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Biophysical Reviews

, Volume 7, Issue 4, pp 421–447 | Cite as

Historical perspective on heart function: the Frank–Starling Law

  • Vasco Sequeira
  • Jolanda van der Velden
Review

Abstract

More than a century of research on the Frank–Starling Law has significantly advanced our knowledge about the working heart. The Frank–Starling Law mandates that the heart is able to match cardiac ejection to the dynamic changes occurring in ventricular filling and thereby regulates ventricular contraction and ejection. Significant efforts have been attempted to identify a common fundamental basis for the Frank–Starling heart and, although a unifying idea has still to come forth, there is mounting evidence of a direct relationship between length changes in individual constituents (cardiomyocytes) and their sensitivity to Ca2+ ions. As the Frank–Starling Law is a vital event for the healthy heart, it is of utmost importance to understand its mechanical basis in order to optimize and organize therapeutic strategies to rescue the failing human heart. The present review is a historic perspective on cardiac muscle function. We “revive” a century of scientific research on the heart’s fundamental protein constituents (contractile proteins), to their assemblies in the muscle (the sarcomeres), culminating in a thorough overview of the several synergistically events that compose the Frank–Starling mechanism. It is the authors’ personal beliefs that much can be gained by understanding the Frank–Starling relationship at the cellular and whole organ level, so that we can finally, in this century, tackle the pathophysiologic mechanisms underlying heart failure.

Keywords

Frank–Starling Heart Cardiomyocytes Myofilaments History 

Notes

Acknowledgments

We acknowledge support from the Netherlands organization for scientific research (NWO; VIDI grant 91711344).

Compliance with ethical standards

Conflict of interest

Vasco Sequeira declares that he has no conflict of interest.

Jolanda van der Velden declares that she has no conflict of interest.

Ethical approval

This article does not contain any studies with human or animal subjects performed by the authors.

