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Abstract:

Alternative precursor messenger RNA (pre-mRNA) splicing plays a pivotal role in the flow of genetic information from DNA to proteins by expanding the coding capacity of genomes. Regulation of alternative splicing is as important as regulation of transcription to determine cell- and tissue-specific features, normal cell functioning, and responses of eukaryotic cells to external cues. Its importance is confirmed by the evolutionary conservation and diversification of alternative splicing and the fact that its deregulation causes hereditary disease and cancer. This review discusses the multiple layers of cotranscriptional regulation of alternative splicing in which chromatin structure, DNA methylation, histone marks, and nucleosome positioning play a fundamental role in providing a dynamic scaffold for interactions between the splicing and transcription machineries. We focus on evidence for how the kinetics of RNA polymerase II (RNAPII) elongation and the recruitment of splicing factors and adaptor proteins to chromatin components act in coordination to regulate alternative splicing. Copyright © 2015 by Annual Reviews. All rights reserved.

Registro:

Documento: Artículo
Título:Regulation of alternative splicing through coupling with transcription and chromatin structure
Autor:Naftelberg, S.; Schor, I.E.; Ast, G.; Kornblihtt, A.R.
Filiación:Sackler Medical School, Tel Aviv University, Tel Aviv, 69978, Israel
Instituto de Fisiología, Biología Molecular y Neurociencias, Departamento de Fisiología, Biología Molecular y Celular, Ciudad Universitaria, Buenos Aires, C1428EHA, Argentina
Palabras clave:Alternative splicing; Chromatin organization; Histone modifications; Molecular evolution; Nucleosome positioning; Transcription; adaptor protein; histone; RNA polymerase II; chromatin; nucleosome; alternative RNA splicing; chromatin structure; density; DNA methylation; histone modification; human; kinetics; machine; nonhuman; nucleosome; priority journal; Review; animal; biological model; chromatin; gene expression regulation; genetic transcription; metabolism; protein processing; Eukaryota; Alternative Splicing; Animals; Chromatin; DNA Methylation; Gene Expression Regulation; Histones; Humans; Models, Genetic; Nucleosomes; Protein Processing, Post-Translational; Transcription, Genetic
Año:2015
Volumen:84
Página de inicio:165
Página de fin:198
DOI: http://dx.doi.org/10.1146/annurev-biochem-060614-034242
Título revista:Annual Review of Biochemistry
Título revista abreviado:Annu. Rev. Biochem.
ISSN:00664154
CODEN:ARBOA
CAS:histone, 9062-68-4; Chromatin; Histones; Nucleosomes
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00664154_v84_n_p165_Naftelberg

Referencias:

  • Hynes, R.O., The evolution of metazoan extracellular matrix (2012) J. Cell Biol., 196, pp. 671-679
  • Keren, H., Lev-Maor, G., Ast, G., Alternative splicing and evolution: Diversification, exon definition and function (2010) Nat. Rev. Genet., 11, pp. 345-355
  • Pan, Q., Shai, O., Lee, L.J., Frey, B.J., Blencowe, B.J., Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing (2008) Nat. Genet., 40, pp. 1413-1415
  • Barash, Y., Calarco, J.A., Gao, W., Pan, Q., Wang, X., Deciphering the splicing code (2010) Nature, 465, pp. 53-59
  • Liang, X.H., Haritan, A., Uliel, S., Michaeli, S., Trans and cis splicing in trypanosomatids: Mechanism, factors, and regulation (2003) Eukaryot. Cell, 2, pp. 830-840
  • Howe, K.J., Kane, C.M., Ares, M., Jr., Perturbation of transcription elongation influences the fidelity of internal exon inclusion in Saccharomyces cerevisiae (2003) RNA, 9, pp. 993-1006
  • Kornblihtt, A.R., Schor, I.E., Alló, M., Dujardin, G., Petrillo, E., Muñoz, M.J., Alternative splicing: A pivotal step between eukaryotic transcription and translation (2013) Nat. Rev. Mol. Cell Biol., 14, pp. 153-165
  • Ast, G., How did alternative splicing evolve? (2004) Nat. Rev. Genet., 5, pp. 773-782
  • Kafasla, P., Mickleburgh, I., Llorian, M., Coelho, M., Gooding, C., Defining the roles and interactions of PTB (2012) Biochem. Soc. Trans, 40, pp. 815-820
  • Jelen, N., Ule, J., Zivin, M., Darnell, R.B., Evolution of Nova-dependent splicing regulation in the brain (2007) PLOS Genet., 3, pp. 1838-1847
  • Lee, J.A., Tang, Z.Z., Black, D.L., An inducible change in Fox-1/A2BP1 splicing modulates the alternative splicing of downstream neuronal target exons (2009) Genes Dev., 23, pp. 2284-2293
  • Ule, J., Stefani, G., Mele, A., Ruggiu, M., Wang, X., An RNA map predicting Nova-dependent splicing regulation (2006) Nature, 444, pp. 580-586
  • Chasin, L.A., Searching for splicing motifs (2007) Adv. Exp. Med. Biol., 623, pp. 85-106
  • Liu, Q., Pante, N., Misteli, T., Elsagga, M., Crisp, M., Functional association of Sun1 with nuclear pore complexes (2007) J. Cell Biol., 178, pp. 785-798
  • Martinez-Contreras, R., Cloutier, P., Shkreta, L., Fisette, J.F., Revil, T., Chabot, B., HnRNP proteins and splicing control (2007) Adv. Exp. Med. Biol., 623, pp. 123-147
  • Berget, S.M., Exon recognition in vertebrate splicing (1995) J. Biol. Chem., 270, pp. 2411-2414
  • Ardehali, M.B., Lis, J.T., Tracking rates of transcription and splicing in vivo (2009) Nat. Struct. Mol. Biol., 16, pp. 1123-1124
  • Amit, M., Donyo, M., Hollander, D., Goren, A., Kim, E., Differential GC content between exons and introns establishes distinct strategies of splice-site recognition (2012) Cell Rep., 1, pp. 543-556
  • Eperon, L.P., Graham, I.R., Griffiths, A.D., Eperon, I.C., Effects of RNA secondary structure on alternative splicing of pre-mRNA: Is folding limited to a region behind the transcribing RNA polymerase? (1988) Cell, 54, pp. 393-401
  • Cramer, P., Caceres, J.F., Cazalla, D., Kadener, S., Muro, A.F., Coupling of transcription with alternative splicing: RNA Pol II promoters modulate SF2/ASF and 9G8 effects on an exonic splicing enhancer (1999) Mol. Cell, 4, pp. 251-258
  • Cramer, P., Pesce, C.G., Baralle, F.E., Kornblihtt, A.R., Functional association between promoter structure and transcript alternative splicing (1997) PNAS, 94, pp. 11456-11460
