Generation of functionally distinct isoforms of PTBP3 by alternative splicing and translation initiation

Nucleic Acids Research

Volumn 43, Issue 11, 2015, Pages 5586-5600

  Tan, Lit Yeen ^a   Whitfield, Peter ^a   Llorian, Miriam ^a   Monzon Casanova, Elisa ^a,b   Diaz Munoz, Manuel D ^b   Turner, Martin ^b   Smith, Christopher W J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHYMOTRYPSIN; ISOPROTEIN; POLYPYRIMIDINE TRACT BINDING PROTEIN; POLYPYRIMIDINE TRACT BINDING PROTEIN 1; POLYPYRIMIDINE TRACT BINDING PROTEIN 2; POLYPYRIMIDINE TRACT BINDING PROTEIN 3; UNCLASSIFIED DRUG; PTBP3 PROTEIN, HUMAN; RNA; START CODON;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELLULAR DISTRIBUTION; CODON; CONTROLLED STUDY; GENE; HUMAN; HUMAN CELL; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PTBP1 GENE; PTBP2 GENE; PTBP3 GENE; REAL TIME POLYMERASE CHAIN REACTION; RNA BINDING; RNA RECOGNITION MOTIF DOMAIN; TRANSLATION INITIATION; UPREGULATION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; GENETICS; K562 CELL LINE; METABOLISM; RNA TRANSLATION; START CODON;

VERTEBRATA;

ALTERNATIVE SPLICING; ANIMALS; CELLS, CULTURED; CODON, INITIATOR; HUMANS; K562 CELLS; MICE, INBRED C57BL; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; POLYPYRIMIDINE TRACT-BINDING PROTEIN; PROTEIN ISOFORMS; RNA;

EID: 84936792238     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv429     Document Type: Article

References (43)

