Elevated Genome-wide instability in yeast mutants lacking RNase H activity

Genetics

Volumn 201, Issue 3, 2015, Pages 963-975

  O’Connell, Karen ^a   Jinks Robertson, Sue ^a   Petes, Thomas D ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Loss of heterozygosity; Microarrays; Mitotic recombination; RNase H1; RNase H2

Indexed keywords

DNA DIRECTED DNA POLYMERASE EPSILON; DNA POLYMERASE; FUNGAL DNA; GENOMIC DNA; RIBONUCLEASE H; RIBONUCLEASE H2; RNA POLYMERASE II; UNCLASSIFIED DRUG; FUNGAL RNA; RIBONUCLEASE; RIBONUCLEASE HI; RNH201 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ALLELE; ARTICLE; CENTROMERE; CHROMOSOME 11; CHROMOSOME 13; CHROMOSOME 4; CHROMOSOME LOSS; DIPLOIDY; DNA DAMAGE; DNA HYBRIDIZATION; DNA SEQUENCE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; FUNGAL STRAIN; FUNGUS MUTANT; GENE CONVERSION; GENE MAPPING; GENOMIC INSTABILITY; GENOTYPE; HETEROZYGOSITY LOSS; MICROARRAY ANALYSIS; MITOTIC RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SINGLE NUCLEOTIDE POLYMORPHISM; SISTER CHROMATID; TELOMERE; WILD TYPE; YEAST; CHROMOSOME; CONFORMATION; DNA REPLICATION; GENETIC RECOMBINATION; GENETICS; METABOLISM; MUTATION;

CHROMOSOMES, FUNGAL; DNA REPLICATION; DNA, FUNGAL; GENOMIC INSTABILITY; LOSS OF HETEROZYGOSITY; MUTATION; NUCLEIC ACID CONFORMATION; RECOMBINATION, GENETIC; RIBONUCLEASE H; RIBONUCLEASES; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84946963032     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.115.182725     Document Type: Article

References (39)

