The RNA-binding protein SUP-12 controls muscle-specific splicing of the ADF/cofilin pre-mRNA in C. elegans

Journal of Cell Biology

Volumn 167, Issue 4, 2004, Pages 639-647

  Anyanful, Akwasi ^a   Ono, Kanako ^a   Johnsen, Robert C ^b   Ly, Hinh ^a   Jensen, Victor ^b   Baillie, David L ^b   Ono, Shoichiro ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SIMON FRASER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; COFILIN; GUANINE; ISOPROTEIN; MESSENGER RNA; MUTANT PROTEIN; PROTEIN SUBUNIT; URACIL;

ARTICLE; CAENORHABDITIS ELEGANS; CELL NUCLEUS; GENE MUTATION; INTRON; NONHUMAN; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN MOTIF; RNA BINDING; RNA SPLICING; TISSUE SPECIFICITY; UPREGULATION;

ACTIN DEPOLYMERIZING FACTORS; ACTINS; ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BINDING SITES; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL NUCLEUS; DESTRIN; DNA, COMPLEMENTARY; MICROFILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; MUSCLE DEVELOPMENT; MUSCLES; MUTATION; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RNA PRECURSORS; RNA SPLICE SITES; RNA-BINDING PROTEINS; UP-REGULATION;

CAENORHABDITIS; CAENORHABDITIS ELEGANS;

EID: 9444284320     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200407085     Document Type: Article

References (60)

