DOI QR코드

DOI QR Code

SR Proteins: Binders, Regulators, and Connectors of RNA

  • Jeong, Sunjoo (Department of Bioconvergent Science and Technology, Dankook University)
  • Received : 2016.12.30
  • Accepted : 2017.01.06
  • Published : 2017.01.31

Abstract

Serine and arginine-rich (SR) proteins are RNA-binding proteins (RBPs) known as constitutive and alternative splicing regulators. As splicing is linked to transcriptional and post-transcriptional steps, SR proteins are implicated in the regulation of multiple aspects of the gene expression program. Recent global analyses of SR-RNA interaction maps have advanced our understanding of SR-regulated gene expression. Diverse SR proteins play partially overlapping but distinct roles in transcription-coupled splicing and mRNA processing in the nucleus. In addition, shuttling SR proteins act as adaptors for mRNA export and as regulators for translation in the cytoplasm. This mini-review will summarize the roles of SR proteins as RNA binders, regulators, and connectors from transcription in the nucleus to translation in the cytoplasm.

Keywords

export;RNA-binding proteins;SR proteins;splicing;transcription;translation

Acknowledgement

Supported by : Dankook University

References

  1. Ajiro, M., Jia, R., Yang, Y., Zhu, J., and Zheng, Z.M. (2016). A genome landscape of SRSF3-regulated splicing events and gene expression in human osteosarcoma U2OS cells. Nucleic Acids Res. 44, 1854-1870. https://doi.org/10.1093/nar/gkv1500
  2. Allemand, E., Batsche, E., and Muchardt, C. (2008). Splicing, transcription, and chromatin: a menage a trois. Curr. Opin. Genet. Dev. 18, 145-151. https://doi.org/10.1016/j.gde.2008.01.006
  3. Anczukow, O., Akerman, M., Clery, A., Wu, J., Shen, C., Shirole, N.H., Raimer, A., Sun, S., Jensen, M.A., Hua, Y., et al. (2015). SRSF1-Regulated Alternative Splicing in Breast Cancer. Mol. Cell 60, 105-117. https://doi.org/10.1016/j.molcel.2015.09.005
  4. Anko, M.L. (2014). Regulation of gene expression programmes by serine-arginine rich splicing factors. Semin. Cell Dev. Biol. 32, 11-21. https://doi.org/10.1016/j.semcdb.2014.03.011
  5. Anko, M.L., Morales, L., Henry, I., Beyer, A., and Neugebauer, K.M. (2010). Global analysis reveals SRp20- and SRp75-specific mRNPs in cycling and neural cells. Nat. Struct. Mol. Biol. 17, 962-970. https://doi.org/10.1038/nsmb.1862
  6. Anko, M.L., Muller-McNicoll, M., Brandl, H., Curk, T., Gorup, C., Henry, I., Ule, J., and Neugebauer, K.M. (2012). The RNA-binding landscapes of two SR proteins reveal unique functions and binding to diverse RNA classes. Genome Biol. 13, R17. https://doi.org/10.1186/gb-2012-13-3-r17
  7. Aubol, B.E., Wu, G., Keshwani, M.M., Movassat, M., Fattet, L., Hertel, K.J., Fu, X.D., and Adams, J.A. (2016). Release of SR proteins from CLK1 by SRPK1: a smbiotic kinase sstem for phosphorylation control of pre-mRNA splicing. Mol. Cell 63, 218-228. https://doi.org/10.1016/j.molcel.2016.05.034
  8. Bedard, K.M., Daijogo, S., and Semler, B.L. (2007). A nucleo-cytoplasmic SR protein functions in viral IRES-mediated translation initiation. EMBO J. 26, 459-467. https://doi.org/10.1038/sj.emboj.7601494
