Characterization of human cyclin-dependent kinase 12 (CDK12) and CDK13 complexes in C-terminal domain phosphorylation, gene transcription, and RNA processing

Molecular and Cellular Biology

Volumn 35, Issue 6, 2015, Pages 928-938

  Liang, Kaiwei ^a   Gao, Xin ^a   Gilmore, Joshua M ^a   Florens, Laurence ^a   Washburn, Michael P ^a,b   Smith, Edwin ^a,c   Shilatifard, Ali ^a,c  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 12; CYCLIN DEPENDENT KINASE 13; CYCLIN DEPENDENT KINASE 9; FLAG TAGGED PROTEIN; PROTEIN; PROTEIN SERINE THREONINE KINASE; SMALL NUCLEOLAR RNA; TRANSCRIPTOME; UNCLASSIFIED DRUG; CDK12 PROTEIN, HUMAN; CDK13 PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 1; RNA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; DNA DAMAGE; GENETIC TRANSCRIPTION; HCT116 CELL LINE; HUMAN; HUMAN CELL; INTERACTIONS WITH RNA; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; RNA INTERFERENCE; RNA PROCESSING; CELL LINE; GENETICS; HEK293 CELL LINE; PHOSPHORYLATION; TUMOR CELL LINE;

CDC2 PROTEIN KINASE; CELL LINE; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASES; DNA DAMAGE; HCT116 CELLS; HEK293 CELLS; HUMANS; PHOSPHORYLATION; RNA; RNA PROCESSING, POST-TRANSCRIPTIONAL; TRANSCRIPTION, GENETIC;

EID: 84923196896     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01426-14     Document Type: Article

References (45)

