletal muscle. Am J Physiol 1986; 251:E515–E523. PubMedGoogle Scholar
  104. 104.
    Nishida K, Ohara T, Johnson J, Wallner JS, Wilk J, Sherman N, Kawakami K, Sussman KE, Draznin B. Na+/K+-ATPase activity and its all subunit gene expression in rat skeletal muscle: Influence of diabetes, fasting and refeeding. Metabolism 1992; 41:56–63.PubMedCrossRefGoogle Scholar
  105. 105.
    Sahai A, Ganguly PK. Lack of response of (Ca2+ + Mg24>ATPase to atrial natriuretic peptide in basolateral membranes from kidney cortex of chronic diabetic rats. Biochem Biophys Res Commun 1990; 169:537–544.PubMedCrossRefGoogle Scholar
  106. 106.
    Studer RK, Ganas L. Effect of diabetes on hormone-stimulated and basal hepatocyte calcium metabolism. Endocrinology 1989; 125:2421–2433.PubMedCrossRefGoogle Scholar
  107. 107.
    Chan KM, Junger KD. The effect of streptozocin-induced diabetes on the plasma membrane calcium uptake activity of rat liver. Diabetes 1984; 33:1072–1077.PubMedCrossRefGoogle Scholar
  108. 108.
    Zemel MB, Sowers JR, Shehin S, Walsh MF, Levy J. Impaired calcium metabolism associated with hypertension in Zucker obese rats. Metabolism 1990; 39:704–708.PubMedCrossRefGoogle Scholar
  109. 109.
    Levy J, Sowers JR, Zemel MB. Abnormal Ca2+-ATPase activity in erythrocytes of non-insulin-dependent diabetic rats. Horm Metab Res 1990; 22:136–140.PubMedCrossRefGoogle Scholar
  110. 110.
    Pierce GN, Afzal N, Kroeger EA, Lockwood MK, Kutryk JB, Eckhert CD, Dhalla NS. Cataract formation is prevented by administration of verapamil to diabetic rats. Endocrinology 1989; 125:730–735.PubMedCrossRefGoogle Scholar
  111. 111.
    Cowan T, Levy J, Dunbar J. Role of cell calcium metabolism in cataract formation of diabetic rats. Clin Res 1992; 40:239A. Abstract. Google Scholar
  112. 112.
    Levy J, Reid I, Halstad L, Gavin JR III, Avioli LV. Abnormal cell calcium concentration in cultured bone cells obtained from femurs of obese and noninsulin-dependent diabetic rats. Calcif Tissue Int 1989; 44:131–137.PubMedCrossRefGoogle Scholar
  113. 113.
    Maser RE, Wolfson SK, Ellis D, Stein EA, Drash AL, Becker DJ, Dorman JS, Orchard TJ. Cardiovascular disease and arterial calcification in insulin-dependent diabetes mellitus: Interrelations and risk factor profiles. Pittsburgh Epidemiology of Diabetes Complications Study—V. Arterioscler Thromb 1991; 11:958–965. PubMedCrossRefGoogle Scholar
  114. 114.
    Fleckenstein A, Frey M, Fleckenstein-Grum G. Antihypertensive and arterial anticalcinotic effects of calcium antagonists. Am J Cardiol 1986; 57:1D–10D.PubMedCrossRefGoogle Scholar
  115. 115.
    Katz MA, McNeill G. Defective vasodilation response to exercise in cutaneous precapillary vessels in diabetic humans. Diabetes 1987; 36:1386–1396.PubMedCrossRefGoogle Scholar
  116. 116.
    Baldini P, Incerpi S, Lambert-Gardini S, Spinedi A, Luly P. Membrane lipid alterations and Na+-pumping activity in erythrocytes from IDDM and NIDDM subjects. Diabetes 1989; 38:825–831.PubMedCrossRefGoogle Scholar
  117. 117.
    Schaefer W, Priben J, Mannhold R, Gries AF. (Ca2+ + Mg2+)-ATPase activity of human red blood cells in healthy and diabetic volunteers. Klin Wochenschr 1987; 65:17–21.PubMedCrossRefGoogle Scholar
  118. 118.
    Zemel MB, Bedford BA, Zemel PC, Marwan O, Sowers JR. Altered cation transport in non-insulin dependent diabetic hypertension: Effect of dietary calcium. J Hypertension 1988; 6(suppl 4):S228–S230.Google Scholar
  119. 119.
