CTD kinase I is required for the integrity of the rDNA tandem array

Nucleic Acids Research

Volumn 34, Issue 17, 2006, Pages 4996-5006

  Grenetier, Sabrina ^a   Bouchoux, Céline ^a,b   Goguel, Valérie ^a,c  

^a CEA SACLAY   (France)

^b National Cancer Research Institute   (United Kingdom)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 1; DNA DIRECTED RNA POLYMERASE; FUNGAL PROTEIN; MESSENGER RNA; PROTEIN FOB1; RIBOSOME DNA; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; DNA ISOLATION; ENZYME ACTIVITY; FUNGAL STRAIN; FUNGUS CULTURE; FUNGUS MUTANT; GENE SILENCING; NONHUMAN; PRIORITY JOURNAL; RNA SYNTHESIS; SCHIZOSACCHAROMYCES POMBE; SOUTHERN BLOTTING; TANDEM REPEAT; WESTERN BLOTTING;

CELL CYCLE PROTEINS; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA, RIBOSOMAL; DNA-BINDING PROTEINS; GENE DELETION; GENE SILENCING; GENES, RRNA; MULTIGENE FAMILY; NUCLEAR PROTEINS; PROTEIN KINASES; RNA POLYMERASE I; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION, GENETIC;

EID: 33750219783     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl493     Document Type: Article

References (66)

