Journal of Bioenergetics and Biomembranes

, Volume 23, Issue 6, pp 823–854 | Cite as

Dehydrogenase activation by Ca2+ in cells and tissues

  • Richard G. Hansford
Mini-Review

Abstract

The activation of intramitochondrial dehydrogenases by Ca2+ provides a link between the intensity of work performance by a tissue and the activity of pyruvate dehydrogenase and the tricarboxylate cycle, and hence the rate of ATP production by the mitochondria. Several aspects of this model of the control of oxidative phosphorylation are examined in this article, with particular emphasis on mitochondrial functioning in situ in cardiac myocytes and in the intact heart. Recent use of the fluorescent Ca2+ chelating agents indo-1 and fura-2 has allowed a more quantitative description of the dependence of dehydrogenase activity upon concentration of free intramitochondrial Ca2+, in experiments with isolated mitochondria. Further, a novel technique developed by Miyataet al. has allowed description of free intramitochondrial Ca2+ within a single cardiac myocyte, and the conclusion that this parameter changes in response to electrical excitation of the cell over a range which would be expected to give substantial modulation of dehydrogenase activity.

Key Words

Pyruvate dehydrogenase 2-oxoglutarate dehydrogenase glycerol 3-phosphate dehydrogenase intramitochondrial free Ca2+ mitochondrial Ca2+ transport adenine nucleotide phosphorylation potential 

