UV light-induced DNA lesions cause dissociation of yeast RNA polymerases-I and establishment of a specialized chromatin structure at rRNA genes

Nucleic Acids Research

Volumn 42, Issue 1, 2014, Pages 380-395

  Tremblay, Maxime ^a   Charton, Romain ^a   Wittner, Manuel ^b   Levasseur, Geneviève ^a   Griesenbeck, Joachim ^b   Conconi, Antonio ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

^b UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED RNA POLYMERASE; HIGH MOBILITY GROUP B PROTEIN; PROTEIN HMO1; PSORALEN; PYRIMIDINE DIMER; RIBOSOME RNA; RNA POLYMERASE II; UNCLASSIFIED DRUG; HIGH MOBILITY GROUP A PROTEIN; RNA POLYMERASE;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; CROSS LINKING; DISSOCIATION; DNA DAMAGE; ELECTRON MICROSCOPY; EXCISION REPAIR; GENE REARRANGEMENT; GENETIC ASSOCIATION; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; RNA CLEAVAGE; RNA GENE; RNA STABILITY; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; ULTRAVIOLET IRRADIATION; CYTOTOXICITY; DNA CLEAVAGE; DOWNSTREAM PROCESSING; FUNGAL STRAIN; FUNGUS GROWTH; GENE REPLICATION; GENETIC TRANSCRIPTION; ULTRAVIOLET RADIATION; ULTRAVIOLET RADIATION INDUCED DNA DAMAGE; YEAST;

EID: 84891815229     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt871     Document Type: Article

References (43)

