Effects of cardiac thin filament Ca2+: Statistical mechanical analysis of a troponin C site II mutant

Biophysical Journal

Volumn 70, Issue 3, 1996, Pages 1447-1455

  Huynh, Quang ^a   Butters, Carol A ^a   Leiden, Jeffrey M ^c   Tobacman, Larry S ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE TRIPHOSPHATASE (MAGNESIUM); CALCIUM ION; MAGNESIUM; MYOSIN; TROPOMYOSIN; TROPONIN C;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING COMPETITION; BINDING SITE; CATTLE; HEART; MOUSE; MUSCLE; MUTANT; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; RABBIT; STATISTICAL MODEL;

ACTINS; ANIMALS; BINDING SITES; BINDING, COMPETITIVE; BIOPHYSICS; CALCIUM; CATTLE; MACROMOLECULAR SUBSTANCES; MICE; MYOCARDIUM; POINT MUTATION; PROTEIN BINDING; TROPOMYOSIN; TROPONIN; TROPONIN C;

ANIMALIA; BOS TAURUS; ORYCTOLAGUS CUNICULUS;

EID: 0030033871     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(96)79704-7     Document Type: Article

References (70)

1. Ackers, G. K., M. L. Doyle, D. Myers, and M. A. Daugherty. 1992. Molecular code for cooperativity in hemoglobin. Science. 255:54-63.
2. Babu, A, S. P Scordilis, E. H. Sonnenblick, and J Gulati. 1987. The control of myocardial contraction with skeletal fast muscle troponin C. J Biol Chem. 262:5815-5822.
3. 2+ coordination, by genetic engineering. J. Biol. Chem. 267:15469-15474.
4. Brandt, P. W., M. S Diamond, J. S. Rutchik, and F. H. Schachat. 1987. Cooperative interactions between troponin-tropomyosin units that extend the length of the thin filament in skeletal muscle. J. Mol Biol. 195:885-896.
5. Brito, R. M., J. A. Putkey, N. C. J. Strynadka, M. N. G. James, and P. R. Rosevear. 1991. Comparative NMR studies on cardiac troponin C and a mutant incapable of binding calcium at site II. Biochemistry. 30: 10236-10245.
6. Butters, C. A.. K. A. Willadsen, and L. S. Tobacman. 1993. Cooperative interactions between adjacent troponin-tropomyosin complexes may be transmitted through the thin filament. J. Biol. Chem. 268:15565-15570.
7. Cassell, M , and L. S. Tobacman. 1995. Opposite effects of myosin subfragment 1 on binding of troponin and tropomyosin to actin. Biophys. J. 68.A167.
8. Chalovich, J. M. 1992. Actin mediated regulation of muscle contraction. Pharmacol. Ther. 55:95-148.
9. Chalovich, J. M , and E. Eisenberg. 1982. Inhibition of actomyosin ATPase activity by troponin-tropomyosin without blocking the binding of myosin to actin. J. Biol. Chem. 257:2432-2437.
10. Dahiya, R., C. A. Butters, and L. S. Tobacman. 1994. Equilibrium linkage analysis of cardiac thin filament assembly. Implications for the regulation of muscle contraction. J. Biol. Chem. 269:29457-29461.
11. 2+ binding activity in mutated EF-hands of cardiac troponin C. J. Biol. Chem. 268:24067-24073.
12. Fabiato, A., and F. Fabiato. 1978. Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiac and skeletal muscles. J. Physiol. (Lond) 276:233-255.
13. 2+ sensitivity of thin filament assembly. J. Biol. Chem. 270:25455-25460.
14. Greene, L. E. 1982. The effect of nucleotide on the binding of myosin subfragment 1 to regulated actin. J. Biol. Chem. 257:13993-13999
15. Greene, L. E. 1986. Cooperative binding of myosin subfragment one to regulated actin as measured by fluorescence changes of troponin I modified with different fluorophores. J. Biol. Chem. 261:1279-1285.
16. 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.
17. Head, J. G., M. D. Ritchie, and M. A. Geeves. 1995. Characterization of the blocked and closed states of muscle thin filaments. Eur. J. Biochem. 227:694-699.
18. 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.
19. Hill, T. L., E. Eisenberg, and L. E. Greene. 1980. Theoretical model for cooperative equilibrium binding of myosin subfragment-1 to the actintroponin-tropomyosin complex. Proc. Natl. Acad. Sci. USA. 77: 3186-3190.
20. Hitchcock, S. E., H. E. Huxley, and A. G. Szent-Gyorgyi. 1973. Calcium sensitive binding of troponin to actin-tropomyosin: a two-site model for troponin action. J. Mol. Biol. 80:825-836.
21. Holmes, K. C., D Popp, W. Gebhard, and W. Kabsch. 1990. Atomic model of the actin filament. Nature. 347:44-49.