1. Corden JL. 1990. Tails of RNA polymerase II. Trends Biochem Sci 15:383-387. http://dx.doi.org/10.1016/0968-0004(90)90236-5.
2. Phatnani HP, Greenleaf AL. 2006. Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev 20:2922-2936. http://dx.doi.org/10.1101/gad.1477006.
3. Hsin JP, Manley JL. 2012. The RNA polymerase II CTD coordinates transcription and RNA processing. Genes Dev 26:2119-2137. http://dx.doi.org/10.1101/gad.200303.112.
4. Buratowski S. 2009. Progression through the RNA polymerase II CTD cycle. Mol Cell 36:541-546. http://dx.doi.org/10.1016/j.molcel.2009.10.019.
5. Komarnitsky P, Cho EJ, Buratowski S. 2000. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev 14:2452-2460. http://dx.doi.org/10.1101/gad.824700.
6. Marshall NF, Peng J, Xie Z, Price DH. 1996. Control of RNA polymerase II elongation potential by a novel carboxyl-terminal domain kinase. J Biol Chem 271:27176-27183. http://dx.doi.org/10.1074/jbc.271.43.27176.
7. Yamaguchi Y, Takagi T, Wada T, Yano K, Furuya A, Sugimoto S, Hasegawa J, Handa H. 1999. NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 97:41-51. http://dx.doi.org/10.1016/S0092-8674(00)80713-8.
8. Wada T, Takagi T, Yamaguchi Y, Ferdous A, Imai T, Hirose S, Sugimoto S, Yano K, Hartzog GA, Winston F, Buratowski S, Handa H. 1998. DSIF, a novel transcription elongation factor that regulates RNA polymerase II processivity, is composed of human Spt4 and Spt5 homologs. Genes Dev 12:343-356. http://dx.doi.org/10.1101/gad.12.3.343.
9. Wood A, Shilatifard A. 2006. Bur1/Bur2 and the Ctk complex in yeast: the split personality of mammalian P-TEFb. Cell Cycle 5:1066-1068. http://dx.doi.org/10.4161/cc.5.10.2769.
10. Bartkowiak B, Liu P, Phatnani HP, Fuda NJ, Cooper JJ, Price DH, Adelman K, Lis JT, Greenleaf AL. 2010. CDK12 is a transcription elongation-associated CTD kinase, the metazoan ortholog of yeast Ctk1. Genes Dev 24:2303-2316. http://dx.doi.org/10.1101/gad.1968210.
11. Blazek D, Kohoutek J, Bartholomeeusen K, Johansen E, Hulinkova P, Luo Z, Cimermancic P, Ule J, Peterlin BM. 2011. The cyclin K/Cdk12 complex maintains genomic stability via regulation of expression of DNA damage response genes. Genes Dev 25:2158-2172. http://dx.doi.org/10.1101/gad.16962311.
12. Cheng SW, Kuzyk MA, Moradian A, Ichu TA, Chang VC, Tien JF, Vollett SE, Griffith M, Marra MA, Morin GB. 2012. Interaction of cyclin-dependent kinase 12/CrkRS with cyclin K1 is required for the phosphorylation of the C-terminal domain of RNA polymerase II. Mol Cell Biol 32:4691-4704. http://dx.doi.org/10.1128/MCB.06267-11.
13. Dai Q, Lei T, Zhao C, Zhong J, Tang YZ, Chen B, Yang J, Li C, Wang S, Song X, Li L, Li Q. 2012. Cyclin K-containing kinase complexes maintain self-renewal in murine embryonic stem cells. J Biol Chem 287:25344-25352. http://dx.doi.org/10.1074/jbc.M111.321760.
14. Bowman EA, Bowman CR, Ahn JH, Kelly WG. 2013. Phosphorylation of RNA polymerase II is independent of P-TEFb in the C. elegans germline. Development 140:3703-3713. http://dx.doi.org/10.1242/dev.095778.
15. Joshi PM, Sutor SL, Huntoon CJ, Karnitz LM. 2014. Ovarian cancerassociated mutations disable catalytic activity of CDK12, a kinase that promotes homologous recombination repair and resistance to cisplatin and poly(ADP-ribose) polymerase inhibitors. J Biol Chem 289:9247-9253. http://dx.doi.org/10.1074/jbc.M114.551143.
16. Kohoutek J, Blazek D. 2012. Cyclin K goes with Cdk12 and Cdk13. Cell Div 7:12. http://dx.doi.org/10.1186/1747-1028-7-12.
17. Ko TK, Kelly E, Pines J. 2001. CrkRS: a novel conserved Cdc2-related protein kinase that colocalises with SC35 speckles. J Cell Sci 114:2591-2603.
18. Chen HH, Wang YC, Fann MJ. 2006. Identification and characterization of the CDK12/cyclin L1 complex involved in alternative splicing regulation. Mol Cell Biol 26:2736-2745. http://dx.doi.org/10.1128/MCB.26.7.2736-2745.2006.
19. Rodrigues F, Thuma L, Klambt C. 2012. The regulation of glial-specific splicing of neurexin IV requires HOW and Cdk12 activity. Development 139:1765-1776. http://dx.doi.org/10.1242/dev.074070.
20. Davidson L, Muniz L, West S. 2014. 3' end formation of pre-mRNA and phosphorylation of Ser2 on the RNA polymerase II CTD are reciprocally coupled in human cells. Genes Dev 28:342-356. http://dx.doi.org/10.1101/gad.231274.113.
21. Berro R, Pedati C, Kehn-Hall K, Wu W, Klase Z, Even Y, Geneviere AM, Ammosova T, Nekhai S, Kashanchi F. 2008. CDK13, a new potential human immunodeficiency virus type 1 inhibitory factor regulating viral mRNA splicing. J Virol 82:7155-7166. http://dx.doi.org/10.1128/JVI.02543-07.
22. Even Y, Durieux S, Escande ML, Lozano JC, Peaucellier G, Weil D, Geneviere AM. 2006. CDC2L5, a Cdk-like kinase with RS domain, interacts with the ASF/SF2-associated protein p32 and affects splicing in vivo. J Cell Biochem 99:890-904. http://dx.doi.org/10.1002/jcb.20986.
