Animal electricity, Ca2+ and muscle contraction. A brief history of muscle research

• Authors: Anthony N Martonosi
• Languages of publication: EN

Abstracts

EN

This brief review attempts to summarize some of the major phases of muscle research from Leeuwenhoek's description of sarcomeres in 1674, through Galvani's observation of "animal electricity" in 1791, to the discovery of Ca2+ as the key messenger in the coupling of nerve excitation to muscle contraction. The emerging molecular mechanism of the contraction process is one of the great achievements of biology, reflecting the intimate links between physics, chemistry and the life Sciences in the solution of biological problems.

Keywords

EN

cardiac and smooth muscles; skeletal; Ca2+; Mg-ATP; sarcoplasmic reticulum; contraction-relaxation cycle

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2000
• Volume: 47
• Issue: 3
• Pages: 493-516

Dates

published

2000

received

2000-06-16

accepted

2000-07-20

Contributors

author

Anthony N Martonosi

• Department of Biochemistry and Molecular Biology, Health Science Center at Syracuse, State University of New York, 750 East Adams Street, Syracuse, NY 13210-2339, U.S.A.

References

• 1. Needham, D.M. (1971) Machina Carnis. The Biochemistry of Muscular Contraction in its Historical Development. Cambridge University Press, Cambridge.
• 2. Leeuwenhoek, A. van (1939) The collected letters of Antoni van Leeuwenhoek (edited by a Committee of Dutch Scientists) III. p. 385 ff, Letter to the Royal Society of London addressed to Mr. R. Hooke, Swets and Zeitlinger, Amsterdam.
• 3. Hoole, S. (1798) Select works of A. van Leeuwenhoek, II pt. 3, p. 113, London.
• 4. Croone, W. (1675) An Hypothesis of the Structure of a Muscle and the reason of its Contraction; from Lectures to Barber Surgeons read in the Surgeon's Theatre, Anno 1674, 1675; in Robert Hooke, Philosophical Collections No. 2, Section 8, p. 22, 1675.
• 5. Galvani, A. & Aldini, J. (1792) De viribus electricitatis in motu musculari commentarius. Apud Societatem Typographicam. Translated in Abhandlung über die Kräfte der Electricität bei der Muskelbewegung, W. Engelmann, Leipzig, 1894.
• 6. Fulton, J.F. (1930) Selected Reading in the History of Physiology; pp. 209-213, Charles C. Thomas, Publisher, Springfield, Illinois/ Baltimore.
• 7. Piccolino, M. (1997) Luigi Galvani and animal electricity: Two centuries after the foundation of electrophysiology. Trends Neurosci. 20, 443-448.
• 8. Piccolino, M. (2000) The bicentennial of the Voltaic battery (1800-2000): The artificial electric organ. Trends Neurosci. 23, 147-151.
• 9. Volta, A. (1800) On the electricity excited by the mere contact of conducting substances of different species. Phil. Trans. Roy. Soc. London 90, 403-431.
• 10a. Schuetze, S.M. (1983) The discovery of the action potential. Trends Neurosci. 6, 164-168.
• 10b. De Weer, P. (2000) A century of thinking about cell membranes. Annu. Rev. Physiol. 62, 919-926.
• 11a. Hodgkin, A.L. (1958) The Croonian Lecture. Ionic movements and electrical activity in giant nerve fibers. Proc. Roy. Soc. London, Series B 148, 1-37.
• 11b. Hodgkin, A.L. (1964) The Conduction of Nervous Impulse. Sherrington Lectures 7, Liverpool University Press, Liverpool.
• 12. Huxley, A.F. (1977) Looking back on muscle; in The Pursuit of Nature. Informal Essays on the History of Physiology (Hodgkin, A.L., Huxley, A.F., Feldberg, W., Rushton, W.A.H., Gregory, R.A. & McLance, R.A., eds.) pp. 23-64, Cambridge University Press, Cambridge.
• 13. Huxley, A.F. (1980) Reflections on Muscle. Princeton University Press, Princeton.
• 14. Kühne, W. (1859) Untersuchungen über Bewegungen und Vernderung der contractilen Substanzen. Arch. Anat. Physiol. Wissensch. Med. 748-835.
• 15. Kuehne, W. (1864) Untersuchungen über das Protoplasma und die Contractilitt. Engelmann, Leipzig.
• 16. Kuehne, W. (1888) On the origin and causation of vital movement. Proc. Roy. Soc. London 44, 427-448.
• 17. Halliburton, W.D. (1887) On muscle plasma. J. Physiol. (London) 8, 133-202.
• 18. Finck, H. (1968) On the discovery of actin. Science 160, 332.
• 19. Mommaerts, W.F.H.M. (1992) Who discovered actin? BioEssays 14, 57-59.
• 20. Retzius, G. (1881) Zur Kenntnis der quergestreiften Muskelfaser. Biologische Untersuchungen Series I, pp.1-26.
• 21. Retzius, G. (1890) Muskelfibrille und Sarcoplasma. Biologische Untersuchungen. Neue Folge 1, 51-88.
• 22. Veratti, E. (1902) Richerche sulle fine struttura della fibra muscolare striata. Memorie Inst. Lomb. Cl. Sci. Mat. e Nat. 19, 87-133.
• 23. Veratti, E. (1961) Investigations on the fine structure of striated muscle fiber (translation of the paper of 1902 by Bruni, C., Bennett, J.S. & de Koven, D.). J. Biophys. Biochem. Cytol. 10, Part 2, 3-59.