References

  1. Abbott BC, Mommaerts WFHM (1959) A study of inotropic mechanisms in the papillary muscle preparation. J Gen Physiol 42:533–561PubMedCentralPubMedCrossRefGoogle Scholar
  2. Agarkova I, Perriard J-C (2005) The M-band: an elastic web that crosslinks thick filaments in the center of the sarcomere. Trends Cell Biol 15:477–485PubMedCrossRefGoogle Scholar
  3. Aird W (2011) Discovery of the cardiovascular system: from Galen to William Harvey. J Thromb Haemost 9:118–129PubMedCrossRefGoogle Scholar
  4. Allen DG, Kentish JC (1985) The cellular basis of the length-tension relation in cardiac muscle. J Mol Cell Cardiol 17:821–840PubMedCrossRefGoogle Scholar
  5. Allen D, Kentish J (1988) Calcium concentration in the myoplasm of skinned ferret ventricular muscle following changes in muscle length. J Physiol 407:489–503PubMedCentralPubMedCrossRefGoogle Scholar
  6. Allen DG, Kurihara S (1982) The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. J Physiol 327:79–94PubMedCentralPubMedCrossRefGoogle Scholar
  7. Allen DG, Orchard CH (1987) Myocardial contractile function during ischemia and hypoxia. Circ Res 60:153–168PubMedCrossRefGoogle Scholar
  8. Allen DG, Jewell BR, Murray JW (1974) The contribution of activation processes to the length-tension relation of cardiac muscle. Nature 248:606–607PubMedCrossRefGoogle Scholar
  9. Arteaga GM, Palmiter KA, Leiden JM, Solaro RJ (2000) Attenuation of length dependence of calcium activation in myofilaments of transgenic mouse hearts expressing slow skeletal troponin I. J Physiol 526:541–549PubMedCentralPubMedCrossRefGoogle Scholar
  10. Babu A, Sonnenblick E, Gulati J (1988) Molecular basis for the influence of muscle length on myocardial performance. Science 240:74–76PubMedCrossRefGoogle Scholar
  11. Bailey K (1942) Myosin and adenosinetriphosphatase. Biochem J 36:121–139PubMedCentralPubMedCrossRefGoogle Scholar
  12. Bailey K (1946) Tropomyosin: a new asymmetric protein component of muscle. Nature 157:368–369PubMedCrossRefGoogle Scholar
  13. Bailey K (1948) Tropomyosin: a new asymmetric protein component of the muscle fibril. Biochem J 43:271–279PubMedCentralPubMedCrossRefGoogle Scholar
  14. Behrmann E et al (2012) Structure of the rigor actin-tropomyosin-myosin complex. Cell 150:327–338PubMedCentralPubMedCrossRefGoogle Scholar
  15. Bendall JR (1953) Further observations on a factor (the ‘Marsh’ factor) effecting relaxation of ATP-shortened muscle-fibre models, and the effect of Ca and Mg ions upon it. J Physiol 121:232–254PubMedCentralPubMedCrossRefGoogle Scholar
  16. Bendall JR (1954) The relaxing effect of myokinase on muscle fibres; Its identity with the ‘Marsh’ factor. Proc R Soc Lond B Biol Sci 142:409–426PubMedCrossRefGoogle Scholar
  17. Bhuiyan MS, Gulick J, Osinska H, Gupta M, Robbins J (2012) Determination of the critical residues responsible for cardiac myosin binding protein C’s interactions. J Mol Cell Cardiol 53:838–847PubMedCentralPubMedCrossRefGoogle Scholar
  18. Biesiadecki BJ, Chong SM, Nosek TM, Jin J-P (2007) Troponin T core structure and the regulatory NH2-terminal variable region. Biochemistry 46:1368–1379PubMedCentralPubMedCrossRefGoogle Scholar
  19. Biesiadecki BJ et al (2010) Removal of the cardiac troponin I N-terminal extension improves cardiac function in aged mice. J Biol Chem 285:19688–19698PubMedCentralPubMedCrossRefGoogle Scholar
  20. Blasius W (1872) Am Froschherzen angestellte versuche uber die Herz-Arbeit unter verschiedenen innerhalb des Kreislaufes herrschenden Druck-Verhaltnissen. Verhandl Phys Med Ges 2:49Google Scholar
  21. Blix M (1891) Die Lange und Spannung des Muskels. Skandinavisches Archiv Physiol 5:173–206CrossRefGoogle Scholar
  22. Boontje NM et al (2011) Enhanced myofilament responsiveness upon b-adrenergic stimulation in post-infarct remodeled myocardium. J Mol Cell Biol 50:487–499Google Scholar
  23. Bowman W (1840) On the minute structure and movements of voluntary muscle. Phil Trans Royal Soc Lond 130:457–501CrossRefGoogle Scholar
  24. Bozler E (1954) Relaxation in extracted muscle fibers. J Gen Physiol 38:149–159PubMedCentralPubMedCrossRefGoogle Scholar
  25. Brandt P, Lopez E, Reuben J, Grundfest H (1967) The relationship between myofilament packing density and sarcomere length in frog striated muscle. J Cell Biol 33:255–263PubMedCentralPubMedCrossRefGoogle Scholar
  26. Bremel RD, Weber A (1972) Cooperation within actin filament in vertebrate skeletal muscle. Nat New Biol 238:97–101PubMedCrossRefGoogle Scholar
  27. Brutsaert DL, Sys SU (1989) Relaxation and diastole of the heart. Physiol Rev 69:1228–1315PubMedGoogle Scholar
  28. Cazorla O, Vassort G, Garnier D, Le Guennec J-Y (1999) Length modulation of active force in tat cardiac myocytes: is titin the sensor? J Mol Cell Cardiol 31:1215–1227PubMedCrossRefGoogle Scholar
  29. Cazorla O, Wu Y, Irving TC, Granzier H (2001) Titin-based modulation of calcium sensitivity of active tension in mouse skinned cardiac myocytes. Circ Res 88:1028–1035PubMedCrossRefGoogle Scholar
  30. Cazorla O et al (2006) Length and protein kinase A modulations of myocytes in cardiac myosin binding protein C-deficient mice. Cardiovasc Res 69:370–380PubMedCrossRefGoogle Scholar
  31. Chalovich JM, Eisenberg E (1982) Inhibition of actomyosin ATPase activity by troponin-tropomyosin without blocking the binding of myosin to actin. J Biol Chem 257:2432–2437PubMedCentralPubMedGoogle Scholar
  32. Chapman CB, Mitchell JH (1965) Starling on the heart. Facsimile reprints including the Linacre Lecture on the Law of the Heart. Dawsons of Pall MallGoogle Scholar
  33. Chung CS, Granzier HL (2011) Contribution of titin and extracellular matrix to passive pressure and measurement of sarcomere length in the mouse left ventricle. J Mol Cell Cardiol 50:731–739PubMedCentralPubMedCrossRefGoogle Scholar
  34. Close RI (1972) The relations between sarcomere length and characteristics of isometric twitch contractions of frog sartorius muscle. J Physiol 220:745–762PubMedCentralPubMedCrossRefGoogle Scholar
  35. Cooke R, Bialek W (1979) Contraction of glycerinated muscle fibers as a function of the ATP concentration. Biophys J 28:241–258PubMedCentralPubMedCrossRefGoogle Scholar
  36. Craig R, Offer G (1976) The location of C-protein in rabbit skeletal muscle. Proc R Soc Lond B Biol Sci 192:451–461PubMedCrossRefGoogle Scholar
  37. de Tombe PP et al (2010) Myofilament length dependent activation. J Mol Cell Cardiol 48:851–858PubMedCentralPubMedCrossRefGoogle Scholar
  38. Dobie WM (1849) XII - ”Observations on the minute structure and mode of contraction of voluntary muscular fibre"; being the abstract of a paper read before the Royal Medical Society, Edinburgh, December 15th, 1848. J Nat Hist 3:109–119CrossRefGoogle Scholar
  39. Donaldson SK, Kerrick WG (1975) Characterization of the effects of Mg2+ on Ca2+- and Sr2+-activated tension generation of skinned skeletal muscle fibers. J Gen Physiol 66:427–444PubMedCrossRefGoogle Scholar
  40. dos Remedios CG, Millikan RGC, Morales MF (1972) Polarization of tryptophan fluorescence from single striated muscle fibers. A molecular probe of contractile state. J Gen Physiol 59:103–120PubMedCentralPubMedCrossRefGoogle Scholar
  41. Drabikowski W, Nonomura Y (1968) The interaction of troponin with F-actin and its abolition by tropomyosin. Biochim Biophys Acta 160:129–131PubMedCrossRefGoogle Scholar
  42. Drabikowski W, Dabrowska R, Barylko B (1971a) Separation and characterization of the constituents of troponin. FEBS Lett 12:148–152PubMedCrossRefGoogle Scholar
  43. Drabikowski W, Rafalowska U, Dabrowska R, Szpacenko A, Barylko B (1971b) The effect of proteolytic enzymes on the troponin complex. FEBS Lett 19:259–263PubMedCrossRefGoogle Scholar
  44. Dreser H (1887) Ueber Herzarbeit und Herzgifte. Naunyn-Schmiedeberg’s Archiv Pharmacol 24:221–240CrossRefGoogle Scholar
  45. Ebashi S (1960) Calcium binding and relaxation in the actomyosin system. Biochem J 48:150–151Google Scholar
  46. Ebashi S (1961a) Calcium binding activity of vesicular relaxing factor. J Biochem 50:236–244Google Scholar
  47. Ebashi S (1961b) The "role" of the relaxing factor and the contraction-relaxation cycle of skeletal muscle. Prog Theor Phys 17:35–40CrossRefGoogle Scholar
  48. Ebashi S (1963) Third component participating in the super precipitation of ‘natural actomyosin’. Nature 200:1010PubMedCrossRefGoogle Scholar
  49. Ebashi S (1968) E.M. Calcium ion and muscle contraction. Prog Biophys Mol Biol 18:123–183PubMedCrossRefGoogle Scholar
  50. Ebashi F, Ebashi S (1962) Removal of calcium and relaxation in actomyosin systems. Nature 194:378–379PubMedCrossRefGoogle Scholar
