Length-dependent Ca2+ activation in cardiac muscle: some remaining questions
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- 作者：Franklin Fuchs (1)
Donald A. Martyn (2) - 刊名：Journal of Muscle Research and Cell Motility
- 出版年：2005
- 出版时间：November 2005
- 年：2005
- 卷：26
- 期：4-5
- 页码：199-212
- 全文大小：321KB
- 参考文献：1. Adhikari BB, Fajer PG, (1996) Myosin head orientation and mobility during isometric contraction: effects of osmotic compression Biophys J 70: 1872880
2. Adhikari B, Regnier M, Rivera AJ, Kreutziger KL, Martyn DA, (2004) Cardiac length dependence of force and force redevelopment kinetics with altered cross-bridge cycling Biophys J 87: 1784794 CrossRef
3. Allen DG, Jewell BR, Murray JW, (1974) The contribution of activation process to the length-tension relation in cardiac muscle Nature 248: 50913
4. Allen DG, Kentish JC, (1985) The cellular basis of the length-tension relation in cardiac muscle J Mol Cell Cardiol 17: 82140 CrossRef
5. Allen DG, Kentish JC, (1988) Calcium concentration in the myoplasm of skinned ferret ventricular muscle following changes in muscle length J Physiol 407:48903
6. Allen DG, Kurihara S, (1982) The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle J Physiol 327: 794
7. 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: 54149 CrossRef
8. Balnave CD, Allen DG, (1996) The effect of muscle length on intracellular calcium and force in single fibres from mouse skeletal muscle J Physiol 492: 70513
9. Bremel RD, Weber A, (1972) Cooperation within actin filament in striated muscle Nature New Biol 238: 9701
10. Brenner B, Yu LC, (1985) Equatorial X-ray diffraction from single skinned rabbit psoas fibers at various degrees of activation Biophys J 48: 82934 CrossRef
11. Brenner B, Yu LC, Chalovich JM, (1991) Parallel inhibition of active force and relaxed fiber stiffness in skeletal muscle by caldesmon Proc Nat Acad Sci USA 88: 5739743 CrossRef
12. Brenner B, Yu LC, Podolsky RJ, (1984) X-ray diffraction evidence for cross-bridge formation in relaxed muscle fibers at various ionic strengths Biophys J 46: 29906
13. Cazorla O, Pascarel C, Garnier D, LeGuennec J-Y, (1997) Resting tension participates in the modulation of active tension in isolated guinea pig ventricular myocytes J Mol Cell Cardiol 29: 1629637 CrossRef
14. Cazorla O, Vassort G, Garnier D, LeGuennec J-Y, (1999) Length modulation of active force in rat cardiac myocytes: is titin the sensor? J Mol Cell Cardiol 31: 1215227 CrossRef
15. 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: 1028035 CrossRef
16. Close RI, (1972) The relations between sarcomere length and characteristics of isometric twitch contractions of frog sartorius muscle J Physiol 220: 74562
17. Endo M, (1972) Stretch-induced increase in activation of skinned muscle fibres by calcium Nature New Biol 237: 21113 CrossRef
18. Fabiato A, (1981) Myoplasmic free calcium concentration reached during the twitch of an intact isolated cardiac cell and during calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned cardiac cell from the adult rat or rabbit ventricle J Gen Physiol 78: 45797 CrossRef
19. 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: 67799 CrossRef
20. Fitzsimons DP, Moss RL, (1998) Strong binding of myosin modulates length-dependent Ca2+ activation of rat ventricular myocytes Circ Res 83: 60207