1. Jangi, M. and Sharp, P.A. (2014) Building robust transcriptomes with master splicing factors. Cell, 159, 487-498.
2. Garcia-Blanco, M.A., Jamison, S.F. and Sharp, P.A. (1989) Identification and purification of a 62, 000-dalton protein that binds specifically to the polypyrimidine tract of introns. Genes Dev., 3, 1874-1886.
3. Patton, J.G., Mayer, S.A., Tempst, P. and Nadal-Ginard, B. (1991) Characterization and molecular cloning of polypyrimidine tract-binding protein: a component of a complex necessary for pre-mRNA splicing. Genes Dev., 5, 1237-1251.
4. Perez, I., Lin, C.H., McAfee, J.G. and Patton, J.G. (1997) Mutation of PTB binding sites causes misregulation of alternative 3-splice site selection in vivo. RNA, 3, 764-778.
5. Singh, R., Valcarcel, J. and Green, M.R. (1995) Distinct binding specificities and functions of higher eukaryotic polypyrimidine tract-binding proteins. Science, 268, 1173-1176.
6. Llorian, M., Schwartz, S., Clark, T.A., Hollander, D., Tan, L.Y., Spellman, R., Gordon, A., Schweitzer, A.C., de la Grange, P., Ast, G. et al. (2010) Position-dependent alternative splicing activity revealed by global profiling of alternative splicing events regulated by PTB. Nat. Struct. Mol. Biol., 17, 1114-1123.
7. Xue, Y., Zhou, Y., Wu, T., Zhu, T., Ji, X., Kwon, Y.S., Zhang, C., Yeo, G., Black, D.L., Sun, H. et al. (2009) Genome-wide analysis of PTB-RNA interactions reveals a strategy used by the general splicing repressor to modulate exon inclusion or skipping. Mol. Cell, 36, 996-1006.
8. Licatalosi, D.D., Yano, M., Fak, J.J., Mele, A., Grabinski, S.E., Zhang, C. and Darnell, R.B. (2012) Ptbp2 represses adult-specific splicing to regulate the generation of neuronal precursors in the embryonic brain. Genes Dev., 26, 1626-1642.
9. Yap, K., Lim, Z.Q., Khandelia, P., Friedman, B. and Makeyev, E.V. (2012) Coordinated regulation of neuronal mRNA steady-state levels through developmentally controlled intron retention. Genes Dev., 26, 1209-1223.
10. Sawicka, K., Bushell, M., Spriggs, K.A. and Willis, A.E. (2008) Polypyrimidine-tract-binding protein: a multifunctional RNA-binding protein. Biochem. Soc. Trans., 36, 641-647.
11. Knoch, K.P., Bergert, H., Borgonovo, B., Saeger, H.D., Altkruger, A., Verkade, P. and Solimena, M. (2004) Polypyrimidine tract-binding protein promotes insulin secretory granule biogenesis. Nat. Cell Biol., 6, 207-214.
12. Xie, J., Lee, J.A., Kress, T.L., Mowry, K.L. and Black, D.L. (2003) Protein kinase A phosphorylation modulates transport of the polypyrimidine tract-binding protein. Proc. Natl. Acad. Sci. U.S.A., 100, 8776-8781.
13. Knoch, K.P., Meisterfeld, R., Kersting, S., Bergert, H., Altkruger, A., Wegbrod, C., Jager, M., Saeger, H.D. and Solimena, M. (2006) cAMP-dependent phosphorylation of PTB1 promotes the expression of insulin secretory granule proteins in beta cells. Cell Metab., 3, 123-134.
14. Keppetipola, N., Sharma, S., Li, Q. and Black, D.L. (2012) Neuronal regulation of pre-mRNA splicing by polypyrimidine tract binding proteins, PTBP1 and PTBP2. Crit. Rev. Biochem. Mol. Biol., 47, 360-378.
15. Boutz, P.L., Stoilov, P., Li, Q., Lin, C.H., Chawla, G., Ostrow, K., Shiue, L., Ares, M. Jr and Black, D.L. (2007) A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons. Genes Dev., 21, 1636-1652.
16. Makeyev, E.V., Zhang, J., Carrasco, M.A. and Maniatis, T. (2007) The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell, 27, 435-448.
17. Spellman, R., Llorian, M. and Smith, C.W. (2007) Crossregulation and functional redundancy between the splicing regulator PTB and its paralogs nPTB and ROD1. Mol. Cell, 27, 420-434.
18. Li, Q., Zheng, S., Han, A., Lin, C.H., Stoilov, P., Fu, X.D. and Black, D.L. (2014) The splicing regulator PTBP2 controls a program of embryonic splicing required for neuronal maturation. eLife, 3, e01201.
19. Yamamoto, H., Tsukahara, K., Kanaoka, Y., Jinno, S. and Okayama, H. (1999) Isolation of a mammalian homologue of a fission yeast differentiation regulator. Mol. Cell Biol., 19, 3829-3841.
20. Robinson, F., Jackson, R.J. and Smith, C.W. (2008) Expression of human nPTB is limited by extreme suboptimal codon content. PLoS One, 3, e1801.
