hnRNP H and hnRNP F complex with Fox2 to silence fibroblast growth factor receptor 2 exon IIIc

Molecular and Cellular Biology

Volumn 28, Issue 17, 2008, Pages 5403-5419

  Mauger, David M ^a   Lin, Carolina ^a   Garcia Blanco, Mariano A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASF SF2 PROTEIN; FIBROBLAST GROWTH FACTOR RECEPTOR 2; FOX2 PROTEIN; NUCLEAR RIBONUCLEOPROTEIN F; NUCLEAR RIBONUCLEOPROTEIN H; PROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; EMBRYO; EXON; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN MOTIF; RNA INTERFERENCE; RNA SPLICING;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BINDING, COMPETITIVE; CELL LINE; CONSERVED SEQUENCE; DNA MUTATIONAL ANALYSIS; EXONS; GENE SILENCING; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP F-H; HUMANS; IMMUNOPRECIPITATION; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEIN BINDING; RATS; RECEPTOR, FIBROBLAST GROWTH FACTOR, TYPE 2; REGULATORY SEQUENCES, NUCLEIC ACID; REPRESSOR PROTEINS; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 50249176008     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00739-08     Document Type: Article

References (40)

1. Abdul-Manan, N., S. M. O'Malley, and K. R. Williams. 1996. Origins of binding specificity of the A1 heterogeneous nuclear ribonucleoprotein. Biochemistry 35:3545-3554.
2. An, P., and P. J. Grabowski. 2007. Exon silencing by UAGG motifs in response to neuronal excitation. PLoS Biol. 5:e36.
3. Auweter, S. D., R. Fasan, L. Reymond, J. G. Underwood, D. L. Black, S. Pitsch, and F. H. Allain. 2006. Molecular basis of RNA recognition by the human alternative splicing factor Fox-1. EMBO J. 25:163-173.
4. Baraniak, A. P., J. R. Chen, and M. A. Garcia-Blanco. 2006. Fox-2 mediates epithelial cell-specific fibroblast growth factor receptor 2 exon choice. Mol. Cell. Biol. 26:1209-1222.
5. Black, D. L. 2003. Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 72:291-336.
6. Caputi, M., and A. M. Zahler. 2001. Determination of the RNA binding specificity of the heterogeneous nuclear ribonucleoprotein (hnRNP) H/H′/F/2H9 family. J. Biol. Chem. 276:43850-43859.
7. Caputi, M., and A. M. Zahler. 2002. SR proteins and hnRNP H regulate the splicing of the HIV-1 tev-specific exon 6D. EMBO J. 21:845-855.
8. Carstens, R. P., J. V. Eaton, H. R. Krigman, P. J. Walther, and M. A. Garcia-Blanco. 1997. Alternative splicing of fibroblast growth factor receptor 2 (FGF-R2) in human prostate cancer. Oncogene 15:3059-3065.
9. Carstens, R. P., W. L. McKeehan, and M. A. Garcia-Blanco. 1998. An intronic sequence element mediates both activation and repression of rat fibroblast growth factor receptor 2 pre-mRNA splicing. Mol. Cell. Biol. 18:2205-2217.
10. Carstens, R. P., E. J. Wagner, and M. A. Garcia-Blanco. 2000. An intronic splicing silencer causes skipping of the IIIb exon of fibroblast growth factor receptor 2 through involvement of polypyrimidine tract binding protein. Mol. Cell. Biol. 20:7388-7400.
11. Cartegni, L., and A. R. Krainer. 2002. Disruption of an SF2/ASF-dependent exonic splicing enhancer in SMN2 causes spinal muscular atrophy in the absence of SMN1. Nat. Genet. 30:377-384.
12. Cartegni, L., J. Wang, Z. Zhu, M. Q. Zhang, and A. R. Krainer. 2003. ESEfinder: a Web resource to identify exonic splicing enhancers. Nucleic Acids Res. 31:3568-3571.
13. Champion-Arnaud, P., C. Ronsin, E. Gilbert, M. C. Gesnel, E. Houssaint, and R. Breathnach. 1991. Multiple mRNAs code for proteins related to the BEK fibroblast growth factor receptor. Oncogene 6:979-987.
14. Chen, C. D., R. Kobayashi, and D. M. Helfman. 1999. Binding of hnRNP H to an exonic splicing silencer is involved in the regulation of alternative splicing of the rat beta-tropomyosin gene. Genes Dev. 13:593-606.
15. Chou, M. Y., N. Rooke, C. W. Turck, and D. L. Black. 1999. hnRNP H is a component of a splicing enhancer complex that activates a c-src alternative exon in neuronal cells. Mol. Cell. Biol. 19:69-77.
16. Crawford, J. B., and J. G. Patton. 2006. Activation of alpha-tropomyosin exon 2 is regulated by the SR protein 9G8 and heterogeneous nuclear ribonucleoproteins H and F. Mol. Cell. Biol. 26:8791-8802.
17. Del Gatto-Konczak, F., M. Olive, M. C. Gesnel, and R. Breathnach. 1999. hnRNP A1 recruited to an exon in vivo can function as an exon splicing silencer. Mol. Cell. Biol. 19:251-260.
18. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