  9. Bentley, D.L. (2014). Coupling mRNA processing with transcription in time and space. Nat. Rev. Genet. 15, 163-175.
  10. Bjerregaard, N., Andreasen, P.A., and Dupont, D.M. (2016). Expected and unexpected features of protein-binding RNA aptamers. Wiley interdisciplinary reviews RNA 7, 744-757. https://doi.org/10.1002/wrna.1360
  11. Blencowe, B.J. (2006). Alternative splicing: new insights from global analyses. Cell 126, 37-47. https://doi.org/10.1016/j.cell.2006.06.023
  12. Braunschweig, U., Gueroussov, S., Plocik, A.M., Graveley, B.R., and Blencowe, B.J. (2013). Dynamic integration of splicing within gene regulatory pathways. Cell 152, 1252-1269. https://doi.org/10.1016/j.cell.2013.02.034
  13. Bunka, D.H., and Stockley, P.G. (2006). Aptamers come of age - at last. Nat. Rev. Microbiol. 4, 588-596. https://doi.org/10.1038/nrmicro1458
  14. Caceres, J.F., Screaton, G.R., and Krainer, A.R. (1998). A specific subset of SR proteins shuttles continuously between the nucelus and the cytoplasm. Genes Dev. 12, 55-66. https://doi.org/10.1101/gad.12.1.55
  15. Cartegni, L. (2003). ESEfinder: a web resource to identify exonic splicing enhancers. Nucleic Acids Res. 31, 3568-3571. https://doi.org/10.1093/nar/gkg616
  16. Castello, A., Fischer, B., Frese, C.K., Horos, R., Alleaume, A.M., Foehr, S., Curk, T., Krijgsveld, J., and Hentze, M.W. (2016). Comprehensive identification of RNA-binding domains in human cells. Mol. Cell 63, 696-710. https://doi.org/10.1016/j.molcel.2016.06.029
  17. Champlin, D.T., Frasch, M., Saumweber, H., and Lis, J.T. (1991). Characterization of a Drosophila protein associated with boundaries of transcriptionally active chromatin. Genes Dev. 5, 1611-1621. https://doi.org/10.1101/gad.5.9.1611
  18. Colwill, K., Feng, L.L., Yeakley, J.M., Gish, G.D., Caceres, J.F., Pawson, T., and Fu, X.D. (1996a). SRPK1 and Clk/Sky protein kinases show distinct substrate specificities for Serine/Arginine-rich splicing factors. J. Biol. Chem. 271, 24569-24575. https://doi.org/10.1074/jbc.271.40.24569
  19. Colwill, K., Pawson, T., Andrews, B., Prasad, J., Manley, J.L., Bell, J.C., and Duncan, P.I. (1996b). The Clk/Sky protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution. EMBO J. 15, 265-275.
  20. Corkery, D.P., Holly, A.C., Lahsaee, S., and Dellaire, G. (2015). Connecting the speckles: Splicing kinases and their role in tumorigenesis and treatment response. Nucleus 6, 279-288. https://doi.org/10.1080/19491034.2015.1062194
  21. Coulter, L.R., Landree, M.A., and Cooper, T.A. (1997). Identification of a new class of exonic splicing enhancers by in vivo selection. Mol. Cell. Biol. 17, 2143-2150. https://doi.org/10.1128/MCB.17.4.2143
  22. Das, R., Dufu, K., Romney, B., Feldt, M., Elenko, M., and Reed, R. (2006). Functional coupling of RNAP II transcription to spliceosome assembly. Genes Dev. 20, 1100-1109. https://doi.org/10.1101/gad.1397406
  23. Das, R., Yu, J., Zhang, Z., Gygi, M.P., Krainer, A.R., Gygi, S.P., and Reed, R. (2007). SR proteins function in coupling RNAP II transcription to pre-mRNA splicing. Mol. Cell 26, 867-881. https://doi.org/10.1016/j.molcel.2007.05.036
