Ca2+ and cross-bridge-induced changes in troponin C in skinned skeletal muscle fibers: Effects of force inhibition

Biophysical Journal

Volumn 76, Issue 3, 1999, Pages 1480-1493

  Freitag, C J ^a   Chase, P B ^b   Gordon, A M ^c  

^a University of Washington   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AZIRIDINE DERIVATIVE; CALCIUM; PYRROLE DERIVATIVE; TROPONIN C; FLUORESCENT DYE; MYOSIN ADENOSINE TRIPHOSPHATASE; RHODAMINE; TETRAMETHYLRHODAMINE IODOACETAMIDE; TROPONIN;

ANIMAL TISSUE; ARTICLE; LINEAR DICHROISM; MUSCLE FORCE; MUSCLE RIGIDITY; NONHUMAN; PROTEIN STRUCTURE; RABBIT; SARCOMERE LENGTH; SKELETAL MUSCLE; THIN FILAMENT; ANIMAL; BIOPHYSICS; CHEMISTRY; COMPARATIVE STUDY; DRUG EFFECT; IN VITRO STUDY; MUSCLE CELL; MUSCLE CONTRACTION; PHYSIOLOGY; PROTEIN BINDING; PSOAS MUSCLE; SPECTROSCOPY;

ANIMALIA; ORYCTOLAGUS CUNICULUS;

ACTOMYOSIN; ANIMALS; BIOPHYSICS; CALCIUM; FLUORESCENT DYES; MUSCLE CONTRACTION; MUSCLE FIBERS; PROTEIN BINDING; PSOAS MUSCLES; RABBITS; RHODAMINES; SPECTRUM ANALYSIS; TROPONIN;

EID: 0032589143     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/s0006-3495(99)77308-x     Document Type: Article

References (71)

