UNC-60B, an ADF/cofilin family protein, is required for proper assembly of actin into myofibrils in Caenorhabditis elegans body wall muscle

Journal of Cell Biology

Volumn 145, Issue 3, 1999, Pages 491-502

  Ono, Shoichiro ^a   Baillie, David L ^b   Benian, Guy M ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SIMON FRASER UNIVERSITY   (Canada)

Author keywords

Actin polymerization; ADF cofilin; Myofibrils; Thin filaments; Unc 60

Indexed keywords

COFILIN; GENE PRODUCT;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CYTOSKELETON; GENETIC CODE; MISSENSE MUTATION; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FAMILY; RECEPTOR UPREGULATION; SARCOMERE LENGTH; SKELETAL MUSCLE; THIN FILAMENT;

ACTIN DEPOLYMERIZING FACTORS; ACTINS; ANIMALS; CAENORHABDITIS ELEGANS; CYTOSKELETON; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICROFILAMENT PROTEINS; MUSCLES; MUTAGENESIS; MYOFIBRILS; MYOSINS; PHENOTYPE; POLYMERS; POU DOMAIN FACTORS; TRANSCRIPTION FACTORS;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 0033519332     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.145.3.491     Document Type: Article

References (60)

1. Abe, H., and T. Obinata, 1989. An actin-depolymerizing protein in embryonic chicken skeletal muscle: purification and characterization. J. Biochem. 106: 172-180.
2. Abe, H., S. Ohshima, and T. Obinata. 1989. A cofilin-like protein is involved in the regulation of actin assembly in developing skeletal muscle. J. Biochem. 106:696-702.
3. Abe, H., R. Nagaoka, and T. Obinata. 1993. Cytoplasmic localization and nuclear transport of cofilin in cultured myotubes. Exp. Cell Res. 206:1-10.
4. Abe, H., T. Obinata, L.S. Minamide, and J.R. Bamburg. 1996. Xenopus laevis actin-depolymerizing factor/cofilin: a phosphorylation-regulated protein essential for development. J. Cell Biol. 132:871-885.
5. Agnew, B.J., L.S. Minamide, and J.R. Bamburg. 1995. Reactivation of phosphorylated actin depolymerizing factor and identification of the regulatory site. J. biol. Chem. 270:17582-17587.
6. Aizawa, H., K. Sutoh, and I. Yahara. 1996. Overexpression of cofilin stimulates bundling of actin filaments, membrane ruffling, and cell movement in Dictyostelium. J. Cell Biol. 132:335-344.
7. Albertson, D.G. 1984. Formation of the first cleavage spindle in nematode embryos. Dev. Biol. 101:61-72.
8. Bamburg, J.R. and D. Bray. 1987. Distribution and cellular localization of actin depolymerizing factor. J. Cell Biol. 105:2817-2825.
9. Bamburg, J.R., H.E. Harris, and A.G. Weeds. 1980. Partial purification and characterization of an actin depolymerizing factor from brain. FEBS (Fed. Eur. Biochem. Soc.) Lett. 121:178-182.
10. Barstead, R.J., and R.H. Waterston. 1991. Vinculin is essential for muscle function in the nematode. J. Cell Biol. 114:715-724.
11. Benian, G.M., T.L. Tinley, X. Tang, and M. Borodovsky. 1996. The Caenorhabditis elegans gene unc-89, required for muscle M-line assembly, encodes a giant modular protein composed of Ig and signal transduction domains. J. Cell Biol. 132:835-848.
12. Blikstad, I., F. Markey, L. Carlsson, T. Persson, and U. Lindberg. 1978. Selective assay of monomeric and filamentous actin in cell extracts, using inhibition of deoxyribonuclease I. Cell. 15:935-943.
13. Carlier, M.F., V. Laurent, J. Santolini, R. Melki, D. Didry, G.X. Xia, Y. Hong, N.H. Chua, and D. Pantaloni. 1997. Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J. Cell Biol. 136:1307-1322.
14. Du, J., and C. Frieden. 1998. Kinetic studies on the effect of yeast cofilin on yeast actin polymerization. Biochemistry. 37:13276-13284.
15. Eddy, R.J., J. Han, and J.S. Condeelis. 1997. Capping protein terminates but does not initiate chemoattractant-induced actin assembly in Dictyoslelium. J. Cell Biol. 139:1243-1253.
16. Epstein, H.F., and J.N. Thomson. 1974. Temperature-sensitive mutation affecting myofilament assembly in Caenorhabditis elegans. Nature. 250:579-580.
17. Epstein, H.F., D.L. Casey, and I. Ortiz. 1993. Myosin and paramyosin of Caenorhabditis elegans embryos assemble into nascent structures distinct from thick filaments and multifilament assemblages. J. Cell Biol. 122:845-858.
