Cardiac thin filament regulation and the Frank–Starling mechanism
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  • 作者:Fuyu Kobirumaki-Shimozawa (1)
    Takahiro Inoue (2)
    Seine A. Shintani (3)
    Kotaro Oyama (3)
    Takako Terui (4)
    Susumu Minamisawa (1)
    Shin’ichi Ishiwata (3) (5)
    Norio Fukuda (1)
  • 关键词:Calcium ; Cardiac muscle ; Troponin ; Titin
  • 刊名:The Journal of Physiological Sciences
  • 出版年:2014
  • 出版时间:July 2014
  • 年:2014
  • 卷:64
  • 期:4
  • 页码:221-232
  • 全文大小:934 KB
  • 参考文献:1. Katz AM (2002) Ernest Henry Starling, his predecessors, and the “Law of the Heart- Circulation 106:2986-992 CrossRef
    2. Plotnick GD, Becker LC, Fisher ML, Gerstenblith G, Renlund DG, Fleg JL, Weisfeldt ML, Lakatta EG (1986) Use of the Frank–Starling mechanism during submaximal versus maximal upright exercise. Am J Physiol 251:H1101–H1105
    3. Lakatta EG (1987) Starling law of the hearts explained by an intimate interaction of muscle length and myofilament calcium activation. J Am Coll Cardiol 10(5):1157-164 CrossRef
    4. Needham DM (1971) Machina Carnis: the biochemistry of muscular contraction and its historical development. Cambridge University Press, London CrossRef
    5. Terui T, Sodnomtseren M, Matsuba D, Udaka J, Ishiwata S, Ohtsuki I, Kurihara S, Fukuda N (2008) Troponin and titin coordinately regulate length-dependent activation in skinned porcine ventricular muscle. J Gen Physiol 131:275-83 CrossRef
    6. Fukuda N, Terui T, Ohtsuki I, Ishiwata S, Kurihara S (2009) Titin and troponin: central players in the Frank–Starling mechanism of the heart. Curr Cardiol Rev 5:119-24 CrossRef
    7. Terui T, Shimamoto Y, Yamane M, Kobirumaki F, Ohtsuki I, Ishiwata S, Kurihara S, Fukuda N (2010) Regulatory mechanism of length-dependent activation in skinned porcine ventricular muscle: role of thin filament cooperative activation in the Frank–Starling relation. J Gen Physiol 136:469-82 CrossRef
    8. Inoue T, Kobirumaki-Shimozawa F, Kagemoto T, Fujii T, Terui T, Kusakari Y, Hongo K, Morimoto S, Ohtsuki I, Hashimoto K, Fukuda N (2013) Depressed Frank–Starling mechanism in the left ventricular muscle of the knock-in mouse model of dilated cardiomyopathy with troponin T deletion mutation ΔK210. J Mol Cell Cardiol 63:69-8 CrossRef
    9. Bers DM (2001) Excitation–contraction coupling and cardiac contractile force. Kluwer, Dordrecht CrossRef
    10. Bers DM (2002) Cardiac excitation–contraction coupling. Nature 415:198-05 CrossRef
    11. Minamisawa S, Sato Y, Cho MC (2004) Calcium cycling proteins in heart failure, cardiomyopathy and arrhythmias. Exp Mol Med 36:193-03 CrossRef
    12. Bub G, Camelliti P, Bollensdorff C, Stuckey DJ, Picton G, Burton RA, Clarke K, Kohl P (2010) Measurement and analysis of sarcomere length in rat cardiomyocytes in situ and in vitro. Am J Physiol Heart Cric Physiol 298:H1616–H1625 CrossRef
    13. Kobirumaki-Shimozawa F, Oyama K, Serizawa T, Mizuno A, Kagemoto T, Shimozawa T, Ishiwata S, Kurihara S, Fukuda N (2012) Sarcomere imaging by quantum dots for the study of cardiac muscle physiology. J Biomed Biotechnol 2012:313814 CrossRef
    14. Solaro RJ, Rarick HM (1998) Troponin and tropomyosin: proteins that switch on and tune in the activity of cardiac myofilaments. Circ Res 83:471-80 CrossRef
    15. Takeda S, Yamashita A, Maeda K, Maéda Y (2003) Structure of the core domain of human cardiac troponin in the Ca2+-saturated form. Nature 424:35-1 CrossRef
    16. Ohtsuki I, Morimoto S (2008) Troponin: regulatory function and disorders. Biochem Biophys Res Commun 369:62-3 CrossRef