1. Petes,T.D. (1979) Yeast ribosomal DNA genes are located on chromosome XII. Proc. Natl Acad. Sci. USA, 76, 410-414.
2. Brewer,B.J. and Fangman,W.L. (1988) A replication fork barrier at the 3′ end of yeast ribosomal RNA genes. Cell, 55, 637-643.
3. Kobayashi,T. and Ganley,A.R. (2005) Recombination regulation by transcription-induced cohesin dissociation in rDNA repeats. Science, 309, 1581-1584.
4. Skryabin,K.G., Eldarov,M.A., Larionov,V.L., Bayev,A.A., Klootwijk,J., de Regt,V.C., Veldman,G.M., Planta,R.J., Georgiev,O.I. and Hadjiolov,A.A. (1984) Structure and function of the nontranscribed spacer regions of yeast rDNA. Nucleic Acids Res., 12, 2955-2968.
5. Laloraya,S., Guacci,V. and Koshland,D. (2000) Chromosomal addresses of the cohesin component Mcd1p. J. Cell. Biol., 151, 1047-1056.
6. Kobayashi,T., Heck,D.J., Nomura,M. and Horiuchi,T. (1998) Expansion and contraction of ribosomal DNA repeats in Saccharomyces cerevisiae: requirement of replication fork blocking (Fob1) protein and the role of RNA polymerase I. Genes Dev., 12, 3821-3830.
7. Gotta,M., Strahl-Bolsinger,S., Renauld,H., Laroche,T., Kennedy,B.K., Grunstein,M. and Gasser,S.M. (1997) Localization of Sir2p: The nucleolus as a compartment for silent information regulators. EMBO J., 16, 3243-3255.
8. Defossez,P.A., Prusty,R., Kaeberlein,M., Lin,S.J., Ferrigno,P., Silver,P.A., Keil,R.L. and Guarente,L. (1999) Elimination of replication block protein Fob1 extends the life span of yeast mother cells. Mol. Cell, 3, 447-455.
9. Kobayashi,T. (2003) The replication fork barrier site forms a unique structure with Fob1p and inhibits the replication fork. Mol. Cell. Biol., 23, 9178-9188.
10. Takeuchi,Y., Horiuchi,T. and Kobayashi,T. (2003) Transcription-dependent recombination and the role of fork collision in yeast rDNA. Genes Dev., 17, 1497-1506.
11. Kobayashi,T., Horiuchi,T., Tongaonkar,P., Vu,L. and Nomura,M. (2004) SIR2 regulates recombination between different rDNA repeats, but not recombination within individual rRNA genes in yeast. Cell, 117, 441-453.
12. Smith,J.S. and Boeke,J.D. (1997) An unusual form of transcriptional silencing in yeast ribosomal DNA. Genes Dev., 11, 241-254.
13. Gottlieb,S. and Esposito,R.E. (1989) A new role for a yeast transcriptional silencer gene, SIR2, in regulation of recombination in ribosomal DNA. Cell, 56, 771-776.
14. Pappas,D.L.,Jr, Frisch,R. and Weinreich,M. (2004) The NAD(+)-dependent Sir2p histone deacetylase is a negative regulator of chromosomal DNA replication. Genes Dev., 18, 769-781.
15. Benguria,A., Hernandez,P., Krimer,D.B. and Schvartzman,J.B. (2003) Sir2p suppresses recombination of replication forks stalled at the replication fork barrier of ribosomal DNA in Saccharomyces cerevisiae. Nucleic Acids Res., 31, 893-898.
16. Dammann,R., Lucchini,R., Koller,T. and Sogo,J.M. (1993) Chromatin structures and transcription of rDNA in yeast Saccharomyces cerevisiae. Nucleic Acids Res., 21, 2331-2338.
17. French,S.L., Osheim,Y.N., Cioci,F., Nomura,M. and Beyer,A.L. (2003) In exponentially growing Saccharomyces cerevisiae cells, rRNA synthesis is determined by the summed RNA polymerase I loading rate rather than by the number of active genes. Mol. Cell. Biol., 23, 1558-1568.
18. Nomura,M. (1998) Transcription factors used by Saccharomyces cerevisiae RNA polymerase I and the mechanism of initiation. In Paule,M.R. (ed.), Transcription of Ribosomal RNA Genes by Eucaryotic RNA Polymerase I. Springer Verlag, Berlin, Germany, pp. 155-172.
19. Keys,D.A., Lee,B.S., Dodd,J.A., Nguyen,T.T., Vu,L., Fantino,E., Burson,L.M., Nogi,Y. and Nomura,M. (1996) Multiprotein transcription factor UAF interacts with the upstream element of the yeast RNA polymerase I promoter and forms a stable preinitiation complex. Genes Dev., 10, 887-903.
20. Keener,J., Josaitis,C.A., Dodd,J.A. and Nomura,M. (1998) Reconstitution of yeast RNA polymerase I transcription in vitro from purified components. TATA-binding protein is not required for basal transcription. J. Biol. Chem., 273, 33795-33802.