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References

  1. Akerboom, T. P. M., Bookelman, H., Zuurendonk, P. F., van der Meer, R., and Tager, J. M. (1978).Eur. J. Biochem. 84 413–420.Google Scholar
  2. Akerman, K. E. O., and Nicholls, D. G. (1983).Rev. Physiol. Biochem. Pharmacol. 95 149–201.Google Scholar
  3. Allen, D. G., and Orchard, C. H. (1987).Circ. Res. 60 153–168.Google Scholar
  4. Ashley, R. H., Brammer, M. J., and Marchbanks, R. (1984).Biochem. J. 219 149–158.Google Scholar
  5. Assimacopoulos-Jeannet, F., McCormack, J. G., and Jeanrenaud, B. (1983).FEBS Lett. 159 83–89.Google Scholar
  6. Assimacopoulos-Jeannet, F., McCormack, J. G., and Jeanrenaud, B. (1986).J. Biol. Chem. 261 8799–8804.Google Scholar
  7. Balaban, R. S., Blum, J. J. (1982).Am. J. Physiol. 242 C172-C177.Google Scholar
  8. Balaban, R. S., Kantor, H. L., Katz, L. A., and Briggs, R. W. (1986).Science 232 1121–1123.Google Scholar
  9. Beleznai, Z., Szalay, L., and Jancsik, V. (1988).Eur. J. Biochem. 170 631–636.Google Scholar
  10. Berridge, M. J. (1990).J. Biol. Chem. 265 9583–9586.Google Scholar
  11. Berridge, M. J., and Galione, A. (1988).FASEB J. 2 3074–3082.Google Scholar
  12. Berridge, M. J., Cobbold, P. H., and Cuthbertson, K. S. R. (1988).Philos. Trans. R. Soc. London B 320 325–343.Google Scholar
  13. Berthon, B., Binet, A., Mauger, J.-P., and Claret, M. (1984).FEBS Lett. 167 19–24.Google Scholar
  14. Blackmore, P. F., Hughes, B. P., Charest, R. Shuman, E. A., IV, and Exton, J. H. (1983).J. Biol. Chem. 258 10488–10494.Google Scholar
  15. Blatter, L. A., and Wier, W. G. (1990).Biophys. J. 58 1491–1499.Google Scholar
  16. Bond, M., Vadasz, G., Somlyo, A. V., and Somlyo, A. P. (1987).J. Biol. Chem. 262 15630–15636.Google Scholar
  17. Borst, P. (1963). InFunktionelle und Morphologische Organisation der Zelle (Karlson, P., ed.), Springer-Verlag, New York, pp. 137–158.Google Scholar
  18. Bukowiecki, L. J., and Lindberg, O. (1974).Biochim. Biophys. Acta 348 115–125.Google Scholar
  19. Bünger, R., Permanetter, B., Sommer, O., and Yaffe, S. (1982).Am. J. Physiol. 242 H30-H36.Google Scholar
  20. Carafoli, E., and Lehninger, A. L. (1971).Biochem. J. 122 681–690.Google Scholar
  21. Chance, B., and Williams, G. R. (1956).Adv. Enzymol. 17 65–134.Google Scholar
  22. Chance, B., Leigh, J. S., Jr., Kent, J., McCully, K., Nioka, S., Clark, B. J., Maris, J. M., and Graham, T. (1986).Proc. Natl. Acad. Sci. USA 83 9458–9462.Google Scholar
  23. Charest, R., Blackmore, P. F., Berthon, B., and Exton, J. H. (1983).J. Biol. Chem. 258 8769–8773.Google Scholar
  24. Clarke, K., and Willis, R. J. (1987).J. Mol. Cell. Cardiol. 19 1153–1160.Google Scholar
  25. Cobbold, P. H. (1989).News Physiol. Sci. 4 211–215.Google Scholar
  26. Coll, K. E., Joseph, S. K., Corkey, B. E., and Williamson, J. R. (1982).J. Biol. Chem. 257 8696–8704.Google Scholar
  27. Cooper, R. H., Randle, P. J., and Denton, R. M. (1975).Nature (London)257 808–809.Google Scholar
  28. Crompton, M. (1985).Curr. Top. Membr. Transp. 25 231–276.Google Scholar
  29. Crompton, M., and Heid, I. (1978).Eur. J. Biochem. 91 599–608.Google Scholar
  30. Crompton, M., Sigel, E., Salzmann, M., and Carafoli, E. (1976a).Eur. J. Biochem. 69 429–434.Google Scholar
  31. Crompton, M., Capano, M., and Carafoli, E. (1976b).Eur. J. Biochem. 69 453–462.Google Scholar
  32. Davis, E. J., and Lumeng, L. (1975).J. Biol. Chem. 250 2275–2282.Google Scholar
