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The Calcium-Activated Photoprotein Obelin—Effects of Calcium and Strontium and Its Use in the Measurement of Intracellular Ionized Calcium

  • Anthony K. Campbell
  • Robert L. Dormer

Abstract

It is now nearly one hundred years since the experiments of Ringer (1) showed that Sr2+ could replace extracellular Ca2+ and allow contraction of frog heart to take place. During the time that has elasped since these experiments were carried out not only has the role of Ca2+ in muscle contraction been well defined (2,3), but there has also been increasing evidence for an important role for Ca2+ in hormone action and secretion (4–6). In order to define the role of Ca2+ in a control process five principal approaches have been adopted, involving five distinct questions (Table 1). The first four of these approaches have provided some indirect evidence of a role for Ca2+ in a particular control process, and in a number of cases it has been shown that Sr2+ can replace Ca2+ and allow the physiological stimulus to take place. However no one has yet been able to directly demonstrate the effect of a hormone on the intracellular concentration of ionized Ca2+ or Sr2+ in small cells.

Keywords

Single Muscle Fibre Squid Giant Axon Transient Recorder Intracellular Free Calcium Concentration Blue Fluorescent Protein 
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. 1.
    S. Ringer, An investigation regarding the actions of rubidium and caesium salts compared with the action of potassium salts on the ventricle of the frog’s heart, J. Physiol. (London) 4, 370–379 (1883).Google Scholar
  2. 2.
    C. C. Ashley, Calcium and the activation of skeletal muscle, Endeavor 30, 18–25 (1971).Google Scholar
  3. 3.
    C. C. Ashley and P. C. Caldwell, Calcium movements in relation to contraction, Biochem. Soc. Trans. 39, 29–50 (1974).Google Scholar
  4. 4.
    H. Rasmussen, D. B. P. Goodman, and A. Tenenhouse, The role of cyclic AMP and calcium in cell activation, Crit. Rev. Biochem. 1, 95–148 (1971).CrossRefGoogle Scholar
  5. 5.
    M. J. Berridge, The interaction of cyclic nucleotides and calcium in the control of cellular activity, Adv. Cyclic Nucl. Res. 6, 1–98 (1976).Google Scholar
  6. 6.
    C. N. Hales, A. K. Campbell, J. P. Luzio, and K. Siddle, Calcium as a mediator of hormone action, Biochem. Soc. Trans. 5, 866–872 (1977).Google Scholar
  7. 7.
    C. C. Ashley and E. B. Ridgeway, Simultaneous recording of membrane potential, calcium transient and tension in single muscle fibres, Nature (London) 219, 1168–1169 (1968).CrossRefGoogle Scholar
  8. 8.
    C. C. Ashely and E. B. Ridgeway, On the relationship between membrane potential, calcium transient and tension in single barnacle muscle fibres, J. Physiol. (London) 209, 105–130 (1970).Google Scholar
  9. 9.
    C. C. Ashely, P. C. Caldwell, A. K. Campbell, D. G. Moisescu, and T. J. Lea, Calcium movements in muscle, Soc. Exp. Biol. Symp. 30, 397–422 (1977).Google Scholar
  10. 10.
    J. R. Blinks, F. G. Prendergast, and D. G. Allen, Photoproteins as biological calcium indicators, Pharmacol. Rev. 28, 1–93 (1977).Google Scholar
  11. 11.
    P. F. Baker, A. L. Hodgkin, and E. B. Ridgeway, Depolarization and calcium entry in squid giant axons, J. Physiol. (London) 218, 709–755 (1971).Google Scholar
  12. 12.
    P. F. Baker, Transport and metabolism of calcium ions in nerve, Progr. Biophys. Mol. Biol. 24, 177–223 (1972).CrossRefGoogle Scholar