  • Beyer, A.L., Osheim, Y.N., Splice site selection, rate of splicing, and alternative splicing on nascent transcripts (1988) Genes Dev., 2, pp. 754-765
  • Ameur, A., Zaghlool, A., Halvardson, J., Wetterbom, A., Gyllensten, U., Total RNA sequencing reveals nascent transcription and widespread co-transcriptional splicing in the human brain (2011) Nat. Struct. Mol. Biol., 18, pp. 1435-1440
  • Carrillo Oesterreich, F., Preibisch, S., Neugebauer, K.M., Global analysis of nascent RNA reveals transcriptional pausing in terminal exons (2010) Mol. Cell, 40, pp. 571-581
  • Khodor, Y.L., Rodriguez, J., Abruzzi, K.C., Tang, C.H., Marr, M.T., II, Rosbash, M., Nascent-seq indicates widespread cotranscriptional pre-mRNA splicing in Drosophila (2011) Genes Dev., 25, pp. 2502-2512
  • Tilgner, H., Knowles, D.G., Johnson, R., Davis, C.A., Chakrabortty, S., Deep sequencing of subcellular RNA fractions shows splicing to be predominantly co-transcriptional in the human genome but inefficient for lncRNAs (2012) Genome Res., 22, pp. 1616-1625
  • Pandya-Jones, A., Black, D.L., Co-transcriptional splicing of constitutive and alternative exons (2009) RNA, 15, pp. 1896-1908
  • Tardiff, D.F., Lacadie, S.A., Rosbash, M., A genome-wide analysis indicates that yeast pre-mRNA splicing is predominantly posttranscriptional (2006) Mol. Cell, 24, pp. 917-929
  • Görnemann, J., Kotovic, K.M., Hujer, K., Neugebauer, K.M., Cotranscriptional spliceosome assembly occurs in a stepwise fashion and requires the cap binding complex (2005) Mol. Cell, 19, pp. 53-63
  • Lacadie, S.A., Rosbash, M., Cotranscriptional spliceosome assembly dynamics and the role of U1 snRNA: 5′ss base pairing in yeast (2005) Mol. Cell, 19, pp. 65-75
  • Listerman, I., Sapra, A.K., Neugebauer, K.M., Cotranscriptional coupling of splicing factor recruitment and precursor messenger RNA splicing in mammalian cells (2006) Nat. Struct. Mol. Biol., 13, pp. 815-822
  • Wada, Y., Ohta, Y., Xu, M., Tsutsumi, S., Minami, T., A wave of nascent transcription on activated human genes (2009) PNAS, 106, pp. 18357-18361
  • Bhatt, D.M., Pandya-Jones, A., Tong, A.J., Barozzi, I., Lissner, M.M., Transcript dynamics of proinflammatory genes revealed by sequence analysis of subcellular RNA fractions (2012) Cell, 150, pp. 279-290
  • Singh, J., Padgett, R.A., Rates of in situ transcription and splicing in large human genes (2009) Nat. Struct. Mol. Biol., 16, pp. 1128-1133
  • Veloso, A., Kirkconnell, K.S., Magnuson, B., Biewen, B., Paulsen, M.T., Rate of elongation by RNA polymerase II is associated with specific gene features and epigenetic modifications (2014) Genome Res., 24, pp. 896-905
  • Jonkers, I., Kwak, H., Lis, J.T., Genome-wide dynamics of Pol II elongation and its interplay with promoter proximal pausing, chromatin, and exons (2014) ELife, 3, p. e02407
  • Darzacq, X., Shav-Tal, Y., De Turris, V., Brody, Y., Shenoy, S.M., In vivo dynamics of RNA polymerase II transcription (2007) Nat. Struct. Mol. Biol., 14, pp. 796-806
  • Boireau, S., Maiuri, P., Basyuk, E., De La Mata, M., Knezevich, A., The transcriptional cycle of HIV-1 in real-time and live cells (2007) J. Cell Biol., 179, pp. 291-304
  • Schmidt, U., Basyuk, E., Robert, M.C., Yoshida, M., Villemin, J.P., Real-time imaging of cotranscriptional splicing reveals a kinetic model that reduces noise: Implications for alternative splicing regulation (2011) J. Cell Biol., 193, pp. 819-829
  • Martin, R.M., Rino, J., Carvalho, C., Kirchhausen, T., Carmo-Fonseca, M., Live-cell visualization of pre-mRNA splicing with single-molecule sensitivity (2013) Cell Rep., 4, pp. 1144-1155
  • Vargas, D.Y., Shah, K., Batish, M., Levandoski, M., Sinha, S., Single-molecule imaging of transcriptionally coupled and uncoupled splicing (2011) Cell, 147, pp. 1054-1065
  • Pagani, F., Stuani, C., Zuccato, E., Kornblihtt, A.R., Baralle, F.E., Promoter architecture modulates CFTR exon 9 skipping (2003) J. Biol. Chem., 278, pp. 1511-1517
  • Nogues, G., Kadener, S., Cramer, P., Bentley, D., Kornblihtt, A.R., Transcriptional activators differ in their abilities to control alternative splicing (2002) J. Biol. Chem., 277, pp. 43110-43114
  • Auboeuf, D., Honig, A., Berget, S.M., O'malley, B.W., Coordinate regulation of transcription and splicing by steroid receptor coregulators (2002) Science, 298, pp. 416-419
  • Auboeuf, D., Dowhan, D.H., Kang, Y.K., Larkin, K., Lee, J.W., Differential recruitment of nuclear receptor coactivatorsmay determine alternative RNA splice site choice in target genes (2004) PNAS, 101, pp. 2270-2274
  • Auboeuf, D., Dowhan, D.H., Li, X., Larkin, K., Ko, L., CoAA, a nuclear receptor coactivator protein at the interface of transcriptional coactivation and RNA splicing (2004) Mol. Cell. Biol., 24, pp. 442-453
  • Monsalve, M., Wu, Z., Adelmant, G., Puigserver, P., Fan, M., Spiegelman, B.M., Direct coupling of transcription and mRNA processing through the thermogenic coactivator PGC-1 (2000) Mol. Cell, 6, pp. 307-316
  • Guillouf, C., Gallais, I., Moreau-Gachelin, F., Spi-1/PU.1 oncoprotein affects splicing decisions in a promoter binding-dependent manner (2006) J. Biol. Chem., 281, pp. 19145-19155
  • Sánchez-Alvarez, M., Goldstrohm, A.C., Garcia-Blanco, M.A., Suñé, C., Humantranscription elongation factor CA150 localizes to splicing factor-rich nuclear speckles and assembles transcription and splicing components into complexes through its amino and carboxyl regions (2006) Mol. Cell. Biol., 26, pp. 4998-5014
  • Pearson, J.L., Robinson, T.J., Muñoz M..J, Kornblihtt, A.R., Garcia-Blanco, M.A., Identification of the cellular targets of the transcription factor TCERG1 reveals a prevalent role in mRNA processing (2008) J. Biol. Chem., 283, pp. 7949-7961
  • Eliseeva, I.A., Kim, E.R., Guryanov, S.G., Ovchinnikov, L.P., Lyabin, D.N., Y-box-binding protein 1 (YB-1) and its functions (2011) Biochem. Biokhimiia, 76, pp. 1402-1433
  • Das, R., Yu, J., Zhang, Z., Gygi, M.P., Krainer, A.R., SR proteins function in coupling RNAP II transcription to pre-mRNA splicing (2007) Mol. Cell, 26, pp. 867-881
  • Misteli, T., Spector, D.L., RNA polymerase II targets pre-mRNA splicing factors to transcription sites in vivo (1999) Mol. Cell, 3, pp. 697-705