  33. Davis, M. H., Altschuld, R. A., Jung, D. W., and Brierley, G. P. (1987).Biochem. Biophys. Res. Commun. 149 40–45.Google Scholar
  34. Denton, R. M., and McCormack, J. G. (1985).Am. J. Physiol. 249 E543-E554.Google Scholar
  35. Denton, R. M., Randle, P. J., and Martin, B. R. (1972).Biochem. J. 128 161–163.Google Scholar
  36. Denton, R. M., Richards, D. A., and Chin, J. G. (1978).Biochem. J. 176 899–906.Google Scholar
  37. Denton, R. M., McCormack, J. G., and Edgell, N. J. (1980).Biochem. J. 190 107–117.Google Scholar
  38. Erecinska, M., and Wilson, D. F. (1982).J. Membr. Biol. 70 1–14.Google Scholar
  39. Estabrook, R. W., and Sacktor, B. (1958).J. Biol. Chem. 233 1014–1019.Google Scholar
  40. Fein, A., and Tsacopoulos, M. (1988a).J. Gen. Physiol. 91 515–527.Google Scholar
  41. Fein, A., and Tsacopoulos, M. (1988b).Nature (London)331 437–440.Google Scholar
  42. Fisher, A. B., Scarpa, A., La Nove, K. F., Bassett, D., and Williamson, J. R. (1973).Biochemistry 12 1438–1445.Google Scholar
  43. From, A. H. L., Petein, M. A., Michurski, S. P., Zimmer, S. D., and Ugurbill, K. (1986).FEBS Lett. 206 257–261.Google Scholar
  44. Groen, A. K., Wanders, R. J. A., Westerhoff, H. V., van der Meer, R., and Tager, J. M. (1982).J. Biol. Chem. 257 2754–2757.Google Scholar
  45. Groen, A. K., Vervoorn, R. C., van der Meer, R., and Tager, J. M. (1983).J. Biol. Chem. 258 14346–14353.Google Scholar
  46. Grynkiewicz, G., Poenie, M., and Tsien, R. Y. (1985).J. Biol. Chem. 260 3440–3450.Google Scholar
  47. Gunter, T. E., and Pfeiffer, D. R. (1990).Am. J. Physiol. 258 C755-C786.Google Scholar
  48. Gunter, T. E., Restrepo, D., and Gunter, K. K. (1988).Am. J. Physiol. 255 C304-C310.Google Scholar
  49. Halestrap, A. P. (1987a).Biochim. Biophys. Acta 927 280–290.Google Scholar
  50. Halestrap, A. P. (1987b).Biochem. J. 244 159–164.Google Scholar
  51. Halestrap, A. P. (1989).Biochim. Biophys. Acta 973 355–382.Google Scholar
  52. Hansford, R. G. (1977).J. Biol. Chem. 252 1552–1560.Google Scholar
  53. Hansford, R. G. (1980).Curr. Top. Bioenerg. 10 217–278.Google Scholar
  54. Hansford, R. G. (1981).Biochem. J. 194 721–732.Google Scholar
  55. Hansford, R. G. (1985).Rev. Physiol. Biochem. Pharmacol. 102 1–72.Google Scholar
  56. Hansford, R. G. (1987).Biochem. J. 241 145–151.Google Scholar
  57. Hansford, R. G., and Castro, F. (1981).Biochem. J. 198 525–533.Google Scholar
  58. Hansford, R. G., and Castro, F. (1982).J. Bioenerg. Biomembr. 14 361–376.Google Scholar
  59. Hansford, R. G., and Castro, F. (1985).Biochem. J. 227 129–136.Google Scholar
  60. Hansford, R. G., and Chappell, J. B. (1967).Biochem. Biophys. Res. Commun. 27 686–692.Google Scholar
  61. Hansford, R. G. and Cohen, L. (1978).Arch. Biochem. Biophys. 191 65–81.Google Scholar
  62. Hansford, R. G., and Johnson, R. N. (1975).J. Biol. Chem. 250 8361–8375.Google Scholar
  63. Hansford, R. G., Moreno-Sánchez, R., and Staddon, J. (1988). InIntegration of Mitochondrial Function (Lemasters, J. J., Hackenbrock, C. R., Thurman, R. G., and Westerhoff, H. V., eds.). Plenum Press, New York, pp. 235–244.Google Scholar
  64. Hansford, R. G., Hogue, B., Prokopczuk, A., Wasilewska, E., and Lewartowski, B. (1990).Biochim. Biophys. Acta 1018 282–286.Google Scholar
  65. Haussinger, D., and Sies, H. (1984).Biochem. J. 221 651–658.Google Scholar