21. Vu,L., Siddiqi,I., Lee,B.S., Josaitis,C.A. and Nomura,M. (1999) RNA polymerase switch in transcription of yeast rDNA: Role of transcription factor UAF (upstream activation factor) in silencing rDNA transcription by RNA polymerase II. Proc. Natl Acad. Sci. USA, 96, 4390-4395.
22. Oakes,M., Siddiqi,I., Vu,L., Aris,J. and Nomura,M. (1999) Transcription factor UAF, expansion and contraction of ribosomal DNA (rDNA) repeats, and RNA polymerase switch in transcription of yeast rDNA. Mol. Cell. Biol., 19, 8559-8569.
23. Lee,J.M. and Greenleaf,A.L. (1991) CTD kinase large subunit is encoded by CTK1, a gene required for normal growth of Saccharomyces cerevisiae. Gene Expr., 1, 149-167.
24. Hautbergue,G. and Goguel,V. (2001) Activation of the cyclin-dependent kinase CTDK-I requires the heterodimerization of two unstable subunits. J. Biol. Chem., 15, 8005-8013.
25. Cho,E.J., Kobor,M.S., Kim,M., Greenblatt,J. and Buratowski,S. (2001) Opposing effects of Ctk1 kinase and Fcp1 phosphatase at Ser 2 of the RNA polymerase II C-terminal domain. Genes Dev., 15, 3319-3329.
26. 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.
27. Skaar,D.A. and Greenleaf,A.L. (2002) The RNA Polymerase II CTD Kinase CTDK-I Affects Pre-mRNA 30 Cleavage/Polyadenylation through the Processing Component Pti1p. Mol. Cell, 10, 1429-1439.
28. Ahn,S.H., Kim,M. and Buratowski,S. (2004) Phosphorylation of serine 2 within the RNA polymerase II C-terminal domain couples transcription and 3′ end processing. Mol. Cell. Biol., 13, 67-76.
29. Ostapenko,D. and Solomon,M.J. (2003) Budding yeast CTDK-I is required for DNA damage-induced transcription. Eukaryot. Cell, 2, 274-283.
30. Xiao,T., Hall,H., Kizer,K.O., Shibata,Y., Hall,M.C., Borchers,C.H. and Strahl,B.D. (2003) Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes Dev., 17, 654-663.
31. Hurt,E., Luo,M.J., Rother,S., Reed,R. and Strasser,K. (2004) Cotranscriptional recruitment of the serine-arginine-rich (SR)-like proteins Gbp2 and Hrb1 to nascent mRNA via the TREX complex. Proc. Natl Acad. Sci. USA, 101, 1858-1862.
32. Bradsher,J., Auriol,J., Proietti de Santis,L., Iben,S., Vonesch,J.L., Grummt,I. and Egly,J.M. (2002) CSB is a component of RNA pol I transcription. Mol. Cell, 10, 819-829.
33. Hoogstraten,D., Nigg,A.L., Heath,H., Mullenders,L.H., van Driel,R., Hoeijmakers,J.H., Vermeulen,W. and Houtsmuller,A.B. (2002) Rapid switching of TFIIH between RNA polymerase I and II transcription and DNA repair in vivo. Mol. Cell, 10, 1163-1174.
34. Iben,S., Tschochner,H., Bier,M., Hoogstraten,D., Hozak,P., Egly,J.M. and Grummt,I. (2002) TFIIH plays an essential role in RNA polymerase I transcription. Cell, 109, 297-306.
35. Lin,C.Y., Tuan,J., Scalia,P., Bui,T. and Comai,L. (2002) The cell cycle regulatory factor TAF1 stimulates ribosomal DNA transcription by binding to the activator UBF. Curr. Biol., 12, 2142-2146.
36. Fath,S., Kobor,M.S., Philippi,A., Greenblatt,J. and Tschochner,H. (2004) Dephosphorylation of RNA polymerase I by Fcp1p is required for efficient rRNA synthesis. J. Biol. Chem., 279, 25251-25259.
37. Bouchoux,C., Hautbergue,G., Grenetier,S., Carles,C., Riva,M. and Goguel,V. (2004) CTD kinase I is involved in RNA polymerase I transcription. Nucleic Acids Res., 32, 5851-5860.
38. Rothstein,R.J. (1983) One step gene disruption in yeast. Methods Enzymol., 101, 202-211.
39. Longtine,M.S., McKenzie,A., Demarini,D.J., Shah,N.G., Wach,A., Brachat,A., Philippsen,P. and Pringle,J.R. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast, 14, 953-961.
40. Hautbergue,G. and Goguel,V. (1999) The yeast C-type cyclin Ctk2p is phosphorylated and rapidly degraded by the ubiquitin-proteasome pathway. Mol. Cell. Biol., 19, 2527-2534.
41. Buck,S.W., Sandmeier,J.J. and Smith,J.S. (2002) RNA polymerase I propagates unidirectional spreading of rDNA silent chromatin. Cell, 111, 1003-1014.
42. Sinclair,D.A. and Guarente,L. (1997) Extrachromosomal rDNA circles - a cause of aging in yeast. Cell, 91, 1033-1042.
43. Schmitt,M.E., Brown,T.A. and Trumpower,B.L. (1990) A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res., 18, 3091-3092.
44. Buhler,J.M., Huet,J., Davies,K.E., Sentenac,A. and Fromageot,P. (1980) Immunological studies of yeast nuclear RNA polymerases at the subunit level. J. Biol. Chem., 255, 9949-9954.