• 24. Porter, K.R. (1961) The sarcoplasmic reticulum. Its recent history and present status. J. Biophys. Biochem. Cytol. 10, Part 2, 211-226.
• 25. Ringer, S. (1883) A further contribution regarding the influence of the different constituents of the blood on the contraction of the heart. J. Physiol. (London) 4, 29-42.
• 26. Ringer, S. (1886) Further experiments regarding the influence of small quantities of lime, potassium and other salts on muscular tissue. J. Physiol. (London) 7, 291-308.
• 27. Ringer, S. & Buxton, L.W. (1887) Concerning the action of calcium, potassium and sodium salts upon the eel's heart and upon the skeletal muscles of the frog. J. Physiol. (London) 8, 15-19.
• 28. Ringer, S. (1887) Regarding the action of lime, potassium and sodium salts on skeletal muscle. J. Physiol. (London) 8, 20-24.
• 29. Campbell, A.K. (1983) Intracellular Calcium its Universal Role as Regulator. John Wiley and Sons, New York.
• 30. Nayler, W.G. (1984) Sydney Ringer physician and scientist. J. Mol. Cell Cardiol. 16, 113-116.
• 31. Smith, D.S. (1961) Reticular organization within the striated muscle cell. An historical survey of light microscopic studies. J. Biophys. Biochem. Cytol. 10, Part 2, 61-87.
• 32. Bowman, W. (1890) On the minute structure and movements of voluntary muscle. Phil. Trans. Roy. Soc. 130, Part 2, 457-501.
• 33. Nystrom, G. (1897) ueber die Lymphbanen des Herzens. Arch. Anat. Physiol. (Anat. Abt.) 21, 361-378.
• 34. Holmgren, E. (1908) Über die Trophospongien der quergestreiften Muskelfasern, nebst Bemerkungen über die allgemeinen Bau dieser Fasern. Arch. Mikr. Anat. 71, 165-247.
• 35. Huxley, A.F. (1971) The Croonian Lecture 1967. The activation of striated muscle and its mechanical response. Proc. Roy. Soc. London, Series B 178, 1-27.
• 36. Franzini-Armstrong, C. (1994) The sarcoplasmic reticulum and the transverse tubules; in Myology, (Engel, A.G. & Franzini-Armstrong, C., eds.) 2nd edn., vol. 1, pp. 176-199, McGraw-Hill Inc., New York.
• 37. Peachey, L.D. & Franzini-Armstrong, C. (1983) Structure and function of membrane systems of skeletal muscle cells; in Handbook of Physiology. Section 10. Skeletal Muscle (Peachey, L.D., Adrian, R.H. & Geiger, S.R., eds.) pp. 23-71, American Physiological Society, Bethesda.
• 38. Franzini-Armstrong, C. & Peachey, L.D. (1981) Striated muscle contractile and control mechanisms. J. Cell Biol. 91, 166s-186s.
• 39. Bennett, H.S. (1960) The structure of striated muscle as seen by the electron microscope; in The Structure and Function of Muscle (Bourne, G.H., ed.) vol. 1, pp. 137-181, Academic Press, New York.
• 40. Simpson, F.O. & Oertelis, S.J. (1962) The fine structure of sheep myocardial cells: Sarcolemmal invaginations and the transverse tubular system. J. Cell Biol. 12, 91-100.
• 41. Nelson, D.A. & Benson, E.S. (1963) On the structural continuities of the transverse tubular system of rabbit and human myocardial cells. J. Cell Biol. 16, 297-313.
• 42. Franzini-Armstrong, C. & Porter, K.R. (1964) Sarcolemmal invaginations and the T system in fish skeletal muscle. Nature 202, 355-357.
• 43. Franzini-Armstrong, C. & Porter, K.R. (1964) Sarcolemmal invaginations constituting the T-system in fish muscle fibers. J. Cell Biol. 22, 675-696.
• 44. Page, S. (1964) The organization of the sarcoplasmic reticulum in frog muscle. J. Physiol. (London) 175, 10P-11P.
• 45. Huxley, H.E. (1964) Evidence for continuity between the central elements of the triads and extracellular space in frog sartorius muscle. Nature 202, 1067-1071.
• 46. Simpson, F.O. (1965) The transverse tubular system in mammalian myocardial cells. Amer. J. Anat. 117, 1-18.
• 47. Rayns, D.G., Simpson, F.O. & Bertaud, W.S. (1967) Transverse tubule apertures in mammalian myocardial cells: Surface array. Science 156, 656-657.
• 48. Franzini-Armstrong, C. (1970) Studies of the triad. I. Structure of the junction in frog twitch fibers. J. Cell Biol. 47, 488-499.
• 49. Endo, M. (1966) Entry of fluorescent dyes into the sarcotubular system of the frog muscle. J. Physiol. (London) 185, 224-238.
• 50. Hill, D.K. (1964) The space accessible to albumin within the striated muscle fiber of the toad. J. Physiol. (London) 175, 275-294.
• 51. Franzini-Armstrong, C. & Jorgensen, A.O. (1994) Structure and development of E-C coupling units in skeletal muscle. Annu. Rev. Physiol. 56, 509-534.
• 52. Schneider, M.F. (1994) Control of calcium release in functioning skeletal muscle. Annu. Rev. Physiol. 56, 463-484.
• 53. Peachey, L.D. (1965) The sarcoplasmic reticulum and transverse tubules of the frog's sartorius. J. Cell Biol. 25, 209-231.
