An extensive program of periodic alternative splicing linked to cell cycle progression

eLife

Volumn 5, Issue MARCH2016, 2016, Pages

  Dominguez, Daniel ^a,b   Tsai, Yi Hsuan ^a,b   Weatheritt, Robert ^c   Wang, Yang ^a,b   Blencowe, Benjamin J ^c   Wang, Zefeng ^a,d  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

^d MAX PLANCK INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL CYCLE ASSAY; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; FLOW CYTOMETRY; GENE EXPRESSION; GENE FUNCTION; GENE ONTOLOGY; GENE OVEREXPRESSION; GENE SILENCING; HEALTH PROGRAM; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOPRECIPITATION; KIDNEY CANCER; MITOSIS; PLASMID; PROTEIN PROTEIN INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SPLICING; WESTERN BLOTTING; ALTERNATIVE RNA SPLICING; CELL CYCLE; EPITHELIUM CELL; GENE EXPRESSION PROFILING; GENE INACTIVATION; GENETICS; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

CLK DUAL-SPECIFICITY KINASES; PROTEIN SERINE THREONINE KINASE; PROTEIN TYROSINE KINASE;

ALTERNATIVE SPLICING; CELL CYCLE; CELL LINE, TUMOR; EPITHELIAL CELLS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE KNOCKOUT TECHNIQUES; HUMANS; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES;

EID: 84979547553     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.10288     Document Type: Article

References (62)

