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Subcellular distributions of calcium/calmodulin-stimulated and guanine nucleotide-regulated adenylate cyclase activities in the cerebral cortex

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Abstract

The subcellular distribution of Ca2+/calmodulin-stimulated adenylate cyclase activity was studied in comparison with that of guanine nucleotide-stimulated cyclase activity. The distributions of these activities were similar among the crude fractions but differed among the purified subsynaptosomal fractions. The specific activity of Ca2+/calmodulin-stimulated cyclase was highest in a light synaptic membrane fraction, which has few, if any, postsynaptic densities, whereas that of guanine nucleotide-stimulated cyclase was highest in a heavier synaptic membrane fraction rich in postsynaptic densities. These results suggest that the Ca2+/calmodulin-stimulated cyclase has, at least in part, a different cellular or subcellular location than the guanine nucleotide-stimulated cyclase.

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Abbreviations

CaM:

calmodulin

GppNHp:

guanosine 5′-(β,γ-imino) triphosphate

References

  1. Rodbell, M. 1980. The role of hormone receptors and GTP-regulatory proteins in membrane transduction. Nature 284:17–22.

    PubMed  Google Scholar 

  2. Ross, E. M., andGilman, A. G. 1980. Biochemical properties of hormone-sensitive adenylate cyclase. Ann. Rev. Biochem. 49:533–564.

    PubMed  Google Scholar 

  3. Jakobs, K. H., Aktories, K., andSchultz, G. 1981. Inhibition of adenylate cyclase by hormones and neurotransmitters. Adv. Cyclic Nucleotide Res. 14:173–187.

    PubMed  Google Scholar 

  4. Londos, C., Cooper, D. M. F., andRodbell, M. 1981. Receptor-mediated stimulation and inhibition of adenylate cyclases: the fat cell as a model system. Adv. Cyclic Nucleotide Res. 14:163–171.

    PubMed  Google Scholar 

  5. Cooper, D. M. F. 1982. Bimodal regulation of adenylate cyclase. FEBS Lett. 138:157–163.

    PubMed  Google Scholar 

  6. Pfeuffer, T. 1977. GTP-binding proteins in membranes and the control of adenylate cyclase activity. J. Biol. Chem. 252:7224–7234.

    PubMed  Google Scholar 

  7. Northup, J. K., Sternweis, P. C., Smigel, M. D., Schleifer, L. S., Ross, E. M., andGilman, A. G. 1980. Purification of the regulatory component of adenylate cyclase. Proc. Natl. Acad. Sci. USA 77:6516–6520.

    PubMed  Google Scholar 

  8. Sternweis, P. C., Northup, J. K., Smigel, M. D., andGilman, A. G. 1981. The regulatory component of adenylate cyclase. Purification and properties. J. Biol. Chem. 256:11517–11526.

    PubMed  Google Scholar 

  9. Hanski, E., Sternweis, P. C., Northup, J. K., Dromerick, A. W., andGilman, A. G., 1981. The regulatory component of adenylate cyclase. Purification and properties of the turkey erythrocyte protein. J. Biol. Chem. 256:12911–12919.

    PubMed  Google Scholar 

  10. Katada, T., andUi, M. 1982. ADP ribosylation of the specific membrane protein of C6 cells by islet-activating protein associated with modification of adenylate cyclase activity. J. Biol. Chem. 257:7210–7216.

    PubMed  Google Scholar 

  11. Bokoch, G. M., Katada, T., Northup, J. K., Hewlett, E. L., andGilman, A. G. 1983. Identification of the predominant substrate for ADP-ribosylation by islet activating protein. J. Biol. Chem. 258:2072–2075.

    PubMed  Google Scholar 

  12. Codina, J., Hildebrandt, J., Iyengar, R., Birnbaumer, L., Sekura, R. D., andManclark, C. R. 1983. Pertussis toxin substrate, the putative Ni component of adenylyl cyclases, is an αβ heterodimer regulated by guanine nucleotide and magnesium. Proc. Natl. Acad. Sci. USA 80:4276–4280.

    PubMed  Google Scholar 

  13. Brostrom, C. O., Huang, Y.-C., Breckenridge, B. M., andWolff, D. 1975. Identification of a calcium-binding protein as a calcium-dependent regulator of brain adenylate cyclase. Proc. Natl. Acad. Sci. USA 72:64–68.

    PubMed  Google Scholar 

  14. Cheung, W. Y., Bradham, L. S., Lynch, J. J., Lin, Y. M., andTallant, E. A. 1975. Protein activator of cyclic 3′:5′-nucleotide phosphodiesterase of bovine or rat brain also activates its adenylate cyclase. Biochem. Biophys. Res. Comm. 66:1055–1062.

    PubMed  Google Scholar 

  15. Salter, R. S., Krinks, M. H., Klee, C. B., andNeer, E. J. 1981. Calmodulin activates the isolated catalytic unit of brain adenylate cyclase. J. Biol. Chem. 256:9830–9833.

    PubMed  Google Scholar 

  16. Bitonti, A. J., Moss, J., Hjelmeland, L., andVaughn, M. 1982. Resolution and activity of adenylate cyclase components in a Zwitter-ionic cholate derivative [3-[(3-cholamidopropyl)dimethylammonio]-1-propanesulfonate]. Biochemistry 21:3650–3653.

    PubMed  Google Scholar 

  17. Andreasen, T. J., Heideman, W., Rosenberg, G. B., andStorm, D. R. 1983. Photoaffinity labeling of brain adenylate cyclase preparations with azido [125I] iodo calmodulin. Biochemistry 22:2757–2762.