  51. Ebashi S, Ebashi F (1964) A new protein component participating in the superprecipitation of myosin B. J Biochem 55:604–613PubMedGoogle Scholar
  52. Ebashi S, Endo M (1968) Calcium ion and muscle contraction. Prog Biophys Mol Biol 18:121–139CrossRefGoogle Scholar
  53. Ebashi S, Kodama A (1965) A new protein factor promoting aggregation of tropomyosin. J BIochem 58:107–108PubMedGoogle Scholar
  54. Ebashi S, Kodama A (1966) Native tropomyosin-like action of troponin on trypsin-treated myosin B. J Biochem 60:733–734PubMedGoogle Scholar
  55. Ebashi S, Lipmann F (1962) Adenosine triphosphate-linked concentration of calcium ions in a particulate fraction of rabbit muscle. J Cell Biol 14:389–400PubMedCentralPubMedCrossRefGoogle Scholar
  56. Ebashi S, Endo M, Ohtsuki I (1969) Control of muscle contraction. Quatert Rev Biophys 2:351–384CrossRefGoogle Scholar
  57. Ebashi S, Wakabayashi T, Ebashi F (1971) Troponin and its components. J Biochem 69:441–445PubMedGoogle Scholar
  58. Edman KAP (2010) Contractile performance of striated Muscle. Muscle Biophys 682:7–40CrossRefGoogle Scholar
  59. Edman K, Kiessling A (1971) The time course of the active state in relation to sarcomere length and movement studied in single skeletal muscle fibres of the frog. Acta Physiol Scand 81:182–196PubMedCrossRefGoogle Scholar
  60. Eisenberg E, Kielley WW (1970) Native tropomyosin: Effect on the interaction of actin with heavy meromyosin and subfragment-1. Biochem Biophy Res Comm 40:50–56CrossRefGoogle Scholar
  61. Elliott T (1912) The control of the suprarenal glands by the splanchnic nerves. J Physiol 44:374–409PubMedCentralPubMedCrossRefGoogle Scholar
  62. Elliott GF, Lowy J, Worthington CR (1963) An X-ray and light-diffraction study of the filament lattice of striated muscle in the living state and in rigor. J Mol Biol 6:295–305CrossRefGoogle Scholar
  63. Elliott GF, Lowy J, Millman BM (1967) Low-angle X-ray diffraction studies of living striated muscle during contraction. J Mol Biol 25:31–45PubMedCrossRefGoogle Scholar
  64. Endo M (1972) Stretch-induced increase in activation of skinned muscle fibres by calcium. Nat New Biol 237:211–213PubMedCrossRefGoogle Scholar
  65. Endo M (1973) Length dependence of activation of skinned muscle fibers by calcium. Cold Spring Harb Symp Quant Biol 37:505–510CrossRefGoogle Scholar
  66. Endo M, Tanaka M, Ogawa Y (1970) Calcium Induced Release of Calcium from the Sarcoplasmic Reticulum of Skinned Skeletal Muscle Fibres. Nature 228:34–36PubMedCrossRefGoogle Scholar
  67. Engelhardt W (1942) Enzymatic and mechanical properties of muscle proteins. Yale J Biol Med 15:21–38PubMedCentralPubMedGoogle Scholar
  68. Engelhardt WA, Liubimova MN (1939) Myosine and adenosinetriphosphatase. Nature 144:668–669CrossRefGoogle Scholar
  69. Engelmann TW (1873) Mikroskopische Untersuchungen über die quergestreifte Muskelsubstanz. Pflügers Archiv Eur J Physiol 7:33–71CrossRefGoogle Scholar
  70. Engelmann TW (1904) Das herz und seine tätigkeit im lichte neuerer forschung. Th Wilhelm Engelmann 1:44Google Scholar
  71. Evans CL, Hill AV (1914) The relation of length to tension development and heat production on contraction in muscle. J Physiol 49:10–16PubMedCentralPubMedCrossRefGoogle Scholar
  72. Fabiato A, Fabiato F (1975) Dependence of the contractile activation of skinned cardiac cells on the sarcomere length. Nature 256:54–56PubMedCrossRefGoogle Scholar
  73. Fabiato A, Fabiato F (1978) Myofilament-generated tension oscillations during partial calcium activation and activation dependence of the sarcomere length-tension relation of skinned cardiac cells. J Gen Physiol 72:667–699PubMedCrossRefGoogle Scholar
  74. Farman GP, Allen EJ, Schoenfelt KQ, Backx PH, de Tombe PP (2010) The role of thin filament cooperativity in cardiac length-dependent calcium activation. Biophys J 99:2978–2986PubMedCentralPubMedCrossRefGoogle Scholar
  75. Farman GP et al (2011) Myosin head orientation: a structural determinant for the Frank-Starling relationship. Am J Physiol 300:2155–2160Google Scholar
  76. Filo RS, Bohr DF, Ruegg JC (1965) Glycerinated skeletal and smooth muscle: calcium and magnesium dependence. Science 147:1581–1583PubMedCrossRefGoogle Scholar
  77. Fiske CH, Subbarow Y (1927) The nature of the "inorganic phosphate" in voluntary muscle. Science 65:401–403PubMedCrossRefGoogle Scholar
  78. Ford LE, Podolsky RJ (1970) Regenerative calcium release within muscle cells. Science 167:58–59PubMedCrossRefGoogle Scholar
  79. Frank O (1895) Zur Dynamik des Herzmuskels. Ztschr Biol 32:370Google Scholar
  80. Frank O (1959) On the dynamics of cardiac muscle (Translation). Am Heart J 58:282–317CrossRefGoogle Scholar
  81. Frank D, Kuhn C, Katus H, Frey N (2006) The sarcomeric Z-disc: a nodal point in signalling and disease. J Mol Med 84:446–468PubMedCrossRefGoogle Scholar
  82. Freiburg A, Gautel M (1996) A molecular map of the interactions between titin and myosin-binding protein C. Implications for sarcomeric assembly in familial hypertrophic cardiomyopathy. Eur J Biochem 235:317–323PubMedCrossRefGoogle Scholar
  83. Freiburg A et al (2000) Series of exon-skipping events in the elastic spring region of titin as the structural basis for myofibrillar elastic diversity. Circ Res 86:1114–1121PubMedCrossRefGoogle Scholar
  84. Fuchs F, Wang Y-P (1996) Sarcomere length versus interfilament spacing as determinants of cardiac myofilament Ca2+ sensitivity and Ca2+ binding. J Mol Cell Cardiol 28:1375–1383PubMedCrossRefGoogle Scholar
  85. Fukuda N, Sasaki D (2001) Ishiwata, S.i. & Kurihara, S. Length dependence of tension generation in rat skinned cardiac muscle: role of titin in the Frank-Starling mechanism of the heart. Circulation 104:1639–1645PubMedCrossRefGoogle Scholar
  86. Fukuda N, Kajiwara H, Ishiwata SI, Kurihara S (2000) Effects of MgADP on length dependence of tension generation in skinned rat cardiac muscle. Circ Res 86:e1–e6PubMedCrossRefGoogle Scholar
  87. Fukuda N, Wu Y, Farman G, Irving TC, Granzier H (2003) Titin isoform variance and length dependence of activation in skinned bovine cardiac muscle. J Physiol 553:147–154PubMedCentralPubMedCrossRefGoogle Scholar
  88. Fürth O (1895) Ueber die Eiweisskörper des Muskelplasmas. Naunyn-Schmiedeberg’s Archiv Pharmacol 36:231–274CrossRefGoogle Scholar
  89. Gautel M, Goulding D, Bullard B, Weber K, Furst DO (1996) The central Z-disk region of titin is assembled from a novel repeat in variable copy numbers. J Cell Sci 109:2747–2754PubMedGoogle Scholar
  90. Geeves M, Conibear P (1995) The role of three-state docking of myosin S1 with actin in force generation. Biophys J 68:199S–201SGoogle Scholar
  91. Geeves MA, Holmes KC (1999) Structural mechanism of muscle contraction. Annu Rev Biochem 68:687–728PubMedCrossRefGoogle Scholar
  92. Geeves MA, Lehrer SS (1994) Dynamics of the muscle thin filament regulatory switch: the size of the cooperative unit. Biophys J 67:273–282PubMedCentralPubMedCrossRefGoogle Scholar
  93. Gergely J (1953) Studies on myosin-adenosinetriphosphatase. J Biol Chem 200:543–550PubMedGoogle Scholar
  94. Gilbert R, Kelly MG, Mikawa T, Fischman DA (1996) The carboxyl terminus of myosin binding protein C (MyBP-C, C-protein) specifies incorporation into the A-band of striated muscle. J Cell Sci 109:101–111PubMedGoogle Scholar
  95. Godt R, Maughan D (1977) Swelling of skinned muscle fibers of the frog. Biophys J 19:103–116PubMedCentralPubMedCrossRefGoogle Scholar
  96. Godt RE, Maughan DW (1981) Influence of osmotic compression on calcium activation and tension in skinned muscle fibers of the rabbit. Pflugers Arch 391:334–337PubMedCrossRefGoogle Scholar
  97. Goldman Y, Simmons R (1977) Active and rigor muscle stiffness. J Physiol 269:55P–57PPubMedGoogle Scholar
  98. Goldman YE, Hibberd MG, Trentham DR (1984) Relaxation of rabbit psoas muscle fibres from rigor by photochemical generation of adenosine-5′-triphosphate. J Physiol 354:577–604PubMedCentralPubMedCrossRefGoogle Scholar
  99. Gollapudi, Sampath K, Mamidi R, Mallampalli, Sri L, Chandra M (2012) The N-terminal extension of cardiac troponin T stabilizes the blocked state of cardiac thin filament. Biophys J 103:940–948PubMedCentralPubMedCrossRefGoogle Scholar
  100. Gordon AM, Huxley A, Julian F (1966) The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol 184:170–192PubMedCentralPubMedCrossRefGoogle Scholar
  101. Gordon AM, Homsher E, Regnier M (2000) Regulation of contraction in striated muscle. Physiol Rev 80:853–924PubMedGoogle Scholar
  102. Granzier HL, Irving TC (1995) Passive tension in cardiac muscle: contribution of collagen, titin, microtubules, and intermediate filaments. Biophys J 68:1027–1044PubMedCentralPubMedCrossRefGoogle Scholar