  66. Heineman, F. W., and Balaban, R. S. (1990).Annu. Rev. Physiol. 52 523–542.Google Scholar
  67. Hems, D. A., McCormack, J. G., and Denton, R. M. (1978).Biochem. J. 176 627–629.Google Scholar
  68. Henry, P. D., Schuchleib, R., Davis, J., Weiss, E. S., and Sobel, B. E. (1977).Am. J. Physiol. 233 H677-H684.Google Scholar
  69. Hess, P., Metzger, P., and Weingart, R. (1982).J. Physiol. (London)333 173–188.Google Scholar
  70. Hiltunen, J. K., and Hassinen, I. E. (1976).Biochim. Biophys. Acta 440 377–390.Google Scholar
  71. Hoerter, J. A., Miceli, M. V., Jacobus, W. E., Renlund, D. G., Gerstenblith, G., and Lakatta, E. G. (1986).Circ. Res. 58 539–551.Google Scholar
  72. Honenjager, P., and Reiter, M. (1975).Naunyn-Schmiedelberg's Arch. Pharmacol. 289 1–28.Google Scholar
  73. Horackova, M., and Vassort, G. (1974).Pfluegers Arch. 352 291–302.Google Scholar
  74. Houštek, J., Cannon, B., and Lindberg, O. (1975).Eur. J. Biochem. 54 11–18.Google Scholar
  75. Hucho, F., Randall, D. D., Roche, T. E., Burgett, M. W., Pelley, J. W., and Reed, L. J. (1972).Arch. Biochem. Biophys. 151 328–340.Google Scholar
  76. Illingworth, J. A., and Mullings, R. (1976).Biochem. Soc. Trans. 4 291–292.Google Scholar
  77. Jacobus, W. E., Moreadith, R. W., and Vandegaer, K. M. (1982).J. Biol. Chem. 257 2397–2402.Google Scholar
  78. Jacobus, W. E., Tiozzo, R., Lugli, G., Lehninger, A. L., and Carafoli, E. (1975).J. Biol. Chem. 250 7863–7870.Google Scholar
  79. Johnston, J. D., and Brand, M. D. (1987).Biochem. J. 245 217–222.Google Scholar
  80. Jou, M-J., and Sheu, S-S. (1990).Biophys. J. 57, 343a.Google Scholar
  81. Kauppinen, R. A., and Nicholls, D. G. (1986).FEBS Lett. 199 222–226.Google Scholar
  82. Kawanishi, T., Blank, L. M., Harootunian, A. T., Smith, M. T., and Tsien, R. Y. (1989).J. Biol. Chem. 264 12859–12866.Google Scholar
  83. Keilin, D. (1925).Proc. R. Soc. London Ser. B. 98, 312-Google Scholar
  84. Klingenberg, M., and Bücher, T. (1961).Biochem Z. 334 1–17.Google Scholar
  85. Kneer, N. N., and Lardy, H. A. (1983).Arch. Biochem. Biophys. 225 187–195.Google Scholar
  86. Kobayashi, K., and Neely, J. R. (1983).J. Mol. Cell. Cardiol. 15 369–382.Google Scholar
  87. Koretsky, A. P., and Balaban, R. S. (1987).Biochim. Biophys. Acta 893 398–408.Google Scholar
  88. Kunz, W., Bohnensack, R., Bohme, G., Kuster, V., Letko, G., and Schonfeld, P. (1981).Arch. Biochem. Biophys. 209 219–229.Google Scholar
  89. Kunz, W., Bohnensack, R., Kuster, V., Letko, G., Bohme, G., Duszynski, J., and Wojtczak, L. (1983).FEBS Lett. 151 1–9.Google Scholar
  90. LaNoue, K. F., and Schoolwerth, A. C. (1979).Annu. Rev. Biochem. 48 871–922.Google Scholar
  91. Lardy, H., and Wellman, H. (1952).J. Biol. Chem. 195 215–224.Google Scholar
  92. Lawlis, V. B., and Roche, T. E. (1981a).Biochem. 20 2512–2518.Google Scholar
  93. Lawlis, V. B., and Roche, T. E. (1981b).Biochem. 20 2519–2524.Google Scholar
  94. Lee, C. O., and Fozzard, H. A. (1975).J. Gen. Physiol. 65 695–708.Google Scholar
  95. Leverve, X. M., Verhoeven, A. J., Groen, A. K., Meijer, A. J., and Tager, J. M. (1986).Eur. J. Biochem. 155 551–556.Google Scholar
  96. Lewartowski, B., Hansford, R. G., Langer, G. A., and Lakatta, E. G. (1990).Am. J. Physiol. 259 H1222-H1229.Google Scholar
  97. Lukács, G. L., and Kapus, A. (1987).Biochem J. 248 609–613.Google Scholar
  98. Lukács, G. L., Kapus, A., and Fonyo, A. (1988).FEBS Lett. 229 219–223.Google Scholar