1. Bamburg, J.R. 1999. Proteins of the ADF/cofilin family: essential regulators of actin dynamics. Annu. Rev. Cell Dev. Biol. 15:185-230.
2. Bamburg, J.R., A. McGough, and S. Ono. 1999. Putting a new twist on actin: ADF/cofilins modulate actin dynamics. Trends Cell Biol 9:364-370.
3. Bentley, D. 2002. The mRNA assembly line: transcription and processing machines in the same factory. Curr. Opin. Cell Biol. 14:336-342.
4. Black, D.L. 2003. Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 72:291-336.
5. Boy, S., J. Souopgui, M.A. Amato, M. Wegnez, T. Pieler, and M. Perron. 2004. XSEB4R, a novel RNA-binding protein involved in retinal cell differentiation downstream of bHLH proneural genes. Development. 131:851-862.
6. Buratti, E., A. Brindisi, F. Pagani, and F.E. Baralle. 2004. Nuclear factor TDP-43 binds to the polymorphic TG repeats in CFTR intron 8 and causes skipping of exon 9: a functional link with disease penetrance. Am. J. Hum. Genet. 74:1322-1325.
7. elegans Sequencing Consortium. 1998. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science. 282:2012-2018.
8. Dundr, M., and T. Misteli. 2001. Functional architecture in the cell nucleus. Biochem. J. 356:297-310.
9. Epstein, H.F., and J.N. Thomson. 1974. Temperature-sensitive mutation affecting myofilament assembly in Caenorhabditis elegans. Nature. 250:579-580.
10. 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 multi-filament assemblages. J. Cell Biol. 122:845-858.
11. Evans, D., I. Perez, M. MacMorris, D. Leake, C.J. Wilusz, and T. Blumenthal. 2001. A complex containing CstF-64 and the SL2 snRNP connects mRNA 3′ end formation and trans-splicing in C. elegans operons. Genes Dev. 15:2562-2571.
12. Faustino, N.A., and T.A. Cooper. 2003. Pre-mRNA splicing and human disease. Genes Dev. 17:419-437.
13. Fetka, I., A. Radeghieri, and T. Bouwmeester. 2000. Expression of the RNA recognition motif-containing protein SEB-4 during Xenopus embryonic development. Mech. Dev. 94:283-286.
14. Francis, G.R., and R.H. Waterston. 1985. Muscle organization in Caenorhabditis elegans: localization of proteins implicated in thin filament attachment and I-band organization. J. Cell Biol. 101:1532-1549.
15. Gillett, G.T., M.F. Fox, P.S. Rowe, C.M. Casimir, and S. Povey. 1996. Mapping of human non-muscle type cofilin (CFL1) to chromosome 11q13 and muscle-type cofilin (CFL2) to chromosome 14. Ann. Hum. Genet. 60:201-211.
16. 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.
17. Ho, T.H., B.N. Charlet, M.G. Poulos, G. Singh, M.S. Swanson, and T.A. Cooper. 2004. Muscleblind proteins regulate alternative splicing. EMBO J. 23:3103-3112.
18. Jurica, M.S., and M.J. Moore. 2003. Pre-mRNA splicing: awash in a sea of proteins. Mol. Cell. 12:5-14.
19. Kanadia, R.N., K.A. Johnstone, A. Mankodi, C. Lungu, C.A. Thornton, D. Esson, A.M. Timmers, W.W. Hauswirth, and M.S. Swanson. 2003. A muscleblind knockout model for myotonic dystrophy. Science. 302:1978-1980.
20. Lamond, A.I., and D.L. Spector. 2003. Nuclear speckles: a model for nuclear organelles. Nat. Rev. Mol. Cell Biol. 4:605-612.
21. Lappalainen, P., and D.G. Drubin. 1997. Cofilin promotes rapid actin filament turnover in vivo. Nature. 388:78-82.
22. Lee, M.H., and T. Schedl. 2001. Identification of in vivo mRNA targets of GLD-1, a maxi-KH motif containing protein required for C. elegans germ cell development. Genes Dev. 15:2408-2420.
23. Lundquist, E.A., R.K. Herman, T.M. Rogalski, G.P. Mullen, D.G. Moerman, and J.E. Shaw. 1996. The mec-8 gene of C. elegans encodes a protein with two RNA recognition motifs and regulates alternative splicing of unc-52 transcripts. Development. 122:1601-1610.
24. Maciver, S.K., and P.J. Hussey. 2002. The ADF/cofflin family: actin-remodeling proteins. Genome Biol. 3:reviews3007.
25. Maniatis, T., and B. Tasic. 2002. Alternative pre-mRNA splicing and proteome expansion in metazoans. Nature. 418:236-243.
26. Matsuzaki, F., S. Matsumoto, I. Yahara, N. Yonezawa, E. Nishida, and H. Sakai. 1988. Cloning and characterization of porcine brain cofilin cDNA. Cofilin contains the nuclear transport signal sequence. J. Biol. Chem. 263:11564-11568.
27. McKim, K.S., M.F. Heschl, R.E. Rosenbluth, and D.L. Baillie. 1988. Genetic organization of the unc-60 region in Caenorhabdilis elegans. Genetics. 118:49-59.
28. McKim, K.S., C. Matheson, M.A. Marra, M.F. Wakarchuk, and D.L. Baillie. 1994. The Caenorhabdilis elegans unc-60 gene encodes proteins homologous to a family of actin-binding proteins. Mol. Gen. Genet. 242:346-357.
29. Merendino, L., S. Guth, D. Bilbao, C. Martinez, and J. Valcarcel. 1999. Inhibition of msl-2 splicing by Sex-lethal reveals interaction between U2AF35 and the 3′ splice site AG. Nature. 402:838-841.
