Regulation of Calcium Signalling in Cells

  • Ernesto Carafoli

Abstract

Ca controls numerous cellular functions (see Carafoli, 1987, for a comprehensive review). Its signalling role demands its maintenance within cells at a very low free concentration; thus, mechanisms exist to modulate it in the cell domains where the Ca-sensitive targets are located. To achieve this, evolution has selected the reversible complexation by proteins, which are either soluble, organized in non-membranous structures, or intrinsic to membranes: they complex intracellular Ca from concentrations which are about 10,000 fold lower than in the external spaces. The Ca controlling function of the plasma membrane is based on the operation of membrane-intrinsic Ca transporting proteins, and is responsible for the long-term maintenance of the Ca gradient between cells and the extracellular space. The large inwardly directed Ca gradient maintained by the plasma membrane transporters ensures that even minor changes in the Ca permeability of the plasma membrane will produce significant swings in its intracellular concentration, and thus in turn efficiently modulate its signalling function.

Keywords

Sarcoplasmic Reticulum Calcium Signalling Myosin Light Chain Kinase Plasmic Reticulum Calcium Pump 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Babu, Y.S., Sack, J.S., Greenhough, T.J., Bugg, C.E., Means, A.R., & Cook, W.J. (1985). Three-dimensional structure of calmodulin. Nature, 315: 37–40.PubMedCrossRefGoogle Scholar
  2. Barton, G.J., Newman, R.H., Freemont, P.S., & Crumpton, M.J. (1991). Amino acid sequence analysis of the annexin super-gene family of proteins. Eur. J. Biochem., 198: 749–760.PubMedCrossRefGoogle Scholar
  3. Berridge, M.J. (1993). Inositol trisphosphate and calcium signalling. Nature, 361: 315–325.PubMedCrossRefGoogle Scholar
  4. Bewley, M.C., Bonstead, C.M., Walker, J.H., Waller, D.A., & Huber, R. (1993). Structure of chicken annexin Va at 2.25-A resolution. Biochemistry, 32: 3923–3929.PubMedCrossRefGoogle Scholar
  5. Carafoli, E. (1979). The calcium cycle of mitochondria. FEBS Letts., 104: 1–5.CrossRefGoogle Scholar
  6. Carafoli, E. (1982). The transport of calcium across the inner membrane of mitochondria. In Membrane Transport of Calcium. Edited by Carafoli E. London: Academic Press, 109–139.Google Scholar
  7. Carafoli, E. (1987). Intracellular calcium homeostasis Ann. Rev. Biochem., 56: 395–433.PubMedCrossRefGoogle Scholar
  8. Carafoli, E. (1991). Calcium pump of the plasma membrane. Physiol. Rev., 71: 129–153.PubMedGoogle Scholar
  9. Carafoli, E. (1992). The Cat’ pump of the plasma membrane. J. Biol. Chem., 267: 2115–2118.PubMedGoogle Scholar
  10. Carafoli, E., Tiozzo, G., Lugli, F., Crovetti, F., & Kratzing, C. (1974). The release of calcium from heart mitochondria by sodium. J. Molec. Cell. Cardiol., 6: 361–371.CrossRefGoogle Scholar
  11. Concha, N.O., Head, J.F., Kaetzel, M.A., Dedman, J.R., & Seaton, B.A. (1993). Rat annexin V crystal structure: Ca`’ induced conformational changes. Science, 261: 1321–1324.PubMedCrossRefGoogle Scholar
  12. Cornwell, T.L., Prywantky, K.B., Wyatt, T.A., & Lincoln, T.M. (1991). Regulation of sarcoplasmic reticulum protein kinase phosphorylation by localized c-GMP-dependent protein kinase in vascular smooth muscle cells. Mol. Pharmacol., 40: 923–931PubMedGoogle Scholar
  13. Crompton, M., Sigel, E., Salzmann, M., & Carafoli, E. (1976). A kinetic study of energy-linked influx of Ca“ into heart mitochondria. Eur. J. Biochem., 69: 429–434.CrossRefGoogle Scholar
