Structure of the N terminus of a nonmuscle α-Tropomyosin in complex with the C terminus: Implications for actin binding

Biochemistry

Volumn 48, Issue 6, 2009, Pages 1272-1283

  Greenfield, Norma J ^a   Kotlyanskaya, Lucy ^a   Hitchcock DeGregori, Sarah E ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN FILAMENTS; ACTIN-BINDING PROTEINS; AFFINITY BINDINGS; C TERMINUS; C-TERMINAL PEPTIDES; CIRCULAR DICHROISMS; COILED COILS; COMPLEX FORMATIONS; CYTOSKELETON; DATA SUPPORTS; HIGH-MOLECULAR WEIGHTS; LOW MOLECULAR WEIGHTS; N TERMINALS; NMR DATUM; NON-MUSCLE CELLS; STRIATED MUSCLES; TROPOMYOSIN;

DICHROISM; FILAMENTS (LAMP); MOLECULAR WEIGHT; MUSCLE; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

AMINES;

ACTIN BINDING PROTEIN; ALPHA TROPOMYOSIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; MOLECULAR WEIGHT; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN STRUCTURE; SKELETAL MUSCLE;

ACTINS; AMINO ACID SEQUENCE; KINETICS; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUSCLES; PEPTIDES; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; TROPOMYOSIN;

EID: 64349086823     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801861k     Document Type: Article

References (65)

