Tropomyosin regulates elongation by formin at the fast-growing end of the actin filament

Biochemistry

Volumn 46, Issue 27, 2007, Pages 8146-8155

  Wawro, Barbara ^a,d   Greenfield, Norma J ^a   Wear, Martin A ^b,e   Cooper, John A ^b   Higgs, Henry N ^c   Hitchcock DeGregori, Sarah E ^a  

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

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

^d University of Edinburgh ^*  (Poland)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINESIS; CYTOSKELETON; FILAMENT GROWTH;

CELLS; GROWTH KINETICS; POLYMERIZATION;

PROTEINS;

BINDING PROTEIN; CYTOSKELETON PROTEIN; ISOPROTEIN; METHENAMINE; MYOSIN; PROTEIN FH1; PROTEIN FH2; PROTEIN SUBUNIT; TROPOMYOSIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ARTICLE; BARBED END; BINDING SITE; CELL ELONGATION; CELL FUNCTION; CELL GROWTH; CELL MIGRATION; CELL POLARITY; CELL SHAPE; CELL STRUCTURE; CYTOKINESIS; CYTOSKELETON; FORMIN HOMOLOGY DOMAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION;

ACTINS; ANIMALS; CHICKENS; CIRCULAR DICHROISM; FETAL PROTEINS; MICROFILAMENT PROTEINS; NUCLEAR PROTEINS; TROPOMYOSIN;

EID: 34447307946     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi700686p     Document Type: Article

References (78)