  • Dower, K., Rosbash, M., T7 RNA polymerase-directed transcripts are processed in yeast and link 3′ end formation to mRNA nuclear export (2002) RNA, 8, pp. 686-697
  • McCracken, S., Rosonina, E., Fong, N., Sikes, M., Beyer, A., Role of RNA polymerase II carboxyterminal domain in coordinating transcription with RNA processing (1998) Cold Spring Harb. Symp. Quant. Biol., 63, pp. 301-309
  • Sisodia, S.S., Sollner-Webb, B., Cleveland, D.W., Specificity of RNA maturation pathways: RNAs transcribed by RNA polymerase III are not substrates for splicing or polyadenylation (1987) Mol. Cell. Biol., 7, pp. 3602-3612
  • Smale, S.T., Tjian, R., Transcription of herpes simplex virus tk sequences under the control of wild-type and mutant human RNA polymerase i promoters (1985) Mol. Cell. Biol., 5, pp. 352-362
  • McCracken, S., Fong, N., Yankulov, K., Ballantyne, S., Pan, G., The C-terminal domain of RNA polymerase II couples mRNA processing to transcription (1997) Nature, 385, pp. 357-361
  • Das, R., Dufu, K., Romney, B., Feldt, M., Elenko, M., Reed, R., Functional coupling of RNAP II transcription to spliceosome assembly (2006) Genes Dev., 20, pp. 1100-1109
  • Hicks, M.J., Yang, C.R., Kotlajich, M.V., Hertel, K.J., Linking splicing to Pol II transcription stabilizes pre-mRNAs and influences splicing patterns (2006) PLOS Biol., 4, p. e147
  • Lazarev, D., Manley, J.L., Concurrent splicing and transcription are not sufficient to enhance splicing efficiency (2007) RNA, 13, pp. 1546-1557
  • Romano, M., Marcucci, R., Baralle, F.E., Splicing of constitutive upstream introns is essential for the recognition of intra-exonic suboptimal splice sites in the thrombopoietin gene (2001) Nucleic Acids Res., 29, pp. 886-894
  • Fededa, J.P., Petrillo, E., Gelfand, M.S., Neverov, A.D., Kadener, S., A polar mechanism coordinates different regions of alternative splicing within a single gene (2005) Mol. Cell, 19, pp. 393-404
  • Lenasi, T., Peterlin, B.M., Dovc, P., Distal regulation of alternative splicing by splicing enhancer in equine β-casein intron 1 (2006) RNA, 12, pp. 498-507
  • Ares, M., Jr., Grate, L., Pauling, M.H., A handful of intron-containing genes produces the lion's share of yeast mRNA (1999) RNA, 5, pp. 1138-1139
  • Reed, R., Hurt, E., A conserved mRNA export machinery coupled to pre-mRNA splicing (2002) Cell, 108, pp. 523-531
  • Moore, M.J., Proudfoot, N.J., Pre-mRNA processing reaches back to transcription and ahead to translation (2009) Cell, 136, pp. 688-700
  • Fong, Y.W., Zhou, Q., Stimulatory effect of splicing factors on transcriptional elongation (2001) Nature, 414, pp. 929-933
  • Kwek, K.Y., Murphy, S., Furger, A., Thomas, B., O'gorman, W., U1 snRNA associates with TFIIH and regulates transcriptional initiation (2002) Nat. Struct. Biol., 9, pp. 800-805
  • Furger, A., O'sullivan, J.M., Binnie, A., Lee, B.A., Proudfoot, N.J., Promoter proximal splice sites enhance transcription (2002) Genes Dev., 16, pp. 2792-2799
  • Spiluttini, B., Gu, B., Belagal, P., Smirnova, A.S., Nguyen, V.T., Splicing-independent recruitment of U1 snRNP to a transcription unit in living cells (2010) J. Cell Sci., 123, pp. 2085-2093
  • Brody, Y., Neufeld, N., Bieberstein, N., Causse, S.Z., Böhnlein, E.M., The in vivo kinetics of RNA polymerase II elongation during co-transcriptional splicing (2011) PLOS Biol., 9, p. e1000573
  • Core, L.J., Lis, J.T., Transcription regulation through promoter-proximal pausing of RNA polymerase II (2008) Science, 319, pp. 1791-1792
  • Almada, A.E., Wu, X., Kriz, A.J., Burge, C.B., Sharp, P.A., Promoter directionality is controlled by U1 snRNP and polyadenylation signals (2013) Nature, 499, pp. 360-363
  • Lin, S., Coutinho-Mansfield, G., Wang, D., Pandit, S., Fu, X.D., The splicing factor SC35 has an active role in transcriptional elongation (2008) Nat. Struct. Mol. Biol., 15, pp. 819-826
  • Ji, X., Zhou, Y., Pandit, S., Huang, J., Li, H., SR proteins collaborate with 7SK and promoterassociated nascent RNA to release paused polymerase (2013) Cell, 153, pp. 855-868
  • Alexander, R.D., Innocente, S.A., Barrass, J.D., Beggs, J.D., Splicing-dependent RNA polymerase pausing in yeast (2010) Mol. Cell, 40, pp. 582-593
  • Chathoth, K.T., Barrass, J.D., Webb, S., Beggs, J.D., A splicing-dependent transcriptional checkpoint associated with prespliceosome formation (2014) Mol. Cell, 53, pp. 779-790
  • Muñoz, M.J., De La Mata, M., Kornblihtt, A.R., The carboxy terminal domain of RNA polymerase II and alternative splicing (2010) Trends Biochem. Sci., 35, pp. 497-504
  • Gerber, H.P., Hagmann, M., Seipel, K., Georgiev, O., West, M.A., RNA polymerase II C-terminal domain required for enhancer-driven transcription (1995) Nature, 374, pp. 660-662
  • McCracken, S., Fong, N., Rosonina, E., Yankulov, K., Brothers, G., 5′-Capping enzymes are targeted to pre-mRNA by binding to the phosphorylated carboxy-terminal domain of RNA polymerase II (1997) Genes Dev., 11, pp. 3306-3318
  • Buratowski, S., Progression through the RNA polymerase II CTD cycle (2009) Mol. Cell, 36, pp. 541-546
  • Egloff, S., Dienstbier, M., Murphy, S., Updating the RNA polymerase CTD code: Adding gene-specific layers (2012) Trends Genet., 28, pp. 333-341
  • Heidemann, M., Hintermair, C., Voss, K., Eick, D., Dynamic phosphorylation patterns of RNA polymerase II CTD during transcription (2013) Biochim. Biophys. Acta, 1829, pp. 55-62
  • Hsin, J.P., Manley, J.L., The RNA polymerase IICT Dcoordinates transcription and RNA processing (2012) Genes Dev., 26, pp. 2119-2137
  • Fabrega, C., Shen, V., Shuman, S., Lima, C.D., Structure of an mRNA capping enzyme bound to the phosphorylated carboxy-terminal domain of RNA polymerase II (2003) Mol. Cell, 11, pp. 1549-1561
  • Kim, M., Krogan, N.J., Vasiljeva, L., Rando, O.J., Nedea, E., The yeast Rat1 exonuclease promotes transcription termination by RNA polymerase II (2004) Nature, 432, pp. 517-522
  • Egloff, S., O'reilly, D., Chapman, R.D., Taylor, A., Tanzhaus, K., Serine-7 of the RNA polymerase II CTD is specifically required for snRNA gene expression (2007) Science, 318, pp. 1777-1779
