The RNAPII-CTD Maintains Genome Integrity through Inhibition of Retrotransposon Gene Expression and Transposition

1. Allison LA, Moyle M, Shales M, Ingles CJ. Extensive homology among the largest subunits of eukaryotic and prokaryotic RNA polymerases. Cell 1985 09/01;42(2):599–610. 3896517

2. Corden JL, Cadena DL, Ahearn JM Jr, Dahmus ME. A unique structure at the carboxyl terminus of the largest subunit of eukaryotic RNA polymerase II. Proc Natl Acad Sci U S A 1985 Dec;82(23):7934–7938. 2999785

3. Heidemann M, Hintermair C, Voss K, Eick D. Dynamic phosphorylation patterns of RNA polymerase II CTD during transcription. Biochim Biophys Acta 2012 Sep 7.

4. Hsin JP, Manley JL. The RNA polymerase II CTD coordinates transcription and RNA processing. Genes Dev 2012 Oct 1;26(19):2119–2137. doi: 10.1101/gad.200303.112 23028141

5. Zhang DW, Rodriguez-Molina JB, Tietjen JR, Nemec CM, Ansari AZ. Emerging Views on the CTD Code. Genet Res Int 2012;2012:347214. doi: 10.1155/2012/347214 22567385

6. Max T, Sogaard M, Svejstrup JQ. Hyperphosphorylation of the C-terminal repeat domain of RNA polymerase II facilitates dissociation of its complex with mediator. J Biol Chem 2007 May 11;282(19):14113–14120. 17376774

7. Hengartner CJ, Myer VE, Liao SM, Wilson CJ, Koh SS, Young RA. Temporal regulation of RNA polymerase II by Srb10 and Kin28 cyclin-dependent kinases. Mol Cell 1998 Jul;2(1):43–53. 9702190

8. Chapman RD, Heidemann M, Albert TK, Mailhammer R, Flatley A, Meisterernst M, et al. Transcribing RNA polymerase II is phosphorylated at CTD residue serine-7. Science 2007 12/14;318(5857):1780–2. 18079404

9. Mayer A, Heidemann M, Lidschreiber M, Schreieck A, Sun M, Hintermair C, et al. CTD tyrosine phosphorylation impairs termination factor recruitment to RNA polymerase II. Science 2012 Jun 29;336(6089):1723–1725. doi: 10.1126/science.1219651 22745433

10. Komarnitsky P, Cho EJ, Buratowski S. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev 2000 Oct 1;14(19):2452–2460. 11018013

11. Nonet ML, Young RA. Intragenic and extragenic suppressors of mutations in the heptapeptide repeat domain of Saccharomyces cerevisiae RNA polymerase II. Genetics 1989 12/01;123(4):715–24. 2693207

12. Aristizabal MJ, Negri GL, Benschop JJ, Holstege FC, Krogan NJ, Kobor MS. High-throughput genetic and gene expression analysis of the RNAPII-CTD reveals unexpected connections to SRB10/CDK8. PLoS Genet 2013 Aug;9(8):e1003758. doi: 10.1371/journal.pgen.1003758 24009531

13. Nonet M, Sweetser D, Young RA. Functional redundancy and structural polymorphism in the large subunit of RNA polymerase II. Cell 1987 Sep 11;50(6):909–915. 3304659

14. Scafe C, Chao D, Lopes J, Hirsch JP, Henry S, Young RA. RNA polymerase II C-terminal repeat influences response to transcriptional enhancer signals. Nature 1990 10/04;347(6292):491–4. 2215664

15. Wong JMS, Ingles CJ. A compromised yeast RNA Polymerase II enhances UV sensitivity in the absence of global genome nucleotide excision repair. Molecular and General Genetics MGG 2001 02/22;264(6):842–851. 11254132

16. Elder RT, St John TP, Stinchcomb DT, Davis RW, Scherer S, Davis RW. Studies on the transposable element Ty1 of yeast. I. RNA homologous to Ty1. II. Recombination and expression of Ty1 and adjacent sequences. Cold Spring Harb.Symp.Quant.Biol. 1981;45(2):581.

