Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Adenylate cyclase and membrane fluidity

The repressor hypothesis

  • 21 Accesses

  • 28 Citations

Summary

The relationships between membrane fluidity as induced by drug addition and the stimulation of adenylate cyclase by hormones (mainly catecholamines), GTP, Gpp(NH)p and NaF are reviewed. In particular, the data corresponding to pigeon erythrocyte membranes are reviewed and compared with other data published in the literature. A brief summary of the theories involved in fluidity measurements and their significance at the molecular level is also given for anisotropy of fluorescence and electron spin resonance.

One of the conclusions is that the cationic drugs and neutral alcohols by perturbing preferentially the inner half-layer of the bilayer induced in pigeon erythrocyte membrane correlated multiphasic changes on fluidity and adenylate cyclase activity.

This and other experimental data concerning the regulation of the adenylate cyclase are discussed in regard to a new interpretation of cyclase stimulation: the repressor hypothesis. In cell membrane the catalytic unit C is repressed by its association with a repressor complex made of the hormone receptor R and the regulatory protein N. The activation of cyclase activity is the dissociation of the catalytic unit C from the repressor complex R.N according to the equilibrium: R.N.C (inactive) ⇌ R.N + C (active). Hormones, metal ions (magnesium), and nucleotides (GTP) are the allosteric ligands which shift this equilibrium towards the dissociation. state with the liberation of the active form, membrane-bound, C unit. Gpp(NH)p, fluoride and forskolin will also shift the equilibrium toward the right. GDP and free receptors favour the associated repressed state of the system.

This is a preview of subscription content, log in to check access.

References

  1. 1.

    Davoren, P. R. and Sutherland, E. W., 1963. J. Biol. Chem. 238: 3016–3023.

  2. 2.

    Singer, S. J. and Nicolson, G., 1972. Science 175: 720–731.

  3. 3.

    Singer, S. J., 1974. Annu. Rev. Biochem. 43: 805–833.

  4. 4.

    Warren, G. B., Toon, P. A., Birdsall, N. J. M., Lee, A. G. and Metcalfe, J. C., 1974. Biochemistry 13: 5501–5507.

  5. 5.

    Warren, G. B., Houslay, M. D., Metcalfe, J. C. and Birdsall, N. J. M., 1975. Nature 255: 684–687.

  6. 6.

    Marcelja, S., 1976. Biochim. Biophys. Acta 455: 1–7.

  7. 7.

    Marsh, D., Watts, A., Maschke, W. and Knowles, P. F., 1978. Biochem. Biophys. Res. Commun. 81: 397–402.

  8. 8.

    Cornell, B. A., Sacre, M. M., Peel, W. E. and Chapman, D., 1978. FEBS Lett. 90: 29–35.

  9. 9.

    Owicki, J. C. and McConnell, H. M., 1979. Proc. Natl. Acad. Sci. U.S.A. 7: 4750–4754.

  10. 10.

    Rice, D. M., Hsung, J. C., King, T. E. and Oldfield, E., 1979. Biochemistry 18: 5885–5892.

  11. 11.

    Davoust, J., Bienvenue, A., Fellmann, P. and Devaux, P. F., 1980. Biochim. Biophys. Acta 596: 28–42.

  12. 12.

    Heyn, M. P., Cherry, R. J. and Dencher, N. A., 1981. Biochemistry 20: 840–849.

  13. 13.

    Taylor, M. G. and Smith, I. C. P., 1980. Biochim. Biophys. Acta 599: 140–149.

  14. 14.

    Demel, R. A., Bruckdorfer, K. R. and Van Deenen, L. L. M., 1972. Biochim. Biophys. Acta 255: 311–320.

  15. 15.

    Franks, N. P. and Lieb, W. R., 1979. J. Mol. Biol. 133: 469–500.

  16. 16.

    Ahmad, P. and Mellors, A., 1978. J. Membrane Biol. 41: 235–247.