1. dos Remedios, C. G., Chhabra, D., Kekic, M., Dedova, I. V., Tsubakihara, M., Berry, D. A., and Nosworthy, N. J. (2003) Actin binding proteins: regulation of cytoskeletal microfilaments, Physiol. Rev. 83, 433-473.
2. Nicholson-Dykstra, S., Higgs, H. N., and Harris, E. S. (2005) Actin dynamics: growth from dendritic branches, Curr. Biol. 15, R346-357.
3. Faix, J., and Grosse, R. (2006) Staying in shape with formins, Dev. Cell 10, 693-706.
4. Kovar, D. R. (2006) Cell polarity: formin on the move, Curr. Biol. 16, R535-R538.
5. Higgs, H. N. (2005) Formin proteins: a domain-based approach, Trends Biochem. Sci. 30, 342-353.
6. Kovar, D. R., and Pollard, T. D. (2004) Insertional assembly of actin filament barbed ends in association with formins produces piconewton forces, Proc. Natl. Acad. Sci. U.S.A. 101, 14725-14730.
7. Romero, S., Le Clainche, C., Didry, D., Egile, C., Pantaloni, D., and Carlier, M. F. (2004) Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis, Cell 119, 419-429.
8. Watanabe, N., and Higashida, C. (2004) Formins: processive cappers of growing actin filaments, Exp. Cell Res. 301, 16-22.
9. Michelot, A., Delivery, E., Paterski-Boujemaa, R., Guerin, C., Huang, S., Parcy, F., Staiger, C. J., and Blanchoin, L. (2006) A novel mechanism for the formation of actin-filament bundles by a nonprocessive formin, Curr. Biol. 16, 1924-1930.
10. Mejillano, M. R., Kojima, S., Applewhite, D. A., Gertler, F. B., Svitkina, T. M., and Borisy, G. G. (2004) Lamellipodial versus filopodial mode of the actin nanomachinery: pivotal role of the filament barbed end, Cell 118, 363-373.
11. Wear, M. A., and Cooper, J. A. (2004) Capping protein: new insights into mechanism and regulation, Trends Biochem. Sci. 29, 418-428.
12. Waddle, J. A., Karpova, T. S., Waterston, R. H., and Cooper, J. A. (1996) Movement of cortical actin patches in yeast, J. Cell Biol. 132, 861-870.
13. Kim, K., Yamashita, A., Wear, M. A., Maeda, Y., and Cooper, J. A. (2004) Capping protein binding to actin in yeast: biochemical mechanism and physiological relevance, J. Cell Biol. 164, 567-580.
14. Engqvist-Goldstein, A. E., and Drubin, D. G. (2003) Actin assembly and endocytosis: from yeast to mammals, Annu. Rev. Cell Dev. Biol. 19, 287-332.
15. Schafer, D. A., Jennings, P. B., and Cooper, J. A. (1996) Dynamics of capping protein and actin assembly in vitro: uncapping barbed ends by polyphosphoinositides, J. Cell Biol. 135, 169-179.
16. Uruno, T., Remmert, K., and Hammer, J. A., III. (2006) CARMIL is a potent capping protein antagonist: identification of a conserved CARMIL domain that inhibits the activity of capping protein and uncaps capped actin filaments, J. Biol. Chem. 281, 10635-10650.
17. Bhattacharya, N., Ghosh, S., Sept, D., and Cooper, J. A. (2006) Binding of myotrophin/V-1 to actin-capping protein: implications for how capping protein binds to the filament barbed end, J. Biol. Chem. 281, 31021-31030.
18. Kovar, D. R., Harris, E. S., Mahaffy, R., Higgs, H. N., and Pollard, T. D. (2006) Control of the assembly of ATP- and ADP-actin by formins and profilin, Cell 124, 423-435.
19. Gunning, P. W., Schevzov, G., Kee, A. J., and Hardeman, E. C. (2005) Tropomyosin isoforms: divining rods for actin cytoskeleton function, Trends Cell Biol. 15, 333-341.
20. Perry, S. V. (2001) Vertebrate tropomyosin: distribution, properties and function, J. Muscle Res. Cell Motil. 22, 5-49.
21. 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.
22. Ishiwata, S., and Fujime, S. (1972) Effect of calcium ions on the flexibility of reconstituted thin filaments of muscle studied by quasielastic scattering of laser light, J. Mol. Biol. 68, 511-522.
23. Hitchcock, S. E., Carisson, L., and Lindberg, U. (1976) Depolymerization of F-actin by deoxyribonuclease I, Cell 7, 531-542.
24. Bernstein, B. W., and Bamburg, J. R. (1982) Tropomyosin binding to F-actin protects the F-actin from disassembly by brain actin-depolymerizing factor (ADF), Cell Motil. 2, 1-8.
25. Kobayashi, R., Nonomura, Y., Okano, A., and Tashima, Y. (1983) Purification and some properties of porcine kidney tropomyosin, J. Biochem. (Tokyo) 94, 171-179.
26. Pruliere, G., d'Albis, A., and der Terrossian, E. (1986) Effect of tropomyosin on the interactions of actin with actin-binding proteins isolated from pig platelets, Eur. J. Biochem. 159, 535-547.
