Endocrine

, Volume 10, Issue 1, pp 1–6 | Cite as

Abnormal cell calcium homeostasis in type 2 diabetes mellitus

A new look on old disease
Review

Abstract

Cumulative evidence reveals that diabetes is a condition in which cell Ca2+ homeostasis is impaired. Defects in cell Ca2+ regulation were found in erythrocytes, cardiac muscle, platelets, skeletal muscle, kidney, aorta, adipocytes, liver, osteoblasts, arteries, lens, peripheral nerves, brain synaptosomes, retinal tissue, and pancreatic β cells, confirming that this defect in cell Ca2+ metabolism is a basic pathology associated with the diabetic state. Though different defects in a variety of functions that regulate cell Ca2+ homeostasis were described in diabetes, the most common finding is an increase in [Ca2+]i levels. However, it is not clear whether the defect in cell Ca2+ metabolism in diabetes precedes or succeeds the overt diabetic condition. It is also not clear which of the multiple functions involved in cell Ca2+ regulation has the primary defect.

Defects in cell Ca2+ metabolism may be significant for the observed pathologies in insulin secretion and insulin action in diabetes. They may also play an important role in the vascular complications seen in this condition, such as hypertension, atherosclerosis, and microangiopathy. Therefore, better understanding of the impairment in cell Ca2+ metabolism in diabetes may markedly enhance our understanding of this condition.

