The molecular basis of the steep force-calcium relation in heart muscle

Journal of Molecular and Cellular Cardiology

Volumn 48, Issue 5, 2010, Pages 859-865

  Sun, Yin Biao ^a   Irving, Malcolm ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Calcium regulation; Force calcium relation; Muscle regulation; Troponin

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; FLUORESCENT DYE; MYOSIN; TROPONIN;

CALCIUM BINDING; CALCIUM CELL LEVEL; HEART CONTRACTION; HEART MUSCLE; HEART MUSCLE CELL; HEART MUSCLE POTENTIAL; HEART OUTPUT; HUMAN; MUSCLE FORCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; STEADY STATE; THIN FILAMENT;

ANIMALS; CALCIUM; HUMANS; MYOCARDIUM; MYOSINS; PROTEIN BINDING; TROPONIN;

EID: 77951623260     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2009.11.019     Document Type: Review

References (70)

1. Tobacman L.S. Thin filament-mediated regulation of cardiac contraction. Annu. Rev. Physiol. 1996, 58:447-481.
2. Gordon A.M., Homsher E., Regnier M. Regulation of contraction in striated muscle. Physiol. Rev. 2000, 80:853-924.
3. Kobayashi T., Solaro R.J. Calcium, thin filaments, and the integrative biology of cardiac contractility. Annu. Rev. Physiol. 2005, 67:39-67.
4. Gordon A.M., Regnier M., Homsher E. Skeletal and cardiac muscle contractile activation: tropomyosin "rocks and rolls". News Physiol. Sci. 2001, 16:49-55.
5. Moss R.L., Razumova M., Fitzsimons D.P. Myosin crossbridge activation of cardiac thin filaments: implications for myocardial function in health and disease. Circ. Res. 2004, 94:1290-1300.
6. Hinken A.C., Solaro R.J. A dominant role of cardiac molecular motors in the intrinsic regulation of ventricular ejection and relaxation. Physiology 2007, 22:73-80.
7. Sun Y.-B., Lou F., Irving M. Calcium- and myosin-dependent changes in troponin structure during activation of heart muscle. J. Physiol. 2009, 587:155-163.
8. Holroyde M.J., Robertson S.P., Johnson J.D., Solaro R.J., Potter J.D. The calcium and magnesium binding sites on cardiac troponin and their role in the regulation of myofibrillar adenosine triphosphatase. J. Biol. Chem. 1980, 255:11688-11693.
9. Pan B.S., Solaro R.J. Calcium-binding properties of troponin C in detergent-skinned heart muscle fibers. J. Biol. Chem. 1987, 262:7839-7849.
10. 2+ sensitivity in intact versus skinned rat ventricular muscle. Circ. Res. 1994, 74:408-415.
11. Allen D.G., Blinks J.R. Calcium transients in aequorin-injected frog cardiac muscle. Nature 1978, 273:509-513.
12. 2+] in intact rat cardiac trabeculae. J. Gen. Physiol. 1995, 105:1-19.
13. Allen D.G., Kentish J.C. Calcium concentration in the myoplasm of skinned ferret ventricular muscle following changes in muscle length. J. Physiol. 1988, 407:489-503.
14. Baran D., Ogino K., Stennett R., Schnellbacher M., Zwas D., Morgan J.P., et al. Interrelating of ventricular pressure and intracellular calcium in intact hearts. Am. J. Physiol. 1997, 273:H1509-H1522.
15. Smith N.P., Crampin E.J., Niederer S.A., Bassingthwaighte J.B., Beard D.A. Computational biology of cardiac myocytes: proposed standards for the physiome. J. Exp. Biol. 2007, 210:1576-1583.
16. Campbell K.B., Simpson A.M., Campbell S.G., Granzier H.L., Slinker B.K. Dynamic left ventricular elastance: a model for integrating cardiac muscle contraction into ventricular pressure-volume relationships. J. Appl. Physiol. 2008, 104:958-975.
17. Holmes K.C., Popp D., Gebhard W., Kabsch W. Atomic model of the actin filament. Nature 1990, 347:44-49.
18. Oda T., Iwasa M., Aihara T., Maeda Y., Narita A. The nature of the globular- to fibrous-actin transition. Nature 2009, 457:441-445.
19. Brown J.H., Zhou Z., Reshetnikova L., Robinson H., Yammani R.D., Tobacman L.S., et al. Structure of the mid-region of tropomyosin: bending and binding sites for actin. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:18878-18883.
20. Sia S.K., Li M.X., Spyracopoulos L., Gagne S.M., Liu W., Putkey J.A., et al. Structure of cardiac muscle troponin C unexpectedly reveals a closed regulatory domain. J. Biol. Chem. 1997, 272:18216-18221.
21. 2+-saturated form. Nature 2003, 424:35-41.