27. Ludescher, R. D., and Liu, Z. (1993) Characterization of skeletal muscle actin labeled with the triplet probe erythrosin-5-iodoacetamide, Photochem. Photobiol. 58, 858-866.
28. 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.
29. Ono, S., and Ono, K. (2002) Tropomyosin inhibits ADF/cofilin-dependent actin filament dynamics, J. Cell Biol. 156, 1065-1076.
30. Yu, R., and Ono, S. (2006) Dual roles of tropomyosin as an F-actin stabilizer and a regulator of muscle contraction in Caenorhabditis elegans body wall muscle, Cell Motil. Cytoskeleton 63, 659-672.
31. Fischer, R. S., and Fowler, V. M. (2003) Tropomodulins: life at the slow end, Trends Cell Biol. 13, 593-601.
32. Broschat, K. O., Weber, A., and Burgess, D. R. (1989) Tropomyosin stabilizes the pointed end of actin filaments by slowing depolymerization, Biochemistry 28, 8501-8506.
33. Broschat, K. O. (1990) Tropomyosin prevents depolymerization of actin filaments from the pointed end, J. Biol. Chem. 265, 21323-21329.
34. Kostyukova, A. S., and Hitchcock-DeGregori, S. E. (2004) Effect of the structure of the N terminus of tropomyosin on tropomodulin function, J. Biol. Chem. 279, 5066-5071.
35. Ishikawa, R., Yamashiro, S., and Matsumura, F. (1989) Annealing of gelsolin-severed actin fragments by tropomyosin in the presence of Ca2+. Potentiation of the annealing process by caldesmon, J. Biol. Chem. 264, 16764-16770.
36. Koepf, E. K., and Burtnick, L. D. (1992) Interaction of plasma gelsolin with tropomyosin, FEBS Lett. 309, 56-58.
37. Maciver, S. K., Ternent, D., and McLaughlin, P. J. (2000) Domain 2 of gelsolin binds directly to tropomyosin, FEBS Lett. 473, 71-75.
38. Nyakern-Meazza, M., Narayan, K., Schutt, C. E., and Lindberg, U. (2002) Tropomyosin and gelsolin cooperate in controlling the microfilament system, J. Biol. Chem. 277, 28774-28779.
39. Liu, H. P., and Bretscher, A. (1989) Disruption of the single tropomyosin gene in yeast results in the disappearance of actin cables from the cytoskeleton, Cell 57, 233-242.
40. Evangelista, M., Blundell, K., Longtine, M. S., Chow, C. J., Adames, N., Pringle, J. R., Peter, M., and Boone, C. (1997) Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis, Science 276, 118-122.
41. Sagot, I., Klee, S. K., and Pellman, D. (2002) Yeast formins regulate cell polarity by controlling the assembly of actin cables, Nat. Cell Biol. 4, 42-50.
42. Spudich, J. A., and Watt, S. (1971) The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin, J. Biol. Chem. 246, 4866-4871.
43. Kouyama, T., and Mihashi, K. (1981) Fluorimetry study of N-(1-pyrenyl)iodoacetamide-labelled F-actin. Local structural change of actin protomer both on polymerization and on binding of heavy meromyosin, Eur. J. Biochem. 114, 33-38.
44. 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.
45. Hitchcock-DeGregori, S. E., Lewis, S. F., and Chou, T. M. (1985) Tropomyosin lysine reactivities and relationship to coiled-coil structure, Biochemistry 24, 3305-3314.
46. Harris, E. S., Li, F., and Higgs, H. N. (2004) The mouse formin, FRLalpha, slows actin filament barbed end elongation, competes with capping protein, accelerates polymerization from monomers, and severs filaments, J. Biol. Chem. 279, 20076-20087.
47. Schafer, D. A., Korshunova, Y. O., Schroer, T. A., and Cooper, J. A. (1994) Differential localization and sequence analysis of capping protein beta-subunit isoforms of vertebrates, J. Cell Biol. 127, 453-465.
48. Edelhoch, H. (1967) Spectroscopic determination of tryptophan and tyrosine in proteins, Biochemistry 6, 1948-1954.
49. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
50. Brahms, S., and Brahms, J. (1980) Determination of protein secondary structure in solution by vacuum ultraviolet circular dichroism, J. Mol. Biol. 138, 149-178.
51. Harris, E. S., Rouiller, I., Hanein, D., and Higgs, H. N. (2006) Mechanistic differences in actin bundling activity of two mammalian formins, FRL1 and mDia2, J. Biol. Chem. 281, 14383-14392.
52. Ohtsuki, I. (1979) Molecular arrangement of troponin-T in the thin filament, J. Biochem. (Tokyo) 86, 491-497.
53. Teubner, A., and Wegner, A. (1996) The rate of annealing of actin tropomyosin filaments depends strongly on the length of the filaments, Biochim. Biophys. Acta 1297, 214-218.
54. Hitchcock-DeGregori, S. E., Sampath, P., and Pollard, T. D. (1988) Tropomyosin inhibits the rate of actin polymerization by stabilizing actin filaments, Biochemistry 27, 9182-9185.