22. Holroyde, M. J., S. P. Robertson, J. D. Johnson, R. J. Solaro, and J. D Potter. 1980. The calcium and magnesium binding sites on cardiac troponin and their role in the regulation of myofibrillar adenosine triphosphatase. J. Biol. Chem. 255:11688-11693.
23. Huxley, H. E 1972. Structural changes in the actin and myosin containing filaments during contraction. Cold Spring Harb. Symp. Quant. Biol 37.361-376.
24. Ishii, Y., and S. S. Lehrer. 1990. Excimer fluorescence of pyrenyliodoacetamide-labeled tropomyosin: a probe of the state of tropomyosin in reconstituted muscle thin filaments. Biochemistry. 29:1160-1166.
25. Ishii, Y., and S. S. Lehrer. 1991. Two-site attachment of troponin to pyrene-labeled tropomyosin. J. Biol. Chem. 266.6894-6903.
26. Karpinski, B. A., L.-H. Yang, P. Cacheris, G. D. Morle, and J. M. Leiden. 1989. The first intron of the 4F2 heavy chain gene contains a transcriptional enhancer element that binds multiple nuclear proteins. Mol. Cell Biol. 9:2588-2597.
27. Kentish, J. C., H. ter Keurs, L. Riccardi, J. Bucx, and M. Noble. 1986. Comparison between the sarcomere length-force relations of intact and skinned trabeculae from rat right ventricle. Circ. Res. 58:755-768.
28. Kress, M., H. E. Huxley, A. R. Faruqi, and J. Hendrix. 1986. Structural changes during activation of frog muscle studied by time-resolved x-ray diffraction. J. Mol. Biol. 188:325-342.
29. Leavis, P. C., and J. Gergely. 1984. Thin filament proteins and thin filament-linked regulation of vertebrate muscle contraction. CRC Crit. Rev. Biochem. 16:235-305.
30. 2+-induced tropomyosin movement in Limulus thin filaments revealed by three-dimensional reconstruction. Nature. 368:65-67.
31. Lin, X., G A. Krudy, J. Howarth, P. R. Rosevear, and J. A. Putkey. 1994. Assignment and calcium dependence of methionyl epsilon C and epsilon H resonances in cardiac troponin C. Biochemistry. 33:14434-14442.
32. Lorenz, M., K. J. V. Poole, D. Popp, G. Rosenbaum, and K. C. Holmes. 1995. An atomic model of the unregulated thin filament obtained by x-ray fiber diffraction on oriented actin-tropomyosin gels. J. Mol. Biol. 246:108-119.
33. Lorenz, M., D. Popp, and K. C. Holmes. 1993. Refinement of the F-actin model against x-ray fiber diffraction data by the use of a directed mutation algorithm. J. Mol. Biol. 234:826-836.
34. Mak, A. S., and L. B. Smillie. 1981. Structural interpretation of the two-site binding of troponin on the muscle thin filament. J. Mol. Biol. 149: 541-550.
35. Margossian, S. S., and C. Cohen 1973 Troponin subunit interactions. J. Mol. Biol. 81:409-413.
36. McKillop, D. F. A., and M. A. Geeves. 1993. Regulation of the interaction between actin and myosin subfrasment 1: evidence for three states of the thin filament. Biophys. J. 65:693-701.
37. Mehegan, J. P., and L. S. Tobacman. 1991. Cooperative interactions between troponin molecules bound to the cardiac thin filament. J. Biol. Chem. 266:966-972.
38. Metzger, J. M., M. S. Parmacek, E. Barr, K Pasyk. W. Lin, K. L. Cochrane, L. J. Field, and J. M. Leiden. 1993. Skeletal troponin C reduces contractile sensitivity to acidosis in cardiac myocytes from transgenic mice. Proc. Natl. Acad. Sci. USA. 90:9036-9040.
39. Moss, R. L., J D. Allen, and M. L. Greaser. 1986. Effects of partial extraction of troponin complex upon the tension-pCa relation in rabbit skeletal muscle. Further evidence that tension development involves cooperative effects within the thin filament. J. Gen. Physiol. 87: 761-774.
40. Negele, J. C., D. G. Dotson, W. Liu, H. L. Sweeney, and J. A. Putkey. 1992. Mutation of the high affinity calcium binding sites in cardiac troponin C. J. Biol. Chem. 267:825-831.
41. Pan, B.-S., A. M Gordon, and Z. Luo. 1989. Removal of tropomyosin overlap modifies cooperative binding of myosin S-1 to reconstituted thin filaments of rabbit striated muscle. J. Biol. Chem. 264-8495-8498.
42. Pan. B.-S., and R. J. Solaro. 1987. Calcium-binding properties of troponin C in detergent-skinned heart muscle fibers. J. Biol. Chem. 262:7839-7849.
43. Parmacek, M. S., and Leiden, J. M 1989. Structure and expression of the murine slow/cardiac troponin C gene. J. Biol. Chem. 264:13217-13225.
44. Parry, D. A. D., and J. M Squire. 1973. 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.
