Myofilament calcium sensitivity does not affect cross-bridge activation-relaxation kinetics

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 292, Issue 3, 2007, Pages

  De Tombe, Pieter P ^a   Belus, Alexandra ^b   Piroddi, Nicoletta ^b   Scellini, Beatrice ^b   Walker, John S ^a   Martin, Anne F ^a   Tesi, Chiara ^b   Poggesi, Corrado ^b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Contraction kinetics; Muscle mechanics; Regulation; Single myofibril; Troponin

Indexed keywords

BEPRIDIL; CALCIUM ION; TROPONIN I;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; MUSCLE FIBER CONTRACTION; MUSCLE FIBRIL; MYOFILAMENT; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RABBIT; SENSITIVITY ANALYSIS; SKELETAL MUSCLE;

ANIMALS; CALCIUM; CROSS-LINKING REAGENTS; KINETICS; MICROFILAMENTS; MUSCLE FIBERS, SLOW-TWITCH; MUSCLE RELAXATION; MUSCLE, SKELETAL; MYOCARDIUM; PROTEIN ISOFORMS; RABBITS; RECOMBINANT PROTEINS; TROPONIN I;

EID: 33847750735     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00630.2006     Document Type: Article

References (56)

1. Arteaga GM, Palmiter KA, Leiden JM, Solaro RJ. Attenuation of length dependence of calcium activation in myofilaments of transgenic mouse hearts expressing slow skeletal troponin I. J Physiol 526: 541-549, 2000.
2. 2+] in intact rat cardiac trabeculae. J Gen Physiol 105: 1-19, 1995.
3. 2+ regulates the kinetics of tension development in intact cardiac muscle. Am J Physiol Heart Circ Physiol 275: H744-H750, 1998.
4. Bartoo ML, Popov VI, Fearn LA, Pollack GH. Active tension generation in isolated skeletal myofibrils. J Muscle Res Cell Motil 14: 498-510, 1993.
5. Bers DM. Excitation-Contraction Coupling and Cardiac Contractile Force. Dordrecht, The Netherlands: Kluwer Academic, 2001.
6. Bhavsar PK, Dhoot GK, Cumming DV, Butler-Browne GS, Yacoub MH, Barton PJ. Developmental expression of troponin I isoforms in fetal human heart. FEBS Lett 292: 5-8, 1991.
7. 2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: implications for regulation of muscle contraction. Proc Natl Acad Sci USA 85: 3265-3269, 1988.
8. Brenner B, Kraft T, Yu LC, Chalovich JM. Thin-filament activation probed by fluorescence of N-{[2-(Iodoacetoxy)ethyl]-N-methyl} amino-7-nitrobenz-2-oxa-1, 3-diazole-labeled troponin I incorporated into skinned fibers of rabbit psoas muscle. Biophys J 77: 2677-2691, 1999.
9. Chandra M, Kim JJ, Solaro RJ. An improved method for exchanging troponin subunits in detergent skinned rat cardiac fiber bundles. Biochem Biophys Res Commun 263: 219-223, 1999.
10. Clemmens EW, Entezari M, Martyn DA, Regnier M. Different effects of cardiac versus skeletal muscle regulatory proteins on in vitro measures of actin filament speed and force. J Physiol 566: 737-746, 2005.
11. Day SM, Westfall MV, Fomicheva EV, Hoyer K, Yasuda S, La Cross NC, D'Alecy LG, Ingwall JS, Metzger JM. Histidine button engineered into cardiac troponin I protects the ischemic and failing heart. Nat Med 12: 181-189, 2006.
12. de Tombe PP. Cardiac myofilaments: mechanics and regulation. J Biomech 36: 721-730, 2003.
13. Fentzke RC, Buck SH, Patel JR, Lin H, Wolska BM, Stojanovic MO, Martin AF, Solaro RJ, Moss RL, Leiden JM. Impaired cardiomyocyte relaxation and diastolic function in transgenic mice expressing slow skeletal troponin I in the heart. J Physiol 517: 143-157, 1999.
14. Gibson LM, Wendt IR, Stephenson DG. Contractile activation properties of ventricular myocardium from hypothyroid, euthyroid and juvenile rats. Pflügers Arch 422: 16-23, 1992.