  17. 17.

    Dahlen, B., 1979. Chem. Phys. Lipid 23: 179–188.

  18. 18.

    Oldfield, E. and Chapman, D., 1972. FEBS Lett. 23: 285–297.

  19. 19.

    Ito, T. and Onishi, S.I., 1974. Biochim. Biophys. Acta 352: 29–37.

  20. 20.

    Schnepel, G. H., Hegner, D. and Schummer, U., 1974. Biochim. Biophys. Acta 367: 67–74.

  21. 21.

    Hauser, H., Phillips, M. C. and Barratt, M. D., 1975. Biochim. Biophys. Acta 413: 341–353.

  22. 22.

    Schlessinger, J., Elson, E. L., Webb, W. W., Yakara, I., Rutishauser, U. and Edelman, M., 1977. Proc. Natl. Acad. Sci. U.S.A. 74: 1110–1114.

  23. 23.

    Koppel, D. E., Sheetz, M. P. and Schindler, M., 1981. Proc. Natl. Acad. Sci. U.S.A. 78: 3576–3580.

  24. 24.

    Seeman, P., 1972. Pharmacol. Rev. 24: 583–655.

  25. 25.

    Leterrier, F., 1978. In: Mises au point de Biochimie Pharmacologique, 2nd series, pp. 50–93. Masson, Paris.

  26. 26.

    Wolff, J. and Jones, A. B., 1970. Proc. Natl. Acad. Sci. U.S.A. 65: 454–459.

  27. 27.

    Rubalcava, B. and Rodbell, M., 1973. J. Biol. Chem. 248: 3831–3837.

  28. 28.

    Garnier, J. and Singer, S. J., 1977. In: Electrical Phenomena at the Biological Membrane Level (Roux, E., ed.), pp. 35–41. Elsevier, Amsterdam.

  29. 29.

    Deuticke, B., 1968. Biochim. Biophys. Acta 163: 494–500.

  30. 30.

    Sheetz, M. P. and Singer, S. J., 1974. Proc. Natl. Acad. Sci. U.S.A. 71: 4457–4461.

  31. 31.

    Sutherland, E. W., Rall, T. W. and Menon, T., 1962. J. Biol. Chem. 237: 1220–1227.

  32. 32.

    Frenzel, J., Arnold, K. and Nuhn, P., 1978. Biochim. Biophys. Acta 507: 185–197.

  33. 33.

    Boulanger, Y., Schreier, S. and Smith, I. C. P., 1981. Biochemistry 20: 6824–6830.

  34. 34.

    Low, P. S., Lloyd, D. H., Stein, T. M. and Rogers, J. A. III, 1979. J. Biol. Chem. 254: 4119–4125.

  35. 35.

    Yeagle, P. L., 1978. Acc. Chem. Res. 11: 321–327.

  36. 36.

    Breton, J., Viret, J. and Leterrier, F., 1977. Arch. Biochem. Biophys. 179: 625–633.

  37. 37.

    Neal, M. J., Butler, K. W., Polnaszek, C. F. and Smith, I. C. P., 1976. Mol. Pharmacol. 12: 144–155.

  38. 38.

    Pang, K.-Y. Y. and Miller, K. W., 1978. Biochim. Biophys. Acta 511: 1–9.

  39. 39.

    Leterrier, F., Rieger, F. and Mariaud, J.-F., 1974. Biochem. Pharmacol. 23: 103–113.

  40. 40.

    Leterrier, F., Mendyk, A. and Viret, J. 1976. Biochem. Pharmacol. 25: 2469–2474.

  41. 41.

    Chatelain, P., Reckinger, N. and Roncucci, R., 1979. Biochem. Pharmacol. 28: 3677–3680.

  42. 42.

    Ogiso, T., Kurobe, M., Masuda, H. and Kato, Y., 1977. Chem. Pharm. Bull. 25: 1078–1088.