  103. Greaser ML, Gergely J (1971) Reconstitution of troponin Activity from three protein components. J Biol Chem 246:4226–4233PubMedGoogle Scholar
  104. Greaser ML, Gergely J (1973) Purification and properties of the components from troponin. J Biol Chem 248:2125–2133PubMedGoogle Scholar
  105. Greaser ML et al (2008) Mutation that dramatically alters rat titin isoform expression and cardiomyocyte passive tension. J Mol Cell Cardiol 44:983–991PubMedCentralPubMedCrossRefGoogle Scholar
  106. Greene LE, Eisenberg E (1980) Cooperative binding of myosin subfragment-1 to the actin-troponin-tropomyosin complex. Proc Natl Acad Sci U S A 77:2616–2620PubMedCentralPubMedCrossRefGoogle Scholar
  107. Greenfield NJ et al (2006) Solution NMR structure of the junction between tropomyosin molecules: implications for actin binding and regulation. J Mol Biol 364:80–96PubMedCrossRefGoogle Scholar
  108. Gremels H (1936) Über die Steuerung der energetischen Vorgänge am Säugetierherzen. Naunyn Schmiedeberg’s Arch Pharmacol 182:1–54CrossRefGoogle Scholar
  109. Grimm AF, Whitehorn WV (1966) Characteristics of resting tension of myocardium and localization of its elements. Am J Physiol 210:1362–1368PubMedGoogle Scholar
  110. Grimm A, Whitehorn W (1968) Myocardial length-tension sarcomere relationships. Am J Physiol 214:1378–1387PubMedGoogle Scholar
  111. Gruen M, Gautel M (1999) Mutations in β-myosin S2 that cause familial hypertrophic cardiomyopathy (FHC) abolish the interaction with the regulatory domain of myosin-binding protein-C. J Mol Biol 286:933–949PubMedCrossRefGoogle Scholar
  112. Gruen M, Prinz H, Gautel M (1999) cAPK-phosphorylation controls the interaction of the regulatory domain of cardiac myosin binding protein C with myosin-S2 in an on-off fashion. FEBS Lett 453:254–259PubMedCrossRefGoogle Scholar
  113. Guz A (1974) Chairman’s Introduction. In: Ciba Foundation Symposium 24 - Physiological Basis of Starling’s Law of the Heart 1–5Google Scholar
  114. Haller AV (1754) Physiology: being a course of lectures upon the visceral anatomy & vital economy of human bodies. Translated by Samuel Mihles. Innys and Richardson, LondonGoogle Scholar
  115. Hanft LM, McDonald KS (2010) Length dependence of force generation exhibit similarities between rat cardiac myocytes and skeletal muscle fibres. J Physiol 588:2891–2903PubMedCentralPubMedCrossRefGoogle Scholar
  116. Hanft LM, Biesiadecki BJ, McDonald KS (2013) Length dependence of striated muscle force generation is controlled by phosphorylation of cTnI at serines 23/24. J Physiol 591(Pt 18):4535–4547PubMedCentralPubMedCrossRefGoogle Scholar
  117. Hanson J, Huxley HE (1953) Structural basis of the cross-striations in muscle. Nature 172:530–532PubMedCrossRefGoogle Scholar
  118. Hartshorne DJ, Mueller H (1968) Fractionation of troponin into two distinct proteins. Biochim Biophys Acta Res Comm 31:647–653CrossRefGoogle Scholar
  119. Hartshorne DJ, Pyun HY (1971) Calcium binding by the troponin complex, and the purification and properties of troponin A. Biochim Biophys Acta 229:698–711PubMedCrossRefGoogle Scholar
  120. Harvey W (1889) On the motion of the heart and blood in animals. G. Bell and SonsGoogle Scholar
  121. Haselgrove JC (1973) X-Ray evidence for a conformational change in the actin-containing filaments of vertebrate striated muscle. Cold Spring Harb Symp Quant Biol 37:341–352CrossRefGoogle Scholar
  122. Haselgrove JC, Huxley HE (1973) X-ray evidence for radial cross-bridge movement and for the sliding filament model in actively contracting skeletal muscle. J Mol Biol 77:549–568PubMedCrossRefGoogle Scholar
  123. Head JG, Ritchie MD, Geeves MA (1995) Characterization of the equilibrium between blocked and closed states of muscle thin filaments. Eur J Biochem 227:694–699PubMedCrossRefGoogle Scholar
  124. Heeley DH, Smillie LB, Lohmeier-Vogel EM (1989) Effects of deletion of tropomyosin overlap on regulated actomyosin subfragment 1 ATPase. Biochem J 258:831–836PubMedCentralPubMedCrossRefGoogle Scholar
  125. Heidenhain M (1913) Über die Entstehung der quergestreiften Muskelsubstanz bei der Forelle. Archiv für Mikros Anat 83:A427–A447CrossRefGoogle Scholar
  126. Heilbrunn LV (1940) The action of calcium on muscle protoplasm. Physiol Zool 13:88–94CrossRefGoogle Scholar
  127. Hellam DC, Podolsky RJ (1969) Force measurements in skinned muscle fibres. J Physiol 200:807–819PubMedCentralPubMedCrossRefGoogle Scholar
  128. Helmes M, Granzier H (2011) Cardiomyocyte stretch-sensing. OUP, OxfordCrossRefGoogle Scholar
  129. Herron TJ et al (2006) Activation of myocardial contraction by the N-terminal domains of myosin binding protein-C. Circ Res 98:1290–1298PubMedCrossRefGoogle Scholar
  130. Herzberg O, Moult J, James MN (1986) A model for the Ca2+-induced conformational transition of troponin C. A trigger for muscle contraction. J Biol Chem 261:2638–2644PubMedGoogle Scholar
  131. Hibberd M, Jewell B (1982) Calcium- and length-dependent force production in rat ventricular muscle. J Physiol 329:527–540PubMedCentralPubMedCrossRefGoogle Scholar
  132. Hill AV (1913) The combinations of haemoglobin with oxygen and with carbon monoxide. I. Biochem J 7:471–480PubMedCrossRefGoogle Scholar
  133. Hill AV (1964) The effect of tension in prolonging the active state in a twitch. Proc R Soc Lond B Biol Sci 159:589–595PubMedCrossRefGoogle Scholar
  134. Hill C, Weber K (1986) Monoclonal antibodies distinguish titins from heart and skeletal muscle. J Cell Biol 102:1099–1108PubMedCrossRefGoogle Scholar
  135. Hill TL, Eisenberg E, Greene L (1980) Theoretical model for the cooperative equilibrium binding of myosin subfragment 1 to the actin-troponin-tropomyosin complex. Proc Natl Acad Sci U S A 77:3186–3190PubMedCentralPubMedCrossRefGoogle Scholar
  136. Hofmann PA, Fuchs F (1987a) Evidence for a force-dependent component of calcium binding to cardiac troponin C. Am J Physiol 253:C541–C546PubMedGoogle Scholar
  137. Hofmann PA, Fuchs F (1987b) Effect of length and cross-bridge attachment on Ca2+ binding to cardiac troponin C. Am J Physiol 253:C90–C96PubMedGoogle Scholar
  138. Hofmann PA, Fuchs F (1988) Bound calcium and force development in skinned cardiac muscle bundles: Effect of sarcomere length. J Mol Cell Cardiol 20:667–677PubMedCrossRefGoogle Scholar
  139. Holmes KC, Lehman W (2008) Gestalt-binding of tropomyosin to actin filaments. J Muscle Res Cell Motil 29:213–219PubMedCrossRefGoogle Scholar
  140. Houmeida A et al (2008) Evidence for the oligomeric state of ‘elastic’ titin in muscle sarcomeres. J Mol Biol 384:299–312PubMedCrossRefGoogle Scholar
  141. Housmans PR, Lee NK, Blinks (1983) Active shortening retards the decline of the intracellular calcium transient in mammalian heart muscle. Science 221:159–161PubMedCrossRefGoogle Scholar
  142. Howell WH, Donaldson F (1884) Experiments upon the heart of the dog with reference to the maximum volume of blood sent out by the left ventricle in a single beat, and the influence of variations in venous pressure, arterial pressure, and pulse-rate upon the work done by the heart. Phil Trans Royal Soc Lond 175:139–160CrossRefGoogle Scholar
  143. Huxley HE (1953a) Electron microscope studies of the organisation of the filaments in striated muscle. Biochim Biophys Acta 12:387–394PubMedCrossRefGoogle Scholar
  144. Huxley HE (1953b) X-Ray analysis and the problem of muscle. Proc R Soc Lond 141:59–62PubMedCrossRefGoogle Scholar
  145. Huxley A (1957a) Muscle structure and theories of contraction. Prog Biophys Biophys Chem 7:255–318PubMedGoogle Scholar
  146. Huxley HE (1957b) The double array of filaments in cross-striated muscle. J Biophys Biochem Cytol 3:631–648PubMedCentralPubMedCrossRefGoogle Scholar
  147. Huxley HE (1961) The contractile structure of cardiac and skeletal muscle. Circulation 24:328–335PubMedCrossRefGoogle Scholar
  148. Huxley HE (1963) Electron microscope studies on the structure of natural and synthetic protein filaments from striated muscle. J Mol Biol 7:281–308PubMedCrossRefGoogle Scholar
  149. Huxley HE (1969) The mechanism of muscular contraction. Science 20:1356–1365CrossRefGoogle Scholar
  150. Huxley HE (1971) The Croonian Lecture, 1970: The structural basis of muscular contraction. Proc R Soc Lond 178:131–149PubMedCrossRefGoogle Scholar
  151. Huxley HE (1973a) Muscle 1972: progress and problems. Cold Spring Harb Symp Quant Biol 37:689–693CrossRefGoogle Scholar
  152. Huxley AF (1973b) A note suggesting that the cross-bridge attachment during muscle contraction may take place in two stages. Proc R Soc Lond B Biol Sci 183:83–86PubMedCrossRefGoogle Scholar