21. Fuchs F, (1995) Mechanical modulation of the Ca2+ regulatory protein complex in cardiac muscle News Physiol Sci 10:62
22. Fuchs F, (2002) The Frank–Starling relationship: cellular and molecular mechanisms. In: Solaro RJ, Moss RL, (eds.) Molecular Control Mechanisms in Striated Muscle Contraction. Kluwer, Dordrecht, pp. 37915
23. Fuchs F, Smith SH, (2001) Calcium, cross-bridges, and the Frank–Starling relationship News Physiol Sci 16: 50
24. Fuchs F, Wang YP, (1991) Force, length, and Ca2+-troponin C affinity in skeletal muscle Am J Physiol 261: C787–C792
25. Fuchs F, Wang Y, (1996) Sarcomere length vs. interfilament spacing as determinants of cardiac myofilament Ca2+ sensitivity and Ca2+ binding J Mol Cell Cardiol 28: 1375383 CrossRef
26. Fujino K, Sperelakis N, Solaro RJ, (1988) Sensitization of dog and guinea pig heart myofilaments to Ca2+ activation and the inotropic effect of pimobendan: comparison with milrinone Circ Res 63: 91122
27. Fujita H, Labeit D, Gerull B, Labeit S, Granzier HL, (2004) Titin isoform-dependent effect of calcium on passive myocardial tension Am J Physiol 287: H2528–H2534
28. 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
29. Fukuda N, Jin O-U, Sasaki D, Kajiwara H, Ishiwata S, Kurihara S, (2001a) Acidosis or inorganic phosphate enhances the length dependence of tension in rat skinned cardiac muscle J Physiol 536: 15360 CrossRef
30. Fukuda N, Sasaki D, Ishiwata S, Kurihara S, (2001b) Length dependence of tension generation in rat skinned cardiac muscle. Role of titin in the Frank–Starling mechanism of the heart Circulation 104:1639645 CrossRef
31. Fukuda N, Wu Y, Irving TC, Granzier H, (2003) Titin isoform variance and length dependence of activation in skinned bovine cardiac muscleJ Physiol 553:14754 CrossRef
32. Fukuda N, Wu Y, Farman G, Irving TC, Granzier H, (2005a) Titin-based modulation of active tension and interfilament lattice spacing in skinned rat cardiac muscle Pflugers Arch 449: 44957 CrossRef
33. Fukuda N, Wu Y, Nair P, Granzier HL, (2005b) Phosphorylation of titin modulates passive stiffness of cardiac muscle in a titin isoform-dependent manner J Gen Physiol 124: 25771 CrossRef
34. Gao WD, Backx PH, Azan-Backx M, Marban E, (1994) Myofilament Ca2+ sensitivity in intact versus skinned rat ventricular muscle Circ Res 74: 40815
35. Godt RE, Maughan DW, (1977) Swelling of skinned muscle fibres of the frog Biophys J 19: 10316 CrossRef
36. Godt RE, Maughan DW, (1981) Influence of osmotic compression on calcium activation and tension in skinned muscle fibres of the rabbit Pflugers Arch 391: 33437
37. Gordon AM, Homsher E, Regnier M, (2000) Regulation of contraction in striated muscle Physiol Rev 80: 85324
38. Gordon AM, Huxley AF, Julian FJ, (1966) The variation in isometric tension with sarcomere length in vertebrate muscle fibres J Physiol 184: 17092
39. Granzier H, Labeit S, (2002) Cardiac titin: an adjustable multifunctional spring J Physiol 541: 33542 CrossRef
40. Harrison SM, Lamont C, Miller DJ, (1988) Hysteresis and the length dependence of calcium sensitivity in chemically-skinned rat cardiac muscle J Physiol 401:11543
41. Head JG, Ritchie MD, Geeves MA, (1995) Characterization of the equilibrium between blocked and closed states of muscle thin filaments Eur J Biochem 227: 69499 CrossRef
42. Hibberd MJ and Jewell BR (1982) Calcium and length dependent force production in rat ventricular muscle. J Physiol 329: 52740.