  14. Crumpton, M.J., & Dedman, J.R. (1990). Protein terminology tangle. Nature, 345: 212.PubMedCrossRefGoogle Scholar
  15. Fabiato, A., & Fabiato, F. (1975). Contractions induced by a calcium triggered release of calcium from the sarcoplasmic reticulum of single skinned cardiac cells. J. Physiol., 249: 469–495.PubMedGoogle Scholar
  16. Fleckenstein, A. (1973). Calcium antagonism in heart and smooth muscle. John Wiley, New York.Google Scholar
  17. Furuichi, T., Yoshikawa, S., Miyawaki, A., Wada, K., Maeda, N., & Mikoshiba, K. (1989). Primary structure and functional expression of the inositol 1,4,5-triphosphate-binding protein P400. Nature, 342: 32–38.PubMedCrossRefGoogle Scholar
  18. Galione, A. (1993). Cyclic ADPribose, a new way to control calcium. Science, 259: 325–328PubMedCrossRefGoogle Scholar
  19. Herzberg, O., & James, M.N.G. (1985). Structure of the calcium regulatory muscle protein troponin-C at 2.8. A resolution. Nature, 313: 653–659.Google Scholar
  20. Hofmann, F., Anagli, J., Carafoli, E., & Vorherr T. (1994). Phosphorylation of the calmodulin binding domain of the plasma membrane Ca2+ pump by protein kinase C reduces its interaction with calmodulin and with the receptor site in the pump. J. Biol. Chem. (in press).Google Scholar
  21. Hofmann, F., Biel, M.,& Flockerzi, V. (1994). Molecular basis for Ca2` channel diversity. Ann. Rev. Neuroscience, 17: 399–418.CrossRefGoogle Scholar
  22. Huber, R., Römisch, J., & Paques, E.P. (1990). The crystal and molecular structure of human annexin V, an anticoagulant protein that binds to calcium and membranes. EMBO J., 9: 3867–3874.PubMedGoogle Scholar
  23. Huber, R., Schneider. M., Mayr, I., Römisch, J., & Paques, E.P. (1990). The calcium binding sites in human annexin V by crystal structure analysis at 2.0 A resolution. FEBS Lett., 275: 15–21.Google Scholar
  24. Ikura, M., Marius, Clore, G., Gronenbom, A.M., Zhu, G.. Klee, C.B., & Bax, A. (1992). Solution structure of a calmodulin-target peptide complex by multidimensional NMR. Science, 256: 632–638.Google Scholar
  25. James, P., lnui, M., Tada, M., Chiesi, M., & Carafoli, E. (1989). Nature and site of phospholamban regulation of the Ca’* pump of sarcoplasmic reticulum. Nature, 342: 90–92.PubMedCrossRefGoogle Scholar
  26. Kofuii, P., Lederer, W.J., & Schulze, D.H. (1994). Mutually exclusive and cassette exons underlie alternatively spliced isoforms of the Na/Ca exchanger. J. Biol. Chem., 269: 5145–5149.Google Scholar
  27. Kretsinger, R.H., & Nockolds, C.E. (1973). Carp muscle calcium-binding protein. J. Biol. Chem., 248: 3313–3326.PubMedGoogle Scholar
  28. MacLennan, D.H. (1970). Purification and properties of an adenosine triphosphatase from sarcoplasmic reticulum. J. Biol. Chem., 245: 4508–4513.PubMedGoogle Scholar
  29. MacLennan, D.H., Brand!, C.J., Korczak, B., & Green, N.M. (1985). Amino acid sequence of a Ca2+ + Mg2+ dependent ATPase from rabbit muscle sarcoplasmic reticulum deduced from its complementary DNA sequence. Nature, 316: 696–700.PubMedCrossRefGoogle Scholar
  30. Matsuoka, S., Nicoll, D.A., Reilly, R.F., Hilgemann, D.W., & Philipson, K.D. (1993). Initial localization ofregula-tory regions of the cardiac sarcolemmal Na+-Ca“ exchanger. Proc. Nat. Acad. Sci. ( USA ), 90: 3870–3874.CrossRefGoogle Scholar
  31. Meador, W.E., Means, A.R.,& Quiocho, F.A. (1992). Target enzyme recognition by calmodulin: 2.4 Â structure of a calmodulin-peptide complex. Science, 257: 1251–1255.Google Scholar