  153. Huxley HE, Brown W (1967) The low-angle X-ray diagram of vertebrate striated muscle and its behaviour during contraction and rigor. J Mol Biol 30:383–434PubMedCrossRefGoogle Scholar
  154. Huxley H, Hanson J (1954) Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173:973–976PubMedCrossRefGoogle Scholar
  155. Huxley A, Niedergerke R (1954) Structural changes in muscle during contraction; interference microscopy of living muscle fibres. Nature 173:917–973Google Scholar
  156. Irving TC, Konhilas J, Perry D, Fischetti R, de Tombe PP (2000) Myofilament lattice spacing as a function of sarcomere length in isolated rat myocardium. Am J Physiol 279:H2568–H2573Google Scholar
  157. Jewell B, Wilkie D (1960) The mechanical properties of relaxing muscle. J Physiol 152:30–47PubMedCentralPubMedCrossRefGoogle Scholar
  158. Johansson JE (1891) Die reizung der vasomotoren nach der lähmung der cerebrospinalen herznerven. Archiv für Physiol, 103–156Google Scholar
  159. Johnson P, Smillie LB (1977) Polymerizability of rabbit skeletal tropomyosin: effects of enzymic and chemical modifications. Biogeosciences 16:2264–2269Google Scholar
  160. Kabsch W, Mannherz HG, Suck D, Pai EF, Holmes KC (1990) Atomic structure of the actin: DNase I complex. Nature 347:37–44PubMedCrossRefGoogle Scholar
  161. Kentish JC, ter Keurs HE, Ricciardi L, Bucx JJ, Noble MI (1986) Comparison between the sarcomere length-force relations of intact and skinned trabeculae from rat right ventricle. Influence of calcium concentrations on these relations. Circ Res 58:755–768PubMedCrossRefGoogle Scholar
  162. Kielley WW, Meyerhof O (1948) A new magnesium-activated adenosinetriphosphatase from muscle. J Biol Chem 174:387–388PubMedGoogle Scholar
  163. Kielley WW, Meyerhof O (1950) Studies on adenosinetriphosphatase of muscle; a new magnesium-activated a denosinetriphosphatase. J Biol Chem 176:591–601Google Scholar
  164. Knowlton FP, Starling EH (1912) The influence of variations in temperature and blood-pressure on the performance of the isolated mammalian heart. J Physiol 44:206–219PubMedCentralPubMedCrossRefGoogle Scholar
  165. Kominz DR, Mitchell ER, Nihei T, Kay CM (1965) The papain digestion of skeletal myosin A. Biochemistry 4:2373–2382CrossRefGoogle Scholar
  166. Komukai K, Kurihara S (1997) Length dependence of Ca2+-tension relationship in aequorin-injected ferret papillary muscles. Am J Physiol 273:1068–1074Google Scholar
  167. Konhilas JP, Irving TC, de Tombe PP (2002a) Myofilament calcium sensitivity in skinned rat cardiac trabeculae: role of interfilament spacing. Circ Res 90:59–65PubMedCrossRefGoogle Scholar
  168. Konhilas JP, Irving TC, de Tombe PP (2002b) Length-dependent activation in three striated muscle types of the rat. J Physiol 544:225–236PubMedCentralPubMedCrossRefGoogle Scholar
  169. Konhilas JP et al (2003) Troponin I in the murine myocardium: influence on length-dependent activation and interfilament spacing. J Physiol 547:951–961PubMedCentralPubMedCrossRefGoogle Scholar
  170. Kostin S, Hein S, Arnon E, Scholz D, Schaper J (2000) The cytoskeleton and related proteins in the human failing heart. Heart Fail Rev 5:271–280PubMedCrossRefGoogle Scholar
  171. Krause W (1869) Die motorischen Endplatten der quergestreiften Muskelfasern. Hahn, HannoverGoogle Scholar
  172. Kuster DWD et al (2013) GSK3β phosphorylates newly identified site in the Pro-Ala rich region of cardiac myosin binding protein C and alters cross-Bridge cycling kinetics in human. Circ Res 112:633–639PubMedCentralPubMedCrossRefGoogle Scholar
  173. Labeit S, Kolmerer B (1995) Titins: giant proteins in charge of muscle ultrastructure and elasticity. Science 270:293–296PubMedCrossRefGoogle Scholar
  174. Labeit SGM, Lakey A, Trinick J (1992) Towards a molecular understanding of titin. EMBO J 11:1711–1716PubMedCentralPubMedGoogle Scholar
  175. Labeit S, Kolmerer B, Linke WA (1997) The giant protein titin. Emerging roles in physiology and pathophysiology. Circ Res 80:290–294PubMedCrossRefGoogle Scholar
  176. Lehman W et al (2000) Tropomyosin and actin isoforms modulate the localization of tropomyosin strands on actin filaments. J Mol Biol 302:593–606PubMedCrossRefGoogle Scholar
  177. Lehndorff A (1908) Über die ursachen der typischen schwankungen des allgemeinen blutdruckes bei reizung der vasomotoren. Archiv für Physiol, 362–391Google Scholar
  178. Linke WA (2008) Sense and stretchability: The role of titin and titin-associated proteins in myocardial stress-sensing and mechanical dysfunction. Cardiovasc Res 77:637–648PubMedGoogle Scholar
  179. Linke WA, Kruger M (2010) The giant protein titin as an integrator of myocyte signaling pathways. Physiology 25:186–198PubMedCrossRefGoogle Scholar
  180. Locke FS, Rosenheim O (1907) Contributions to the physiology of the isolated heart. The consumption of dextrose by mammalian cardiac muscle. J Physiol 36:205–220PubMedCentralPubMedCrossRefGoogle Scholar
  181. Lohmann K (1934) Uber die enzymatische aufspaltung der kreatinphosphorsaure; zugleich ein beitrag zum chemismus der muskelkontraktion. Biochem Z 271:264–277Google Scholar
  182. Lohmann K (1935) Konstitution der adenylpyrophosphorsaure and adeninediphosphorsaure. Biochem Z 282:120–123Google Scholar
  183. Lowey S, Goldstein L, Cohen C, Luck SM (1967) Proteolytic degradation of myosin and the meromyosins by a water-insoluble polyanionic derivative of trypsin: Properties of a helical subunit isolated from heavy meromyosin. J Mol Biol 23:287–304PubMedCrossRefGoogle Scholar
  184. Ludwig C (1856) Lehrbuch Der Physiologie Des Menschen. C.F. Winter, Heidelberg 1852-1856 2Google Scholar
  185. Lundsgaard E (1930a) Untersuchungen fiber muskelkontraktion ohne milchsaure. Biochem Z 217:162–177Google Scholar
  186. Lundsgaard E (1930b) Weitere untersuchungen uber muskelkontraktionen ohne milchsaurebildung. Biochem Z 227:51–83Google Scholar
  187. Lundsgaard E (1930c) Uber die einwirkung der monoiodoessigsaure auf den spaltungs- und oxydationsstoffwechsel. Biochem Z 220:8–18Google Scholar
  188. Luther PK et al (2011) Direct visualization of myosin-binding protein C bridging myosin and actin filaments in intact muscle. Proc Natl Acad Sci U S A 108:11423–11428PubMedCentralPubMedCrossRefGoogle Scholar
  189. Lymn RW, Taylor EW (1971) Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10:4617–4624PubMedCrossRefGoogle Scholar
  190. Magid A, Reedy M (1980) X-ray diffraction observations of chemically skinned frog skeletal muscle processed by an improved method. Biophys J 30:270–340Google Scholar
  191. Malinchik S, Xu S, Yu LC (1997) Temperature-induced structural changes in the myosin thick filament of skinned rabbit psoas muscle. Biophys J 73:2304–2312PubMedCentralPubMedCrossRefGoogle Scholar
  192. Manning EP, Tardiff JC, Schwartz SD (2011) A model of calcium activation of the cardiac thin filament. Biochemistry 50:7405–7413PubMedCentralPubMedCrossRefGoogle Scholar
  193. Manning EP, Tardiff JC, Schwartz SD (2012) Molecular effects of familial hypertrophic cardiomyopathy-related mutations in the TNT1 domain of cTnT. J Mol Biol 421:54–66PubMedCentralPubMedCrossRefGoogle Scholar
  194. Marey EJ (1881) La circulation du sang à l’ état physiologique et dans les maladies. Libraire de L’Academie de Medecine, ParisGoogle Scholar
  195. Marsh BB (1951) A factor modifying muscle fibre syneresis. Nature 167:1065–1066PubMedCrossRefGoogle Scholar
  196. Marsh BB (1952) The effects of adenosine triphosphate on the fibre volume of a muscle homogenate. Biochim Biophys Acta 9:247–260PubMedCrossRefGoogle Scholar
  197. Martyn DA, Gordon AM (1988) Length and myofilament spacing-dependent changes in calcium sensitivity of skeletal fibres: effects of pH and ionic strength. J Muscle Res Cell Motil 9:428–445PubMedCrossRefGoogle Scholar
  198. Maruyama K et al (1977) Connectin, an elastic protein of muscle. Characterization and function. J Biochem 82:317–337PubMedGoogle Scholar
  199. Maruyama K, Kimura S, Yoshidomi H, Sawada H, Kikuchi M (1984) Molecular size and shape of beta-connectin, an elastic protein of striated muscle. J Biochem 95:1423–1433PubMedGoogle Scholar
  200. Maruyama K et al (1985) Connectin filaments link thick filaments and Z lines in frog skeletal muscle as revealed by immunoelectron microscopy. J Cell Biol 101:2167–2172PubMedCrossRefGoogle Scholar
  201. Mateja RD, Greaser ML, de Tombe PP (2012) Impact of titin isoform on length dependent activation and cross-bridge cycling kinetics in rat skeletal muscle. Biochim Biophys Acta 1833:804–811PubMedCentralPubMedCrossRefGoogle Scholar