19. Dominguez, C., and F. H. Allain. 2006. NMR structure of the three quasi RNA recognition motifs (qRRMs) of human hnRNP F and interaction studies with Bcl-x G-tract RNA: a novel mode of RNA recognition. Nucleic Acids Res. 34:3634-3645.
20. Domsic, J. K., Y. Wang, A. Mayeda, A. R. Krainer, and C. M. Stoltzfus. 2003. Human immunodeficiency virus type 1 hnRNP A/B-dependent exonic splicing silencer ESSV antagonizes binding of U2AF65 to viral polypyrimidine tracts. Mol. Cell. Biol. 23:8762-8772.
21. Expert-Bezancon, A., A. Sureau, P. Durosay, R. Salesse, H. Groeneveld, J. P. Lecaer, and J. Marie. 2004. hnRNP A1 and the SR proteins ASF/SF2 and SC35 have antagonistic functions in splicing of beta-tropomyosin exon 6B. J. Biol. Chem. 279:38249-38259.
22. Garneau, D., T. Revil, J. F. Fisette, and B. Chabot. 2005. Heterogeneous nuclear ribonucleoprotein F/H proteins modulate the alternative splicing of the apoptotic mediator Bcl-x. J. Biol. Chem. 280:22641-22650.
23. Han, K., G. Yeo, P. An, C. B. Burge, and P. J. Grabowski. 2005. A combinatorial code for splicing silencing: UAGG and GGGG motifs. PLoS Biol. 3:e158.
24. Jacquenet, S., A. Mereau, P. S. Bilodeau, L. Damier, C. M. Stoltzfus, and C. Branlant. 2001. A second exon splicing silencer within human immunodeficiency virus type 1 tat exon 2 represses splicing of Tat mRNA and binds protein hnRNP H. J. Biol. Chem. 276:40464-40475.
25. Liu, H. X., L. Cartegni, M. Q. Zhang, and A. R. Krainer. 2001. A mechanism for exon skipping caused by nonsense or missense mutations in BRCA1 and other genes. Nat. Genet. 27:55-58.
26. Martinez-Contreras, R., J. F. Fisette, F. U. Nasim, R. Madden, M. Cordeau, and B. Chabot. 2006. Intronic binding sites for hnRNP A/B and hnRNP F/H proteins stimulate pre-mRNA splicing. PLoS Biol. 4:e21.
27. Mayeda, A., S. H. Munroe, J. F. Caceres, and A. R. Krainer. 1994. Function of conserved domains of hnRNP A1 and other hnRNP A/B proteins. EMBO J. 13:5483-5495.
28. Mayeda, A., S. H. Munroe, R. M. Xu, and A. R. Krainer. 1998. Distinct functions of the closely related tandem RNA-recognition motifs of hnRNP A1. RNA 4:1111-1123.
29. Min, H., R. C. Chan, and D. L. Black. 1995. The generally expressed hnRNP F is involved in a neural-specific pre-mRNA splicing event. Genes Dev. 9:2659-2671.
30. Rooke, N., V. Markovtsov, E. Cagavi, and D. L. Black. 2003. Roles for SR proteins and hnRNP A1 in the regulation of c-src exon N1. Mol. Cell. Biol. 23:1874-1884.
31. Smith, P. J., E. L. Spurrell, J. Coakley, C. J. Hinds, R. J. Ross, A. R. Krainer, and S. L. Chew. 2002. An exonic splicing enhancer in human IGF-I pre-mRNA mediates recognition of alternative exon 5 by the serine-arginine protein splicing factor-2/alternative splicing factor. Endocrinology 143:146- 154.
32. Smith, P. J., C. Zhang, J. Wang, S. L. Chew, M. Q. Zhang, and A. R. Krainer. 2006. An increased specificity score matrix for the prediction of SF2/ASF-specific exonic splicing enhancers. Hum. Mol. Genet. 15:2490-2508.
33. Wagner, E. J., and M. A. Garcia-Blanco. 2001. Polypyrimidine tract binding protein antagonizes exon definition. Mol. Cell. Biol. 21:3281-3288.
34. Wang, E., N. Dimova, and F. Cambi. 2007. PLP/DM20 ratio is regulated by hnRNPH and F and a novel G-rich enhancer in oligodendrocytes. Nucleic Acids Res. 35:4164-4178.
35. Wang, J., P. J. Smith, A. R. Krainer, and M. Q. Zhang. 2005. Distribution of SR protein exonic splicing enhancer motifs in human protein-coding genes. Nucleic Acids Res. 33:5053-5062.
36. Wang, Z., M. E. Rolish, G. Yeo, V. Tung, M. Mawson, and C. B. Burge. 2004. Systematic identification and analysis of exonic splicing silencers. Cell 119: 831-845.
37. Woppmann, A., C. L. Will, U. Kornstadt, P. Zuo, J. L. Manley, and R. Luhrmann. 1993. Identification of an snRNP-associated kinase activity that phosphorylates arginine/serine rich domains typical of splicing factors. Nucleic Acids Res. 21:2815-2822.
38. Xiao, S. H., and J. L. Manley. 1997. Phosphorylation of the ASF/SF2 RS domain affects both protein-protein and protein-RNA interactions and is necessary for splicing. Genes Dev. 11:334-344.
39. Zahler, A. M., C. K. Damgaard, J. Kjems, and M. Caputi. 2004. SC35 and heterogeneous nuclear ribonucleoprotein A/B proteins bind to a juxtaposed exonic splicing enhancer/exonic splicing silencer element to regulate HIV-1 tat exon 2 splicing. J. Biol. Chem. 279:10077-10084.
40. Zhu, J., A. Mayeda, and A. R. Krainer. 2001. Exon identity established through differential antagonism between exonic splicing silencer-bound hnRNP A1 and enhancer-bound SR proteins. Mol. Cell 8:1351-1361.