1. Ahn EY, DeKelver RC, Lo MC, Nguyen TA, Matsuura S, Boyapati A, Pandit S, Fu XD, Zhang DE. 2011. SON controls cell-cycle progression by coordinated regulation of RNA splicing. Molecular Cell 42: 185-198. doi: 10.1016/j.molcel.2011.03.014
2. Aviner R, Shenoy A, Elroy-Stein O, Geiger T. 2015. Uncovering hidden layers of cell cycle regulation through integrative multi-omic analysis. PLoS Genetics 11: e1005554. doi: 10.1371/journal.pgen.1005554
3. Bar-Joseph Z, Siegfried Z, Brandeis M, Brors B, Lu Y, Eils R, Dynlacht BD, Simon I. 2008. Genome-wide transcriptional analysis of the human cell cycle identifies genes differentially regulated in normal and cancer cells. Proceedings of the National Academy of Sciences of the United States of America 105: 955-960. doi: 10.1073/pnas.0704723105
4. Ben-David Y, Letwin K, Tannock L, Bernstein A, Pawson T. 1991. A mammalian protein kinase with potential for serine/threonine and tyrosine phosphorylation is related to cell cycle regulators. The EMBO Journal 10: 317-325.
5. Ben-Yehuda S, Dix I, Russell CS, McGarvey M, Beggs JD, Kupiec M. 2000. Genetic and physical interactions between factors involved in both cell cycle progression and pre-mRNA splicing in Saccharomyces cerevisiae. Genetics 156: 1503-1517.
6. Bertoli C, Skotheim JM, de Bruin RA. 2013. Control of cell cycle transcription during G1 and S phases. Nature Reviews. Molecular Cell Biology 14: 518-528. doi: 10.1038/nrm3629
7. Bettencourt-Dias M, Giet R, Sinka R, Mazumdar A, Lock WG, Balloux F, Zafiropoulos PJ, Yamaguchi S, Winter S, Carthew RW, Cooper M, Jones D, Frenz L, Glover DM. 2004. Genome-wide survey of protein kinases required for cell cycle progression. Nature 432: 980-987. doi: 10.1038/nature03160
8. Björklund M, Taipale M, Varjosalo M, Saharinen J, Lahdenperä J, Taipale J. 2006. Identification of pathways regulating cell size and cell-cycle progression by RNAi. Nature 439: 1009-1013. doi: 10.1038/nature04469
9. Bomont P, Maddox P, Shah JV, Desai AB, Cleveland DW. 2005. Unstable microtubule capture at kinetochores depleted of the centromere-associated protein CENP-F. The EMBO Journal 24: 3927-3939. doi: 10.1038/sj.emboj.7600848
10. Boutz PL, Bhutkar A, Sharp PA. 2015. Detained introns are a novel, widespread class of post-transcriptionally spliced introns. Genes & Development 29: 63-80. doi: 10.1101/gad.247361.114
11. Cancer Genome Atlas Research Network. 2013. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 499: 43-49. doi: 10.1038/nature12222
12. Cappell KM, Larson B, Sciaky N, Whitehurst AW. 2010. Symplekin specifies mitotic fidelity by supporting microtubule dynamics. Molecular and Cellular Biology 30: 5135-5144. doi: 10.1128/MCB.00758-10
13. Carmena M, Wheelock M, Funabiki H, Earnshaw WC. 2012. The chromosomal passenger complex (CPC): from easy rider to the godfather of mitosis. Nature Reviews. Molecular Cell Biology 13: 789-803. doi: 10.1038/nrm3474
14. Chaves-Pérez A, Mack B, Maetzel D, Kremling H, Eggert C, Harréus U, Gires O. 2013. EpCAM regulates cell cycle progression via control of cyclin D1 expression. Oncogene 32: 641-650. doi: 10.1038/onc.2012.75
15. Ciriello G, Miller ML, Aksoy BA, Senbabaoglu Y, Schultz N, Sander C. 2013. Emerging landscape of oncogenic signatures across human cancers. Nature Genetics 45: 1127-1133. doi: 10.1038/ng.2762
16. David CJ, Manley JL. 2010. Alternative pre-mRNA splicing regulation in cancer: pathways and programs unhinged. Genes & Development 24: 2343-2364. doi: 10.1101/gad.1973010
17. Duncan PI, Stojdl DF, Marius RM, Bell JC. 1997. In vivo regulation of alternative pre-mRNA splicing by the Clk1 protein kinase. Molecular and Cellular Biology 17: 5996-6001. doi: 10.1128/mcb.17.10.5996
18. Edmond V, Moysan E, Khochbin S, Matthias P, Brambilla C, Brambilla E, Gazzeri S, Eymin B. 2011. Acetylation and phosphorylation of SRSF2 control cell fate decision in response to cisplatin. The EMBO Journal 30: 510-523. doi: 10.1038/emboj.2010.333
19. Fedorov O, Huber K, Eisenreich A, Filippakopoulos P, King O, Bullock AN, Szklarczyk D, Jensen LJ, Fabbro D, Trappe J, Rauch U, Bracher F, Knapp S. 2011. Specific CLK inhibitors from a novel chemotype for regulation of alternative splicing. Chemistry & Biology 18: 67-76. doi: 10.1016/j.chembiol.2010.11.009
20. Grabek KR, Diniz Behn C, Barsh GS, Hesselberth JR, Martin SL. 2015. Enhanced stability and polyadenylation of select mRNAs support rapid thermogenesis in the brown fat of a hibernator. eLife 4. doi: 10.7554/eLife.04517
