Advertisement

Highlights of the History of Calcium Regulation of Striated Muscle

  • John Gergely
Conference paper
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 592)

Abstract

First of all, I should like to express my gratitude for the invitation, making it possible for me to participate in the celebration of the fortieth anniversary of the discovery of troponin by Professor Ebashi and his colleagues. This discovery opened up new vistas of the regulation of striated muscle contraction and the role of ionized calcium in it.

Keywords

Sarcoplasmic Reticulum Malignant Hyperthermia Relaxing Factor Calcium Regulation Calcium Binding Site 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

3.6. References

  1. 1.
    H. Kumagai, S. Ebashi, and F. Takeda, Essential relaxing factor in muscle other than myokinase and creatine phosphokinase, Nature 176, 166 (1955).PubMedCrossRefGoogle Scholar
  2. 2.
    B. B. Marsh, A factor modifying muscle fibre syneresis, Nature 167, 1065–1066 (1951).PubMedCrossRefGoogle Scholar
  3. 3.
    B. B. Marsh, The effects of adenosine triphosphate on the fibre volume of a muscle homogenate, Biochim. Biophys. Acta 9, 247–260 (1952).PubMedCrossRefGoogle Scholar
  4. 4.
    W. W. Kielley, and O. Meyerhof, A new magnesium-activated adenosinetriphosphatase from muscle, J. Biol. Chem. 174, 387–388 (1948).PubMedGoogle Scholar
  5. 5.
    W. W. Kielley, and O. Meyerhof, Studies on adenosinetriphosphatase from muscle. II. A new magnesium-activated adenosinetriphosphatase, J. Biol. Chem. 176, 591–601 (1948).PubMedGoogle Scholar
  6. 6.
    W. W. Kielley, and O. Meyerhof, Studies on adenosinetriphosphatase from muscle. III, The lipoprotein nature of the magnesium-activated adenosinetriphosphatase, J. Biol. Chem. 183, 391–401 (1950).Google Scholar
  7. 7.
    A. Weber, On the role of calcium in the activity of adenosine 5′-triphosphate hydrolysis by actomyosin, J. Biol. Chem. 234, 2764–2769 (1959).PubMedGoogle Scholar
  8. 8.
    A. Weber, and S. Winicur, The role of calcium in the superprecipitation of myosin, J. Biol. Chem. 236, 3198–3202 (1961).PubMedGoogle Scholar
  9. 9.
    S. Ebashi, and F. Lipmann, Adenosine triphosphate-linked concentration of calcium ions in a particulate fraction of rabbit muscle, J. Cell. Biol. 14, 389–400 (1962).CrossRefPubMedGoogle Scholar
  10. 10.
    W. Hasselbach, and M. Makinose, The calcium pump of the relaxing granules of muscle and its dependence on ATP-splitting, Biochem. Z. 196, 518–528 (1961).Google Scholar
  11. 11.
    K. R. Porter, The sarcoplasmic reticulum. Its recent history and present status, J. Biophys. Biochem. Cytol. 10, 219–226 (1961).CrossRefPubMedGoogle Scholar
  12. 12.
    K. Bailey, Tropomyosin: a new asymmetric protein of muscle, Nature 57, 368–369 (1946).Google Scholar
  13. 13.
    J. Hanson, and J. Lowy, The structure of F-actin and of actin filaments isolated from muscle, J. Mol. Biol. 6, 46–60 (1963).Google Scholar
  14. 14.
    S. Ebashi, Third component participating in the superprecipitation of ‘natural actomyosin’. Nature (London) 200, 1010 (1963).CrossRefGoogle Scholar
  15. 15.
    S. Ebashi, and A. Kodama, A new protein factor promoting aggregation of tropomyosin, J. Biochem. (Tokyo) 58, 107–108 (1965)Google Scholar
  16. 16.
    S. Ebashi, and A. Kodama, Interaction of troponin with F-actin in the presence of tropomyosin, J. Biochem. (Tokyo) 59, 425–426 (1966).Google Scholar
  17. 17.
    S. Ebashi, F. Ebashi, and A. Kodama, Troponin as the Ca2+ receptive protein in the contractile system, J. Biochem. (Tokyo) 62, 137–138, (1965).Google Scholar
  18. 18.