43. Hofmann PA, Fuchs F, (1987a) Effect of length and cross-bridge attachment on Ca2+ binding to cardiac troponin C Am J Physiol 253: C90–C96
44. Hofmann PA, Fuchs F, (1987b) Evidence for a force-dependent component of calcium binding to cardiac troponin C Am J Physiol 253: C541–C546
45. Hofmann PA, Fuchs F, (1988) Bound calcium and force development in skinned cardiac muscle bundles: effect of sarcomere length J Mol Cell Cardiol 20: 66777 CrossRef
46. Irving TC, Konhilas J, Perry D, Fischetti R, DeTombe PP, (2000) Myofilament lattice spacing as a function of sarcomere length in isolated myocardium Am J Physiol 279: H2568–H2573
47. Jewell BR, (1977) A reexamination of the influence of muscle length on cardiac performance Circ Res 40: 22130
48. 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 Comm 272: 10410 CrossRef
49. Kawai M, Wray JS, Zhao Y, (1993) The effect of lattice spacing change on cross-bridge kinetics in chemically skinned rabbit psoas muscle fibers. I. proportionality between the lattice spacing and the fiber width Biophys J 64: 18796
50. Kentish JC, ter Keurs HEDJ, Ricciardi L, Bucx JJJ, Noble MIM, (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: 75568
51. Komukai K, Kurihara S, (1997) Length dependence of Ca2+–tension relationship in aequorin-injected ferret papillary muscles Am J Physiol 273: H1068–H1074
52. Konhilas JP, Irving TC, deTombe PP, (2002a) Frank–Starling law of the heart and the cellular mechanisms of length-dependent activation Pflugers Arch 445:30510 CrossRef
53. Konhilas JP, Irving TC, deTombe PP, (2002b) Myofilament calcium sensitivity in skinned rat cardiac trabeculae: role of interfilament spacing Circ Res 90: 595 CrossRef
54. Konhilas JP, Irving TC, deTombe PP, (2002c) Length-dependent activation in three striated muscle types of the rat J Physiol 544: 22536 CrossRef
55. Konhilas JP, Irving TC, Wolska BM, Jwied EE, Martin AF, Solaro RJ, deTombe PP, (2003) Troponin I in the murine myocardium: influence on length-dependent activation and interfilament spacing J Physiol 537: 95161 CrossRef
56. Kraft T, Brenner B, (1997) Force enhancement without changes in cross-bridge turnover kinetics: the effect of EMD 57033 Biophys J 72: 27282
57. Lakatta EG, (1992) Length modulation of muscle performance: Frank–Starling law of the heart. In: Fozzard HA, Jennings RB, Haber E, Katz AM, Morgan HA, (eds.). The Heart and Cardiovascular System Vol. II. Raven Press, New York, pp.1325351
58. Lakatta EG, Jewell BR, (1977) Length-dependent activation. Its’effect on the length-tension relation in cat ventricular muscle Circ Res 40: 25157
59. Lehman W, Hatch V, Korman V, Rosol M, Thomas L, Maytum R, Geeves MA, Van Eyck JE, Tobacman LS, Craig R, (2000) Tropomyosin and actin isoforms modulate the localization of tropomyosin strands on actin filaments J Mol Biol 302: 59306 CrossRef
60. Lehrer SS, (1994) The regulatory switch of the muscle thin filament: Ca2+ or myosin heads? J Muscle Res Cell Motil 15:23236 CrossRef
61. Levine RJC, Kensler RW, Yang Z, Stull JT, Sweeney HL, (1996) Myosin light chain phosphorylation affects the structure of rabbit skeletal muscle thick filaments Biophys J 71: 89807
62. 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 9:42845 CrossRef
63. Martyn DA, Gordon AM, (2001) Influence of length or force on activation-dependent changes in troponin C structure in skinned cardiac and fast skeletal muscle Biophys J 80: 2798808 CrossRef
64. Martyn DA, Regnier M, Xu D, Gordon AM, (2001) Ca2+- and cross-bridge-dependent changes in N- and C- terminal structure of troponin C in rat cardiac muscle Biophys J 80: 36070
65. Martyn DA, Adhikari BB, Regnier M, Gu J, Xu S, Yu LC, (2004) Response of equatorial X-ray reflections and stiffness to altered sarcomere length and myofilament lattice spacing in relaxed skinned cardiac muscle Biophys J 86: 1002011
66. Martyn DA, Smith L, (2005a) The temperature dependence of length-dependent contractile activation in cardiac muscle Biophys J 88: 120a