17. Kim JM, Vanguri S, Boeke JD, Gabriel A, Voytas DF. Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res 1998 May;8(5):464–478. 9582191

18. Havecker ER, Gao X, Voytas DF. The diversity of LTR retrotransposons. Genome Biol 2004;5(6):225. 15186483

19. Boeke JD, Garfinkel DJ, Styles CA, Fink GR. Ty elements transpose through an RNA intermediate. Cell 1985 Mar;40(3):491–500. 2982495

20. Lesage P, Todeschini AL. Happy together: the life and times of Ty retrotransposons and their hosts. Cytogenet Genome Res 2005;110(1–4):70–90. 16093660

21. Williamson VM, Young ET, Ciriacy M. Transposable elements associated with constitutive expression of yeast alcohol dehydrogenase II. Cell 1981 Feb;23(2):605–614. 6258806

22. Roeder GS, Fink GR. DNA rearrangements associated with a transposable element in yeast. Cell 1980 Aug;21(1):239–249. 6250713

23. Errede B, Cardillo TS, Sherman F, Dubois E, Deschamps J, Wiame JM. Mating signals control expression of mutations resulting from insertion of a transposable repetitive element adjacent to diverse yeast genes. Cell 1980 Nov;22(2 Pt 2):427–436. 6256080

24. Todeschini AL, Morillon A, Springer M, Lesage P. Severe adenine starvation activates Ty1 transcription and retrotransposition in Saccharomyces cerevisiae. Mol Cell Biol 2005 Sep;25(17):7459–7472. 16107695

25. Bradshaw VA, McEntee K. DNA damage activates transcription and transposition of yeast Ty retrotransposons. Mol Gen Genet 1989 Sep;218(3):465–474. 2555668

26. Sacerdot C, Mercier G, Todeschini AL, Dutreix M, Springer M, Lesage P. Impact of ionizing radiation on the life cycle of Saccharomyces cerevisiae Ty1 retrotransposon. Yeast 2005 Apr 30;22(6):441–455. 15849797

27. Morillon A, Benard L, Springer M, Lesage P. Differential effects of chromatin and Gcn4 on the 50-fold range of expression among individual yeast Ty1 retrotransposons. Mol Cell Biol 2002 Apr;22(7):2078–2088. 11884596

28. Laloux I, Dubois E, Dewerchin M, Jacobs E. TEC1, a gene involved in the activation of Ty1 and Ty1-mediated gene expression in Saccharomyces cerevisiae: cloning and molecular analysis. Mol Cell Biol 1990 Jul;10(7):3541–3550. 2192259

29. Errede B. MCM1 binds to a transcriptional control element in Ty1. Mol Cell Biol 1993 Jan;13(1):57–62. 8380228

30. Gray WM, Fassler JS. Isolation and analysis of the yeast TEA1 gene, which encodes a zinc cluster Ty enhancer-binding protein. Mol Cell Biol 1996 Jan;16(1):347–358. 8524314

31. Gray WM, Fassler JS. Role of Saccharomyces cerevisiae Rap1 protein in Ty1 and Ty1-mediated transcription. Gene Expr 1993;3(3):237–251. 8019126

32. Madison JM, Dudley AM, Winston F. Identification and analysis of Mot3, a zinc finger protein that binds to the retrotransposon Ty long terminal repeat (delta) in Saccharomyces cerevisiae. Mol Cell Biol 1998 Apr;18(4):1879–1890. 9528759

33. Morillon A, Springer M, Lesage P. Activation of the Kss1 invasive-filamentous growth pathway induces Ty1 transcription and retrotransposition in Saccharomyces cerevisiae. Mol Cell Biol 2000 Aug;20(15):5766–5776. 10891512

34. Conte D Jr, Curcio MJ. Fus3 controls Ty1 transpositional dormancy through the invasive growth MAPK pathway. Mol Microbiol 2000 Jan;35(2):415–427. 10652102

35. Bleykasten-Grosshans C, Friedrich A, Schacherer J. Genome-wide analysis of intraspecific transposon diversity in yeast. BMC Genomics 2013 Jun 14;14:399-2164-14-399.