• 54. Porter, K.R. & Palade, G.E. (1957) Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells. J. Biophys. Biochem. Cytol. 3, 269-300.
• 55. Robertson, J.D. (1956) Some features of the ultrastructure of reptilian skeletal muscle. J. Biophys. Biochem. Cytol. 2, 369-379.
• 56. Robertson, J.D. (1989) Membranes, molecules, nerves, and people; in Membrane Transport. People and Ideas (Tosteson, D.C., ed.) pp. 51-124, American Physiological Society, Bethesda.
• 57. Fawcett, D.W. & Revel, J.P. (1961) The sarcoplasmic reticulum of a fast-acting fish muscle. J. Biophys. Biochem. Cytol. 10, Part 2, 89-109.
• 58. Andersson-Cedergren, E. (1959) Ultrastructure of motor end-plate and sarcoplasmic reticulum components of mouse skeletal muscle fiber as revealed by three-dimensional reconstructions from serial sections. J. Ultrastructure Res. (Suppl.) 1, 1-191.
• 59. Revel, J.P. (1962) The sarcoplasmic reticulum of bat cricothyroid muscle. J. Cell Biol. 12, 571-588.
• 60. Reger, J.F. (1961) The fine structure of neuromuscular junctions and the sarcoplasmic reticulum of extrinsic eye muscles of Fundulus heteroclitus. J. Biophys. Biochem. Cytol. 10, Part 2, 111-121.
• 61. Huxley, A.F. & Taylor, R.E. (1955) Function of Krause's membrane. Nature 176, 1068.
• 62. Huxley, A.F. & Taylor, R.E. (1958) Local activation of striated muscle fibres. J. Physiol. (London) 144, 426-441.
• 63. Podolsky, R.J. (1989) Membrane transport in excitation-contraction coupling; in Membrane Transport. People and Ideas (Tosteson, D.C., ed.) pp. 291-302, American Physiological Society, Bethesda.
• 64. Ashley, C.C., Mulligan, I.P. & Lea, T.J. (1991) Ca2+ and activation mechanisms in skeletal muscle. Quart. Rev. Biophys. 24, 1-73.
• 65. Rios, E. & Pizarro, G. (1991) Voltage sensor of excitation contraction coupling in skeletal muscle. Physiol. Rev. 71, 849-908.
• 66. Meissner, G. (1994) Ryanodine receptor/Ca2+ release channels and their regulation by endogenous effectors. Annu. Rev. Physiol. 56, 485-508.
• 67a. Hill, A.V. (1948) On the time required for diffusion and its relation to processes in muscle. Proc. Roy. Soc. London, Series B 135, 446- 453.
• 67b. Hill, A.V. (1949) The abrupt transition from rest to activity in muscle. Proc. Roy. Soc. London, Series B 136, 399-420.
• 68. Weber, A. (1972) Pysiological regulation of the activity of the actomyosin system; in Molecular Bioenergetics and Macromolecular Biochemistry; pp. 111-117, Springer Verlag, Berlin.
• 69. Ebashi, S. & Endo, M. (1968) Calcium and muscle contraction. Prog. Biophys. Mol. Biol. 18, 123-183.
• 70. Ebashi, S. (1980) The Croonian Lecture, 1979. Regulation of muscle contraction. Proc. Roy. Soc. London, Series B 207, 259-286.
• 71. Hasselbach, W. (1989) From frog lung to calcium pump; in Membrane Transport. People and Ideas (Tosteson, D.C., ed.) pp. 187-201, American Physiological Society, Bethesda.
• 72. Stiles, P.G. (1903) On the rhythmic activity of the oesophagus and the influence upon it of various media. Am. J. Physiol. 5, 338-357.
• 73. Armstrong, C.M., Bezanilla, F.M. & Horowicz, P. (1972) Twitches in the presence of ethylene glycol bis (β-amino-ethylether)-N,N'-tetraacetic acid. Biochim. Biophys. Acta 267, 605-608.
• 74. Bianchi, C.P. & Shanes, A.M. (1959) Calcium influx in skeletal muscle at rest, during activity and during potassium contraction. J. Gen. Physiol. 42, 803-815.
• 75. Bianchi, C.P. & Shanes, A.M. (1960) The effect of the ionic milieu on the emergence of radiocalcium from tendon and from sartorius muscle. J. Cell. Comp. Physiol. 55, 67-76.
• 76. Winegrad, S. (1961) The possible role of calcium in excitation-contraction coupling of heart muscle. Circulation 24, 523-529.
• 77. Gibbons, W.R. & Zygmunt, A.C. (1992) Excitation-contraction coupling in heart; in The Heart and Cardiovascular System (Fozzard, H.A., Haber, E., Jennings, R.B., Katz, A.M. & Morgan, H.E., eds.) 2nd edn., vol. 2, pp. 1249- 1279, Raven Press Ltd., New York.
• 78. Langer, G.A. (1992) Calcium and the heart: Exchange at the tissue, cell and organelle levels. FASEB J. 6, 893-902.
• 79. Thomas, C., Lipp, P., Tovey, S.C., Berridge, M.J., Li, W., Tsien, R.Y. & Bootman, M.D. (2000) Microscopic properties of elementary Ca2+ release sites in nonexcitable cells. Curr. Biol. 10, 8-15.
• 80. Reznikoff, P. & Chambers, R. (1927) Micrurgical studies in cell physiology. III. The action of CO2 and some salts of Na, Ca and K on the protoplasm of Amoeba dubia. J. Gen. Physiol. 10, 731-738.
• 81. Pollack, H. (1928) Micrurgical studies in cell physiology. VI. Calcium ions in living protoplasm. J. Gen. Physiol. 11, 539-545.
• 82. Chambers, R. & Hale, H.P. (1932) The formation of ice in protoplasm. Proc. Roy. Soc. London, Series B 110, 336-352.