Key Words

Type 2 diabetes cellular calcium insulin secretion insulin action complications 

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References

  1. 1.
    Weir, G. C. (1982). Am. J. Med. 73, 461–464.PubMedCrossRefGoogle Scholar
  2. 2.
    Levy, J., Gavin, J. R., III, and Sowers, J. R. (1994). Am. J. Med. 96, 260–273.PubMedCrossRefGoogle Scholar
  3. 3.
    Levy, J., Zemel, M. B., and Sowers, J. R. (1989). Am. J. Med. 87(6A Suppl.), 7–15.CrossRefGoogle Scholar
  4. 4.
    Levy, J., and Sowers, J. R. (1994). In: Piero, P. F. and Walsh, M. F. (eds.), Endocrinology and Metabolism, vol. 6, Springer-Verlag: New York, NY, pp. 116–136.Google Scholar
  5. 5.
    Draznin, B. (1988). Am. J. Med. 85 (Suppl. 5A), 44–58.PubMedCrossRefGoogle Scholar
  6. 6.
    Okamoto, Y., Ishida, H., Taminato, T., Tsugi, K., Kurose, T., Tsuura, Y., et al. (1992). Diabetes 41, 1555–1561.PubMedCrossRefGoogle Scholar
  7. 7.
    Rasmussen, H. (1989). Bone Miner. 5, 233–248.PubMedCrossRefGoogle Scholar
  8. 8.
    Galione, A. (1993). Science 229, 325–326.CrossRefGoogle Scholar
  9. 9.
    Rasmussen, H. (1986). N. Engl. J. Med. 314, 1094–1011, 1164–1170.PubMedGoogle Scholar
  10. 10.
    Petersen, O. H., Petersen, C. C. H., and Kasai, H. (1994) Annu. Rev. Physiol. 56, 297–319.PubMedCrossRefGoogle Scholar
  11. 11.
    Berridge, M. J. (1993). Nature 361, 315–325.PubMedCrossRefGoogle Scholar
  12. 12.
    Clapham, D. E. (1993). Nature 364, 763, 764.PubMedCrossRefGoogle Scholar
  13. 13.
    Logan, A. (1993). Lancet 341, 1248.PubMedCrossRefGoogle Scholar
  14. 14.
    Takasawa, S., Naja, K., Annexure, H., and Oxamide, H. (1993). Science 259, 370–373.PubMedCrossRefGoogle Scholar
  15. 15.
    Aviv, A. (1996). Curr. Opinion Cardiol. 11, 477–482.CrossRefGoogle Scholar
  16. 16.
    Allbritton, N. L., Meyer, T., and Stryer, L. (1992). Science 258, 1812–1815.PubMedCrossRefGoogle Scholar
  17. 17.
    Roe, M. W., Philipson, L. H., Frangakis, C. J., Kuznestov, A., Mertz, R. J., Lancaster, M. E., et al. (1994). J. Biol. Chem. 269, 18,279–18,282.Google Scholar
  18. 18.
    Janicki, P. K., Horn, J. L., Singh, G., Franks, W. T., and Franks, J. J. (1994). Life Sci. 55, 359–364.CrossRefGoogle Scholar
  19. 19.
    Tomizawa, H., Yamazaki, M., Kunika, K., Itakura, M., and Yamashita, K. (1993). Diab. Res. Clin. Pract. 19, 1–8.CrossRefGoogle Scholar
  20. 20.
    Kern, T. S., Kowluru, R. A., and Engerman, R. L. (1994). Invest. Ophthalmol. Vis. Sci. 35, 2962–2967.PubMedGoogle Scholar
  21. 21.
    Levy, J., Zhu, Z., and Dunbar, J. (1998). Metabolism 47, 185–189.PubMedCrossRefGoogle Scholar
  22. 22.
    Yu, Z., Quamme, G. A., and McNeill, J. H. (1994). Am. J. Physiol. 266, H2334-H2342.PubMedGoogle Scholar
  23. 23.
    Yu, J. Z., Rodrigues, B., and McNeil, J. H. (1994). Cardiovasc. Res. 34, 91–98.CrossRefGoogle Scholar
  24. 24.
    Schaffer, S. W. and Mozaffari, M. (1996) Coronary Artery Dis. 7, 109–115.CrossRefGoogle Scholar
  25. 25.
    Hayashi, H. and Noda, N. (1997). Cardiovasc. Res. 34, 99–103.PubMedCrossRefGoogle Scholar
  26. 26.
    Levy, J., Rempinski, D., and Kuo, T. H. (1994). Metabolism 43, 604–613.PubMedCrossRefGoogle Scholar
  27. 27.