21. Gui JF, Lane WS, Fu XD. 1994. A serine kinase regulates intracellular localization of splicing factors in the cell cycle. Nature 369: 678-682. doi: 10.1038/369678a0
22. Harashima H, Dissmeyer N, Schnittger A. 2013. Cell cycle control across the eukaryotic kingdom. Trends in Cell Biology 23: 345-356. doi: 10.1016/j.tcb.2013.03.002
23. Irimia M, Weatheritt RJ, Ellis JD, Parikshak NN, Gonatopoulos-Pournatzis T, Babor M, Quesnel-Vallières M, Tapial J, Raj B, O’Hanlon D, Barrios-Rodiles M, Sternberg MJ, Cordes SP, Roth FP, Wrana JL, Geschwind DH, Blencowe BJ. 2014. A highly conserved program of neuronal microexons is misregulated in autistic brains. Cell 159: 1511-1523. doi: 10.1016/j.cell.2014.11.035
24. Jiang K, Patel NA, Watson JE, Apostolatos H, Kleiman E, Hanson O, Hagiwara M, Cooper DR. 2009. Akt2 regulation of Cdc2-like kinases (Clk/Sty), serine/arginine-rich (SR) protein phosphorylation, and insulin-induced alternative splicing of PKCbetaII messenger ribonucleic acid. Endocrinology 150: 2087-2097. doi: 10.1210/en.2008-0818
25. Karni R, de Stanchina E, Lowe SW, Sinha R, Mu D, Krainer AR. 2007. The gene encoding the splicing factor SF2/ASF is a proto-oncogene. Nature Structural & Molecular Biology 14: 185-193. doi: 10.1038/nsmb1209
26. Katz Y, Wang ET, Airoldi EM, Burge CB. 2010. Analysis and design of RNA sequencing experiments for identifying isoform regulation. Nature Methods 7: 1009-1015. doi: 10.1038/nmeth.1528
27. Kim Y, Heuser JE, Waterman CM, Cleveland DW. 2008. CENP-E combines a slow, processive motor and a flexible coiled coil to produce an essential motile kinetochore tether. The Journal of Cell Biology 181: 411-419. doi: 10.1083/jcb.200802189
28. Lai MC, Lin RI, Tarn WY. 2003. Differential effects of hyperphosphorylation on splicing factor SRp55. The Biochemical Journal 371: 937-945. doi: 10.1042/BJ20021827
29. Lens SM, Voest EE, Medema RH. 2010. Shared and separate functions of polo-like kinases and aurora kinases in cancer. Nature Reviews. Cancer 10: 825-841. doi: 10.1038/nrc2964
30. Leva V, Giuliano S, Bardoni A, Camerini S, Crescenzi M, Lisa A, Biamonti G, Montecucco A. 2012. Phosphorylation of SRSF1 is modulated by replicational stress. Nucleic Acids Research 40: 1106-1117. doi: 10.1093/nar/gkr837
31. Long JC, Caceres JF. 2009. The SR protein family of splicing factors: master regulators of gene expression. The Biochemical Journal 417: 15-27. doi: 10.1042/BJ20081501
32. Ly T, Ahmad Y, Shlien A, Soroka D, Mills A, Emanuele MJ, Stratton MR, Lamond AI. 2014. A proteomic chronology of gene expression through the cell cycle in human myeloid leukemia cells. eLife 3: e01630. doi: 10.7554/elife.01630
33. Maslon MM, Heras SR, Bellora N, Eyras E, Cáceres JF. 2014. The translational landscape of the splicing factor SRSF1 and its role in mitosis. eLife: e02028. doi: 10.7554/eLife.02028
34. Matera AG, Wang Z. 2014. A day in the life of the spliceosome. Nature Reviews. Molecular Cell Biology 15: 108-121. doi: 10.1038/nrm3742
35. Mayr C, Bartel DP. 2009. Widespread shortening of 3‘UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138: 673-684. doi: 10.1016/j.cell.2009.06.016
36. McDonald WH, Ohi R, Smelkova N, Frendewey D, Gould KL. 1999. Myb-related fission yeast cdc5p is a component of a 40S snRNP-containing complex and is essential for pre-mRNA splicing. Molecular and Cellular Biology 19: 5352-5362. doi: 10.1128/mcb.19.8.5352
37. Mocciaro A, Rape M. 2012. Emerging regulatory mechanisms in ubiquitin-dependent cell cycle control. Journal of Cell Science 125: 255-263. doi: 10.1242/jcs.091199
38. Moore MJ, Wang Q, Kennedy CJ, Silver PA. 2010. An alternative splicing network links cell-cycle control to apoptosis. Cell 142: 625-636. doi: 10.1016/j.cell.2010.07.019
39. Muraki M, Ohkawara B, Hosoya T, Onogi H, Koizumi J, Koizumi T, Sumi K, Yomoda J, Murray MV, Kimura H, Furuichi K, Shibuya H, Krainer AR, Suzuki M, Hagiwara M. 2004. Manipulation of alternative splicing by a newly developed inhibitor of Clks. The Journal of Biological Chemistry 279: 24246-24254. doi: 10.1074/jbc.M314298200
40. Ninomiya K, Kataoka N, Hagiwara M. 2011. Stress-responsive maturation of Clk1/4 pre-mRNAs promotes phosphorylation of SR splicing factor. The Journal of Cell Biology 195: 27-40. doi: 10.1083/jcb.201107093