• 83. Keil, E.M. & Sichel, F.J.M. (1936) The injection of aqueous solutions including acetylcholine into the isolated muscle fiber. Biol. Bull. 71, 402.
• 84. Weise, E. (1934) Untersuchungen zur Frage der Verteilung und der Bindungsart des Calcium im Muskel. Naunyn-Schmiedeberg's Arch. Exp. Path. Pharm. 176, 367-372.
• 85. Wacker, L. (1929) Zur Kenntniss der Vorgänge bei der Arbeit und Ermüdung des Muskels. Klin. Wochenschrift 8, 244-249.
• 86. Beznak, A. (1931) Über die Erhohung des Calciumgehaltes des Blutserums bei Strychninvergiftung. Naunyn-Schmiedeberg's Arch. Exptl. Pathol. Pharmakol. 160, 397-400.
• 87. Lissak, K. (1934) Beitrage zur Frage der Beziehung zwischen Tetanie und Tetanus. Naunyn-Schmiedeberg's Arch. Exptl. Pathol. Pharmakol. 176, 425-428.
• 88. Woodward, A.A., Jr. (1949) The release of radioactive 45Ca from muscle during stimulation. Biol. Bull. 97, 264.
• 89. Bailey, K. (1942) Myosin and adenosinetriphosphatase. Biochem. J. 36, 121-139.
• 90. Heilbrunn, L.V. (1940) The action of calcium on muscle protoplasm. Physiol. Zool. 13, 88-94.
• 91. Heilbrunn, L.V. (1943) An Outline of General Physiology; 2nd edn., Saunders, Philadelphia.
• 92. Heilbrunn, L.V. (1956) The Dynamics of Living Protoplasm, Academic Press, New York.
• 93. Heilbrunn, L.V. & Wiercinsky, F.J. (1947) Action of various cations on muscle protoplasm. J. Cell. Comp. Physiol. 19, 15-32.
• 94. Kamada, T. & Kinoshita, H. (1943) Disturbances initiated from the naked surface of muscle protoplasm. Japan. J. Zool. 10, 469- 493.
• 95. Campbell, A.K. (1986) Lewis Victor Heilbrunn. Pioneer of calcium as an intracellular regulator. Cell Calcium 7, 287-296.
• 96. Szent-Györgyi, A. (1945) Studies on muscle. Acta Physiol. Scand. 9, Suppl. XXV.
• 97. Szent-Györgyi, A. (1951) Chemistry of Muscular Contraction; 2nd edn., Academic Press, New York.
• 98. Raaflaub, J. (1956) Applications of metal buffers and metal indicators in biochemistry. Methods Biochem. Anal. 3, 301-325.
• 99. Chaberek, S. & Martell, A.E. (1959). Organic sequestering agents, Wiley, New York.
• 100. Weber, A. (1959) On the role of calcium in the activity of adenosine-5'-triphosphate hydrolysis by actomyosin. J. Biol. Chem. 234, 2764-2769.
• 101. Weber, A. & Herz, R. (1961) Requirement for calcium in the synaeresis of myofibrils. Biochem. Biophys. Res. Commun. 6, 364-368.
• 102. Weber, A. & Winicur, S. (1961) The role of calcium in the superprecipitation of actomyosin. J. Biol. Chem. 236, 3198-3202.
• 103. Weber, A. & Herz, R. (1963) The binding of calcium to actomyosin systems in relation to their biological activity. J. Biol. Chem. 238, 599-605.
• 104. Weber, A., Herz, R. & Reiss, I. (1963) On the mechanism of the relaxing effect of fragmented sarcoplasmic reticulum. J. Gen. Physiol. 46, 679-702.
• 105. Weber, A., Herz, R. & Reiss, I. (1964) Role of calcium in contraction and relaxation of muscle. Fed. Proc. 23, 896-900.
• 106. Weber, A., Herz, R. & Reiss, I. (1964) The regulation of myofibrillar activity by calcium. Proc. Roy. Soc. London, Series B 160, 489-501.
• 107. Weber, A. (1966) Energized calcium transport and relaxing factors. Curr. Top. Bioenerg. 1, 203-254.
• 108. Ebashi, S. (1960) Calcium binding and relaxation in the actomyosin system. J. Biochem. (Tokyo) 48, 150-151.
• 109. Ebashi, S., Ebashi, F. & Fujie, Y. (1960) The effect of EDTA and its analogues on glycerinated muscle fibers and myosin adenosine triphosphatase. J. Biochem. (Tokyo) 47, 5459.
• 110. Ebashi, S. (1961) Calcium binding activity of vesicular relaxing factor. J. Biochem. (Tokyo) 50, 236-244.
• 111. Ebashi, S. (1961) The role of relaxing factor in contraction-relaxation cycle of muscle. Progr. Theoretical Physics, Suppl. 17, 35-40.
• 112. Natori, (1965) Effects of Na and Ca ions on the excitability of isolated myofibrils; in Molecular Biology of Muscular Contraction (Ebashi, S., Oosawa, F., Sekine, T. & Tonomura, Y., eds.) vol. 9, pp. 190-196, Elsevier, Amsterdam.
• 113. Podolsky, R.J. & Costantin, L.L. (1964) Regulation by calcium of the contraction and relaxation of muscle fibers. Fed. Proc. 23, 933-939.
• 114. Portzehl, H., Caldwell, P.C. & Ruegg, J.C. (1964) The dependence of contraction and relaxation of muscle fibers from the crab Maia squinado on the internal concentration of free calcium ions. Biochim. Biophys. Acta 79, 581-591.
• 115. Blinks, J.R. (1992) Intracellular [Ca2+] measurements; in The Heart and the Cardiovascular System, 2nd edn. (Fozzard, H.A. et al., eds.) pp. 1171-1201, Raven Press Ltd., New York.
• 116. Ridgway, E.G. & Ashley, C.C. (1967) Calcium transients in single muscle fibers. Biochem. Biophys. Res. Commun. 29, 229-234.