67. Martyn DA, Smith L, (2005b) The length sensitivity of contractile activation in cardiac muscle is dependent on the extent of strong CB binding Biophys J 88: 121a
68. 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: 19905
69. McKillop DFA, Geeves MA, (1993) Regulation of the interaction between actin and myosin subfragmant 1: evidence for three states of the thin filament Biophys J 65: 69301
70. Metzger J, (1995) Myosin binding-induced cooperative activation of the thin filament in cardiac myocytes and skeletal muscle fibers Biophys J 68: 1430442
71. Millman BM, (1998) The filament lattice of striated muscle Physiol Rev 78: 35991
72. Muhle-Goll C, Habeck M, Cazorla O, Nilges M, Labeit, Granzier H, (2001) Structural and functional studies of titin’s fn3 modules reveal conserved surface patterns and binding to myosin S1–a possible role in the Frank–Starling mechanism of the heart J Mol Biol 313: 43147 CrossRef
73. Olsson MC, Patel JR, Fitzsimons DP, Walker JW, Moss RL, (2004) Basal myosin light chain phosphorylation is a determinant of Ca2+ sensitivity and force and activation dependence of the kinetics of myocardial force development Am J Physiol 287: H2712–H2718
74. Patel JR, McDonald KS, Wolff MR, Moss RL, (1997) Ca2+ binding to troponin C in skinned skeletal muscle fibers assessed with caged Ca2+ and a Ca2+ fluophore: invariance of Ca2+ binding as a function of sarcomere length J Biol Chem 272: 6018027 CrossRef
75. Pirani A, Xu C, Hatch V, Craig R, Tobacman LS, Lehman W, (2005) Single particle analysis of relaxed and activated muscle thin filaments J Mol Biol 346:76172 CrossRef
76. Regnier M, Rivera AJ, Wang C-K, Bates MA, Chase PB, Gordon AM, (2002) Thin filament near-neighbor regulatory unit interactions affect rabbit skeletal muscle steady-state force-Ca2+ relations J Physiol 540: 48597 CrossRef
77. Rice JJ, deTombe PP, (2004) Approaches to modeling cross-bridges and calcium-dependent activation in cardiac muscle Prog Biophys Mol Biol 85: 17995 CrossRef
78. Robinson JM, Dong W-J, Xing J, Cheung HC, (2004) Switching of troponin I: Ca2+ and myosin induced activation of heart muscle J Mol Biol 340: 29505 CrossRef
79. Saeki Y, Kurihara S, Hongo K, Tanaka E, (1993) Alterations in intracellular calcium and tension of activated ferret papillary muscle in response to step length changes J Physiol 463: 29106
80. Smith SH, Fuchs F, (1999) Effect of ionic strength on length-dependent Ca2+ activation in skinned cardiac muscle J Mol Cell Cardiol 31:2115125 CrossRef
81. Smith SH, Fuchs F, (2000) Length-dependence of cross-bridge mediated activation of the cardiac thin filament J Mol Cell Cardiol 32: 83138 CrossRef
82. Smith SH, Fuchs F, (2002) Length dependence of cardiac myofilament Ca2+ sensitivity in the presence of substitute nucleoside triphosphates J Mol Cell Cardiol 34:54754 CrossRef
83. Stephenson DG, Wendt IR, (1984) Length dependence of changes in sarcoplasmic calcium concentration and myofibrillar calcium sensitivity in striated muscle fibres J Musc Res Cell Motil 5: 24372 CrossRef
84. Stienen GJM, Blange T, Treijtel BW, (1985) Tension development and calcium sensitivity in skinned muscle fibers of the frog Pflugers Arch 405: 193 CrossRef
85. ter Keurs HEDJ, Rignsburger WH, van Heuningen R, Nagelsmit MJ, (1980) Tension development and sarcomere length in rat cardiac trabeculae: evidence of length-dependent activation Circ Res 46: 70314
86. Tskhovrebova L, Trinick J, (2003) Titin: properties and family relationships Nat Rev Mol Cell Biol 4: 67989 CrossRef
87. van der Velden J, deJong JW, Owen VJ, BurtonPBJ, Stienen GJM, (2000) Effect of protein kinase A on calcium sensitivity of force and itssarcomere length dependence in human cardiomyocytes Cardiovasc Res 46: 48795 CrossRef
88. van der Velden J, Papp Z, Zaremba R, Boontje NM, deJong JW, Owen VJ, Burton PBJ, Goldmann P, Jaquet K, Stienen GJM, (2003). Increased Ca2+ sensitivity of the contractile apparatus in end-stage human heart failure results from altered phosphorylation of contractile proteins Cardiovasc Res 57: 377 CrossRef