    17. Fukuda N, Fujita H, Fujita T, Ishiwata S (1998) Regulatory roles of MgADP and calcium in tension development of skinned cardiac muscle. J Muscle Res Cell Motil 19:909-21 CrossRef
    18. Fitzsimons DP, Moss RL (1998) Strong binding of myosin modulates length-dependent Ca2+ activation of rat ventricular myocytes. Circ Res 83:602-07 CrossRef
    19. Fukuda N, Kajiwara H, Ishiwata S, Kurihara S (2000) Effects of MgADP on length dependence of tension generation in skinned rat cardiac muscle. Circ Res 86:E1–E6 CrossRef
    20. Ishiwata S (1978) Studies on the F-actin.tropomyosin.troponin complex. III. Effects of troponin components and calcium ion on the binding affinity between tropomyosin and F-actin. Biochim Biophys Acta 534:350-57 CrossRef
    21. Oyama K, Mizuno A, Shintani SA, Itoh H, Serizawa T, Fukuda N, Suzuki M, Ishiwata S (2012) Microscopic heat pulses induce contraction of cardiomyocytes without calcium transients. Biochem Biophys Res Commun 417:607-12 CrossRef
    22. Sakai T (1986) Rapid cooling contracture. Jpn J Physiol 36:423-31 CrossRef
    23. Ishiwata S, Shimamoto Y, Fukuda N (2011) Contractile system of muscle as an auto-oscillator. Prog Biophys Mol Biol 105:187-98 CrossRef
    24. 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 72:667-99 CrossRef
    25. Sweitzer NK, Moss RL (1990) The effect of altered temperature on Ca2+-sensitive force in permeabilized myocardium and skeletal muscle. Evidence for force dependence of thin filament activation. J Gen Physiol 96:1221-245 CrossRef
    26. Fukuda N, Fujita H, Fujita T, Ishiwata S (1996) Spontaneous tension oscillation in skinned bovine cardiac muscle. Pflugers Arch 433:1- CrossRef
    27. Fukuda N, Ishiwata S (1999) Effects of pH on spontaneous tension oscillation in skinned bovine cardiac muscle. Pflugers Arch 438:125-32 CrossRef
    28. Sasaki D, Fukuda N, Ishiwata S (2006) Myocardial sarcomeres spontaneously oscillate with the period of heartbeat under physiological conditions. Biochem Biophys Res Commun 343:1146-152 CrossRef
    29. Sato K, Ohtaki M, Shimamoto Y, Ishiwata S (2011) A theory on auto-oscillation and contraction in striated muscle. Prog Biophys Mol Biol 105:199-07 CrossRef
    30. Sasaki D, Fujita H, Fukuda N, Kurihara S, Ishiwata S (2005) Auto-oscillations of skinned myocardium correlating with heartbeat. J Muscle Res Cell Motil 26:93-01 CrossRef
    31. Serizawa T, Terui T, Kagemoto T, Mizuno A, Shimozawa T, Kobirumaki F, Ishiwata S, Kurihara S, Fukuda N (2011) Real-time measurement of the length of a single sarcomere in rat ventricular myocytes: a novel analysis with quantum dots. Am J Physiol Cell Physiol 301:C1116–C1127 CrossRef
    32. Shintani SA, Oyama K, Kobirumaki-Shimozawa F, Ohki T, Ishiwata S, Fukuda N (2014) Sarcomere length nanometry in rat neonatal cardiomyocytes expressed with α-actinin-AcGFP in Z discs. J Gen Physiol 143:513-24
    33. Stehle R, Solzin J, Iorga B, Gomez D, Blaudeck N, Pfitzer G (2006) Mechanical properties of sarcomeres during cardiac myofibrillar relaxation: stretch-induced cross-bridge detachment contributes to early diastolic filling. J Muscle Res Cell Motil 27:423-34 CrossRef
    34. Allen DG, Kurihara S (1982) The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. J Physiol 327:79-4
    35. Hibberd MG, Jewell BR (1982) Calcium- and length-dependent force production in rat ventricular muscle. J Physiol 329:527-40
    36. Walker JS, Li X, Buttrick PM (2010) Analysing force–pCa curves. J Muscle Res Cell Motil 31:59-9 CrossRef
    37. Gordon AM, Huxley AF, Julian FJ (1966) The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol 184:170-92