• 117. Ashley, C.C. & Ridgway, E.G. (1970) On the relationships between membrane potential, calcium transient and tension in single barnacle muscle fibres. J. Physiol. 209, 105- 130.
• 118. Jobsis, F.F. & O'Connor, M.J. (1966) Calcium release and reabsorption in the sartorius muscle of the toad. Biochem. Biophys. Res. Commun. 25, 246-252.
• 119. Tsien, R.Y. (1992) Intracellular signal transduction in 4 dimensions From molecular design to physiology. Am. J. Physiol. 263, C723-C728.
• 120. Tsien, R.Y. (1999) Monitoring cell calcium; in Calcium as a Cellular Regulator (Carafoli, E. & Klee, C., eds.) pp. 28-54, Oxford University Press, New York.
• 121. Ashley, C.C., Griffiths, P.J., Lea, T.J., Mulligan, I.P., Palmer, R.E., Simmett, S.J. (1993) Barnacle muscle: Ca.ctivation and mechanics. Rev. Physiol. Biochem. Pharmacol. 122, 149-258.
• 122. Niggli, E. (1999) Localized intracellular calcium signalling in muscle: Calcium sparks and calcium quarks. Annu. Rev. Physiol. 61, 311-335.
• 123. Engelhardt, W.A. & Ljubimova, M.N. (1939) Myosin and adenosine triphosphatase. Nature 144, 668-669.
• 124. Engelhardt, W.A. (1946) Adenosine triphosphatase properties of myosin. Adv. Enzymol. 6, 147-191.
• 125. Engelhardt, W.A. (1982) Life and science. Annu. Rev. Biochem. 51, 1-19.
• 126. Banga, I. & Szent-Györgyi, A. (1941) Preparation and properties of myosin A and B. Studies from the Institute of Medical Chemistry, University of Szeged Vol. 1, 5-15.
• 127. Straub, F.B. (1942) Actin. Studies from the Institute of Medical Chemistry, University of Szeged, vol. 2, 3-15.
• 128. Straub, F.B. (1943) Actin II. Studies from the Institute of Medical Chemistry, University of Szeged, vol. 3, 23-37.
• 129. Szent-Györgyi, A. (1941) The Contraction of Myosin Threads. Studies from the Institute of Medical Chemistry, University of Szeged, vol. 1, 17-26.
• 130. Szent-Györgyi, A. (1963) Lost in the twentieth century. Annu. Rev. Biochem. 32, 1-14.
• 131. Moss, R.W. (1988) Free Radical. Albert Szent- Gyoergyi and the Battle over Vitamin C. Paragon House Publ., New York.
• 132. Szent-Györgyi, A. (1942) The Reversibility of the Contraction of Myosin Threads. Studies from the Institute of Medical Chemistry, University of Szeged, vol. 2, 25-26.
• 133. Marsh, B.B. (1951) A factor modifying muscle fiber syneresis. Nature 167, 1065-1066.
• 134. Marsh, V.B. (1952) The effects of adenosine triphosphate on the fibre volume of a muscle homogenate. Biochim. Biophys. Acta 9, 247- 260.
• 135. Bendall, J.R. (1952) Effect of the Marsh factor on the shortening of muscle fiber models in the presence of adenosine triphosphate. Nature 170, 1058-1060.
• 136. Bendall, J.R. (1953) Further observations on a factor (the Marsh factor) effecting relaxation of ATP-shortened muscle fiber models and the effect of Ca and Mg ions upon it. J. Physiol. (London) 121, 232-254.
• 137. Bendall, J.R. (1958) Relaxation of glycerol- treated muscle fibers by ethylenediamine tetraacetate. Arch. Biochem. Biophys. 73, 283-285.
• 138. Bendall, J.R. (1969) Muscles, Molecules, Movement. American Elsevier Publ. Co., New York.
• 139. Hasselbach, W. & Weber, H.H. (1953) Der Einfluss des MB-Factors auf die Kontraktion des Faser modells. Biochim. Biophys. Acta 11, 160-161.
• 140. Fujita, K. (1954) Action of adenosine derivatives on muscle activity. Part II. Glycerol- treated muscle and relaxing factor. Folia Pharmacol. Japonica 50, 183-192.
• 141. Kumagai, H., Ebashi, S. & Takeda, F. (1955) Essential relaxing factor in muscle other than myokinase and creatine phosphokinase. Nature 176, 166.
• 142. Ebashi, S. (1957) Kielley-Meyerhof's granules and the relaxation of glycerinated muscle fibers. Conference on the Chemistry of Muscle Contraction; pp. 89-94, Igaku Shoin Ltd, Osaka.
• 143. Ebashi, S. (1958) A granule-bound relaxation factor in skeletal muscle. Arch. Biochem. Biophys. 76, 410-423.
• 144. Kielley, W.N. & Meyerhof, O. (1948) A new magnesium-activated adenosine triphosphatase from muscle. J. Biol. Chem. 174, 387-388.
• 145. Kielley, W.W. & Meyerhof, O. (1948) Studies on adenosine triphosphatase of muscle. II. A new magnesium activated adenosine triphosphatase. J. Biol. Chem. 176, 591-601.
• 146. Kielley, W.W. & Meyerhof, O. (1950) Studies on adenosine triphosphatase of muscle. III. The lipoprotein nature of the magnesium activated adenosine triphosphatase. J. Biol. Chem. 183, 391-401.
• 147. Muscatello, U., Andersson-Cedergren, E., Azzone, G.G. & Von der Decken, A. (1961) The sarcotubular system of frog skeletal muscle. A morphological and biochemical study. J. Biophys. Biochem. Cytol. 10, Part 2, 201-218.