36. Voytas DF, Boeke JD. Yeast retrotransposon revealed. Nature 1992 Aug 27;358(6389):717.

37. Cassart C, Drogat J, Migeot V, Hermand D. Distinct requirement of RNA polymerase II CTD phosphorylations in budding and fission yeast. Transcription 2012 Sep-Oct;3(5):231–234. doi: 10.4161/trns.21066 22771993

38. Scholes DT, Banerjee M, Bowen B, Curcio MJ. Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance. Genetics 2001 Dec;159(4):1449–1465. 11779788

39. Bryk M, Banerjee M, Conte D Jr, Curcio MJ. The Sgs1 helicase of Saccharomyces cerevisiae inhibits retrotransposition of Ty1 multimeric arrays. Mol Cell Biol 2001 Aug;21(16):5374–5388. 11463820

40. Liu Y, Kung C, Fishburn J, Ansari AZ, Shokat KM, Hahn S. Two cyclin-dependent kinases promote RNA polymerase II transcription and formation of the scaffold complex. Mol Cell Biol 2004 02/01;24(4):1721–35. 14749387

41. Akoulitchev S, Chuikov S, Reinberg D. TFIIH is negatively regulated by cdk8-containing mediator complexes. Nature 2000 Sep 7;407(6800):102–106. 10993082

42. Mayer A, Lidschreiber M, Siebert M, Leike K, Soding J, Cramer P. Uniform transitions of the general RNA polymerase II transcription complex. Nat Struct Mol Biol 2010 Oct;17(10):1272–1278. doi: 10.1038/nsmb.1903 20818391

43. Tietjen JR, Zhang DW, Rodriguez-Molina JB, White BE, Akhtar MS, Heidemann M, et al. Chemical-genomic dissection of the CTD code. Nat Struct Mol Biol 2010 Sep;17(9):1154–1161. doi: 10.1038/nsmb.1900 20802488

44. Kim H, Erickson B, Luo W, Seward D, Graber JH, Pollock DD, et al. Gene-specific RNA polymerase II phosphorylation and the CTD code. Nat Struct Mol Biol 2010 Oct;17(10):1279–1286. doi: 10.1038/nsmb.1913 20835241

45. Bataille AR, Jeronimo C, Jacques PE, Laramee L, Fortin ME, Forest A, et al. A universal RNA polymerase II CTD cycle is orchestrated by complex interplays between kinase, phosphatase, and isomerase enzymes along genes. Mol Cell 2012 Jan 27;45(2):158–170. doi: 10.1016/j.molcel.2011.11.024 22284676

46. Galbraith MD, Donner AJ, Espinosa JM. CDK8: a positive regulator of transcription. Transcription 2010 Jul-Aug;1(1):4–12. doi: 10.4161/trns.1.1.12373 21327159

47. Hirst M, Kobor MS, Kuriakose N, Greenblatt J, Sadowski I. GAL4 is regulated by the RNA polymerase II holoenzyme-associated cyclin-dependent protein kinase SRB10/CDK8. Mol Cell 1999 05/01;3(5):673–8. 10360183

48. Servant G, Pennetier C, Lesage P. Remodeling yeast gene transcription by activating the Ty1 long terminal repeat retrotransposon under severe adenine deficiency. Mol Cell Biol 2008 Sep;28(17):5543–5554. doi: 10.1128/MCB.00416-08 18591253

49. Wong Sak Hoi J, Dumas B. Ste12 and Ste12-like proteins, fungal transcription factors regulating development and pathogenicity. Eukaryot Cell 2010 Apr;9(4):480–485. doi: 10.1128/EC.00333-09 20139240

50. Nelson C, Goto S, Lund K, Hung W, Sadowski I. Srb10/Cdk8 regulates yeast filamentous growth by phosphorylating the transcription factor Ste12. Nature 2003 Jan 9;421(6919):187–190. 12520306

51. Raithatha S, Su TC, Lourenco P, Goto S, Sadowski I. Cdk8 regulates stability of the transcription factor Phd1 to control pseudohyphal differentiation of Saccharomyces cerevisiae. Mol Cell Biol 2011 Nov 28.