  13. 13.
    P. F. Baker, H. Meves, and E. B. Ridgeway, Effects of manganese and other agents on the calcium uptake that follows depolarization of squid axons, J. Physiol. (London) 231, 511–526 (1973).Google Scholar
  14. 14.
    P. F. Baker, H. Meves, and E. B. Ridgeway, Calcium entry in response to maintained depolarization of squid axons, J. Physiol. (London) 231, 527–548 (1973).Google Scholar
  15. 15.
    P. F. Baker and A. E. Warner, Intracellular calcium and cell cleavage in early embryos of Xenopus laevis, J. Cell. Biol. 53, 579–581 (1972).CrossRefGoogle Scholar
  16. 16.
    J. E. Brown and J. R. Blinks, Changes in intracellular free calcium concentration during illumination of invertebrate photoreceptors: Detection with aequorin, J. Gen. Physiol. 64, 643–665 (1974).CrossRefGoogle Scholar
  17. 17.
    C. C. Ashley and A. K. Campbell, Aequorin light and tension transients in response to the external application of L-glutamate, J. Physiol. (London) 263, 162–163 P (1976).Google Scholar
  18. 18.
    E. M. Ettiene, Control of contractility in Spirostomum by dissociated calcium ions, J. Gen. Physiol. 56, 168–179 (1970).CrossRefGoogle Scholar
  19. 19.
    B. Rose and W. R. Loewenstein, Permeability of cell junction depends on local cytoplasmic calcium activity, Nature (London) 254, 250–252 (1975).CrossRefGoogle Scholar
  20. 20.
    B. Rose and W. R. Loewenstein, Calcium ion distribution in cytoplasm visualized by aequorin: diffusion in cytosol restricted by energized sequestering, Science 190, 1204–1206 (1975).CrossRefGoogle Scholar
  21. 21.
    G. P. S. Pliny, Natural History, Vols. 1–3 (translated by J. Bostock and H. T. Riley), Bohn, London (1855).Google Scholar
  22. 22.
    E. N. Harvey, Cnidaria and ctenophora, in: Bioluminescence, pp. 148–194, Academic Press, New York (1956).Google Scholar
  23. 23.
    E. N. Harvey, Oxygen and luminescence with a description of methods for removing oxygen from cells and tissues, Biol. Bull. Wood’s Hole 51, 89–97 (1926).CrossRefGoogle Scholar
  24. 24.
    R. Dubois, Note sur la physiologie des pyrophores, Compt. Rend. Soc. Biol. 37, 559–562 (1885).Google Scholar
  25. 25.
    O. Shimomura, F. H. Johnson, and Y. Saiga, Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea, J. Cell. Comp. Physiol. 59, 223–239 (1962).CrossRefGoogle Scholar
  26. 26.
    O. Shimomura, F. H. Johnson, and Y. Saiga, Further data on the bioluminescent protein, aequorin, J. Cell. Comp. Physiol. 62, 1–8 (1963).CrossRefGoogle Scholar
  27. 27.
    J. G. Morin and J. W. Hastings, Biochemistry of the bioluminescence of colonial hydroids and other coelenterates, J. Cell. Physiol. 77, 305–312 (1971).CrossRefGoogle Scholar
  28. 28.
    A. K. Campbell, Extraction, partial purification and properties of obelin, the calcium-activated luminescent protein from the hydroid Obelia geniculata, Biochem. J. 143, 411–418 (1974).Google Scholar
  29. 29.
    O. Shimomura, F. H. Johnson, and Y. Saiga, Extraction and properties of halistaurin, a bioluminescent protein from the hydromedusan, Halistaura, J. Cell. Comp. Physiol. 62, 9–15 (1963).CrossRefGoogle Scholar
  30. 30.
    W. W. Ward and H.H. Seliger, Extraction and purification of calcium-activated photoproteins from the ctenophores Mnemiopsis sp. and Beroeorata. Biochemistry 13, 1491–1499 (1974).Google Scholar
  31. 31.
    W. W. Ward and H. H. Seliger, Properties of mnemiopsis and berovin, calcium-activated photoproteins from the ctenophores Mnemiopsis sp. and Beroeorata, Biochemistry 13, 1500–1509 (1974).Google Scholar