  24. de la Mata, M., and Kornblihtt, A.R. (2006). RNA polymerase II C-terminal domain mediates regulation of alternative splicing by SRp20. Nat. Struct. Mol. Biol. 13, 973-980. https://doi.org/10.1038/nsmb1155
  25. Erkelenz, S., Mueller, W.F., Evans, M.S., Busch, A., Schoneweis, K., Hertel, K.J., and Schaal, H. (2013). Position-dependent splicing activation and repression by SR and hnRNP proteins rely on common mechanisms. RNA 19, 96-102. https://doi.org/10.1261/rna.037044.112
  26. Fregoso, O.I., Das, S., Akerman, M., and Krainer, A.R. (2013). Splicing-factor oncoprotein SRSF1 stabilizes p53 via RPL5 and induces cellular senescence. Mol. Cell 50, 56-66. https://doi.org/10.1016/j.molcel.2013.02.001
  27. Fu, X.D. (2004). Towards a splicing code. Cell 119, 736-738. https://doi.org/10.1016/j.cell.2004.11.039
  28. Fu, X.D., and Ares, M., Jr. (2014). Context-dependent control of alternative splicing by RNA-binding proteins. Nat. Rev. Genet. 15, 689-701. https://doi.org/10.1038/nrg3778
  29. Geuens, T., Bouhy, D., and Timmerman, V. (2016). The hnRNP family: insights into their role in health and disease. Hum. Genet. 135, 851-867. https://doi.org/10.1007/s00439-016-1683-5
  30. Ghosh, G., and Adams, J.A. (2011). Phosphorylation mechanism and structure of serine-arginine protein kinases. FEBS J. 278, 587-597. https://doi.org/10.1111/j.1742-4658.2010.07992.x
  31. Glisovic, T., Bachorik, J.L., Yong, J., and Dreyfuss, G. (2008). RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett. 582, 1977-1986. https://doi.org/10.1016/j.febslet.2008.03.004
  32. Gui, J.F., Tronchere, H., Chandler, S.D., and Fu, X.D. (1994). Purification and characterization of a kinase specific for the serine and srginine-rich pre-mRNA splicing factors. Proc. Natl. Acad. Sci. USA 91, 10824-10828. https://doi.org/10.1073/pnas.91.23.10824
  33. Han, J., Ding, J.H., Byeon, C.W., Kim, J.H., Hertel, K.J., Jeong, S., and Fu, X.D. (2011a). SR proteins induce alternative exon skipping through their activities on the flanking constitutive exons. Mol. Cell. Biol. 31, 793-802. https://doi.org/10.1128/MCB.01117-10
  34. Han, J., Xiong, J., Wang, D., and Fu, X.D. (2011b). Pre-mRNA splicing: where and when in the nucleus. Trends Cell Biol. 21, 336-343. https://doi.org/10.1016/j.tcb.2011.03.003
  35. Hargous, Y., Hautbergue, G.M., Tintaru, A.M., Skrisovska, L., Golovanov, A.P., Stevein, J., Lian, L.Y., Wilson, S.A., and Allain, F.H.T. (2006). Molecular basis of RNA recognition and TAP binding by the SR proteins SRp20 and 9G8. EMBO J. 25, 5126-5137. https://doi.org/10.1038/sj.emboj.7601385
  36. Howard, J.M., and Sanford, J.R. (2015). The RNAissance family: SR proteins as multifaceted regulators of gene expression. Wiley interdisciplinary reviews RNA 6, 93-110. https://doi.org/10.1002/wrna.1260
  37. Hsin, J.P., and Manley, J.L. (2012). The RNA polymerase II CTD coordinates transcription and RNA processing. Genes Dev. 26, 2119-2137. https://doi.org/10.1101/gad.200303.112
  38. Huang, Y.S., and Steitz, J.A. (2001). Splicing factors SRp20 and 9G8 promote the nucleocytoplasmic export of mRNA. Mol. Cell 7, 899-905. https://doi.org/10.1016/S1097-2765(01)00233-7
  39. Huang, Y., and Steitz, J.A. (2005). SRprises along a messenger's journey. Mol. Cell 17, 613-615. https://doi.org/10.1016/j.molcel.2005.02.020