15. Gordon AM, Homsher E, Regnier M. Regulation of contraction in striated muscle. Physiol Rev 80: 853-924, 2000.
16. Hunkeler NM, Kullman J, Murphy AM. Troponin I isoform expression in human heart. Circ Res 69: 1409-1414, 1991.
17. Iwazumi T. High-speed ultrasensitive instrumentation for myofibril mechanics measurements. Am J Physiol Cell Physiol 252: C253-C262, 1987.
18. Johns EC, Simnett SJ, Mulligan IP, Ashley CC. Troponin I phosphorylation does not increase the rate of relaxation following laser flash photolysis of diazo-2 in guinea-pig skinned trabeculae. Pflügers Arch 433: 842-844, 1997.
19. Kentish JC, McCloskey DT, Layland J, Palmer S, Leiden JM, Martin AF, Solaro RJ. Phosphorylation of troponin I by protein kinase A accelerates relaxation and crossbridge cycle kinetics in mouse ventricular muscle. Circ Res 88: 1059-1065, 2001.
20. Konhilas JP, Irving TC, de Tombe PP. Length-dependent activation in three striated muscle types of the rat. J Physiol 544: 225-236, 2002.
21. Konhilas JP, Irving TC, Wolska BM, Jweied EE, Martin AF, Solaro RJ, de Tombe PP. Troponin I in the murine myocardium: influence on length-dependent activation and interfilament spacing. J Physiol 547: 951-961, 2003.
22. 2+ sensitivity due to titin and troponin-I isoform switching are not critically triggered by birth. Am J Physiol Heart Circ Physiol 291: H496-H506, 2006.
23. Li G, Martin AF, Solaro JR. Localization of regions of troponin I important in deactivation of cardiac myofilaments by acidic pH. J Mol Cell Cardiol 33: 1309-1320, 2001.
24. Li Y, Love ML, Putkey JA, Cohen C. Bepridil opens the regulatory N-terminal lobe of cardiac troponin C. Proc Natl Acad Sci USA 97: 5140-5145, 2000.
25. Linke WA, Bartoo ML, Pollack GH. Spontaneous sarcomeric oscillations at intermediate activation levels in single isolated cardiac myofibrils. Circ Res 73: 724-734, 1993.
26. Martin AF, Ball K, Gao LZ, Kumar P, Solaro RJ. Identification and functional significance of troponin I isoforms in neonatal rat heart myofibrils. Circ Res 69: 1244-1252, 1991.
27. Maytum R, Lehrer SS, Geeves MA. Cooperativity and switching within the three-state model of muscle regulation. Biochemistry 38: 1102-1110, 1999.
28. Metzger JM, Michele DE, Rust EM, Borton AR, Westfall MV. Sarcomere thin filament regulatory isoforms. Evidence of a dominant effect of slow skeletal troponin I on cardiac contraction. J Biol Chem 278: 13118 -13123, 2003.
29. Metzger JM, Moss RL. Calcium-sensitive cross-bridge transitions in mammalian fast and slow skeletal muscle fibers. Science 247: 1088-1090, 1990.
30. 2+ regulation in developing rabbit cardiac muscle. Biochem Biophys Res Commun 267: 912-917, 2000.
31. Morris CA, Tobacman LS, Homsher E. Thin filament activation and unloaded shortening velocity of rabbit skinned muscle fibres. J Physiol 550: 205-215, 2003.
32. Noguchi T, Camp P Jr, Alix SL, Gorga JA, Begin KJ, Leavitt BJ, Ittleman FP, Alpert NR, LeWinter MM, VanBuren P. Myosin from failing and non-failing human ventricles exhibit similar contractile properties. J Mol Cell Cardiol 35: 91-97, 2003.
33. Pagani ED, Shemi R, Julian FJ. Tension-pCa relations of saponin-skinned rabbit and human heart muscle. J Mol Cell Cardiol 18: 55-66, 1986.
34. Page E, Fozzard HA, Solaro RJ. Handbook of Physiology: The Heart. New York: Oxford University Press, 2002.
35. Palmiter KA, Tyska MJ, Dupuis DE, Alpert NR, Warshaw DM. Kinetic differences at the single molecule level account for the functional diversity of rabbit cardiac myosin isoforms. J Physiol 519: 669-678, 1999.
