RBFOX and SUP-12 sandwich a G base to cooperatively regulate tissue-specific splicing

Nature Structural and Molecular Biology

Volumn 21, Issue 9, 2014, Pages 778-786

  Kuwasako, Kanako ^a,b   Takahashi, Mari ^a   Unzai, Satoru ^c   Tsuda, Kengo ^a   Yoshikawa, Seiko ^a   He, Fahu ^a   Kobayashi, Naohiro ^a,d   Güntert, Peter ^a,e,f,g   Shirouzu, Mikako ^a   Ito, Takuhiro ^a   Tanaka, Akiko ^a   Yokoyama, Shigeyuki ^a   Hagiwara, Masatoshi ^h,i   Kuroyanagi, Hidehito ^h   Muto, Yutaka ^a,b  

^a RIKEN   (Japan)

^b MUSASHINO UNIVERSITY   (Japan)

^c YOKOHAMA CITY UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY   (Japan)

^e GOETHE UNIVERSITY   (Germany)

^f FRANKFURT INSTITUTE FOR ADVANCED STUDIES   (Germany)

^g TOKYO METROPOLITAN UNIVERSITY   (Japan)

^h TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

ⁱ KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ASD1 PROTEIN; CIS ACTING ELEMENT; EGL 15 PROTEIN; MESSENGER RNA PRECURSOR; RBFOX PROTEIN; RNA; RNA BINDING PROTEIN; RNA RECOGNITION MOTIF; SUP12 PROTEIN; TERNARY COMPLEX FACTOR; UNCLASSIFIED DRUG; ASD-1 PROTEIN, C ELEGANS; CAENORHABDITIS ELEGANS PROTEIN; SUP-12 PROTEIN, C ELEGANS;

ALTERNATIVE RNA SPLICING; ARTICLE; BASE PAIRING; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; IN VIVO STUDY; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RNA BINDING; TISSUE SPECIFICITY; ANIMAL; CAENORHABDITIS ELEGANS; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; NUCLEOTIDE SEQUENCE; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

CAENORHABDITIS ELEGANS;

ALTERNATIVE SPLICING; ANIMALS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY; RNA; RNA-BINDING PROTEINS;

EID: 84921948299     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2870     Document Type: Article

References (49)

