Cooperative effects of rigor and cycling cross-bridges on calcium binding to troponin C

Biophysical Journal

Volumn 92, Issue 2, 2007, Pages 525-534

  Cantino, Marie E ^a,b   Quintanilla, Abraham ^a,b  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b Amgen Manufacturing Limited   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE MAGNESIUM; CALCIUM; TROPONIN C;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM BINDING; CONTROLLED STUDY; MUSCLE CELL; NONHUMAN; RIGOR; SARCOMERE LENGTH; X RAY MICROANALYSIS;

ORYCTOLAGUS CUNICULUS;

EID: 33846446434     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.093757     Document Type: Article

References (59)

1. Haselgrove, J. C. 1972. X-ray evidence for a conformational change in the actin containing filaments of vertebrate striated muscle. Cold Spring Harb. Symp. Quant. Biol. 37:341-352.
2. Parry, D. A., and J. M. Squire. 1973. The structural role of tropomyosin in muscle regulation: analysis of the x-ray diffraction patterns from relaxed and contracting muscles. J. Mol. Biol. 75:33-55.
3. McKillop, D. F. A., and M. A. Geeves. 1993. Regulation of the interaction between actin and myosin subfragment 1: evidence for three states of the thin filament. Biophys. J. 65:693-701.
4. Gordon, A. M., E. Homsher, and M. Regnier. 2000. Regulation of contraction in striated muscle. Physiol. Rev. 80:853-924.
5. Lehrer, S. S., and M. A. Geeves. 1998. The muscle thin filament as a classical cooperative/allosteric regulatory system. J. Mol. Biol. 277:1081-1089.
6. Squire, J. M., and E. P. Morris. 1998. A new look at thin filament regulation in vertebrate skeletal muscle. FASEB J. 12:761-771.
7. Tobacman, L. S. 1996. Thin filament-mediated regulation of cardiac contraction. Annu. Rev. Physiol. 58:447-481.
8. Pirani, A., M. V. Vinogradova, P. M. G. Curmi, W. A. King, R. J. Fletterick, R. Craig, L. S. Tobacman, C. Xu, V. Hatch, and W. Lehman. 2006. An atomic model of the thin filament in the relaxed and Ca2+-activated states. J. Mol. Biol. 357:707-717.
9. Lehman, W., P. Vilbert, P. Uman, and R. Craig. 1995. Steric blocking by tropomyosin visualized in relaxed vertebrate thin filaments. J. Mol. Biol. 251:191-196.
10. Bremel, R. D., and A. Weber. 1972. Cooperation within actin filament in vertebrate skeletal muscle. Nature. 238:97-101.
11. 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.
12. Fuchs, F. 1977. The binding of calcium to glycerinated muscle fibers in rigor, the effect of filament overlap. Biochim. Biophys. Acta. 491:523-531.
13. Fuchs, F. 1977. Cooperative interactions between calcium-binding sites on glycerinated muscle fibers. The influence of cross-bridge attachment. Biochim. Biophys. Acta. 462:314-322.
14. Fuchs, F. 1978. On the relation between filament overlap and the number of calcium binding sites on glycerinated muscle fibers. Biophys. J. 21:273-276.
15. Hofmann, P. A., and F. Fuchs. 1987. Effect of length and cross-bridge attachment on Ca2+ binding to cardiac troponin C. Am. J. Physiol. 253:C90-C96.
16. Pan, B.-S., and J. R. Solaro. 1987. Calcium-binding properties of troponin C in detergent-skinned heart muscle fibers. J. Biol. Chem. 262:7839-7849.
17. Martyn, D. A., C. J. Freitag, P. B. Chase, and A. M. Gordon. 1999. Ca2+ and crossbridge-induced changes in troponin C in skinned skeletal muscle fibers: effects of force inhibition. Biophys. J. 76:1480-1493.
18. Hofmann, P. A., and F. Fuchs. 1988. Bound calcium and force development in skinned cardiac muscle bundles: effect of sarcomere length. J. Mol. Cell. Cardiol. 20:667-677.