  40. Huang, Y., Gattoni, R., Stévenin, J., and Steitz, J.A. (2003). SR splicing factors Serve as adapter proteins for TAP-dependent mRNA export. Mol. Cell 11, 837-843. https://doi.org/10.1016/S1097-2765(03)00089-3
  41. Huang, Y., Yario, T.A., and Steitz, J.A. (2004). A molecular link between SR protein dephosphorylation and mRNA export. Proc. Natl. Acad. Sci. USA 101, 9666-9670. https://doi.org/10.1073/pnas.0403533101
  42. Jangi, M., and Sharp, P.A. (2014). Building robust transcriptomes with master splicing factors. Cell 159, 487-498. https://doi.org/10.1016/j.cell.2014.09.054
  43. Jankowsky, E., and Harris, M.E. (2015). Specificity and nonspecificity in RNA-protein interactions. Nat. Rev. Mol. Cell Biol. 16, 533-544. https://doi.org/10.1038/nrm4032
  44. Ji, X., Zhou, Y., Pandit, S., Huang, J., Li, H., Lin, C.Y., Xiao, R., Burge, C.B., and Fu, X.D. (2013). SR proteins collaborate with 7SK and promoter-associated nascent RNA to release paused polymerase. Cell 153, 855-868. https://doi.org/10.1016/j.cell.2013.04.028
  45. Jiang, L., Huang, J., Higgs, B.W., Hu, Z., Xiao, Z., Yao, X., Conley, S., Zhong, H., Liu, Z., Brohawn, P., et al. (2016). Genomic landscape survey identifies SRSF1 as a key oncodriver in small cell lung cancer. PLoS Genet. 12, e1005895. https://doi.org/10.1371/journal.pgen.1005895
  46. Jonkers, I., and Lis, J.T. (2015). Getting up to speed with transcription elongation by RNA polymerase II. Nat. Rev. Mol. Cell Biol. 16, 167-177. https://doi.org/10.1038/nrm3953
  47. Kalsotra, A., and Cooper, T.A. (2011). Functional consequences of developmentally regulated alternative splicing. Nat. Rev. Genet. 12, 715-729.
  48. Karni, R., de Stanchina, E., Lowe, S.W., Sinha, R., Mu, D., and Krainer, A.R. (2007). The gene encoding the splicing factor SF2/ASF is a proto-oncogene. Nat. Struct. Mol. Biol. 14, 185-193. https://doi.org/10.1038/nsmb1209
  49. Karni, R., Hippo, Y., Lowe, S.W., and Krainer, A.R. (2008). The splicing-factor oncoprotein SF2/ASF activates mTORC1. Proc. Natl. Acad. Sci. USA 105, 15323-15327. https://doi.org/10.1073/pnas.0801376105
  50. Katz, Y., Wang, E.T., Airoldi, E.M., and Burge, C.B. (2010). Analysis and design of RNA sequencing experiments for identifying isoform regulation. Nat. Methods 7, 1009-1015. https://doi.org/10.1038/nmeth.1528
  51. Kim, I., Kwak, H., Lee, H.K., Hyun, S., and Jeong, S. (2012). beta-Catenin recognizes a specific RNA motif in the cyclooxygenase-2 mRNA 3'-UTR and interacts with HuR in colon cancer cells. Nucleic Acids Res. 40, 6863-6872. https://doi.org/10.1093/nar/gks331
  52. Kim, J., Park, R.Y., Chen, J.K., Kim, J., Jeong, S., and Ohn, T. (2014). Splicing factor SRSF3 represses the translation of programmed cell death 4 mRNA by associating with the 5'-UTR region. Cell Death Differ. 21, 481-490. https://doi.org/10.1038/cdd.2013.171
  53. Konig, A., Zarnack, K., Luscombe, N.M., and Ule, J. (2012). Protein-RNA interactions: new genomic technologies and perspectives. Nat. Rev. Genet. 13, 77-83. https://doi.org/10.1038/nrg3141
  54. Kornblihtt, A.R., Schor, I.E., Allo, M., Dujardin, G., Petrillo, E., and Munoz, M.J. (2013). Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat. Rev. Mol. Cell Biol. 14, 153-165.