  43. 43.

    Lahrichi, M., Houpert, Y., Tarallo, P., Loppinet, V. and Siest, G., 1977. Chem. Biol. Interactions 19: 173–183.

  44. 44.

    Nicolson, G. L. and Poste, G., 1976. J. Supramol. Struct. 5: 65–72.

  45. 45.

    Kornberg, R. D. and McConnell, H. M., 1971. Biochemistry 10: 1111–1120.

  46. 46.

    Sackmann, E., Traüble, H., Galla, H.-J. and Overath, P., 1973. Biochemistry 12: 5360–5369.

  47. 47.

    Mantulin, W. W. and Pownall, H. J., 1977. Photochem. Photobiol. 26: 69–73.

  48. 48.

    Dembo, M., Glushko, V., Aberlin, M. E. and Sonenberg, M., 1979. Biochim. Biophys. Acta 552: 201–211.

  49. 49.

    Roseman, M., Litman, B. J. and Thompson, T. E., 1975. Biochemistry 14: 4826–4830.

  50. 50.

    Poznansky, M. and Lange, Y., 1976. Nature 259: 420–421.

  51. 51.

    Bretscher, M. S., 1973. Science 181: 622–629.

  52. 52.

    Hirata, F., Strittmatter, W. J. and Axelrod, J., 1979. Proc. Natl. Acad. Sci. U.S.A. 76: 368–372.

  53. 53.

    Hare, F., Amiell, J. and Lussan, C., 1979. Biochim. Biophys. Acta 555: 388–408.

  54. 54.

    Smith, I. C. P., 1979. Can. J. Biochem. 57: 1–14.

  55. 55.

    Lakowicz, J. R. and Knutson, J. R., 1980. Biochemistry 19: 905–911.

  56. 56.

    Salesse, R., Brochon, J.-C. and Garnier, J., 1981. Biochimie 63: 915–920.

  57. 57.

    Vincent, M., De Foresta, B., Gallay, J. and Alfsen, A., 1982. Biochemistry 21: 708–716.

  58. 58.

    Griffith, O. H. and Jost, P. C., 1976. In: Spin Labeling (Berliner, E., ed.), pp. 453–523. Academic Press, New York.

  59. 59.

    Schreier, S., Polnaszek, C. F. and Smith, I. C. P., 1978. Biochim. Biophys. Acta 515: 395–436.

  60. 60.

    Pesce, A. J., Rosen, C.-G. and Pasby, T. L., 1971. Fluorescence Spectroscopy. Marcel Dekker, New York.

  61. 61.

    Kano, K. and Fendler, J. H., 1979. Chem. Phys. Lipid 23: 189–200.

  62. 62.

    Johansson, L. B.-A. and Lindblom, G., 1980. Quart. Rev. Biophys. 13: 63–118.

  63. 63.

    Shinitzky, M. and Yuli, I., 1982. Chem. Phys. Lipid 30: 261–282.

  64. 64.

    Shinitzky, M. and Barenholz, Y., 1978. Biochim. Biophys. Acta 515: 367–394.

  65. 65.

    Perrin, F., 1926. J. Phys. Rad. 7: 390.

  66. 66.

    Kinosita, K. Jr., Kawato, S. and Ikegami, A., 1977. Biophys. J. 20: 289–305.

  67. 67.

    Jahnig, F., 1979. Proc. Natl. Acad. Sci. U.S.A. 76: 6361–6365.

  68. 68.

    Berliner, L. J., 1976. Spin Labeling. Academic Press, New York.

  69. 69.

    Seelig, J., 1970. J. Am. Chem. Soc. 92: 3881–3887.

  70. 70.

    Hubbell, W. L. and McConnell, H. M., J. Am. Chem. Soc. 93: 314–326.

  71. 71.

    Gordon, L. M., Sauerheber, R. D., Esgate, J. A., Dipple, I., Marchmont, R. J. and Houslay, M. D., 1980. J. Biol. Chem. 255: 4519–4527.