    Levy, J. and Rempinski, D. (1994). Metabolism 43, 1055–1061.PubMedCrossRefGoogle Scholar
  28. 28.
    Levy, J. and Gavin, J. R., II (1995). Int. J. Obesity 19, 97–102.Google Scholar
  29. 29.
    Gonzalez Flecha, F. L., Bermudez, M. C., Cedola, N. V., Gag Liardio, J. J., and Rossi, J. P. F. C. (1990). Diabetes 39, 704–711.CrossRefGoogle Scholar
  30. 30.
    Williams, R. and Schrier, R. W. (1993). Kidney Int. 44, 344–351.PubMedCrossRefGoogle Scholar
  31. 31.
    Mene, P., Pugliese, G., Pricci, F., DiMario, U., Cinotti, G. A., and Pugliese, F. (1993). Kidney Int. 43, 585–591.PubMedCrossRefGoogle Scholar
  32. 32.
    Bialecki, R. A., Tulenko, T. N., and Colucci, W. S. (1991). J. Clin. Invest. 86, 1894–1900.Google Scholar
  33. 33.
    Levy, J., Gavin, J. R., III, Grunberger, G., and Abioli, L. V. (1988). Diabetologia 31, 315–321.PubMedGoogle Scholar
  34. 34.
    Giroix, M. H., Portha, B., Kerogoat, M., Bailbe, D., and Picon, L. (1983). Diabetes 32, 445–451.PubMedCrossRefGoogle Scholar
  35. 35.
    Tsuji, K., Taminato, T., Ishida, H., Okamota, Y., Tsuura, Y., Kato, S., et al. (1993). Metabolism 42, 1424–1428.PubMedCrossRefGoogle Scholar
  36. 36.
    Kato, S., Ishida, H., Tsuura, Y., Okamoto, Y., Tsuji, K., Horie, M., et al. (1994). Metabolism 43, 1395–1400.PubMedCrossRefGoogle Scholar
  37. 37.
    Leahy, J. L. (1990). Diabetes Care 13, 992–1010.PubMedCrossRefGoogle Scholar
  38. 38.
    Juntti-Berggren, L., Larson, O., Rorsman, P., Ammala, C., Bokvist, K., Vahlander, K., et al. (1993) Science 261, 86–90.PubMedCrossRefGoogle Scholar
  39. 39.
    Hellman, B., Gylfe, E., Bergsten, P., Grapengiesser, E., Lund, P. E., Berts, A., et al. (1994). Diabetologia 37 (2 Suppl.), S11-S20.PubMedCrossRefGoogle Scholar
  40. 40.
    Dunbar, J. C., Houser, F., and Levy, J. (1989). Diab. Res. Clin. Pract. 7, 187–196.CrossRefGoogle Scholar
  41. 41.
    Gagliardino, J. J. and Rossi, J. P. (1994). Diab. Metab. Rev. 10, 1–17.Google Scholar
  42. 42.
    Reitner, R. (1993). Int. J. Biochem. 25, 297–305.CrossRefGoogle Scholar
  43. 43.
    Koike, M., Kashiwagura, T., and Takeguchi, N. (1992). Biochem. J. 283, 265–272.PubMedGoogle Scholar
  44. 44.
    Begum, N., Sussman, K. E., and Draznin, B. (1991). Cell Calcium 12, 423–430.PubMedCrossRefGoogle Scholar
  45. 45.
    Begum, N., Leitner, W., Reusch, J. E. B., Sussman, K. E., and Draznin, B. (1993). J. Biol. Chem. 268, 3352–3356.PubMedGoogle Scholar
  46. 46.
    Levy, J., Gavin, J. R., Morimoto, S., and Avioli, L. V. (1986). Diabetes 35, 899–905.PubMedCrossRefGoogle Scholar
  47. 47.
    Pershadsingh, H. A., Shade, D. L., Delfert, D. M., and McDonald, J. M. (1987). Proc. Natl. Acad. Sci. USA 84, 1025–1029.PubMedCrossRefGoogle Scholar
  48. 48.
    Draznin, B., Kao, M., and Sussman, K. E. (1986). Diabetes 36, 174–178.CrossRefGoogle Scholar
  49. 49.
    Carpentier, J. L., Gorden, P., and Lew, D. P. (1992). Exp. Cell. Res. 198, 144–149.PubMedCrossRefGoogle Scholar
  50. 50.
    Williams, P. F., Caterson, I. D., Cooney, G. J., Zilkens, R. R., and Turtle, J. R. (1990). Calcium 11, 547–556.CrossRefGoogle Scholar
  51. 51.