    38. Fukuda N, Inoue T, Yamane M, Terui T, Kobirumaki F, Ohtsuki I, Ishiwata S, Kurihara S (2011) Sarcomere length-dependent Ca2+ activation in skinned rabbit psoas muscle fibers: coordinated regulation of thin filament cooperative activation and passive force. J Physiol Sci 61:515-23 CrossRef
    39. Moss RL, Fitzsimons DP (2002) Frank–Starling relationship: long on importance, short on mechanism. Circ Res 90:11-3 CrossRef
    40. Allen DG, Kentish JC (1985) The cellular basis of the length–tension relation in cardiac muscle. J Mol Cell Cardiol 17:821-40 CrossRef
    41. Fukuda N, Sasaki D, Ishiwata S, Kurihara S (2001) Length dependence of tension generation in rat skinned cardiac muscle: role of titin in the Frank–Starling mechanism of the heart. Circulation 104:1639-645 CrossRef
    42. 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 77:199-05 CrossRef
    43. Fuchs F, Wang YP (1996) Sarcomere length versus interfilament spacing as determinants of cardiac myofilament Ca2+ sensitivity and Ca2+ binding. J Mol Cell Cardiol 28:1375-383 CrossRef
    44. Fukuda N, O-Uchi J, Sasaki D, Kajiwara H, Ishiwata S, Kurihara S (2001) Acidosis or inorganic phosphate enhances the length dependence of tension in rat skinned cardiac muscle. J Physiol 536:153-60 CrossRef
    45. Huxley AF (1957) Muscle structure and theories of contraction. Prog Biophys Biophys Chem 7:255-18
    46. Ishiwata S, Oosawa F (1974) A regulatory mechanism of muscle contraction based on the flexibility change of the thin filaments. J Mechanochem Cell Motil 3:9-7
    47. 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 Heart Circ Physiol 279:H2568–H2573
    48. Granzier H, Labeit S (2002) Cardiac titin: an adjustable multi-functional spring. J Physiol 541:335-42 CrossRef
    49. Granzier HL, Labeit S (2004) The giant protein titin: a major player in myocardial mechanics, signaling, and disease. Circ Res 94:284-95 CrossRef
    50. Fukuda N, Granzier HL, Ishiwata S, Kurihara S (2008) Physiological functions of the giant elastic protein titin in mammalian striated muscle. J Physiol Sci 58:151-59 CrossRef
    51. Fukuda N, Terui T, Ishiwata S, Kurihara S (2010) Titin-based regulations of diastolic and systolic functions of mammalian cardiac muscle. J Mol Cell Cardiol 48:876-81 CrossRef
    52. Udaka J, Ohmori S, Terui T, Ohtsuki I, Ishiwata S, Kurihara S, Fukuda N (2008) Disuse-induced preferential loss of the giant protein titin depresses muscle performance via abnormal sarcomeric organization. J Gen Physiol 131:33-1 CrossRef
    53. 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 88:1028-035 CrossRef
    54. Fukuda N, Wu Y, Irving TC, Granzier H (2003) Titin isoform variance and length dependence of activation in skinned bovine cardiac muscle. J Physiol 553:147-54 CrossRef
    55. Konhilas JP, Irving TC, de Tombe PP (2002) Myofilament calcium sensitivity in skinned rat cardiac trabeculae: role of interfilament spacing. Circ Res 90:59-5 CrossRef
    56. Konhilas JP, Irving TC, de Tombe PP (2002) Length-dependent activation in three striated muscle types of the rat. J Physiol 544:225-36 CrossRef
    57. Konhilas JP, Irving TC, Wolska BM, Jweied EE, Martin AF, Solaro RJ, de Tombe PP (2003) Troponin I in the murine myocardium: influence on length-dependent activation and interfilament spacing. J Physiol 547:951-61 CrossRef
    58. Fukuda N, Wu Y, Farman G, Irving TC, Granzier H (2005) Titin-based modulation of active tension and interfilament lattice spacing in skinned rat cardiac muscle. Pflugers Arch 449:449-57 CrossRef
    59. Wakabayashi K, Sugimoto Y, Tanaka H, Ueno Y, Takezawa Y, Amemiya Y (1994) X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys J 67:2422-435 CrossRef