  55. Lemaire, R., Prasad, J., Kashima, T., Gustafson, J., Manley, J.L., and Lafyatis, R. (2002). Stability of PKCI-1-related mRNA is controlled by the splicing factor ASF/SF2: a novel function for SR proteins. Genes Dev. 16, 594-607. https://doi.org/10.1101/gad.939502
  56. Listerman, I., Sapra, A.K., and Neugebauer, K.M. (2006). Cotranscriptional coupling of splicing factor recruitment and precursor messenger RNA splicing in mammalian cells. Nat. Struct. Mol. Biol. 13, 815-822. https://doi.org/10.1038/nsmb1135
  57. Liu, H.X., Zhang, M., and Krainer, A.R. (1998). Identification of functional exonic splicing enhacer motifs recognized by individual SR proteins. Genes Dev. 12, 1988-2012.
  58. 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. https://doi.org/10.1042/BJ20081501
  59. Loomis, R.J., Naoe, Y., Parker, J.B., Savic, V., Bozovsky, M.R., Macfarlan, T., Manley, J.L., and Chakravarti, D. (2009). Chromatin binding of SRp20 and ASF/SF2 and dissociation from mitotic chromosomes is modulated by histone H3 serine 10 phosphorylation. Mol. Cell 33, 450-461. https://doi.org/10.1016/j.molcel.2009.02.003
  60. Lou, H., Neugebauer, K.M., Gagel, R.F., and Berget, S.A. (1998). Regulation of alternative polyadenylation by U1 snRNPs and SRp20. Mol. Cell. Biol. 18, 4977, 4985.
  61. Luco, R.F., Pan, Q., Tominaga, K., Blencowe, B.J., Pereira-Smith, O.M., and Misteli, T. (2010). Regulation of alternative splicing by histone modifications. Science 327, 996-1000. https://doi.org/10.1126/science.1184208
  62. Luco, R.F., Allo, M., Schor, I.E., Kornblihtt, A.R., and Misteli, T. (2011). Epigenetics in alternative pre-mRNA splicing. Cell 144, 16-26. https://doi.org/10.1016/j.cell.2010.11.056
  63. Maniatis, T., and Reed, R. (2002). An extensive network of coupling among gene expression machines. Nature 416, 499-506. https://doi.org/10.1038/416499a
  64. Maniatis, T., and Tasik, B. (2002). Alternative pre-mRNA splicing and proteome expansion in metazoans. Nature 418, 236-243. https://doi.org/10.1038/418236a
  65. Manley, J.L., and Krainer, A.R. (2010). A rational nomenclature for serine/arginine-rich protein splicing factors (SR proteins). Genes Dev. 24, 1073-1074. https://doi.org/10.1101/gad.1934910
  66. Maslon, M.M., Heras, S., Bellora, N., Eyras, E., and Caceres, J.F. (2014). The translational landscape of the splicing factor SRSF1 and its role in mitosis. eLIFE 3, e02028.
  67. Michlewski, G., Sanford, J.R., and Caceres, J.F. (2008). The splicing factor SF2/ASF regulates translation initiation by enhancing phosphorylation of 4E-BP1. Mol. Cell 30, 179-189. https://doi.org/10.1016/j.molcel.2008.03.013
  68. Moore, M.J., and Proudfoot, N.J. (2009). Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 136, 688-700. https://doi.org/10.1016/j.cell.2009.02.001
  69. Muller-McNicoll, M., and Neugebauer, K.M. (2013). How cells get the message: dynamic assembly and function of mRNA-protein complexes. Nat. Rev. Genet. 14, 275-287. https://doi.org/10.1038/nrg3434
  70. Muller-McNicoll, M., Botti, V., Domingues, A.M., Brandl, H., Schwich, O.D., Steiner, M.C., Curk, T., Poser, I., Zarnack, K., and Neugebauer, K.M. (2016). SR proteins are NXF1 adaptors that link alternative RNA processing to mRNA export. Genes Dev. 30, 553-566. https://doi.org/10.1101/gad.276477.115
