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Regulation by Myosin: How Calcium Regulates Some Myosins, Past and Present

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Regulatory Mechanisms of Striated Muscle Contraction

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 592))

Abstract

This symposium celebrates the seminal discovery of troponin by Professor Ebashi. In the 1960s we knew quite a bit about how muscle functions. It was established that contraction was the result of the interaction of ATP with the complex formed from actin and myosin.1 The filamentous structure2 and the constancy of the A-band of striated muscle led to the sliding filament theory.3,4 A detailed model relating muscle mechanics with the cross bridge cycle was produced.5 A change in orientation of the cross bridge between rest and rigor in insect muscle was also demonstrated.6 However, we were ignorant regarding how muscles stay relaxed.

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21.9. References

  1. A. Szent-Györgyi, Studies on muscle, Acta Physiol. Scand. 9(Suppl. 25), 25 (1945).

    Google Scholar 

  2. H. E. Huxley, The double array of filaments in cross-striated muscle, J. Biophys. Biochem. Cytol. 3, 631–648 (1957).

    Article  PubMed  CAS  Google Scholar 

  3. A. F. Huxley and A. F. Niedergerke, Structural changes in muscle during contraction. Interference microscopy of living muscle fibers, Nature 173, 971–978 (1954).

    Article  PubMed  CAS  Google Scholar 

  4. H. E. Huxley and J. Hanson, Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation, Nature 173, 979–978 (1954).

    Google Scholar 

  5. A. F. Huxley, Muscle structure and theories of contraction, Progr. Biophys. Biophys. Chem. 7, 255–318 (1957).

    CAS  Google Scholar 

  6. M. K. Reedy, K. C. Holmes, and R. T. Tregear, Induced changes in orientation of the cross bridges of glycerinated insect flight muscle, Nature 207, 1276–1280 (1965).

    Article  PubMed  CAS  Google Scholar 

  7. S. Kumagai, S. Ebashi, and F. Takeda, Essential relaxing factor in muscle other than myokinase and creatine-phosphokinase, Nature 176, 166 (1955).

    Article  PubMed  CAS  Google Scholar 

  8. A. Weber, R. Herz, and I. Reiss, Study of the kinetics of calcium transport by isolated fragmented sarcoplasmic reticulum, Biochem. Z. 345, 329–369 (1966).

    CAS  Google Scholar 

  9. W. Hasselbach and N. Makinose, Die calciumpumpe der “erschlaffungsgrana” des muskels und ihre abhangigkeit von der ATP-spaltung, Biochem. Z. 333, 94–111 (1961).

    Google Scholar 

  10. S. Ebashi and F. Lippman, Adenosine triphosphate-linked concentration of calcium ions in a particular fraction of rabbit muscle, J. Cell. Biol. 14, 389–400 (1962).

    Article  CAS  PubMed  Google Scholar 

  11. S. Ebashi, Third component participating in the superprecipitation of “natural actomyosin”, Nature 200, 1010 (1963).

    Article  PubMed  CAS  Google Scholar 

  12. S. Ebashi and F. Ebashi, A new protein component participating in the superprecipitation of myosin B, J. Biochem. 55, 604–613 (1964).

    PubMed  CAS  Google Scholar 

  13. S. Ebashi and M. Endo, Calcium ion and muscle contraction, Progr. Biophys. Mol. Biol. 18, 123–183 (1968).

    Article  CAS  Google Scholar 

  14. A. G. Szent-Györgyi, C. Cohen, and J. Kendrick-Jones. Paramyosin and the filaments of molluscan “catch” muscles II. Native filaments: isolation and characterization, J. Mol. Biol. 56, 239–258 (1971).

    Article  PubMed  Google Scholar 

  15. J. Kendrick-Jones, W. Lehman, and A. G. Szent-Györgyi, Regulation in molluscan muscles, J. Mol. Biol. 54, 313–326 (1970).

    Article  PubMed  CAS  Google Scholar 

  16. W. Lehman and A. G. Szent-Györgyi, Regulation of muscular contraction: Distribution of actin control and myosin control in the animal kingdom, J. Gen. Physiol. 66, 1–30 (1975).