  32. 32.
    M. J. Cormier, K. Hori, and J. M. Anderson, Bioluminescence in coelenterates, Biochim. Biophys. Acta 346, 137–164 (1974).Google Scholar
  33. 33.
    J. M. Anderson, H. Charbonneau, and M. J. Cormier, Mechanisms of calcium induction of Renilla bioluminescence. Involvement of a calcium-triggered luciferin binding protein, Biochemistry 13, 1195–1200 (1974).CrossRefGoogle Scholar
  34. 34.
    J. M. Anderson and M. J. Cormier, Lumisomes, the cellular site of luminescence in coelenterates, J. Biol. Chem. 248, 2937–2943 (1973).Google Scholar
  35. 35.
    O. Shimomura and F. H. Johnson, Calcium-triggered luminescence of the photoprotein aequorin, Soc. Exp. Biol. Symp. 30, 41–54 (1977).Google Scholar
  36. 36.
    O. Shimomura and F. H. Johnson, Mechanism of the luminescent oxidation of Cypridina luciferin, Biochem. Biophys. Res. Commun. 44, 340–346 (1971).CrossRefGoogle Scholar
  37. 37.
    J. W. Hastings, Bioluminescence, Annu. Rev. Biochem. 37, 597–630 (1968).CrossRefGoogle Scholar
  38. 38.
    F. McCapra, The chemistry of bioluminescence, Endeavour 32, 139–145 (1973).Google Scholar
  39. 39.
    O. Shimomura and F. H. Johnson, Calcium binding, quantum yield, and emitting molecule in aequorin bioluminescence, Nature (London) 227, 1356–1357 (1970).CrossRefGoogle Scholar
  40. 40.
    O. Shimomura and F. H. Johnson, Regeneration of the photoprotein aequorin, Nature (London) 256, 236–238 (1975).CrossRefGoogle Scholar
  41. 41.
    J. R. Blinks, Calcium transients in striated muscle cells, Eur. J. Cardiol. 1, 135–142 (1973).Google Scholar
  42. 42.
    D. G. Moisescu, C. C. Ashley, and A. K. Campbell, Comparative aspects of the calcium-sensitive photoproteins aequorin and obelin, Biochim. Biophys. Acta 396, 133–140 (1975).CrossRefGoogle Scholar
  43. 43.
    D. G. Moisescu and C. C. Ashley, The effect of physiologically occuring cations upon aequorin light emission. Determination of binding constants, Biochim. Biophys. Acta 460, 189–205 (1977).CrossRefGoogle Scholar
  44. 44.
    O. Shimomura and F. A. Johnson, Properties of the bioluminescent protein aequorin, Biochemistry 8, 3991–3997 (1969).CrossRefGoogle Scholar
  45. 45.
    K. T. Itzutsu, S. P. Felton, I. A. Siegel, et al., Aequorin, its ionic specificity, Biochem. Biophys. Res. Commun. 49, 1034–1039 (1972).CrossRefGoogle Scholar
  46. 46.
    K. T. Itzutsu, S. P. Felton, I. A. Siegel, et al., Ion specificity of the aequorin luminescent reaction, Physiol. Chem. Phys. 6, 299–308 (1974).Google Scholar
  47. 47.
    O. Shimomura and F. H. Johnson, Further data on the specificity of aequorin luminescence to calcium, Biochem. Biophys. Res. Commun. 53, 490–494 (1974).CrossRefGoogle Scholar
  48. 48.
    F. S. Russell, The Medusae of the British Isles, Vols. I and II, Cambridge University Press, New York, (1953, 1960).Google Scholar
  49. 49.
    T. Hincks, A History of the British Hydroid Zoophytes, Vols. I and II, John van Voorst, London (1868).CrossRefGoogle Scholar
  50. 50.
    A. K. Campbell and R. L. Dormer, The permeability to calcium of pigeon erythrocyte “ghosts” studied by using the calcium-activated luminescent protein, obelin, Biochem. J. 152, 255–265 (1975).Google Scholar
  51. 51.
    J. R. Blinks and G. C. Harrer, Multiple forms of the calcium-sensitive bioluminescent protein aequorin, Fed. Proc. 34, 474 (1975).Google Scholar
  52. 52.