  202. Matsubara I, Millman BM (1974) X-Ray diffraction studies on cardiac muscle. In: Ciba Foundation Symposium 24 - Physiological Basis of Starling’s Law of the Heart 31-41. John Wiley & Sons, LtdGoogle Scholar
  203. Matsubara I, Millman BM (1974b) X-ray diffraction patterns from mammalian heart muscle. J Mol Biol 82:527–536PubMedCrossRefGoogle Scholar
  204. Maytum R, Lehrer SS, Geeves MA (1998) Cooperativity and Switching within the Three-State Model of Muscle Regulation. Biochemistry 38:1102–1110CrossRefGoogle Scholar
  205. McDonald KS, Moss RL (1995) Osmotic compression of single cardiac myocytes eliminates the reduction in Ca2+ sensitivity of tension at short sarcomere length. Circ Res 77:199–205PubMedCrossRefGoogle Scholar
  206. McDonald KS et al (1995) Length dependence of Ca2+ sensitivity of tension in mouse cardiac myocytes expressing skeletal troponin C. J Physiol 483:131–139PubMedCentralPubMedCrossRefGoogle Scholar
  207. McKillop DF, Geeves MA (1993) Regulation of the interaction between actin and myosin subfragment 1: evidence for three states of the thin filament. Biophys J 65:693–701PubMedCentralPubMedCrossRefGoogle Scholar
  208. Meek WJ, Eyster JAE (1915) The effect of adrenalin on the heart-rate. Am J Physiol 38:62–66Google Scholar
  209. Mihalyi E, Szent-Gyorgyi AG (1953) Trypsin digestion of muscle proteins. I. Ultracentrifugal analysis of the process. J Biol Chem 201:189–196PubMedGoogle Scholar
  210. Mines GR (1913) On functional analysis by the action of electrolytes. J Physiol 46:188–235PubMedCentralPubMedCrossRefGoogle Scholar
  211. Miyamoto CA, Fischman DA, Reinach FC (1999) The interface between MyBP-C and myosin: site-directed mutagenesis of the CX myosin-binding domain of MyBP-C. J Muscle Res Cell Motil 20:703–716PubMedCrossRefGoogle Scholar
  212. Moos C, Mason CM, Besterman JM, Feng INM, Dubin JH (1978) The binding of skeletal muscle C-protein to F-actin, and its relation to the interaction of actin with myosin subfragment-1. J Mol Biol 124:571–586PubMedCrossRefGoogle Scholar
  213. Morris EP, Lehrer SS (1984) Troponin-tropomyosin interactions. Fluorescence studies of the binding of troponin, troponin T and chymotryptic troponin T fragments to specifically labeled tropomyosin. Biogeosciences 23:2214–2220Google Scholar
  214. Moss L, Swinford A, Greaser M (1983) Alterations in the Ca2+ sensitivity of tension development by single skeletal muscle fibers at stretched lengths. Biophys J 43:115–119PubMedCentralPubMedCrossRefGoogle Scholar
  215. Moss RL, Nwoye LO, Greaser ML (1991) Substitution of cardiac troponin C into rabbit muscle does not alter the length dependence of Ca2+ sensitivity of tension. J Physiol 440:273–289PubMedCentralPubMedCrossRefGoogle Scholar
  216. Mueller H (1965) Characterization of the molecular region containing the active sites of myosin. J Biol Chem 240:3816–3828PubMedGoogle Scholar
  217. Mueller H, Perry SV (1961) Studies on the tryptic digestion of heavy meromyosin. Biochim Biophys Acta 50:599–601PubMedCrossRefGoogle Scholar
  218. Müller J (1844) Handbuch der Physiologie des Menschen für Vorlesungen. Vierte Auflage, Coblenz. J Hölscher 1837 1Google Scholar
  219. Mun JY et al (2011) Electron microscopy and 3D reconstruction of F-actin decorated with cardiac myosin-binding protein C. J Mol Biol 410:214–225PubMedCentralPubMedCrossRefGoogle Scholar
  220. Murakami K et al (2005) Structural basis for Ca2+-regulated muscle relaxation at interaction sites of troponin with actin and tropomyosin. J Mol Biol 352:178–201PubMedCrossRefGoogle Scholar
  221. Murakami K et al (2008) Structural basis for tropomyosin overlap in thin (actin) filaments and the generation of a molecular swivel by troponin-T. Proc Natl Acad Sci U S A 105:7200–7205PubMedCentralPubMedCrossRefGoogle Scholar
  222. Murakami K et al (2010) Structural basis for actin assembly, activation of ATP hydrolysis, and delayed phosphate release. Cell 143:275–287PubMedCrossRefGoogle Scholar
  223. Murray AC, Kay CM (1971) Separation and characterization of the inhibitory factor of the troponin system. Biochem Biophys Res Comm 44:237–244PubMedCrossRefGoogle Scholar
  224. Nagashima H, Asakura S (1982) Studies on co-operative properties of tropomyosin-actin and tropomyosin-troponin-actin complexes by the use of N-ethylmaleimide-treated and untreated species of myosin subfragment 1. J Mol Biol 155:409–428PubMedCrossRefGoogle Scholar
  225. Offer G (1973) C-protein and the periodicity in the thick filaments of vertebrate skeletal muscle. Cold Spring Harb Symp Quant Biol 37:87–93CrossRefGoogle Scholar
  226. Offer G, Moos C, Starr R (1973) A new protein of the thick filaments of vertebrate skeletal myofibrils: Extraction, purification and characterization. J Mol Biol 74:653–676PubMedCrossRefGoogle Scholar
  227. Ohtsuka H, Yajima H, Maruyama K, Kimura S (1997) Binding of the N-terminal 63 kDa portion of connectin/titin to α-actinin as revealed by the yeast two-hybrid system. FEBS Lett 401:65–67PubMedCrossRefGoogle Scholar
  228. Orlova A, Galkin VE, Jeffries CMJ, Egelman EH, Trewhella J (2011) The N-terminal domains of myosin binding protein C can bind polymorphically to F-actin. J Mol Biol 412:379–386PubMedCentralPubMedCrossRefGoogle Scholar
  229. Page SG (1974) Measurements of structural parameters in cardiac muscle. In: Ciba Foundation Symposium 24 - Physiological Basis of Starling’s Law of the Heart 13-30. John Wiley & Sons, LtdGoogle Scholar
  230. Palm T, Greenfield NJ, Hitchcock-DeGregori SE (2003) Tropomyosin ends determine the stability and functionality of overlap and troponin T complexes. Biophys J 84:3181–3189PubMedCentralPubMedCrossRefGoogle Scholar
  231. Pan BS, Gordon AM, Luo ZX (1989) Removal of tropomyosin overlap modifies cooperative binding of myosin S-1 to reconstituted thin filaments of rabbit striated muscle. J Biol Chem 264:8495–8498PubMedGoogle Scholar
  232. Parmley W, Chuck L (1973) Length-dependent changes in myocardial contractile state. Am J Physiol 224:1195–1199PubMedGoogle Scholar
  233. Parry DAD, Squire JM (1973) Structural role of tropomyosin in muscle regulation: Analysis of the X-ray diffraction patterns from relaxed and contracting muscles. J Mol Biol 75:33–55PubMedCrossRefGoogle Scholar
  234. Pate E, Cooke R (1989) Addition of phosphate to active muscle fibers probes actomyosin states within the powerstroke. Pflugers Arch 414:73–81PubMedCrossRefGoogle Scholar
  235. Patterson SW, Starling EH (1914) On the mechanical factors which determine the output of the ventricles. J Physiol 48:357–379PubMedCentralPubMedCrossRefGoogle Scholar
  236. Patterson SW, Piper H, Starling E (1914) The regulation of the heart beat. J Physiol 48:465–513PubMedCentralPubMedCrossRefGoogle Scholar
  237. Paul DM, Morris EP, Kensler RW, Squire JM (2009) Structure and orientation of troponin in the thin filament. J Biol Chem 284:15007–15015PubMedCentralPubMedCrossRefGoogle Scholar
  238. Pearlstone JR, Smillie LB (1982) Binding of troponin-T fragments to several types of tropomyosin. Sensitivity to Ca2+ in the presence of troponin-C. J Biol Chem 257:10587–10592PubMedGoogle Scholar
  239. Pearlstone JR, Smillie LB (1983) Effects of troponin-I plus -C on the binding of troponin-T and its fragments to alpha-tropomyosin. J Biol Chem 254:2534–2542Google Scholar
  240. Pepe FA (1966) Some aspects of the structural organization of the myofibril as revealed by antibody-staining methods. J Cell Biol 28:505–525PubMedCentralPubMedCrossRefGoogle Scholar
  241. Perry SV, Corsi A (1958) Extraction of proteins other than myosin from the isolated rabbit myofibril. Biochem J 68:5–12PubMedCentralPubMedCrossRefGoogle Scholar
  242. Perry SV, Cole HA, Head JF, Wilson FJ (1973) Localization and mode of action of the inhibitory protein component of the troponin complex. Cold Spring Harb Symp Quant Biol 37:251–262CrossRefGoogle Scholar
  243. Perz-Edwards RJ et al (2011) X-ray diffraction evidence for myosin-troponin connections and tropomyosin movement during stretch activation of insect flight muscle. Proc Natl Acad Sci U S A 108:120–125PubMedCentralPubMedCrossRefGoogle Scholar
  244. Pfuhl M, Gautel M (2012) Structure, interactions and function of the N-terminus of cardiac myosin binding protein C (MyBP-C): who does what, with what, and to whom? J Muscle Res Cell Motil 33:83–94PubMedCrossRefGoogle Scholar
  245. Pirani A et al (2005) Single particle analysis of relaxed and activated muscle thin filaments. J Mol Biol 346:761–772PubMedCrossRefGoogle Scholar
  246. Poole KJV et al (2006) A comparison of muscle thin filament models obtained from electron microscopy reconstructions and low-angle X-ray fibre diagrams from non-overlap muscle. J Struct Biol 155:273–284PubMedCrossRefGoogle Scholar