    PubMed  Google Scholar 

  18. Heideman, W., Wierman, B. M., andStorm, D. R. 1982. GTP is not required for calmodulin stimulation of bovine brain adenylate cyclase. Proc. Natl. Acad. Sci. USA 79:1462–1465.

    PubMed  Google Scholar 

  19. Seamon, K. B., andDaly, J. W. 1982. Calmodulin stimulation of adenylate cyclase in rat brain membranes does not require GTP. Life Sci. 30:1457–1464.

    PubMed  Google Scholar 

  20. Westcott, K. R., LaPorte, D. C., andStorm, D. R. 1979. Resolution of adenylate cyclase sensitive and insensitive to Ca2+ and calcium-dependent regulatory protein (CDR) by CDR-Sepharose affinity chromatography. Proc. Natl. Acad. Sci. USA 76:204–208.

    PubMed  Google Scholar 

  21. Sano, M., andDrummond, G. I. 1981. Properties of detergent-dispersed adenylate cyclase from cerebral cortex. Presence of an inhibitor protein. J. Neurochem. 37:558–566.

    PubMed  Google Scholar 

  22. Brostrom, M. A., Brostrom, C. O., andWolff, D. J. 1978. Calcium-dependent adenylate cyclase from rat cerebral cortex: activation by guanine nucleotides. Arch. Biochem. Biophys. 191:341–350.

    PubMed  Google Scholar 

  23. Treisman, G. J., Bagley, S., andGnegy, M. E. 1983. Calmodulin-sensitive and calmodulin-insensitive components of adenylate cyclase activity in rat striatum have differential responsiveness to guanyl nucleotides. J. Neurochem. 41:1398–1406.

    PubMed  Google Scholar 

  24. Ueda, T., Greengard, P., Berzins, K., Cohen, R. S., Blomberg, F., Grab, D. J., andSiekevitz, P. 1979. Subcellular distribution in cerebral cortex of two proteins phosphorylated by a cAMP-dependent protein kinase. J. Cell Biol. 83:308–319.

    PubMed  Google Scholar 

  25. Salomon, Y., Londos, C., andRodbell, M. 1974. A highly sensitive adenylate cyclase assay. Anal. Biochem. 58:541–548.

    PubMed  Google Scholar 

  26. Lowry, O. H., Rosebrough, N. J., Farr, A. L., andRandall, R. J. 1951. Protein measurements with the folin phenol reagent. J. Biol. Chem. 193:265–275.

    PubMed  Google Scholar 

  27. Fabiato, A., andFabiato, F. 1979. Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J. Physiol. (Paris) 75:463–505.

    Google Scholar 

  28. Whittaker, V. P., Michaelson, I. A., andKirkland, R. J. A. 1964. The separation of synaptic vesicles from nerve ending particles (“synaptosomes”). Biochem. J. 90:293–303.

    PubMed  Google Scholar 

  29. De Robertis, E., Rodriguez de Lores Arnaiz, G., Alberici, M., Butcher, R. W., andSutherland, E. W. 1967. Subcellular distribution of adenyl cyclase and cyclic phosphodiesterase in rat brain cortex. J. Biol. Chem. 242:3487–3493.

    Google Scholar 

  30. Clement-Cormier, Y. C., Parrish, R. G., Petzold, G. L., Kebabian, J. W., andGreengard, P. 1975. Characterization of a dopamine-sensitive adenylate cyclase in the rat caudate nucleus. J. Neurochem. 25:143–149.

    PubMed  Google Scholar 

  31. Rodriguez de Lores Arnaiz, G., Alberici, M., andDe Robertis, E. 1967. Ultrastructural and enzymic studies of cholinergic and noncholinergic synaptic membranes isolated from brain cortex. J. Neurochem. 14:215–225.

    PubMed  Google Scholar 

  32. Cotman, C. W., Banker, G., Churchill, L., andTaylor, D. 1974. Isolation of postsynaptic densities from rat brain. J. Cell Biol. 63:441–455.

    PubMed  Google Scholar 

  33. Morgan, I. G., Wolfe, L. S., Mandel, P., andGombos, G. 1971. Isolation of plasma membranes from rat brain. Biochim. Biophys. Acta 241:737–751.

    PubMed  Google Scholar 

  34. Gurd, J. W., Jones, L. R., Mahler, H. R., andMoore, W. J. 1974. Isolation and partial characterization of rat brain synaptic plasma membranes. J. Neurochem. 22:281–290.

    PubMed  Google Scholar 

  35. Sorenson, R. G., andMahler, H. R. 1982. Localization of endogenous ATPases at the nerve terminal. J. Bioenerg. Biomembr. 14:257–277.

    Google Scholar 

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Author notes

  1. Shirley T. Bissen

    Present address: Department of Zoology, University of California, 94720, Berkeley, CA

Authors and Affiliations

  1. Department of Pharmacology, The University of Michigan, 48109, Ann Arbor, Michigan

    Shirley T. Bissen & Tetsufumi Ueda

  2. Department of Psychiatry, The University of Michigan, 48109, Ann Arbor, Michigan

    Tetsufumi Ueda

  3. Mental Health Research Institute, The University of Michigan, 48109, Ann Arbor, Michigan

    Tetsufumi Ueda

Authors
  1. Shirley T. Bissen
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  2. Tetsufumi Ueda
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Bissen, S.T., Ueda, T. Subcellular distributions of calcium/calmodulin-stimulated and guanine nucleotide-regulated adenylate cyclase activities in the cerebral cortex. Neurochem Res 11, 453–463 (1986). https://doi.org/10.1007/BF00965018

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  • DOI: https://doi.org/10.1007/BF00965018

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