21. Brazao, T.F., Demmers, J., van, I.W., Strouboulis, J., Fornerod, M., Romao, L. and Grosveld, F.G. (2012) A new function of ROD1 in nonsense-mediated mRNA decay. FEBS Lett., 586, 1101-1110.
22. Wollerton, M.C., Gooding, C., Wagner, E.J., Garcia-Blanco, M.A. and Smith, C.W. (2004) Autoregulation of polypyrimidine tract binding protein by alternative splicing leading to nonsense-mediated decay. Mol. Cell, 13, 91-100.
23. Wagner, E.J. and Garcia-Blanco, M.A. (2001) Polypyrimidine tract binding protein antagonizes exon definition. Mol. Cell Biol., 21, 3281-3288.
24. Izquierdo, J.M., Majos, N., Bonnal, S., Martinez, C., Castelo, R., Guigo, R., Bilbao, D. and Valcarcel, J. (2005) Regulation of Fas alternative splicing by antagonistic effects of TIA-1 and PTB on exon definition. Mol. Cell, 19, 475-484.
25. Mickleburgh, I., Kafasla, P., Cherny, D., Llorian, M., Curry, S., Jackson, R.J. and Smith, C.W. (2014) The organization of RNA contacts by PTB for regulation of FAS splicing. Nucleic Acids Res., 42, 8605-8620.
26. Mercer, T.R., Clark, M.B., Andersen, S.B., Brunck, M.E., Haerty, W., Crawford, J., Taft, R.J., Nielsen, L.K., Dinger, M.E. and Mattick, J.S. (2015) Genome-wide discovery of human splicing branchpoints. Genome Res., 25, 290-303.
27. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R. and Salzberg, S.L. (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol., 14, R36.
28. Diaz-Munoz, M.D., Bell, S.E., Fairfax, K., Monzon-Casanova, E., Cunningham, A.F., Gonzalez-Porta, M., Andrews, S.R., Bunik, V.I., Zarnack, K., Curk, T. et al. (2015) The RNA-binding protein HuR is essential for the B cell antibody response. Nat. Immunol., 16, 415-425.
29. Thorvaldsdottir, H., Robinson, J.T. and Mesirov, J.P. (2013) Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform., 14, 178-192.
30. Kozak, M. (2002) Pushing the limits of the scanning mechanism for initiation of translation. Gene, 299, 1-34.
31. Jackson, R.J., Hellen, C.U. and Pestova, T.V. (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol., 11, 113-127.
32. Ghetti, A., Pinol-Roma, S., Michael, W.M., Morandi, C. and Dreyfuss, G. (1992) hnRNP I, the polypyrimidine tract-binding protein: distinct nuclear localization and association with hnRNAs. Nucleic Acids Res., 20, 3671-3678.
33. Romanelli, M.G., Weighardt, F., Biamonti, G., Riva, S. and Morandi, C. (1997) Sequence determinants for hnRNP I protein nuclear localization. Exp. Cell Res., 235, 300-304.
34. Barbosa, C., Peixeiro, I. and Romao, L. (2013) Gene expression regulation by upstream open reading frames and human disease. PLoS Genet., 9, e1003529.
35. Andrews, S.J. and Rothnagel, J.A. (2014) Emerging evidence for functional peptides encoded by short open reading frames. Nat. Rev. Genet., 15, 193-204.
36. Damianov, A. and Black, D.L. (2010) Autoregulation of Fox protein expression to produce dominant negative splicing factors. RNA, 16, 405-416.
37. Kim, M.S., Pinto, S.M., Getnet, D., Nirujogi, R.S., Manda, S.S., Chaerkady, R., Madugundu, A.K., Kelkar, D.S., Isserlin, R., Jain, S. et al. (2014) A draft map of the human proteome. Nature, 509, 575-581.
38. Wolfe, A.L., Singh, K., Zhong, Y., Drewe, P., Rajasekhar, V.K., Sanghvi, V.R., Mavrakis, K.J., Jiang, M., Roderick, J.E., Van der Meulen, J. et al. (2014) RNA G-quadruplexes cause eIF4A-dependent oncogene translation in cancer. Nature, 513, 65-70.
39. Jangi, M., Boutz, P.L., Paul, P. and Sharp, P.A. (2014) Rbfox2 controls autoregulation in RNA-binding protein networks. Genes Dev., 28, 637-651.
40. Oberdoerffer, S., Moita, L.F., Neems, D., Freitas, R.P., Hacohen, N. and Rao, A. (2008) Regulation of CD45 alternative splicing by heterogeneous ribonucleoprotein, hnRNPLL. Science, 321, 686-691.
41. Rossbach, O., Hung, L.H., Schreiner, S., Grishina, I., Heiner, M., Hui, J. and Bindereif, A. (2009) Auto-and cross-regulation of the hnRNP L proteins by alternative splicing. Mol. Cell Biol., 29, 1442-1451.
42. Shankarling, G. and Lynch, K.W. (2013) Minimal functional domains of paralogues hnRNP L and hnRNP LL exhibit mechanistic differences in exonic splicing repression. Biochem. J., 453, 271-279.
43. Topp, J.D., Jackson, J., Melton, A.A. and Lynch, K.W. (2008) A cell-based screen for splicing regulators identifies hnRNP LL as a distinct signal-induced repressor of CD45 variable exon 4. RNA, 14, 2038-2049.