23. Luo Z, Lin C, Guest E, Garrett AS, Mohaghegh N, Swanson S, Marshall S, Florens L, Washburn MP, Shilatifard A. 2012. The super elongation complex family ofRNApolymerase II elongation factors: gene target specificity and transcriptional output. Mol Cell Biol 32:2608-2617. http://dx.doi.org/10.1128/MCB.00182-12.
24. Wu M, Wang PF, Lee JS, Martin-Brown S, Florens L, Washburn M, Shilatifard A. 2008. Molecular regulation of H3K4 trimethylation by Wdr82, a component of human Set1/COMPASS. Mol Cell Biol 28:7337-7344. http://dx.doi.org/10.1128/MCB.00976-08.
25. Trapnell C, Pachter L, Salzberg SL. 2009. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105-1111. http://dx.doi.org/10.1093/bioinformatics/btp120.
26. 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. Nat Biotechnol 28:511-515. http://dx.doi.org/10.1038/nbt.1621.
27. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139-140. http://dx.doi.org/10.1093/bioinformatics/btp616.
28. Petersen-Mahrt SK, Estmer C, Ohrmalm C, Matthews DA, Russell WC, Akusjarvi G. 1999. The splicing factor-associated protein, p32, regulates RNA splicing by inhibiting ASF/SF2 RNA binding and phosphorylation. EMBO J 18:1014-1024. http://dx.doi.org/10.1093/emboj/18.4.1014.
29. Huang da W, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44-57. http://dx.doi.org/10.1038/nprot.2008.211.
30. Li H, Bingham PM. 1991. Arginine/serine-rich domains of the su(wa) and tra RNA processing regulators target proteins to a subnuclear compartment implicated in splicing. Cell 67:335-342. http://dx.doi.org/10.1016/0092-8674(91)90185-2.
31. O'Keeffe B, Fong Y, Chen D, Zhou S, Zhou Q. 2000. Requirement for a kinase-specific chaperone pathway in the production of a Cdk9/cyclin T1 heterodimer responsible for P-TEFb-mediated tat stimulation of HIV-1 transcription. J Biol Chem 275:279-287. http://dx.doi.org/10.1074/jbc.275.1.279.
32. Chapman RD, Heidemann M, Albert TK, Mailhammer R, Flatley A, Meisterernst M, Kremmer E, Eick D. 2007. Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7. Science 318:1780-1782. http://dx.doi.org/10.1126/science.1145977.
33. Bosken CA, Farnung L, Hintermair C, Merzel Schachter M, Vogel-Bachmayr K, Blazek D, Anand K, Fisher RP, Eick D, Geyer M. 2014. The structure and substrate specificity of human Cdk12/cyclin K. Nat Commun 5:3505. http://dx.doi.org/10.1038/ncomms4505.
34. Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, Burge CB, Sharp PA, Young RA. 2010. c-Myc regulates transcriptional pause release. Cell 141:432-445. http://dx.doi.org/10.1016/j.cell.2010.03.030.
35. Chao SH, Price DH. 2001. Flavopiridol inactivates P-TEFb and blocks most RNA polymerase II transcription in vivo. J Biol Chem 276:31793-31799. http://dx.doi.org/10.1074/jbc.M102306200.
36. Malumbres M, Harlow E, Hunt T, Hunter T, Lahti JM, Manning G, Morgan DO, Tsai LH, Wolgemuth DJ. 2009. Cyclin-dependent kinases: a family portrait. Nat Cell Biol 11:1275-1276. http://dx.doi.org/10.1038/ncb1109-1275.
37. Akaike Y, Kurokawa K, Kajita K, Kuwano Y, Masuda K, Nishida K, Kang SW, Tanahashi T, Rokutan K. 2011. Skipping of an alternative intron in the srsf1 3' untranslated region increases transcript stability. J Med Invest 58:180-187. http://dx.doi.org/10.2152/jmi.58.180.
38. Das S, Anczukow O, Akerman M, Krainer AR. 2012. Oncogenic splicing factor SRSF1 is a critical transcriptional target of MYC. Cell Rep 1:110-117. http://dx.doi.org/10.1016/j.celrep.2011.12.001.
39. Anczukow O, Rosenberg AZ, Akerman M, Das S, Zhan L, Karni R, Muthuswamy SK, Krainer AR. 2012. The splicing factor SRSF1 regulates apoptosis and proliferation to promote mammary epithelial cell transformation. Nat Struct Mol Biol 19:220-228. http://dx.doi.org/10.1038/nsmb.2207.
40. Spector DL, Lamond AI. 2011. Nuclear speckles. Cold Spring Harb Perspect Biol 3:a000646. http://dx.doi.org/10.1101/cshperspect.a000646.
41. Tollervey D, Kiss T. 1997. Function and synthesis of small nucleolar RNAs. Curr Opin Cell Biol 9:337-342. http://dx.doi.org/10.1016/S0955-0674(97)80005-1.
42. Kiss T. 2004. Biogenesis of small nuclear RNPs. J Cell Sci 117:5949-5951. http://dx.doi.org/10.1242/jcs.01487.
43. Cheng D, Cote J, Shaaban S, Bedford MT. 2007. The arginine methyltransferaseCARM1regulates the coupling of transcription andmRNAprocessing. Mol Cell 25:71-83. http://dx.doi.org/10.1016/j.molcel.2006.11.019.
44. Sims RJ, III, Rojas LA, Beck D, Bonasio R, Schuller R, Drury WJ, III, Eick D, Reinberg D. 2011. The C-terminal domain of RNA polymerase II is modified by site-specific methylation. Science 332:99-103. http://dx.doi.org/10.1126/science.1202663.
45. Kim MY, Hur J, Jeong S. 2009. Emerging roles of RNA and RNA-binding protein network in cancer cells. BMB Rep 42:125-130. http://dx.doi.org/10.5483/BMBRep.2009.42.3.125.