The two actin-interacting protein 1 genes have overlapping and essential function for embryonic development in Caenorhabditis elegans

Molecular Biology of the Cell

Volumn 22, Issue 13, 2011, Pages 2258-2269

  Ono, Shoichiro ^a   Nomura, Kazumi ^a   Hitosugi, Sadae ^a   Tu, Domena K ^b   Lee, Jocelyn A ^c   Baillie, David L ^b   Ono, Kanako ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SIMON FRASER UNIVERSITY   (Canada)

^c EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ACTIN DEPOLYMERIZING FACTOR; COFILIN;

ACTIN FILAMENT; ARTICLE; CAENORHABDITIS ELEGANS; EMBRYO DEVELOPMENT; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION;

ACTIN CYTOSKELETON; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DESTRIN; EMBRYONIC DEVELOPMENT; MICROFILAMENT PROTEINS; MUSCLES; MUTATION; NEURONS; PHENOTYPE; PROTEIN ISOFORMS;

CAENORHABDITIS ELEGANS;

EID: 79959893244     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-12-0934     Document Type: Article

References (72)

1. Agrawal PB et al. (2007). Nemaline myopathy with minicores caused by mutation of the CFL2 gene encoding the skeletal muscle actin-binding protein, cofilin-2. Am J Hum Genet 80, 162-167. (Pubitemid 46047659)
2. 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. (Pubitemid 29359447)
3. Allwood EG, Anthony RG, Smertenko AP, Reichelt S, Drobak BK, Doonan JH, Weeds AG, Hussey PJ (2002). Regulation of the pollen-specific actin-depolymerizing factor LlADF1. Plant Cell 14, 2915-2927. (Pubitemid 35326312)
4. Andrianantoandro E, Pollard TD (2006). Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol Cell 24, 13-23. (Pubitemid 44466682)
5. 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 C. elegans. J Cell Biol 167, 639-647. (Pubitemid 39565145)
6. Bernstein BW, Bamburg JR (2010). ADF/cofilin: a functional node in cell biology. Trends Cell Biol 20, 187-195.
7. Brenner S (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
8. Brieher WM, Kueh HY, Ballif BA, Mitchison TJ (2006). Rapid actin monomer-insensitive depolymerization of Listeria actin comet tails by cofilin, coronin, and Aip1. J Cell Biol 175, 315-324. (Pubitemid 44631425)
9. Cai L, Makhov AM, Bear JE (2007a). F-actin binding is essential for coronin 1B function in vivo. J Cell Sci 120, 1779-1790. (Pubitemid 46930416)
10. Cai L, Marshall TW, Uetrecht AC, Schafer DA, Bear JE (2007b). Coronin 1B coordinates Arp2/3 complex and cofilin activities at the leading edge. Cell 128, 915-929. (Pubitemid 46341411)
11. Carlier MF, Laurent V, Santolini J, Melki R, Didry D, Xia GX, Hong Y, Chua NH, Pantaloni D (1997). Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J Cell Biol 136, 1307-1322. (Pubitemid 27421917)
12. Clark MG, Amberg DC (2007). Biochemical and genetic analyses provide insight into the structural and mechanistic properties of actin filament disassembly by the Aip1p cofilin complex in Saccharomyces cerevisiae. Genetics 176, 1527-1539.
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. (Pubitemid 44011611)
14. Epstein HF, Casey DL, Ortiz I (1993). Myosin and paramyosin of Caenorhabditis elegans embryos assemble into nascent structures distinct from thick filaments and multi-filament assemblages. J Cell Biol 122, 845-858. (Pubitemid 23241094)
15. Epstein HF, Thomson JN (1974). Temperature-sensitive mutation affecting myofilament assembly in Caenorhabditis elegans. Nature 250, 579-580.
16. Gandhi M, Achard V, Blanchoin L, Goode BL (2009). Coronin switches roles in actin disassembly depending on the nucleotide state of actin. Mol Cell 34, 364-374.
17. Gunsalus KC, Bonaccorsi S, Williams E, Verni F, Gatti M, Goldberg ML (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.