    Rahmini-Jourdheuil, Mourayre Y, Vague P, Boyer J, Juhan-Vague I. In vivo insulin effect on ATPase activities in erythrocyte membrane from insulin-dependent diabetics. Diabetes 1987; 36:991–995. CrossRefGoogle Scholar
  120. 120.
    Ishi H, Umeda F, Hashimoto T, Hawata H. Changes in phosphoinositide turnover, Ca2+ mobilization, and protein phosphorylation in platelets from NIDDM patients. Diabetes 1990; 39:1561–1568.CrossRefGoogle Scholar
  121. 121.
    Mazzanti L, Rabini RA, Faloia E, Fumelli P, Bertoli E, De-Pirro R. Altered cellular Ca2+ and Na+ transport in diabetes mellitus. Diabetes 1990; 39:850–854.PubMedCrossRefGoogle Scholar
  122. 122.
    Ishii H, Umeda F, Hashimoto T, Nawata H. Increased intracellular calcium mobilization in platelets from patients with type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia 1991; 34:332–336.PubMedCrossRefGoogle Scholar
  123. 123.
    Tschöpe D, Rosen P, Gries FA. Increase in cytosolic concentration of calcium in platelets of diabetes type II. Thromb Res 1991; 62:421–428.PubMedCrossRefGoogle Scholar
  124. 124.
    Segal S, Lloyd S, Sherman N, Sussman KE, Draznin B. Postprandial changes in cytosolic free calcium and glucose uptake in adipocytes in obesity and non-insulin dependent diabetes mellitus. Horm Res 1990; 34:39–44.PubMedCrossRefGoogle Scholar
  125. 125.
    Levy J, Stern Z, Gutman A, Naparstek Y, Gavin JR III, Avioli LV. Plasma calcium and phosphate levels in an adult noninsulin-dependent diabetic population. Calcif Tissue Int 1986; 39:316–318.PubMedCrossRefGoogle Scholar
  126. 126.
    Sorva A, Tilvis RS. Low serum ionized to total calcium ratio: Association with geriatric diabetes mellitus and with other cardiovascular risk factors? Gerontology 1990; 36:212–216.PubMedCrossRefGoogle Scholar
  127. 127.
    Pedrazzoni M, Ciotti G, Pioli G, Girasole G, Davioli L, Palummeri E, Passeri M. Osteocalcin levels in diabetic subjects. Calcif Tissue Int 1989; 45:331–336.PubMedCrossRefGoogle Scholar
  128. 128.
    Levy J, Teitelbaum SL, Gavin JR III, Fausto A, Kurose H, Avioli LV. Bone calcification and calcium homeostasis in rats with non-insulin-dependent diabetes induced by streptozotocin. Diabetes 1985; 34:365–372.PubMedCrossRefGoogle Scholar
  129. 129.
    Khandelwal RL, Zinman SM, Zebrowski EJ. The effect of streptozotocin-induced diabetes and insulin supplementation on glycogen metabolism in rat liver. Biochem J 1977; 168:541–548.PubMedGoogle Scholar
  130. 130.
    Lee SL, Dhalla NS. Ca2+-channels and adrenoceptors in diabetic skeletal muscle. Biochem Biophys Res Commun 1992; 184:353–358.PubMedCrossRefGoogle Scholar
  131. 131.
    Kalofoutis A, Lekakis J. Changes of platelet phospholipids in diabetes mellitus. Diabetologia 1981; 21:540–543.PubMedGoogle Scholar
  132. 132.
    Flecha FLG, Bermudez MC, Cedola NV, Gagliardino JJ, Rossi JPFC. Decreased Ca2+-ATPase activity after glycosylation of erythrocyte membranes in vivo and in vitro. Diabetes 1990; 39:707–711.CrossRefGoogle Scholar
  133. 133.
    Greene DA, Lattimer SA. Impaired rat sciatic nerve sodium-potassium adenosine triphosphatase in acute streptozotocin diabetes and its correction by dietary myo-inositol supplementation. J Clin Invest 1983; 72:1058–1063.PubMedCrossRefGoogle Scholar
  134. 134.
    Resnick LM, Gupta RK, Bhargava KK, Gruenspan H, Alderman MH, Laragh JH. Cellular ions in hypertension, diabetes and obesity: A nuclear magnetic resonance spectroscopic study. Hypertension 1991; 17:951–957.PubMedGoogle Scholar
  135. 135.