89. Vibert P, Craig R, Lehman W, (1997) Steric-model for activation of muscle thin filaments J Mol Biol 266: 84 CrossRef
90. Wang Y-P, Fuchs F, (1994) Length, force, and Ca2+-troponin C affinity in cardiac and slow skeletal muscle Am J Physiol 266: C1077–C1082
91. Wang Y, Fuchs F, (1995) Osmotic compression of skinned cardiac and skeletal muscle bundles: effects on force generation, Ca2+ sensitivity, and Ca 2+ binding J Mol Cell Cardiol 27: 1235244 CrossRef
92. Wang Y, Fuchs F, (2001) Interfilament spacing, Ca2+ sensitivity, and Ca2+ binding in skinned bovine cardiac muscle J Muscle Res Cell Motil 22: 25157 CrossRef
93. Wolska BM, Kitada Y, Palmiter KA, Westfall MV, Johnson MD, Solaro RJ, (1996) CGP-48506 increases contractility of ventricular myocytes and myofilaments by effects on actin–myosin reaction Am J Physiol 270: H24–H32
94. Yamasaki R, Wu Y, McNabb M, Greaser M, Labeit S, Granzier H, (2002) Protein kinase A phosphorylates titin’s cardiac specific N2B domain and reduces passive tension in rat cardiac myocytes Circ Res 90: 1181188 CrossRef
95. Yagi N, Shimizu J, Mohri S, Araki J, Nakamura K, Okuyama H, Toyota H, Morimoto T, Morizane Y, Kurusu M, Hashimoto K, Tsujioka K, Suga H, Kaliya F, (2004) X-ray diffraction from a left ventricular wall of rat heart Biophys J 86: 2286294
96. Yang Z, Stull JT, Levine RJC, Sweeney HL, (1998) Changes in interfilament spacing mimic the effects of myosin regulatory light chain phosphorylation in rabbit psoas fibers J Struct Biol 122: 13948 CrossRef
97. Zuurbier CJ, Lee-de Groot MBE, Van der Laarse WJ, Huijing PA, (1998) Effects of in vivo-like activation frequency on the length-dependent force generation of skeletal muscle fiber bundles Eur J Appl Physiol 77: 50310 CrossRef - 作者单位：Franklin Fuchs (1)
Donald A. Martyn (2)
1. Department of Cell Biology and Physiology, University of Pittsburgh School of Medicine, Pittsburgh, PA, 15261, USA
2. Department of Bioengineering, University of Washington, Box 357962, Seattle, WA, 98195, USA
文摘
The steep relationship between systolic force and end diastolic volume in cardiac muscle (Frank–Starling relation) is, to a large extent, based on length-dependent changes in myofilament Ca2+ sensitivity. How sarcomere length modulates Ca2+ sensitivity is still a topic of active investigation. Two general themes have emerged in recent years. On the one hand, there is a large body of evidence indicating that length-dependent changes in lattice spacing determine changes in Ca2+ sensitivity for a given set of conditions. A model has been put forward in which the number of strong-binding cross-bridges that are formed is directly related to the proximity of the myosin heads to binding sites on actin. On the other hand, there is also a body of evidence suggesting that lattice spacing and Ca2+ sensitivity are not tightly linked and that there is a length-sensing element in the sarcomere, which can modulate actin–myosin interactions independent of changes in lattice spacing. In this review, we examine the evidence that has been cited in support of these viewpoints. Much recent progress has been based on the combination of mechanical measurements with X-ray diffraction analysis of lattice spacing and cross-bridge interaction with actin. Compelling evidence indicates that the relationship between sarcomere length and lattice spacing is influenced by the elastic properties of titin and that changes in lattice spacing directly modulate cross-bridge interactions with thin filaments. However, there is also evidence that the precise relationship between Ca2+ sensitivity and lattice spacing can be altered by changes in protein isoform expression, protein phosphorylation, modifiers of cross-bridge kinetics, and changes in titin compliance. Hence although there is no unique relationship between Ca2+ sensitivity and lattice spacing the evidence strongly suggests that under any given set of physiological circumstances variation in lattice spacing is the major determinant of length-dependent changes in Ca2+ sensitivity.