Dual roles of tropomyosin as an F-actin stabilizer and a regulator of muscle contraction in Caenorhabditis elegans body wall muscle

Cell Motility and the Cytoskeleton

Volumn 63, Issue 11, 2006, Pages 659-672

  Yu, Robinson ^a   Ono, Shoichiro ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Actin dynamics; ADF cofilin; AIP1; Myofibrils; Tropomyosin

Indexed keywords

ACTIN DEPOLYMERIZING FACTOR; ACTING INTERACTING PROTEIN 1; COFILIN; F ACTIN; GENE PRODUCT; ISOPROTEIN; MUTANT PROTEIN; MYOSIN HEAVY CHAIN; TROPOMYOSIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ALLELE; ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; CYTOSKELETON; IN VITRO STUDY; IN VIVO STUDY; MUSCLE CELL; MUSCLE CONTRACTION; MUTANT; MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY;

ACTINS; ALLELES; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELLS, CULTURED; MICROFILAMENT PROTEINS; MOVEMENT; MUSCLE CONTRACTION; MUSCLES; MUTATION; PHENOTYPE; RNA INTERFERENCE; TROPOMYOSIN;

CAENORHABDITIS ELEGANS;

EID: 33750534805     PISSN: 08861544     EISSN: 10970169     Source Type: Journal    
DOI: 10.1002/cm.20152     Document Type: Article

References (91)