52. Borneman AR, Gianoulis TA, Zhang ZD, Yu H, Rozowsky J, Seringhaus MR, et al. Divergence of transcription factor binding sites across related yeast species. Science 2007 Aug 10;317(5839):815–819. 17690298

53. Wilson MD, Harreman M, Svejstrup JQ. Ubiquitylation and degradation of elongating RNA polymerase II: the last resort. Biochim Biophys Acta 2013 Jan;1829(1):151–157. doi: 10.1016/j.bbagrm.2012.08.002 22960598

54. Somesh BP, Sigurdsson S, Saeki H, Erdjument-Bromage H, Tempst P, Svejstrup JQ. Communication between distant sites in RNA polymerase II through ubiquitylation factors and the polymerase CTD. Cell 2007 Apr 6;129(1):57–68. 17418786

55. Gold MO, Rice AP. Targeting of CDK8 to a promoter-proximal RNA element demonstrates catalysis-dependent activation of gene expression. Nucleic Acids Res 1998 Aug 15;26(16):3784–3788. 9685496

56. Belakavadi M, Fondell JD. Cyclin-dependent kinase 8 positively cooperates with Mediator to promote thyroid hormone receptor-dependent transcriptional activation. Mol Cell Biol 2010 May;30(10):2437–2448. doi: 10.1128/MCB.01541-09 20231357

57. Longtine MS, McKenzie A 3rd, Demarini DJ, Shah NG, Wach A, Brachat A, et al. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998 Jul;14(10):953–961. 9717241

58. Schulze JM, Jackson J, Nakanishi S, Gardner JM, Hentrich T, Haug J, et al. Linking Cell Cycle to Histone Modifications: SBF and H2B Monoubiquitination Machinery and Cell-Cycle Regulation of H3K79 Dimethylation. Mol Cell 2009 11/09;35(5):626–641. doi: 10.1016/j.molcel.2009.07.017 19682934

59. Droit A, Cheung C, Gottardo R. rMAT—an R/Bioconductor package for analyzing ChIP-chip experiments. Bioinformatics 2010 Mar 1;26(5):678–679. doi: 10.1093/bioinformatics/btq023 20089513

60. Guarente L, Ptashne M. Fusion of Escherichia coli lacZ to the cytochrome c gene of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 1981 Apr;78(4):2199–2203. 6264467

61. Guarente L. Yeast promoters and lacZ fusions designed to study expression of cloned genes in yeast. Methods Enzymol 1983;101:181–191. 6310321

62. Lu PY, Kobor MS. Maintenance of Heterochromatin Boundary and Nucleosome Composition at Promoters by the Asf1 Histone Chaperone and SWR1-C Chromatin Remodeler in Saccharomyces cerevisiae. Genetics 2014 Feb 27.

63. Hall BM, Ma CX, Liang P, Singh KK. Fluctuation AnaLysis CalculatOR: a web tool for the determination of mutation rate using Luria-Delbr?ck fluctuation analysis. Bioinformatics 2009 Jun 15;25(12):1564–1565. doi: 10.1093/bioinformatics/btp253 19369502

64. Hentrich T, Schulze JM, Emberly E, Kobor MS. CHROMATRA: a Galaxy tool for visualizing genome-wide chromatin signatures. Bioinformatics 2012 Mar 1;28(5):717–718. doi: 10.1093/bioinformatics/bts007 22238257

65. Holstege FC, Jennings EG, Wyrick JJ, Lee TI, Hengartner CJ, Green MR, et al. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 1998 Nov 25;95(5):717–728. 9845373