    Article  PubMed  CAS  Google Scholar 

  17. A. Goldberg and W. Lehman, Troponin-like proteins from muscles of the scallop, Aequipecten irradians. Biochem. J. 171, 413–418 (1978).

    PubMed  CAS  Google Scholar 

  18. T. Ojima and K. Mishita, Troponin from Akazara scallop striated adductor muscles, J. Biol. Chem. 261, 16749–16754 (1986).

    PubMed  CAS  Google Scholar 

  19. G. Ashiba, T. Asada, and S. Watanabe, Calcium regulation in clam foot muscle. Calcium sensitivity of clam foot myosin, J. Biochem. 58, 837–846 (1980).

    Google Scholar 

  20. C. Wells and C. R. Bagshaw, Calcium regulation of molluscan myosin ATPase in the absence of actin, Nature 313, 696–697 (1985).

    Article  PubMed  CAS  Google Scholar 

  21. R. N. Simmons and A. G. Szent-Györgyi, Reversible loss of calcium control of tension in scallop striated muscle associated with the removal of regulatory light chains, Nature 273, 62–64 (1978).

    Article  PubMed  CAS  Google Scholar 

  22. E. M. Szentkiralyi, Tryptic digestion of scallop S1: evidence for a complex between the two light chains and a heavy-chain peptide, J. Muscle Res. Cell. Motil. 5, 147–164 (1987).

    Article  Google Scholar 

  23. A. G. Szent-Györgyi, E. M. Szentkiralyi, and J. Kendrick-Jones, The light chains of scallop myosin as regulatory subunits, J. Mol. Biol. 74, 179–203 (1973).

    Article  PubMed  Google Scholar 

  24. C. R. Bagshaw and J. Kendrick-Jones, Characterization of homologous divalent metal ion binding sites of vertebrate myosins using paramagnetic resonance spectroscopy, J. Mol Biol. 130, 317–336 (1979).

    Article  PubMed  CAS  Google Scholar 

  25. P. D. Chantler and A. G. Szent-Györgyi, Regulatory light chains and scallop myosin: full dissociation and cooperative effects, J. Mol. Biol. 138, 473–499 (1980).

    Article  PubMed  CAS  Google Scholar 

  26. L. Nyitray, E. B. Goodwin, and A. G. Szent-Györgyi, Complete primary structure of a scallop striated muscle myosin heavy chain, J. Biol. Chem. 266, 18469–18476 (1991).

    PubMed  CAS  Google Scholar 

  27. J. H. Collins, Myosin light chains and troponin C: structural and evolutionary relationships revealed by amino acid sequence comparisons, J. Muscle Res. Cell Motil. 12, 3–25 (1991).

    Article  PubMed  CAS  Google Scholar 

  28. J. R. Sellers, P. D. Chantler, and A. G. Szent-Györgyi, Hybrid formation between scallop myofibrils and foreign regulatory light-chains, J. Mol. Biol. 144, 223–245 (1980).

    Article  PubMed  CAS  Google Scholar 

  29. J. M. Scholey, K. A. Taylor, and J. Kendrick-Jones, The role of myosin light chains in regulating actin-myosin interaction, Biochimie 63, 255–271 (1981).

    PubMed  CAS  Google Scholar 

  30. H. Kwon, E. B. Goodwin, L. Nyitray, E. Berliner, E. O’Neall-Hennessey, F. D. Melandri, and A. G. Szent-Györgyi, Isolation of the regulatory domain of scallop myosin. Role of the essential light chain in calcium binding, Proc. Natl. Acad. Sci. USA 87, 4771–4775 (1990).

    Article  PubMed  CAS  Google Scholar 

  31. J. H. Collins, J. R. Jakes, J. Kendrick-Jones, J. Leszyk, W. Baruch, J. L. Theibert, J. Spiegel, and A. G. Szent-Györgyi, Amino acid sequence of myosin essential light chain from the scallop Aequipecten irradians, Biochemistry 25, 7651–7656 (1986).

