Human RBMY regulates germline-specific splicing events by modulating the function of the serine/arginine-rich proteins 9G8 and Tra2-β

Journal of Cell Science

Volumn 123, Issue 1, 2010, Pages 40-50

  Dreumont, Natacha ^a,b,c   Bourgeois, Cyril F ^a,b,c,f   Lejeune, Fabrice ^d   Liu, Yilei ^e   Ehrmann, Ingrid E ^e   Elliott, David J ^e   Stévenin, James ^a,b,c  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b INSERM   (France)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d INSTITUT PASTEUR DE LILLE   (France)

^e NEWCASTLE UNIVERSITY   (United Kingdom)

^f SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Alternative splicing; Exon junction complex; hRBMY; SR proteins; Testis

Indexed keywords

CELL PROTEIN; RNA BINDING MOTIF PROTEIN Y LINKED; RNA BINDING PROTEIN; TRANSFORMER 2 PROTEIN HOMOLOG BETA; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; EXON; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REGULATORY MECHANISM;

ALTERNATIVE SPLICING; ANIMALS; ARGININE; HELA CELLS; HUMANS; MALE; MICE; NERVE TISSUE PROTEINS; NIH 3T3 CELLS; NUCLEAR PROTEINS; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; PROTEIN BINDING; PROTEIN ENGINEERING; PROTEIN TRANSPORT; RNA POLYMERASE II; RNA-BINDING PROTEINS; SERINE; TESTIS; TRANSCRIPTIONAL ACTIVATION;

EID: 72449183741     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.055889     Document Type: Article

References (47)