22. Huxley H.E. Structural changes in the actin- and myosin-containing filaments during contraction. Cold Spring Harbor Symp. Quant. Biol. 1973, 37:361-376.
23. Parry D.A.D., Squire J.M. Structural role of tropomyosin in muscle regulation: analysis of the X-ray diffraction patterns from relaxed and contracting muscles. J. Mol. Biol. 1973, 75:33-55.
24. 2+-induced tropomyosin movement in Limulus thin filaments revealed by three-dimensional reconstruction. Nature 1994, 368:65-67.
25. Kimura-Sakiyama C., Ueno Y., Wakabayashi K., Miki M. Fluorescence resonance energy transfer between residues on troponin and tropomyosin in the reconstituted thin filament: modeling the troponin-tropomyosin complex. J. Mol. Biol. 2008, 376:80-91.
26. Chalovich J.M., Eisenberg E. Inhibition of actomyosin ATPase activity by troponin-tropomyosin without blocking the binding of myosin to actin. J. Biol. Chem. 1982, 257:2432-2437.
27. Kress M., Huxley H.E., Faruqi A.R., Hendrix J. Structural changes during activation of frog muscle studied by time-resolved X-ray diffraction. J. Mol. Biol. 1986, 188:325-342.
28. Matsuo T., Yagi N. Structural changes in the muscle thin filament during contractions caused by single and double electrical pulses. J. Mol. Biol. 2008, 383:1019-1036.
29. Huxley A.F. Muscle structure and theories of contraction. Prog. Biophys. Biophys. Chem. 1957, 7:255-318.
30. Huxley A.F., Simmons R.M. Proposed mechanism of force generation in striated muscle. Nature 1971, 233:533-538.
31. McKillop D.F.A., Geeves M.A. Regulation of the interaction between actin and myosin subfragment 1: evidence for three states of the thin filament. Biophys. J. 1993, 65:693-701.
32. Hill T.L., Eisenberg E., Greene L. Theoretical model for the cooperative equilibrium binding of myosin subfragment 1 to the actin-troponin-tropomyosin complex. Proc. Natl. Acad. Sci. U. S. A. 1980, 77:3186-3190.
33. Brandt P.W., Diamond M.S., Rutchik J.S., Schachat F.H. Co-operative interactions between troponin-tropomyosin units extend the length of the thin filament in skeletal muscle. J. Mol. Biol. 1987, 195:885-896.
34. Tobacman L.S., Sawyer D. Calcium binds cooperatively to the regulatory sites of the cardiac thin filament. J. Biol. Chem. 1990, 265:931-939.
35. Rosenfeld S.S., Taylor E.W. Kinetic studies of calcium binding to regulatory complexes from skeletal muscle. J. Biol. Chem. 1985, 260:252-261.
36. 2+ and myosin-induced activation of heart muscle. J. Mol. Biol. 2004, 340:295-305.
37. Davis J.P., Norman C., Kobayashi T., Solaro R.J., Swartz D.R., Tikunova S.B. Effects of thin and thick filament proteins on calcium binding and exchange with cardiac troponin C. Biophys. J. 2007, 92:3195-3206.
38. Hofmann P.A., Fuchs F. Evidence for a force-dependent component of calcium binding to cardiac troponin C. Am. J. Physiol. 1987, 253:C541-C546.
39. 2+-troponin C affinity in cardiac and slow skeletal muscle. Am. J. Physiol. 1994, 266:C1077-C1082.
40. Strauss J.D., Zeugner C., Van Eyk J.E., Bletz C., Troschka M., Ruegg J.C. Troponin replacement in permeabilized cardiac muscle. Reversible extraction of troponin I by incubation with vanadate. FEBS Lett. 1992, 310:229-234.
41. Agianian B., Krzic U., Qiu F., Linke W.A., Leonard K., Bullard B. A troponin switch that regulates muscle contraction by stretch instead of calcium. EMBO J. 2004, 23:772-779.
42. De Simone A.D., Corrie J.E.T., Dale R.E., Irving M., Fraternali F. Conformation and dynamics of a rhodamine probe attached at two sites on a protein: implications for molecular structure determination in situ. J. Am. Chem. Soc. 2008, 130:17120-17128.
43. Ferguson R.E., Sun Y.-B., Mercier P., Brack A.S., Sykes B.D., Corrie J.E.T., et al. In situ orientations of protein domains: troponin C in skeletal muscle fibers. Mol. Cell 2003, 11:865-874.
44. 2+-dependent events in vitro and in situ. Biochemistry 1997, 36:970-978.
45. Bell M.G., Lankford E.B., Gonye G.E., Ellis-Davies G.C.R., Martyn D.A., Regnier M., et al. Kinetics of cardiac thin-filament activation probed by fluorescence polarization of rhodamine-labeled troponin C in skinned guinea pig trabeculae. Biophys. J. 2006, 90:531-543.