45. 2- sensitivity and cooperativity. J. Biol. Chem. 258:2534-2542.
46. Pollard, T. D., and E. D. Korn 1973. Acanthamoeba myosin. Isolation from Acanthamoeba castellani of an enzyme similar to muscle myosin J. Biol. Chem 248:4682-4690.
47. Poole, K. J. V., G. Evans, G. Rosenbaum, M. Lorenz, and K. C. Holmes, 1995. The effect of crossbridges on the calcium sensitivity of the structural change of the regulated thin filament. Biophys. J. 68:A365.
48. Potter, J. D., and J. Gergely. 1974. Troponin, tropomyosin, and actin interactions in the Ca2+ regulation of muscle contraction. Biochemistry. 13:2697-2703.
49. Potter, J. D., and J. Gergely. 1975. The calcium and magnesium binding sites on troponin and their role in the regulation of myofibrillar adenosine triphosphatase. J. Biol. Chem. 250:4628-4633.
50. Putkey, J. A., H. L. Sweeney, and S. T. Campbell. 1989. Site-directed mutation of the trigger calcium-binding sites in cardiac troponin C. J. Biol Chem. 264:12370-12378.
51. Sanger, F., S. Nikben, and A. R. Coulsen. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA. 74:5463-5467.
52. 2+-specific sites of skeletal muscle TnC are required for full activity. J. Biol. Chem. 265:21554-21560.
53. Spudich, J. A., and S. Watt. 1971. The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosintroponin complex with actin and the proteolytic fragments of myosin. J. Biol. Chem. 246:4866-4871.
54. Studier, F. W., A. H. Rosenberg, J. J. Dunn, and J. W. Dubendorff. 1990. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185:60-89
55. 2+-sensitive force in permeabilized myocardium and skeletal muscle. J. Gen. Physiol. 96:1221-1245.
56. Syska, H., J. M. Wilkinson, R. J. A. Grand, and S. V. Perry. 1976. The relationship between biological activity and primary structure of troponin I from white skeletal muscle of the rabbit. Biochem. J. 153:375-387.
57. Talbot, J. A., and R. S. Hodges. 1981. Comparative studies on the inhibitory region of selected species of troponin-I. The use of synthetic peptide analogs to probe structure-function relationships. J. Biol. Chem. 256:12374-12378.
58. 2+ shows cooperativity intrinsic to the thin filament. Biochemistry. 26:492-497.
59. Tobacman, L. S. 1988. Structure-function studies of the amino-terminal region of bovine cardiac troponin T. J. Biol. Chem. 263:2668-2672.
60. Tobacman, L. S. 1996. Thin filament mediated regulation of cardiac contraction. Annu. Rev. Physiol. 58:447-481.
61. Tobacman, L. S., and R. S. Adelstein. 1986. Mechanism of regulation of cardiac actin-myosin subfragment 1 by troponin-tropomyosin. Biochemistry. 25:798-802
62. Tobacman, L. S., and R. Lee. 1987. Isolation and functional comparison of bovine cardiac troponin T isoforms. J. Biol. Chem. 262:4059-4064.
63. Tobacman, L. S . and D. Sawyer 1990. Calcium binds cooperatively to the regulatory sites of the cardiac thin filament. J. Biol. Chem. 265:931-939.
64. van Eerd, J.-P., and K. Takahashi. 1975. The amino acid sequence of bovine cardiac troponin C Comparison with rabbit skeletal troponin C. Biochem. Biophys. Res. Commun. 64.122-127.
65. Van Eyk, J. E., C. M. Kay, and R. S. Hodges. 1991. A comparative study of the interactions of synthetic peptides of the skeletal and cardiac troponin I inhibitory region with skeletal and cardiac troponin C. Biochemistry 30:9974-9981.
66. Weeds, A. G., and R. S. Taylor. 1975. Separation of subfragment-1 isoenzymes from rabbit skeletal muscle myosin. Nature. 257:54-56.
67. Wegner, A., and T. P. Walsh. 1981. Interaction of tropomyosin-troponin with actin filaments. Biochemistry. 20:5633-5642.
68. Willadsen, K. A., C. A. Butters, L. E. Hill, and L S. Tobacman. 1992. Effects of the amino-terminal regions of tropomyosin and troponin T on thin filament assembly. J. Biol. Chem. 267:23746-23752.
69. Williams, D. L., L. E. Greene, and E. Eisenberg. 1988. Cooperative turning on of myosin subfragment 1 adenosine triphosphatase activity by the troponin-tropomyosin-actin complex. Biochemistry. 27: 6897-6993
70. Zot, A. S., and J. D. Potter 1987. Structural aspects of troponin-tropomyosin regulation of skeletal muscle contraction. Annu. Rev. Biophys. Biophys. Chem. 16:535-559