1. Aizawa H, Katadae M, Maruya M, Sameshima M, Murakami-Murofushi K, Yahara I. 1999. Hyperosmotic stress-induced reorganization of actin bundles in Dictyostelium cells over-expressing cofilin. Genes Cells 4:311-324.
2. Anyanful A, Ono K, Johnsen RC, Ly H, Jensen V, Baillie DL, Ono S. 2004. The RNA-binding protein SUP-12 controls muscle-specific splicing of the ADF/cofilin pre-mRNA in Caenorhabditis elegans. J Cell Biol 167:639-647.
3. Balcer HI, Goodman AL, Rodal AA, Smith E, Kugler J, Heuser JE, Goode BL. 2003. Coordinated regulation of actin filament turnover by a high-molecular-weight Srv2/CAP complex, cofilin, profilin, and Aipl. Curr Biol 13:2159-2169.
4. Bamburg JR. 1999. Proteins of the ADF/cofilin family: Essential regulators of actin dynamics. Annu Rev Cell Dev Biol 15:185-230.
5. Bamburg JR, McGough A, Ono S. 1999. Putting a new twist on actin: ADF/cofilins modulate actin dynamics. Trends Cell Biol 9:364-370.
6. Bernstein BW, Bamburg JR. 1982. Tropomyosin binding to F-actin protects the F-actin from disassembly by brain actin-depolymerizing factor (ADF). Cell Motil 2:1-8.
7. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71-94.
8. Broschat KO. 1990. Tropomyosin prevents depolymerization of actin filaments from the pointed end. J Biol Chem 265:21323-21329.
9. Broschat KO, Weber A, Burgess DR. 1989. Tropomyosin stabilizes the pointed end of actin filaments by slowing depolymerization. Biochemistry 28:8501-8506.
10. Brown JH, Cohen C. 2005. Regulation of muscle contraction by tropomyosin and troponin: How structure illuminates function. Adv Protein Chem 71:121-159.
11. Bryce NS, Schevzov G, Ferguson V, Percival JM, Lin JJ, Matsumura F, Bamburg JR, Jeffrey PL, Hardeman EC, Gunning P, Weinberger RP. 2003. Specification of actin filament function and molecular composition by tropomyosin isoforms. Mol Biol Cell 14:1002-1016.
12. Chang AN, Potter JD. 2005. Sarcomeric protein mutations in dilated cardiomyopathy. Heart Fail Rev 10:225-235.
13. Clark MG, Teply J, Haarer BK, Viggiano SC, Sept D, Amberg DC. 2006. A genetic dissection of Aip1p's interactions leads to a model for Aip1p-cofilin cooperative activities. Mol Biol Cell 17:1971-1984.
14. Clarkson E, Costa CF, Machesky LM. 2004. Congenital myopathies: Diseases of the actin cytoskeleton. J Pathol 204:407-417.
15. Cooper J. 2002. Actin dynamics: Tropomyosin provides stability. Curr Biol 12:R523-R525.
16. Dabiri GA, Ayoob JC, Turnacioglu KK, Sanger JM, Sanger JW. 1999. Use of green fluorescent proteins linked to cytoskeletal proteins to analyze myofibrillogenesis in living cells. Methods Enzymol 302:171-186.
17. De Deyne PG. 2000. Formation of sarcomeres in developing myotubes: Role of mechanical stretch and contractile activation. Am J Physiol Cell Physiol 279:C1801-C1811.
18. DesMarais V, Ichetovkin I, Condeelis J, Hitchcock-DeGregori SE. 2002. Spatial regulation of actin dynamics: A tropomyosin-free, actin-rich compartment at the leading edge. J Cell Sci 115:4649-4660.
19. Dibb NJ, Brown DM, Karn J, Moerman DG, Bolten SL, Waterston RH. 1985. Sequence analysis of mutations that affect the synthesis, assembly and enzymatic activity of the unc-54 myosin heavy chain of Caenorhabditis elegans. J Mol Biol 183:543-551.
20. 2+ and the contractile proteins. J Mol Cell Cardiol 16:129-136.
21. Ebashi S, Kodama A. 1966. Interaction of troponin with F-actin in the presence of tropomyosin. J Biochem (Tokyo) 59:425-426.
22. Epstein HF, Thomson JN. 1974. Temperature-sensitive mutation affecting myofilament assembly in Caenorhabditis elegans. Nature 250:579-580.
23. Fattoum A, Hartwig JH, Stossel TP. 1983. Isolation and some structural and functional properties of macrophage tropomyosin. Biochemistry 22:1187-1193.
24. Friden J, Lieber RL. 1992. Structural and mechanical basis of exercise-induced muscle injury. Med Sci Sports Exerc 24:521-530.
25. Goetinck S, Waterston RH. 1994. The Caenorhabditis elegans UNC-87 protein is essential for maintenance, but not assembly, of bodywall muscle. J Cell Biol 127:71-78.