1. Allen, T. S., N. Ling, M. Irving, and Y. E. Goldman. 1996. Orientation changes in myosin regulatory light chains following photorelease of ATP in skinned muscle fibers. Biophys. J. 70:1847-1862.
2. 2+ dependence of structural changes in troponin C in demembranated fibers of rabbit psoas muscle. Biophys. J. 61:399-409.
3. Bagni, M. A., G. Cecchi, F. Colomo, and C. Poggesi. 1990. Tension and stiffness of frog muscle fibres at full filament overlap. J. Muscle Res. Cell Motil. 11:371-377.
4. Brandt, P. W., M. S. Diamond, J. S. Rutchik, and F. H. Schachal. 1987. Co-operative interations between troponin-tropomyosin units extend the length of the thin filament in skeletal muscle. J. Mol. Biol. 195:885-896.
5. Brandt, P. W., D. Roemer, and F. H. Schachat. 1990. Co-operative activation of skeletal muscle thin filaments by rigor cross-bridges. The effect of troponin C extraction. J. Mol. Biol. 212:473-480.
6. Bremel, R. D., J. M. Murray, and A. Weber. 1972. Manifestations of cooperative behavior in the regulated actin filament during actin-activated ATP hydrolysis in the presence of calcium. Cold Spring Harb. Symp. Quant. Biol. 37:267-275.
7. Bremel, R. D., and A. Weber. 1972. Cooperation within actin filament in vertebrate skeletal muscle. Nature New Biol. 238:91-101.
8. Brenner, B. 1983. Technique for stabilizing the striation pattern in maximally calcium-activated skinned rabbit psoas fibers. Biophys. J. 41: 99-102.
9. Brenner, B., M. Schoenberg, J. M. Chalovich, L. E. Greene, and E. Eisenberg. 1982. Evidence for cross-bridge attachment in relaxed muscle at low ionic strength. Proc. Natl. Acad. Sci. USA. 79:7288-7291.
10. Brenner, B., and L. C. Yu. 1985. Equitorial x-ray diffraction from single skinned rabbit psoas fibers at various degrees of activation. Biophys. J. 48:829-834.
11. Cantino, M. E., T. S. Allen and A. M. Gordon. 1993. Subsarcomeric distribution of calcium in demembranated fibers of rabbit psoas muscle. Biophys. J. 64:211-222.
12. 2+ concentration during contraction and relaxation studied by the indicator fluo-3 in frog muscle fibres. J. Physiol. (Lond.). 478:137-148.
13. Chase, P. B., and M. J. Kushmerick. 1988. Effects of pH on contraction of rabbit fast and slow skeletal muscle fibers. Biophys. J. 53:935-946.
14. Chase, P. B., D. A. Martyn, and J. D. Hannon. 1994a. Activation dependence and kinetics of force and stiffness inhibition by aluminiofluoride, a slowly dissociating analogue of inorganic phosphate, in chemically skinned fibres from rabbit psoas muscle. J. Muscle Res. Cell Motil. 15:119-129.
15. 2+. Biophys. J. 67:1994-2001.
16. Corrie, J. E. T., and J. S. Craik. 1994. Synthesis and characterization of pure isomers of iodoacetamidotetramethylrhodamine. J. Chem. Soc. Perkin Trans. 1:2967-2963.
17. Daniel, T. L., A. C. Trimble, and P. B. Chase. 1998. Compliant realignment of binding sites in muscle: transient behavior and mechanical tuning. Biophys. J. 74:1611-1621.
18. Farah, C. S., and F. C. Reinach. 1995. The troponin complex and regulation of muscle contraction. FASEB. J. 9:755-767.
19. Ford, L. E., A. F. Huxley, and R. M. Simmons. 1981. The relation between stiffness and filament overlap in stimulated frog muscle fibres. J. Physiol. (Lond.). 311:219-249.
20. Fuchs, F. 1977. The binding of calcium to glycerinated muscle fibers in rigor. The effect of filament overlap. Biochim. Biophys. Acta. 491: 523-531.
21. Fuchs, F. 1985. The binding of calcium to detergent-extracted rabbit psoas muscle fibres during relaxation and force generation. J. Muscle Res. Cell Motil. 6:477-486.
22. 2+-troponin C affinity in skeletal muscle. Am. J. Phyisol. 253:C541-C546.
23. Geeves, M. A., and P. B. Conibear. 1995. The role of three-state docking of myosin S1 with actin in force generation. Biophys. J. 68:194S-201S.
24. Goldman, Y. E., M. G. Hibberd, and D. R. Trentham. 1984. Relaxation of rabbit psoas muscle fibres from rigor by photochemical generation of adenosine-5′-triphosphate. J. Physiol. (Lond.). 354:577-604.
25. Gordon, A. M., A. F. Huxley, and F. J. Julian. 1966. The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J. Physiol. (Lond.). 184:170-192.
26. Gordon, A. M., and E. B. Ridgway. 1987. Extra calcium on shortening in barnacle muscle. Is the decrease in calcium binding related to decreased cross-bridge attachment, force, or length? J. Gen. Physiol. 90:321-340.
27. Granzier, H. L. M., and K. Wang. 1993. Passive tension and stiffness of vertebrate skeletal and insect flight muscles: the contribution of weak cross-bridges and elastic filaments. Biophys. J. 65:2141-2159.
28. Greaser, M. L., and J. Gergley. 1971. Reconstitution of troponin from three protein components. J. Biol. Chem. 246:4226-4233.
29. 2+-specific regulatory sites in skinned rabbit psoas fibers. J. Biol. Chem. 262:13627-13635.
30. Hancock, W. O., L. L. Huntsman, and A. M. Gordon. 1997. Models of calcium activation account for differences between skeletal and cardiac force redevelopment kinetics. J. Muscle Res. Cell Motil. 18:671-681.
31. Hannon, J. D., D. A. Martyn, and A. M. Gordon. 1992. Effects of cycling and rigor cross-bridges on the conformation of cardiac troponin C. Circ. Res. 71:984-991.
32. Heeley, D. H., K. Golosinska, and L. B. Smillie. 1987. The effects of troponin T fragments T1 and T2 on the binding of nonpolymerizable tropomyosin to F-actin in the presence and absence of troponin I and troponin C. J. Biol. Chem. 262:9971-9978.
33. Herzberg, O., and M. N. G. James. 1988. Refined crystal structure of troponin C from turkey skeletal muscle at 2.0 Å resolution. J. Mol. Biol. 203:761-779.
34. Hill, L. E., J. P. Mehegan, C. A. Butters, and L. S. Tobacman. 1992. Analysis of troponin-tropomyosin binding to actin. Troponin does not promote interactions between tropomyosin molecules. J. Biol. Chem. 267:16106-16113.