1. Berkowitz, L. A. and Gilman, M. Z. (1990). Two distinct forms of active transcription factor CREB (cAMP response element binding protein). Proc. Natl. Acad. Sci. USA 87, 5258-5262.
2. Bourgeois, C. F., Popielarz, M., Hildwein, G. and Stevenin, J. (1999). Identification of a bidirectional splicing enhancer: differential involvement of SR proteins in 5′ or 3′ splice site activation. Mol. Cell. Biol. 19, 7347-7356.
3. Bourgeois, C. F., Lejeune, F. and Stevenin, J. (2004). Broad specificity of SR (serine/arginine) proteins in the regulation of alternative splicing of pre-messenger RNA. Prog. Nucleic Acid Res. Mol. Biol. 78, 37-88.
4. Buratti, E., Stuani, C., De Prato, G. and Baralle, F. E. (2007). SR protein-mediated inhibition of CFTR exon 9 inclusion: molecular characterization of the intronic splicing silencer. Nucleic Acids Res. 35, 4359-4368.
5. Caceres, J. F., Screaton, G. R. and Krainer, A. R. (1998). A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev. 12, 55-66.
6. Custodio, N., Carvalho, C., Condado, I., Antoniou, M., Blencowe, B. J. and Carmo-Fonseca, M. (2004). In vivo recruitment of exon junction complex proteins to transcription sites in mammalian cell nuclei. RNA 10, 622-633.
7. Degot, S., Le Hir, H., Alpy, F., Kedinger, V., Stoll, I., Wendling, C., Seraphin, B., Rio, M. C. and Tomasetto, C. (2004). Association of the breast cancer protein MLN51 with the exon junction complex via its speckle localizer and RNA binding module. J. Biol. Chem. 279, 33702-33715.
8. Elliott, D. J. (2004). The role of potential splicing factors including RBMY, RBMX, hnRNPG-T and STAR proteins in spermatogenesis. Int. J. Androl. 27, 328-334.
9. Elliott, D. J. and Grellscheid, S. N. (2006). Alternative RNA splicing regulation in the testis. Reproduction 132, 811-819.
10. Elliott, D. J., Ma, K., Kerr, S. M., Thakrar, R., Speed, R., Chandley, A. C. and Cooke, H. (1996). An RBM homologue maps to the mouse Y chromosome and is expressed in germ cells. Hum. Mol. Genet. 5, 869-874.
11. Elliott, D. J., Millar, M. R., Oghene, K., Ross, A., Kiesewetter, F., Pryor, J., McIntyre, M., Hargreave, T. B., Saunders, P. T., Vogt, P. H. et al. (1997). Expression of RBM in the nuclei of human germ cells is dependent on a critical region of the Y chromosome long arm. Proc. Natl. Acad. Sci. USA 94, 3848-3853.
12. Elliott, D. J., Oghene, K., Makarov, G., Makarova, O., Hargreave, T. B., Chandley, A. C., Eperon, I. C. and Cooke, H. J. (1998). Dynamic changes in the subnuclear organisation of pre-mRNA splicing proteins and RBM during human germ cell development. J. Cell Sci. 111, 1255-1265.
13. Elliott, D. J., Bourgeois, C. F., Klink, A., Stevenin, J. and Cooke, H. J. (2000). A mammalian germ cell-specific RNA-binding protein interacts with ubiquitously expressed proteins involved in splice site selection. Proc. Natl. Acad. Sci. USA 97, 5717-5722.
14. Ghigna, C., Giordano, S., Shen, H., Benvenuto, F., Castiglioni, F., Comoglio, P. M., Green, M. R., Riva, S. and Biamonti, G. (2005). Cell motility is controlled by SF2/ASF through alternative splicing of the Ron protooncogene. Mol. Cell 20, 881-890.
15. Grabowski, P. J. (2000). Genetic evidence for a Nova regulator of alternative splicing in the brain. Neuron 25, 254-256.
16. Haaf, T. and Ward, D. C. (1996). Inhibition of RNA polymerase II transcription causes chromatin decondensation, loss of nucleolar structure, and dispersion of chromosomal domains. Exp. Cell Res. 224, 163-173.
17. Hall, L. L., Smith, K. P., Byron, M. and Lawrence, J. B. (2006). Molecular anatomy of a speckle. Anat. Rec. A Discov. Mol. Cell Evol. Biol. 288, 664-675.
18. Heinrich, B., Zhang, Z., Raitskin, O., Hiller, M., Benderska, N., Hartmann, A. M., Bracco, L., Ben-Ari, S., Soreq, H., Sperling, J. et al. (2009). hnRNP G regulates splice site selection by binding to CC(A/C)-rich regions in pre-mRNA. J. Biol. Chem. 284, 14303-14315.
19. Hofmann, Y. and Wirth, B. (2002). hnRNP-G promotes exon 7 inclusion of survival motor neuron (SMN) via direct interaction with Htra2-beta1. Hum. Mol. Genet. 11, 2037-2049.
20. Huang, Y. and Steitz, J. A. (2001). Splicing factors SRp20 and 9G8 promote the nucleocytoplasmic export of mRNA. Mol. Cell 7, 899-905.
21. Huang, Y., Gattoni, R., Stevenin, J. and Steitz, J. A. (2003). SR splicing factors serve as adapter proteins for TAP-dependent mRNA export. Mol. Cell 11, 837-843.
22. Iwamoto, F., Stadler, M., Chalupnikova, K., Oakeley, E. and Nagamine, Y. (2008). Transcription-dependent nucleolar cap localization and possible nuclear function of DExH RNA helicase RHAU. Exp. Cell Res. 314, 1378-1391.
23. Kan, Z., Garrett-Engele, P. W., Johnson, J. M. and Castle, J. C. (2005). Evolutionarily conserved and diverged alternative splicing events show different expression and functional profiles. Nucleic Acids Res. 33, 5659-5666.
