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http://dx.doi.org/10.14348/molcells.2017.2319

SR Proteins: Binders, Regulators, and Connectors of RNA  

Jeong, Sunjoo (Department of Bioconvergent Science and Technology, Dankook University)
Publication Information
Molecules and Cells / v.40, no.1, 2017 , pp. 1-9 More about this Journal
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;
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1 Moore, M.J., and Proudfoot, N.J. (2009). Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 136, 688-700.   DOI
2 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.   DOI
3 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.
4 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.   DOI
5 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.   DOI
6 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.   DOI
7 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.   DOI
8 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.   DOI
9 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.   DOI
10 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.   DOI
11 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.   DOI
12 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.   DOI
13 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.   DOI
14 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.   DOI
15 Papasaikas, P., and Valcarcel, J. (2016). The Spliceosome: the ultimate RNA chaperone and sculptor. Trends Biochem. Sci. 41, 33-45.   DOI
16 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.   DOI
17 Perales, R., and Bentley, D. (2009). "Cotranscriptionality": the transcription elongation complex as a nexus for nuclear transactions. Mol. Cell 36, 178-191.   DOI
18 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.   DOI
19 Fu, X.D. (2004). Towards a splicing code. Cell 119, 736-738.   DOI
20 Fu, X.D., and Ares, M., Jr. (2014). Context-dependent control of alternative splicing by RNA-binding proteins. Nat. Rev. Genet. 15, 689-701.   DOI
21 Popp, M.W., and Maquat, L.E. (2014). The dharma of nonsense-mediated mRNA decay in mammalian cells. Mol. Cells 37, 1-8.   DOI
22 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.   DOI
23 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.   DOI
24 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.   DOI
25 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.   DOI
26 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.   DOI
27 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.   DOI
28 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.
29 Ghosh, G., and Adams, J.A. (2011). Phosphorylation mechanism and structure of serine-arginine protein kinases. FEBS J. 278, 587-597.   DOI
30 Geuens, T., Bouhy, D., and Timmerman, V. (2016). The hnRNP family: insights into their role in health and disease. Hum. Genet. 135, 851-867.   DOI
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.   DOI
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.   DOI
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.   DOI
34 Huang, Y.S., and Steitz, J.A. (2001). Splicing factors SRp20 and 9G8 promote the nucleocytoplasmic export of mRNA. Mol. Cell 7, 899-905.   DOI
35 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.   DOI
36 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.   DOI
37 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.   DOI
38 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.   DOI
39 Hsin, J.P., and Manley, J.L. (2012). The RNA polymerase II CTD coordinates transcription and RNA processing. Genes Dev. 26, 2119-2137.   DOI
40 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.   DOI
41 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.   DOI
42 Shepard, P.J., and Hertel, K.J. (2009). The SR protein family. Genome Biol. 10, 242.   DOI
43 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.   DOI
44 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.   DOI
45 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.   DOI
46 Tuerk, C., and Gold, L. (1990). Systemic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 249, 505-510.   DOI
47 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.   DOI
48 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.   DOI
49 Wahl, M.C., Will, C.L., and Luhrmann, R. (2009). The spliceosome: design principles of a dynamic RNP machine. Cell 136, 701-718.   DOI
50 Huang, Y., and Steitz, J.A. (2005). SRprises along a messenger's journey. Mol. Cell 17, 613-615.   DOI
51 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.   DOI
52 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.   DOI
53 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.   DOI
54 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.   DOI
55 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.
56 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.   DOI
57 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.   DOI
58 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.   DOI
59 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.   DOI
60 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.   DOI
61 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.   DOI
62 Jangi, M., and Sharp, P.A. (2014). Building robust transcriptomes with master splicing factors. Cell 159, 487-498.   DOI
63 Jankowsky, E., and Harris, M.E. (2015). Specificity and nonspecificity in RNA-protein interactions. Nat. Rev. Mol. Cell Biol. 16, 533-544.   DOI
64 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.   DOI
65 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.   DOI
66 Kalsotra, A., and Cooper, T.A. (2011). Functional consequences of developmentally regulated alternative splicing. Nat. Rev. Genet. 12, 715-729.
67 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.   DOI
68 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.   DOI
69 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.   DOI
70 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.   DOI
71 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.   DOI
72 Allemand, E., Batsche, E., and Muchardt, C. (2008). Splicing, transcription, and chromatin: a menage a trois. Curr. Opin. Genet. Dev. 18, 145-151.   DOI
73 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.   DOI
74 Anko, M.L. (2014). Regulation of gene expression programmes by serine-arginine rich splicing factors. Semin. Cell Dev. Biol. 32, 11-21.   DOI
75 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.   DOI
76 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.   DOI
77 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.   DOI
78 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.   DOI
79 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.   DOI
80 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.   DOI
81 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.
82 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.   DOI
83 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.   DOI
84 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.
85 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.   DOI
86 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.   DOI
87 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.   DOI
88 Zhou, Z., and Fu, X.D. (2013). Regulation of splicing by SR proteins and SR protein-specific kinases. Chromosoma 122, 191-207.   DOI
89 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.   DOI
90 Bentley, D.L. (2014). Coupling mRNA processing with transcription in time and space. Nat. Rev. Genet. 15, 163-175.
91 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.   DOI
92 Zhang, Z., and Krainer, A.R. (2004). Involvement of SR proteins in mRNA surveillance. Mol. Cell 16, 597-607.   DOI
93 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.   DOI
94 Blencowe, B.J. (2006). Alternative splicing: new insights from global analyses. Cell 126, 37-47.   DOI
95 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.   DOI
96 Bunka, D.H., and Stockley, P.G. (2006). Aptamers come of age - at last. Nat. Rev. Microbiol. 4, 588-596.   DOI
97 Cartegni, L. (2003). ESEfinder: a web resource to identify exonic splicing enhancers. Nucleic Acids Res. 31, 3568-3571.   DOI
98 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.   DOI
99 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.   DOI
100 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.   DOI
101 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.   DOI
102 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.   DOI
103 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.
104 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.   DOI
105 Maniatis, T., and Reed, R. (2002). An extensive network of coupling among gene expression machines. Nature 416, 499-506.   DOI
106 Maniatis, T., and Tasik, B. (2002). Alternative pre-mRNA splicing and proteome expansion in metazoans. Nature 418, 236-243.   DOI
107 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.   DOI
108 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.
109 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.   DOI