    Article  PubMed  CAS  Google Scholar 

  32. S. Fromherz and A. G. Szent-Györgyi, Role of essential light chain EF hand domain in calcium binding and regulation of scallop myosin, Proc. Natl. Acad. Sci. USA 92, 7652–7656 (1995).

    Article  PubMed  CAS  Google Scholar 

  33. X. Xie, D. H. Harrison, I. Schlichting, R. M. Sweet, V. N. Kalabokis, A. G. Szent-Györgyi, and C. Cohen, Structure of the regulatory domain of scallop myosin at 2.8 Å resolution, Nature 368, 316–394 (1994).

    Article  Google Scholar 

  34. A. Houdusse and C. Cohen, Structure of the regulatory domain of scallop myosin at 2 Å resolution; implications for regulation, Structure (London) 4, 21–32 (1996).

    CAS  Google Scholar 

  35. A. Jancso and A. G. Szent-Györgyi, Regulation of scallop myosin by the regulatory light chain depends on a single glycine residue, Proc. Natl. Acad. Sci. USA 91, 8762–8766 (1994).

    Article  PubMed  CAS  Google Scholar 

  36. C. Wells, K. E. Warriner, and C. R. Bagshaw, Fluorescence studies on the nucleotide and Ca2+ binding domains of molluscan myosin, Biochem. J. 231, 31–38 (1985).

    PubMed  CAS  Google Scholar 

  37. A. P. Jackson and C. R. Bagshaw, Transient-kinetic studies of the adenosine triphosphate activity of scallop heavy meronyosin, Biochem. J. 251, 515–526 (1988).

    PubMed  CAS  Google Scholar 

  38. A. P. Jackson. and C. R. Bagshaw, Kinetic trapping of intermediates of the scallop heavy meromyosin adenosine triphosphatase reaction revealed by formycin nucleotides, Biochem. J. 251, 527–540 (1988).

    PubMed  CAS  Google Scholar 

  39. L. Nyitray, A. Jancso, Y. Ochiai, L. Graf, and A. G. Szent-Györgyi, Scallop striated and smooth muscle myosin heavy chain isoforms are produced by alternative RNA splicing from a single gene, Proc. Natl. Acad. Sci. USA 91, 12686–12690 (1994).

    Article  PubMed  CAS  Google Scholar 

  40. C. L. Perreault-Micale, V. N. Kalabokis, L. Nyitray, and A. G. Szent-Györgyi, Sequence variations in the surface loop near the nucleotide binding site modulate the ATP turnover rates of molluscan myosins, J. Muscle. Res. Cell Motil. 14, 543–553 (1996).

    Article  Google Scholar 

  41. S. E. Kurzawa-Goertz, C. L. Perreault-Micale, K. M. Trybus, A. G. Szent-Györgyi, and M. A. Geeves, Loop I can modulate ADP affinity, ATPase activity, and motility of different scallop myosins. Transient kinetic analysis of S1 isoforms, Biochemistry 37, 7517–7525 (1998).

    Article  PubMed  CAS  Google Scholar 

  42. P. D. Chantler, J. R. Sellers, and A. G. Szent-Györgyi, Cooperativity in scallop myosin, Biochemistry 20, 210–216 (1981).

    Article  PubMed  CAS  Google Scholar 

  43. V. N. Kalabokis and A. G. Szent-Györgyi, Cooperativity and regulation of scallop myosin and myosin fragments, Biochemistry 36, 15834–15840 (1997).

    Article  PubMed  CAS  Google Scholar 

  44. W. F. Stafford, M. P. Jacobsen, J. Woodhead, R. Craig, E. O’Neall-Hennessey, and A. G. Szent-Györgyi, Calcium-dependent structural changes in scallop heavy meromyosin, J. Mol. Biol. 307, 137–147 (2001).

    Article  PubMed  CAS  Google Scholar 

  45. M. Nyitrai, A. G. Szent-Györgyi, and M. A. Geeves, A kinetic model of the co-operative binding of calcium and ADP to scallop (Argo-pecten irradians) heavy meromyosin, Biochem. J. 365, 19–30 (2002).