1. Pan, Q., Shai, O., Lee, L.J., Frey, B.J. & Blencowe, B.J. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat. Genet. 40, 1413-1415 (2008).
2. Cáceres, J.F. & Kornblihtt, A.R. Alternative splicing: multiple control mechanisms and involvement in human disease. Trends Genet. 18, 186-193 (2002).
3. Faustino, N.A. & Cooper, T.A. Pre-mRNA splicing and human disease. Genes Dev. 17, 419-437 (2003).
4. Busch, A. & Hertel, K.J. Evolution of SR protein and hnRNP splicing regulatory factors. Wiley Interdiscip. Rev. RNA 3, 1-12 (2012).
5. Chen, Y.I. Et al. Proteomic analysis of in vivo-assembled pre-mRNA splicing complexes expands the catalog of participating factors. Nucleic Acids Res. 35, 3928-3944 (2007).
6. Ruskin, B., Zamore, P.D. & Green, M.R. A factor, U2AF, is required for U2 snRNP binding and splicing complex assembly. Cell 52, 207-219 (1988).
7. Wang, E.T. Et al. Alternative isoform regulation in human tissue transcriptomes. Nature 456, 470-476 (2008).
8. Wu, S., Romfo, C.M., Nilsen, T.W. & Green, M.R. Functional recognition of the 3′ splice site AG by the splicing factor U2AF35. Nature 402, 832-835 (1999).
9. Zhuang, Y. & Weiner, A.M. A compensatory base change in U1 snRNA suppresses a 5′ splice site mutation. Cell 46, 827-835 (1986).
10. Kuroyanagi, H. Fox-1 family of RNA-binding proteins. Cell. Mol. Life Sci. 66, 3895-3907 (2009).
11. Auweter, S.D. Et al. Molecular basis of RNA recognition by the human alternative splicing factor Fox-1. EMBO J. 25, 163-173 (2006).
12. Castle, J.C. Et al. Expression of 24,426 human alternative splicing events and predicted cis regulation in 48 tissues and cell lines. Nat. Genet. 40, 1416-1425 (2008).
13. Das, D. Et al. A correlation with exon expression approach to identify cis-regulatory elements for tissue-specific alternative splicing. Nucleic Acids Res. 35, 4845-4857 (2007).
14. Minovitsky, S., Gee, S.L., Schokrpur, S., Dubchak, I. & Conboy, J.G. The splicing regulatory element, UGCAUG, is phylogenetically and spatially conserved in introns that flank tissue-specific alternative exons. Nucleic Acids Res. 33, 714-724 (2005).
15. Sugnet, C.W. Et al. Unusual intron conservation near tissue-regulated exons found by splicing microarrays. PLoS Comput. Biol. 2, e4 (2006).
16. Takeuchi, A., Hosokawa, M., Nojima, T. & Hagiwara, M. Splicing reporter mice revealed the evolutionally conserved switching mechanism of tissue-specific alternative exon selection. PLoS ONE 5, e10946 (2010).
17. Underwood, J.G., Boutz, P.L., Dougherty, J.D., Stoilov, P. & Black, D.L. Homologues of the Caenorhabditis elegans Fox-1 protein are neuronal splicing regulators in mammals. Mol. Cell. Biol. 25, 10005-10016 (2005).
18. Kim, K.K., Adelstein, R.S. & Kawamoto, S. Identification of neuronal nuclei (NeuN) as Fox-3, a new member of the Fox-1 gene family of splicing factors. J. Biol. Chem. 284, 31052-31061 (2009).
19. Zhang, C. Et al. Defining the regulatory network of the tissue-specific splicing factors Fox-1 and Fox-2. Genes Dev. 22, 2550-2563 (2008).
20. Yeo, G.W. Et al. An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells. Nat. Struct. Mol. Biol. 16, 130-137 (2009).
21. Goodman, S.J., Branda, C.S., Robinson, M.K., Burdine, R.D. & Stern, M.J. Alternative splicing affecting a novel domain in the C. Elegans EGL-15 FGF receptor confers functional specificity. Development 130, 3757-3766 (2003).
22. Birnbaum, D., Popovici, C. & Roubin, R. A pair as a minimum: the two fibroblast growth factors of the nematode Caenorhabditis elegans. Dev. Dyn. 232, 247-255 (2005).
23. Burdine, R.D., Branda, C.S. & Stern, M.J. EGL-17(FGF) expression coordinates the attraction of the migrating sex myoblasts with vulval induction in C. Elegans. Development 125, 1083-1093 (1998).
24. Burdine, R.D., Chen, E.B., Kwok, S.F. & Stern, M.J. Egl-17 encodes an invertebrate fibroblast growth factor family member required specifically for sex myoblast migration in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 94, 2433-2437 (1997).
25. DeVore, D.L., Horvitz, H.R. & Stern, M.J. An FGF receptor signaling pathway is required for the normal cell migrations of the sex myoblasts in C. Elegans hermaphrodites. Cell 83, 611-620 (1995).
26. Kuroyanagi, H., Kobayashi, T., Mitani, S. & Hagiwara, M. Transgenic alternative-splicing reporters reveal tissue-specific expression profiles and regulation mechanisms in vivo. Nat. Methods 3, 909-915 (2006).
27. Kuroyanagi, H., Ohno, G., Mitani, S. & Hagiwara, M. The Fox-1 family and SUP-12 coordinately regulate tissue-specific alternative splicing in vivo. Mol. Cell. Biol. 27, 8612-8621 (2007).
28. Anyanful, A. Et al. 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 (2004).
29. Leeper, T.C., Qu, X., Lu, C., Moore, C. & Varani, G. Novel protein-protein contacts facilitate mRNA 3′-processing signal recognition by Rna15 and Hrp1. J. Mol. Biol. 401, 334-349 (2010).
30. Handa, N. Et al. Structural basis for recognition of the tra mRNA precursor by the Sex-lethal protein. Nature 398, 579-585 (1999).
31. Kuroyanagi, H., Watanabe, Y. & Hagiwara, M. CELF family RNA-binding protein UNC-75 regulates two sets of mutually exclusive exons of the unc-32 gene in neuron-specific manners in Caenorhabditis elegans. PLoS Genet. 9, e1003337 (2013).
32. Kuroyanagi, H., Watanabe, Y., Suzuki, Y. & Hagiwara, M. Position-dependent and neuron-specific splicing regulation by the CELF family RNA-binding protein UNC-75 in Caenorhabditis elegans. Nucleic Acids Res. 41, 4015-4025 (2013).
33. Damianov, A. & Black, D.L. Autoregulation of Fox protein expression to produce dominant negative splicing factors. RNA 16, 405-416 (2010).
34. Kuroyanagi, H. Switch-like regulation of tissue-specific alternative pre-mRNA processing patterns revealed by customized fluorescence reporters. Worm 2, e23834 (2013).
35. Ohno, G. Et al. Muscle-specific splicing factors ASD-2 and SUP-12 cooperatively switch alternative pre-mRNA processing patterns of the ADF/Cofilin gene in Caenorhabditis elegans. PLoS Genet. 8, e1002991 (2012).
36. Ohno, G., Hagiwara, M. & Kuroyanagi, H. STAR family RNA-binding protein ASD-2 regulates developmental switching of mutually exclusive alternative splicing in vivo. Genes Dev. 22, 360-374 (2008).
37. Kuwasako, K. Et al. Solution structures of the SURP domains and the subunit-assembly mechanism within the splicing factor SF3a complex in 17S U2 snRNP. Structure 14, 1677-1689 (2006).
38. Delaglio, F. Et al. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 (1995).
39. Johnson, B.A. Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol. 278, 313-352 (2004).
40. Kobayashi, N. Et al. KUJIRA, a package of integrated modules for systematic and interactive analysis of NMR data directed to high-throughput NMR structure studies. J. Biomol. NMR 39, 31-52 (2007).
41. Güntert, P. Automated NMR structure calculation with CYANA. Methods Mol. Biol. 278, 353-378 (2004).
42. Cornilescu, G., Delaglio, F. & Bax, A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13, 289-302 (1999).
43. Case, D.A. Et al. The Amber biomolecular simulation programs. J. Comput. Chem. 26, 1668-1688 (2005).
44. Duan, Y. Et al. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J. Comput. Chem. 24, 1999-2012 (2003).
45. Tsuda, K. Et al. Structural basis for the dual RNA-recognition modes of human Tra2-β RRM. Nucleic Acids Res. 39, 1538-1553 (2011).
46. Zweckstetter, M. NMR: prediction of molecular alignment from structure using the PALES software. Nat. Protoc. 3, 679-690 (2008).
47. Laskowski, R.A., Rullmannn, J.A., MacArthur, M.W., Kaptein, R. & Thornton, J.M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8, 477-486 (1996).
48. Koradi, R., Billeter, M. & Wuthrich, K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14, 51-55, 29-32 (1996).
49. Kuroyanagi, H., Ohno, G., Sakane, H., Maruoka, H. & Hagiwara, M. Visualization and genetic analysis of alternative splicing regulation in vivo using fluorescence reporters in transgenic Caenorhabditis elegans. Nat. Protoc. 5, 1495-1517 (2010).