  72. 72.

    Salesse, R., Garnier, J., Leterrier, F., Daveloose, D. and Viret, J., 1982. Biochemistry 21: 1581–1586.

  73. 73.

    Rodbell, M., Lad, P. M., Nielsen, T. B., Cooper, D. M. F., Schlegel, W., Preston, M. S., Londos, C. and Kempner, E. S., 1981. Adv. Cyclic Nucl. Res. 14: 3–14.

  74. 74.

    Haga, T., Haga, K. and Gilman, A. G., 1977. J. Biol. Chem. 252: 5776–5782.

  75. 75.

    Hanski, E., Sternweis, P. C., Northup, J. K., Dromerick, A. W. and Gilman, A. G., 1981. J. Biol. Chem. 256: 12911–12919.

  76. 76.

    Maguire, M. E., Wiklund, R. A., Anderson, J. M. and Gilman, A. G., 1976. J. Biol. Chem. 251: 1221–1231.

  77. 77.

    Stengel, D., Guenet, L. and Hanoune, J., 1982. J. Biol. Chem. 257: 10818–10886.

  78. 78.

    Atlas, D. and Levitzki, A., 1978. Nature 272: 370–371.

  79. 79.

    Strosberg, A. D., Vauquelin, G., Durieu, O., Klutchko, C., Bottari, S. and André, C., 1980. Trends Biochem. Sci. 5: 11–14.

  80. 80.

    Pfeuffer, T. and Helmreich, J. M., 1975. J. Biol. Chem. 250: 867–876.

  81. 81.

    Pfeuffer, T., 1977. J. Biol. Chem. 252: 7224–7234.

  82. 82.

    Cassel, D., Levkowitz, H. and Selinger, Z., 1977. J. Cyclic Nucl. Res. 3: 393–406.

  83. 83.

    Rodbell, M., 1980. Nature 284: 17–22.

  84. 84.

    Northup, J. K., Sternweiss, P. C., Smigel, M. P., Schleifer, L. S., Ross, E. M. and Gilman, A. G., 1980. Proc. Natl. Acad. Sci. U.S.A. 77: 6516–6520.

  85. 85.

    Bottari, S., Vauquelin, G., Durieu, O., Klutchko, C. and Strosberg, A. D., 1979. Biochem. Biophys. Res. Commun. 86: 1311–1318.

  86. 86.

    Vauquelin, G., Bottari, S., Kanarek, L. and Strosberg, A. D., 1979. J. Biol. Chem. 254: 4462–4469.

  87. 87.

    Pike, L. J. and Lefkowitz, R. J., 1980. J. Biol. Chem. 255: 6860–6867.

  88. 88.

    Cassel, D. and Selinger, Z., 1977. Proc. Natl. Acad. Sci. U.S.A. 74: 3307–3311.

  89. 89.

    Citri, Y. and Schramm, M., 1980. Nature 287: 297–300.

  90. 90.

    Cassel, D. and Selinger, Z., 1976. Biochim. Biophys. Acta 452: 538–551.

  91. 91.

    Cassel, D. and Selinger, Z., 1977. Biochem. Biophys. Res. Common. 77: 868–873.

  92. 92.

    Iyengar, R. and Birnbaumer, L., 1982. Proc. Natl. Acad. Sci. U.S.A. 79: 5179–5183.

  93. 93.

    Rodbell, M., Krans, H. M. J., Pohl, S. L. and Birnbaumer, L., 1971. J. Biol. Chem. 246: 1872–1876.

  94. 94.

    Cassel, D. and Pfeuffer, T., 1978. Proc. Natl. Acad. Sci. U.S.A. 75: 2669–2673.

  95. 95.

    Rodbell, M., Lin, M. C. and Salomon, Y., 1974. J. Biol. Chem. 249: 59–65.