    Fuijii S, Takemura T, Wada M, Akia T, Okuda K. Magnesium levels in plasma, erythrocyte and urine in patients with diabetes mellitus. Horm Metab Res 1982; 14:161–62.CrossRefGoogle Scholar
  136. 136.
    Grafton G, Bunce CM, Sheppard MC, Brown G, Baxter MA. Effect of Mg2+ on Na+-dependent inositol transport. Role for Mg2“1” in etiology of diabetic complications. Diabetes 1992; 41:35–39. PubMedCrossRefGoogle Scholar
  137. 137.
    Levy J, Avioli LV, Roberts ML, Gavin JR III. (Na+ + K+)-ATPase activity in kidney basolateral membranes of non insulin dependent diabetic rats. Biochem Biophys Res Commun 1986; 139:1313–1319.PubMedCrossRefGoogle Scholar
  138. 138.
    Strazzullo P, Nunziata V, Cirillo M, Biannattasio R, Ferrara LA, Mattioli PL, Mancini M. Abnormalities of Calcium metabolism in essential hypertension. Clin Sei 1983; 65:137–141.Google Scholar
  139. 139.
    Resnick LM, Laragh JH, Sealey JE, Alderman MH. Divalent cations in essential hypertension. Relations between serum Ionized calcium, magnesium and plasma renin activity. N Engl J Med 1983; 309:888–891. PubMedCrossRefGoogle Scholar
  140. 140.
    Orlov SN, Postnov YV. Ca2+ binding and membrane fluidity in essential and renal hypertension. Clin Sei 1982; 63:281–284.Google Scholar
  141. 141.
    Vincenzi FF, Morris CD, Kinnel LB, Kenny M, McCarron DA. Decreased calcium pump adenosine triphosphatase in red cells of hypertensive subjects. Hypertension 1986; 8:1058–1066.PubMedGoogle Scholar
  142. 142.
    Erne P, Bolli P, Burgisser E, Buhler FR. Correlation of platelet calcium with blood pressure. Effect of antihypertensive therapy. N Engl J Med 1984; 310:1084–1088.Google Scholar
  143. 143.
    Wheling M, Theisen K. Altered calcium metabolism in red blood cells of hypertnesives: Persistent marker or sequel of essential hypertension? Klin Wochenschr 1987; 65:769–772.CrossRefGoogle Scholar
  144. 144.
    Dominiczak AF, Bohr DF. Cell membrane abnormalities and the regulation of intracellular calcium concentration in hypertension. Clin Sei 1990; 79:415–423.Google Scholar
  145. 145.
    Resnik TJ, Tkachuk VA, Erne P, Buhler FR. Platelet membrane calmodulin-stimulated calcium-adenosine triphosphatase. Altered activity in essential hypertension. Hypertension 1986; 8:159–166.Google Scholar
  146. 146.
    Zemel MB, Kraniak J, Standley PR, Sowers JR. Erythrocyte cation metabolism in salt-sensitive blacks as affected by dietary sodium and calcium. Am J Hypertens 1988; 1:386–392.PubMedGoogle Scholar
  147. 147.
    Sugiyama T, Yoshizumi M, Takaku F, Urabe H, Tsukakoschi M, Kasuya T, Yazaki Y. The elevation of the cytoplasmic calcium ions in vascular smooth muscle cells in SHR. Measurement of the free calcium ions in single living cells by laser micro fluorospectroscopy. Biochem Biophys Res Commun 1986; 141:340–345.Google Scholar
  148. 148.
    Bruschi G, Bruschi ME, Caroppo M, Orlandini G, Pavarani C, Cavatorta A. Intracellular free [Ca2+]j in circulating lymphocytes of spontaneously hypertensive rats. Life Sei 1984; 35:535–542.CrossRefGoogle Scholar
  149. 149.
    Epstein M, Sowers JR. Diabetes mellitus and hypertension. Hypertension 1992; 19:403–418.PubMedGoogle Scholar
  150. 150.
    Gilbert D’Angelo EK, Singer HA, Rembold CM. Magnesium relaxes arterial smooth muscle by decreasing intracellular Ca2+ without changing intracellular Mg2+. J Clin Invest 1992; 89:1988–1994. CrossRefGoogle Scholar
  151. 151.
