Transcriptional responses to loss of RNase H2 in Saccharomyces cerevisiae

DNA Repair

Volumn 11, Issue 12, 2012, Pages 933-941

  Arana, Mercedes E ^a   Kerns, Robnet T ^a,b   Wharey, Laura ^a   Gerrish, Kevin E ^a   Bushel, Pierre R ^a   Kunkel, Thomas A ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

Genome instability; R loops; Ribonucleotides; RNase H2; Stress response

Indexed keywords

DNA; DOUBLE STRANDED RNA; NUCLEIC ACID; RIBONUCLEASE; RIBONUCLEASE H2; RIBOSOME RNA; RNA; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; AUTOIMMUNE DISEASE; BIOGENESIS; DNA REPLICATION; ENZYME ACTIVE SITE; ENZYME SUBUNIT; GENE DELETION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENOME; GENOMIC INSTABILITY; HUMAN; IMMUNE RESPONSE; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; RNA TRANSCRIPTION; RNA VIRUS; SACCHAROMYCES CEREVISIAE; YEAST;

BASE COMPOSITION; CATALYTIC DOMAIN; DNA REPAIR; DNA REPLICATION; DNA, FUNGAL; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; GENE REGULATORY NETWORKS; GENES, RRNA; GENOMIC INSTABILITY; RIBONUCLEASES; RIBOSOMES; RNA, FUNGAL; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRESS, PHYSIOLOGICAL; TELOMERE; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC;

DSRNA VIRUSES; SACCHAROMYCES CEREVISIAE;

EID: 84869173630     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2012.09.006     Document Type: Article

References (62)