1. Gunning, P., O'Neill, G., and Hardeman, E. (2008) Tropomyosin-based regulation of the actin cytoskeleton in time and space. Physiol. Rev. 88, 1-35.
2. Kostyukova, A. S., Hitchcock-Degregori, S. E., and Greenfield, N. J. (2007) Molecular basis of tropomyosin binding to tropomodulin, an actin-capping protein. J. Mol. Biol. 372, 608-618.
3. Kostyukova, A. S. (2008) Tropomodulins and tropomodulin/ tropomyosin interactions. Cell. Mol. Life Sci. 65, 563-569.
4. Brown, J. H., and Cohen, C. (2005) Regulation of muscle contraction by tropomyosin and troponin: how structure illuminates function. Adv. Protein Chem. 71, 121-159.
5. Moraczewska, J., Nicholson-Flynn, K., and Hitchcock-DeGregori, S. E. (1999) The ends of tropomyosin are major determinants of actin affinity and myosin subfragment 1-induced binding to F-actin in the open state. Biochemistry 38, 15885-15892.
6. Palm, T., Greenfield, N. J., and Hitchcock-DeGregori, S. E. (2003) Tropomyosin ends determine the stability and functionality of overlap and troponin T complexes. Biophys. J. 84, 3181-3189.
7. Greenfield, N. J., Montelione, G T., Farid, R. S., and Hitchcock-DeGregori, S. E. (1998) The structure of the N-terminus of striated muscle alpha-tropomyosin in a chimeric peptide: nuclear magnetic resonance structure and circular dichroism studies. Biochemistry 37, 7834-7843.
8. Brown, J. H., Kim, K H., Jun, G., Greenfield, N. J., Dominguez, R., Volkmann, N., Hitchcock-DeGregori, S. E., and Cohen, C. (2001) Deciphering the design of the tropomyosin molecule. Proc. Natl. Acad. Sci. U.S.A. 98, 8496-8501.
9. Greenfield, N. J., Huang, Y. J., Palm, T., Swapna, G. V., Monleon, D., Montelione, G. T., and Hitchcock-DeGregori, S. E. (2001) Solution NMR structure and folding dynamics of the N terminus of a rat non-muscle alpha-tropomyosin in an engineered chimeric protein. J. Mol. Biol. 312, 833-847.
10. Li, Y., Mui, S., Brown, J. H., Strand, J., Reshetnikova, L., Tobacman, L. S., and Cohen, C. (2002) The crystal structure of the C-terminal fragment of striated-muscle alpha-tropomyosin reveals a key troponin T recognition site. Proc. Natl. Acad. Sci. U.S.A. 99, 7378-7383.
11. Greenfield, N. J., Swapna, G V., Huang, Y., Palm, T., Graboski, S., Montelione, G. T., and Hitchcock-DeGregori, S. E. (2003) The structure of the carboxyl terminus of striated alpha-tropomyosin in solution reveals an unusual parallel arrangement of interacting alpha-helices. Biochemistry 42, 614-619.
12. Nitanai, Y., Minakata, S., Maeda, K., Oda, N., and Maeda, Y. (2007) Crystal structures of tropomyosin: flexible coiled-coil. Adv. Exp. Med. Biol. 592, 137-151.
13. Greenfield, N. J., Huang, Y. J., Swapna, G. V., Bhattacharya, A., Rapp, B., Singh, A., Montelione, G. T, and Hitchcock-Degregori, S. E. (2006) Solution NMR structure of the junction between tropomyosin molecules: implications for actin binding and regulation. J. Mol. Biol. 364, 80-96.
14. Phillips, G. N., Jr. (1986) Construction of an atomic model for tropomyosin and implications for interactions with actin. J. Mol. Biol. 192, 128-131.
15. Ozeki, S., Kato, T., Holtzer, M. E., and Holtzer, A. (1991) The kinetics of chain exchange in two-chain coiled coils: alpha alpha-and beta beta-tropomyosin. Biopolymers 31, 957-966.
16. Goa, J. (1953) A micro biuret method for protein determination. Scand. J. Clin. Lab. Invest. 5, 218-222.
17. Greenfield, N. J. (2006) Using circular dichroism, collected as a function of temperature, to determine the thermodynamics of protein folding and binding interactions. Nat. Protocols 1, 2527-2535.
18. Bohm, G., Muhr, R., and Jaenicke, R. (1992) Quantitative analysis of protein far UV circular dichroism spectra by neural networks. Protein Em. 5, 191-195.
19. Greenfield, N. J. (2006) Determination of the folding of proteins as a function of denaturants, osmolytes or ligands using circular dichroism. Nat. Protocols 1, 2733-2741.
20. Engel, G. (1974) Estimation of binding parameters of enzyme-ligand complex from fluorometric data by a curve fitting procedure: seryl-tRNA synthetase- tRNA Ser complex. Anal. Biochem. 61, 184-191.