  96. 96.

    Lin, M. C., Nicosia, S., Lad, P. M. and Rodbell, M., 1977. J. Biol. Chem. 252: 2790–2792.

  97. 97.

    Maguire, M. E., Van Arsdale, P. M. and Gilman, A. G., 1976. Mol. Pharmacol. 12: 335–339.

  98. 98.

    Mukherjee, C. and Lefkowitz, R. J., 1977. Mol. Pharmacol. 13: 291–303.

  99. 99.

    Ross, E. M., Maguire, M. E., Sturgill, T. W., Biltonen, R. L. and Gilman, A. G., 1977. J. Biol. Chem. 252: 5761–5775.

  100. 100.

    Williams, L. T. and Lefkowitz, R. J., 1977. J. Biol. Chem. 252: 7207–7213.

  101. 101.

    Sternweis, P. C. and Gilman, A. G., 1979. J. Biol. Chem. 254: 3334–3340.

  102. 102.

    Lin, M. C., Welton, A. F. and Berman, M. F., 1978. J. Cyclic Nucl. Res. 4: 159–168.

  103. 103.

    Stadel, J. M., De Lean, A. and Lefkowitz, R. J., 1980. J. Biol. Chem. 255: 1436–1414.

  104. 104.

    Iyengar, R. and Birnbaumer, L., 1981. J. Biol. Chem. 256: 11036–11041.

  105. 105.

    Iyengar, R., 1981. J. Biol. Chem. 256: 11042–11050.

  106. 106.

    Limbird, L. E., Hickey, A. R. and Lefkowitz, R. J., 1979. J. Biol. Chem. 254: 2677–2683.

  107. 107.

    Ross, E. M., Howlett, A. C., Ferguson, K. M. and Gilman, A. G., 1978. J. Biol. Chem. 253: 6401–6412.

  108. 108.

    Stengel,, Guenet, L., Desmier, M., Insel, P. and Hanoune, J., 1982. Mol. Cell. Endocrinol. 28: 681–690.

  109. 109.

    Yamamura, H., Lad, P. M. and Rodbell, M., 1977. J. Biol. Chem. 252: 7964–7966.

  110. 110.

    Cooper, D. M. F., Schlegel, W., Lin, M. C. and Rodbell, M., 1979. J. Biol. Chem. 254: 8927–8931.

  111. 111.

    Katada, T. and Ui, M., 1980. J. Biol. Chem. 255: 9580–9588.

  112. 112.

    Garcia-Sociuz, J. A., 1981. FEBS Lett. 126: 306–308.

  113. 113.

    Hareki, O. and Ui, M., 1981. J. Biol. Chem. 256: 2856–2862.

  114. 114.

    Katada, T. and Ui, M., 1981. J. Biol. Chem. 256: 8310–8317.

  115. 115.

    Cronin, M. J., Myers, G. A., Dabury, L. G. and Hewlett, E. L., 1982. Proc. 64th Meet. Endue. Soc., pp. A857.

  116. 116.

    Katada, T. and Ui, M., 1982. Proc. Natl. Acad. Sci. U.S.A. 79:3129–3133.

  117. 117.

    Hildebrandt, J. D., Sekura, R. D., Codina, J., Iyengar, R., Manclark, C. R. and Birnbaumer, L., 1983. Nature 302: 706–709.

  118. 118.

    Puchwein, G., Pfeuffer, T. and Helmreich, E. J. M., 1974. J. Biol. Chem. 249: 3232–3240.

  119. 119.

    Triner, L., Vulliemoz, Y. and Verosky, M., 1977. Mol. Pharmacoll. 13: 976–979.

  120. 120.

    Karobath, M. and Leitich, H., 1974. Proc. Natl. Acad. Sci. U.S.A. 71:2915–2918.

  121. 121.

    Anderson, W. B. and Jaworski, C. J., 1977. Arch. Biochem. Biophys. 180: 374–383.