    T. Nakamura, Standardization of an aqueous light source containing luminol: Application to measurement of quantum yields of bioluminescent reactions, J. Biochem. 72, 173–177 (1972).Google Scholar
  53. 53.
    O. Shimomura and F. H. Johnson, Structure of the light-emitting moeity of aequorin, Biochemistry 11, 1602–1608 (1972).CrossRefGoogle Scholar
  54. 54.
    H. Morise, O. Shimomura, F. H. Johnson, and J. Winant, Intermodular energy transfer in the bioluminescent system of Aequorea, Biochemistry 13, 2656–2662 (1974).CrossRefGoogle Scholar
  55. 55.
    Y. Kohama, O. Shimomura, and F. H. Johnson, Molecular weight of the photoprotein aequorin, Biochemistry 10, 4149–4152 (1971).CrossRefGoogle Scholar
  56. 56.
    J. W. Hastings, G. Mitchell, P. H. Mattingly, et al., Response of aequorin bioluminescence to rapid changes in calcium concentration, Nature (London) 222, 1047–1050 (1969).CrossRefGoogle Scholar
  57. 57.
    B. Loschen and B. Chance, Rapid kinetic studies of the light emitting protein aequorin, Nature (London) New Biol. 233, 273–274 (1971).CrossRefGoogle Scholar
  58. 58.
    D. W. Yates and A. K. Campbell, Unpublished observations.Google Scholar
  59. 59.
    A. K. Campbell and K. Siddle, The effect of intracellular calcium ions on adrenalin-stimulated adenosine 3’ : 5’-cyclic monophosphate concentrations in pigeon erythrocytes, studied by using the ionophore A23187, Biochem. J. 158, 211–221 (1976).Google Scholar
  60. 60.
    L. G. Sillen and A. E. Martell, Stability Constants of Metal-Ion Complexes, Vol. 17, Chemical Society Publications, London (1964).Google Scholar
  61. 61.
    C. C. Ashley, A. K. Campbell, and D. G. Moisescu, A demonstration of some of the properties of obelin: A calcium-sensitive luminescent protein, J. Physiol. (London) 245, 9–10 P (1974).Google Scholar
  62. 62.
    R. J. Lefkowitz, C. Mukherjee, L. E. Limbird, et al., Regulation of adenylate cyclase coupled to β-adrenergic response, Rec. Prog. Horm. Res. 32, 597–632 (1976).Google Scholar
  63. 63.
    A. K. Campbell and R. L. Dormer, Relationships between the effect of adrenalin and ionophore A23187 on adenosine 3’ : 5’cyclic monophosphate and free intracellular calcium concentrations in pigeon erythrocyte “ghosts,” Biochem. Soc. Trans. 6, 570–572 (1978).Google Scholar
  64. 64.
    A. K. Campbell and K. Siddle, The effect of 5-hydroxytryptamine and other indole derivatives on the formation of adenosine 3’,5’ : cyclic monophosphate in pigeon erythrocytes, Biochim Biophys. Acta 497, 62–74 (1977).CrossRefGoogle Scholar
  65. 65.
    R. L. Dormer and A. K. Campbell, Further purification and properties of the calcium-activated luminescent protein obelin, and its entrapment in liposomes, Biochem. Soc. Trans. 3, 768–769 (1975).Google Scholar
  66. 66.
    R. L. Dormer, G. R. Newman, and A. K. Campbell, Studies on the entrapment of the calcium-activated photoprotein, obelin and carbonic anhydrase in liposomes and their interaction with isolated adipocytes, Biochem. Soc. Trans. 5, 1151–1154 (1977).Google Scholar
  67. 67.
    J. E. Brown, L. B. Cohen, P. DeWeer, et al., Rapid changes in intracellular free calcium concentration. Detection by metallochromic indicator dyes in squid giant axon, Biophys. J. 15, 1155–1160 (1975).CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1981

Authors and Affiliations

  • Anthony K. Campbell
    • 1
  • Robert L. Dormer
    • 1
  1. 1.Department of Medical BiochemistryWelsh National School of MedicineCardiff, WalesUK

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