  32. Nicoll, D.A., Longoni, S., & Philipson, K.D. (1990). Molecular cloning and functional expression of the cardiac sarcolemmal Na-Ca`exchanger. Science, 250: 562–565.PubMedCrossRefGoogle Scholar
  33. Reiländer, H., Achilles, A., Friedel, U., Maul, G., Lottspeich, F., & Cook, N.J. (1992). Primary structure and functional expression of the Na/Ca, K-exchanger from bovine rod photoreceptors. EMBO J.. I I: 1689–1695.Google Scholar
  34. Reuter, H. (1984). Ion channels in cardiac cell membranes. Ann. Rev. Physiol., 46: 473–484.Google Scholar
  35. Reuter, H., Stevens, C.F., Tsien, R.W., & Yellen, G. (1982), Properties of single calcium channels in cardiac cell culture. Nature, 297: 501–504.PubMedCrossRefGoogle Scholar
  36. Richter, C. (1992). Mitochondrial calcium transport. In: New Comprehensive Biochemistry. Edited by Neuberger A, Van Deenen LLM., Elsevier: Amsterdam, 349–358.Google Scholar
  37. Rosen, L.B., Ginty, D.D., & Greenberg, M.E. (1995), Calcium regulation of gene expression. Adv. Sec. Messengers and Phosphoprot. Res., 30: 225–253.Google Scholar
  38. Santella, L. (1996). The cell nucleus: an eldorado to future calcium research? J. Membr. Biol, in press.Google Scholar
  39. Shull, G.E., & Greeb, J. (1988). Molecular cloning of two isoforms of the plasma membrane Ca2+ transporting ATPase from rat brain. Structural and functional domains exhibit similarity to Na+, K+ and other cation transport ATPases. J. Biol. Chem., 263: 8646–8657.Google Scholar
  40. Stauffer, T., Hilfiker, H., Carafoli, E., & Strehler, E.E. (1993). Quantative analysis of alternative splicing options of human plasma membrane calcium pump genes. J. Biol. Chem., 268: 25993–26003.Google Scholar
  41. Streb, H., Irvine, R.F., Berridge, M.J., & Schulz, I. (1983). Release of Ca2+ from a non-mitochondrial intracellular store in pancreatic acinar cells by inositol-1.4,5-trisphosphate. Nature, 306: 66–69.CrossRefGoogle Scholar
  42. Szebenyi, D.M.E., Obendorf, S.K., & Moffat., K., (1981). Structure of vitamin D-dependent calcium binding protein from bovine intestine. Nature, 294: 327–332.PubMedCrossRefGoogle Scholar
  43. Tada, M., Kirchberger, M.A., & Katz, A.M. (1975). Phosphorylation of 22.000-Dalton component of the cardiac sarcoplasmic reticulum by adenosine 3“:5”-monophosphate-dependent protein kinase. J. Biol. Chem., 250: 2640–2647.Google Scholar
  44. Takeshima, H., Nishimura, S., Matsumoto, T., Ishida, H., Kangawa, K., Minamino, N., Matsuo, H., Ueda, M., Hanaoka, M., Hirose, T., & Numa, S. (1989). Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature, 339: 439–445.PubMedCrossRefGoogle Scholar
  45. Vaghy, P.L., Johnson, J.D., Matlib, M.A., Wang, T., & Schwarz, A. (1982). Selective inhibition of Na-induced Ca“ release from heart mitochondria by diltiazem and certain other Ca’. antagonist drugs. J. Biol. Chem., 257: 6000–66002.Google Scholar
  46. Verma, A.K., Filoteo, A.G., Stanford, D.R., Wieben, E.D., Penniston, J.T., Strehler, E.E., Fischer, R., Heim, R., Vogel, G., Mathews, S., Strehler-Page, M.A., James, P., Vorherr, T., Krebs, J., & Carafoli, E. (1988). Complete primary structure of a human plasma membrane Ca2+ pump. J. Biol. Chem., 263: 14152–14159.Google Scholar
  47. Weng, X., Luecke, H., Song, I.S., Kang, D.S., Kim, S.H., & Huber, R. (1993). Crystal structure of human annexin I at 2.5A resolution. Prot. Sci. 2: 448–458.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1997

Authors and Affiliations

  • Ernesto Carafoli
    • 1
  1. 1.Institute of BiochemistrySwiss Federal Institute of Technology (ETH)ZürichSwitzerland

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