41. Oltean S, Bates DO. 2014. Hallmarks of alternative splicing in cancer. Oncogene 33: 5311-5318. doi: 10.1038/onc.2013.533
42. Pan Q, Shai O, Misquitta C, Zhang W, Saltzman AL, Mohammad N, Babak T, Siu H, Hughes TR, Morris QD, Frey BJ, Blencowe BJ. 2004. Revealing global regulatory features of mammalian alternative splicing using a quantitative microarray platform. Molecular Cell 16: 929-941. doi: 10.1016/j.molcel.2004.12.004
43. Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ. 2008. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nature Genetics 40: 1413-1415. doi: 10.1038/ng.259
44. Paronetto MP, Miñana B, Valcárcel J. 2011. The Ewing sarcoma protein regulates DNA damage-induced alternative splicing. Molecular Cell 43: 353-368. doi: 10.1016/j.molcel.2011.05.035
45. Prasad J, Colwill K, Pawson T, Manley JL. 1999. The protein kinase Clk/Sty directly modulates SR protein activity: both hyper- and hypophosphorylation inhibit splicing. Molecular and Cellular Biology 19: 6991-7000. doi: 10.1128/mcb.19.10.6991
46. Satyanarayana A, Kaldis P. 2009. Mammalian cell-cycle regulation: several Cdks, numerous cyclins and diverse compensatory mechanisms. Oncogene 28: 2925-2939. doi: 10.1038/onc.2009.170
47. Shen H, Kan JL, Green MR. 2004. Arginine-serine-rich domains bound at splicing enhancers contact the branchpoint to promote prespliceosome assembly. Molecular Cell 13: 367-376. doi: 10.1016/s1097-2765(04)00025-5
48. Shin C, Manley JL. 2002. The SR protein SRp38 represses splicing in M phase cells. Cell 111: 407-417. doi: 10.1016/s0092-8674(02)01038-3
49. Staalesen V, Falck J, Geisler S, Bartkova J, Børresen-Dale AL, Lukas J, Lillehaug JR, Bartek J, Lønning PE. 2004. Alternative splicing and mutation status of CHEK2 in stage III breast cancer. Oncogene 23: 8535-8544. doi: 10.1038/sj.onc.1207928
50. Sterne-Weiler T, Martinez-Nunez RT, Howard JM, Cvitovik I, Katzman S, Tariq MA, Pourmand N, Sanford JR. 2013. Frac-seq reveals isoform-specific recruitment to polyribosomes. Genome Research 23: 1615-1623. doi: 10.1101/gr.148585.112
51. Stumpf CR, Moreno MV, Olshen AB, Taylor BS, Ruggero D. 2013. The translational landscape of the mammalian cell cycle. Molecular Cell 52: 574-582. doi: 10.1016/j.molcel.2013.09.018
52. Tejedor JR, Papasaikas P, Valcárcel J. 2015. Genome-wide identification of Fas/CD95 alternative splicing regulators reveals links with iron homeostasis. Molecular Cell 57: 23-38. doi: 10.1016/j.molcel.2014.10.029
53. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. 2010. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 28: 511-515. doi: 10.1038/nbt.1621
54. Tsai YS, Dominguez D, Gomez SM, Wang Z. 2015. Transcriptome-wide identification and study of cancer-specific splicing events across multiple tumors. Oncotarget 6: 6825-6839. doi: 10.18632/oncotarget.3145
55. Vermeulen K, Van Bockstaele DR, Berneman ZN. 2003. The cell cycle: a review of regulation, deregulation and therapeutic targets in cancer. Cell Proliferation 36: 131-149. doi: 10.1046/j.1365-2184.2003.00266.x
56. Wang GS, Cooper TA. 2007. Splicing in disease: disruption of the splicing code and the decoding machinery. Nature Reviews. Genetics 8: 749-761. doi: 10.1038/nrg2164
57. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. 2008. Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476. doi: 10.1038/nature07509
58. Wang Z, Burge CB. 2008. Splicing regulation: from a parts list of regulatory elements to an integrated splicing code. RNA 14: 802-813. doi: 10.1261/rna.876308
59. Wang K, Singh D, Zeng Z, Coleman SJ, Huang Y, Savich GL, He X, Mieczkowski P, Grimm SA, Perou CM, MacLeod JN, Chiang DY, Prins JF, Liu J. 2010. MapSplice: accurate mapping of RNA-seq reads for splice junction discovery. Nucleic Acids Research 38: e178. doi: 10.1093/nar/gkq622
60. Wang Y, Chen D, Qian H, Tsai YS, Shao S, Liu Q, Dominguez D, Wang Z. 2014. The splicing factor RBM4 controls apoptosis, proliferation, and migration to suppress tumor progression. Cancer Cell 26: 374-389. doi: 10.1016/j.ccr.2014.07.010
61. Whitfield ML, Sherlock G, Saldanha AJ, Murray JI, Ball CA, Alexander KE, Matese JC, Perou CM, Hurt MM, Brown PO, Botstein D. 2002. Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Molecular Biology of the Cell 13: 1977-2000. doi: 10.1091/mbc.02-02-0030.
62. Zhou Z, Fu XD. 2013. Regulation of splicing by SR proteins and SR protein-specific kinases. Chromosoma 122: 191-207. doi: 10.1007/s00412-013-0407-z