  122. 122.

    Vesin, M.-F., Do Khac, L. and Harbon, S., 1977. Mol. Pharmacol. 23: 24–37.

  123. 123.

    Orly, J. and Schramm, M., 1975. Proc. Natl. Acad. Sci. U.S.A. 72: 3433–3437.

  124. 124.

    Hanski, E., Rimon, G. and Levitzki, A., 1979. Biochemistry 18: 846–853.

  125. 125.

    Houslay, M. D., Dipple, J. and Gordon, L. M., 1981. Biochem. J. 197: 675–681.

  126. 126.

    Salesse, R. and Garnier, J., 1979. Biochim. Biophys. Acta 554: 102–113.

  127. 127.

    Lin, M. C., Lin, C. S. and Whitlock, J. P., 1979. J. Biol. Chem. 254: 4684–4688.

  128. 128.

    Salesse, R., Garnier, J. and Daveloose, D., 1982. Biochemistry 21: 1584–1590.

  129. 129.

    Sandermann, H. Jr., 1978. Biochim. Biophys. Acta 515: 209–237.

  130. 130.

    Jones, G. L. and Woodbury, D. M., 1978. J. Pharmacol. Exp. Ther. 207: 203–211.

  131. 131.

    Lee, A. G., 1977. Mol. Pharmacol. 13: 474–487.

  132. 132.

    Dipple, I. and Houslay, M. D., 1979. FEBS Lett. 106: 21–24.

  133. 133.

    Houslay, M. D. and Gordon, L. M., 1983. Curr. Top. Membrane Transp. 18: 179–231.

  134. 134.

    Rimon, G., Hanski, E., Braun, S. and Levitzki, A., 1978. Nature 76: 394–396.

  135. 135.

    Tolkovski, A. M. and Levitzki, A., 1978. Biochemistry 17: 3795–3810.

  136. 136.

    Sinensky, M., Minneman, K. P. and Molinoff, P. B., 1979. J. Biol. Chem. 254: 9135–9141.

  137. 137.

    McMurphie, E. J. and Raison, J. K., 1979. Biochim. Biophys. Acta 554: 364–374.

  138. 138.

    Borochov, H. and Shinitzky, M., 1976. Proc. Natl. Acad. Sci. U.S.A. 73: 4526–4530.

  139. 139.

    Armond, P. A. and Staehelin, L. A., 1979. Proc. Natl. Acad. Sci. U.S.A. 76: 1901–1905.

  140. 140.

    Levitzki, A. and Helmreich, J. M., 1979. FEBS Lett. 101: 213–219.

  141. 141.

    Bakardjeeva, A., Galla, H. J. and Helmreich, E. J. M., 1979. Biochemistry 18: 3016–3023.

  142. 142.

    Sheetz, M. P. and Singer, S. J., 1976. J. Cell. Biol. 70: 247–251.

  143. 143.

    Elferink, J. G. R., 1977. Biochem. Pharmacol. 26: 2411–2416.

  144. 144.

    Houslay, M. D. and Palmer, R. W., 1978. Biochem. J. 174: 909–919.

  145. 145.

    Ferguson, K. M., Northup, J. K. and Gilman, A. G., 1982. Fed. Proc., 41: 1407–1407.

  146. 146.

    Schlegel, W., Kempner, E. S. and Rodbell, M., 1979. J. Biol. Chem. 254: 5168–5176.

  147. 147.

    Howlett, A. C. and Gilman, A. G., 1980. J. Biol. Chem. 255: 2861–2866.

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Salesse, R., Garnier, J. Adenylate cyclase and membrane fluidity. Mol Cell Biochem 60, 17–31 (1984). https://doi.org/10.1007/BF00226298

Download citation

Keywords

  • Fluoride
  • Electron Spin Resonance
  • Catecholamine
  • Hormone Receptor
  • Adenylate Cyclase