    Levy, J. and Rempinski, D. (1992). Inhibition of insulin bioeffects in adipocytes by monoclonal antibodies to the membrane (Ca2++Mg2+)-adenosine triphosphatase. Proceedings of the 74th Annual Meeting the Endocrine Society, San Antonio, TX, June 24–27:22 (Abstract).Google Scholar
  52. 52.
    Levy, J. and Rempinski, D. (1992). Insulin phosphorylates the membrane (Ca2++Mg2+)-adenosine triphosphatase. Proceedings of the 74th Annual Meeting the Endocrine Society, San Antonio TX, June 24–27:22 (Abstract).Google Scholar
  53. 53.
    Solomon, S. S., Palazzolo, M. R., Elam, M. B., Green, S., and Raghow, R. (1994). J. Lab. Clin. Med. 124, 348–358.PubMedGoogle Scholar
  54. 54.
    Ferrannini, E., Buzzigoli, G., Bonadonna, R., Giorico, M. A., Oleggini, M., Graziade, L., et al. (1987). N. Engl. J. Med. 317, 350–357.PubMedGoogle Scholar
  55. 55.
    Levy, J., Grunberger, G., Karl, I., and Gavin, J. R., III. (1990). Metabolism 39, 25–33.PubMedCrossRefGoogle Scholar
  56. 56.
    Draznin, B. (1993). Am. J. Kidney Disease 21 (6 Suppl.), 32–38.Google Scholar
  57. 57.
    Touyz, R. M. and Schiffrim, E. L. (1994). Hypertension 23, 931–935.PubMedGoogle Scholar
  58. 58.
    Brimble, K. S. and Ananthanarayanan, V. S. (1992). Biochim. Biophys. Acta 1105, 319–327.PubMedCrossRefGoogle Scholar
  59. 59.
    Dick, G. M. and Sturek, M. (1996). Diabetes 45, 876–880.PubMedCrossRefGoogle Scholar
  60. 60.
    Gonzalez, J. M. and Suki, W. N. (1995). Semin. Nephrol. 15, 564–568.PubMedGoogle Scholar
  61. 61.
    Oshima, T. and Toung, E. W. (1995). Semin. Nephrol. 15, 496–503.PubMedGoogle Scholar
  62. 62.
    Paoletti, R., Corsini, A., Soma, M. R., and Bernini, F. (1996). Blood Pressure Suppl. 4, 12–15.Google Scholar
  63. 63.
    Tulenko, T. N., Laury-Kleintop, L., Walter, M. F., and Mason, R. P. (1997). Int. J. Cardiol. (62 Suppl.) 2, S55-S66.CrossRefGoogle Scholar
  64. 64.
    Demer, L. L. (1995). Circulation 92, 2029–2032.PubMedGoogle Scholar
  65. 65.
    Chang, K. C., Screur, H., Weiner, M. W., and Camacho, S. A. (1996). Am. J. Physiol. 271, H228-H234.PubMedGoogle Scholar
  66. 66.
    Christlieb, A. R., Janka, H. U., Kraus, B., Gleason, R. E., Icasas-Cabral, E. A., Aiello, L. M., et al. (1976). Diabetes 25, 268–274.PubMedCrossRefGoogle Scholar
  67. 67.
    Dandona, P., James, I. M., and Beckett, A. G. (1981). Lancet 2, 694.PubMedCrossRefGoogle Scholar
  68. 68.
    Rhie, F. H., Christlieb, A. R., Sandor, T., Gleason, R. E., Rand, L. I., Shah, S. T., et al. (1982). Diabetes 31, 1056–1060.PubMedCrossRefGoogle Scholar
  69. 69.
    Sowers, J. R., Khoury, S., Standley, P., Zemel, P., and Zemel, M. (1991). Am. J. Hypertens. 4, 177–182.PubMedGoogle Scholar
  70. 70.
    Orlov, S. N., Li, J. M., Tremblay, J., and Hanet, P. (1995). Semin. Nephrol. 15, 569–592.PubMedGoogle Scholar
  71. 71.
    Borda, E. Pascual, J., Wald, M., and Sterin-Borda, L. (1988). Can. J. Cardiol. 4, 57–101.Google Scholar
  72. 72.
    Nobe, S., Aomine, M., Artia, M., Ito, S., and Takaki, R. (1990). Cardiovasc. Res. 24, 381–389.PubMedCrossRefGoogle Scholar
  73. 73.
    Schaffer, S. W. (1991). Mol. Cell. Biochem. 107, 1–20.PubMedCrossRefGoogle Scholar
  74. 74.
    Strickberger, S. A., Russek, L. N., and Phair, R. D. (1988). Circ. Res. 62, 75–80.PubMedGoogle Scholar
  75. 75.
    Ross, R. and Glomset, J. A. (1976). N. Engl. J. Med. 295, 420–425.PubMedGoogle Scholar