  71. Munoz, M.J., de la Mata, M., and Kornblihtt, A.R. (2010). The carboxy terminal domain of RNA polymerase II and alternative splicing. Trends Biochem. Sci. 35, 497-504. https://doi.org/10.1016/j.tibs.2010.03.010
  72. Ninomiya, K., Kataoka, N., and Hagiwara, M. (2011). Stress-responsive maturation of Clk1/4 pre-mRNAs promotes phosphorylation of SR splicing factor. J. Cell Biol. 195, 27-40. https://doi.org/10.1083/jcb.201107093
  73. Pan, Q., Shai, O., Lee, L.J., Frey, B.J., and Blencowe, B.J. (2008). Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat. Genet. 40, 1413-1415. https://doi.org/10.1038/ng.259
  74. Pandit, S., Zhou, Y., Shiue, L., Coutinho-Mansfield, G., Li, H., Qiu, J., Huang, J., Yeo, G.W., Ares, M., Jr., and Fu, X.D. (2013). Genome-wide analysis reveals SR protein cooperation and competition in regulated splicing. Mol. Cell 50, 223-235. https://doi.org/10.1016/j.molcel.2013.03.001
  75. Papasaikas, P., and Valcarcel, J. (2016). The Spliceosome: the ultimate RNA chaperone and sculptor. Trends Biochem. Sci. 41, 33-45. https://doi.org/10.1016/j.tibs.2015.11.003
  76. Park, S.K., and Jeong, S. (2016). SRSF3 represses the expression of PDCD4 protein by coordinated regulation of alternative splicing, export and translation. Biochem. Biophys. Res. Commun. 470, 431-438. https://doi.org/10.1016/j.bbrc.2016.01.019
  77. Perales, R., and Bentley, D. (2009). "Cotranscriptionality": the transcription elongation complex as a nexus for nuclear transactions. Mol. Cell 36, 178-191. https://doi.org/10.1016/j.molcel.2009.09.018
  78. Popp, M.W., and Maquat, L.E. (2014). The dharma of nonsense-mediated mRNA decay in mammalian cells. Mol. Cells 37, 1-8. https://doi.org/10.14348/molcells.2014.2193
  79. Ray, D., Kazan, H., Cook, K.B., Weirauch, M.T., Najafabadi, H.S., Li, X., Gueroussov, S., Albu, M., Zheng, H., Yang, A., et al. (2013). A compendium of RNA-binding motifs for decoding gene regulation. Nature 499, 172-177. https://doi.org/10.1038/nature12311
  80. Roth, M.B., and Gall, J.G. (1987). Monoclonal antibodies that recognize transcription unit proteins on newt lambrush chromosomes. J. Cell Biol. 105, 1047-1054. https://doi.org/10.1083/jcb.105.3.1047
  81. Roth, M.B., Murphy, C., and Gall, J.G. (1990). A monoclonal antibody that recognizes a phosphorylated epitope stains lampbrush chromosome loops and small granules in the amphibian germinal vesicle. J. Cell Biol. 111, 2217-2223. https://doi.org/10.1083/jcb.111.6.2217
  82. Sanford, J.R., Gray, N.K., Beckmann, K., and Caceres, J.F. (2004). A novel role for shuttling SR proteins in mRNA translation. Genes Dev. 18, 755-768. https://doi.org/10.1101/gad.286404
  83. Sanford, J.R., Ellis, J.D., Cazalla, D., and Caceres, J.F. (2005). Reversible phosphorylation differentially affects nuclear and cytoplasmic functions of splicing factor 2/alternative splicing factor. Proc. Natl. Acad. Sci. USA 102, 15042-15047. https://doi.org/10.1073/pnas.0507827102
  84. Sanford, J.R., Coutinho, P., Hackett, P.A., Wang, X., Ranahan, W., and Caceres, J.F. (2008). Identification of nuclear and cytoplasmic mRNA targets for the shuttling protein SF2/ASF. PloS One 3, e3369. https://doi.org/10.1371/journal.pone.0003369
  85. Sanford, J.R., Wang, X., Mort, M., Vanduyn, N., Cooper, D.N., Mooney, S.D., Edenberg, H.J., and Liu, Y. (2009). Splicing factor SFRS1 recognizes a functionally diverse landscape of RNA transcripts. Genome Res. 19, 381-394.