    I. Ohtsuki, T. Masaki, Y. Nonomura, and S. Ebashi, Periodic distribution of troponin along the thin filament, J. Biochem. 61, 817–819 (1967)Google Scholar
  19. 19.
    S. Ebashi, and M. Endo, Calcium ion and muscle contraction, Prog. Biophys. Mol. Biol. 18, 123–183 (1968).PubMedCrossRefGoogle Scholar
  20. 20.
    S. Ebashi, M. Endo, and I. Ohtsuki, Control of muscle contraction. Q. Rev. Biophys. 2, 351–384 (1969).PubMedGoogle Scholar
  21. 21.
    A. Weber, Energized calcium transport and relaxing factors, in: Current Topics in Bioenergetics, Vol. 1, edited by D. R. Sanadi (New York, Academic Press, 1966), pp. 203–249.Google Scholar
  22. 22.
    D. J. Hartshorne, and H. Mueller, Fractionation of troponin into two distinct proteins. Biochem. Biophys. Res. Commun. 31, 647–653 (1968).PubMedCrossRefGoogle Scholar
  23. 23.
    M. C. Schaub, and S. V. Perry, The relaxing factor system of striated muscle. Resolution of the troponin complex into inhibitory and calcium ion-sensitizing factors and their relatonship to tropomyosin, Biochem. J. 115, 993–1004 (1969).PubMedGoogle Scholar
  24. 24.
    S. Ebashi, T. Wakabayashi, and F. Ebashi, Troponin and its components, J. Biochem. (Tokyo) 69, 441–445 (1971).Google Scholar
  25. 25.
    M. L. Greaser, and J. Gergely, Reconstitution of troponin activity from three protein components, J. Biol. Chem. 246, 4226–4233 (1971).PubMedGoogle Scholar
  26. 26.
    M. L. Greaser, and J. Gergely, Purification and properties of the components from troponin, J. Biol. Chem. 248, 2125–2133 (1973).PubMedGoogle Scholar
  27. 27.
    J. H. Collins, J. D. Potter, M. J. Wilshire, and N. Jackman, The amino acid sequence of rabbit skeletal muscle: gene replication and homology with Ca-binding proteins from carp and hake muscle, FEBS Lett. 36, 268–272 (1973).PubMedCrossRefGoogle Scholar
  28. 28.
    C. E. Nockolds, R. H. Kretsinger, C. E, Coffee, and R. A. Bradshaw, Structure of a calcium-binding carp protein, Proc. Natl. Acad. Sci. USA 69, 581–584 (1972).PubMedCrossRefGoogle Scholar
  29. 29.
    R. H. Kretsinger, and C. E. Nockolds, Carp muscle and calcium binding proteins II. Structure determination and general description, J. Biol. Chem. 248, 3313–3316 (1973).PubMedGoogle Scholar
  30. 30.
    J. D. Potter, and J. Gergely, Troponin, tropomyosin and actin interactions in the Ca2+ regulation of muscle contrction, Biochemistry 13, 2697–2703 (1974).PubMedCrossRefGoogle Scholar
  31. 31.
    J. D. Potter, and J. Gergely, The calcium and magnesium binding sites on troponin and their role in the regulation of myofibrillar adenosine triphosphatase, J. Biol. Chem. 250, 4628–4633 (1975).PubMedGoogle Scholar
  32. 32.
    W. Drabikowski, Z. Grabarek, and B. Barylko, Degradation of the Tn-C component of troponin by trypsin, Biochim. Biophys. Acta 490, 216–224 (1977).PubMedGoogle Scholar
  33. 33.
    P. C. Leavis, S. S. Rosenfeld, J. Gergely, Z. Grabarek, and W. Drabikowski, Proteolytic fragments of troponin C. Localization of high and low affinity Ca2+ binding sites and interactions with troponin I and troponin T, J. Biol. Chem. 253, 5452–5459 (1978).PubMedGoogle Scholar
  34. 34.
    I. L. Sin, R. Fernandes, and D. Mercola, Direct identification of the high and low affinity calcium binding sites of troponin-C, Biochem. Biophys. Res. Commun. 82, 1132–1139 (1978).PubMedCrossRefGoogle Scholar
  35. 35.
    H. Syska, J. M. Wilkinson, R. J. Grand, and S. V. Perry, The relationship between biological activity and primary structure of troponin I from white skeletal muscle of the rabbit, Biochem. J. 153, 375–387 (1976).PubMedGoogle Scholar
  36. 36.
    J. A. Talbot, and R. S. Hodges, Synthetic studies on the inhibitory region of rabbit skeletal troponin I. Relationship of amino acid sequence to biological activity, J. Biol. Chem. 256, 2798–2802 (1981).PubMedGoogle Scholar
