Can Förster resonance energy transfer measurements uniquely position troponin residues on the actin filament? A case study in multiple-acceptor FRET

Journal of Molecular Biology

Volumn 329, Issue 2, 2003, Pages 371-380

  Robinson, John M ^a   Dong, Wen Ji ^a   Cheung, Herbert C ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Actin model; Ca2+ regulation; Cross transfer; Macromolecular complex; Muscle activation

Indexed keywords

ACTIN; ADENOSINE DIPHOSPHATE; CALCIUM; CYSTEINE; GLUTAMINE; LYSINE; MAGNESIUM; TROPOMYOSIN; TROPONIN I;

ACTIN FILAMENT; AMINO ACID SUBSTITUTION; ANALYTIC METHOD; ARTICLE; CARBOXY TERMINAL SEQUENCE; DATA ANALYSIS; FORSTER RESONANCE ENERGY TRANSFER; MEASUREMENT; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; REGULATORY MECHANISM; SURFACE PROPERTY; THIN FILAMENT;

EID: 0038399765     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00424-8     Document Type: Article

References (26)

1. Lorenz M., Popp D., Holmes K.C. Refinement of the F-actin model against X-ray fiber diffraction data by the use of a directed mutation algorithm. J. Mol. Biol. 234:1993;826-836.
2. Squire J.M., Morris E.P. A new look at thin filament regulation in vertebrate skeletal muscle. FASEB J. 12:1998;761-771.
3. Craig R., Lehman W. The ultrastructural basis of actin filament regulation. Thomas D.D., dos Remedios C.G. Molecular Interactions of Actin. 2002;149-165 Springer, Berlin.
4. Miki M. Structural changes between regulatory proteins and actin: a regulation model by tropomyosin-troponin based on FRET measurements. Thomas D.D., dos Remedios C.G. Molecular Interactions of Actin. 2002;191-203 Springer, Berlin.
5. Kobayashi T., Kobayashi M., Collins J.H. Ca2+-dependent, myosin subfragment 1-induced proximity changes between actin and the inhibitory region of troponin I. Biochim. Biophys. Acta. 1549:2001;148-154.
6. Johnson M.L., Faunt L.M. Parameter estimation by least-squares methods. Methods Enzymol. 210:1992;1-37.
7. Yasunaga T., Suzuki Y., Ohkura R., Sutoh K., Wakabayashi T. ATP-induced transconformation of myosin revealed by determining three-dimensional positions of fluorophores from fluorescence energy transfer measurements. J. Struct. Biol. 132:2000;6-18.
8. Bacchiocchi C., Lehrer S.S. Ca2+-induced movement of tropomyosin in skeletal muscle thin filaments observed by multi-site FRET. Biophys. J. 82:2002;1524-1536.
9. Miki M., Kobayashi T., Kimura H., Hagiwara A., Hai H., Maeda Y. Ca2+-induced distance change between points on actin and troponin in skeletal muscle thin filaments estimated by fluorescence energy transfer spectroscopy. J. Biochem., (Tokyo). 123:1998;324-331.
10. Miki M. Resonance energy transfer between points in a reconstituted skeletal muscle thin filament. A conformational change of the thin filament in response to a change in Ca2+ concentration. Eur. J. Biochem. 187:1990;155-162.
11. Tao T., Gong B.J., Leavis P.C. Calcium-induced movement of troponin-I relative to actin in skeletal muscle thin filaments. Science. 247:1990;1339-1341.
12. Luo Y., Leszyk J., Li B., Li Z., Gergely J., Tao T. Troponin-I interacts with the Met47 region of skeletal muscle actin. Implications for the mechanism of thin filament regulation by calcium. J. Mol. Biol. 316:2002;429-434.
13. Narita A., Yasunaga T., Ishikawa T., Mayanagi K., Wakabayashi T. Ca2+-induced switching of troponin and tropomyosin on actin filaments as revealed by electron cryo-microscopy. J. Mol. Biol. 308:2001;241-261.
14. Li M.X., Spyracopoulos L., Sykes B.D. Binding of cardiac troponin-I147-163 induces a structural opening in human cardiac troponin-C. Biochemistry. 38:1999;8289-8298.
15. Cheung H.C. Resonance energy transfer. Lakowicz J.R. Topics in Fluorescence Spectroscopy. vol. 2:1991;127-176 Plenum Press, New York.
16. Lillo M.P., Beechem J.M., Szpikowska B.K., Sherman M.A., Mas M.T. Design and characterization of a multisite fluorescence energy-transfer system for protein folding studies: a steady-state and time-resolved study of yeast phosphoglycerate kinase. Biochemistry. 36:1997;11261-11272.
17. Yan Y., Marriott G. Fluorescence resonance energy transfer imaging microscopy and fluorescence polarization imaging microscopy. Methods Enzymol. 360:2003;561-580.
18. Levine B.A., Moir A.J., Perry S.V. The interaction of troponin-I with the N-terminal region of actin. Eur. J. Biochem. 172:1988;389-397.
19. Tripet B., Van Eyk J.E., Hodges R.S. Mapping of a second actin-tropomyosin and a second troponin C binding site within the C terminus of troponin I, and their importance in the Ca2+-dependent regulation of muscle contraction. J. Mol. Biol. 271:1997;728-750.
20. Milligan R.A. Protein-protein interactions in the rigor actomyosin complex. Proc. Natl Acad. Sci. USA. 93:1996;21-26.
21. Tung C.S., Wall M.E., Gallagher S.C., Trewhella J. A model of troponin-I in complex with troponin-C using hybrid experimental data: the inhibitory region is a beta-hairpin. Protein Sci. 9:2000;1312-1326.
22. Dong W.J., Robinson J.M., Stagg S., Xing J., Cheung H.C. Ca2+-induced conformational transition in the inhibitory and regulatory regions of cardiac troponin I. J. Biol. Chem. 278:2003;8686-8692.
23. Finley N.L., Ward D.G., Trayer I.P., Rosevear P.R. Modification of cardiac tropoin C upon binding cardiac troponin T and PKC phosphorylated cardiac troponin I. Biophys. J. 84:2003;566a.
24. Robinson J.M., Wang Y., Kerrick W.G., Kawai R., Cheung H.C. Activation of striated muscle: nearest-neighbor regulatory-unit and cross-bridge influence on myofilament kinetics. J. Mol. Biol. 322:2002;1065-1088.
25. Goldstein H. Classical Mechanics. 2nd edit. 1980;Addison-Wesley, Reading, MA.
26. Humphrey W., Dalke A., Schulten K. VMD: visual molecular dynamics. J. Mol. Graph. 14:1996;33-38.