45. Kuras,L. and Struhl,K. (1999) Binding of TBP to promoters in vivo is stimulated by activators and requires Pol II holoenzyme. Nature, 399, 609-613.
46. Kuras,L., Borggrefe,T. and Kornberg,R.D. (2003) Association of the Mediator complex with enhancers of active genes. Proc. Natl Acad. Sci. USA, 100, 13887-13891.
47. Sterner,D.E., Moon Lee,J., Hardin,S.E. and Greenleaf,A.L. (1995) The yeast carboxyl-terminal repeat domain kinase CTDK-I is a divergent cyclin-cyclin-dependent kinase complex. Mol. Cell. Biol., 15, 5716-5724.
48. Oakes,M., Aris,J.P., Brockenbrough,J.S., Wai,H., Vu,L. and Nomura,M. (1998) Mutational analysis of the structure and localization of the nucleolus in the yeast Saccharomyces cerevisiae. J. Cell. Biol., 143, 23-34.
49. Rustchenko,E.P. and Sherman,F. (1994) Physical constitution of ribosomal genes in common strains of Saccharomyces cerevisiae. Yeast, 10, 1157-1171.
50. Winston,F., Dollard,C. and Ricupero-Hovasse,S.L. (1995) Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast, 11, 53-55.
51. Thomas,B.J. and Rothstein,R. (1989) Elevated recombination rates in transcriptionally active DNA. Cell, 56, 619-630.
52. Hallstrom,T.C., Katzmann,D.J., Torres,R.J., Sharp,W.J. and Moye-Rowley,W.S. (1998) Regulation of transcription factor Pdr1p function by an Hsp70 protein in Saccharomyces cerevisiae. Mol. Cell. Biol., 18, 1147-1155.
53. Gangloff,S., Zou,H. and Rothstein,R. (1996) Gene conversion plays the major role in controlling the stability of large tandem repeats in yeast. EMBO J., 15, 1715-1725.
54. Askree,S.H., Yehuda,T., Smolikov,S., Gurevich,R., Hawk,J., Coker,C., Krauskopf,A., Kupiec,M. and McEachern,M.J. (2004) A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length. Proc. Natl Acad. Sci. USA, 101, 8658-8663.
55. Guacci,V., Koshland,D. and Strunnikov,A. (1997) A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S.cerevisiae. Cell, 91, 47-57.
56. Merker,R.J. and Klein,H.L. (2002) hpr1Delta affects ribosomal DNA recombination and cell life span in Saccharomyces cerevisiae. Mol. Cell. Biol., 22, 421-429.
57. Johzuka,K., Terasawa,M., Ogawa,H., Ogawa,T. and Horiuchi,T. (2006) Condensin loaded onto the replication fork barrier site in the rRNA gene repeats during S phase in a FOB1-dependent fashion to prevent contraction of a long repetitive array in Saccharomyces cerevisiae. Mol. Cell. Biol., 26, 2226-2236.
58. Kim,R.A. and Wang,J.C. (1989) A subthreshold level of DNA topoisomerases leads to the excision of yeast rDNA as extrachromosomal rings. Cell, 57, 975-985.
59. Johzuka,K. and Horiuchi,T. (2002) Replication fork block protein, Fob1, acts as an rDNA region specific recombinator in S. cerevisiae. Genes Cells, 7, 99-113.
60. Park,P.U., Defossez,P.A. and Guarente,L. (1999) Effects of mutations in DNA repair genes on formation of ribosomal DNA circles and life span in Saccharomyces cerevisiae. Mol. Cell. Biol., 19, 3848-3856.
61. Smith,J.S., Caputo,E. and Boeke,J.D. (1999) A genetic screen for ribosomal DNA silencing defects identifies multiple DNA replication and chromatin-modulating factors. Mol. Cell. Biol., 19, 3184-3197.
62. Klootwijk,J., de Jonge,P. and Planta,R.J. (1979) The primary transcript of the ribosomal repeating unit in yeast. Nucleic Acids Res., 6, 27-39.
63. Ford,E., Voit,R., Liszt,G., Magin,C., Grummt,I. and Guarente,L. (2006) Mammalian Sir2 homolog SIRT7 is an activator of RNA polymerase I transcription. Genes Dev., 20, 1075-1080.
64. Cioci,F., Vu,L., Eliason,K., Oakes,M., Siddiqi,I.N. and Nomura,M. (2003) Silencing in yeast rDNA chromatin: Reciprocal relationship in gene expression between RNA polymerase I and II. Mol. Cell, 12, 135-145.
65. Holmes,S.G., Rose,A.B., Steuerle,K., Saez,E., Sayegh,S., Lee,Y.M. and Broach,J.R. (1997) Hyperactivation of the silencing proteins, Sir2p and Sir3p, causes chromosome loss. Genetics, 145, 605-614.
66. Michel,A.H., Kornmann,B., Dubrana,K. and Shore,D. (2005) Spontaneous rDNA copy number variation modulates Sir2 levels and epigenetic gene silencing. Genes Dev., 19, 1199-1210.