  76. 76.
    Orimo, H. and Ouchi, Y. (1990). Ann. NY Acad. Sci. 598, 444–457.PubMedCrossRefGoogle Scholar
  77. 77.
    Shi, H., Severs, N. J., and Robenek, H. (1996). FASEB J. 10, 491–501.PubMedGoogle Scholar
  78. 78.
    Wells, K. E., Miguel, R., and Alexander, J. J. (1997). J. Surg. Res. 67, 126–131.PubMedCrossRefGoogle Scholar
  79. 79.
    Jerome, D. S., Clifford, L. D., Fromm, B. S., Marsh, J. D., and Levy, J. (1996). J. Bone Min. Res. II, 260 (Abstract).Google Scholar
  80. 80.
    Johnson, P. C., Bendel, K., and Meezan, E. (1982). Arch. Pathol. Lab. Med. 106, 214–217.PubMedGoogle Scholar
  81. 81.
    Deckret, T., Feldt-Rasmussen, B. F., Borch-Johnson, T., and Kofoed-Enevoldsen, A. (1989). Diabetologia 32, 219–226.CrossRefGoogle Scholar
  82. 82.
    Boshell, B. R. and Austria, M. J. (1989). Diabetic Complications 3, 183–186.CrossRefGoogle Scholar
  83. 83.
    Williamson, J. R., Tilton, R. G., Chang, K., and Kilo, C. (1982). Arch. Pathol. Lab. Med. 106, 214–217.Google Scholar
  84. 84.
    Siperstein, M. D. (1972). Adv. Intern. Med. 18, 325–344.PubMedGoogle Scholar
  85. 85.
    Barnett, A. H. (1991). Am. J. Med. 90 (6A Suppl.), 67S-73S.PubMedCrossRefGoogle Scholar
  86. 86.
    Yurchenco P. D. and Schittny, J. C. (1990). FASEB J. 4, 1577–1590.PubMedGoogle Scholar
  87. 87.
    Roy, S., Sala, R., Cagliero, E., and Lorenzi, M. (1990). Proc. Natl. Acad. Sci. USA 87, 404–408.PubMedCrossRefGoogle Scholar
  88. 88.
    Couchman, J. R. (1987). J. Cell. Biol. 105, 1901–1916.PubMedCrossRefGoogle Scholar
  89. 89.
    Fujiwara, S., Wiedemann, H., Timple, R., Lustig, A., and Engel, J. (1984). Eur. J. Biochem. 143, 145–157.PubMedCrossRefGoogle Scholar
  90. 90.
    Papadimitriou, E., Manolopoulos, V. G., Hayman, G. T., Maragoudakis, M. E., Unsworth, B. R., Frenton, J. W., II, et al. (1997). Am. J. Physiol. 272, C1112-C1122.PubMedGoogle Scholar
  91. 91.
    Kamihagi, K., Katayama, M., Ouchi, R., and Kato, I. (1994). Biochem. Biophys. Res. Commun. 200, 423–428.PubMedCrossRefGoogle Scholar
  92. 92.
    Lodish, H. F. and Kong, N. (1990). J. Biol. Chem. 265, 10,893–10,899.Google Scholar
  93. 93.
    Lodish, H. F. (1988). J. Biol. Chem. 263, 2107–2110.PubMedGoogle Scholar
  94. 94.
    Williamson, J. R., Tilton, R. G., Chang, K., and Kilo, C. (1988). Metab. Rev. 4, 339–370.CrossRefGoogle Scholar
  95. 95.
    Paulsson, M. (1988). Biol. Chem. 263, 5425–5430.Google Scholar
  96. 96.
    Paulsson, M., Saladin, K., and Landwehr, R. (1988). Eur. J. Biochem. 177, 477–481.PubMedCrossRefGoogle Scholar
  97. 97.
    Michel, C. C. and Philips, M. E. (1989). Quat. J. Exp. Phys. 74, 7–18.Google Scholar
  98. 98.
    Majno, G., Shea, S. M., and Leventhal, M. (1969). J. Cell. Biol. 42, 647–672.PubMedCrossRefGoogle Scholar
  99. 99.
    Fox, J., Galey, F., and Wayland, H. (1980). Microvas. Res. 19, 108–126.CrossRefGoogle Scholar

Copyright information

© Humana Press Inc. 1999

Authors and Affiliations

  1. 1.Department of Medicine, Diabetes SectionWayne State University School of MedicineDetroit
  2. 2.Division of Endocrinology and MetabolismUniversity Health Center-4HDetroit

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