26. Golitsina N, An Y, Greenfield NJ, Thierfelder L, lizuka K, Seidman JG, Seidman CE, Lehrer SS, Hitchcock-DeGregori SE. 1997. Effects of two familial hypertrophic cardiomyopathy-causing mutations on alpha-tropomyosin structure and function. Biochemistry 36:4637-4642.
27. Gordon AM, Homsher E, Regnier M. 2000. Regulation of contraction in striated muscle. Physiol Rev 80:853-924.
28. Gunning PW, Schevzov G, Kee AJ, Hardeman EC. 2005. Tropomyosin isoforms: Divining rods for actin cytoskeleton function. Trends Cell Biol 15:333-341.
29. Gupton SL, Anderson KL, Kole TP, Fischer RS, Ponti A, Hitchcock-DeGregori SE, Danuser G, Fowler VM, Wirtz D, Hanein D, Waterman-Storer CM. 2005. Cell migration without a lamellipodium: Translation of actin dynamics into cell movement mediated by tropomyosin. J Cell Biol 168:619-631.
30. Hillberg L, Zhao Rathje L-S, Nyakern-Meazza M, Helfand B, Goldman RD, Schutt CE, Lindberg U. 2006. Tropomyosins are present in lamellipodia of motile cells. Eur J Cell Biol 85:399-409.
31. Hitchcock-DeGregori SE, Sampath P, Pollard TD. 1988. Tropomyosin inhibits the rate of actin polymerization by stabilizing actin filaments. Biochemistry 27:9182-9185.
32. Imanaka-Yoshida K, Sanger JM, Sanger JW. 1993. Contractile protein dynamics of myofibrils in paired adult rat cardiomyocytes. Cell Motil Cytoskeleton 26:301-312.
33. 2+. Potentiation of the annealing process by caldesmon. J Biol Chem 264:16764-16770.
34. Ishikawa R, Yamashiro S, Matsumura F. 1989b. Differential modulation of actin-severing activity of gelsolin by multiple isoforms of cultured rat cell tropomyosin. Potentiation of protective ability of tropomyosins by 83-kDa nonmuscle caldesmon. J Biol Chem 264:7490-7497.
35. Kagawa H, Sugimoto K, Matsumoto H, Inoue T, Imadzu H, Takuwa K, Sakube Y. 1995. Genome structure, mapping and expression of the tropomyosin gene tmy-1 of Caenorhabditis elegans. J Mol Biol 251:603-613.
36. Kagawa M, Sato N, Obinata T. Effects of BTS (N-benzyl-p-toluene sulphonamide), an inhibitor for myosin-actin interaction, on myofibrillogenesis in skeletal muscle cells in culture. Zool Sci. (in press).
37. Komiyama M, Kouchi K, Maruyama K, Shimada Y. 1993. Dynamics of actin and assembly of connectin (titin) during myofibrillogenesis in embryonic chick cardiac muscle cells in vitro. Dev Dyn 196:291-299.
38. Lal AA, Korn ED. 1986. Effect of muscle tropomyosin on the kinetics of polymerization of muscle actin. Biochemistry 25:1154-1158.
39. Lieber RL, Woodburn TM, Friden J. 1991. Muscle damage induced by eccentric contractions of 25% strain. J Appl Physiol 70:2498-2507.
40. Lin JJ, Warren KS, Wamboldt DD, Wang T, Lin JL. 1997. Tropomyosin isoforms in nonmuscle cells. Int Rev Cytol 170:1-38.
41. Lippincott-Schwartz J, Altan-Bonnet N, Patterson GH. 2003. Photo-bleaching and photoactivation: Following protein dynamics in living cells. Nat Cell Biol 5 [Suppl]:S7-S14.
42. Littlefield R, Almenar-Queralt A, Fowler VM. 2001. Actin dynamics at pointed ends regulates thin filament length in striated muscle. Nat Cell Biol 3:544-551.
43. Mabuchi I. 1982. Effects of muscle proteins on the interaction between actin and an actin-depolymerizing protein from starfish oocytes. J Biochem (Tokyo) 92:1439-1447.
44. MacLeod AR, Waterston RH, Fishpool RM, Brenner S. 1977. Identification of the structural gene for a myosin heavy-chain in Caenorhabditis elegans. J Mol Biol 114:133-140.
45. McKim KS, Heschl MF, Rosenbluth RE, Baillie DL. 1988. Genetic organization of the unc-60 region in Caenorhabditis elegans. Genetics 118:49-59.
46. McKim KS, Matheson C, Marra MA, Wakarchuk MF, Baillie DL. 1994. The Caenorhabditis elegans unc-60 gene encodes proteins homologous to a family of actin-binding proteins. Mol Gen Genet 242:346-357.
47. Michele DE, Metzger JM. 2000. Physiological consequences of tropomyosin mutations associated with cardiac and skeletal myopathies. J Mol Med 78:543-553.
48. Michele DE, Albayya FP, Metzger JM. 1999. Thin filament protein dynamics in fully differentiated adult cardiac myocytes: Toward a model of sarcomere maintenance. J Cell Biol 145:1483-1495.