  37. 37.
    P. C. Leavis, and J. Gergely, Thin filament proteins and thin filament-linked regulation of vertebrate muscle contraction, Crit. Rev. Biochem. Mol. Biol. 16, 235–305 (1984).Google Scholar
  38. 38.
    I. Ohtsuki, K. Maruyama, and S. Ebashi, Regulatory and cytoskeletal proteins of vertebrate skeletal muscle, in: Advances in Protein Chemistry, Vol. 38, edited by C. B. Anfinsen, J. T. Edsall, and F. M. Richards (Academic Press, Inc. Orlando, 1986), pp. 1–68.Google Scholar
  39. 39.
    O. Herzberg, and M. N. James, Structure of the calcium regulatory muscle protein troponin-C at 2.8 A resolution. Nature 313, 653–659 (1985).PubMedCrossRefGoogle Scholar
  40. 40.
    M. Sundaralingam, R. Bergstrom, and G. Strasburg, Molecular structure of troponin C from chicken skeletal muscle at 3-angstrom resolution, Science 227, 945–948 (1985)PubMedCrossRefGoogle Scholar
  41. 41.
    R. H. Kretsinger, and C. D. Barry, The predicted structure of the calcium-binding component of troponin, Biochim. Biophys. Acta 405, 40–52 (1975).PubMedGoogle Scholar
  42. 42.
    O. Herzberg, J. Moult, and M. N. James, A model for the Ca2+-induced conformational transition of troponin C. A trigger for muscle contraction, J. Biol. Chem. 261, 2638–2644 (1986).PubMedGoogle Scholar
  43. 43.
    Z. Grabarek, R. Y. Tan, J. Wang, T. Tao, and J. Gergely, Inhibition of mutant troponin C activity by an intra-domain disulphide bond, Nature 345, 132–135 (1990).PubMedCrossRefGoogle Scholar
  44. 44.
    K. Fujimori, M. Sorenson, O. Herzberg, J. Moult, and F. C. Reinach, Probing the calcium-induced conformational transition of troponin C with site-directed mutants [see comments], Nature 345, 182–184 (1990)PubMedCrossRefGoogle Scholar
  45. 45.
    S. K. Sia, M. X. Li, L. Spyracopoulos, S. M. Gagne, W. Liu, J. A. Putkey, B. C. Sykes, Structure of cardiac muscle troponin C unexpectedly reveals a closed regulatory domain, J. Biol. Chem. 272, 18216–18221 (1997).PubMedCrossRefGoogle Scholar
  46. 46.
    A. M. Gordon, E. Homsher, and M. Regnier, Regulation of contraction in striated muscle, Physiol. Rev. 80, 853–924 (2000).PubMedGoogle Scholar
  47. 47.
    H. C. Cheung, Calcium-induced molecular and structural signaling in striated muscle contraction, in: Molecular Control Mechanisms in Striated Muscle Contraction, edited by R. J. Solaro, and R. L. L. Moss (Kluwer Acad. Publishers, Dordrecht, 2002), pp. 199–246.Google Scholar
  48. 48.
    R. T. McKay, B. P. Tripet, J. R. Pearlstone, L. B. Smilley, and B. D. Sykes, Defining the region of troponin-I that binds to troponin-C, Biochemistry 38, 5478–5489 (1999).PubMedCrossRefGoogle Scholar
  49. 49.
    B. P. Tripet, J. E. Van Eyk, and R. S. Hodges, Mapping of a second actin tropomyosin and a second troponin C binding site within the C terminus of troponin I, and their importance in the Ca2+-dependent regulation of muscle contraction, J. Mol. Biol. 271, 728–750 (1997).PubMedCrossRefGoogle Scholar
  50. 50.
    Y. Luo, J. L. Wu, B. Li, K. Langsetmo, J. Gergely, and T. Tao, Photocrosslinking of benzophenone-labeled single cysteine troponin I mutants to other thin filament proteins, J. Mol. Biol. 296, 899–910 (2000).PubMedCrossRefGoogle Scholar
  51. 51.
    D. G. Vassylyev, S. Takeda, S. Wakatsuki, K. Maeda, and Y. Maeda, Crystal structure of troponin C in complex with troponin I fragment at 2.3A resolution, Proc. Natl. Acad. Sci. USA 95, 4847–4852 (1998).PubMedCrossRefGoogle Scholar
  52. 52.
    S. Takeda, A. Yamashita, K. Maeda, and Y. Maeda, Structure of the core domain of human cardiac troponin in the Ca2+-saturated form, Nature 424, 35–41 (2003).PubMedCrossRefGoogle Scholar