  • Hsin, J.P., Sheth, A., Manley, J.L., RNAP II CTD phosphorylated on threonine-4 is required for histone mRNA 3′ end processing (2011) Science, 334, pp. 683-686
  • Rosonina, E., Blencowe, B.J., Analysis of the requirement for RNA polymerase II CTD heptapeptide repeats in pre-mRNA splicing and 3′-end cleavage (2004) RNA, 10, pp. 581-589
  • De La Mata, M., Kornblihtt, A.R., RNA polymerase II C-terminal domain mediates regulation of alternative splicing by SRp20 (2006) Nat. Struct. Mol. Biol., 13, pp. 973-980
  • Huang, Y., Li, W., Yao, X., Lin, Q.J., Yin, J.W., Mediator complex regulates alternative mRNA processing via the MED23 subunit (2012) Mol. Cell, 45, pp. 459-469
  • Roberts, G.C., Gooding, C., Mak, H.Y., Proudfoot, N.J., Smith, C.W., Co-transcriptional commitment to alternative splice site selection (1998) Nucleic Acids Res., 26, pp. 5568-5572
  • Nogues, G., Muñoz, M.J., Kornblihtt, A.R., Influence of polymerase II processivity on alternative splicing depends on splice site strength (2003) J. Biol. Chem., 278, pp. 52166-52171
  • Ip, J.Y., Schmidt, D., Pan, Q., Ramani, A.K., Fraser, A.G., Global impact of RNA polymerase II elongation inhibition on alternative splicing regulation (2011) Genome Res., 21, pp. 390-401
  • Kadener, S., Cramer, P., Nogues, G., Cazalla, D., De La Mata, M., Antagonistic effects of T-Ag and VP16 reveal a role for RNA Pol II elongation on alternative splicing (2001) EMBO J., 20, pp. 5759-5768
  • Schor, I.E., Rascovan, N., Pelisch, F., Alló, M., Kornblihtt, A.R., Neuronal cell depolarization induces intragenic chromatin modifications affecting NCAM alternative splicing (2009) PNAS, 106, pp. 4325-4330
  • Shukla, S., Kavak, E., Gregory, M., Imashimizu, M., Shutinoski, B., CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing (2011) Nature, 479, pp. 74-79
  • Oberdoerffer, S., A conserved role for intragenic DNA methylation in alternative pre-mRNA splicing (2012) Transcription, 3, pp. 106-109
  • Young, J.I., Hong, E.P., Castle, J.C., Crespo-Barreto, J., Bowman, A.B., Regulation of RNA splicing by the methylation-dependent transcriptional repressor methyl-CpG binding protein 2 (2005) PNAS, 102, pp. 17551-17558
  • Maunakea, A.K., Chepelev, I., Cui, K., Zhao, K., Intragenic DNA methylation modulates alternative splicing by recruiting MeCP2 to promote exon recognition (2013) Cell Res., 23, pp. 1256-1269
  • Close, P., East, P., Dirac-Svejstrup, A.B., Hartmann, H., Heron, M., DBIRD complex integrates alternative mRNA splicing with RNA polymerase II transcript elongation (2012) Nature, 484, pp. 386-389
  • Chen, Y., Chafin, D., Price, D.H., Greenleaf, A.L., Drosophila RNA polymerase II mutants that affect transcription elongation (1996) J. Biol. Chem., 271, pp. 5993-5999
  • De La Mata, M., Alonso, C.R., Kadener, S., Fededa, J.P., Blaustein, M., A slow RNA polymerase II affects alternative splicing in vivo (2003) Mol. Cell, 12, pp. 525-532
  • Montes, M., Cloutier, A., Sánchez-Hernández, N., Michelle, L., Lemieux, B., TCERG1 regulates alternative splicing of the Bcl-x gene by modulating the rate of RNA polymerase II transcription (2012) Mol. Cell. Biol., 32, pp. 751-762
  • De La Mata, M., Lafaille, C., Kornblihtt, A.R., First come, first served revisited: Factors affecting the same alternative splicing event have different effects on the relative rates of intron removal (2010) RNA, 16, pp. 904-912
  • Dutertre, M., Sanchez, G., De Cian, M.C., Barbier, J., Dardenne, E., Cotranscriptional exon skipping in the genotoxic stress response (2010) Nat. Struct. Mol. Biol., 17, pp. 1358-1366
  • Solier, S., Barb, J., Zeeberg, B.R., Varma, S., Ryan, M.C., Genome-wide analysis of novel splice variants induced by topoisomerase i poisoning shows preferential occurrence in genes encoding splicing factors (2010) Cancer Res., 70, pp. 8055-8065
  • Dujardin, G., Buratti, E., Charlet-Berguerand, N., Martins De Araujo, M., Mbopda, A., CELF proteins regulate CFTR pre-mRNA splicing: Essential role of the divergent domain of ETR-3 (2010) Nucleic Acids Res., 38, pp. 7273-7285
  • Dujardin, G., Lafaille, C., De La Mata, M., Marasco, L.E., Muñoz, M.J., How slow RNA polymerase II elongation favors alternative exon skipping (2014) Mol. Cell, 54, pp. 683-690
  • Fong, N., Kim, H., Zhou, Y., Ji, X., Qiu, J., Pre-mRNA splicing is facilitated by an optimal RNA polymerase II elongation rate (2014) Genes Dev., 28, pp. 2663-2676
  • Krainer, A.R., Maniatis, T., Ruskin, B., Green, M.R., Normal and mutant human β-globin pre-mRNAs are faithfully and efficiently spliced in vitro (1984) Cell, 36, pp. 993-1005
  • Padgett, R.A., Hardy, S.F., Sharp, P.A., Splicing of adenovirus RNA in a cell-free transcription system (1983) PNAS, 80, pp. 5230-5234
  • Hernandez, N., Keller, W., Splicing of in vitro synthesized messenger RNA precursors in HeLa cell extracts (1983) Cell, 35, pp. 89-99
  • Huranova, M., Ivani, I., Benda, A., Poser, I., Brody, Y., The differential interaction of snRNPs with pre-mRNA reveals splicing kinetics in living cells (2010) J. Cell Biol., 191, pp. 75-86
  • Simon, J.M., Hacker, K.E., Singh, D., Brannon, A.R., Parker, J.S., Variation in chromatin accessibility in human kidney cancer links H3K36 methyltransferase loss with widespread RNA processing defects (2014) Genome Res., 24, pp. 241-250
  • Zraly, C.B., Dingwall, A.K., The chromatin remodeling and mRNA splicing functions of the Brahma (SWI/SNF) complex are mediated by the SNR1/SNF5 regulatory subunit (2012) Nucleic Acids Res., 40, pp. 5975-5987
  • Zhou, H.L., Luo, G., Wise, J.A., Lou, H., Regulation of alternative splicing by local histonemodifications: Potential roles for RNA-guided mechanisms (2014) Nucleic Acids Res., 42, pp. 701-713
  • Spies, N., Nielsen, C.B., Padgett, R.A., Burge, C.B., Biased chromatin signatures around polyadenylation sites and exons (2009) Mol. Cell, 36, pp. 245-254
  • Schwartz, S., Meshorer, E., Ast, G., Chromatin organizationmarks exon-intron structure (2009) Nat. Struct. Mol. Biol., 16, pp. 990-995
  • Huang, H., Yu, S., Liu, H., Sun, X., Nucleosome organization in sequences of alternative events in human genome (2012) Biosystems, 109, pp. 214-219