1. Aguilera, A., and T. Garcia-Muse, 2012 R loops: from transcription byproducts to threats to genome stability. Mol. Cell 46: 115-124.
2. Altman, D. G., 1991 Practical Statistics for Medical Research, Chapman and Hall/CRC Press, Boca Raton, FL.
3. Arudchandran, A., S. Cerritelli, S. Narimatsu, M. Itaya, D. Y. Shin et al., 2000 The absence of ribonuclease H1 or H2 alters the sensitivity of Saccharomyces cerevisiae to hydroxyurea, caffeine and ethyl methanesulphonate: implications for roles of RNases H in DNA replication and repair. Genes Cells 5: 789-802.
4. Azvolinsky, A., P. G. Giresi, J. D. Lieb, and V. A. Zakian, 2009 Highly transcribed RNA polymerase II genes are impediments to replication fork progression in Saccharomyces cerevisiae. Mol. Cell 34: 722-734.
5. Cerritelli, S. M., and R. J. Crouch, 2009 Ribonuclease H: the enzymes in eukaryotes. FEBS J. 276: 1494-1505.
6. Chan, Y. A., M. J. Aristizabal, P. Y. Lu, Z. Luo, A. Hamza et al., 2014 Genome-wide profiling of yeast DNA:RNA hybrid prone sites with DRIP-chip. PLoS Genet. 10: e1004288.
7. Clausen, A. R., S. A. Lujan, A. B. Burkholder, C. D. Orebaugh, J. S. Williams et al., 2015 Tracking replication enzymology in vivo by genome-wide mapping of ribonucleotide incorporation. Nat. Struct. Mol. Biol. 22: 185-191.
8. Conover, H., and S. Lujan, M. Chapman, D. Cornelio, R. Sharif et al. 2015 Stimulation of chromosomal rearrangements by ribonucleotides. Genetics 947-957.
9. Crow, Y. J., A. Leitch, B. E. Hayward, A. Garner, R. Parmar et al., 2006 Mutations in genes encoding ribonuclease H2 subunits cause Aicardi-Goutiéres syndrome and mimic congenital viral brain infection. Nat. Genet. 38: 910-916.
10. El Hage, A., S. Webb, A. Kerr, and D. Tollervey, 2014 Genomewide distribution of RNA-DNA hybrids identifies RNase H targets in tRNA genes, retrotransposons and mitochondria. PLoS Genet. 10: e1004716.
11. Errede, B., T. S. Cardillo, F. Sherman, E. Dubois, J. Deschamps et al., 1980 Mating signals control expression of mutations resulting from insertion of a transposable repetitive element adjacent to diverse yeast genes. Cell 22: 427-436.
12. Fachinetti, D., R. Bermejo, A. Cocito, S. Minardi, Y. Katou et al., 2010 Replication termination at eukaryotic chromosomes is mediated by Top2 and occurs at genomic loci containing pausing elements. Mol. Cell 39: 595-605.
13. Günther, C., B. Kind, M. A. Reijns, N. Berndt, M. Martinez-Bueno et al., 2015 Defective removal of ribonucleotides from DNA promotes systemic autoimmunity. J. Clin. Invest. 125: 413-424.
14. Hackett, J. A., and C. W. Greider, 2003 End resection initiates genomic instability in the absence of telomerase. Mol. Cell. Biol. 23: 8450-8461.
15. Hamperl, S., and K. A. Cimprich, 2014 The contribution of cotranscriptional RNA:DNA hybrid structures to DNA damage and genome instability. DNA Repair (Amst.) 19: 84-94.
16. Hochberg, Y., and Y. Benjamini, 1990 More powerful procedures for multiple significance testing. Stat. Med. 9: 811-818.
17. Ii, M., T. Ii, L. I. Mironova, and S. J. Brill, 2011 Epistasis analysis between homologous recombination genes in Saccharomyces cerevisiae identifies multiple repair pathways for Sgs1, Mus81- Mms4 and RNase H2. Mutat. Res. 714: 33-43.
18. Kim, N., S. Y. Huang, J. S. Williams, Y. C. Li, A. B. Clark et al., 2011 Mutagenic processing of ribonucleotides in DNA by yeast topoisomerase I. Science 332: 1561-1564.
19. Koh, K. D., S. Balachander, J. R. Hesselberth, and F. Storici, 2015 Ribose-seq: global mapping of ribonucleotides embedded in genomic DNA. Nat. Methods 12: 251-257.
20. Lazzaro, F., D. Novarina, F. Amara, D. L. Watt, J. E. Stone et al., 2012 RNase H and postreplication repair protect cells from ribonucleotides incorporated in DNA. Mol. Cell 45: 99-110.
21. Lea, D. E., and C. A. Coulson, 1949 The distribution of the numbers of mutants in bacterial populations. J. Genet. 49: 264-285.
22. Lee, P. S., and T. D. Petes, 2010 Mitotic gene conversion events induced in G1-synchronized yeast cells by gamma rays are similar to spontaneous conversion events. Proc. Natl. Acad. Sci. USA 107: 7383-7388.
23. Lim, Y. W., L. A. Sanz, X. Xu, S. R. Hartono, and F. Chédin, 2015 Genome-wide DNA hypomethylation and RNA:DNA hybrid accumulation in Aicardi-Goutières syndrome. eLife 4: doi: 10.7554/eLife.08007.
24. McCulley, J. L., and T. D. Petes, 2010 Chromosome rearrangements and aneuploidy in yeast strains lacking both Tel1p and Mec1p reflect deficiencies in two different mechanisms. Proc. Natl. Acad. Sci. USA 107: 11465-11470.
25. Mischo, H. E., B. Gomez-Gonzalez, P. Grzechnik, A. G. Rondon, W. Wei et al., 2011 Yeast Sen1 helicase protects the genome from transcription-associated instability. Mol. Cell 41: 21-32.
26. Nick McElhinny, S. A., D. Kumar, A. B. Clark, D. L. Watt, B. E. Watts et al., 2010a Genome instability due to ribonucleotide incorporation into DNA. Nat. Chem. Biol. 6: 774-781.
27. Nick McElhinny, S. A., B. E. Watts, D. Kumar, D. L. Watt, E. B. Lundstrom et al., 2010b Abundant ribonucleotide incorporation into DNA by yeast replicative polymerases. Proc. Natl. Acad. Sci. USA 107: 4949-4954.
28. Potenski, C. J., H. Niu, P. Sung, and H. L. Klein, 2014 Avoidance of ribonucleotide-induced mutations by RNase H2 and Srs2- Exo1 mechanisms. Nature 511: 251-254.
29. Prado, F., and A. Aguilera, 2005 Impairment of replication fork progression mediates RNA polII transcription-associated recombination. EMBO J. 24: 1267-1276.
30. Pramila, T., W. Wu, S. Miles, W. S. Noble, and L. L. Breeden, 2006 The Forkhead transcription factor Hcm1 regulates chromosome segregation genes and fills the S-phase gap in the transcriptional circuitry of the cell cycle. Genes Dev. 20: 2266-2278.
31. Reijns, M. A., H. Kemp, J. Ding, S. M. De Proce, A. P. Jackson et al., 2015 Lagging-strand replication shapes the mutational landscape of the genome. Nature 518: 502-506.
32. Song, W., M. Dominska, P. W. Greenwell, and T. D. Petes, 2014 Genome-wide high-resolution mapping of chromosome fragile sites in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 111: E2210-E2218.
33. St Charles, J., and T. D. Petes, 2013 High-resolution mapping of spontaneous mitotic recombination hotspots on the 1.1 Mb arm of yeast chromosome IV. PLoS Genet. 9: e1003434.
34. St Charles, J., E. Hazkani-Covo, Y. Yin, S. L. Andersen, F. S. Dietrich et al., 2012 High-resolution genome-wide analysis of irradiated (UV and gamma-rays) diploid yeast cells reveals a high frequency of genomic loss of heterozygosity (LOH) events. Genetics 190: 1267-1284.
35. Wahba, L., J. D. Amon, D. Koshland, and M. Vuica-Ross, 2011 RNase H and multiple RNA biogenesis factors cooperate to prevent RNA:DNA hybrids from generating genome instability. Mol. Cell 44: 978-988.
36. Williams, J. S., and T. A. Kunkel, 2014 Ribonucleotides in DNA: origins, repair and consequences. DNA Repair (Amst.) 19: 27-37.
37. Williams, J. S., D. J. Smith, L. Marjavaara, S. A. Lujan, A. Chabes et al., 2013 Topoisomerase 1-mediated removal of ribonucleotides from nascent leading-strand DNA. Mol. Cell 49: 1010- 1015.
38. Yin, Y., and T. D. Petes, 2013 Genome-wide high-resolution mapping of UV-induced mitotic recombination events in Saccharomyces cerevisiae. PLoS Genet. 9: e1003894.
39. Yu, T. Y., Y. W. Kao, and J. J. Lin, 2014 Telomeric transcripts stimulate telomere recombination to suppress senescence in cells lacking telomerase. Proc. Natl. Acad. Sci. USA 111: 3377-3382.