    Article  PubMed  CAS  Google Scholar 

  46. M. Nyitrai, A. G. Szent-Györgyi, and M. A. Geeves, Interactions of the two heads of scallop (Argo-pecten irradians) heavy meromyosin with actin: influence of calcium and nucleotides, Biochem. J. 370, 839–848 (2003).

    Article  PubMed  CAS  Google Scholar 

  47. M. Nyitray, W. F. Stafford, A. G. Szent-Györgyi, and M. A. Geeves, Ionic interactions play a role in the regulatory mechanism of scallop heavy meromyosin, Biophys. J. 85, 1053–1562 (2003).

    Article  Google Scholar 

  48. H. Suzuki, W. F. Stafford, H. S. Slayter, and J. C. Seidel, A conformational transition in gizzard heavy meromyosin involving the head tail junction, resulting in changes in sedimentation coefficient, ATPase activity, and orientation of heads, J. Biol. Chem. 260, 4810–14817 (1985).

    Google Scholar 

  49. D. Wendt, D. Taylor, T. Messier, K. M. Trybus, and K. A. Taylor, Visualization of head-interactions in the inhibited state of smooth muscle myosin, J. Cell. Biol. 147, 1385–1389 (1999).

    Article  PubMed  CAS  Google Scholar 

  50. J. Liu, T. Wendt, D. Taylor, and K. Taylor, Refined model of the 10S conformation of smooth muscle by cryo-electron microscopy 3D image reconstruction, J. Mol. Biol. 329, 963–972 (2003).

    Article  PubMed  CAS  Google Scholar 

  51. A. Houdusse, A. G. Szent-Györgyi, and C. Cohen, Three conformational state of scallop myosin S1, Proc. Natl. Acad. Sci. USA 97, 11238–11243 (2000).

    Article  PubMed  CAS  Google Scholar 

  52. H. S. Jung, S. A. Burggess, M. Colegrave, H. Patel, P. D. Chantler, J. M. Chalovich, J. Trinick, and P. J. Knight, Comparative studies of the folded structures of scallop striated and vertebrate smooth muscle myosins, Biophys. J. 86, 406a (2004).

    Google Scholar 

  53. J. Woodhead, F.-Q. Zhao, R. Craig, E. H. Egelman, L. Alamo, and R. Padron, Atomic model of a myosin filament in the relaxed state, Nature 436, 1195–1199 (2005).

    Article  PubMed  CAS  Google Scholar 

  54. J. A. Rall, Mechanics and energetics of contraction in striated muscle of the sea scallop, Placopecten magellanicus, J. Physiol. 321, 287–295 (1981).

    PubMed  CAS  Google Scholar 

  55. P. Vibert and R. Craig, Structural changes that occur in scallop myosin filaments upon activation, J. Cell. Biol. 101, 830–837 (1985).

    Article  PubMed  CAS  Google Scholar 

  56. F.-Q. Zhao and R. Craig, Ca2+ causes release of myosin heads from the thick filament surface on the milliseconds time scale, J. Mol. Biol. 327, 145–158 (2003).

    Article  PubMed  CAS  Google Scholar 

  57. F. Wang, K. Thirumurugan, W. F. Stafford, J. A. Hammer, P. J. Knight, and J. R. Sellers, Regulated conformation of myosin V, J. Biol. Chem. 279, 2333–2336 (2003).

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Brandeis University, Waltham, USA

    Andrew G. Szent-Györgyi

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  1. Andrew G. Szent-Györgyi
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Editors and Affiliations

  1. National Institute of Physiological Sciences, Okazaki, Japan

    Setsuro Ebashi

  2. The Jikei University School of Medicine, Tokyo, Japan

    Iwao Ohtsuki

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Szent-Györgyi, A.G. (2007). Regulation by Myosin: How Calcium Regulates Some Myosins, Past and Present. In: Ebashi, S., Ohtsuki, I. (eds) Regulatory Mechanisms of Striated Muscle Contraction. Advances in Experimental Medicine and Biology, vol 592. Springer, Tokyo. https://doi.org/10.1007/978-4-431-38453-3_21

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