55. Greenfield, N. J. (2004) Analysis of circular dichroism data, Methods Enzymol. 383, 282-317.
56. Greenfield, N. J., Kostyukova, A. S., and Hitchcock-DeGregori, S. E. (2005) Structure and tropomyosin binding properties of the N-terminal capping domain of tropomodulin 1, Biophys. J. 88, 372-383.
57. Kostyukova, A. S., Rapp, B. A., Choy, A., Greenfield, N. J., and Hitchcock-DeGregori, S. E. (2005) Structural requirements of tropomodulin for tropomyosin binding and actin filament capping, Biochemistry 44, 4905-4910.
58. Hammell, R. L., and Hitchcock-DeGregori, S. E. (1996) Mapping the functional domains within the carboxyl terminus of alpha-tropomyosin encoded by the alternatively spliced ninth exon, J. Biol. Chem. 271, 4236-4242.
59. Harris, E. S., and Higgs, H. N. (2006) Biochemical analysis of mammalian formin effects on actin dynamics, Methods Enzymol. 406, 190-214.
60. Bugyi, B., Papp, G., Hild, G., Lorinczy, D., Nevalainen, E. M., Lappalainen, P., Somogyi, B., and Nyitrai, M. (2006) Formins regulate actin filament flexibility through long range allosteric interactions, J. Biol. Chem. 281, 10727-10736.
61. Heald, R. W., and Hitchcock-DeGregori, S. E. (1988) The structure of the amino terminus of tropomyosin is critical for binding to actin in the absence and presence of troponin, J. Biol. Chem. 263, 5254-5259.
62. Urbancikova, M., and Hitchcock-DeGregori, S. E. (1994) Requirement of amino-terminal modification for striated muscle alpha-tropomyosin function, J. Biol. Chem. 269, 24310-24315.
63. Blanchoin, L., Pollard, T. D., and Hitchcock-DeGregori, S. E. (2001) Inhibition of the Arp2/3 complex-nucleated actin polymerization and branch formation by tropomyosin, Curr. Biol. 11, 1300-1304.
64. Hart, M. C., Korshunova, Y. O., and Cooper, J. A. (1997) Vertebrates have conserved capping protein alpha isoforms with specific expression patterns, Cell Motil. Cytoskeleton 38, 120-132.
65. Hart, M. C., and Cooper, J. A. (1999) Vertebrate isoforms of actin capping protein beta have distinct functions in vivo, J. Cell Biol. 147, 1287-1298.
66. Papp, G., Bugyi, B., Ujfalusi, Z., Barko, S., Hild, G., Somogyi, B., and Nyitrai, M. (2006) Conformational changes in actin filaments induced by formin binding to the barbed end, Biophys. J. 91, 2564-2572.
67. Prochniewicz, E., Zhang, Q., Janmey, P. A., and Thomas, D. D. (1996) Cooperativity in F-actin: binding of gelsolin at the barbed end affects structure and dynamics of the whole filament, J. Mol. Biol. 260, 756-766.
68. Otomo, T., Tomchick, D. R., Otomo, C., Panchal, S. C., Machius, M., and Rosen, M. K. (2005) Structural basis of actin filament nucleation and processive capping by a formin homology 2 domain, Nature 433, 488-494.
69. 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.
70. 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.
71. 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.
72. Yamashita, A., Maeda, K., and Maeda, Y. (2003) Crystal structure of CapZ: structural basis for actin filament barbed end capping, EMBO J. 22, 1529-1538.
73. Xu, Y., Moseley, J. B., Sagot, I., Poy, F., Pellman, D., Goode, B. L., and Eck, M. J. (2004) Crystal structures of a formin homology-2 domain reveal a tethered dimer architecture, Cell 116, 711-723.
74. Narita, A., Takeda, S., Yamashita, A., and Maeda, Y. (2006) Structural basis of actin filament capping at the barbed-end: a cryo-electron microscopy study, EMBO J. 25, 5626-5633.
75. Krause, M., Dent, E. W., Bear, J. E., Loureiro, J. J., and Gertler, F. B. (2003) Ena/VASP proteins: regulators of the actin cytoskeleton and cell migration, Annu. Rev. Cell Dev. Biol. 19, 541-564.
76. Barzik, M., Kotova, T. I., Higgs, H. N., Hazelwood, L., Hanein, D., Gertler, F. B., Schafer, D. A. (2005) Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins, J. Biol. Chem. 280, 28653-286562.
77. Scott, J. A., Shewan, A. M., den Elzen, N. R., Loureiro, J. J., Gertler, F. B., and Yap, A. S. (2006) Ena/VASP proteins can regulate distinct modes of actin organization at cadherin-adhesive contacts, Mol. Biol. Cell 17, 1085-1095.
78. Casella, J. F., Maack, D. J., and Lin, S. (1986) Purification and initial characterization of a protein from skeletal muscle that caps the barbed ends of actin filaments, J. Biol. Chem. 261, 10915-10921.