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Calcium transport by cardiac sarcoplasmic reticulum and phosphorylation of phospholamban

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Summary

Active calcium transport by cardiac sarcoplasmic reticulum assumes a central role in the excitation-concentration coupling of the myocardium, in that Ca2+-dependent ATPase (mol.wt. 100 000) of cardiac sarcoplasmic reticulum serves as an energy transducer and a translocator of Ca2+ across the membrane. During the translocation of Ca2+, the ATPase undergoes a complex series of reactions during which the phosphorylated intermediate EP is formed. We documented how the elementary steps of the ATPase reaction are coupled with calcium translocation, and provided evidences to indicate that two key steps of ATPase correspond to the conformational change of the enzyme, and appear to alter the affinity of the enzyme for Ca2+.

A line of evidence also indicated that Ca2+-dependent ATPase of cardiac sarcoplasmic reticulum is regulated by a specific protein named phospholamban (mol.wt. 22 000), which serves as a substrate for cyclic AMP-dependent protein kinase. Cyclic AMP-dependent phosphorylation of phospholamban resulted in a marked increase in the rate of turnover of the ATPase, by enhancing the rates of the key elementary steps, i.e. the steps at which the intermediate EP is formed and decomposed. Thus phospholamban is putatively thought to serve as a modulator of Cat2+-dependent ATPase of cardiac sarcoplasmic reticulum. A working model was proposed to interpret the mechanism. Also documented is a possibility that another protein kinase activatable by Ca2+ and calmodulin is functional in regulating the phospholamban-ATPase system, thus suggesting the existence of a dual control system, in which both cyclic AMP- and calmodulin-dependent phosphorylation are in control of the Cat2+-dependent ATPase.

Such a control mechanism may provide the interpretation, at the cellular level, that catecholamines exert actions on myocardial contractility. Thus, catecholamine-mediated increases in intracellular cyclic AMP could enhance calcium fluxes across the membrane of sarcoplasmic reticulum, thus resulting in the increased rates of relaxation and, at the same time, the increased rate and extent of contraction. Such a mechanism could also be operational in the tissues, other than the myocardium, in which catecholamines and other hormones serve as the ‘first messenger’, producing intracellular cyclic AMP as the ‘second messenger’.

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References

  1. 1.

    Tada, M., Yamamoto, T. & Tonomura, Y., 1978. Physiol. Rev. 58:1–79.

  2. 2.

    Endo, M., 1977. Physiol. Rev. 57: 71–108.

  3. 3.

    Fabiato, A. & Fabiato, F., 1979. Ann. Rev. Physiol. 41: 473–484.

  4. 4.

    Sutherland, E. W. & Rall, T. W., 1960. Pharmacol. Rev. 12: 265–299.

  5. 5.

    Tsien, R. W., 1977. Adv. Cyclic Nuc. Res. 8: 363–420.

  6. 6.

    Krebs, E. G., 1972. Curr. Top. Cell. Regul. 5: 99–133.

  7. 7.

    Brostrom, M. A., Reimann, E. M., Walsh, D. A. & Krebs, E. G., 1970. Adv. Enzyme Regul. 8: 191–203.

  8. 8.

    Soderling, T. R. & Park, C. R., 1974. Adv. Cyclic Nuc. Res. 4: 283–333.

  9. 9.

    Tada, M. & Katz, A. M., 1982. Ann. Rev. Physiol. 44: 401–423.

  10. 10.

    Tada, M., Kirchberger, M. A., Iorio, J.-A. & Katz, A. M., 1973. Circulation 48 (Suppl): IV-25.

  11. 11.

    Tada, M., Kirchberger, M. A. & Katz, A. M., 1975. J. Biol. Chem. 250: 2640–2647.

  12. 12.

    Katz, A. M., 1977. In: Physiology of the Heart, pp. 137–159, Raven Press, New York.

  13. 12a.

    McNutt, N. S. & Fawcett, D. W., 1969. J. Cell Biol. 42: 1–45.

  14. 13.

    Ashley, C. C. & Ridgway, E. B., 1968. Nature 219: 1168–1169.

  15. 13a.

    Allen, D. G. & Blinks, J. R., 1978. Nature 273: 509–513.

  16. 14.

    Marban, E., Rink, T. J., Tsien, R. W. & Tsien, R. Y., 1980. Nature 286: 845–850.

  17. 15.

    Ebashi, S., 1976. Ann. Rev. Physiol. 38: 293–313.

  18. 16.

    Harigaya, S. & Schwartz, A., 1969. Circ. Res. 25: 781–794.

  19. 17.