  99. MacDonald, M. J. (1981).J. Biol. Chem. 256 8287–8290.Google Scholar
  100. Matschinsky, F. M., Corkey, B. E., Prentki, M., Meglasson, M. D., Erecinska, M., Shimizu, T., Ghosh, A., and Parker, J. (1989). InDiabetes 1988 (Larkins, R., Zimmet, P., and Chisholm, D., eds.), Elsevier, Amsterdam, pp. 17–26.Google Scholar
  101. Mauger, J. P., Poggioli, J., Guesdon, F., and Claret, M. (1984).Biochem. J. 221 121–127.Google Scholar
  102. Mauger, J. P., Poggioli, J., and Claret, M. (1985).J. Biol. Chem. 260 11635–11642.Google Scholar
  103. McCormack, J. G. (1985a).Biochem. J. 231 581–595.Google Scholar
  104. McCormack, J. G. (1985b).Biochem. J. 231 597–608.Google Scholar
  105. McCormack, J. G., and Denton, R. M. (1979).Biochem. J. 180 533–544.Google Scholar
  106. McCormack, J. G., and Denton, R. M. (1980).Biochem. J. 190 95–105.Google Scholar
  107. McCormack, J. G., and Denton, R. M. (1981a).Biochem. J. 194 639–643.Google Scholar
  108. McCormack, J. G., and Denton, R. M. (1981b).Biochem. J. 196 619–624.Google Scholar
  109. McCormack, J. G., and Denton, R. M. (1984).Biochem. J. 218 235–247.Google Scholar
  110. McCormack, J. G., and England, P. J. (1983).Biochem. J. 214 581–585.Google Scholar
  111. McCormack, J. G., Edgell, N. J., and Denton, R. M. (1982).Biochem. J. 202 419–427.Google Scholar
  112. McCormack, J. G., Browne, H. M., and Dawes, N. J. (1989).Biochim. Biophys. Acta 973 420–427.Google Scholar
  113. McCormack, J. G., Halestrap, A. P., and Denton, R. M. (1990a).Physiol Rev. 70 391–425.Google Scholar
  114. McCormack, J. G., Longo, E. A., Corkey, B. E. (1990b).Biochem. J. 267 527–530.Google Scholar
  115. Meglasson, M. D., and Matschinsky, F. M. (1986).Diabetes Metab. Rev. 2 163–214.Google Scholar
  116. Miyata, H. Silverman, H. S., Hansford, R. G., Sollott, S. J., Lakatta, E. G., and Stern, M. D. (1991a).Biophys. J. 59, 238a.Google Scholar
  117. Miyata, H., Silverman, H. S., Sollott, S. J., Lakatta, E. G., Stern, M. D., and Hansford, R. G. (1991b).Am. J. Physiol. 261 H1123-H1134.Google Scholar
  118. Moreno-Sánchez, R. (1985a).J. Biol. Chem. 260 4028–4034.Google Scholar
  119. Moreno-Sánchez, R. (1985b).J. Biol. Chem. 260 12554–12560.Google Scholar
  120. Moreno-Sánchez, R., and Hansford, R. G. (1988a).Biochem. J. 256 403–412.Google Scholar
  121. Moreno-Sánchez, R., and Hansford, R. G. (1988b).Am. J. Physiol. 255 H347-H357.Google Scholar
  122. Moreno-Sánchez, R., Hogue, B. A., and Hansford, R. G. (1990).Biochem. J. 268 421–428.Google Scholar
  123. Murphy, E., Freudenrich, C. C., Levy, L. A., London, R. E., and Lieberman, M. (1989).Proc. Natl. Acad. Sci. USA 86 2981–2984.Google Scholar
  124. Nicholls, D. G. (1974).Eur. J. Biochem. 50 306–315.Google Scholar
  125. Nicholls, D. G. (1977).Eur. J. Biochem. 77 349–356.Google Scholar
  126. Patel, T. B., and Olson, M. S. (1986).Biochim. Biophys. Acta 888 315–324.Google Scholar
  127. Patel, T. B., Sambasivarao, D., and Rashed, H. M. (1988).Arch. Biochem. Biophys. 264 368–375.Google Scholar
  128. Pearce, F. J., Walajtys-Rode, E., and Williamson, J. R. (1980).J. Mol. Cell. Cardiol. 12 499–510.Google Scholar
  129. Pettit, F. H., Roche, T. E., and Reed, L. J. (1972).Biochem. Biophys. Res. Commun. 49 563–571.Google Scholar
  130. Pettit, F. H., Pelley, J. W., and Reed, L. J. (1975).Biochem. Biophys. Res. Commun. 65 575–582.Google Scholar