  247. Potter JD, Gergely J (1974) Troponin, tropomyosin, and actin interactions in the Ca2+ ion regulation of muscle contraction. Biochemistry 13:2697–2703PubMedCrossRefGoogle Scholar
  248. Pringle JWS (1949) The excitation and contraction of the flight muscles of insects. J Physiol 108:226–232PubMedCentralPubMedCrossRefGoogle Scholar
  249. Pringle JWS (1978) The Croonian Lecture, 1977: stretch activation of muscle: function and mechanism. Proc Royal Soc Lond 201:107–130CrossRefGoogle Scholar
  250. Rack PMH, Westbury DR (1969) The effects of length and stimulus rate on tension in the isometric cat soleus muscle. J Physiol 204:443–460PubMedCentralPubMedCrossRefGoogle Scholar
  251. Rall JA (2014) Birth of the sliding filament model of muscular contraction: proposal. In: Mechanism of muscular contraction. Springer, New York, pp 29–57Google Scholar
  252. Ramsey RW, Street SF (1940) The isometric length-tension diagram of isolated skeletal muscle fibers of the frog. J Cell Comp Biol 15:11–34Google Scholar
  253. Ratti J, Rostkova E, Gautel M, Pfuhl M (2011) Structure and interactions of myosin-binding protein C domain C0: cardiac-specific regulation of myosin at its neck? J Biol Chem 286:12650–12658PubMedCentralPubMedCrossRefGoogle Scholar
  254. Regnier M et al (2002) Thin filament near-neighbour regulatory unit interactions affect rabbit skeletal muscle steady-state force-Ca2+ relations. J Physiol 540:485–497PubMedCentralPubMedCrossRefGoogle Scholar
  255. Rice RV (1961) Conformation of individual macromolecular particles from myosin solutions. Biochim Biophys Acta 52:602–604PubMedCrossRefGoogle Scholar
  256. Richard Zobel C, Carlson FD (1963) An electron microscopic investigation of myosin and some of its aggregates. J Mol Biol 7:78–89CrossRefGoogle Scholar
  257. Ringer S (1882) Concerning the influence exerted by each of the constituents of the blood on the contraction of the ventricle. J Physiol 3:380–393PubMedCentralPubMedCrossRefGoogle Scholar
  258. Ringer S (1883) A further contribution regarding the influence of the different constituents of the blood on the contraction of the Heart. J Physiol 4:29–42PubMedCentralPubMedCrossRefGoogle Scholar
  259. Robinson TF, Winegrad S (1979) The measurement and dynamic implications of thin filament lengths in heart muscle. J Physiol 286:607–619PubMedCentralPubMedCrossRefGoogle Scholar
  260. Rome E (1972) Relaxation of glycerinated muscle: Low-angle X-ray diffraction studies. J Mol Biol 65:331–345PubMedCrossRefGoogle Scholar
  261. Rosenblueth A, Alanís J, López E, Rubio R (1959) The adaptation of ventricular muscle to different circulatory conditions. Arch Int Physiol Biochim 67:358–373PubMedGoogle Scholar
  262. Roy CS (1879) On the Influences which modify the work of the heart. J Physiol 1:452–496PubMedCentralPubMedCrossRefGoogle Scholar
  263. Roy CSA, Adami JG (1892) Contributions to the physiology and pathology of the mammalian heart. Br Med J 1:428–430PubMedCentralPubMedCrossRefGoogle Scholar
  264. Rϋdel R, Taylor SR (1971) Striated muscle fibers: facilitation of contraction at short lengths by caffeine. Science 172:387–388CrossRefGoogle Scholar
  265. Sandow A (1952) Excitation-contraction coupling in muscular response. Yale J Biol Med 25:176–201PubMedCentralPubMedGoogle Scholar
  266. Sarkar S, Sreter FA, Gergely J (1971) Light chains of myosins from white, red, and cardiac muscles. Proc Natl Acad Sci U S A 68:946–950PubMedCentralPubMedCrossRefGoogle Scholar
  267. Sarnoff SJ, Mitchell JH (1961) The regulation of the performance of the heart. Am J Med 30:747–771PubMedCrossRefGoogle Scholar
  268. Sarnoff SJ, Mitchell JH, Gilmore JP, Remensnyder JP (1960) Homeometric autoregulation in the heart. Circ Res 8:1077–1091PubMedCrossRefGoogle Scholar
  269. Schafer EA (1890) On the minute structure of the muscle-columns or sarcostyles which form the wing-muscles of insects. Proc R Soc Lond 49:280–286CrossRefGoogle Scholar
  270. Schaub MP (1971) SV. The regulatory proteins of the myofibril. Characterization and properties of the inhibitory factor (troponin B). Biochem J 123:367–377PubMedCentralPubMedCrossRefGoogle Scholar
  271. Schaub MC, Perry SV (1969) The relaxing protein system of striated muscle. Resolution of the troponin complex into inhibitory and calcium ion-sensitizing factors and their relationship to tropomyosin. Biochem J 115:993–1005PubMedCentralPubMedCrossRefGoogle Scholar
  272. Schaub M, Perry S, Häcker W (1972) The regulatory proteins of the myofibril. Characterization and biological activity of the calcium-sensitizing factor (troponin A). Biochem J 126:237–249PubMedCentralPubMedCrossRefGoogle Scholar
  273. Seo K et al (2014) Hyperactive adverse mechanical stress responses in dystrophic heart are coupled to transient receptor potential canonical 6 and blocked by cGMP-protein kinase G modulation. Circ Res 114:823–832PubMedCentralPubMedCrossRefGoogle Scholar
  274. Sequeira V, Nijenkamp LLAM, Regan JA, van der Velden J (2013a) The physiological role of cardiac cytoskeleton and its alterations in heart failure. Biochim Biophys Acta 1838:700–722PubMedCrossRefGoogle Scholar
  275. Sequeira V et al (2013b) Perturbed length-sependent activation in human hypertrophic cardiomyopathy with missense sarcomeric gene mutations. Circ Res 112:1491–1505PubMedCentralPubMedCrossRefGoogle Scholar
  276. Sequeira V, Witjas-Paalberends ER, Kuster DD, Velden J (2013c) Cardiac myosin-binding protein C: hypertrophic cardiomyopathy mutations and structure-function relationships. Pflugers Arch 2:201–206Google Scholar
  277. Sequeira V, Najafi A, Wijnker PJM, dos Remedios C, Michels M, Kuster DWD, van der Velden J (2015) ADP-stimulated contraction: a predictor of thin-filament activation in cardiac disease. Proc Natl Acad Sci. (in press)Google Scholar
  278. Shaffer JF, Kensler RW, Harris SP (2009) The myosin-binding protein C motif binds to F-actin in a phosphorylation-sensitive manner. J Biol Chem 284:12318–12327PubMedCentralPubMedCrossRefGoogle Scholar
  279. Slayter H, Lowey S (1967) Substructure of the myosin molecule as visualized by electron microscopy. Proc Natl Acad Sci U S A 58:1611–1618PubMedCentralPubMedCrossRefGoogle Scholar
  280. Smith SH, Fuchs F (1999) Effect of ionic strength on length-dependent Ca2+ activation in skinned cardiac muscle. J Mol Cell Cardiol 31:2115–2125PubMedCrossRefGoogle Scholar
  281. Sonnenblick EH (1968) Correlation of myocardial ultrastructure and function. Circulation 38:29–44PubMedCrossRefGoogle Scholar
  282. Sonnenblick EH, Skelton CL (1974) Reconsideration of the ultrastructural basis of cardiac length-tension relations. Circ Res 35:517–526PubMedCrossRefGoogle Scholar
  283. Sonnenblick EH, Spiro D, Cottrell TS (1963) Fine structural changes in heart muscle in relation of the lengthtension curve. Proc Natl Acad Sci U S A 49:193–200PubMedCentralPubMedCrossRefGoogle Scholar
  284. Sonnenblick EH, Spotnitz H, Spiro D (1964) Role of the sarcomere in ventricular function and the mechanism of heart failure. Circ Res 15:70–81PubMedGoogle Scholar
  285. Sorimachi H et al (1997) Tissue-specific expression and α-actinin binding properties of the Z-disc titin: implications for the nature of vertebrate Z-discs. J Mol Biol 270:688–695PubMedCrossRefGoogle Scholar
  286. Squire JM, Al-Khayat HA, Yagi N (1993) Muscle thin-filament structure and regulation. Actin sub-domain movements and the tropomyosin shift modelled from low-angle X-ray diffraction. J Chem Soci 89:2717–2726Google Scholar
  287. Squire JM, Harford JJ, Al-Khayat HA (1994) Molecular movements in contracting muscle: towards "muscle - the movie". Biophys Chem 50:87–96PubMedCrossRefGoogle Scholar
  288. Starling EH (1918) The linacre lecture on the law of the heart given at Cambridge, 1915. Nature 101:18CrossRefGoogle Scholar
  289. Starling EH (1920) On the circulatory changes associated with exercise. J Royal Army Med Corps 34:258Google Scholar
  290. Starr R, Offer G (1978) The interaction of C-protein with heavy meromyosin and subfragment-2. Biochem J 171:813–816PubMedCentralPubMedCrossRefGoogle Scholar
  291. Stein LA, Schwarz RP (1979) Chock, P.B. & Eisenberg, E. Mechanism of the actomyosin adenosine triphosphatase. Evidence that adenosine 5′-triphosphate hydrolysis can occur without dissociation of the actomyosin complex. Biochemistry 18:3895–3909PubMedCrossRefGoogle Scholar
  292. Stelzer JE, Dunning SB, Moss RL (2006a) Ablation of cardiac myosin-binding protein-C accelerates stretch activation in murine skinned myocardium. Circ Res 98:1212–1218PubMedCrossRefGoogle Scholar