21. Marquardt, D. W. (1963) An algorithm for the estimation of nonlinear parameters. J. Soc. Indust. Appl. Math. 11, 431-441.
22. Bodenhausen, G., and Ruben, D. J. (1980) Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem. Phys. Lett. 69, 185-189.
23. Kay, L. E., Keifer, P., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 114, 10663-10665.
24. Muhandiram, D. R., and Kay, L. E. (1994) Gradient-enhanced triple-resonance three-dimensional NMR experiments with improved sensitivity. J. Magn. Reson., Ser. B 103, 203-216.
25. Boucher, W., Laue, E. D., Campbell-Burk, S. L., and Domaille, P. J. (1991) Four dimensional heteronuclear triple resonance NMR methods for the assignment of backbone nuclei in proteins. J. Am. Chem. Soc. 114, 2262-2264.
26. Feng, W., Rios, C. B., and Montelione, G. T. (1996) Phase labeling of C-H and C-C spin-system topologies: application in PFG-HACANH and PFG-HACA(CO)NH triple-resonance experiments for determining backbone resonance assignments in proteins. J. Biomol. NMR 8, 98-104.
27. Rios, C. B., Feng, W., Tashiro, M., Shang, Z., and Montelione, G. T. (1996) Phase labeling of C-H and C-C spin-system topologies: application in constant-time PFG-CBCA(CO)NH experiments for discriminating amino acid spin-system types. J. Biomol. NMR 8, 345-350.
28. 15N- enriched proteins. J. Biomol. NMR 3, 185-204.
29. Kay, L. E., Ikura, M., and Bax, A. (1990) Proton proton correlation via carbon-carbon couplings. A three dimensional NMR approach for the assignment of aliphatic resonances in proteins labeled with C-13. J. Am. Chem. Soc. 112, 888-889.
30. 13C enriched proteins. J. Magn. Reson. 88, 425-431.
31. Driscoll, P. C., Clore, G. M., Marion, D., Wingfield, P. T., and Gronenborn, A. M. (1990) Complete resonance assignment for the polypeptide backbone of interleukin 1 using three-dimensional heteronuclear NMR spectroscopy. Biochemistry 29, 3542-3556.
32. 15N spectra of proteins: heteronuclear triple-resonance three-dimensional NMR spectroscopy. Application to calmodulin. Biochemistry 29, 4659-4667.
33. Zwahlen, C., Legault, P., Vincent, S. J. F., Grdenblatt, J., Konrat, R., and Kay, L. E. (1997) Methods for measurement of intermolecular NOEs by multinuclear NMR spectroscopy: application to a bacteriophage 107 N-peptide/boxB RNA complex. J. Am. Chem. Soc. 119, 6711-6721.
34. Huang, Y. J. (2001) Automated determination of protein structures from NMR data by iterative analysis of self-consistent contact patterns, Ph.D. Thesis, Rutgers University, New Brunswick, NJ.
35. Huang, Y. J., Moseley, H. N., Baran, M. C., Arrowsmith, C., Powers, R., Tejero, R., Szyperski, T., and Montelione, G. T. (2005) An integrated platform for automated analysis of protein NMR structures. Methods Enzymol. 394, 111-141.
36. Güntert, P., Mumenthaler, C., and Wüthrich, K. (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273, 283-298.
37. Brunger, A. T., Adams, P. D., Clore, G M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr., Sect. D: Biol. Crystallogr. 54 (Part 5), 905-921.
38. Whitby, F. G., and Phillips, G. N., Jr. (2000) Crystal structure of tropomyosin at 7 angstroms resolution. Proteins 38, 49-59.
39. Goodwin, L. O., Lees-Miller, J. P., Leonard, M. A., Cheley, S. B., and Helfman, D. M. (1991) Four fibroblast tropomyosin isoforms are expressed from the rat alpha-tropomyosin gene via alternative RNA splicing and the use of two promoters. J. Biol. Chem. 266, 8408-8415.
40. Jancso, A., and Graceffa, P. (1991) Smooth muscle tropomyosin coiled-coil dimers. Subunit composition, assembly, and end-to-end interaction. J. Biol. Chem. 266, 5891-5897.
41. Greenfield, N. J., and Hitchcock-DeGregori, S. E. (1995) The stability of tropomyosin, a two-stranded coiled-coil protein, is primarily a function of the hydrophobicity of residues at the helix-helix interface. Biochemistry 34, 16797-16805.
42. Kremneva, E., Nikolaeva, O., Maytum, R., Arutyunyan, A. M., Kleimenov, S. Y., Geeves, M. A., and Levitsky, D. I. (2006) Thermal unfolding of smooth muscle and nonmuscle tropomyosin alpha-homodimers with alternatively spliced exons. FEBS J. 273, 588-600.