35. Holmes, K. C. 1995. The actomyosin interaction and its control by tropomyosin. Biophys. J. 68:2S-5S.
36. Howard, J. 1997. Molecular motors: structural adaptations to cellular functions. Nature. 389:561-567.
37. Ishii, Y., and S. S. Lehrer. 1990. Eximer fluorescence of pyrenyliodoacetamide-labeled tropomyosin: a probe of the state of tropomyosin in reconstituted muscle thin filaments. Biochem. J. 29:1160-1166.
38. Johnson, J. D., J. H. Collins, and J. D. Potter. 1978. Dansylaziridine-labeled troponin C. J. Biol. Chem. 253:6451-6458.
39. Kawai, M., J. S. Wray, and Y. Zhao. 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. 64:187-196.
40. Kress, M., H. E. Huxley, and A. R. Faruqui. 1986. Structural changes during activation of frog muscle studied by time-resolved x-ray diffraction. J. Mol. Biol. 188:325-342.
41. Lancet, D., and I. Pecht. 1977. Spectroscopic and immunochemical studies with nitrobenzoxadiazolealanine, a fluorescent dinotrophenyl analogue. Biochemistry: 16:5150-5157.
42. 2+-induced tropomyosin movement in Limulus thin filaments revealed by three-dimensional reconstruction. Nature. 368:65-67.
43. 2+ or myosin heads? J. Muscle Res. Cell Motil. 15:232-236.
44. Li, H.-C., and P. G. Fajer. 1994. Orientational changes of troponin C associated with thin filament activation. Biochem. J. 33:14324-14332.
45. Linari, M., I. Dobbie, M. Reconditi, N. Koubassova, M. Irving, G. Piazzesi, and V. Lombardi. 1998. The stiffness of skeletal muscle in isometric contraction and rigor: the fraction of heads bound to actin. Biophys. J. 74:2459-2473.
46. 2- and COOH-terminal domains of troponin T. J. Biol. Chem. 273: 10594-10601.
47. 2+ activation of skinned psoas fibers from rabbit. Biophys. J. 68:235-242.
48. Martyn, D. A., and A. M. Gordon. 1988. Length and myofilament spacing-dependent changes in calcium sensitivity of skeletal fibres: effects of pH and ionic strength. J. Muscle Res. Cell Motil. 9:428-445.
49. Matsubara, I., Y. Umazume, and N. Yagi. 1985. Lateral filamentary spacing in chemically skinned murine muscles during contraction. J. Physiol. (Lond.). 360:135-148.
50. McKillop, D. F. A., N. S. Fortune, K. W. Ranatunga and M. A. Geeves. 1994. The influence of 2,3-butanedione 2-monoxime (BDM) on the interaction between actin and myosin in solution and in skinned muscle fibres. J. Muscle Res. Cell Motil. 15:309-318.
51. McKillop, D. F. A., and M. A. Geeves. 1993. Regulation of the interaction between actin and myosin subfragment I: evidence for three states of the thin filament. Biophys. J. 65:693-701.
52. Morano, I., and J. C. Ruegg. 1991. What does TnCDANZ fluorescence reveal about the thin filament state? Pflugers Arch. 418:333-337.
53. 2+ regulation of mechanical properties of striated muscle. Mechanistic studies using extraction and replacement of regulatory proteins. Circ. Res. 70:865-884.
54. Moss, R. L., G. G. Giulian, and M. L. Greaser. 1985. The effects of partial extraction of TnC upon the tension-pCa relationship in rabbit skinned skeletal muscle fibers. J. Gen. Physiol. 86:585-600.
55. Pearlstone, J. R., and L. S. Smillie. 1983. Effects of troponin-I plus troponin-C on the binding of troponin-T and its fragments to a-tropomyosin. J. Biol. Chem. 258:2534-2542.
56. Phan, B. C. and E. Reisler. 1993. Aluminum fluoride infractions with troponin C. Biophys. J. 65:2511-2516.
57. 2+ regulation of tension redevelopment rate in skinned skeletal muscle. Biophys. J. 71:2786-2794.
58. Regnier, M., C. Morris, and E. Homsher. 1995. Regulation of the cross-bridge transition from a weakly to strongly bound state in skinned rabbit muscle fibers. Am. J. Physiol. 269:C1532-C1539.
59. Suzuki, S., and H. Sugi. 1983. Extensibility of the myofilaments in vertebrate skeletal muscle as revealed by stretching rigor muscle fibers. J. Gen. Physiol. 81:531-546.
60. Swartz, D. R., and R. L. Moss. 1992. Influence of a strong-binding myosin analogue on calcium-sensitive mechanical properties of skinned skeletal muscle fibers. J. Biol. Chem. 267:20497-20506.
61. Swartz, D. R., R. L. Moss, and M. L. Greaser. 1996. Calcium alone does not fully activate the thin filament for S1 binding to rigor myofibrills. Biophys. J. 71:1891-1904.
62. Swartz, D. R., R. L. Moss, and M. L. Greaser. 1997. Characteristics of troponin C binding to the myofibrillar thin filament: extraction of troponin C is not random along the length of the thin filament. Biophys. J. 73:293-305.
63. Tanner, J. W., D. D. Thomas, and Y. E. Goldman. 1992. Transients in orientation of a fluorescent cross-bridge probe following photolysis of caged nucleotides in skeletal muscle fibres. J. Mol. Biol. 223:185-203.
64. Tobacman, L. S. 1996. Thin filament-mediated regulation of cardiac contraction. Annu. Rev. Physiol. 58:447-481.
65. 2+] in intact frog skeletal muscle fibres. J. Physiol. (Lond.). 511.1:171-180.
66. Vibert, P., R. Craig, and W. Lehman. 1997. Steric model for activation of muscle thin filaments. J. Mol. Biol. 266:8-14.
67. Wang, Y. P., and F. Fuchs. 1994. Length, force, and Ca(2+)-troponin C affinity in cardiac and slow skeletal muscle. Am. J. Physiol. 266: C1077-C1082.
68. Yamamoto, T., and J. W. Herzig. 1978. Series elastic properties of skinned muscle fibres in contraction and rigor. Pflugers Arch. 373:21-24.
69. Yates, L. D., R. L. Coby, Z. Luo, and A. M. Gordon. 1993. Filament overlap affects TnC extraction from skinned muscle fibres. J. Muscle Res. Cell Motil. 14:392-400.
70. Yates, L. D., and M. L. Greaser. 1983. Troponin subunit stoichiometry and content in rabbit skeletal muscle and myofibrils. J. Biol. Chem. 258: 5770-5774.
71. Zot, H. G., and J. D. Potter. 1987. Calcium binding and fluorescence measurements of dansylaziridine-labelled troponin C in reconstituted thin filaments. J. Muscle Res. Cell Molil. 8:428-436.