• 148. Muscatello, U., Andersson-Cedergren, E. & Azzone, G.F. (1962) The mechanism of muscle-fiber relaxation, adenosine triphosphatase and relaxing activity of the sarcotubular system. Biochim. Biophys. Acta 63, 55-74.
• 149. Ebashi, S. & Lipmann, F. (1962) Adenosine triphosphate-linked concentration of calcium ions in a particulate fraction of rabbit muscle. J. Cell Biol. 14, 389-400.
• 150. Hasselbach, W. & Makinose, M. (1961) Die Calciumpumpe der Erschlaffungsgrana des Muskels und ihre Abhngigkeit von der ATP-Spaltung. Biochem. Z. 333, 518-528.
• 151. Hasselbach, W. & Makinose, M. (1962) ATP and active transport. Biochem. Biophys. Res. Commun. 7, 132-136.
• 152. Hasselbach, W. & Makinose, M. (1963) über den Mechanismus des Calciumtransportes durch die Membranen des Sarkoplasmatischen Reticulums. Biochem. Z. 339, 94-111.
• 153. Vasington, F. & Murphy, J.V. (1962) Ca2+ uptake by rat kidney mitochondria and its dependence on respiration and phosphorylation. J. Biol. Chem. 237, 2670-2677.
• 154. Hasselbach, W. (1964) Relaxation and the sarcotubular calcium pump. Fed. Proc. 23, 909-912.
• 155. Costantin, L.L., Franzini-Armstrong, C. & Podolsky, R.J. (1965) Localization of calcium-accumulating structures in striated muscle fibers. Science 147, 158-160.
• 156. Podolsky, R.J., Hall, T. & Hatchett, S.L. (1970) Identification of oxalate precipitates in striated muscle fibers. J. Cell Biol. 44, 699-702.
• 157. Skou, J.C. (1957) The influence of some cations on an adenosine triphosphatase from peripheral nerves. Biochim. Biophys. Acta 23, 394-401.
• 158. Skou, J.C. (1960) Further investigations on a Mg2+ + Na+ activated adenosine triphosphatase, possibly related to the active, linked transport of Na+ and K+ across the nerve membrane. Biochim. Biophys. Acta 42, 6-23.
• 159. Skou, J.C. (1989) Sodium-potassium pump; in Membrane Transport. People and Ideas (Tosteson, D.C., ed.) pp. 155-185, American Physiological Society, Bethesda.
• 160. Post, R.L. & Jolly, P.C. (1957) The linkage of sodium, potassium and ammonium active transport across the human erythrocyte membrane. Biochim. Biophys. Acta 25, 118-128.
• 161. Post, R.L., Merritt, C.R., Kinsolving, C.R. & Albright, C.D. (1960) Membrane adenosine triphosphatase as a participant in the active transport of sodium and potassium in the human erythrocyte. J. Biol. Chem. 235, 1796-1802.
• 162. Post, R.L. (1989) Seeds of sodium, potassium ATPase. Annu. Rev. Physiol. 51, 1-15.
• 163. Moller, J.V., Juul, B. & Lemaire, M. (1996) Structural organization, ion transport and energy transduction of P-type ATPases. Biochim. Biophys. Acta 1286, 1-51.
• 164. Geering, K. (2000) Topogenic motifs in P-type ATPases. J. Membr. Biol. 174, 181-190.
• 165. Mueller, H. (1960) The action of relaxing factor on actomyosin. Biochim. Biophys. Acta 39, 93-103.
• 166. Bozler, E. (1954) Relaxation in extracted muscle fibers. J. Gen. Physiol. 38, 149-159.
• 167. Bozler, E. (1955) Binding of calcium and magnesium by the contractile elements. J. Gen. Physiol. 38, 735-742.
• 168. Watanabe, S. & Sleator, W., Jr. (1957) EDTA relaxation of glycerol-treated muscle fibers and the effects of magnesium, calcium and manganese ions. Arch. Biochem. Biophys. 68, 81-101.
• 169. Ebashi, F. (1961) Does EDTA bind to actomyosin? J. Biochem. (Tokyo) 50, 77-78.
• 170. Baird, G.D. & Perry, S.V. (1960) The inhibitory action of relaxing factor preparations on the myofibrillar adenosine triphosphatase. Biochem. J. 77, 262-271.
• 171. Makinose, M. & Hasselbach, W. (1965) Der Einfluss von Oxalat auf den Calcium Transport isolierter Vesikel des sarkoplasmatischen Reticulum. Biochem. Z. 343, 360-382.
• 172. Martonosi, A. & Feretos, R. (1964) Sarcoplasmic reticulum. I. The uptake of calcium by sarcoplasmic reticulum fragments. J. Biol. Chem. 239, 648-658.
• 173. Seidel, J.C. & Gergely, J. (1964) Studies on myofibrillar adenosine triphosphatase with calcium-free adenosine triphosphate. II. Concerning the mechanism of inhibition by the fragmented sarcoplasmic reticulum. J. Biol. Chem. 239, 3331-3335.
• 174. Lorand, L. (1964) Relaxing particles of skeletal muscle. Fed. Proc. 23, 905-908.
• 175. Perry, S.V. & Grey, T.C. (1956) Ethylenediamine tetraacetate and the adenosine triphosphatase activity of actomyosin. Biochem. J. 64, 5P.
• 176. Ebashi, S. (1963) Third component participating in the superprecipitation of natural actomyosin. Nature 200, 1010.
• 177. Ebashi, S. & Ebashi, F. (1964) A new protein component participating in the superprecipitation of myosin B. J. Biochem. (Tokyo) 55, 604-613.
• 178. Ebashi, S., Endo, M. & Ohtsuki, I. (1969) Control of muscle contraction. Quart. Rev. Biophys. 2, 351-384.
• 179a. Ebashi, S. (1993) From the relaxing factor to troponin. Biomedical Res. 14, Suppl. 2, 1-7.