18. Gurniak CB, Perlas E, Witke W (2005). The actin depolymerizing factor n-cofilin is essential for neural tube morphogenesis and neural crest cell migration. Dev Biol 278, 231-241. (Pubitemid 40092863)
19. Hobert O (2002). PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32, 728-730.
20. Ichetovkin I, Han J, Pang KM, Knecht DA, Condeelis JS (2000). Actin filaments are severed by both native and recombinant Dictyostelium cofilin but to different extents. Cell Motil Cytoskeleton 45, 293-306. (Pubitemid 30196645)
21. Iida K, Moriyama K, Matsumoto S, Kawasaki H, Nishida E, Yahara I (1993). Isolation of a yeast essential gene, COF1, that encodes a homologue of mammalian cofilin, a low-Mr actin-binding and depolymerizing protein. Gene 124, 115-120. (Pubitemid 23065976)
22. Iida K, Yahara I (1999). Cooperation of two actin-binding proteins, cofilin and Aip1, in Saccharomyces cerevisiae. Genes Cells 4, 21-32.
23. Ishikawa-Ankerhold HC, Gerisch G, Muller-Taubenberger A (2010). Genetic evidence for concerted control of actin dynamics in cytokinesis, endocytic traffic, and cell motility by coronin and Aip1. Cytoskeleton 67, 442-455.
24. Kamath RS et al. (2003). Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421, 231-237. (Pubitemid 36139121)
25. Kato A, Kurita S, Hayashi A, Kaji N, Ohashi K, Mizuno K (2008). Critical roles of actin-interacting protein 1 in cytokinesis and chemotactic migration of mammalian cells. Biochem J 414, 261-270.
26. Ketelaar T, Allwood EG, Anthony R, Voigt B, Menzel D, Hussey PJ (2004). The actin-interacting protein AIP1 is essential for actin organization and plant development. Curr Biol 14, 145-149.
27. Kile BT et al. (2007). Mutations in the cofilin partner Aip1/Wdr1 cause autoinflammatory disease and macrothrombocytopenia. Blood 110, 2371-2380. (Pubitemid 47523157)
28. Konzok A, Weber I, Simmeth E, Hacker U, Maniak M, Muller-Taubenberger A (1999). DAip1, a Dictyostelium homologue of the yeast actin-interacting protein 1, is involved in endocytosis, cytokinesis, and motility. J Cell Biol 146, 453-464. (Pubitemid 29369780)
29. Kueh HY, Charras GT, Mitchison TJ, Brieher WM (2008). Actin disassembly by cofilin, coronin, and Aip1 occurs in bursts and is inhibited by barbed-end cappers. J Cell Biol 182, 341-353.
30. Maciver SK, Pope BJ, Whytock S, Weeds AG (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. (Pubitemid 28404803)
31. Maciver SK, Zot HG, Pollard TD (1991). Characterization of actin filament severing by actophorin from Acanthamoeba castellanii. J Cell Biol 115, 1611-1620. (Pubitemid 21910001)
32. McKim KS, Heschl MF, Rosenbluth RE, Baillie DL (1988). Genetic organization of the unc-60 region in Caenorhabditis elegans. Genetics 118, 49-59. (Pubitemid 18038077)
33. 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. (Pubitemid 24061216)
34. Mello C, Fire A (1995). DNA transformation. Methods Cell Biol 48, 451-482.
35. Miller DM, Ortiz I, Berliner GC, Epstein HF (1983). Differential localization of two myosins within nematode thick filaments. Cell 34, 477-490.
36. Moerman DG, Williams BD (2006). Sarcomere assembly in C. elegans muscle. WormBook 1-16.
37. 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. (Pubitemid 44011735)
38. 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. (Pubitemid 37337085)
39. 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. (Pubitemid 39037841)
40. Moon AL, Janmey PA, Louie KA, Drubin DG (1993). Cofilin is an essential component of the yeast cortical cytoskeleton. J Cell Biol 120, 421-435. (Pubitemid 23040081)
41. 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.
42. 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. (Pubitemid 43993492)