    Levitsky, D. O., Aliev, M. K., Kuzmin, A. V., Levchenko, T. S., Smirnov, V. N. & Chazov, E. I., 1976. Biochim. Biophys. Acta 443: 468–484.

  20. 18.

    Jones, L. R., Besch, H. R., Jr., Fleming, J. W., McConnaughey, M. M. & Watanabe, A. M., 1979. J. Biol. Chem. 254: 530–539.

  21. 19.

    Affolter, H., Chiesi, M., Dabrowska, R. & Carafori, E., 1976. Eur. J. Biochem. 67: 389–396.

  22. 20.

    Suko, J. & Hasselbach, W., 1976. Eur. J. Biochem. 64: 123–130.

  23. 21.

    Van Winkle, W. B., Pitts, B. J. R. & Entman, M. L., 1978. J. Biol. Chem. 253: 8671–8673.

  24. 22.

    MacLennan, D. H. & Holland, P. C., 1976. In: The Enzymes of Biological Membranes (Martonosi, A., ed.), pp. 221–259, Plenum Press, New York.

  25. 23.

    Fleischer, S. Wang, C.-T., Hymel, L., Seeling, J., Brown, M. F., Herbette, L., Scarpa, A., McLaughlin, A. C. & Blasie, J. K., 1979. In: Function and Molecular Aspects of Biomembrane Transport (Quagliariello, E., Palmieri, F., Papa, S., Klingenberg, M., eds.), pp. 465–485, Elsevier/North-Holland, Amsterdam.

  26. 24.

    MacLennan, D. H. & Holland, P. C., 1975. Ann. Rev. Biophys. Bioeng. 4: 377–404.

  27. 25.

    Thorley-Lawson, D. A. & Green, N. M., 1973. Eur. J. Biochem. 40: 403–413.

  28. 26.

    Thorley-Lawson, D. A. & Green, N. M., 1975. Eur. J. Biochem. 59: 193–200.

  29. 27.

    MacLennan, D. H., Seeman, P., Iles, G. H. & Yip, C. C., 1971. J. Biol. Chem. 246: 2702–2710.

  30. 28.

    Stewart, P. S. & MacLennan, D. H., 1974. J. Biol. Chem. 249: 985–993.

  31. 29.

    Stewart, P. S., MacLennan, D. H. & Shamoo, A. E., 1976. J. Biol. Chem. 251: 712–719.

  32. 30.

    Yamamoto, T. & Tonomura, Y., 1977. J. Biochem. Tokyo 82:653–660.

  33. 31.

    Inesi, G. & Scales, D., 1974. Biochemistry 13: 3298–3306.

  34. 32.

    Louis, C. F., Buonaffina, R. & Binks, B., 1974. Arch. Biochem. Biophys. 161: 83–92.

  35. 33.

    Louis, C. & Shooter, E. M., 1972. Arch. Biochem. Biophys. 153: 641–655.

  36. 34.

    Yu, B. P., Masoro, E. J. & Morley, T. F., 1976. J. Biol. Chem. 251: 2037–2043.

  37. 35.

    Rizzolo, L. J., Le Maire, M., Reynolds, J. A. & Tanford, C., 1976. Biochemistry 15: 3433–3437.

  38. 36.

    Le Maire, M., Jørgensen, K. E., Roigaard, H. & Moller, J. V., 1976. Biochemistry 15: 5805–5812.

  39. 37.

    Tada, M., Ohmori, F., Kinoshita, N. & Abe, H., 1978. Adv. Cyclic Nuc. Res. 9: 355–369.

  40. 38.

    Tada, M., Ohmori, F., Yamada, M. & Abe, H., 1979. J. Biol. Chem. 254: 319–326.

  41. 39.

    Pang, D. C. & Briggs, F. N., 1973. Biochemistry 12: 4905–4911.

  42. 40.

    Shigekawa, M., Finegan, J.-M. & Katz, A. M., 1976. J. Biol. Chem. 251: 6894–6900.

  43. 41.

    Froehlich, J. P. & Taylor, E. W., 1976. J. Biol. Chem. 251: 2307–2315.

  44. 42.

    Shigekawa, M. & Dougherty, J. P., 1978. J. Biol. Chem. 253:1451–1457.

  45. 43.

    Shigekawa, M., Dougherty, J. P. & Katz, A. M., 1978. J. Biol. Chem. 253: 1442–1450.

  46. 44.

    De Meis, L. & Vianna, A. L., 1979. Ann. Rev. Biochem. 48: 275–292.

  47. 45.

    LaRaia, P. J. & Morkin, E., 1974. Circ. Res. 35: 298–306.

  48. 46.