24. Kimmins, S., Kotaja, N., Davidson, I. and Sassone-Corsi, P. (2004). Testis-specific transcription mechanisms promoting male germ-cell differentiation. Reproduction 128, 5-12.
25. Lamond, A. I. and Spector, D. L. (2003). Nuclear speckles: a model for nuclear organelles. Nat. Rev. Mol. Cell. Biol. 4, 605-612.
26. Lareau, L. F., Inada, M., Green, R. E., Wengrod, J. C. and Brenner, S. E. (2007). Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements. Nature 446, 926-929.
27. Lejeune, F., Cavaloc, Y. and Stevenin, J. (2001). Alternative splicing of intron 3 of the serine/arginine-rich protein 9G8 gene. Identification of flanking exonic splicing enhancers and involvement of 9G8 as a trans-acting factor. J. Biol. Chem. 276, 7850-7858.
28. 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 RNA binding proteins hnRNP G-T and RBMY direct inclusion of a testis-specific exon in the human Groucho homologue TLE4. PLoS Genet. 5, e1000707.
29. 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.
30. Ma, K., Inglis, J. D., Sharkey, A., Bickmore, W. A., Hill, R. E., Prosser, E. J., Speed, R. M., Thomson, E. J., Jobling, M., Taylor, K. et al. (1993). A Y chromosome gene family with RNA-binding protein homology: candidates for the azoospermia factor AZF controlling human spermatogenesis. Cell 75, 1287-1295.
31. Martinez-Contreras, R., Cloutier, P., Shkreta, L., Fisette, J. F., Revil, T. and Chabot, B. (2007). hnRNP proteins and splicing control. Adv. Exp. Med. Biol. 623, 123-147.
32. Mintz, P. J., Patterson, S. D., Neuwald, A. F., Spahr, C. S. and Spector, D. L. (1999). Purification and biochemical characterization of interchromatin granule clusters. EMBO J. 18, 4308-4320.
33. Nasim, M. T., Chernova, T. K., Chowdhury, H. M., Yue, B. G. and Eperon, I. C. (2003). HnRNP G and Tra2beta: opposite effects on splicing matched by antagonism in RNA binding. Hum. Mol. Genet. 12, 1337-1348.
34. Phair, R. D. and Misteli, T. (2000). High mobility of proteins in the mammalian cell nucleus. Nature 404, 604-609.
35. Ruppert, S., Cole, T. J., Boshart, M., Schmid, E. and Schutz, G. (1992). Multiple mRNA isoforms of the transcription activator protein CREB: generation by alternative splicing and specific expression in primary spermatocytes. EMBO J. 11, 1503-1512.
36. Sanchez-Alvarez, M., Goldstrohm, A. C., Garcia-Blanco, M. A. and Sune, C. (2006). Human transcription elongation factor CA150 localizes to splicing factor-rich nuclear speckles and assembles transcription and splicing components into complexes through its amino and carboxyl regions. Mol. Cell. Biol. 26, 4998-5014.
37. Schmucker, D. (2007). Molecular diversity of Dscam: recognition of molecular identity in neuronal wiring. Nat. Rev. Neurosci. 8, 915-920.
38. Shav-Tal, Y., Blechman, J., Darzacq, X., Montagna, C., Dye, B. T., Patton, J. G., Singer, R. H. and Zipori, D. (2005). Dynamic sorting of nuclear components into distinct nucleolar caps during transcriptional inhibition. Mol. Biol. Cell 16, 2395-2413.
39. Skrisovska, L., Bourgeois, C. F., Stefl, R., Grellscheid, S. N., Kister, L., Wenter, P., Elliott, D. J., Stevenin, J. and Allain, F. H. (2007). The testis-specific human protein RBMY recognizes RNA through a novel mode of interaction. EMBO Rep. 8, 372-379.
40. Stoilov, P., Daoud, R., Nayler, O. and Stamm, S. (2004). Human tra2-beta1 autoregulates its protein concentration by influencing alternative splicing of its pre-mRNA. Hum. Mol. Genet. 13, 509-524.
41. Swartz, J. E., Bor, Y. C., Misawa, Y., Rekosh, D. and Hammarskjold, M. L. (2007). The shuttling SR protein 9G8 plays a role in translation of unspliced mRNA containing a constitutive transport element. J. Biol. Chem. 282, 19844-19853.
42. Venables, J. P., Elliott, D. J., Makarova, O. V., Makarov, E. M., Cooke, H. J. and Eperon, I. C. (2000). RBMY, a probable human spermatogenesis factor, and other hnRNP G proteins interact with Tra2beta and affect splicing. Hum. Mol. Genet. 9, 685-694.
43. Wang, E. T., Sandberg, R., Luo, S., Khrebtukova, I., Zhang, L., Mayr, C., Kingsmore, S. F., Schroth, G. P. and Burge, C. B. (2008). Alternative isoform regulation in human tissue transcriptomes. Nature 456, 470-476.
44. 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.
45. Warzecha, C. C., Sato, T. K., Nabet, B., Hogenesch, J. B. and Carstens, R. P. (2009). ESRP1 and ESRP2 are epithelial cell-type-specific regulators of FGFR2 splicing. Mol. Cell 33, 591-601.
46. Xu, Q., Modrek, B. and Lee, C. (2002). Genome-wide detection of tissue-specific alternative splicing in the human transcriptome. Nucleic Acids Res. 30, 3754-3766.
47. Yeo, G., Holste, D., Kreiman, G. and Burge, C. B. (2004). Variation in alternative splicing across human tissues. Genome Biol. 5, R74.