43. Okkema PG, Harrison SW, Plunger V, Aryana A, Fire A (1993). Sequence requirements for myosin gene expression and regulation in Caenorhabditis elegans. Genetics 135, 385-404. (Pubitemid 23307595)
44. Okreglak V, Drubin DG (2010). Loss of Aip1 reveals a role in maintaining the actin monomer pool and an in vivo oligomer assembly pathway. J Cell Biol 188, 769-777.
45. 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. (Pubitemid 36622304)
46. Ono K, Yamashiro S, Ono S (2008). Essential role of ADF/cofilin for assembly of contractile actin networks in the C. elegans somatic gonad. J Cell Sci 121, 2662-2670.
47. 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.
48. Ono S (2003). Regulation of actin filament dynamics by actin depolymerizing factor/cofilin and actin-interacting protein 1: new blades for twisted filaments. Biochemistry 42, 13363-13370.
49. Ono S (2007). Mechanism of depolymerization and severing of actin filaments and its significance in cytoskeletal dynamics. Int Rev Cytol 258, 1-82.
50. Ono S (2010). Dynamic regulation of sarcomeric actin filaments in striated muscle. Cytoskeleton 67, 677-692.
51. 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. (Pubitemid 29215714)
52. 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. (Pubitemid 28109808)
53. 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.
54. 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. (Pubitemid 24198378)
55. 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. (Pubitemid 38468959)
56. Ono S, Ono K (2002). Tropomyosin inhibits ADF/cofilin-dependent actin filament dynamics. J Cell Biol 156, 1065-1076. (Pubitemid 34839855)
57. Pardee JD, Spudich JA (1982). Purification of muscle actin. Methods Enzymol 85, 164-181.
58. Pollard TD, Cooper JA (2009). Actin, a central player in cell shape and movement. Science 326, 1208-1212.
59. Ren N, Charlton J, Adler PN (2007). The flare gene, which encodes the AIP1 protein of Drosophila, functions to regulate F-actin disassembly in pupal epidermal cells. Genetics 176, 2223-2234. (Pubitemid 47360655)
60. Richmond JE, Davis WS, Jorgensen EM (1999). UNC-13 is required for synaptic vesicle fusion in C. elegans. Nat Neurosci 2, 959-964. (Pubitemid 30599557)
61. 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. (Pubitemid 29293636)
62. Schnorrer F et al. (2010). Systematic genetic analysis of muscle morphogenesis and function in Drosophila. Nature 464, 287-291.
63. Skwarek-Maruszewska A, Hotulainen P, Mattila PK, Lappalainen P (2009). Contractility-dependent actin dynamics in cardiomyocyte sarcomeres. J Cell Sci 122, 2119-2126.
64. Thacker C, Sheps JA, Rose AM (2006). Caenorhabditis elegans dpy-5 is a cuticle procollagen processed by a proprotein convertase. Cell Mol Life Sci 63, 1193-1204. (Pubitemid 43939005)
65. 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. (Pubitemid 32862940)
66. Tischler J, Lehner B, Chen N, Fraser AG (2006). Combinatorial RNA interference in Caenorhabditis elegans reveals that redundancy between gene duplicates can be maintained for more than 80 million years of evolution. Genome Biol 7, R69.
67. Van Troys M, Huyck L, Leyman S, Dhaese S, Vandekerkhove J, Ampe C (2008). Ins and outs of ADF/cofilin activity and regulation. Eur J Cell Biol 87, 649-667.
68. 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. (Pubitemid 34106068)
69. 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. (Pubitemid 24064460)
70. 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. (Pubitemid 41533048)
71. Yonemura I, Mabuchi I (2001). Heterogeneity of mRNA coding for Caenorhabditis elegans coronin-like protein. Gene 271, 255-259. (Pubitemid 32545403)
72. Yu R, 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. (Pubitemid 44673945)