49. Miller DM, Ortiz I, Berliner GC, Epstein HF. 1983. Differential localization of two myosins within nematode thick filaments. Cell 34:477-490.
50. Moerman DG, Plurad S, Waterston RH, Baillie DL. 1982. Mutations in the unc-54 myosin heavy chain gene of Caenorhabditis elegans that alter contractility but not muscle structure. Cell 29:773-781.
51. Mohri K, Ono S. 2003. Actin filament disassembling activity of Caenorhabditis elegans actin-interacting protein 1 (UNC-78) is dependent on filament binding by a specific ADF/cofilin isoform. J Cell Sci 116:4107-4118.
52. Mohri K, Takano-Ohmuro H, Nakashima H, Hayakawa K, Endo T, Hanaoka K, Obinata T. 2000. Expression of cofilin isoforms during development of mouse striated muscles. J Muscle Res Cell Motil 21:49-57.
53. Mohri K, Vorobiev S, Fedorov AA, Almo SC, Ono S. 2004. Identification of functional residues on Caenorhabditis elegans actin-interacting protein 1 (UNC-78) for disassembly of actin depolymerizing factor/cofilin-bound actin filaments. J Biol Chem 279:31697-31707.
54. Mohri K, Ono K, Yu R, Yamashiro S, Ono S. 2006. Enhancement of actin-depolymerizing factor/cofilin-dependent actin disassembly by actin-interacting protein 1 is required for organized actin filament assembly in the Caenorhabditis elegans body wall muscle. Mol Biol Cell 17:2190-2199.
55. Moraczewska J, Greenfield NJ, Liu Y, Hitchcock-DeGregori SE. 2000. Alteration of tropomyosin function and folding by a nemaline myopathy-causing mutation. Biophys J 79:3217-3225.
56. Mudry RE, Perry CN, Richards M, Fowler VM, Gregorio CC. 2003. The interaction of tropomodulin with tropomyosin stabilizes thin filaments in cardiac myocytes. J Cell Biol 162:1057-1068.
57. Nakashima K, Sato N, Nakagaki T, Abe H, Ono S, Obinata T. 2005. Two mouse cofilin isoforms, muscle-type (MCF) and non-muscle type (NMCF), interact with F-actin with different efficiencies. J Biochem (Tokyo) 138:519-526.
58. Nishida E, Maekawa S, 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.
59. Nishida E, Muneyuki E, Maekawa S, Ohta Y, Sakai H. 1985. An actin-depolymerizing protein (destrin) from porcine kidney. Its action on F-actin containing or lacking tropomyosin. Biochemistry 24:6624-6630.
60. Nyakern-Meazza M, Narayan K, Schutt CE, Lindberg U. 2002. Tropomyosin and gelsolin cooperate in controlling the microfilament system. J Biol Chem 277:28774-28779.
61. Obinata T, Nagaoka-Yasuda R, Ono S, Kusano K, Mohri K, Ohtaka Y, Yamashiro S, Okada K, Abe H. 1997. Low molecular-weight G-actin binding proteins involved in the regulation of actin assembly during myofibrillogenesis. Cell Struct Funct 22:181-189.
62. Okada K, Obinata T, Abe H. 1999. XAIP1: A Xenopus homologue of yeast actin interacting protein 1 (AIP1), which induces disassembly of actin filaments cooperatively with ADF/cofilin family proteins. J Cell Sci 112:1553-1565.
63. Okada K, Ravi H, Smith EM, Goode BL. 2006. Aip1 and cofilin promote rapid turnover of yeast actin patches and cables: A coordinated mechanism for severing and capping filaments. Mol Biol Cell 17:2855-2868.
64. Ono K, Ono S. 2004. Tropomyosin and troponin are required for ovarian contraction in the Caenorhabditis elegans reproductive system. Mol Biol Cell 15:2782-2793.
65. Ono K, Parast M, Alberico C, Benian GM, Ono S. 2003. Specific requirement for two ADF/cofilin isoforms in distinct actin-dependent processes in Caenorhabditis elegans. J Cell Sci 116:2073-2085.
66. Ono K, Yu R, Mohri K, Ono S. 2006. Caenorhabditis elegans kettin, a large immunoglobulin-like repeat protein, binds to filamentous actin and provides mechanical stability to the contractile apparatuses in body wall muscle. Mol Biol Cell 17:2722-2724.
67. Ono S. 2001. The Caenorhabditis elegans unc-78 gene encodes a homologue of actin-interacting protein 1 required for organized assembly of muscle actin filaments. J Cell Biol 152:1313-1319.