19. Hofmann, P. A., and F. Fuchs. 1987. Evidence for a force-dependent component of calcium binding to cardiac troponin C. Am. J. Physiol. 253:C541-C546.
20. Fuchs, F. 1985. The binding of calcium to detergent-extracted rabbit psoas muscle fibers during relaxation and force generation. J. Muscle Res. Cell Motil. 6:477-486.
21. Fuchs, F., and Y.-P. Wang. 1991. Force, length, and Ca2+-troponin C affinity in skeletal muscle. Am. J. Physiol. 261:C787-C792.
22. 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.
23. Guth, K., and J. D. Potter. 1987. Effect of rigor and cycling cross-bridges of the structure of Troponin C and on the Ca2+ affinity of the Ca2+-specific regulatory sites in skinned rabbit psoas fibers. J. Biol. Chem. 262:13627-13635.
24. Allen, T. S., L. D. Yates, and A. M. Gordon. 1992. Ca2+-dependence of structural changes in troponin-C in demembranated fibers of rabbit psoas muscle. Biophys. J. 61:399-409.
25. Morano, I., and J. C. Ruegg. 1991. What does TnCDANZ fluorescence reveal about the thin filament state? Pflugers Arch. 418:333-337.
26. Martyn, D. A., and A. M. Gordon. 2001. Influence of length on force and activation-dependent changes in troponin C structure in skinned cardiac and fast skeletal muscle. Biophys. J. 80:2798-2808.
27. Martyn, D. A., M. Regnier, D. Xu, and A. M. Gordon. 2001. Ca2+- and cross-bridge-dependent changes in N- and C-terminal structure of troponin C in rat cardiac muscle. Biophys. J. 80:360-370.
28. Patel, J. R., K. S. McDonald, M. R. Wolff, and R. L. Moss. 1997. Ca2+ binding to troponin C in skinned skeletal muscle fibers assessed with caged Ca2+ and a Ca2+ fluorophore. Invariance of Ca2+ binding as a function of sarcomere length. J. Biol. Chem. 272:6018-6027.
29. Gordon, A., and E. 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.
30. Caputo, C., K. A. Edman, F. Lou, and Y. Sun. 1994. Variation in myoplasmic Ca2+ concentration during contraction and relaxation studied by the indicator fluo-3 in frog muscle fibres. J. Physiol. 478:137-148.
31. Wang, Y., and W. G. L. Kerrick. 2002. The off rate of Ca2+ from troponin C is regulated by force-generating cross-bridges in skeletal muscle. J. Appl. Physiol. 92:2409-2418.
32. Swartz, D. R., M. L. Greaser, and B. B. Marsh. 1990. Regulation of binding of subfragment 1 in isolated rigor myofibrils. J. Cell Biol. 111:2989-3001.
33. Maytum, R., S. S. Lehrer, and M. A. Geeves. 1999. Cooperativity and switching within the three-state model of muscle regulation. Biochemistry. 38:1102-1110.
34. Regnier, M., A. J. Rivera, C.-K. Wang, M. A. Bates, P. B. Chase, and A. M. Gordon. 2002. Thin filament near-neighbour regulatory unit interactions affect rabbit skeletal muscle steady-state force-Ca2+ relations. J. Physiol. 540:485-497.
35. Gong, H., V. Hatch, L. Ali, W. Lehman, R. Craig, and L. S. Tobacman. 2005. Mini-thin filaments regulated by troponin-tropomyosin. Proc. Natl. Acad. Sci. USA. 102:656-661.
36. Winegrad, S. 1965. The location of muscle calcium with respect to the myofibrils. J. Gen. Physiol. 48:997-1002.
37. Kitazawa, T., H. Shuman, and A. P. Somlyo. 1982. Calcium and magnesium binding to thin and thick filaments in skinned muscle fibers: electron probe analysis. J. Muscle Res. Cell Motil. 3:437-454.
38. 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.
39. Cantino, M. E., J. G. Eichen, and S. B. Daniels. 1998. Distributions of calcium in A and I bands of skinned vertebrate muscle fibers stretched to beyond filament overlap. Biophys. J. 75:948-956.