    60. Babu A, Sonnenblick E, Gulati J (1988) Molecular basis for the influence of muscle length on myocardial performance. Science 240:74-6 CrossRef
    61. Gulati J, Sonnenblick E, Babu A (1991) The role of troponin C in the length dependence of Ca2+-sensitive force of mammalian skeletal and cardiac muscles. J Physiol 441:305-24
    62. 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 440:273-89
    63. McDonald KS, Field LJ, Parmacek MS, Soonpaa M, Leiden JM, Moss RL (1995) Length dependence of Ca2+ sensitivity of tension in mouse cardiac myocytes expressing skeletal troponin C. J Physiol 483:131-39
    64. Kurihara S, Komukai K (1995) Tension-dependent changes of the intracellular Ca2+ transients in ferret ventricular muscles. J Physiol 489:617-25
    65. Fentzke RC, Buck SH, Patel JR, Lin H, Wolska BM, Stojanovic MO, Martin AF, Solaro RJ, Moss RL, Leiden JM (1999) Impaired cardiomyocyte relaxation and diastolic function in transgenic mice expressing slow skeletal troponin I in the heart. J Physiol 517:143-57 CrossRef
    66. 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 526:541-49 CrossRef
    67. Schwinger RH, Bohm M, Koch A, Schmidt U, Morano I, Eissner HJ, Uberfuhr P, Reichart B, Erdmann E (1994) The failing human heart is unable to use the Frank–Starling mechanism. Circ Res 74:959-69 CrossRef
    68. Ter Keurs HE (1996) Heart failure and Starling’s law of the heart. Can J Cardiol 12:1047-057
    69. van der Velden J, de Jong JW, Owen VJ, Burton PB, Stienen GJ (2000) Effect of protein kinase A on calcium sensitivity of force and its sarcomere length dependence in human cardiomyocytes. Cardiovasc Res 46:487-95 CrossRef
    70. Holubarsch C, Ruf T, Goldstein DJ, Ashton RC, Nickl W, Pieske B, Pioch K, Ludemann J, Wiesner S, Hasenfuss G, Posival H, Just H, Burkhoff D (1996) Existence of the Frank–Starling mechanism in the failing human heart. Investigations on the organ, tissue, and sarcomere levels. Circulation 94:683-89 CrossRef
    71. Sequeira V, Wijnker PJ, Nijenkamp LL, Kuster DW, Najafi A, Witjas-Paalberends ER, Regan JA, Boontje N, Ten Cate FJ, Germans T, Carrier L, Sadayappan S, van Slegtenhorst MA, Zaremba R, Foster DB, Murphy AM, Poggesi C, Dos Remedios C, Stienen GJ, Ho CY, Michels M, van der Velden J (2013) Perturbed length-dependent activation in human hypertrophic cardiomyopathy with missense sarcomeric gene mutations. Circ Res 112:1491-505 CrossRef
    72. Kajiwara H, Morimoto S, Fukuda N, Ohtsuki I, Kurihara S (2000) Effect of troponin I phosphorylation by protein kinase A on length-dependence of tension activation in skinned cardiac muscle fibers. Biochem Biophys Res Commun 272:104-10 CrossRef
    73. Manolio TA, Baughman KL, Rodeheffer R, Pearson TA, Bristow JD, Michels VV, Abelmann WH, Harlan WR (1992) Prevalence and etiology of idiopathic dilated cardiomyopathy. Am J Cardiol 69:1458-466 CrossRef
    74. Dec GW, Fuster V (1994) Idiopathic dilated cardiomyopathy. N Engl J Med 331:1564-575 CrossRef
    75. Kasper EK, Agema WR, Hutchins GM, Deckers JW, Hare JM, Baughman KL (1994) The causes of dilated cardiomyopathy: a clinicopathologic review of 673 consecutive patients. J Am Coll Cardiol 23:586-90 CrossRef
    76. Towbin JA, Bowles NE (2002) The failing heart. Nature 415:227-33 CrossRef
    77. Kamisago M, Sharma SD, DePalma SR, Solomon S, Sharma P, McDonough B, Smoot L, Mullen MP, Woolf PK, Wigle ED, Seidman JG, Seidman CE (2000) Mutations in sarcomere protein genes as a cause of dilated cardiomyopathy. N Engl J Med 343:1688-696 CrossRef