  • Tilgner, H., Nikolaou, C., Althammer, S., Sammeth, M., Beato, M., Nucleosome positioning as a determinant of exon recognition (2009) Nat. Struct. Mol. Biol., 16, pp. 996-1001
  • Chen, W., Luo, L., Zhang, L., The organization of nucleosomes around splice sites (2010) Nucleic Acids Res., 38, pp. 2788-2798
  • Gelfman, S., Burstein, D., Penn, O., Savchenko, A., Amit, M., Changes in exon-intron structure during vertebrate evolution affect the splicing pattern of exons (2012) Genome Res., 22, pp. 35-50
  • Schwartz, S., Ast, G., Chromatin density and splicing destiny: On the cross-talk between chromatin structure and splicing (2010) EMBO J., 29, pp. 1629-1636
  • Izban, M.G., Luse, D.S., Transcription on nucleosomal templates by RNA polymerase II in vitro: Inhibition of elongation with enhancement of sequence-specific pausing (1991) Genes Dev., 5, pp. 683-696
  • Petesch, S.J., Lis, J.T., Overcoming the nucleosome barrier during transcript elongation (2012) Trends Genet., 28, pp. 285-294
  • Schor, I.E., Lleres, D., Risso, G.J., Pawellek, A., Ule, J., Perturbation of chromatin structure globally affects localization and recruitment of splicing factors (2012) PLOS ONE, 7, p. e48084
  • Keren-Shaul, H., Lev-Maor, G., Ast, G., Pre-mRNA splicing is a determinant of nucleosome organization (2013) PLOS ONE, 8, p. e53506
  • Beckmann, J.S., Trifonov, E.N., Splice junctions follow a 205-base ladder (1991) PNAS, 88, pp. 2380-2383
  • De Conti, L., Baralle, M., Buratti, E., Exon and intron definition in pre-mRNA splicing (2013) Wiley Interdiscip. Rev. RNA, 4, pp. 49-60
  • Clapier, C.R., Cairns, B.R., The biology of chromatin remodeling complexes (2009) Annu. Rev. Biochem., 78, pp. 273-304
  • Mohrmann, L., Verrijzer, C.P., Composition and functional specificity of SWI2/SNF2 class chromatin remodeling complexes (2005) Biochim. Biophys. Acta, 1681, pp. 59-73
  • Bouazoune, K., Brehm, A., ATP-dependent chromatin remodeling complexes in Drosophila (2006) Chromosome Res., 14, pp. 433-449
  • Zentner, G.E., Tsukiyama, T., Henikoff, S., ISWI and CHD chromatin remodelers bind promoters but act in gene bodies (2013) PLOS Genet., 9, p. e1003317
  • Batsché, E., Yaniv, M., Muchardt, C., The human SWI/SNF subunit Brm is a regulator of alternative splicing (2006) Nat. Struct. Mol. Biol., 13, pp. 22-29
  • Tyagi, A., Ryme, J., Brodin, D., Östlund Farrants, A.K., Visa, N., SWI/SNF associates with nascent pre-mRNPs and regulates alternative pre-mRNA processing (2009) PLOS Genet., 5, p. e1000470
  • Subtil-Rodríguez, A., Reyes, J.C., To cross or not to cross the nucleosome, that is the elongation question (2011) RNA Biol., 8, pp. 389-393
  • Cavellan, E., Asp, P., Percipalle, P., Farrants, A.K., TheWSTF-SNF2h chromatin remodeling complex interacts with several nuclear proteins in transcription (2006) J. Biol. Chem., 281, pp. 16264-16271
  • Yu, S., Waldholm, J., Bohm, S., Visa, N., Brahma regulates a specific trans-splicing event at the mod(mdg4) locus of Drosophila melanogaster (2014) RNA Biol., 11, pp. 134-145
  • Murawska, M., Brehm, A., CHD chromatin remodelers and the transcription cycle (2011) Transcription, 2, pp. 244-253
  • Tai, H.H., Geisterfer, M., Bell, J.C., Moniwa, M., Davie, J.R., CHD1 associates with NCoR and histone deacetylase as well as with RNA splicing proteins (2003) Biochem. Biophys. Res. Commun., 308, pp. 170-176
  • Sims, R.J., III, Millhouse, S., Chen, C.F., Lewis, B.A., Erdjument-Bromage, H., Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing (2007) Mol. Cell, 28, pp. 665-676
  • Hnilicova, J., Hozeifi, S., Duskova, E., Icha, J., Tomankova, T., Stanek, D., Histone deacetylase activity modulates alternative splicing (2011) PLOS ONE, 6, p. e16727
  • Tolstorukov, M.Y., Volfovsky, N., Stephens, R.M., Park, P.J., Impact of chromatin structure on sequence variability in the human genome (2011) Nat. Struct. Mol. Biol., 18, pp. 510-515
  • Gluckman, P.D., Hanson, M.A., Buklijas, T., Low, F.M., Beedle, A.S., Epigenetic mechanisms that underpin metabolic and cardiovascular diseases (2009) Nat. Rev. Endocrinol., 5, pp. 401-408
  • Mehler, M.F., Epigenetic principles and mechanisms underlying nervous system functions in health and disease (2008) Prog. Neurobiol, 86, pp. 305-341
  • Graff, J., Mansuy, I.M., Epigenetic dysregulation in cognitive disorders (2009) Eur. J. Neurosci, 30, pp. 1-8
  • Weidman, J.R., Dolinoy, D.C., Murphy, S.K., Jirtle, R.L., Cancer susceptibility: Epigenetic manifestation of environmental exposuRes (2007) Cancer J., 13, pp. 9-16
  • Cao, F., Townsend, E.C., Karatas, H., Xu, J., Li, L., Targeting MLL1 H3K4 methyltransferase activity in mixed-lineage leukemia (2014) Mol. Cell, 53, pp. 247-261
  • Karlic, R., Chung, H.R., Lasserre, J., Vlahovicek, K., Vingron, M., Histone modification levels are predictive for gene expression (2010) PNAS, 107, pp. 2926-2931
  • Hodges, E., Smith, A.D., Kendall, J., Xuan, Z., Ravi, K., High definition profiling of mammalian DNA methylation by array capture and single molecule bisulfite sequencing (2009) Genome Res., 19, pp. 1593-1605
  • Chodavarapu, R.K., Feng, S., Bernatavichute, Y.V., Chen, P.Y., Stroud, H., Relationship between nucleosome positioning and DNA methylation (2010) Nature, 466, pp. 388-392
  • Hon, G.C., Hawkins, R.D., Ren, B., Predictive chromatin signatures in the mammalian genome (2009) Hum. Mol. Genet., 18, pp. R195-R201
  • Dhami, P., Saffrey, P., Bruce, A.W., Dillon, S.C., Chiang, K., Complex exon-intron marking by histone modifications is not determined solely by nucleosome distribution (2010) PLOS ONE, 5, p. e12339
  • Fuchs, G., Hollander, D., Voichek, Y., Ast, G., Oren, M., Co-transcriptional histone H2B monoubiquitylation is tightly coupled with RNA polymerase II elongation rate (2014) Genome Res., 24, pp. 1572-1583
  • Zhou, H.L., Hinman, M.N., Barron, V.A., Geng, C., Zhou, G., Hu proteins regulate alternative splicing by inducing localized histone hyperacetylation in an RNA-dependent manner (2011) PNAS, 108, pp. E627-E635
  • Khan, D.H., Gonzalez, C., Cooper, C., Sun, J.M., Chen, H.Y., RNA-dependent dynamic histone acetylation regulates MCL1 alternative splicing (2014) Nucleic Acids Res., 42, pp. 1656-1670