46. 2+- and cross-bridge-dependent changes in N- and C-terminal structure of troponin C in rat cardiac muscle. Biophys. J. 2001, 80:360-370.
47. Allingham J.S., Smith R., Rayment I. The structural basis of blebbistatin inhibition and specificity for myosin II. Nat. Struct. Mol. Biol. 2005, 12:378-379.
48. Kovacs M., Toth J., Hetenyi C., Malnasi-Csizmadia A., Sellers J.R. Mechanism of blebbistatin inhibition of myosin II. J. Biol. Chem. 2004, 279:35557-35563.
49. Bremel R.D., Weber A. Cooperation within the actin filament in vertebrate skeletal muscle. Nature New Biol. 1972, 238:97-101.
50. Fitzsimons D.P., Patel J.R., Moss R.L. Cross-bridge interaction kinetics in rat myocardium are accelerated by strong binding of myosin to the thin filament. J. Physiol. 2001, 530:263-272.
51. Brown J.H., Cohen C. Regulation of muscle contraction by tropomyosin and troponin: how structure illuminates function. Advances in Protein Chemistry 2005, 121-159. Academic Press.
52. Brady A.J. Active state in cardiac muscle. Physiol. Rev. 1968, 48:570-600.
53. Harris D.E., Work S.S., Wright R.K., Alpert N.R., Warshaw D.M. Smooth, cardiac and skeletal muscle myosin force and motion generation assessed by cross-bridge mechanical interactions in vitro. J. Muscle Res. Cell Motil. 1994, 15:11-19.
54. Alpert N.R., Brosseau C., Federico A., Krenz M., Robbins J., Warshaw D.M. Molecular mechanics of mouse cardiac myosin isoforms. Am. J. Physiol. 2002, 283:H1446-H1454.
55. Cooke R., Crowder M.S., Thomas D.D. Orientation of spin labels attached to cross-bridges in contracting muscle fibres. Nature 1982, 300:776-778.
56. Ostap E.M., Barnett V.A., Thomas D.D. Resolution of three structural states of spin-labeled myosin in contracting muscle. Biophys. J. 1995, 69:177-188.
57. Piazzesi G., Reconditi M., Linari M., Lucii L., Bianco P., Brunello E., et al. Skeletal muscle performance determined by modulation of number of myosin motors rather than motor force or stroke size. Cell 2007, 131:784-795.
58. Fabiato A. 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. 1981, 78:457-497.
59. Allen D.G., Kurihara S. The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. J. Physiol. 1982, 327:79-94.
60. Dobesh D.P., Konhilas J.P., de Tombe P.P. Cooperative activation in cardiac muscle: impact of sarcomere length. Am. J. Physiol. 2002, 282:H1055-H1062.
61. Konhilas J.P., Irving T.C., Wolska B.M., Jweied E.E., Martin A.F., Solaro R.J., et al. Troponin I in the murine myocardium: influence on length-dependent activation and interfilament spacing. J. Physiol. 2003, 547:951-961.
62. Adhikari B.B., Regnier M., Rivera A.J., Kreutziger K.L., Martyn D.A. Cardiac length dependence of force and force redevelopment kinetics with altered cross-bridge cycling. Biophys. J. 2004, 87:1784-1794.
63. Fukuda N., Kajiwara H., Ishiwata S.i., Kurihara S. Effects of MgADP on length dependence of tension generation in skinned rat cardiac muscle. Circ. Res. 2000, 86:e1-6.
64. 2+ activation and relaxation in rat and guinea pig skinned trabeculae. Circ. Res. 1998, 83:179-186.
65. Kentish J.C., McCloskey D.T., Layland J., Palmer S., Leiden J.M., Martin A.F., et al. Phosphorylation of troponin I by protein kinase A accelerates relaxation and crossbridge cycle kinetics in mouse ventricular muscle. Circ. Res. 2001, 88:1059-1065.
66. Haworth R.S., Cuello F., Herron T.J., Franzen G., Kentish J.C., Gautel M., et al. Protein kinase D is a novel mediator of cardiac troponin I phosphorylation and regulates myofilament function. Circ. Res. 2004, 95:1091-1099.
67. Stelzer J.E., Patel J.R., Moss R.L. Acceleration of stretch activation in murine myocardium due to phosphorylation of myosin regulatory light chain. J. Gen. Physiol. 2006, 128:261-272.
68. Fukuda N., O-Uchi J., Sasaki D., Kajiwara H., Ishiwata S.i., Kurihara S. Acidosis or inorganic phosphate enhances the length dependence of tension in rat skinned cardiac muscle. J. Physiol. 2001, 536:153-160.
69. 2+ activation in cardiac muscle. Biophys. J. 2007, 92:4379-4390.
70. Dou Y., Arlock P., Arner A. Blebbistatin specifically inhibits actin-myosin interaction in mouse cardiac muscle. Am. J. Physiol. 2007, 293:C1148-C1153.