1. Friedberg, E.C., Walker, G.C., Siede, W., Wood, R.D., Schultz, R.A. and Ellenberger, T. (2006) DNA Repair and Mutagenesis. ASM Press, Washington
2. Bohr, V., Smith, C., Okumoto, D. and Hanawalt, P. (1985) DNA repair in an active gene: Removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell, 40, 359-369
3. Mellon, I., Spivak, G. and Hanawalt, P. (1987) Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell, 51, 241-249
4. Lainé, J.P. and Egly, J.M. (2006) Initiation of DNA repair mediated by stalled RNA polymerase IIO. EMBO J., 25, 387-397
5. Fousteri, M., Vermeulen, W., van Zeeland, A.A. and Mullenders, L.H.F. (2006) Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol. Cell, 23, 471-482
6. Tornaletti, S. (2009) Transcription-coupled DNA repair: Directing your effort where it's most needed. Cell. Mol. Life Sci., 66, 1010-1020
7. Fousteri, M. and Mullenders, L.H.F. (2008) Transcription-coupled nucleotide excision repair in mammalian cells: Molecular mechanisms and biological effects. Cell Res., 18, 73-84
8. Walmacq, C., Cheung, A.C.M., Kireeva, M.L., Lubkowska, L., Ye, C., Gotte, D., Strathern, J.N., Carell, T., Cramer, P. and Kashlev, M. (2012) Mechanism of translesion transcription by RNA polymerase II and its role in cellular resistance to DNA damage. Mol. Cell, 46, 18-29
9. Conconi, A., Widmer, R.M., Koller, T. and Sogo, J.M. (1989) Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell, 57, 753-761
10. Dammann, R., Lucchini, R., Koller, T. and Sogo, J.M. (1993) Chromatin structure and transcription of rDNA in yeast Saccharomyces cerevisiae. Nucl. Acids Res., 21, 2331-2338
11. Wittner, M., Hamperl, S., Stockl, U., Seufert, W., Tschochner, H., Milkereit, P. and Griesenbeck, J. (2011) Establishment and maintenance of alternative chromatin states at a multicopy gene locus. Cell, 145, 543-554
12. Merz, K., Hondele, M., Goetze, H., Gmelch, K., Stoeckl, U. and Griesenbeck, J. (2008) Actively transcribed rRNA genes in S. cerevisiae are organized in a specialized chromatin associated with the high-mobility group protein Hmo1 and are largely devoid of histone molecules. Genes & Dev., 22, 1190-1204
13. Toussaint, M., Levasseur, G., Tremblay, M., Paquette, M. and Conconi, A. (2005) Psoralen photocrosslinking, a tool to study the chromatin structure of RNA polymerase I-Transcribed ribosomal genes. Biochem. Cell Biol., 83, 449-459
14. Banditt, M., Koller, T. and Sogo, J.M. (1999) Transcriptional activity and chromatin structure of enhancer-deleted rRNA genes in Saccharomyces cerevisiae. Mol. Cell. Biol., 19, 4953-4960
15. 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
16. Fahy, D., Conconi, A. and Smerdon, M.J. (2005) Rapid changes in transcription and chromatin structure of ribosomal genes in yeast during growth phase transitions. Exp. Cell Res., 305, 365-373
17. Stefanovsky, V., Langlois, F., Gagnon-Kugler, T., Rothblum, L.I. and Moss, T. (2006) Growth factor signaling regulates elongation of RNA polymerase I transcription in mammals via UBF phosphorylation and r-chromatin remodeling. Mol. Cell, 21, 629-639
18. Conconi, A., Paquette, M., Fahy, D., Bespalov, V.A. and Smerdon, M.J. (2005) Repair-independent chromatin assembly onto active ribosomal genes in yeast after UV irradiation. Mol. Cell. Biol., 25, 9773-9783
19. Conconi, A., Bespalov, V.A. and Smerdon, M.J. (2002) Transcription- coupled repair in RNA polymerase I-Transcribed genes of yeast. Proc. Natl Acad. Sci. USA, 99, 649-654
20. Adam, M., Robert, F., Larochelle, M. and Gaudreau, L. (2001) H2A.Z is required for global chromatin integrity and for recruitment of RNA polymerase II under specific conditions. Mol. Cell. Biol., 21, 6270-6279
21. Osheim, Y.N., French, S.L., Sikes, M.L. and Beyer, A.L. (2009) Electron microscope visualization of RNA transcription and processing in Saccharomyces cerevisiae by Miller chromatin spreading. Methods Mol. Biol., 464, 55-69
22. Tremblay, M., Teng, Y., Paquette, M., Waters, R. and Conconi, A. (2008) Complementary roles of yeast Rad4p and Rad34p in nucleotide excision repair of active and inactive rRNA gene chromatin. Mol. Cell. Biol., 28, 7504-7513
23. Woudstra, E.C., Gilbert, C., Fellows, J., Jansen, L., Brouwer, J., Erdjument-Bromage, H., Tempst, P. and Svejstrup, J.Q. (2002) A Rad26-Def1 complex coordinates repair and RNA polII proteolysis in response to DNA damage. Nature, 415, 929-933
24. Bier, M., Fath, S. and Tschochner, H. (2004) The composition of the RNA polymerase I transcription machinery switches from initiation to elongation mode. FEBS Letters, 564, 41-46
25. Keys, D., Vu, L., Steffan, J.S., Dodd, J., Yamamoto, R.T., Nogi, Y. and Nomura, M. (1994) RRN6 and RRN7 encode subunits of a multiprotein complex essential for the initiation of rDNA transcription by RNA polymerase I in Saccharomyces cerevisiae. Genes & Dev., 8, 2349-2362
26. Meier, A. and Thoma, F. (2005) RNA polymerase I transcription factors in active yeast rRNA gene promoters enhance UV damage formation and inhibit repair. Mol. Cell. Biol., 25, 1586-1595
27. Smale, S.T. (2009) Nuclear run-on assay. In: Carey, M., Smale, S. and Peterson, C. (eds), Transcriptional Regulation in Eukaryotes, Concepts, Strategies, and Techniques. Cold Spring Harbor, USA, pp. 63-69
28. Rudolph, C.J., Upton, A.L. and Lloyd, G. (2007) Replication fork stalling and cell cycle arrest in UV-irradiated Escherichia coli. Genes & Dev., 21, 668-681
29. Schmid, M., Durussel, T. and Laemmli, U.K. (2004) ChIC and ChEC: Genomic mapping of chromatin proteins. Mol. Cell, 16, 147-157
30. Lagerwerf, S., Vrouwe, M.G., Overmeer, R.M., Fousteri, M.I. and Mullenders, L.H.F. (2011) DNA damage response and transcription. DNA Repair, 10, 743-750
31. Hara, R., Selby, C.P., Liu, M., Price, D.H. and Sancar, A. (1999) Human transcription release factor 2 dissociates RNA polymerase I and II stalled at a cyclobutane thymine dimer. J. Biol. Chem., 274, 24779-24786
32. Tornaletti, S. (2005) Transcription arrest at DNA damage sites. Mutat. Res., 577, 131-145
33. Jackson, D.A., Iborra, F.J., Manders, E.M.M. and Cook, P.R. (1998) Numbers and organization of RNA polymerases, nascent transcripts, and transcription units in HeLa nuclei. Mol. Biol. Cell, 9, 1523-1536
34. Zhou, Y. and Martin, C.T. (2006) Observed instability of T7 RNA polymerase elongation complexes can be dominated by collisioninduced ''bumping''. J. Biol. Chem., 281, 24441-24448
35. Prakash, S. and Prakash, L. (2000) Nucleotide excision repair in yeast. Mutat. Res., 451, 13-24
36. Lucchini, R. and Sogo, J.M. (1995) Replication of transcriptionally active chromatin. Nature, 374, 276-280
37. Smerdon, M.J. and Conconi, A. (1999) Modulation of DNA damage and DNA repair in chromatin. In: Moldave, K. (ed.), Progress in Nucleic Acid Research and Molecular Biology. Academic Press, San Diego, CA, pp. 227-255
38. Thoma, F. (2005) Repair of UV lesions in nucleosomes-intrinsic properties and remodeling. DNA Repair, 4, 855-869
39. Meier, A., Livingstone-Zatchej, M. and Thoma, F. (2002) Repair of active and silenced rDNA in yeast. J. Biol. Chem., 277, 11845-11852
40. 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
41. Gavin, A-C., Aloy, P., Grandi, P., Krause, R., Boesche, M., Marzioch, M., Rau, C., Jensen, L.J., Bastuck, S., Dümpelfeld, B. et al. (2006) Proteome survey reveals modularity of the yeast cell machinery. Nature, 440, 631-636
42. Philippi, A., Steinbauer, R., Reiter, A., Fath, S., Leger-Silvestre, I., Milkereit, P., Griesenbeck, J. and Tschochner, H. (2010) TORdependent reduction in the expression level of Rrn3p lowers the activity of the yeast RNA PolI machinery, but does not account for the strong inhibition of rRNA production. Nucleic Acids Res., 38, 5315-5326
43. Rubin, D.M., Coux, O., Wefes, I., Hengartner, C., Young, R.A., Goldberg, A.L suppressor Sug1 as a subunit of the yeast 26S proteasome. Nature, 379, 655-657