The RNA recognition motif protein RBM11 is a novel tissue-specific splicing regulator

Nucleic Acids Research

Volumn 40, Issue 3, 2012, Pages 1021-1032

  Pedrotti, Simona ^a,b   Busà, Roberta ^a,b   Compagnucci, Claudia ^a,b   Sette, Claudio ^a,b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN BCL X; PROTEIN RBM11; REGULATOR PROTEIN; SERINE ARGININE RICH PROTEIN; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CELL STRESS; CEREBELLUM; CONTROLLED STUDY; DIMERIZATION; GENE DELETION; GERM CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; KIDNEY; MOUSE; NERVE CELL; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN TRANSPORT; PUBERTY; REGULATORY MECHANISM; RNA ANALYSIS; RNA BINDING; RNA SPLICING; SEQUENCE HOMOLOGY; TESTIS; TRANSCRIPTION TERMINATION;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANIMALS; BCL-X PROTEIN; CELL NUCLEUS; DIMERIZATION; HEK293 CELLS; HELA CELLS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MUTAGENS; NUCLEAR PROTEINS; OXIDATIVE STRESS; RNA-BINDING PROTEINS;

MAMMALIA;

EID: 84856945928     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr819     Document Type: Article

References (43)

1. Chen, M. and Manley, J. L. (2009) Mechanisms of alternative splicing regulation: insights from molecular and genomics approaches. Nat. Rev. Mol. Cell. Biol., 10, 741-754.
2. Nilsen, T. W. and Graveley, B. R. (2010) Expansion of the eukaryotic proteome by alternative splicing. Nature, 463, 457-463.
3. Black, D. L. (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem., 72, 291-336.
4. Han, S. P., Tang, Y. H. and Smith, R. (2010) Functional diversity of the hnRNPs: past, present and perspectives. Biochem. J., 430, 379-392.
5. Long, J. C. and Caceres, J. F. (2009) The SR protein family of splicing factors: master regulators of gene expression. Biochem. J., 417, 15-27.
6. Yeo, G., Holste, D., Kreiman, G. and Burge, C. B. (2004) Variation in alternative splicing across human tissues. Genome Biol., 5, R74.
7. 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.
8. Sun, S., Zhang, Z., Sinha, R., Karni, R. and Krainer, A. R. (2007) SF2/ASF autoregulation involves multiple layers of post-transcriptional and translational control. Nat. Struct. Mol. Biol., 17, 306-312.
9. Valacca, C., Bonomi, S., Buratti, E., Pedrotti, S., Baralle, F. E., Sette, C., Ghigna, C. and Biamonti, G. (2010) Sam68 regulates EMT through alternative splicing-activated nonsense-mediated mRNA decay of the SF2/ASF proto-oncogene. J. Cell. Biol., 191, 87-99.
10. Ule, J. and Darnell, R. B. (2007) Functional and mechanistic insights from genome-wide studies of splicing regulation in the brain. Adv. Exp. Med. Biol., 623, 148-160.
11. Li, Q., Lee, J. A. and Black, D. L. (2007) Neuronal regulation of alternative pre-mRNA splicing. Nat. Rev. Neurosci., 8, 819-831.
12. Kim, K. K., Kim, Y. C., Adelstein, R. S. and Kawamoto, S. (2011) Fox-3 and PSF interact to activate neural cell-specific alternative splicing. Nucleic Acids Res., 39, 3064-3078.
13. Elliott, D. J. and Grellscheid, S. N. (2006) Alternative RNA splicing regulation in the testis. Reproduction, 132, 811-819.
14. Liu, Y., Bourgeois, C. F., Pang, S., Kudla, M., Dreumont, N., Kister, L., Sun, Y. H., Stevenin, J. and Elliott, D. J. (2009) The germ cell nuclear proteins hnRNP G-T and RBMY activate a testis-specific exon. PLoS Genet., 5, e1000707.
15. Dreumont, N., Bourgeois, C. F., Lejeune, F., Liu, Y., Ehrmann, I. E., Elliott, D. J. and Stévenin, J. (2010) Human RBMY regulates germline-specific splicing events by modulating the function of the serine/arginine-rich proteins 9G8 and Tra2-{beta}. J. Cell Sci., 123, 40-50.
16. Venables, J. P., Vernet, C., Chew, S. L., Elliott, D. J., Cowmeadow, R. B., Wu, J., Cooke, H. J., Artzt, K. and Eperon, I. C. (1999) T-STAR/ETOILE: a novel relative of SAM68 that interacts with an RNA-binding protein implicated in spermatogenesis. Hum. Mol. Genet., 8, 959-969.
17. Richard, S., Torabi, N., Franco, G. V., Tremblay, G. A., Chen, T., Vogel, G., Morel, M., Cléroux, P., Forget-Richard, A., Komarova, S. et al. (2005) Ablation of the Sam68 RNA binding protein protects mice from age-related bone loss. PLoS Genet., 1, e74.
18. Paronetto, M. P., Messina, V., Bianchi, E., Barchi, M., Vogel, G., Moretti, C., Palombi, F., Stefanini, M., Geremia, R., Richard, S. et al. (2009) Sam68 regulates translation of target mRNAs in male germ cells, necessary for mouse spermatogenesis. J. Cell Biol., 185, 235-249.