  • Luco, R.F., Pan, Q., Tominaga, K., Blencowe, B.J., Pereira-Smith, O.M., Misteli, T., Regulation of alternative splicing by histone modifications (2010) Science, 327, pp. 996-1000
  • Llorian, M., Schwartz, S., Clark, T.A., Hollander, D., Tan, L.Y., Position-dependent alternative splicing activity revealed by global profiling of alternative splicing events regulated by PTB (2010) Nat. Struct. Mol. Biol., 17, pp. 1114-1123
  • Pradeepa, M.M., Sutherland, H.G., Ule, J., Grimes, G.R., Bickmore, W.A., Psip1/Ledgf p52 binds methylated histoneH3K36 and splicing factors and contributes to the regulation of alternative splicing (2012) PLOS Genet., 8, p. e1002717
  • Loomis, R.J., Naoe, Y., Parker, J.B., Savic, V., Bozovsky, M.R., Chromatin binding of SRp20 and ASF/SF2 and dissociation from mitotic chromosomes is modulated by histone H3 serine 10 phosphorylation (2009) Mol. Cell, 33, pp. 450-461
  • Guo, R., Zheng, L., Park, J.W., Lv, R., Chen, H., BS69/ZMYND11 reads and connects histone H3.3 lysine 36 trimethylation-decorated chromatin to regulated pre-mRNA processing (2015) Mol. Cell, 205, pp. 298-310
  • Park, G., Gong, Z., Chen, J., Kim, J.E., Characterization of theDOT1Lnetwork: Implications of diverse roles for DOT1L (2010) Protein J., 29, pp. 213-223
  • Yuan, W., Xie, J., Long, C., Erdjument-Bromage, H., Ding, X., Heterogeneous nuclear ribonucleoprotein L is a subunit of human KMT3a/Set2 complex required for H3 Lys-36 trimethylation activity in vivo (2009) J. Biol. Chem., 18 (284), pp. 15701-15707
  • Gunderson, F.Q., Johnson, T.L., Acetylation by the transcriptional coactivator Gcn5 plays a novel role in co-transcriptional spliceosome assembly (2009) PLOS Genet., 5, p. e1000682
  • Zhang, Z., Jones, A., Joo, H.Y., Zhou, D., Cao, Y., USP49 deubiquitinates histone H2B and regulates cotranscriptional pre-mRNA splicing (2013) Genes Dev., 27, pp. 1581-1595
  • Moehle, E.A., Ryan, C.J., Krogan, N.J., Kress, T.L., Guthrie, C., The yeast SR-like protein Npl3 links chromatin modification to mRNA processing (2012) PLOS Genet., 8, p. e1003101
  • Hino, K., Hirose, T., Possible involvement of snoRNA in alternative splicing regulation (2009) Tanpakushitsu Kakusan Koso, 54, pp. 2049-2054. , In Japanese
  • Chandrasekharan, M.B., Huang, F., Sun, Z.W., Ubiquitination of histone H2B regulates chromatin dynamics by enhancing nucleosome stability (2009) PNAS, 106, pp. 16686-16691
  • Long, L., Thelen, J.P., Furgason, M., Haj-Yahya, M., Brik, A., The U4/U6 recycling factor SART3 has histone chaperone activity and associates with USP15 to regulate H2B deubiquitination (2014) J. Biol. Chem., 289, pp. 8916-8930
  • Gelfman, S., Cohen, N., Yearim, A., Ast, G., DNA-methylation effect on cotranscriptional splicing is dependent on GC architecture of the exon-intron structure (2013) Genome Res., 23, pp. 789-799
  • Choi, J.K., Contrasting chromatin organization of CpG islands and exons in the human genome (2010) Genome Biol., 11, p. R70
  • Laurent, L., Wong, E., Li, G., Huynh, T., Tsirigos, A., Dynamic changes in the human methylome during differentiation (2010) Genome Res., 20, pp. 320-331
  • Sarraf, S.A., Stancheva, I., Methyl-CpG binding protein MBD1 couples histone H3 methylation at lysine 9 by SETDB1 to DNA replication and chromatin assembly (2004) Mol. Cell, 15, pp. 595-605
  • Klose, R.J., Bird, A.P., Genomic DNA methylation: The mark and its mediators (2006) Trends Biochem. Sci., 31, pp. 89-97
  • Boeke, J., Ammerpohl, O., Kegel, S., Moehren, U., Renkawitz, R., The minimal repression domain of MBD2b overlaps with the methyl-CpG-binding domain and binds directly to Sin3A (2000) J. Biol. Chem., 275, pp. 34963-34967
  • Piazza, R., Magistroni, V., Mogavero, A., Andreoni, F., Ambrogio, C., Epigenetic silencing of the proapoptotic gene BIM in anaplastic large cell lymphoma through an MeCP2/SIN3a deacetylating complex (2013) Neoplasia, 15, pp. 511-522
  • Long, S.W., Ooi, J.Y., Yau, P.M., Jones, P.L., A brain-derived MeCP2 complex supports a role for MeCP2 in RNA processing (2011) Biosci. Rep., 31, pp. 333-343
  • Huang, L., Fu, H., Lin, C.M., Conner, A.L., Zhang, Y., Aladjem, M.I., Prevention of transcriptional silencing by a replicator-binding complex consisting of SWI/SNF, MeCP1, and hnRNP C1/C2 (2011) Mol. Cell. Biol., 31, pp. 3472-3484
  • Mahajan, M.C., Narlikar, G.J., Boyapaty, G., Kingston, R.E., Weissman, S.M., Heterogeneous nuclear ribonucleoprotein C1/C2, MeCP1, and SWI/SNF form a chromatin remodeling complex at theβ-globin locus control region (2005) PNAS, 102, pp. 15012-15017
  • Zarnack, K., König, J., Tajnik, M., Martincorena, I., Eustermann, S., Direct competition between hnRNPCand U2AF65 protects the transcriptome from the exonization of Alu elements (2013) Cell, 152, pp. 453-466
  • Kwon, S.H., Florens, L., Swanson, S.K., Washburn, M.P., Abmayr, S.M., Workman, J.L., Heterochromatin protein 1 (HP1) connects the FACT histone chaperone complex to the phosphorylated CTD of RNA polymerase II (2010) Genes Dev., 24, pp. 2133-2145
  • Grewal, S.I., Moazed, D., Heterochromatin and epigenetic control of gene expression (2003) Science, 301, pp. 798-802
  • Piacentini, L., Fanti, L., Negri, R., Del Vescovo, V., Fatica, A., Heterochromatin protein 1 (HP1a) positively regulates euchromatic gene expression through RNA transcript association and interaction with hnRNPs in Drosophila (2009) PLOS Genet., 5, p. e1000670
  • Freitag, M., Hickey, P.C., Khlafallah, T.K., Read, N.D., Selker, E.U., HP1is essential forDNAmethylation in Neurospora (2004) Mol. Cell, 13, pp. 427-434
  • Yearim, A., Gelfman, S., Shayevitch, R., Melcer, S., Glaich, O., HP1 is involved in regulating the global impact of DNA methylation on alternative splicing (2015) Cell Rep., 10, pp. 1122-1134
  • Salton, M., Voss, T.C., Misteli, T., Identification by high-throughput imaging of the histone methyltransferaseEHMT2as an epigenetic regulator ofVEGFAalternative splicing (2014) Nucleic Acids Res., pp. 4213662-4213673
  • Alló, M., Buggiano, V., Fededa, J.P., Petrillo, E., Schor, I., Control of alternative splicing through siRNA-mediated transcriptional gene silencing (2009) Nat. Struct. Mol. Biol., 16, pp. 717-724
  • Saint-André, V., Batsché, E., Rachez, C., Muchardt, C., Histone H3 lysine 9 trimethylation and HP1γ favor inclusion of alternative exons (2011) Nat. Struct. Mol. Biol., 18, pp. 337-344
  • Ameyar-Zazoua, M., Rachez, C., Souidi, M., Robin, P., Fritsch, L., Argonaute proteins couple chromatin silencing to alternative splicing (2012) Nat. Struct. Mol. Biol., 19, pp. 998-1004
  • De Almeida, S.F., Grosso, A.R., Koch, F., Fenouil, R., Carvalho, S., Splicing enhances recruitment of methyltransferase HYPB/Setd2 and methylation of histone H3 Lys36 (2011) Nat. Struct. Mol. Biol., 18, pp. 977-983
  • Kim, S., Kim, H., Fong, N., Erickson, B., Bentley, D.L., Pre-mRNA splicing is a determinant of histone H3K36 methylation (2011) PNAS, 108, pp. 13564-13569
  • Edmunds, J.W., Mahadevan, L.C., Clayton, A.L., Dynamic histone H3 methylation during gene induction: HYPB/Setd2 mediates all H3K36 trimethylation (2008) EMBO J., 27, pp. 406-420
  • Luco, R.F., Alló, M., Schor, I.E., Kornblihtt, A.R., Misteli, T., Epigenetics in alternative pre-mRNA splicing (2011) Cell, 144, pp. 16-26
  • Convertini, P., Shen, M., Potter, P.M., Palacios, G., Lagisetti, C., SudemycinEinfluences alternative splicing and changes chromatin modifications (2014) Nucleic Acids Res., 42, pp. 4947-4961
  • Yuan, W., Xie, J., Long, C., Erdjument-Bromage, H., Ding, X., Heterogeneous nuclear ribonucleoprotein L is a subunit of human KMT3a/Set2 complex required for H3 Lys-36 trimethylation activity in vivo (2009) J. Biol. Chem., 284, pp. 15701-15707
  • Kalsotra, A., Cooper, T.A., Functional consequences of developmentally regulated alternative splicing (2011) Nat. Rev. Genet., 12, pp. 715-729
  • Tollervey, J.R., Wang, Z., Hortobágyi, T., Witten, J.T., Zarnack, K., Analysis of alternative splicing associated with aging and neurodegeneration in the human brain (2011) Genome Res., 21, pp. 1572-1582
  • Witten, J.T., Ule, J., Understanding splicing regulation through RNA splicing maps (2011) Trends Genet., 27, pp. 89-97
  • Gabut, M., Samavarchi-Tehrani, P., Wang, X., Slobodeniuc, V., O'hanlon, D., An alternative splicing switch regulates embryonic stem cell pluripotency and reprogramming (2011) Cell, 147, pp. 132-146
  • Ungewitter, E., Scrable, H., δ40p53 controls the switch from pluripotency to differentiation by regulating IGF signaling in ESCs (2010) Genes Dev., 24, pp. 2408-2419
  • Revil, T., Gaffney, D., Dias, C., Majewski, J., Jerome-Majewska, L.A., Alternative splicing is frequent during early embryonic development in mouse (2010) BMC Genomics, 11, p. 399
  • Xu, X., Yang, D., Ding, J.H., Wang, W., Chu, P.H., ASF/SF2-regulated CaMKIIδ alternative splicing temporally reprograms excitation-contraction coupling in cardiac muscle (2005) Cell, 120, pp. 59-72
  • Preitner, N., Quan, J., Nowakowski, D.W., Hancock, M.L., Shi, J., APC is an RNA-binding protein, and its interactome provides a link to neural development and microtubule assembly (2014) Cell, 158, pp. 368-382
  • Jiang, H., Shukla, A., Wang, X., Chen, W.Y., Bernstein, B.E., Roeder, R.G., Role forDpy-30 in ES cell-fate specification by regulation of H3K4 methylation within bivalent domains (2011) Cell, 144, pp. 513-525
  • Su, W.L., Modrek, B., Guha Thakurta, D., Edwards, S., Shah, J.K., Exon and junction microarrays detect widespread mouse strain- and sex-bias expression differences (2008) BMC Genomics, 9, p. 273
  • Blekhman, R., Marioni, J.C., Zumbo, P., Stephens, M., Gilad, Y., Sex-specific and lineage-specific alternative splicing in primates (2010) Genome Res., 20, pp. 180-189
  • Salz, H.K., Sex determination in insects: A binary decision based on alternative splicing (2011) Curr. Opin. Genet. Dev., 21, pp. 395-400
  • Wang, G.S., Cooper, T.A., Splicing in disease: Disruption of the splicing code and the decoding machinery (2007) Nat. Rev. Genet., 8, pp. 749-761
  • Baralle, D., Lucassen, A., Buratti, E., Missed threads. The impact of pre-mRNA splicing defects on clinical practice (2009) EMBO Rep., 10, pp. 810-816
  • Wang, E.T., Sandberg, R., Luo, S., Khrebtukova, I., Zhang, L., Alternative isoform regulation in human tissue transcriptomes (2008) Nature, 456, pp. 470-476
  • Merkin, J., Russell, C., Chen, P., Burge, C.B., Evolutionary dynamics of gene and isoform regulation in mammalian tissues (2012) Science, 338, pp. 1593-1599
  • Reyes, A., Anders, S., Weatheritt, R.J., Gibson, T.J., Steinmetz, L.M., Huber, W., Drift and conservation of differential exon usage across tissues in primate species (2013) PNAS, 110, pp. 15377-15382
  • Penalva, L.O., Sanchez, L., RNA binding protein sex-lethal (Sxl) and control of Drosophila sex determination and dosage compensation (2003) Microbiol. Mol. Biol. Rev., 67, pp. 343-359
  • Grosso, A.R., Gomes, A.Q., Barbosa-Morais, N.L., Caldeira, S., Thorne, N.P., Tissue-specific splicing factor gene expression signatuRes (2008) Nucleic Acids Res., 36, pp. 4823-4832
  • Sun, H., Wu, J., Wickramasinghe, P., Pal, S., Gupta, R., Genome-wide mapping of RNA Pol-II promoter usage in mouse tissues by ChIP-seq (2011) Nucleic Acids Res., 39, pp. 190-201
  • Pecci, A., Viegas, L.R., Barañao, J.L., Beato, M., Promoter choice influences alternative splicing and determines the balance of isoforms expressed from the mouse bcl-X gene (2001) J. Biol. Chem., 276, pp. 21062-21069
  • Li, B., Carey, M., Workman, J.L., The role of chromatin during transcription (2007) Cell, 128, pp. 707-719
  • Schor, I.E., Fiszbein, A., Petrillo, E., Kornblihtt, A.R., Intragenic epigenetic changes modulate NCAM alternative splicing in neuronal differentiation (2013) EMBO J., 32, pp. 2264-2274
  • Kucharski, R., Maleszka, J., Foret, S., Maleszka, R., Nutritional control of reproductive status in honeybees via DNA methylation (2008) Science, 319, pp. 1827-1830
  • Foret, S., Kucharski, R., Pellegrini, M., Feng, S., Jacobsen, S.E., DNA methylation dynamics, metabolic fluxes, gene splicing, and alternative phenotypes in honey bees (2012) PNAS, 109, pp. 4968-4973