36. Piroddi N, Tesi C, Pellegrino MA, Tobacman LS, Homsher E, Poggesi C. Contractile effects of the exchange of cardiac troponin for fast skeletal troponin in rabbit psoas single myofibrils. J Physiol 552: 917-931, 2003.
37. Regnier M, Martin H, Barsotti RJ, Rivera AJ, Martyn DA, Clemmens E. Cross-bridge versus thin filament contributions to the level and rate of force development in cardiac muscle. Biophys J 87: 1815-1824, 2004.
38. Ross J, Sobel BE. Regulation of cardiac contraction. Annu Rev Physiol 34: 47-90, 1972.
39. Schiaffino S, Reggiani C. Molecular diversity of myofibrillar proteins: gene regulation and functional significance. Physiol Rev 76: 371-423, 1996.
40. 2+-sensitivity of regulated cardiac thin filament sliding does not depend on myosin isoform. J Physiol. 577: 935-944, 2006.
41. She M, Trimble D, Yu LC, Chalovich JM. Factors contributing to troponin exchange in myofibrils and in solution. J Muscle Res Cell Motil 21: 737-745, 2000.
42. Solaro RJ, Lee JA, Kentish JC, Allen DG. Effects of acidosis on ventricular muscle from adult and neonatal rats. Circ Res 63: 779-787, 1988.
43. Solaro RJ, Moir AJ, Perry SV. Phosphorylation of troponin I and the inotropic effect of adrenaline in the perfused rabbit heart. Nature 262: 615-617, 1976.
44. Solaro RJ, Moss RL. Molecular Control Mechanisms in Striated Muscle Contraction. Dordrecht, The Netherlands: Kluwer Academic, 2002.
45. Spurgeon HA, DuBell WH, Stern MD, Sollott SJ, Ziman BD, Silverman HS, Capogrossi MC, Talo A, Lakatta EG. Cytosolic calcium and myofilaments in single rat cardiac myocytes achieve a dynamic equilibrium during twitch relaxation. J Physiol 447: 83-102, 1992.
46. Spyracopoulos L, Gagne SM, Li MX, Sykes BD. Dynamics and thermodynamics of the regulatory domain of human cardiac troponin C in the apo- and calcium-saturated states. Biochemistry 37: 18032-18044, 1998.
47. Stehle R, Kruger M, Pfitzer G. Force kinetics and individual sarcomere dynamics in cardiac myofibrils after rapid ca(2+) changes. Biophys J 83: 2152-2161, 2002.
48. Stoutamyer A, Dhoot GK. Transient expression of fast troponin C transcripts in embryonic quail heart. J Muscle Res Cell Motil 26: 237-245, 2005.
49. Sumandea MP, Burkart EM, Kobayashi T, De Tombe PP, Solaro RJ. Molecular and integrated biology of thin filament protein phosphorylation in heart muscle. Ann NY Acad Sci 1015: 39-52, 2004.
50. Sumandea MP, Pyle WG, Kobayashi T, de Tombe PP, Solaro RJ. Identification of a functionally critical protein kinase C phosphorylation residue of cardiac troponin T. J Biol Chem 278: 35135-35144, 2003.
51. 2+ reduction in single myofibrils from skeletal muscle. Biophys J 83: 2142-2151, 2002.
52. Vassylyev DG, Takeda S, Wakatsuki S, Maeda K, Maeda Y. Crystal structure of troponin C in complex with troponin I fragment at 2.3 - a resolution. Proc Natl Acad Sci USA 95: 4847-4852, 1998.
53. 2+-activated myofilament tension in adult cardiac myocytes. Circ Res 86: 470-477, 2000.
54. Westfall MV, Rust EM, Metzger JM. Slow skeletal troponin I gene transfer, expression, and myofilament incorporation enhances adult cardiac myocyte contractile function. Proc Natl Acad Sci USA 94: 5444-5449, 1997.
55. Wolff MR, McDonald KS, Moss RL. Rate of tension development in cardiac muscle varies with level of activator calcium. Circ Res 76: 154-160, 1995.
56. Zhang R, Zhao J, Mandveno A, Potter JD. Cardiac troponin I phosphorylation increases the rate of cardiac muscle relaxation. Circ Res 76: 1028-1035, 1995.