Highly Transcribed RNA Polymerase II Genes Are Impediments to Replication Fork Progression in Saccharomyces cerevisiae

Molecular Cell

Volumn 34, Issue 6, 2009, Pages 722-734

  Azvolinsky, Anna ^a   Giresi, Paul G ^b   Lieb, Jason D ^b   Zakian, Virginia A ^a  

^a PRINCETON UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

DNA

Indexed keywords

DNA POLYMERASE; MYC PROTEIN; POL PROTEIN; RAP1 PROTEIN; RNA POLYMERASE II;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA PROTEIN COMPLEX; ENZYME BINDING; GENETIC TRANSCRIPTION; GENOME; NONHUMAN; OPEN READING FRAME; PROMOTER REGION; RNA REPLICATION; SACCHAROMYCES CEREVISIAE; WILD TYPE;

BINDING SITES; DNA HELICASES; DNA POLYMERASE II; DNA REPLICATION; MUTATION; OPEN READING FRAMES; PROMOTER REGIONS, GENETIC; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERE-BINDING PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

SACCHAROMYCES CEREVISIAE;

EID: 67449113551     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2009.05.022     Document Type: Article

References (41)

1. Admire A., Shanks L., Danzl N., Wang M., Weier U., Stevens W., Hunt E., and Weinert T. Cycles of chromosome instability are associated with a fragile site and are increased by defects in DNA replication and checkpoint controls in yeast. Genes Dev. 20 (2006) 159-173
2. Azvolinsky A., Dunaway S., Torres J., Bessler J., and Zakian V.A. The S. cerevisiae Rrm3p DNA helicase moves with the replication fork and affects replication of all yeast chromosomes. Genes Dev. 20 (2006) 3104-3116
3. Bedinger P., Hochstrasser M., Jongeneel C., and Alberts B. Properties of the T4 bacteriophage DNA replication apparatus: the T4 dda DNA helicase is required to pass a bound RNA polymerase molecule. Cell 34 (1983) 115-123
4. Bi X., and Broach J.R. UASrpg can function as a heterochromatin boundary element in yeast. Genes Dev. 13 (1999) 1089-1101
5. Boule J.B., and Zakian V.A. Roles of Pif1-like helicases in the maintenance of genomic stability. Nucleic Acids Res. 34 (2006) 4147-4153
6. Brewer B.J., and Fangman W.L. A replication fork barrier at the 3′ end of yeast ribosomal RNA genes. Cell 55 (1988) 637-643
7. Brewer B.J., Lockshon D., and Fangman W.L. The arrest of replication forks in the rDNA of yeast occurs independently of transcription. Cell 71 (1992) 267-276
8. Buck M.J., Nobel A.B., and Lieb J.D. ChIPOTle: a user-friendly tool for the analysis of ChIP-chip data. Genome Biol. 6 (2005) R97
9. Cha R.S., and Kleckner N. ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297 (2002) 602-606
10. Deshpande A.M., and Newlon C.S. DNA replication fork pause sites dependent on transcription. Science 272 (1996) 1030-1033
11. Dieci G., Giuliodori S., Catellani M., Percudani R., and Ottonello S. Intragenic promoter adaptation and facilitated RNA polymerase III recycling in the transcription of SCR1, the 7SL RNA gene of Saccharomyces cerevisiae. J. Biol. Chem. 277 (2002) 6903-6914
12. Elias-Arnanz M., and Salas M. Bacteriophage phi29 DNA replication arrest caused by codirectional collisions with the transcription machinery. EMBO J. 16 (1997) 5775-5783
13. Felici F., Cesareni G., and Hughes J.M. The most abundant small cytoplasmic RNA of Saccharomyces cerevisiae has an important function required for normal cell growth. Mol. Cell. Biol. 9 (1989) 3260-3268
14. Greenfeder S.A., and Newlon C.S. Replication forks pause at yeast centromeres. Mol. Cell. Biol. 12 (1992) 4056-4066
15. Holstege F.C., Jennings E.G., Wyrick J.J., Lee T.I., Hengartner C.J., Green M.R., Golub T.R., Lander E.S., and Young R.A. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95 (1998) 717-728
16. Ivessa A.S., Lenzmeier B.A., Bessler J.B., Goudsouzian L.K., Schnakenberg S.L., and Zakian V.A. The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes. Mol. Cell 12 (2003) 1525-1536
17. Ivessa A.S., Zhou J.-Q., Schulz V.P., Monson E.M., and Zakian V.A. Saccharomyces Rrm3p, a 5′ to 3′ DNA helicase that promotes replication fork progression through telomeric and sub-telomeric DNA. Genes Dev. 16 (2002) 1383-1396