    Wray, H. L., Gray, R. R. & Olsson, R. A., 1973. J. Biol. Chem. 248: 1496–1498.

  49. 47.

    Kirchberger, M. A., Tada, M. & Katz, A. M., 1974. J. Biol. Chem. 249: 6166–6173.

  50. 48.

    Kirchberger, M. A. & Tada, M., 1976. J. Biol. Chem. 251: 725–729.

  51. 49.

    Schwartz, A., Entman, M. L., Kaniike, K., Lane, L. K., Van Winkle, W. B. & Bornet, E. P., 1976. Biochim. Biophys. Acta 426: 57–72.

  52. 50.

    Wray, H. L. & Gray, R. R., 1977. Biochim. Biophys. Acta 461: 441–459.

  53. 51.

    Will, H., Levchenko, T. S., Levitsky, D. O., Smirnov, V. N. & Wollenberger, A., 1978. Biochim. Biophys. Acta 543: 175–193.

  54. 52.

    St. Louis, P. J. & Sulakhe, P. V., 1979. Arch. Biochem. Biophys. 198: 227–240.

  55. 53.

    Lamers, J. M. J. & Stinis, J. T., 1980. Biochim. Biophys. Acta 624: 443–459.

  56. 54.

    Bidlack, J. M. & Shamoo, A. E., 1980. Biochim. Biophys. Acta 632: 310–325.

  57. 55.

    Le Peuch, C. J., Le Peuch, D. A. M. & Demaille, J. G., 1980. Biochemistry 19: 3368–3373.

  58. 56.

    Tada, M., Inui, M., Yamada, M., Kadoma, M., Kuzuya, T., Abe, H. & Kakiuchi, S., 1982. J. Mol. Cell. Cardiol. (in press).

  59. 57.

    Katz, A. M., Tada, M. & Kirchberger, M. A., 1975. Adv. Cyclic Nuc. Res. 5: 453–472.

  60. 58.

    Le Peuch, C. J., Haiech, J. & Demaille, J. G., 1979. Biochemistry 18: 5150–5157.

  61. 59.

    Nimmo, H. G. & Cohen, P., 1977. Adv. Cyclic Nuc. Res. 8: 145–266.

  62. 60.

    Kirchberger, M. A., Tada, M., Repke, D.I. & Katz, A. M., 1972. J. Mol. Cell. Cardiol. 4: 673–680.

  63. 61.

    Tada, M., Kirchberger, M. A., Repke, D. I. & Katz, A. M., 1974. J. Biol. Chem. 249: 6174–6180.

  64. 62.

    Kirchberger, M. A. & Chu, G., 1976. Biochim. Biophys. Acta 419: 559–562.

  65. 63.

    Hicks, M. J., Shigekawa, M. & Katz, A. M., 1979. Circ. Res. 44: 384–391.

  66. 64.

    Tada, M., Kirchberger, M. A. & Li, H.-C., 1975. J. Cyclic Nuc. Res. 1: 329–338.

  67. 65.

    Kirchberger, M. A. & Raffo, A., 1977. J. Cyclic Nuc. Res. 3: 45–53.

  68. 66.

    Tada, M., Ohmori, F., Nimura, Y. & Abe, H., 1977. J. Biochem. Tokyo 82: 885–892.

  69. 67.

    Ohmori, F., Tada, M., Kinoshita, N., Matsuo, H., Sakakibara, H., Nimura, Y. & Abe, H., 1978. In: Recent Advances in Studies on Cardiac Structure and Metabolism, Vol. 11 (Kobayashi, T., Sano, T., Dhalla, N. S., eds.) pp. 279–284, University Park Press, Baltimore.

  70. 68.

    Will, H., Blanck, J., Smettan, G. & Wollenberger, A., 1976. Biochim. Biophys. Acta 449: 295–303.

  71. 69.

    Tada, M., Yamada, M., Ohmori, F., Kuzuya, T., Inui, M. & Abe, H., 1980. J. Biol. Chem. 255: 1985–1992.

  72. 70.

    Kranias, E. G., Mandel, F., Wang, T. & Schwartz, A., 1980. Biochemistry 19: 5434–5439.

  73. 71.

    Froehlich, J. P., Sullivan, J. V. & Berger, R. L., 1976. Anal. Biochem. 73: 331–341.

  74. 72.

    Kirchberger, M. A. & Wong, D., 1978. J. Biol. Chem. 253: 6941–6945.

  75. 73.

    Katz, A. M., 1979. Adv. Cyclic Nuc. Res. 11: 303–343.

  76. 74.

    Louis, C. F. & Katz, A. M., 1977. Biochim. Biophys. Acta 494: 255–265.