    Postnov YV, Orlov SN, Reznikova MB, Rjazhsky GG, Podukin NI. Calmodulin distribution and Ca2+ transport in the erythrocytes of patients with essential hypertension. Clin Sei 1984; 66:459–463.Google Scholar
  152. 152.
    Robinson BF. Altered calcium handling as a couse of primary hypertension. J Hypertension 1984; 2:453–460.CrossRefGoogle Scholar
  153. 153.
    De Luise M, Blackburn GL, Flier JS. Reduced activity of the red-cell sodium-potassium pump in human obesity. N Engl J Med 1980; 303:1017–1022.PubMedCrossRefGoogle Scholar
  154. 154.
    Beutler E, Kühl W, Sacks P. Sodium-potassium-ATPase activity is influenced by ethnic origin and not by obesity. N Engl J Med 1983; 309:756–760.PubMedCrossRefGoogle Scholar
  155. 155.
    Pasquali R, Strocchi E, Malini P, Casimirri F. Heterogeneity of the erythrocyte N-K pump status in human obesity. Metabolism 1985; 34:802–807.PubMedCrossRefGoogle Scholar
  156. 156.
    Erne P, Hermsmeyer K. Intracellular vascular muscle Ca2+ modulation in genetic hypertension. Hypertension 1989; 14:145–151.PubMedGoogle Scholar
  157. 157.
    Laasko M, Edelman SV, Brechtel G, Baron AD. Decreased effect of insulin to stimulate skeletal muscle blood flow in obese man: A novel mechanism for insulin resistance. J Clin Invest 1990; 85:1844–1852.CrossRefGoogle Scholar
  158. 158.
    Baron AS, Laakso M, Brechtel G, Edelman SV. Mechanism of insulin resistance in insulin-dependent diabetes mellitus: A major role for reduced skeletal muscle blood flow. J Clin Endocrinol Metab 1991; 73:637–643.PubMedCrossRefGoogle Scholar
  159. 159.
    Baron AD, Laakso M, Brechtel G, Holt B, Watt C, Edelman SV. Reduced postprandial skeletal muscle blood flow contributes to glucose intolerance in human obesity. J Clin Endocrinol Metab 1990; 70:1525–1533.PubMedCrossRefGoogle Scholar
  160. 160.
    Lillioja S, Young AA, Culter CL. Skeletal muscle capillary density and fiber type are possible determinants of in vivo imsulin resistance in man. J Clin Invest 1987; 80:415–424.PubMedCrossRefGoogle Scholar
  161. 161.
    Hellman B, Berne C, Grapengiesser E, Grill V, Gylfe E, Lund PE. The cytoplasmic Ca2+ response to glucose as an indicator of impairment of the pancreatic beta-cell function. Eur J Clin Invest 1990; (suppl 1):S10–S17.Google Scholar
  162. 162.
    Stickberger AS, Russek LN, Phair RD. Evidence for increased aortic plasma membrane calcium transport caused by experimental atherosclerosis in rabbits. Circ Res 1988; 62:75–80.Google Scholar
  163. 163.
    Ross R, Glomset JA. The pathogenesis of atherosclerosis. N Engl J Med 1976; 295:420–425.PubMedCrossRefGoogle Scholar
  164. 164.
    Orimo H, Ouchi Y. The role of calcium and magnesium in the development of atherosclerosis. Experimental and clinical evidence. Ann NY Acad Sei 1990; 598:444–457.Google Scholar
  165. 165.
    Blumenthal HT, Lansing AI, Wheeler PA. Calcification of the media of the human aorta and its relation to intimal atherosclerosis, aging, and disease. Am J Pathol 1944; 20:695–679.Google Scholar
  166. 166.
    Toda T, Leszczynski DE, Kummerow FA. The role of 25-hydroxy-vitamin D3 in the induction of atherosclerosis in swine and rabbit by hypervitaminosis D. Acta Pathol Jpn 1983; 33:37–44.PubMedGoogle Scholar
  167. 167.
    Levy J. Insulin resistance in neonatal NIDDM: Role of abnormal cell Ca2+ homeostasis. In: Shafrir E, ed. Frontiers in Diabetes Research: Lessons from Animal Diabetes III. London: Smith-Gordon Press; 1991:567–573.Google Scholar

Copyright information

© Springer-Verlag New York, Inc. 1994

Authors and Affiliations

  • Joseph Levy
  • James R. Sowers

There are no affiliations available

Personalised recommendations