40. Cantino, M. E., and J. G. Eichen. 1998. Determination of myofilament calcium distributions from electron probe x-ray microanalysis images. Microsc. Microanal. 4:133-140.
41. Chiu, Y., J. Asayama, and L. E. Ford. 1982. A sensitive photoelectric force transducer with a resonant frequency of 6 kHz. Am. J. Physiol. 243:C299-C302.
42. Hellam, D. C., and R. J. Podolsky. 1969. Force measurements in skinned muscle fibers. J. Physiol. 200:807-819.
43. Fabiato, A. 1988. Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol. 157:378-413.
44. Laemmli, U. K. 1970. Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature. 227:680-685.
45. Hall, T. A., and B. L. Gupta. 1982. Quantification for the x-ray microanalysis of cryosections. J. Microsc. 126:333-354.
46. Shuman, H., A. V. Somlyo, and A. P. Somlyo. 1976. Quantitative electron probe microanalysis of biological thin sections: methods and validity. Ultramicroscopy. 1:317-339.
47. Trombitas, K., M. Greaser, S. Labeit, J.-P. Jin, M. Kellermayer, M. Helmes, and H. Granzier. 1998. Titin extensibility in situ: entropic elasticity of permanently folded and permanently unfolded molecular segments. J. Cell Biol. 140:853-859.
48. Fuchs, F., and B. Black. 1980. The effect of magnesium ions on the binding of calcium ions to glycerinated rabbit psoas muscle fibers. Biochim. Biophys. Acta. 622:52-62.
49. Vandenboom, R., D. R. Claflin, and F. J. Julian. 1998. Effects of rapid shortening on rate of force regeneration and myoplasmic [Ca2+] in intact frog skeletal muscle fibres. J. Physiol. 511:171-180.
50. Moreno-Gonzalez, A., J. Fredlund, and M. Regnier. 2005. Cardiac troponin C (TnC) and a site I skeletal TnC mutant alter Ca2+ versus crossbridge contribution to force in rabbit skeletal fibres. J. Physiol. 562:873-884.
51. Huxley, H. E., A. Stewart, H. Sosa, and T. Irving. 1994. X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle. Biophys. J. 67:2411-2421.
52. Wakabayashi, K., Y. Sugimoto, H. Tanaka, Y. Ueno, Y. Takezawa, and Y. Amemiya. 1994. X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys. J. 67:2422-2435.
53. Tsaturyan, A. K., N. Koubassova, M. A. Ferenczi, T. Narayanan, M. Roessle, and S. Y. Bershitsky. 2005. Strong binding of myosin heads stretches and twists the actin helix. Biophys. J. 88:1902-1910.
54. Cantino, M. E., and A. Quintanilla. 2002. BDM reduces enhancement of calcium bound in the overlap region of rabbit psoas muscle fibers. Biophys. J. 82:378a. (Abstr.).
55. Zot, H. G., and J. D. Potter. 1982. A structural role for the Ca2+-Mg2+ sites on troponin C in the regulation of muscle contraction. J. Biol. Chem. 257:7678-7683.
56. Finley, N. L., J. W. Howarth, and P. R. Rosevear. 2004. Structure of the Mg 2+-loaded C-lobe of cardiac troponin C bound to the N-domain of cardiac troponin I: comparison with the Ca 2+-loaded structure. Biochemistry. 43:11371-11379.
57. Burkart, E. M., G. M. Arteaga, M. P. Sumandea, R. Prabhakar, D. F. Wieczorek, and R. J. Solaro. 2003. Altered signaling surrounding the C-lobe of cardiac troponin C in myofilaments containing an [alpha]-tropomyosin mutation linked to familial hypertrophic cardiomyopathy. J. Mol. Cell. Cardiol. 35:1285-1293.
58. Tatsumi, R., K. Maeda, A. Hattori, and K. Takahashi. 2001. Calcium binding to an elastic portion of connectin/titin filaments. J. Muscle Res. Cell Motil. 22:149-162.
59. Labeit, D., K. Watanabe, C. Witt, H. Fujita, Y. Wu, S. Lahmers, T. Funck, S. Labeit, and H. Granzier. 2003. Calcium-dependent molecular spring elements in the giant protein titin. Proc. Natl. Acad. Sci. USA. 100:13716-13721.