1. Stein H., Hausen P. Enzyme from calf thymus degrading the RNA moiety of DNA-RNA hybrids: effect on DNA-dependent RNA polymerase. Science 1969, 166:393-395.
2. Cerritelli S.M., Crouch R.J. Ribonuclease H: the enzymes in eukaryotes. FASEB J. 2009, 276:1494-1505.
3. Jeong H.S., Backlund P.S., Chen H.C., Karavanov A.A., Crouch R.J. RNase H2 of Saccharomyces cerevisiae is a complex of three proteins. Nucleic Acids Res. 2004, 32:407-414.
4. Eder P.S., Walder R.Y., Walder J.A. Substrate specificity of human RNase H1 and its role in excision repair of ribose residues misincorporated in DNA. Biochimie 1993, 75:123-126.
5. Frank P., Braunshofer-Reiter C., Wintersberger U., Grimm R., Busen W. Cloning of the cDNA encoding the large subunit of human RNase HI, a homologue of the prokaryotic RNase HII,. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:12872-12877.
6. Chon H., Vassilev A., DePamphilis M.L., Zhao Y., Zhang J., Burgers P.M., Crouch R.J., Cerritelli S.M. Contributions of the two accessory subunits, RNASEH2B and RNASEH2C, to the activity and properties of the human RNase H2 complex,. Nucleic Acids Res. 2009, 37:96-110.
7. Drolet M., Phoenix P., Menzel R., Masse E., Liu L.F., Crouch R.J. Overexpression of RNase H partially complements the growth defect of an Escherichia coli delta topA mutant: R-loop formation is a major problem in the absence of DNA topoisomerase I. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:3526-3530.
8. Huertas P., Aguilera A. Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol. Cell 2003, 12:711-721.
9. Li X., Manley J.L. Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability. Cell 2005, 122:365-378.
10. Drolet M. Growth inhibition mediated by excess negative supercoiling: the interplay between transcription elongation, R-loop formation and DNA topology. Mol. Microbiol. 2006, 59:723-730.
11. Forstemann K., Lingner J. Telomerase limits the extent of base pairing between template RNA and telomeric DNA. EMBO Rep. 2005, 6:361-366.
12. Azzalin C.M., Reichenbach P., Khoriauli L., Giulotto E., Lingner J. Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 2007, 318:798-801.
13. Luke B., Panza A., Redon S., Iglesias N., Li Z., Lingner J. The Rat1p 5' to 3' exonuclease degrades telomeric repeat-containing RNA and promotes telomere elongation in Saccharomyces cerevisiae. Mol. Cell 2008, 32:465-477.
14. Qiu J., Qian Y., Frank P., Wintersberger U., Shen B. Saccharomyces cerevisiae RNase H(35) functions in RNA primer removal during lagging-strand DNA synthesis, most efficiently in cooperation with Rad27 nuclease. Mol. Cell. Biol. 1999, 19:8361-8371.
15. Ayyagari R., Gomes X.V., Gordenin D.A., Burgers P.M. Okazaki fragment maturation in yeast. I. Distribution of functions between FEN1 AND DNA2. J. Biol. Chem. 2003, 278:1618-1625.
16. Jin Y.H., Ayyagari R., Resnick M.A., Gordenin D.A., Burgers P.M. Okazaki fragment maturation in yeast. II. Cooperation between the polymerase and 3'-5'-exonuclease activities of Pol delta in the creation of a ligatable nick. J. Biol. Chem. 2003, 278:1626-1633.
17. Balakrishnan L., Bambara R.A. Eukaryotic lagging strand DNA replication employs a multi-pathway mechanism that protects genome integrity. J. Biol. Chem. 2011, 286:6865-6870.
18. Eder P.S., Walder J.A. Ribonuclease H from K562 human erythroleukemia cells. Purification, characterization, and substrate specificity. J. Biol. Chem. 1991, 266:6472-6479.
19. Ide H., Yagi R., Yamaoka T., Kimura Y. Misincorporation of ribonucleotides by DNA polymerase during in vitro DNA replication. Nucleic Acids Symp. Ser. 1993, 133-134.
20. Rydberg B., Game J. Excision of misincorporated ribonucleotides in DNA by RNase H (type 2) and FEN-1 in cell-free extracts. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:16654-16659.
21. Nick McElhinny S.A., Kumar D., Clark A.B., Watt D.L., Watts B.E., Lundstrom E.B., Johansson E., Chabes A., Kunkel T.A. Genome instability due to ribonucleotide incorporation into DNA. Nat. Chem. Biol. 2010, 6:774-781.
22. Rychlik M.P., Chon H., Cerritelli S.M., Klimek P., Crouch R.J., Nowotny M. Crystal structures of RNase H2 in complex with nucleic acid reveal the mechanism of RNA-DNA junction recognition and cleavage. Mol. Cell 2010, 40:658-670.
23. Kim N., Huang S.N., Williams J.S., Li Y.C., Clark A.B., Cho J.E., Kunkel T.A., Pommier Y., Jinks-Robertson S. Mutagenic processing of ribonucleotides in DNA by yeast topoisomerase I. Science 2011, 332:1561-1564.
24. Lazzaro F., Novarina D., Amara F., Watt D.L., Stone J.E., Costanzo V., Burgers P.M., Kunkel T.A., Plevani P., Muzi-Falconi M. RNase H and postreplication repair protect cells from ribonucleotides incorporated in DNA. Mol. Cell 2012, 45:99-110.
25. Clark A.B., Kunkel T.A. The importance of being DNA. Cell Cycle 2010, 9:4422-4424.
26. Poveda A.M., Le Clech M., Pasero P. Transcription and replication: breaking the rules of the road causes genomic instability. Transcription 2010, 1:99-102.
27. Figiel M., Chon H., Cerritelli S.M., Cybulska M., Crouch R.J., Nowotny M. The structural and biochemical characterization of human RNase H2 complex reveals the molecular basis for substrate recognition and Aicardi-Goutières syndrome defects. J. Biol. Chem. 2011, 286:10540-10550.
28. Goutières F. Aicardi-Goutières syndrome. Brain Dev. 2005, 27:201-206.
29. Crow Y.J., Leitch A., Hayward B.E., Garner A., Parmar R., Griffith E., Ali M., Semple C., Aicardi J., Babul-Hirji R., Baumann C., Baxter P., Bertini E., Chandler K.E., Chitayat D., Cau D., Dery C., Fazzi E., Goizet C., King M.D., Klepper J., Lacombe D., Lanzi G., Lyall H., Martinez-Frias M.L., Mathieu M., McKeown C., Monier A., Oade Y., Quarrell O.W., Rittey C.D., Rogers R.C., Sanchis A., Stephenson J.B., Tacke U., Till M., Tolmie J.L., Tomlin P., Voit T., Weschke B., Woods C.G., Lebon P., Bonthron D.T., Ponting C.P., Jackson A.P. Mutations in genes encoding ribonuclease H2 subunits cause Aicardi-Goutières syndrome and mimic congenital viral brain infection. Nat. Genet. 2006, 38:910-916.