  77. 75.

    Tada, M., Yamada, M., Ohmori, F., Kuzuya, T. & Abe, H., 1979. In: Cation Flux Across Biomembranes (Mukohata, Y. & Packer, L., eds.) pp. 179–190, Academic Press, New York.

  78. 76.

    Katz, A. M., 1980. Trends Phrmacol. Sci. 1: 434–436.

  79. 77.

    Yamamoto, T., Takisawa, H., Tonomura, Y., 1979. Curr. Top. Bioenerg. 9: 179–236.

  80. 78.

    Kranias, E. G., Bilezikjian, L. M., Potter, J. D., Piascik, M. T. & Schwartz, A., 1980. Ann. NY. Acad. Sci. 356: 279–290.

  81. 79.

    Katz, S. & Remtulla, M. A., 1978. Biochem. Biophys. Res. Commun. 83: 1373–1379.

  82. 80.

    Lopaschuk, G. Richter, B. & Katz, S., 1980. Biochemistry 19: 5603–5607.

  83. 81.

    Stull, J. T. & Mayer, S. E.,1979. In: Handbook of Physiology. II. The Cardiovascular System. Vol. 1 (Berne, R. M., Sperelakis, N., eds.), pp. 741–774, American Physiological Society, Bethesda.

  84. 82.

    Morad, M. & Rolett, E. L., 1972. J. Physiol. (London) 224: 537–558.

  85. 83.

    Reuter, H., 1974. J. Physiol. London 242: 429–451.

  86. 84.

    Fabiato, A. & Fabiato, F., 1977. Circ. Res. 40: 119–129.

  87. 85.

    Fabiato, A. & Fabiato, F., 1975. Nature 253: 556–558.

  88. 86.

    Schumann, H. J., Endoh, M. & Brodde, O. E., 1975. Naunyn-Schmiedebergs Arch. Pharmacol. 289: 291–302.

  89. 87.

    Ingebretsen, W. R. Jr., Bercker, E., Friedman, W. F. & Mayer, S. E., 1977. Circ. Res. 40: 474–484.

  90. 88.

    Venter, J. C., Ross, J. Jr. & Kaplan, N. O., 1975. Proc. Natl. Acad. Sci. U.S.A. 72: 824–828.

  91. 89.

    Ong., S. M. & Steiner, A. L., 1977. Science 195: 183–185.

  92. 90.

    Steiner, A. L., Koide, Y., Earp, H. S., Bechtel, P. J. & Beavo, J. A., 1978. Adv. Cyclic Nuc. Res. 9: 691–705.

  93. 91.

    Le Peuch, C. J., Guilleux, J.-C. & Demaille, J. G., 1980. FEBS Lett. 114: 165–168.

  94. 92.

    Lindemann, J. P., Jones, L. R. & Watanabe, A. M., 1980. Clin. Res. 28: 471A (Abstract).

  95. 92a.

    Lindemann, J. P., Jones, L. R. & Watanabe, A. M., 1981. Circulation 64 (Suppl) IV-22.

  96. 93.

    Haslam, R. J., Davidson, M. M. L., Davies, T., Lynham, J. A. & McClenaghan, M. D., 1978. Adv. Cyclic Nuc. Res. 9: 533–552.

  97. 94.

    Kaser-Glanzmann, R., Jakábová, M., George, J. N. & Luscher, E. F., 1977. Biochim. Biophys. Acta 466: 429–440.

  98. 95.

    Bhalla, R. C., Webb, R. C., Singh, D. & Brock, T., 1978. Am. J. Physiol. 234: H508-H514.

  99. 96.

    Kimura, M., Kimura, I. & Kobayashi, S., 1977. Biochem. Pharmacol. 26: 994–996.

  100. 97.

    Kaser-Glanzmann, R., Gerber, E. & Luscher, E. F., 1979. Biochim. Biophys. Acta 558: 344–347.

  101. 98.

    Limas, C. J., 1978. Am. J. Physiol. 234: H426-H431.

  102. 99.

    Limas, C. J., 1978. Am. J. Physiol. 235: H745-H751.

  103. 100.

    Kadoma, M., Sacktor, B. & Froehlich, J. P., 1980. Fed. Proc. 39: 2040 (Abstract).

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Tada, M., Yamada, M., Kadoma, M. et al. Calcium transport by cardiac sarcoplasmic reticulum and phosphorylation of phospholamban. Mol Cell Biochem 46, 73–95 (1982). https://doi.org/10.1007/BF00236776

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Keywords

  • Catecholamine
  • Sarcoplasmic Reticulum
  • Myocardial Contractility
  • Active Calcium
  • Calcium Transport