  131. Pietrobon, D., Zoratti, M., Azzone, G. F., and Caplan, S. R. (1986).Biochemistry 25 767–775.Google Scholar
  132. Prentki, M., and Matschinsky, F. M. (1987).Physiol. Rev. 67 1185–1248.Google Scholar
  133. Prentki, M., and Wollheim, C. B. (1984).Experientia 40 1052–1060.Google Scholar
  134. Prentki, M., Glennon, M. C., Thomas, A. P., Morris, R. L., Matschinsky, F. M., and Corkey, B. E. (1988).J. Biol. Chem. 263 11044–11047.Google Scholar
  135. Quinlan, P. T., and Halestrap, A. P. (1986).Biochem. J. 236 789–800.Google Scholar
  136. Randle, P. J., England, P. J., and Denton, R. M. (1970).Biochem. J. 117 677–695.Google Scholar
  137. Randle, P. J., Denton, R. M., Pask, H. T., and Severson, D. L. (1974).Biochem. Soc. Symp. 39 75–87.Google Scholar
  138. Rashed, H. M., Waller, F. M., and Patel, T. B. (1988).J. Biol. Chem. 263 5700–5706.Google Scholar
  139. Reber, B. F. X., Somogyi, R., and Stucki, J. W. (1990).Biochim. Biophys. Acta 1018 190–193.Google Scholar
  140. Reed, L. J., and Yeaman, S. J. (1987). InThe Enzymes, 3d edn. (Boyer, P. D., and Krebs, E. G., eds.), Academic Press, New York, pp. 77–93.Google Scholar
  141. Reed, L. J., Damuni, Z., and Merryfield, M. L. (1985).Curr. Top. Cell. Regul. 27 41–49.Google Scholar
  142. Reers, M., Kelly, R. A., and Smith, T. W. (1989).Biochem. J. 257 131–142.Google Scholar
  143. Reinhart, P. H., Taylor, W. M., and Bygrave, F. L. (1982).J. Biol. Chem. 257 1906–1912.Google Scholar
  144. Renlund, D. G., Lakatta, E. G., Mellits, E. D., and Gerstenblith, G. (1985).Circ. Res. 57 876–888.Google Scholar
  145. Rich, T. L., Langer, G. A., and Klassen, M. G. (1988).Am. J. Physiol. 254 H937-H946.Google Scholar
  146. Richards, C. D., Metcalfe, J. C., Smith, G. A., and Hesketh, T. R. (1984).Biochim. Biophys. Acta 803 215–220.Google Scholar
  147. Ringler, R. L., and Singer, T. P. (1959).J. Biol. Chem. 234 2211–2217.Google Scholar
  148. Robertson, S. P., Potter, J. P., and Rouslin, W. (1982).J. Biol. Chem. 257 1743–1748.Google Scholar
  149. Rooney, T. A., Sass, E. J., and Thomas, A. P. (1989).J. Biol. Chem. 264 17131–17141.Google Scholar
  150. Rutter, G. A., and Denton, R. M. (1988).Biochem. J. 252 181–189.Google Scholar
  151. Safer, B., Smith, C. M., and Williamson, J. R. (1971).J. Mol. Cell. Cardiol. 2 111–124.Google Scholar
  152. Sanchez-Bueno, A., Dixon, C. J., Woods, N. M., Cuthbertson, K. S. R., and Cobbold, P. H. (1990).Biochem. J. 268 627–632.Google Scholar
  153. Scalou, M., Williams, D. A., and Fay, F. S., (1987).J. Biol. Chem. 262 6308–6312.Google Scholar
  154. Schaffer, W. T., and Olson, M. S. (1980).Biochem. J. 192 741–751.Google Scholar
  155. Scrutton, M. C., and White, M. D. (1974).J. Biol. Chem. 249 5405–5415.Google Scholar
  156. Siess, E. A., Brocks, D. G., Lattke, H. K., and Wieland, O. H. (1977).Biochem. J. 166 225–235.Google Scholar
  157. Siess, E. A., Brocks, D. G., and Wieland, O. H. (1978).Biochem. Soc. Trans. 6 1139–1144.Google Scholar
  158. Sistare, F. D., Picking, R. A., and Haynes, R. C. (1985).J. Biol. Chem. 260 12744–12747.Google Scholar
  159. Smith, C. M., Bryla, J., and Williamson, J. R. (1974).J. Biol. Chem. 249 1497–1505.Google Scholar
  160. Soboll, S., and Scholz, R. (1986)FEBS Lett. 205 109–112.Google Scholar
  161. Somlyo, A. P., and Bond, M., and Somlyo, A. V. (1985).Nature (London)314 622–625.Google Scholar