30. Rohman M.S., Koga Y., Takano K., Chon H., Crouch R.J., Kanaya S. Effect of the disease-causing mutations identified in human ribonuclease (RNase) H2 on the activities and stabilities of yeast RNase H2 and archaeal RNase HII. FASEB J. 2008, 275:4836-4849.
31. Reijns M.A., Bubeck D., Gibson L.C., Graham S.C., Baillie G.S., Jones E.Y., Jackson A.P. The structure of the human RNase H2 complex defines key interaction interfaces relevant to enzyme function and human disease. J. Biol. Chem. 2011, 286:10530-10539.
32. Goutières F., Aicardi J., Barth P.G., Lebon P. Aicardi-Goutières syndrome: an update and results of interferon-alpha studies. Ann. Neurol. 1998, 44:900-907.
33. Rigby R.E., Leitch A., Jackson A.P. Nucleic acid-mediated inflammatory diseases. Bioessays 2008, 30:833-842.
34. Rice G.I., Bond J., Asipu A., Brunette R.L., Manfield I.W., Carr I.M., Fuller J.C., Jackson R.M., Lamb T., Briggs T.A., Ali M., Gornall H., Couthard L.R., Aeby A., Attard-Montalto S.P., Bertini E., Bodemer C., Brockmann K., Brueton L.A., Corry P.C., Desguerre I., Fazzi E., Cazorla A.G., Gener B., Hamel B.C., Heiberg A., Hunter M., van der Knaap M.S., Kumar R., Lagae L., Landrieu P.G., Lourenco C.M., Marom D., McDermott M.F., van der Merwe W., Orcesi S., Prendiville J.S., Rasmussen M., Shalev S.A., Soler D.M., Shinawi M., Spiegel R., Tan T.Y., Vanderver A., Wakeling E.L., Wassmer E., Whittaker E., Lebon P., Stetson D.B., Bonthron D.T., Crow Y.J. Mutations involved in Aicardi-Goutières syndrome implicate SAMHD1 as regulator of the innate immune response. Nat. Genet. 2009, 41:829-832.
35. Benjamini Y., Drai D., Elmer G., Kafkafi N., Golani I. Controlling the false discovery rate in behavior genetics research. Behav. Brain Res. 2001, 125:279-284.
36. Dennis G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., Lempicki R.A. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol. 2003, 4:P3.
37. Huang D.W., Sherman B.T., Lempicki R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 2009, 4:44-57.
38. SGD project. (November, 2010). http://downloads.yeastgenome.org/.
39. Cherry J.M., Hong E.L., Amundsen C., Balakrishnan R., Binkley G., Chan E.T., Christie K.R., Costanzo M.C., Dwight S.S., Engel S.R., Fisk D.G., Hirschman J.E., Hitz B.C., Karra K., Krieger C.J., Miyasato S.R., Nash R.S., Park J., Skrzypek M.S., Simison M., Weng S., Wong E.D. Saccharomyces Genome Database: the genomics resource of budding yeast. Nucleic Acids Res. 2012, 40:D700-D705.
40. Nagalakshmi U., Wang Z., Waern K., Shou C., Raha D., Gerstein M., Snyder M. The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 2008, 320:1344-1349.
41. Lee I., Li Z., Marcotte E.M. An improved, bias-reduced probabilistic functional gene network of baker's yeast, Saccharomyces cerevisiae. PLoS ONE 2007, 2:e988.
42. Shannon P., Markiel A., Ozier O., Baliga N.S., Wang J.T., Ramage D., Amin N., Schwikowski B., Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13:2498-2504.
43. Rusyn I., Fry R.C., Begley T.J., Klapacz J., Svensson J.P., Ambrose M., Samson L.D. Transcriptional networks in S. cerevisiae linked to an accumulation of base excision repair intermediates. PLoS ONE 2007, 2:e1252.
44. Tous C., Aguilera A. Impairment of transcription elongation by R-loops in vitro. Biochem. Biophys. Res. Commun. 2007, 360:428-432.
45. El Hage A., French S.L., Beyer A.L., Tollervey D. Loss of Topoisomerase I leads to R-loop-mediated transcriptional blocks during ribosomal RNA synthesis. Genes Dev. 2010, 24:1546-1558.
46. Lin Y., Dent S.Y., Wilson J.H., Wells R.D., Napierala M. R loops stimulate genetic instability of CTG.CAG repeats. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:692-697.
47. McIvor E.I., Polak U., Napierala M. New insights into repeat instability: role of RNA×DNA hybrids. RNA Biol. 2010, 7:551-558.
48. Lee I., Date S.V., Adai A.T., Marcotte E.M. A probabilistic functional network of yeast genes. Science 2004, 306:1555-1558.
49. Nick McElhinny S.A., Watts B.E., Kumar D., Watt D.L., Lundstrom E.B., Burgers P.M., Johansson E., Chabes A., Kunkel T.A. Abundant ribonucleotide incorporation into DNA by yeast replicative polymerases. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:4949-4954.
50. Watt D.L., Johansson E., Burgers P.M., Kunkel T.A. Replication of ribonucleotide-containing DNA templates by yeast replicative polymerases. DNA Repair (Amst.) 2011, 10:897-902.
51. De Falco M., Ferrari E., De Felice M., Rossi M., Hubscher U., Pisani F.M. The human GINS complex binds to and specifically stimulates human DNA polymerase alpha-primase. EMBO Rep. 2007, 8:99-103.
52. Clark A.B., Lujan S.A., Kissling G.E., Kunkel T.A. Mismatch repair-independent tandem repeat sequence instability resulting from ribonucleotide incorporation by DNA polymerase epsilon. DNA Repair (Amst.) 2011, 10:476-482.
53. Sekiguchi J., Shuman S. Site-specific ribonuclease activity of eukaryotic DNA topoisomerase I. Mol. Cell 1997, 1:89-97.
54. Nick McElhinny S.A., Kissling G.E., Kunkel T.A. Differential correction of lagging-strand replication errors made by DNA polymerases {alpha} and {delta}. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:21070-21075.
55. Vengrova S., Dalgaard J.Z. The wild-type Schizosaccharomyces pombe mat1 imprint consists of two ribonucleotides. EMBO Rep. 2006, 7:59-65.
56. Chan C.T., Dyavaiah M., DeMott M.S., Taghizadeh K., