Identification of U2AF(35)-dependent exons by RNA-Seq reveals a link between 3′ splice-site organization and activity of U2AF-related proteins

Nucleic Acids Research

Volumn 43, Issue 7, 2015, Pages 3747-3763

  Kralovicova, Jana ^a   Knut, Marcin ^a   Cross, Nicholas C P ^a,b   Vorechovsky, Igor ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b SALISBURY DISTRICT HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

SINGLE STRANDED RNA; SMALL NUCLEAR RIBONUCLEOPROTEIN; NUCLEAR PROTEIN; RIBONUCLEOPROTEIN; U2AF1 PROTEIN, HUMAN;

3' UNTRANSLATED REGION; ALTERNATIVE RNA SPLICING; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME ACTIVATION; EXON; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; INTRON; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS REGULATION; RNA PROCESSING; RNA SPLICING; SEQUENCE ANALYSIS; UPREGULATION; GENETICS; HEK293 CELL LINE; VALIDATION STUDY;

EXONS; HEK293 CELLS; HUMANS; NUCLEAR PROTEINS; RIBONUCLEOPROTEINS; RNA SPLICING; SEQUENCE ANALYSIS, RNA;

EID: 84930506414     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv194     Document Type: Article

References (100)

1. Wahl, M.C, Will, C.L. and Lührmann, R. (2009) The spliceosome: design principles of a dynamic RNP machine. Cell, 136, 701-718.
2. Shcherbakova, I., Hoskins, A.A., Friedman, L.J., Serebrov, V, Correa, I.R. Jr, Xu, M.Q., Gelles, J. and Moore, M.J. (2013) Alternative spliceosome assembly pathways revealed by single-molecule fuorescence microscopy. Cell Rep., 5, 151-165.
3. Ruskin, B., Zamore, P.D. and Green, M.R. (1988) A factor, U2AF, is required for U2 snRNP binding and splicing complex assembly. Cell, 52, 207-219.
4. Zamore, P.D. and Green, M.R. (1989) Identifcation, purifcation, and biochemical characterization of U2 small nuclear ribonucleoprotein auxiliary factor. Proc. Natl Acad. Sci. U.S.A., 86, 9243-9247.
5. Zorio, D.A. and Blumenthal, T. (1999) Both subunits of U2AF recognize the 3' splice site in Caenorhabditis elegans. Nature, 402, 835-838.
6. Merendino, L., Guth, S., Bilbao, D., Martinez, C. and Valcarcel, J. (1999) Inhibition of msl-2 splicing by Sex-lethal reveals interaction between U2AF35 and the 3' splice site AG. Nature, 402, 838-841.
7. Wu, S., Romfo, C.M., Nilsen, T.W. and Green, M.R. (1999) Functional recognition of the 3' splice site AG by the splicing factor U2AF35. Nature, 402, 832-835.
8. Guth, S., Tange, T.O., Kellenberger, E. and Valcárcel, J. (2001) Dual function for U2AF(35) in AG-dependent pre-mRNA splicing. Mol Cell. Biol, 21, 7673-7681.
9. Pacheco, T.R., Gomes, A.Q., Barbosa-Morais, N.L., Benes, V., Ansorge, W., Wollerton, M., Smith, C.W., Valcárcel, J. and Carmo-Fonseca, M. (2004) Diversity of vertebrate splicing factor U2AF35: identifcation of alternatively spliced U2AF1 mRNAS. J. Biol. Chem., 279, 27039-27049.
10. Zhang, M., Zamore, PD., Carmo-Fonseca, M., Lamond, A.I. and Green, M.R. (1992) Cloning and intracellular localization of the U2 small nuclear ribonucleoprotein auxiliary factor small subunit. Proc. Natl Acad. Sci. U.S.A., 89, 8769-8773.
11. Birney, E., Kumar, S. and Krainer, A.R. (1993) Analysis of the RNA-recognition motif and RS and RGG domains: conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res., 21, 5803-5816.
12. Rudner, D.Z., Breger, K.S. and Rio, DC. (1998) Molecular genetic analysis of the heterodimeric splicing factor U2AF: the RS domain on either the large or small Drosophila subunit is dispensable in vivo. GenesDev., 12, 1010-1021.
13. Kielkopf, C.L., Lucke, S. and Green, M.R. (2004) U2AF homology motifs: protein recognition in the RRM world. Genes Dev., 18, 1513-1526.
14. Pacheco, T.R., Coelho, M.B., Desterro, J.M., Mollet, I. and Carmo-Fonseca, M. (2006) In vivo requirement of the small subunit of U2AF for recognition of a weak 3' splice site. Mol. Cell. Biol, 26, 8183-8190.
15. Wang, B.B. and Brendel, V. (2006) Molecular characterization and phylogeny of U2AF35 homologs in plants. Plant Physiol., 140, 624-636.
16. Rudner, D., Kannar, K., Breger, S. and Rio, D (1996) Mutations in the small subunit of the Drosophila U2AF splicing factors cause lethality and developmental defects. Proc. Natl Acad. Sci. U.S.A., 93, 10333-10337.
17. Zorio, D.A. and Blumenthal, T. (1999) U2AF35 is encoded by an essential gene clustered in an operon with RRM/cyclophilin in Caenorhabditis elegans. RNA, 5, 487-494.
18. Golling, G., Amsterdam, A., Sun, Z., Antonelli, M., Maldonado, E., Chen, W., Burgess, S., Haldi, M., Artzt, K., Farrington, S. et al. (2002) Insertional mutagenesis in zebrafsh rapidly identifes genes essential for early vertebrate development. Nat. Genet., 31, 135-140.
19. Webb, C.J., Lakhe-Reddy, S., Romfo, C.M. and Wise, J.A. (2005) Analysis of mutant phenotypes and splicing defects demonstrates functional collaboration between the large and small subunits of the essential splicing factor U2AF in vivo. Mol. Biol. Cell, 16, 584-596.
20. Reed, R. (1989) The organization of 3' splice-site sequences in mammalian introns. Genes Dev., 3, 2113-2123.
21. Zuo, P. and Maniatis, T. (1996) The splicing factor U2AF35 mediates critical protein-protein interactions in constitutive and enhancer-dependent splicing. Genes Dev., 10, 1356-1368.
22. Graveley, B.R., Hertel, K.J. and Maniatis, T (2001) The role of U2AF35 and U2AF65 in enhancer-dependent splicing. RNA, 7, 806-818.
23. Pacheco, TR., Moita, L.F, Gomes, A.Q., Hacohen, N. and Carmo-Fonseca, M. (2006) RNA interference knockdown of hU2AF35 impairs cell cycle progression and modulates alternative splicing of Cdc25 transcripts. Mol. Biol. Cell, 17, 4187-4199.
24. Kralovicova, J. and Vorechovsky, I. (2010) Allele-dependent recognition of the 3' splice site of INS intron 1. Hum. Genet., 128, 383-400.
25. Zarnack, K., König, J., Tajnik, M., Martincorena, I., Eustermann, S., Stevant, I., Reyes, A., Anders, S., Luscombe, N.M. and Ule, J. (2013) Direct competition between hnRNP C and U2AF65 protects the transcriptome from the exonization of Alu elements. Cell, 152, 453-466.
26. 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.
27. Trapnell, C, Hendrickson, D.G, Sauvageau, M., Goff, L., Rinn, J.L. and Pachter, L. (2012) Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat. Biotechnol., 31, 46-53.
28. Luo, Z., Lin, C, Guest, E., Garrett, A.S., Mohaghegh, N, Swanson, S., Marshall, S., Florens, L., Washburn, M.P and Shilatifard, A. (2012) The super elongation complex family of RNA polymerase II elongation factors: gene target specifcity and transcriptional output. Mol. Cell. Biol, 32, 2608-2617.
29. Kim, D., Pertea, G, Trapnell, C, Pimentel, H., Kelley, R. and Salzberg, S.L. (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol., 14, R36.
30. Langmead, B. and Salzberg, S.L. (2012) Fast gapped-read alignment with Bowtie 2. Nat. Methods, 9, 357-359.
31. Karolchik, D., Barber, GP, Casper, J., Clawson, H., Cline, M.S., Diekhans, M., Dreszer, TR., Fujita, PA., Guruvadoo, L., Haeussler, M. et al. (2014) The UCSC Genome Browser database: 2014 update. Nucleic Acids Res., 42, D764-D770.
32. Anders, S., Reyes, A. and Huber, W. (2012) Detecting differential usage of exons from RNA-seq data. Genome Res., 22, 2008-2017.
33. Trapnell, C, Roberts, A., Goff, L., Pertea, G, Kim, D., Kelley, D.R., Pimentel, H., Salzberg, S.L., Rinn, J.L. and Pachter, L. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cuffinks. Nat. Protoc, 7, 562-578.
34. Huang da, W., Sherman, B.T and Lempicki, R.A. (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res., 37, 1-13.
35. Huang da, W., Sherman, B.T. and Lempicki, R.A. (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc, 4, 44-57.
36. Kralovicova, J., Gaunt, TR., Rodriguez, S., Wood, PJ., Day, I.NM. and Vorechovsky, I. (2006) Variants in the human insulin gene that affect pre-mRNA splicing: is-23HphI a functional single nucleotide polymorphism at IDDM2? Diabetes, 55, 260-264.
37. Shapiro, M.B. and Senapathy, P (1987) RNA splice junctions of different classes of eukaryotes: sequence statistics and functional implications in gene expression. Nucleic Acids Res., 15, 7155-7174.
38. Yeo, G and Burge, C.B. (2004) Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J. Comput. Biol, 11, 377-394.
39. Vorechovsky, I. (2006) Aberrant 3' splice sites in human disease genes: mutation pattern, nucleotide structure and comparison of computational tools that predict their utilization. Nucleic Acids Res., 34, 4630-4641.
40. Buratti, E., Chivers, M.C, Kralovicova, J., Romano, M., Baralle, M., Krainer, A.R. and Vorechovsky, I. (2007) Aberrant 5' splice sites in human disease genes: mutation pattern, nucleotide structure and comparison of computational tools that predict their utilization. Nucleic Acids Res., 35, 4250-4263.
41. Corvelo, A., Hallegger, M., Smith, C.W. andEyras, E. (2010) Genome-wide association between branch point properties and alternative splicing. PLoS Comput. Biol, 6, e1001016.
42. Bailey, TL., Boden, M., Buske, FA., Frith, M., Grant, C.E., Clementi, L., Ren, J., Li, W.W. and Noble, W.S. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res., 37, W202-W208.
43. Muckstein, U., Tafer, H, Hackermuller, J., Bernhart, S.H, Stadler, PF and Hofacker, I.L. (2006) Thermodynamics of RNA-RNA binding. Bioinformatics, 22, 1177-1182.
44. Hiller, M., Pudimat, R., Busch, A. and Backofen, R. (2006) Using RNA secondary structures to guide sequence motif fnding towards single-stranded regions. Nucleic Acids Res., 34, e 117.
45. Lianoglou, S., GargV., Yang, J.L., Leslie, CS. and Mayr, C (2013) Ubiquitously transcribed genes use alternative polyadenylation to achieve tissue-specifc expression. Genes Dev., 27, 2380-2396.
46. Martinson, H.G (2011) An active role for splicing in 3'-end formation. Wiley Interdiscip. Rev. RNA, 2, 459-470.
47. Taggart, A.J., DeSimone, A.M., Shih, J.S., Filloux, M.E. and Fairbrother, W.G (2012) Large-scale mapping of branchpoints in human pre-mRNA transcripts in vivo. Nat. Struct. Mol. Biol, 19, 719-721.
48. Smith, CW., Chu, TT and Nadal-Ginard, B. (1993) Scanning and competition between AGs are involved in 3' splice site selection in mammalian introns. Mol. Cell. Biol, 13, 4939-4952.
49. Kralovicova, J., Christensen, M.B. and Vorechovsky, I. (2005) Biased exon/intron distribution of cryptic and de novo 3' splice sites. Nucleic Acids Res., 33, 4882-4898.
50. Llorian, M., Schwartz, S., Clark, TA., Hollander, D, Tan, L.Y, Spellman, R., Gordon, A., Schweitzer, A.C, de la Grange, P, Ast, G et al. (2010) Position-dependent alternative splicing activity revealed by global profling of alternative splicing events regulated by PTB. Nat. Struct. Mol. Biol, 17, 1114-1123.
51. Hastings, M.L., Allemand, E., Duelli, D.M., Myers, M.P and Krainer, A.R. (2007) Control of pre-mRNA splicing by the general splicing factors PUF60 and U2AF. PLoS ONE, 2, e538.
52. Tavanez, J.P, Madl, T, Kooshapur, H, Sattler, M. and Valcarcel, J. (2012) hnRNP A1 proofreads 3' splice site recognition by U2AF. Mol. Cell, 45, 314-329.
53. Soares, L.M., Zanier, K., Mackereth, C, Sattler, M. and Valcarcel, J. (2006) Intron removal requires proofreading of U2AF/3' splice site recognition by DEK. Science, 312, 1961-1965.
54. Watakabe, A., Inoue, K., Sakamoto, H. and Shimura, Y (1989) A secondary structure at the 3' splice site affects the in vitro splicing reaction of mouse immunoglobulin mu chain pre-mRNAs. Nucleic Acids Res., 17, 8159-8169.
55. Jacquenet, S., Ropers, D, Bilodeau, PS., Damier, L., Mougin, A., Stoltzfus, CM. and Branlant, C (2001) Conserved stem-loop structures in the HIV-1 RNA region containing the A3 3' splice site and its cis-regulatory element: possible involvement in RNA splicing. Nucleic Acids Res., 29, 464-478.
56. Arning, S., Gruter, P, Bilbe, G and Krämer, A. (1996) Mammalian splicing factor SF1 is encoded by variant cDNAs and binds to RNA. RNA, 2, 794-810.
57. Bedford, M.T, Chan, DC and Leder, P (1997) FBP WW domains and the Abl SH3 domain bind to a specifc class of proline-rich ligands. EMBO J., 16, 2376-2383.
58. Makarov, E.M., Owen, N, Bottrill, A. and Makarova, OV. (2011) Functional mammalian spliceosomal complex E contains SMN complex proteins in addition to U1 and U2 snRNPs. Nucleic Acids Res., 40, 2639-2652.
59. Gooding, C and Smith, CW. (2008) Tropomyosin exons as models for alternative splicing. Adv. Exp. Med. Biol, 644, 27-42.
60. Maytum, R., Bathe, F, Konrad, M. and Geeves, M.A. (2004) Tropomyosin exon 6b is troponin-specifc and required for correct acto-myosin regulation. J. Biol. Chem., 279, 18203-18209.
61. Vrhovski, B., Schevzov, G., Dingle, S., Lessard, J.L., Gunning, P. and Weinberger, R.P. (2003) Tropomyosin isoforms from the gamma gene differing at the C-terminus are spatially and developmentally regulated in the brain. J. Neurosci. Res., 72, 373-383.
62. Hegele, A., Kamburov, A., Grossmann, A., Sourlis, C, Wowro, S., Weimann, M., Will, C.L., Pena, V, Lührmann, R. and Stelzl, U. (2012) Dynamic protein-protein interaction wiring of the human spliceosome. Mol Cell, 45, 567-580.
63. Ajuh, P., Kuster, B., Panov, K., Zomerdijk, J.C, Mann, M. and Lamond, A.I. (2000) Functional analysis of the human CDC5L complex and identifcation of its components by mass spectrometry. EMBO J., 19, 6569-6581.
64. Caspary, F. and Séraphin, B. (1998) The yeast U2A/U2B complex is required for pre-spliceosome formation. EMBO J., 17, 6348-6358.
65. Shepard, J., Reick, M., Olson, S. and Graveley, B.R. (2002) Characterization of U2AF(26), a splicing factor related to U2AF(35). Mol. Cell. Biol, 22, 221-230.
66. DiNardo, A., Gareus, R., Kwiatkowski, D. andWitke, W. (2000) Alternative splicing of the mouse proflin II gene generates functionally different proflin isoforms. J. Cell Sci., 113, 3795-3803.
67. Lambrechts, A., Braun, A., Jonckheere, V, Aszodi, A., Lanier, L.M., Robbens, J., Van Colen, I., Vandekerckhove, J., Fassler, R. and Ampe, C. (2000) Proflin II is alternatively spliced, resulting in proflin isoforms that are differentially expressed and have distinct biochemical properties. Mol Cell. Biol, 20, 8209-8219.
68. Zhao, W., He, X., Hoadley, K.A., Parker, J.S., Hayes, D.N. and Perou, C.M. (2014) Comparison of RNA-Seq by poly (A) capture, ribosomal RNA depletion, and DNA microarray for expression profling. BMC Genomics, 15, 419.
69. Shao, C, Yang, B., Wu, T, Huang, J., Tang, P, Zhou, Y, Zhou, J., Qiu, J., Jiang, L., Li, H. et al (2014) Mechanisms for U2AF to defne 3' splice sites and regulate alternative splicing in the human genome. Nat. Struct. Mol Biol, 21, 997-1005.
70. Millevoi, S., Geraghty, F, Idowu, B., Tam, J.L., Antoniou, M. and Vagner, S. (2002) A novel function for the U2AF 65 splicing factor in promoting pre-mRNA 3'-endprocessing. EMBO Rep., 3, 869-874.
71. David, C.J., Boyne, A.R., Millhouse, S.R. and Manley, J.L. (2011) The RNA polymerase II C-terminal domain promotes splicing activation through recruitment of a U2AF65-Prp19 complex. Genes Dev., 25, 972-983.
72. Girard, C, Will, C.L., Peng, J., Makarov, E.M., Kastner, B., Lemm, I., Urlaub, H., Hartmuth, K. and Lührmann, R. (2012) Post-transcriptional spliceosomes are retained in nuclear speckles until splicing completion. Nat. Commun., 3, 994.
73. Boutz, PL., Bhutkar, A. and Sharp, PA. (2015) Detained introns are novel, widespread class of post-transcriptionally spliced introns. Genes Dev., 29, 63-80.
74. Khodor, Y.L., Menet, J.S., Tolan, M. and Rosbash, M. (2012) Cotranscriptional splicing effciency differs dramatically between Drosophila and mouse. RNA, 18, 2174-2186.
75. Ujvári, A. and Luse, DS. (2004) Newly Initiated RNA encounters a factor involved in splicing immediately upon emerging from within RNA polymerase II. J. Biol. Chem., 279, 49773-49779.
76. Pinto, PA., Henriques, T, Freitas, M.O., Martins, T, Domingues, R.G, Wyrzykowska, PS., Coelho, PA., Carmo, A.M., Sunkel, C.E., Proudfoot, NJ. et al (2011) RNA polymerase II kinetics in polo polyadenylation signal selection. EMBO J., 30, 2431-2444.
77. Fong, N, Kim, H., Zhou, Y, Xiong, J., Qiu, J., Saldi, T, Diener, K., Jones, K., Fu, X.-D and Bentley, D. (2014) Pre-mRNA splicing is facilitated by an optimal RNA polymerase II elongation rate. Genes Dev., 28, 2663-2676.
78. Millevoi, S., Loulergue, C, Dettwiler, S., Karaa, S.Z., Keller, W., Antoniou, M. and Vagner, S. (2006) An interaction between U2AF65 and CF Im links the slicing and 3' end processing machineries. EMBO J., 25, 4854-4864.
79. Martin, G, Gruber, A.R., Keller, W. and Zavolan, M. (2012) Genome-wide analysis of pre-mRNA 3' end processing reveals a decisive role of human cleavage factor I in the regulation of 3' UTR length. Cell Rep., 1, 753-763.
80. Licatalosi, D.D, Geiger, G, Minet, M., Schroeder, S., Cilli, K., McNeil, J.B. and Bentley, D.L. (2002) Functional interaction of yeast pre-mRNA 3' end processing factors with RNA polymerase II. Mol Cell, 9, 1101-1111.
81. Morris, D.P and Greenleaf, A.L. (2000) The splicing factor, Prp40, binds the phosphorylated carboxyl-terminal domain of RNA polymerase II. J. Biol. Chem., 275, 39935-39943.
82. Goldstrohm, A.C, Albrecht, TR., Sune, C, Bedford, M.T and Garcia-Blanco, M.A. (2001) The transcription elongation factor CA150 interacts with RNA polymerase II and the pre-mRNA splicing factor SF1. Mol Cell. Biol, 21, 7617-7628.
83. Emili, A., Shales, M., McCracken, S., Xie, W., Tucker, PW., Kobayashi, R., Blencowe, B.J. and Ingles, C.J. (2002) Splicing and transcription-associated proteins PSF and p54nrb/nonO bind to the RNA polymerase II CTD. RNA, 8, 1102-1111.
84. Jenal, M., Elkon, R., Loayza-Puch, F, van Haaften, G, Kuhn, U., Menzies, FM., Oude Vrielink, J.A., Bos, A.J., Drost, J., Rooijers, K. et al (2012) The poly(A)-binding protein nuclear 1 suppresses alternative cleavage and polyadenylation sites. Cell, 149, 538-553.
85. Elkon, R., Ugalde, A.P and Agami, R. (2013) Alternative cleavage and polyadenylation: extent, regulation and function. Nat. Rev. Genet., 14, 496-506.
86. Kanopka, A., Muhlemann, O. and Akusjärvi, G (1996) Inhibition by SR proteins of splicing of a regulated adenovirus pre-mRNA. Nature, 381, 535-538.
87. Corioni, M., Antih, N, Tanackovic, G, Zavolan, M. and Krämer, A. (2010) Analysis of in situ pre-mRNA targets of human splicing factor SF1 reveals a function in alternative splicing. Nucleic Acids Res., 39, 1868-1879.
88. Page-McCaw, PS., Amonlirdviman, K. and Sharp, PA. (1999) PUF60: a novel U2AF65-related splicing activity. RNA, 5, 1548-1560.
89. Tollervey, J.R., Curk, T, Rogelj, B., Briese, M., Cereda, M., Kayikci, M., König, J., Hortobagyi, T, Nishimura, A.L., Zupunski, V et al (2011) Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat. Neurosci, 14, 452-458.
90. Kralovicova, J. and Vorechovsky, I. (2006) Position-dependent repression and promotion of DQB1 intron 3 splicing by GGGG motifs. J. Immunol, 176, 2381-2388.
91. Zhou, X., Wu, W., Li, H., ChengY., Wei, N, Zong, J., Feng, X., Xie, Z., Chen, D, Manley, J.L. et al (2014) Transcriptome analysis of alternative splicing events regulated by SRSF10 reveals position-dependent splicing modulation. Nucleic Acids Res., 42, 4019-4030.
92. Corsini, L., Hothorn, M., Stier, G, Rybin, V., Scheffzek, K., Gibson, T J. and Sattler, M. (2009) Dimerization and protein binding specifcity of the U2AF homology motif of the splicing factor PUF60. J. Biol. Chem., 284, 630-639.
93. Liu, J., He, L., Collins, I., Ge, H., Libutti, D, Li, J., Egly, J.-M. and Levens, D (2000) The FGB interacting repressor targets TFIIH to inhibits activated transcription. Mol Cell, 5, 331-341.
94. Dowhan, DH., Hong, E.P, Auboeuf, D, Dennis, A.P, Wilson, M.M., Berget, S.M. and O'Malley, B.W. (2005) Steroid hormone receptor coactivation and alternative RNA splicing by U2AF65-related proteins CAPERalpha and CAPERbeta. Mol Cell, 17, 429-439.
95. Olsen, J.V, Vermeulen, M., Santamaria, A., Kumar, C, Miller, M.L., Jensen, L.J., Gnad, F, Cox, J., Jensen, TS., Nigg, E.A. et al (2010) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal, 3, ra3.
96. Kielkopf, C.L., Rodionova, NA., Green, M.R. and Burley, S.K. (2001) A novel peptide recognition mode revealed by the X-ray structure of a core U2AF35/U2AF65 heterodimer. Cell, 106, 595-605.
97. Forch, P, Merendino, L., Martinez, C. and Valcarcel, J. (2003) U2 small nuclear ribonucleoprotein particle (snRNP) auxiliary factor of 65 kDa, U2AF65, can promote U1 snRNP recruitment to 5' splice sites. Biochem. J., 372, 235-240.
98. Shao, W., Kim, H.-S., Cao, Y, Xu, Y-Z. and Query, C.C. (2012) A U1-U2 snRNP interaction network during intron defnition. Mol Cell. Biol, 32, 470-478.
99. Chathoth, K.T, Barrass, J.D., Webb, S. and Beggs, J.D. (2014) A splicing-dependent transcriptional checkpoint associated with prespliceosome formation. Mol Cell, 53, 779-790.
100. Peterson, M.L., Bertolino, S. and Davis, F (2002) An RNA polymerase pause site is associated with the immunoglobulin mus poly(A) site. Mol Cell. Biol, 22, 5606-5615.