  86. Sapra, A.K., Anko, M.L., Grishina, I., Lorenz, M., Pabis, M., Poser, I., Rollins, J., Weiland, E.M., and Neugebauer, K.M. (2009). SR protein family members display diverse activities in the formation of nascent and mature mRNPs in vivo. Mol. Cell 34, 179-190. https://doi.org/10.1016/j.molcel.2009.02.031
  87. Schaal, T., and Maniatis, T. (1999). Selection and characterization of pre-mRNAsplicing enhancers: Identification of novel SR protein-specific enhancer sequences. Mol. Cell. Biol. 19, 1705-1719. https://doi.org/10.1128/MCB.19.3.1705
  88. Shen, M., and Mattox, W. (2012). Activation and repression functions of an SR splicing regulator depend on exonic versus intronic-binding position. Nucleic Acids Res. 40, 428-437. https://doi.org/10.1093/nar/gkr713
  89. Shepard, P.J., and Hertel, K.J. (2009). The SR protein family. Genome Biol. 10, 242. https://doi.org/10.1186/gb-2009-10-10-242
  90. Singh, G., Kucukural, A., Cenik, C., Leszyk, J.D., Shaffer, S.A., Weng, Z., and Moore, M.J. (2012). The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell 151, 750-764. https://doi.org/10.1016/j.cell.2012.10.007
  91. Sun, S., Zhang, Z., Sinha, R., Karni, R., and Krainer, A.R. (2010). SF2/ASF autoregulation involves multiple layers of posttranscriptional and translational control. Nat. Struct. Mol. Biol. 17, 306-312. https://doi.org/10.1038/nsmb.1750
  92. 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. https://doi.org/10.1074/jbc.M701660200
  93. Tuerk, C., and Gold, L. (1990). Systemic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249, 505-510. https://doi.org/10.1126/science.2200121
  94. Ule, J., Jensen, K., Mele, A., and Darnell, R.B. (2005). CLIP: a method for identifying protein-RNA interaction sites in living cells. Methods 37, 376-386. https://doi.org/10.1016/j.ymeth.2005.07.018
  95. Wahl, M.C., Will, C.L., and Luhrmann, R. (2009). The spliceosome: design principles of a dynamic RNP machine. Cell 136, 701-718. https://doi.org/10.1016/j.cell.2009.02.009
  96. Wang, Z., and Burge, C.B. (2008). Splicing regulation: from a parts list of regulatory elements to an integrated splicing code. RNA 14, 802-813. https://doi.org/10.1261/rna.876308
  97. Wang, Z., Rolish, M.E., Yeo, G., Tung, V., Mawson, M., and Burge, C.B. (2004). Systematic identification and analysis of exonic splicing silencers. Cell 119, 831-845. https://doi.org/10.1016/j.cell.2004.11.010
  98. Wang, X., Juan, L., Lv, J., Wang, K., Sanford, J.R., and Liu, Y. (2011). Predicting sequence and structural specificities of RNA binding regions recognized by splicing factor SRSF1. BMC Genom. 12, S8.
  99. Wang, Y., Ma, M., Xiao, X., and Wang, Z. (2012). Intronic splicing enhancers, cognate splicing factors and context-dependent regulation rules. Nat. Struct. Mol. Biol. 19, 1044-1052. https://doi.org/10.1038/nsmb.2377
  100. Wang, Y., Xiao, X., Zhang, J., Choudhury, R., Robertson, A., Li, K., Ma, M., Burge, C.B., and Wang, Z. (2013). A complex network of factors with overlapping affinities represses splicing through intronic elements. Nat. Struct. Mol. Biol. 20, 36-45. https://doi.org/10.1038/nsmb.2459
  101. Weatheritt, R.J., Sterne-Weiler, T., and Blencowe, B.J. (2016). The ribosome-engaged landscape of alternative splicing. Nat. Struct. Mol. Biol. 23, 1117-1123. https://doi.org/10.1038/nsmb.3317
  102. Wickramasinghe, V.O., and Laskey, R.A. (2015). Control of mammalian gene expression by selective mRNA export. Nat. Rev. Mol. Cell Biol. 16, 431-442. https://doi.org/10.1038/nrm4010