• 179b. Ebashi, S., Endo, M. & Ohtsuki, I. (1999) Calcium in muscle contraction; in Calcium as a Cellular Regulator (Carafoli, E. & Klee, C., eds.) pp. 579-595, Oxford University Press, New York.
• 180. Dux, L. (1993) Muscle relaxation and sarcoplasmic reticulum in different muscle types. Rev. Physiol. Biochem. Pharmacol. 122, 69-147.
• 181. Martonosi, A. (1975) Membrane transport during development in animals. Biochim. Biophys. Acta 415, 311-333.
• 182. Sarzala, M.G., Pilarska, M., Zubrzycka, E. & Michalak, M. (1975) Changes in the structure, composition, and function of sarcoplasmic reticulum membrane during development. Eur. J. Biochem. 57, 25-34.
• 183. Martonosi, A. (1982) The development of sarcoplasmic reticulum membranes. Annu. Rev. Physiol. 44, 337-355.
• 184. Martonosi, A. (2000) The Development of Sarcoplasmic Reticulum, Harwood Academic Publishers, Amsterdam.
• 185. Martonosi, A. (1994) The regulation of calcium by the sarcoplasmic reticulum; in Myology (Engel, A.G. & Franzini-Armstrong, C., eds.) 2nd edn., vol. 1, pp. 553-584, McGraw-Hill, New York.
• 186. Jencks, W.P. (1989) How does a calcium pump pump calcium? J. Biol. Chem. 264, 18855-18858.
• 187. MacLennan, D.H., Rice, W.J. & Green, N.M. (1997) The mechanism of Ca2+ transport by sarco(endo)plasmic reticulum Ca2+-ATPase. J. Biol. Chem. 272, 28815-28818.
• 188. Tada, M. (1992) Molecular structure and function of phospholamban in regulating the calcium pump from sarcoplasmic reticulum. Ann. N.Y. Acad. Sci. 671, 92-102.
• 189. MacLennan, D.H., Brandl, 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.
• 190a. Taylor, K.A., Dux, L., Varga, S., Ting-Beall, H.P. & Martonosi, A. (1988) Analysis of two dimensional crystals of Ca2+-ATPase in sarcoplasmic reticulum. Methods Enzymol. 157, 271-289.
• 190b. Pikula, S., Muellner, N., Dux, L. & Martonosi, A. (1988) Stabilization and crystallization of Ca2+-ATPase in detergent-solubilized sarcoplasmic reticulum. J. Biol. Chem. 263, 5277-5286.
• 191. Martonosi, A.N., Taylor, K.A. & Pikula, S. (1991) The crystallization of the Ca2+- ATPase of sarcoplasmic reticulum; in Crystallization of Membrane Proteins (Michel, H., ed.) pp. 167-182, CRC Press, Boca Raton.
• 192. Toyoshima, Ch., Nakasako, M., Nomura, H. & Ogawa, H. (2000) Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 A resolution. Nature 405, 647-655.
• 193a. Huxley, H.E. (1996) A personal view of muscle and motility mechanisms. Annu. Rev. Physiol. 58, 1-20.
• 193b. Huxley, H.E. (2000) Past, present and future experiments on muscle. Philos Trans. R. Soc. Lond B Biol Sci, Series B 355, 539-543.
• 194. Huxley, A.F. (2000) Mechanics and models of the myosin motor. Phil. Trans. Roy. Soc. London, Series B 355, 433-440.
• 195. Rayment, I. & Holden, H.M. (1994) The three-dimensional structure of a molecular motor. Trends Biochem. Sci. 19, 129-134.
• 196. Rayment, I., Smith, C. & Yount, R.G. (1996) The active site of myosin. Annu. Rev. Physiol. 58, 671-702.
• 197a. Holmes, K.C. (1998) Muscle contraction; in The Limits of Reductionism in Biology, Novartis Foundation Symp. 213, pp. 76-92, John Wiley and Sons.
• 197b. Holmes, K.C. & Geeves, M.A. (2000) The structural basis of muscle contraction. Phil. Trans. Roy. Soc. London, Series B 355, 419-431.
• 198. Geeves, M.A. & Holmes, K.C. (1999) Structural mechanism of muscle contraction. Annu. Rev. Biochem. 68, 687-728.
• 199. Yanagida, T., Kitamura, K., Tanaka, H., Iwane, A.H. & Esaki, S. (2000) Single molecule analysis of the actomyosin motor. Curr. Opin. Cell Biol. 12, 20-25.
• 200. Leavis, P.C. & Gergely, J. (1984) Thin filament proteins and thin filament-linked regulation of vertebrate muscle contraction. CRC Crit. Rev. Biochem. 16, 235-305.
• 201. Lehrer, S.S. (1994) The regulatory switch of the muscle thin filament. J. Muscle Res. Cell Motil. 15, 232-236.
• 202. Perry, S.V. (1996) Molecular Mechanisms in Striated Muscle. Cambridge University Press, Cambridge.
• 203. Kress, M., Huxley, H.E., Faruqi, A.R. & Hendrix, J. (1986) Structural changes during activation of frog muscle studied by time-resolved X-ray diffraction. J. Mol. Biol. 188, 325-342.
• 204. Strynadka, N.C.J. & James, M.N.G. (1991) Towards an understanding of the effects of calcium on protein structure and function. Curr. Opin. Struct. Biol. 1, 905-914.
• 205. Farah, C.S. & Reinach, F.C. (1995) The troponin complex and regulation of muscle contraction. FASEB J. 9, 755-767.
• 206. Szent-Györgyi, A.G. & Chantler, P.D. (1994) Control of contraction by calcium binding to myosin; in Myology, (Engel, A.G. & Franzini- Armstrong, C., eds.) 2nd edn., pp. 506-528, McGraw-Hill Inc., New York.
• 207. Kendrick-Jones, J., Lehman, W. & Szent- Gyoergyi, A.G. (1970) Regulation in molluscan muscles. J. Mol. Biol. 54, 313-326.