68. Ono S. 2003a. Function of ADF/cofilin in muscle cells: An important regulator of actin cytoskeletal dynamics in myofibril assembly and muscle diseases. In: Fagan J, Davidson JN, Shimizu N, editors. Recent Developments in Cell Research. Kerala, India: Research Signpost, p 31-44.
69. Ono S. 2003b. Regulation of actin filament dynamics by actin depolymerizing factor/cofilin and actin-interacting protein 1: New blades for twisted filaments. Biochemistry 42:13363-13370.
70. Ono S, Benian GM. 1998. Two Caenorhabditis elegans actin depolymerizing factor/cofilin proteins, encoded by the unc-60 gene, differentially regulate actin filament dynamics. J Biol Chem 273:3778-3783.
71. Ono S, Ono K. 2002. Tropomyosin inhibits ADF/cofilin-dependent actin filament dynamics. J Cell Biol 156:1065-1076.
72. Ono S, Minami N, Abe H, Obinata T. 1994. Characterization of a novel cofilin isoform that is predominantly expressed in mammalian skeletal muscle. J Biol Chem 269:15280-15286.
73. Ono S, Baillie DL, Benian GM. 1999. UNC-60B, an ADF/cofilin family protein, is required for proper assembly of actin into myofibrils in Caenorhabditis elegans body wall muscle. J Cell Biol 145:491-502.
74. Ono S, McGough A, Pope BJ, Tolbert VT, Bui A, Pohl J, Benian GM, Gernert KM, Weeds AG. 2001. The C-terminal tail of UNC-60B (ADF/cofilin) is critical for maintaining its stable association with F-actin and is implicated in the second actin-binding site. J Biol Chem 276:5952-5958.
75. Ono S, Mohri K, Ono K. 2004. Microscopic evidence that actin-interacting protein 1 actively disassembles actin-depolymerizing factor/cofilin-bound actin filaments. J Biol Chem 279:14207-14212.
76. Pardee JD, Spudich JA. 1982. Purification of muscle actin. Methods Enzymol 85:164-181.
77. Perry SV. 2003. What is the role of tropomyosin in the regulation of muscle contraction? J Muscle Res Cell Motil 24:593-596.
78. Pittenger MF, Kazzaz JA, Helfman DM. 1994. Functional properties of non-muscle tropomyosin isoforms. Curr Opin Cell Biol 6:96-104.
79. Ramachandran I, Terry M, Ferrari MB. 2003. Skeletal muscle myosin cross-bridge cycling is necessary for myofibrillogenesis. Cell Motil Cytoskeleton 55:61-72.
80. Rodal AA, Tetreault JW, Lappalainen P, Drubin DG, Amberg DC. 1999. Aip1p interacts with cofilin to disassemble actin filaments. J Cell Biol 145:1251-1264.
81. Soeno Y, Shimada Y, Obinata T. 1999. BDM (2,3-butanedione monoxime), an inhibitor of myosin-actin interaction, suppresses myofibrillogenesis in skeletal muscle cells in culture. Cell Tissue Res 295:307-316.
82. Squire JM, Morris EP. 1998. A new look at thin filament regulation in vertebrate skeletal muscle. FASEB J 12:761-771.
83. Thirion C, Stucka R, Mendel B, Gruhler A, Jaksch M, Nowak KJ, Binz N, Laing NG, Lochmuller H. 2001. Characterization of human muscle type cofilin (CFL2) in normal and regenerating muscle. Eur J Biochem 268:3473-3482.
84. Timmons L, Fire A. 1998. Specific interference by ingested dsRNA. Nature 395:854.
85. Timmons L, Court DL, Fire A. 2001. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263:103-112.
86. Tubridy N, Fontaine B, Eymard B. 2001. Congenital myopathies and congenital muscular dystrophies. Curr Opin Neurol 14:575-582.
87. Vartiainen MK, Mustonen T, Mattila PK, Ojala PJ, Thesleff I, Partanen J, Lappalainen P. 2002. The three mouse actin-depolymerizing factor/cofilins evolved to fulfill cell-type-specific requirements for actin dynamics. Mol Biol Cell 13:183-194.
88. Waterston RH, Thomson JN, Brenner S. 1980. Mutants with altered muscle structure of Caenorhabditis elegans. Dev Biol 77:271-274.
89. Williams BD, Waterston RH. 1994. Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J Cell Biol 124:475-490.
90. Yamashiro S, Mohri K, Ono S. 2005. The two Caenorhabditis elegans actin depolymerizing factor/cofilin proteins differently enhance actin filament severing and depolymerization. Biochemistry 44:14238-14247.
91. Zengel JM, Epstein HF. 1980. Identification of genetic elements associated with muscle structure in the nematode Caenorhabditis elegans. Cell Motil 1:73-97.