  103. Xiao, W., Adhikari, S., Dahal, U., Chen, Y.S., Hao, Y.J., Sun, B.F., Sun, H.Y., Li, A., Ping, X.L., Lai, W.Y., et al. (2016). Nuclear m(6)A reader YTHDC1 regulates mRNA splicing. Mol. Cell 61, 507-519. https://doi.org/10.1016/j.molcel.2016.01.012
  104. Zahler, A.M., Neugebauer, K.M., Lane, W.S., and Roth, M.B. (1993). Distinct functions of SR proteins in alternative pre-mRNA splicing. Science 260, 219-222. https://doi.org/10.1126/science.8385799
  105. Zhang, Z., and Krainer, A.R. (2004). Involvement of SR proteins in mRNA surveillance. Mol. Cell 16, 597-607. https://doi.org/10.1016/j.molcel.2004.10.031
  106. Zhao, B.S., Roundtree, I.A., and He, C. (2017). Post-transcriptional gene regulation by mRNA modifications. Nat. Rev. Mol. Cell Biol. 18, 31-42. https://doi.org/10.1038/nrn.2016.159
  107. Zhong, X.Y., Ding, J.H., Adams, J.A., Ghosh, G., and Fu, X.D. (2009). Regulation of SR protein phosphorylation and alternative splicing by modulating kinetic interactions of SRPK1 with molecular chaperones. Genes Dev. 23, 482-495. https://doi.org/10.1101/gad.1752109
  108. Zhou, Z., and Fu, X.D. (2013). Regulation of splicing by SR proteins and SR protein-specific kinases. Chromosoma 122, 191-207. https://doi.org/10.1007/s00412-013-0407-z
  109. Zhou, Z., Qiu, J., Liu, W., Zhou, Y., Plocinik, R.M., Li, H., Hu, Q., Ghosh, G., Adams, J.A., Rosenfeld, M.G., et al. (2012). The Akt-SRPK-SR axis constitutes a major pathway in transducing EGF signaling to regulate alternative splicing in the nucleus. Mol. Cell 47, 422-433. https://doi.org/10.1016/j.molcel.2012.05.014

Cited by

  1. SRp55 Regulates a Splicing Network That Controls Human Pancreatic β-Cell Function and Survival vol.67, pp.3, 2017, https://doi.org/10.2337/db17-0736
  2. The SR protein B52/SRp55 regulates splicing of the period thermosensitive intron and mid-day siesta in Drosophila vol.8, pp.1, 2018, https://doi.org/10.1038/s41598-017-18167-3
  3. Cellular senescence as the key intermediate in tau-mediated neurodegeneration pp.1557-8577, 2018, https://doi.org/10.1089/rej.2018.2155
  4. Human astroviruses: in silico analysis of the untranslated region and putative binding sites of cellular proteins pp.1573-4978, 2018, https://doi.org/10.1007/s11033-018-4498-8
  5. A synonymous RET substitution enhances the oncogenic effect of an in-cis missense mutation by increasing constitutive splicing efficiency vol.14, pp.10, 2018, https://doi.org/10.1371/journal.pgen.1007678
  6. Molecular interactions connecting the function of the serine-arginine–rich protein SRSF1 to protein phosphatase 1 vol.293, pp.43, 2018, https://doi.org/10.1074/jbc.RA118.004587
  7. Coordinate regulation of alternative pre-mRNA splicing events by the human RNA chaperone proteins hnRNPA1 and DDX5 vol.32, pp.15-16, 2018, https://doi.org/10.1101/gad.316034.118
  8. vol.20, pp.9, 2018, https://doi.org/10.1111/1462-2920.14299
  9. New Insights into GFAP Negative Astrocytes in Calbindin D28k Immunoreactive Astrocytes vol.8, pp.8, 2018, https://doi.org/10.3390/brainsci8080143
  10. SRSF6-regulated alternative splicing that promotes tumour progression offers a therapy target for colorectal cancer vol.68, pp.1, 2017, https://doi.org/10.1136/gutjnl-2017-314983
  11. Effects of SRSF1 on subnuclear localization of topoisomerase I pp.07302312, 2019, https://doi.org/10.1002/jcb.28459