18. Ivessa A.S., Zhou J.-Q., and Zakian V.A. The Saccharomyces Pif1p DNA helicase and the highly related Rrm3p have opposite effects on replication fork progression in ribosomal DNA. Cell 100 (2000) 479-489
19. Iyer V.R., Horak C.E., Scafe C.S., Botstein D., Snyder M., and Brown P.O. Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature 409 (2001) 533-538
20. Kobayashi T., and Horiuchi T. A yeast gene product, Fob1 protein, required for both replication fork blocking and recombinational hotspot activities. Genes Cells 1 (1996) 465-474
21. Lemoine F.J., Degtyareva N.P., Lobachev K., and Petes T.D. Chromosomal translocations in yeast induced by low levels of DNA polymerase a model for chromosome fragile sites. Cell 120 (2005) 587-598
22. Lieb J.D., Liu X., Botstein D., and Brown P.O. Promoter-specific binding of Rap1 revealed by genome-wide maps of protein-DNA association. Nat. Genet. 28 (2001) 327-334
23. Linskens M.H.K., and Huberman J.A. Organization of replication of ribosomal DNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 8 (1988) 4927-4935
24. Liu B., and Alberts B.M. Head-on collision between a DNA replication apparatus and RNA polymerase transcription complex. Science 267 (1995) 1131-1137
25. Mirkin E.V., Castro Roa D., Nudler E., and Mirkin S.M. Transcription regulatory elements are punctuation marks for DNA replication. Proc. Natl. Acad. Sci. USA 103 (2006) 7276-7281
26. Mirkin E.V., and Mirkin S.M. Mechanisms of transcription-replication collisions in bacteria. Mol. Cell. Biol. 25 (2005) 888-895
27. Nagalakshmi U., Wang Z., Waern K., Shou C., Raha D., Gerstein M., and Snyder M. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320 (2008) 1344-1349
28. Pinter S.F., Aubert S.D., and Zakian V.A. The Schizosaccharomyces pombe Pfh1p DNA helicase is essential for the maintenance of nuclear and mitochondrial DNA. Mol. Cell. Biol. 28 (2008) 6594-6608
29. Poloumienko A., Dershowitz A., De J., and Newlon C.S. Completion of replication map of Saccharomyces cerevisiae chromosome III. Mol. Biol. Cell 12 (2001) 3317-3327
30. Prado F., and Aguilera A. Impairment of replication fork progression mediates RNA polII transcription-associated recombination. EMBO J. 24 (2005) 1267-1276
31. Raghuraman M.K., Winzeler E.A., Collingwood D., Hunt S., Wodicka L., Conway A., Lockhart D.J., Davis R.W., Brewer B.J., and Fangman W.L. Replication dynamics of the yeast genome. Science 294 (2001) 115-121
32. Raveendranathan M., Chattopadhyay S., Bolon Y.T., Haworth J., Clarke D.J., and Bielinsky A.K. Genome-wide replication profiles of S-phase checkpoint mutants reveal fragile sites in yeast. EMBO J. 25 (2006) 3627-3639
33. R Foundation for Statistical Computing (2007). R 2.5.0 (http://www.r-project.org/foundation/).
34. Taggart A.K.P., Teng S.-C., and Zakian V.A. Est1p as a cell cycle-regulated activator of telomere-bound telomerase. Science 297 (2002) 1023-1026
35. Takeuchi Y., Horiuchi T., and Kobayashi T. Transcription-dependent recombination and the role of fork collision in yeast rDNA. Genes Dev. 17 (2003) 1497-1506
36. Thomas B.J., and Rothstein R. Elevated recombination rates in transcriptionally active DNA. Cell 56 (1989) 619-630
37. Torres J.Z., Bessler J.B., and Zakian V.A. Local chromatin structure at the ribosomal DNA causes replication fork pausing and genome instability in the absence of the S. cerevisiae DNA helicase Rrm3p. Genes Dev. 18 (2004) 498-503
38. Uptain S.M., Kane C.M., and Chamberlin M.J. Basic mechanisms of transcript elongation and its regulation. Annu. Rev. Biochem. 66 (1997) 117-172
39. Yabuki N., Terashima H., and Kitada K. Mapping of early firing origins on a replication profile of budding yeast. Genes Cells 7 (2002) 781-789
40. Yu Q., Qiu R., Foland T.B., Griesen D., Galloway C.S., Chiu Y.H., Sandmeier J., Broach J.R., and Bi X. Rap1p and other transcriptional regulators can function in defining distinct domains of gene expression. Nucleic Acids Res. 31 (2003) 1224-1233
41. Zhao Y., McIntosh K.B., Rudra D., Schawalder S., Shore D., and Warner J.R. Fine-structure analysis of ribosomal protein gene transcription. Mol. Cell. Biol. 26 (2006) 4853-4862