• 208. Horowitz, A., Menice, C.B., Laporte, R. & Morgan, K.G. (1996) Mechanisms of smooth muscle contraction. Physiol. Rev. 76, 967- 1003.
• 209. Somlyo, A.P., Wu, X., Walker, L.A. & Somlyo, A.V. (1999) Pharmacomechanical coupling: The role of calcium, G proteins, kinases and phosphatases. Rev. Physiol. Biochem. Pharmacol. 134, 201-234.
• 210. Marston, S. (1995) Ca2+ dependent protein switches in actomyosin-based contractile systems. Int. J. Biochem. Cell Biol. 27, 97-108.
• 211. Lehman, W. & Szent-Györgyi, A.G. (1975) Regulation of muscular contraction. Distribution of actin control and myosin control in the animal kingdom. J. Gen. Physiol. 66, 1-30.
• 212. Ozawa, E. & Ebashi, S. (1967) Requirement of Ca2+ ion for the stimulating effect of cyclic 3',5'-AMP on muscle phosphorylase b kinase. J. Biochem. (Tokyo) 62, 285-286.
• 213. Kakiuchi, S., Yamazaki, R. & Nakajima, H. (1970) Properties of a heat stable phosphodiesterase activating factor isolated from brain extract. Proc. Japan Acad. 46, 587- 592.
• 214. Cheung, W.Y. (1970) Cyclic 3',5'-nucleotide phosphodiesterase: Demonstration of an activator. Biochem. Biophys. Res. Commun. 38, 533-538.
• 215. Nakayama, S. & Kretsinger, R.H. (1994) Evolution of the EF-band family of proteins. Annu. Rev. Biophys. Biomol. Struct. 23, 473-507.
• 216. Weinstein, H. & Mehler, E.L. (1994) Ca2+ binding and structural dynamics in the functions of calmodulin. Annu. Rev. Physiol. 56, 213-236.
• 217. Loewenstein, W.R. (1989) From cell theory to cell connectivity: Experiments in cell-to- cell communication; in Membrane Transport. People and Ideas (Tosteson, D.C., ed.) American Physiological Society, Bethesda.
• 218. Costantin, L.L. (1975) Contractile activation in skeletal muscle. Progr. Biophys. Mol. Biol. 29, 197-224.
• 219. Rios, E., Pizarro, G. & Stefani, E. (1992) Charge movement and the nature of signal transduction in skeletal muscle excitation- contraction coupling. Annu. Rev. Physiol. 54, 109-133.
• 220. Catterall, W.A. (1995) Structure and function of voltage-gated ion channels. Annu. Rev. Biochem. 64, 493-531.
• 221. Shoshan-Barmatz, V. & Ashley, R.H. (1998) The structure, function and cellular regulation of ryanodine-sensitive Ca2+-release channels. Int. Rev. Cytol. 183, 185-270.
• 222. Wagenknecht, T. & Radermacher, M. (1997) Ryanodine receptors: Structure and macromolecular interactions. Curr. Opin. Struct. Biol. 7, 258-265.
• 223. Sharma, M.R., Jeyakumar, L.H., Fleischer, S. & Wagenknecht, T. (2000) Three-dimensional structure of ryanodine receptor isoform three in two conformational states as visualized by cryo-electron microscopy. J. Biol. Chem. 275, 9485-9491.
• 224. Wier, W.G. (1992) [Ca2+]: Transients during excitation-contraction coupling of mammalian heart; in The Heart and the Cardiovascular System (Fozzard, H.A. et al., eds.) 2nd edn., vol. 2, pp. 1223-1248, Raven Press Ltd, New York.
• 225. Hauschka, S.D. (1994) The embryonic origin of muscle; in Myology (Engel, A.G. & Franzini-Armstrong, C., eds.) 2nd edn., vol. 1, pp. 3-73, McGraw-Hill, Inc., New York.
• 226. Stockdale, F.E. (1997) Mechanisms of formation of muscle fiber types. Cell Struct. Funct. 22, 37-43.
• 227. Schiaffino, S. & Reggiani, C. (1996) Molecular diversity of myofibrillar proteins: Gene regulation and functional significance. Physiol. Rev. 76, 371-423.
• 228. Williams, R.S. & Neufer, P.D. (1996) Regulation of gene expression in skeletal muscle by contractile activity; in The Handbook of Physiology: Integration of Motor, Circulatory, Respiratory and Metabolic Control During Exercise (Rowell, L.B. & Shepard, J.T., eds.) pp. 1124-1150, American Physiological Society, Bethesda.
• 229. Pette, D. & Staron, R.S. (1997) Mammalian skeletal muscle fiber type transitions. Int. Rev. Cytol. 170, 143-223.
• 230. Pette, D., Peuker, H. & Staron, R.S. (1999) The impact of biochemical methods for single muscle fibre analysis. Acta Physiol. Scand. 166, 261-277.
• 231. Wu, H., Naya, F.J., McKinsey, T.A., Mercer, B., Shelton, J.M., Chiu, E.R., Simard, A.R., Michel, R.N., Bassel-Duby, R., Olson, E.N. & Sanders Williams, R. (2000) MEF2 responds to multiple calcium-regulated signals in the control of skeletal muscle fiber type. EMBO J. 19, 1963-1973.
• 232. Cruzalegui, F.M. & Bading, H. (2000) Calcium regulated protein kinase cascades and their transcription factor targets. Cell. Mol. Life Sci. 57, 402-410.
• 233. Santella, L. & Bolsover, S. (1999) Calcium in the nucleus; in Calcium as a Cellular Regulator (Carafoli, E. & Klee, C., eds.) pp. 487-511, Oxford University Press, New York.
• 234. Siekewitz, P. (1991) Citations and the tenor of the times. FASEB J. 5, 139.