  53. 53.
    R. Stefancsik, P. K. Jha, and S. Sarkar, Identification and mutageness of a highly conserved domain in troponin T responsible for troponin I binding: potential role for coiled coil interaction, Proc. Natl. Acad. Sci. USA 96, 957–962 (1998).CrossRefGoogle Scholar
  54. 54.
    M. V. Vinogradova, D. B. Stone, G. G. Malanina, C. Karatzaferi, R. Cooke, R. A. Mendelson, R. J. Fletterick, Ca2+-regulated structural changes in troponin, Proc. Natl. Acad. Sci. USA 102, 5038–5043 (2005).PubMedCrossRefGoogle Scholar
  55. 55.
    K. Murakami, F. Yumoto, S. Y. Ohki, T. Yasunaga, M. Tanokura, and T. Wakabayashi, Structural basis for Ca2+-regulated muscle relaxation at interaction sites of troponin with actin and tropomyosin, J. Mol. Biol. 352, 178–201 (2005).PubMedCrossRefGoogle Scholar
  56. 56.
    H. E. Huxley, Structural changes in the actin-and myosin-containing filaments during contraction, Cold Spring Harb. Symp. Quant. Biol. 37, 361–376 (1973).Google Scholar
  57. 57.
    J. C. Haselgrove, X-ray evidence for a conformational change in the actin-containing filaments of vertebrate striated muscle, Cold Spring Harb. Symp. Quant. Biol. 37, 341–352 (1973).Google Scholar
  58. 58.
    D. F. A. McKillop, and M. A. Geeves, Regulation of the interaction between actin and myosin subfragment 1: evidence for three states of the thin filament, Biophys. J. 65, 693–701 (1993).PubMedCrossRefGoogle Scholar
  59. 59.
    M. A. Geeves, and S. S. Lehrer, The muscle thin filament as a classical M. cooperative/allosteric regulatory system, J. Mol. Biol. 277, 1081–1089 (1998).PubMedCrossRefGoogle Scholar
  60. 60.
    R. Craig, and W. Lehman, Crossbridge and tropomyosin positions observed in native, interacting thick, and thin filaments, J. Mol. Biol. 311, 1027–1036 (2001).PubMedCrossRefGoogle Scholar
  61. 61.
    S. V. Perry, Troponin I: inhibitor or facilitator? Mol. Cell. Biochem. 190, 9–32, (1999).PubMedCrossRefGoogle Scholar
  62. 62.
    S. V. Perry, What is the role of tropomyosin in the regulation of muscle contraction? J. Muscle Res. Cell Motil. 24, 593–596 (2003).PubMedCrossRefGoogle Scholar
  63. 63.
    V. B. Patchell, C. E. Gallon, J. S. Evans, Y. Gao, S. V. Perry, and B. A. Levine, The regulatory effects of tropomyosin and troponin-I on the interaction of myosin loop regions with F-actin, J. Biol. Chem. 280, 14469–14475 (2005).PubMedCrossRefGoogle Scholar
  64. 64.
    L. S. Tobacman, Structure and regulation of cardiac and skeletal muscle thin filaments, in: Molecular Control Mechanisms in Striated Muscle Contraction, edited by R. J. Moss, and R. L. Salaro (Klewer, Dordrecht, 2002), pp. 143–162.Google Scholar
  65. 65.
    J. H. Brown, and C. Cohen, Regulation of muscle contraction by tropomyosin and troponin: how structure illuminates function, in: Advances in Protein Chemistry, Vol. 7, edited by F. M. Richards, D. S. Eisenberg, and J. Kuriyan, (Elsevier Academic Press, Amsterdam, 2005), pp. 121–165.Google Scholar
  66. 66.
    M. X. Li, X. Wang, and B. D. Sykes, Structural based insights into the role of troponin in cardiac muscle pathophysiology, J. Muscle Res. Cell Motil. 25, 559–579 (2004).PubMedCrossRefGoogle Scholar
  67. 67.
    T. Kobayashi, and R. J. Solaro, Calcium, thin filaments and the integrative biology of cardiac contractility, Ann. Rev. Physiology 67, 9–67 (2005).Google Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • John Gergely
    • 1
    • 2
    • 3
  1. 1.Boston Biomedical Research InstituteBostonUSA
  2. 2.Harvard Medical SchoolBostonUSA
  3. 3.Massachusetts General HospitalBostonUSA

Personalised recommendations