    78. Du CK, Morimoto S, Nishii K, Minakami R, Ohta M, Tadano N, Lu QW, Wang YY, Zhan DY, Mochizuki M, Kita S, Miwa Y, Takahashi-Yanaga F, Iwamoto T, Ohtsuki I, Sasaguri T (2007) Knock-in mouse model of dilated cardiomyopathy caused by troponin mutation. Circ Res 101:185-94 CrossRef
    79. Nagueh SF, Shah G, Wu Y, Torre-Amione G, King NM, Lahmers S, Witt CC, Becker K, Labeit S, Granzier HL (2004) Altered titin expression, myocardial stiffness, and left ventricular function in patients with dilated cardiomyopathy. Circulation 110:155-62 CrossRef
    80. Makarenko I, Opitz CA, Leake MC, Neagoe C, Kulke M, Gwathmey JK, del Monte F, Hajjar RJ, Linke WA (2004) Passive stiffness changes caused by upregulation of compliant titin isoforms in human dilated cardiomyopathy hearts. Circ Res 95:708-16 CrossRef
    81. Hidalgo C, Hudson B, Bogomolovas J, Zhu Y, Anderson B, Greaser M, Labeit S, Granzier H (2009) PKC phosphorylation of titin’s PEVK element: a novel and conserved pathway for modulating myocardial stiffness. Circ Res 105:631-38 CrossRef
    82. Montgomery DE, Rundell VL, Goldspink PH, Urboniene D, Geenen DL, de Tombe PP, Buttrick PM (2005) Protein kinase C epsilon induces systolic cardiac failure marked by exhausted inotropic reserve and intact Frank–Starling mechanism. Am J Physiol Heart Circ Physiol 289:H1881–H1888 CrossRef
    83. Yumoto F, Lu QW, Morimoto S, Tanaka H, Kono N, Nagata K, Ojima T, Takahashi-Yanaga F, Miwa Y, Sasaguri T, Nishita K, Tanokura M, Ohtsuki I (2005) Drastic Ca2+ sensitization of myofilament associated with a small structural change in troponin I in inherited restrictive cardiomyopathy. Biochem Biophys Res Commun 338:1519-526 CrossRef
  • 作者单位:Fuyu Kobirumaki-Shimozawa (1)
    Takahiro Inoue (2)
    Seine A. Shintani (3)
    Kotaro Oyama (3)
    Takako Terui (4)
    Susumu Minamisawa (1)
    Shin’ichi Ishiwata (3) (5)
    Norio Fukuda (1)

    1. Department of Cell Physiology, The Jikei University School of Medicine, 3-25-8 Nishi-shinbashi, Minato-ku, Tokyo, 105-8461, Japan
    2. Department of Cardiac Surgery, The Jikei University School of Medicine, Tokyo, Japan
    3. Department of Physics, Faculty of Science and Engineering, Waseda University, 3-14-9 Okubo, Shinjuku-ku, Tokyo, 169-0072, Japan
    4. Department of Anesthesiology, The Jikei University School of Medicine, Tokyo, Japan
    5. Waseda Bioscience Research Institute in Singapore (WABIOS), 11 Biopolis Way, #05-01/02 Helios, Singapore, 138667, Singapore
  • ISSN:1880-6562
文摘
The heart has an intrinsic ability to increase systolic force in response to a rise in ventricular filling (the Frank–Starling law of the heart). It is widely accepted that the length dependence of myocardial activation underlies the Frank–Starling law of the heart. Recent advances in muscle physiology have enabled the identification of the factors involved in length-dependent activation, viz., titin (connectin)-based interfilament lattice spacing reduction and thin filament “on–off-regulation, with the former triggering length-dependent activation and the latter determining the number of myosin molecules recruited to thin filaments. Patients with a failing heart have demonstrated reduced exercise tolerance at least in part via depression of the Frank–Starling mechanism. Recent studies revealed that various mutations occur in the thin filament regulatory proteins, such as troponin, in the ventricular muscle of failing hearts, which consequently alter the Frank–Starling mechanism. In this article, we review the molecular mechanisms of length-dependent activation, and the influence of troponin mutations on the phenomenon.

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