43. Murakami, K., Stewart, M., Nozawa, K., Tomii, K., Kudou, N., Igarashi, N., Shirakihara, Y., Wakatsuki, S., Yasunaga, T., and Wakabayashi, T. (2008) Structural basis for tropomyosin overlap in thin (actin) filaments and the generation of a molecular swivel by troponin-T. Proc. Natl. Acad. Sci. U.S.A. 105, 7200-7205.
44. Parry, D. A. (1975) Analysis of the primary sequence of alphatropomyosin from rabbit skeletal muscle. J. Mol. Biol. 98, 519-535.
45. McLachlan, A. D., and Stewart, M. (1976) The 14-fold periodicity in tropomyosin and the interaction with actin. J. Mol. Biol. 103, 271-298.
46. Strelkov, S. V., and Burkhard, P. (2002) Analysis of α-helical coiled coils with the program TWISTER reveals a structural mechanism for stutter compensation. J. Struct. Biol. 137, 54-64.
47. McLachlan, A. D., and Stewart, M. (1975) Tropomyosin coiledcoil interactions: evidence for an unstaggered structure. J. Mol. Biol. 98, 293-304.
48. Lorenz, M., Poole, K. J., Popp, D., Rosenbaum, G., and Holmes, K. C. (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.
49. Greenfield, N. J., Palm, T., and Hitchcock-DeGregori, S. E. (2002) Structure and interactions of the carboxyl terminus of striated muscle alpha-tropomyosin: it is important to be flexible. Biophys. J. 83, 2754-2766.
50. Singh, A., and Hitchcock-DeGregori, S. E. (2003) Local destabilization of the tropomyosin coiled coil gives the molecular flexibility required for actin binding. Biochemistry 42, 14114-14121.
51. Singh, A., and Hitchcock-DeGregori, S. E. (2006) Dual requirement for flexibility and specificity for binding of the coiled-coil tropomyosin to its target, actin. Structure 14, 43-50.
52. Cho, Y. J., and Hitchcock-DeGregori, S. E. (1991) Relationship between alternatively spliced exons and functional domains in tropomyosin. Proc. Natl. Acad. Sci. U.S.A. 88, 10153-10157.
53. Maytum, R., Lehrer, S. S., and Geeves, M. A. (1999) Cooperativity and switching within the three-state model of muscle regulation. Biochemistry 38, 1102-1110.
54. Pope, B. J., Zierler-Gould, K. M., Kuhne, R., Weeds, A. G., and Ball, L. J. (2004) Solution structure of human cofilin: actin binding, pH sensitivity, and relationship to actin-depolymerizing factor. J. Biol. Chem. 279, 4840-4848.
55. Fedorov, A. A., Lappalainen, P., Fedorov, E. V., Drubin, D. G., and Almo, S. C. (1997) Structure determination of yeast cofilin. Nat. Struct. Biol. 4, 366-369.
56. Lappalainen, P., Fedorov, E. V., Fedorov, A. A., Almo, S. C., and Drubin, D. G. (1997) Essential functions and actin-binding surfaces of yeast cofilin revealed by systematic mutagenesis. EMBO J. 16, 5520-5530.
57. Guan, J. Q., Vorobiev, S., Almo, S. C., and Chance, M. R. (2002) Mapping the G-actin binding surface of cofilin using synchrotron protein footprinting. Biochemistry 41, 5765-5775.
58. Moriyama, K., and Yahara, I. (2002) The actin-severing activity of cofilin is exerted by the interplay of three distinct sites on cofilin and essential for cell viability. Biochem. J. 365, 147-155.
59. Bernstein, B. W., and Bamburg, J. R. (1982) Tropomyosin binding to F-actin protects the F-actin from disassembly by brain actindepolymerizing factor (ADF). Cell Motil. 2, 1-8.
60. Nishida, E., Maekawa, S., and Sakai, H. (1984) Cofilin, a protein in porcine brain that binds to actin filaments and inhibits their interactions with myosin and tropomyosin. Biochemistry 23, 5307-5313.
61. DesMarais, V., Ichetovkin, I., Condeelis, J., and Hitchcock-DeGregori, S. E. (2002) Spatial regulation of actin dynamics: a tropomyosin-free, actin-rich compartment at the leading edge. J. Cell Sci 115, 4649-4660.
62. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R., and Thornton, J. M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486.
63. Savitsky, A., and Golay, M. J. E. (1964) Smoothing and dIfferentiation of data by simplified least squares procedures. Anal. Chem. 36, 1627-1639.
64. Koradi, R., Billeter, M., and Wüthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graphics 14, 51-55.
65. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J. Commit. Chem. 25, 1605-1612.