  162. Spurgeon, H. A., Stern, M. D., Baartz, G., Raffaeli, S., Hansford, R. G., Talo, A., Lakatta, E. G., and Capogrossi, M. C. (1990).Am. J. Physiol. 258 H574-H586.Google Scholar
  163. Staddon, J. M., and Hansford, R. G. (1986).Biochem. J. 238 737–743.Google Scholar
  164. Staddon, J. M., and Hansford, R. G. (1987).Biochem. J. 241 729–735.Google Scholar
  165. Staddon, J. M., and McGivan, J. D. (1984).Biochem. J. 217 477–483.Google Scholar
  166. Staddon, J. M., and McGivan, J. D. (1985).Biochem. J. 225 327–333.Google Scholar
  167. Starnes, J. W., Wilson, D. F., and Ericińska, M. (1985).Am. J. Physiol. 249 H799-H806.Google Scholar
  168. Strzelecki, T., Strzelecka, D., Koch, C. D., and LaNoue, K. F. (1988).Arch. Biochem. Biophys. 264 310–320.Google Scholar
  169. Sugano, T., Shiota, M., Khono, H., Shimada, M., and Oshino, N. (1980).J. Biochem. (Tokyo).87 465–472.Google Scholar
  170. Taylor, W. M., Reinhart, P. M., and Bygrave, F. L. (1983).Biochem. J. 212 555–565.Google Scholar
  171. Taylor, W. M., Van de Pol, E., and Bygrave, F. L. (1986).Biochem. J. 233 312–324.Google Scholar
  172. Teague, W. M., Pettit, F. H., Wu, T.-L., Silberman, S. R., and Reed, L. J. (1982).Biochemistry 21 5585–5592.Google Scholar
  173. Thomas, A. P., Alexander, J., and Williamson, J. R. (1984).J. Biol. Chem. 259 5574–5583.Google Scholar
  174. Titheradge, M. A., and Haynes, R. C. (1980).Arch. Biochem. Biophys. 201 44–55.Google Scholar
  175. Tsacopoulos, M., Orkand, R. K., Coles, J. A., Levy, S., and Poitry, S. (1983)Nature (London)301 604–606.Google Scholar
  176. Turk, J., Wolf, B. A. and McDaniel, M. L. (1987).Prog. Lipid. Res. 26 125–181.Google Scholar
  177. Unitt, J. F., McCormack, J. G., Reid, D., Maclachlan, L. K., and England, P. J. (1989).Biochem. J. 262 293–301.Google Scholar
  178. van der Meer, R., Akerboom, T. P. M., Groen, A. K., and Tager, J. M. (1978).Eur. J. Biochem. 84 421–428.Google Scholar
  179. Wan, B., LaNoue, K. F., Cheung, J. Y., and Scaduto, R. C., Jr., (1989).J. Biol. Chem. 264 13430–13439.Google Scholar
  180. Wanders, R. J., Van den Berg, G. B., and Tager, J. M. (1984).Biochim. Biophys. Acta 767 113–119.Google Scholar
  181. Wendt-Gallitelli, M. F., and Isenberg, G. (1991).J. Physiol. (London)435 349–372.Google Scholar
  182. Wernette, M. E., Ochs, R. S., and Lardy, H. A. (1981)J. Biol. Chem. 256 12767–12771.Google Scholar
  183. Wieland, O. H. (1983).Rev. Physiol. Biochem. Pharmacol. 96 123–170.Google Scholar
  184. Williford, D. J., Sharma, V. K., Korth, M., and Sheu, S.-S. (1990).Circ. Res. 66 234–241.Google Scholar
  185. Wollheim, C. B., and Sharp, G. W. G. (1981).Physiol. Rev. 61 914–973.Google Scholar
  186. Woods, N. M., Cuthbertson, K. S. R., and Cobbold, P. H. (1986).Nature (London)319 600–602.Google Scholar
  187. Yamada, E. W., and Huzel, N. J. (1985).Cell Calcium 6 469–479.Google Scholar
  188. Yamada, E. W., and Huzel, N. J. (1988).J. Biol. Chem. 263 11498–11503.Google Scholar
  189. Yamada, E. W., Shiffman, F. H., and Huzel, N. J. (1980).J. Biol. Chem. 255 267–273.Google Scholar
  190. Zoratti, M., Favaron, M., Pietrobon, D., and Azzone, G. F. (1986).Biochemistry 25 760–767.Google Scholar

Copyright information

© Plenum Publishing Corporation 1991

Authors and Affiliations

  • Richard G. Hansford
    • 1
  1. 1.Laboratory of Cardiovascular Science, Gerontology Research CenterNational Institute on AgingBaltimore

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