18. Fedorov, A.A., P. Lappalainen, E.V. Fedorov, D.G. Drubin, and S.C. Almo. 1997. Structure determination of yeast cofilin. Nat. Struct. Biol. 4:366-369.
19. Gill, S.C., and P.H. von Hippel. 1989. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182:319-326.
20. Gregorio, C.C., A. Weber, M. Bondad, C.R. Pennise, and V.M. Fowler. 1995. Requirement of pointed-end capping by tropomodulin to maintain actin filament length in embryonic chick cardiac myocytes. Nature. 377:83-86.
21. Gunsalus, K.C., S. Bonaccorsi, E. Williams, F. Verni, M. Gatti, and M.L. Goldberg. 1995. Mutations in twinstar, a Drosophila gene encoding a cofilin/ADF homologue, result in defects in centrosome migration and cytokinesis. J. Cell Biol. 131:1243-1259.
22. Hatanaka, H., K. Ogura, K. Moriyama, S. Ichikawa, I. Yahara, and F. Inagaki. 1996. Tertiary structure of destrin and structural similarity between two actin-regulating protein families. Cell. 85:1047-1055.
23. Hawkins, M., B. Pope, S.K. Maciver, and A.G. Weeds. 1993. Human actin depolymerizing factor mediates a pH-sensitive destruction of actin filaments. Biochemistry. 32:9985-9993.
24. Hayakawa, K., N. Minami, S. Ono, Y. Ogasawara, T. Totsuka, H. Abe, T. Tanaka, and T. Obinata. 1993. Increased expression of cofilin in dystrophic chicken and mouse skeletal muscles. J. Biochem. 114:582-587.
25. Hayden, S.M., P.S. Miller, A. Brauweiler, and J.R. Bamburg. 1993. Analysis of the interactions of actin depolymerizing factor with G-and F-actin. Biochemistry. 32:9994-10004.
26. Heacock, C.S., and J.R. Bamburg. 1983. The quantitation of G-and F-actin in cultured cells. Anal. Biochem. 135:22-36.
27. Jiang, C.J., A.G. Weeds, S. Khan, and P.J. Hussey. 1997. F-actin and G-actin binding are uncoupled by mutation of conserved tyrosine residues in maize actin depolymerizing factor (ZmADF). Proc. Natl. Acad. Sci. USA. 94:9973-9978.
28. Kouyama, T., and K. Mihashi. 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.
29. Lappalainen, P., and D.G. Drubin. 1997. Cofilin promotes rapid actin filament turnover in vivo. Nature. 388:78-82.
30. Lappalainen, P., E.V. Fedorov, A.A. Fedorov, S.C. Almo, and D.G. Drubin. 1997. Essential functions and actin-binding surfaces of yeast cofilin revealed by systematic mutagenesis. EMBO (Eur. Mol. Biol. Organ.) J. 16:5520-5530.
31. Lappalainen, P., M.M. Kessels, M.J. Cope, and D.G. Drubin. 1998. The ADF homology (ADF-H) domain: a highly exploited actin-binding module. Mol. Biol. Cell. 9:1951-1959.
32. Leonard, S.A., A.G. Gittis, E.C. Petrella, T.D. Pollard, and E.E. Lattman. 1997. Crystal structure of the actin-binding protein actophorin from Acanthamoeba. Nat. Struct. Biol. 4:369-373.
33. Lopez, I., R.G. Anthony, S.K. Maciver, C.J. Jiang, S. Khan, A.G. Weeds, and P.J. Hussey. 1996. Pollen specific expression of maize genes encoding actin depolymerizing factor-like proteins. Proc. Natl. Acad. Sci. USA. 93:7415-7420.
34. Maciver, S.K., B.J. Pope, S. Whytock, and A.G. Weeds. 1998. The effect of two actin depolymerizing factors (ADF/cofilins) on actin filament turnover: pH sensitivity of F-actin binding by human ADF, but not of Acanthamoeba actophorin. Eur. J. Biochem. 256:388-397.
35. Maciver, S.K., H.G. Zot, and T.D. Pollard, 1991. Characterization of actin filament severing by actophorin from Acanthamoeba castellanii. J. Cell Biol. 115:1611-1620.
36. McGough, A., B. Pope, W. Chiu, and A. Weeds. 1997. Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J. Cell Biol. 138:771-781.
37. McKim, K.S., C. Matheson, M.A. Marra, M.F. Wakarchuk, and D.L. Baillie. 1994. The Caenorhabditis elegans unc-60 gene encodes proteins homologous to a family of actin-binding proteins. Mol. Gen. Genet. 242:346-357.
38. McKim, K.S., M.F. Heschl, R.E. Rosenbluth, and D.L. Baillie. 1988. Genetic organization of the unc-60 region in Caenorhabditis elegans. Genetics. 118: 49-59.
39. Miller, D.M., I. Ortiz, G.C. Berliner, and H.F. Epstein. 1983. Differential localization of two myosins within nematode thick filaments. Cell. 34:477-490.