30. 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.
31. Misteli, T. 2000. Cell biology of transcription and pre-mRNA splicing: nuclear architecture meets nuclear function. J. Cell Sci. 113:1841-1849.
32. Mittag, M. 1996. Conserved circadian elements in phylogenetically diverse algae. Proc. Natl. Acad. Sci. USA. 93:14401-14404.
33. Mohri, K., and S. Ono. 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.
34. 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.
35. Niksic, M., M. Romano, E. Buratti, F. Pagani, and F.E. Baralle. 1999. Functional analysis of cis-acting elements regulating the alternative splicing of human CFTR exon 9. Hum. Mol Genet. 8:2339-2349.
36. Nilsen, T.W. 2003. The spliceosome: the most complex macromolecular machine in the cell? Bioessays. 25:1147-1149.
37. Nissim-Rafinia, M., and B. Kerem. 2002. Splicing regulation as a potential genetic modifier. Trends Genet. 18:123-127.
38. Okkema, P.G., S.W. Harrison, V. Plunger, A. Aryana, and A. Fire. 1993. Sequence requirements for myosin gene expression and regulation in Caenorhabditis elegans. Genetics. 135:385-404.
39. Ono, S. 1999. Purification and biochemical characterization of actin from Caenorhabdilis elegans: its difference from rabbit muscle actin in the interaction with nematode ADF/cofilin. Cell Motil. Cytoskeleton. 43:128-136.
40. 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.
41. 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.
42. Ono, S., and G.M. Benian. 1998. Two Caenorhabdilis elegans actin depolymerizing factor/cofilin proteins, encoded by the unc-60 gene, differentially regulate actin filament dynamics. J. Biol. Chem. 273:3778-3783.
43. Ono, S., and K. Ono. 2002. Tropomyosin inhibits ADF/cofilin-dependent actin filament dynamics. J. Cell Biol. 156:1065-1076.
44. 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.
45. Ono, S., D.L. Baillie, and G.M. Benian. 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.
46. Ono, K., M. Parast, C. Alberico, G.M. Benian, and S. Ono. 2003. Specific requirement for two ADF/cofilin isoforms in distinct actin-dependent processes in Caenorhabditis elegans. J. Cell Sci. 116:2073-2085.
47. Pagani, F., E. Buratti, C. Stuani, M. Romano, E. Zuccato, M. Niksic, L. Giglio, D. Faraguna, and F.E. Baralle. 2000. Splicing factors induce cystic fibrosis transmembrane regulator exon 9 skipping through a nonevolutionary conserved intronic element. J. Biol. Chem. 275:21041-21047.
48. Shamoo, Y., N. Abdul-Manan, and K.R. Williams. 1995. Multiple RNA binding domains (RBDs) just don't add up. Nucleic Acids Res. 23:725-728.
49. Smith, C.W., and J. Valcarcel. 2000. Alternative pre-mRNA splicing: the logic of combinatorial control. Trends Biochem. Sci. 25:381-388.
50. Spike, C.A., A.G. Davies, J.E. Shaw, and R.K. Herman. 2002. MEC-8 regulates alternative splicing of unc-52 transcripts in C. elegans hypodermal cells. Development. 129:4999-5008.
51. Stoilov, P., E. Meshorer, M. Gencheva, D. Glick, H. Soreq, and S. Stamm. 2002. Defects in pre-mRNA processing as causes of and predisposition to diseases. DNA Cell Biol. 21:803-818.
52. Takahashi, N., N. Sasagawa, K. Suzuki, and S. Ishiura. 2000. The CUG-binding protein binds specifically to UG dinucleotide repeats in a yeast three-hybrid system. Biochem. Biophys. Res. Commun. 277:518-523.
53. Thirion, C., R. Stucka, B. Mendel, A. Gruhler, M. Jaksch, K.J. Nowak, N. Binz, N.G. Laing, and H. Lochmuller. 2001. Characterization of human muscle type cofilin (CFL2) in normal and regenerating muscle. Eur. J. Biochem. 268:3473-3482.
54. Vartiainen, M.K., T. Mustonen, P.K. Mattila, P.J. Ojala, I. Thesleff, J. Partanen, and P. Lappalainen. 2002. The three mouse actin-depolymerizing factor/ cofilins evolved to fulfill cell-type-specific requirements for actin dynamics. Mol. Biol. Cell. 13:183-194.
55. Waterston, R.H. 1988. Muscle. In The Nematode C. elegans. W.B. Wood, editor. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 281-335.
56. Waterston, R.H., J.N. Thomson, and S. Brenner. 1980. Mutants with altered muscle structure of Caenorhabdins elegans. Dev. Biol. 77:271-302.
57. Wicks, S.R., R.T. Yeh, W.R. Gish, R.H. Waterston, and R.H. Plasterk. 2001. Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map. Nat. Genet. 28:160-164.
58. Wu, S., C.M. Romfo, T.W. Nilsen, and M.R. Green. 1999. Functional recognition of the 3′ splice site AG by the splicing factor U2AF35. Nature. 402: 832-835.
59. Zengel, J.M., and H.F. Epstein. 1980. Identification of genetic elements associated with muscle structure in the nematode Caenorhabditis elegans. Cell Motil. 1:73-97.
60. Zorio, D.A., and T. Blumenthal. 1999. Both subunits of U2AF recognize the 3′ splice site in Caenorhabditis elegans. Nature. 402:835-838.