19. Paronetto, M. P., Zalfa, F., Botti, F., Geremia, R., Bagni, C. and Sette, C. (2006) The nuclear RNA-binding protein Sam68 translocates to the cytoplasm and associates with the polysomes in mouse spermatocytes. Mol. Biol. Cell., 17, 14-24.
20. Paronetto, M. P., Messina, V., Barchi, M., Geremia, R., Richard, S. and Sette, C. (2011) Sam68 marks the transcriptionally active stages of spermatogenesis and modulates alternative splicing in male germ cells. Nucleic Acids Res., 39, 4961-4974.
21. Gardiner, K., Slavov, D., Bechtel, L. and Davisson, M. (2002) Annotation of human chromosome 21 for relevance to Down syndrome: gene structure and expression analysis. Genomics, 79, 833-843.
22. Brun, M. E., Ruault, M., Ventura, M., Roizès, G. and De Sario, A. (2003) Juxtacentromeric region of human chromosome 21: a boundary between centromeric heterochromatin and euchromatic chromosome arms. Gene, 312, 41-50.
23. Hu, Y. H., Warnatz, H. J., Vanhecke, D., Wagner, F., Fiebitz, A., Thamm, S., Kahlem, P., Lehrach, H., Yaspo, M. L. and Janitz, M. (2006) Cell array-based intracellular localization screening reveals novel functional features of human chromosome 21 proteins. BMC Genomics, 7, 155.
24. Paronetto, M. P., Achsel, T., Massiello, A., Chalfant, C. E. and Sette, C. (2007) The RNA-binding protein Sam68 modulates the alternative splicing of Bcl-x. J. Cell. Biol., 176, 929-939.
25. Garneau, D., Revil, T., Fisette, J. F. and Chabot, B. (2005) Heterogeneous nuclear ribonucleoprotein F/H proteins modulate the alternative splicing of the apoptotic mediator Bcl-x. J. Biol. Chem., 280, 22641-22650.
26. Revil, T., Pelletier, J., Toutant, J., Cloutier, A. and Chabot, B. (2009) Heterogeneous nuclear ribonucleoprotein K represses the production of pro-apoptotic Bcl-xS splice isoform. J. Biol. Chem., 284, 21458-21467.
27. Denegri, M., Chiodi, I., Corioni, M., Cobianchi, F., Riva, S. and Biamonti, G. (2001) Stress-induced nuclear bodies are sites of accumulation of pre-mRNA processing factors. Mol. Biol. Cell., 12, 3502-3514.
28. Busà, R., Geremia, R. and Sette, C. (2010) Genotoxic stress causes the accumulation of the splicing regulator Sam68 in nuclear foci of transcriptionally active chromatin. Nucleic Acids Res., 38, 3005-3018.
29. Pedrotti, S., Bielli, P., Paronetto, M. P., Ciccosanti, F., Fimia, G. M., Stamm, S., Manley, J. L. and Sette, C. (2010) The splicing regulator Sam68 binds to a novel exonic splicing silencer and functions in SMN2 alternative splicing in spinal muscular atrophy. EMBO J., 29, 1235-1247.
30. Brumwell, C. L. and Curran, T. (2006) Developmental mouse gene expression maps. J. Physiol., 575, 343-346.
31. Hatten, M. E. and Heintz, N. (1995) Mechanisms of neural patterning and specification in the developing cerebellum. Ann. Rev. Neurosci., 18, 385-408.
32. Bellvé, A. R., Millette, C. F., Bhatnagar, Y. M. and O'Brien, D. A. (1977) Dissociation of the mouse testis and characterization of isolated spermatogenic cells. J. Histochem. Cytochem., 25, 480-494.
33. Maris, C., Dominguez, C. and Allain, F. H. (2005) The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J., 72, 2118-2131.
34. Carrillo Oesterreich, F., Preibisch, S. and Neugebauer, K. M. (2010) Global analysis of nascent RNA reveals transcriptional pausing in terminal exons. Mol. Cell., 40, 571-581.
35. Pandya-Jones, A. and Black, D. L. (2009) Co-transcriptional splicing of constitutive and alternative exons. RNA, 15, 1896-1908.
36. Lamond, A. I. and Spector, D. L. (2003) Nuclear speckles: a model for nuclear organelles. Nat. Rev. Mol. Cell Biol., 4, 605-612.
37. Phatnani, H. P. and Greenleaf, A. L. (2006) Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev., 20, 2922-2936.
38. Biamonti, G. and Caceres, J. F. (2009) Cellular stress and RNA splicing. Trends Biochem. Sci., 34, 146-153.
39. Busà, R. and Sette, C. (2010) An emerging role for nuclear RNA-mediated responses to genotoxic stress. RNA Biol., 7, 390-396.
40. de la Grange, P., Gratadou, L., Delord, M., Dutertre, M. and Auboeuf, D. (2010) Splicing factor and exon profiling across human tissues. Nucleic Acids Res., 38, 2825-2838.
41. Grosso, A. R., Gomes, A. Q., Barbosa-Morais, N. L., Caldeira, S., Thorne, N. P., Grech, G., von Lindern, M. and Carmo-Fonseca, M. (2008) Tissue-specific splicing factor gene expression signatures. Nucleic Acids Res., 36, 4823-4832.
42. Roth, K. A. and D'Sa, C. (2001) Apoptosis and brain development. Ment. Retard. Dev. Disabil. Res. Rev., 7, 261-266.
43. Wang, G. S. and Cooper, T. A. (2007) Splicing in disease: disruption of the splicing code and the decoding machinery. Nat. Rev. Genet., 8, 749-761.