40. Minamide, L.S., and J.R. Bamburg. 1990. A filter paper dye-binding assay for quantitative determination of protein without interference from reducing agents or detergents. Anal. Biochem. 190:66-70.
41. Moon, A., and D.G. Drubin. 1995. The ADF/cofilin proteins: stimulus-responsive modulators of actin dynamics. Mol. Biol. Cell. 6:1423-1431.
42. Moriyama, K., E. Nishida, N. Yonezawa, H. Sakai, S. Matsumoto, K. Iida, and I. Yahara. 1990. Destrin, a mammalian actin-depolymerizing protein, is closely related to cofilin. Cloning and expression of porcine brain destrin cDNA. J. Biol. Chem. 265:5768-5773.
43. Moriyama, K., N. Yonezawa, H. Sakai, I. Yahara, and E. Nishida. 1992. Mutational analysis of an actin-binding site of cofilin and characterization of chimeric proteins between cofilin and destrin. J. Biol. Chem. 267:7240-7244.
44. Nagaoka, R., K. Kusano, H. Abe, and T. Obinata. 1995. Effects of cofilin on actin filamentous structures in cultured muscle cells. Intracellular regulation of cofilin action. J. Cell Sci. 108:581-593.
45. Nagaoka, R., H. Abe, and T. Obinata. 1996a. Site-directed mutagenesis of the phosphorylation site of cofilin: its role in cofilin-actin interaction and cytoplasmic localization. Cell Motil. Cytoskeleton. 35:200-209.
46. Nagaoka, R., N. Minami, K. Hayakawa, H. Abe, and T. Obinata. 1996b. Quantitative analysis of low molecular weight G-actin-binding proteins, cofilin, ADF and profilin, expressed in developing and degenerating chicken skeletal muscles. J. Muscle Res. Cell Motil. 17:463-473.
47. Nishida, E., S. Maekawa, and H. Sakai. 1984. Cofilin, a protein in porcine brain that binds to actin filaments and inhibits their interactions with myosin and tropomyosin. Biochemistry. 23:5307-5313.
48. Ohshima, S., H. Abe, and T. Obinata. 1989. Isolation of profilin from embryonic chicken skeletal muscle and evaluation of its interaction with different actin isoforms. J. Biochem. 105:855-857.
49. Ono, S. 1999. Purification and biochemical characterization of actin from Caenorhabditis elegans: its difference from rabbit muscle actin in the interaction with nematode ADF/cofilin. Cell Motil. Cyloskeleton. In press.
50. Ono, S., and G.M. Benian. 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.
51. Ono, S., H. Abe, R. Nagaoka, and T. Obinata. 1993. Colocalization of ADF and cofilin in intranuclear actin rods of cultured muscle cells. J. Muscle Res. Cell Motil. 14:195-204.
52. Ono, S., N. Minami, H. Abe, and T. Obinata. 1994. Characterization of a novel cofilin isoform that is predominantly expressed in mammalian skeletal muscle. J. Biol. Chem. 269:15280-15286.
53. Rosenblatt, J., B.J. Agnew, H. Abe, J.R. Hamburg, and T.J. Mitchison. 1997. Xenopus actin depolymerizing factor/cofilin (XAC) is responsible for the turnover of actin filaments in Listeria monocytogenes tails. J. Cell Biol 136: 1323-1332.
54. Schafer, D.A., C. Hug, and J.A. Cooper. 1995. Inhibition of CapZ during myofibrillogenesis alters assembly of actin filaments. J. Cell Biol. 128:61-70.
55. Shimizu, N., and T. Obinata. 1986. Actin concentration and monomer-polymer ratio in developing chicken skeletal muscle. J. Biochem. 99:751-759.
56. Van Troys, M., D. Dewitte, J.L. Verschelde, M. Goethals, J. Vandekerckhove, and C. Ampe. 1997. Analogous F-actin binding by cofilin and gelsolin segment 2 substantiates their structural relationship. J. Biol. Chem. 272:32750-32758.
57. Waterston, R.H., J.N. Thomson, and S. Brenner. 1980. Mutants with altered muscle structure of Caenorhabditis elegans. Dev. Biol. 77:271-302.
58. Wriggers, W., J.X. Tang, T. Azuma, P.W. Marks, and P.A. Janmey. 1998. Cofilin and gelsolin segment-1: molecular dynamics simulation and biochemical analysis predict a similar actin binding mode. J. Mol. Biol. 282:921-932.
59. Xu, J., J.F. Casella, and T.D. Pollard. 1999. Effect of capping protein, CapZ, on the length of actin filaments and mechanical properties of actin filament networks. Cell Motil. Cytoskeleton. 42:73-81.
60. Yonezawa, N., E. Nishida, K. Iida, H. Kumagai, I. Yahara, and H. Sakai. 1991. Inhibition of actin polymerization by a synthetic dodecapeptide patterned on the sequence around the actin-binding site of cofilin. J. Biol. Chem. 266: 10485-10489.