  293. Stelzer JE, Patel JR, Moss RL (2006b) Protein kinase A-mediated acceleration of the stretch activation response in murine skinned myocardium is eliminated by ablation of cMyBP-C. Circ Res 99:884–890PubMedCrossRefGoogle Scholar
  294. Stenger R, Spiro D (1961) The ultrastructure of mammalian cardiac muscle. J Biophys Biochem Cytol 9:325–351PubMedCentralPubMedCrossRefGoogle Scholar
  295. Stephen H (1740) Foundations of anesthesiology. An account of some hydraulic and hydrostatical experiments made on the blood and blood-vessels of animals. J Clin Monit Comput 16:45–47Google Scholar
  296. Stienen GJM, Blangé T, Treijtel BW (1985) Tension development and calcium sensitivity in skinned muscle fibres of the frog. Pflugers Arch 405:19–23PubMedCrossRefGoogle Scholar
  297. Straub FB (1942) Actin studies. Int Med Chem Univ Szeged 2:3–15Google Scholar
  298. Straub FB (1943) Actin II studies. Int Med Chem Univ Szeged 3:23–37Google Scholar
  299. Sun Y-B, Lou F, Irving M (2009) Calcium- and myosin-dependent changes in troponin structure during activation of heart muscle. J Physiol 587:155–163PubMedCentralPubMedCrossRefGoogle Scholar
  300. Szent-Györgyi A (1942) Myosin and muscular contraction. Inst Med Chem Univ Szeged 1:1–71Google Scholar
  301. Szent-Györgyi A (1946) Contraction and the chemical structure of the muscle fibril. J Colloid Sci 1:1–19CrossRefGoogle Scholar
  302. Szent-Györgyi AG (1953) Meromyosins, the subunits of myosin. Arch Biochem Biophys 42:305–320PubMedCrossRefGoogle Scholar
  303. Takeda S, Yamashita A, Maeda K, Maeda Y (2003) Structure of the core domain of human cardiac troponin in the Ca2+-saturated form. Nature 424:35–41PubMedCrossRefGoogle Scholar
  304. Tardiff J (2011) Thin filament mutations: developing an integrative approach to a complex disorder. Circ Res 108:765–782PubMedCentralPubMedCrossRefGoogle Scholar
  305. Taylor SR, Rϋdel R (1970) Striated muscle fibers: inactivation of contraction induced by shortening. Science 167:882–884PubMedCrossRefGoogle Scholar
  306. Terui T et al (2008) Troponin and titin coordinately regulate length-dependent activation in skinned porcine ventricular muscle. J Gen Physiol 131:275–283PubMedCentralPubMedCrossRefGoogle Scholar
  307. Tobacman LS et al (2002) The troponin tail domain promotes a conformational state of the thin filament that suppresses myosin activity. J Biol Chem 277:27636–27642PubMedCrossRefGoogle Scholar
  308. Trombitás K, Greaser ML, Pollack GH (1997) Interaction between titin and thin filaments in intact cardiac muscle. J Muscle Res Cell Motil 18:345–351PubMedCrossRefGoogle Scholar
  309. Tskhovrebova L et al (2010) Shape and flexibility in the titin 11-domain super-repeat. J Mol Biol 397:1092–1105PubMedCrossRefGoogle Scholar
  310. van der Velden J, de Jong JW, Owen VJ, Burton PBJ, Stienen GJM (2000) Effect of protein kinase A on calcium sensitivity of force and its sarcomere length dependence in human cardiomyocytes. Cardiovasc Res 46:487–495PubMedCrossRefGoogle Scholar
  311. van der Velden J et al (2004) Alterations in myofilament function contribute to left ventricular dysfunction in pigs early after myocardial infarction. Circ Res 95:e85–e95PubMedCrossRefGoogle Scholar
  312. van der Velden J et al (2006) Functional effects of protein kinase C-mediated myofilament phosphorylation in human myocardium. Cardiovasc Res 69:876–887PubMedCrossRefGoogle Scholar
  313. Vaughan KT, Weber FE, Einheber S, Fischman DA (1993) Molecular cloning of chicken myosin-binding protein (MyBP) H (86-kDa protein) reveals extensive homology with MyBP-C (C-protein) with conserved immunoglobulin C2 and fibronectin type III motifs. J Biol Chem 268:3670–3676PubMedGoogle Scholar
  314. Vibert P, Craig R, Lehman W (1997) Steric-model for activation of muscle thin filaments. J Mol Biol 266:8–14PubMedCrossRefGoogle Scholar
  315. Vinogradova MV et al (2005) Ca2 + -regulated structural changes in troponin. PNAS 102:5038–5043PubMedCentralPubMedCrossRefGoogle Scholar
  316. von Anrep G (1912) On the part played by the suprarenals in the normal vascular reactions of the body. J Physiol 45:307–317CrossRefGoogle Scholar
  317. von Kries J (1880) Untersuchungen zur mechanik des quergestreiften muskels. Archiv für Physiol, 348–374Google Scholar
  318. von Kries J (1892) Untersuchungen zur mechanik des quergestreiften muskeln. Archiv für Physiol, 1–21Google Scholar
  319. Wagner D, Weeds A (1977) Studies on the role of myosin alkali light chains. J Mol Biol 109:455–470PubMedCrossRefGoogle Scholar
  320. Wakabayashi K et al (1994) X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys J 67:2422–2435PubMedCentralPubMedCrossRefGoogle Scholar
  321. Wang YP, Fuchs F (1994) Length, force, and Ca(2+)-troponin C affinity in cardiac and slow skeletal muscle. Am J Physiol 266:1077–1082Google Scholar
  322. Wang Y-P, Fuchs F (1995) Osmotic compression of skinned cardiac and skeletal muscle bundles: Effects on force generation, Ca2+ sensitivity and Ca2+ binding. J Mol Cell Cardiol 27:1235–1244PubMedCrossRefGoogle Scholar
  323. Wang K, McClure J, Tu A (1979) Titin: major myofibrillar components of striated muscle. Proc Natl Acad Sci U S A 76:3698–3702PubMedCentralPubMedCrossRefGoogle Scholar
  324. Watanabe S (1955) Relaxing effects of EDTA on glycerol-treated muscle fibers. Arch Biochem Biophys 54:559–562PubMedCrossRefGoogle Scholar
  325. Weber H (1934) Die Muskeleiweisskörper und der Feinbau des Skeletmuskels. Ergebn Physiol Biol Chem Exp Pharmakol 36:109–150CrossRefGoogle Scholar
  326. Weber HHD (1935) Feinbau und die mechanischen Eigenschaften des Myosinfadens. Pflügers Archiv Eur J Physiol 235:205–233CrossRefGoogle Scholar
  327. Weber A (1959) On the role of calcium in the activity of adenosine 5′-triphosphate hydrolysis by actomyosin. J Biol Chem 234:2764–2769PubMedGoogle Scholar
  328. Weber A, Winicur S (1961) The role of calcium in the superprecipitation of actomyosin. J Biol Chem 236:3198–3202PubMedGoogle Scholar
  329. Weeds AG, Pope B (1971) Chemical studies on light chains from cardiac and skeletal muscle myosins. Nature 234:85–88PubMedCrossRefGoogle Scholar
  330. White HD, Taylor EW (1976) Energetics and mechanism of actomyosin adenosine triphosphatase. Biochemistry 15:5818–5826PubMedCrossRefGoogle Scholar
  331. Whitten AE, Jeffries CM, Harris SP, Trewhella J (2008) Cardiac myosin-binding protein C decorates F-actin: Implications for cardiac function. Proc Natl Acad Sci U S A 105:18360–18365PubMedCentralPubMedCrossRefGoogle Scholar
  332. Wiggers CJ (1921a) Studies on the consecutive phases of the cardiac cycle. Am J Physiol 56:415–438Google Scholar
  333. Wiggers CJ (1921b) The present status of cardiodynamic studies on normal and pathologic hearts. JAMA 27:475–502Google Scholar
  334. Wijnker PJM et al (2014) Length-dependent activation is modulated by cardiac troponin I bisphosphorylation at Ser23 and Ser24 but not by Thr143 phosphorylation. Am J Physiol 306:H1171–H1181Google Scholar
  335. Wilkinson JM, Perry SV, Cole H, Trayer IP (1971) Characterization of components of inhibitory-factor (troponin B) preparations of the myofibril. Biochem J 124:55P–56PPubMedCentralPubMedCrossRefGoogle Scholar
  336. Wilkinson JM, Perry S, Cole H, Trayer I (1972) The regulatory proteins of the myofibril. Separation and biological activity of the components of inhibitory-factor preparations. Biochem J 127:215–228PubMedCentralPubMedCrossRefGoogle Scholar
  337. Woods EF, Himmelfarb S, Harrington WF (1963) Studies on the structure of myosin in solution. J Biol Chem 238:2374–2385PubMedGoogle Scholar
  338. Xu S, Kress M, Huxley HE (1987) X-ray diffraction studies of the structural state of crossbridges in skinned frog sartorius muscle at low ionic strength. J Muscle Res Cell Motil 8:39–54PubMedCrossRefGoogle Scholar
  339. Xu S et al (1997) X-ray diffraction studies of cross-bridges weakly bound to actin in relaxed skinned fibers of rabbit psoas muscle. Biophys J 73:2292–2303PubMedCentralPubMedCrossRefGoogle Scholar
  340. Yamamoto K, Moos C (1983) The C-proteins of rabbit red, white, and cardiac muscles. J Biol Chem 258:8395–8401PubMedGoogle Scholar
  341. Zoghbi ME, Woodhead JL, Moss RL, Craig RW (2008) Three-dimensional structure of vertebrate cardiac muscle myosin filaments. Proc Natl Acad Sci U S A 105:2386–2390PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© International Union for Pure and Applied Biophysics (IUPAB) and Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Department of Physiology, Institute for Cardiovascular ResearchVU University Medical CenterAmsterdamThe Netherlands
  2. 2.ICIN- Netherlands Heart InstituteUtrechtThe Netherlands

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