  • Mercer, T.R., Edwards, S.L., Clark, M.B., Neph, S.J., Wang, H., DNase I-hypersensitive exons colocalize with promoters and distal regulatory elements (2013) Nat. Genet., 45, pp. 852-859
  • Mayshar, Y., Rom, E., Chumakov, I., Kronman, A., Yayon, A., Benvenisty, N., Fibroblast growth factor 4 and its novel splice isoform have opposing effects on the maintenance of human embryonic stem cell self-renewal (2008) Stem Cells, 26, pp. 767-774
  • Salomonis, N., Schlieve, C.R., Pereira, L., Wahlquist, C., Colas, A., Alternative splicing regulates mouse embryonic stem cell pluripotency and differentiation (2010) PNAS, 107, pp. 10514-10519
  • Cheong, C.Y., Lufkin, T., Alternative splicing in self-renewal of embryonic stem cells (2011) Stem Cells Int, 2011, p. 560261
  • Ohta, S., Nishida, E., Yamanaka, S., Yamamoto, T., Global splicing pattern reversion during somatic cell reprogramming (2013) Cell Rep., 5, pp. 357-366
  • Lu, X., Goke, J., Sachs, F., Jacques, P.E., Liang, H., SON connects the splicing-regulatory network with pluripotency in human embryonic stem cells (2013) Nat. Cell Biol., 15, pp. 1141-1152
  • Bittencourt, D., Dutertre, M., Sanchez, G., Barbier, J., Gratadou, L., Auboeuf, D., Cotranscriptional splicing potentiates the mRNA production from a subset of estradiol-stimulated genes (2008) Mol. Cell. Biol., 28, pp. 5811-5824
  • Iwasaki, T., Chin, W.W., Ko, L., Identification and characterization of RRM-containing coactivator activator (CoAA) as TRBP-interacting protein, and its splice variant as a coactivator modulator (CoAM) (2001) J. Biol. Chem., 276, pp. 33375-33383
  • Fischle, W., Tseng, B.S., Dormann, H.L., Ueberheide, B.M., Garcia, B.A., Regulation of HP1- chromatin binding by histone H3 methylation and phosphorylation (2005) Nature, 438, pp. 1116-1122
  • Hirota, T., Lipp, J.J., Toh, B.H., Peters, J.M., Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin (2005) Nature, 438, pp. 1176-1180
  • Muñoz, M.J., Perez Santangelo, M.S., Paronetto, M.P., De La Mata, M., Pelisch, F., DNA damage regulates alternative splicing through inhibition of RNA polymerase II elongation (2009) Cell, 137, pp. 708-720
  • Kim, E., Magen, A., Ast, G., Different levels of alternative splicing among eukaryotes (2007) Nucleic Acids Res., 35, pp. 125-131
  • Xiao, X., Wang, Z., Jang, M., Burge, C.B., Coevolutionary networks of splicing cis-regulatory elements (2007) PNAS, 104, pp. 18583-18588
  • Xiao, X., Wang, Z., Jang, M., Nutiu, R., Wang, E.T., Burge, C.B., Splice site strength-dependent activity and genetic buffering by poly-G runs (2009) Nat. Struct. Mol. Biol., 16, pp. 1094-1100
  • Goren, A., Ram, O., Amit, M., Keren, H., Lev-Maor, G., Comparative analysis identifies exonic splicing regulatory sequences - The complex definition of enhancers and silencers (2006) Mol. Cell, 22, pp. 769-781
  • Sorek, R., Ast, G., Intronic sequences flanking alternatively spliced exons are conserved between human and mouse (2003) Genome Res., 13, pp. 1631-1637
  • Xing, Y., Lee, C., Alternative splicing and RNA selection pressure-evolutionary consequences for eukaryotic genomes (2006) Nat. Rev. Genet., 7, pp. 499-509
  • Fairbrother, W.G., Yeh, R.F., Sharp, P.A., Burge, C.B., Predictive identification of exonic splicing enhancers in human genes (2002) Science, 297, pp. 1007-1013
  • Sugnet, C.W., Srinivasan, K., Clark, T.A., O'brien, G., Cline, M.S., Unusual intron conservation near tissue-regulated exons found by splicing microarrays (2006) PLOS Comput. Biol., 2, p. e4
  • Sorek, R., Ast, G., Graur, D., Alu-containing exons are alternatively spliced (2002) Genome Res., 12, pp. 1060-1067
  • Lev-Maor, G., Sorek, R., Shomron, N., Ast, G., The birth of an alternatively spliced exon: 3′ splice-site selection in Alu exons (2003) Science, 300, pp. 1288-1291
  • Sorek, R., Lev-Maor, G., Reznik, M., Dagan, T., Belinky, F., Minimal conditions for exonization of intronic sequences: 5′ splice site formation in Alu exons (2004) Mol. Cell, 14, pp. 221-231
  • Magen, A., Ast, G., The importance of being divisible by three in alternative splicing (2005) Nucleic Acids Res., 33, pp. 5574-5582
  • Sela, N., Mersch, B., Gal-Mark, N., Lev-Maor, G., Hotz-Wagenblatt, A., Ast, G., Comparative analysis of transposed element insertion within human and mouse genomes reveals Alu's unique role in shaping the human transcriptome (2007) Genome Biol., 8, p. R127
  • Lev-Maor, G., Goren, A., Sela, N., Kim, E., Keren, H., The "alternative" choice of constitutive exons throughout evolution (2007) PLOS Genet., 3, p. e203
  • Koren, E., Lev-Maor, G., Ast, G., The emergence of alternative 3′ and 5′ splice site exons from constitutive exons (2007) PLOS Comput. Biol., 3, p. e95
  • Ram, O., Ast, G., SR proteins: A foot on the exon before the transition from intron to exon definition (2007) Trends Genet., 23, pp. 5-7
  • Hertel, K.J., Combinatorial control of exon recognition (2008) J. Biol. Chem., 283, pp. 1211-1215
  • Niu, D.K., Exon definition as a potential negative force against intron losses in evolution (2008) Biol. Direct, 3, p. 46

Citas:

---------- APA ----------
Naftelberg, S., Schor, I.E., Ast, G. & Kornblihtt, A.R. (2015) . Regulation of alternative splicing through coupling with transcription and chromatin structure. Annual Review of Biochemistry, 84, 165-198.
http://dx.doi.org/10.1146/annurev-biochem-060614-034242
---------- CHICAGO ----------
Naftelberg, S., Schor, I.E., Ast, G., Kornblihtt, A.R. "Regulation of alternative splicing through coupling with transcription and chromatin structure" . Annual Review of Biochemistry 84 (2015) : 165-198.
http://dx.doi.org/10.1146/annurev-biochem-060614-034242
---------- MLA ----------
Naftelberg, S., Schor, I.E., Ast, G., Kornblihtt, A.R. "Regulation of alternative splicing through coupling with transcription and chromatin structure" . Annual Review of Biochemistry, vol. 84, 2015, pp. 165-198.
http://dx.doi.org/10.1146/annurev-biochem-060614-034242
---------- VANCOUVER ----------
Naftelberg, S., Schor, I.E., Ast, G., Kornblihtt, A.R. Regulation of alternative splicing through coupling with transcription and chromatin structure. Annu. Rev. Biochem. 2015;84:165-198.
http://dx.doi.org/10.1146/annurev-biochem-060614-034242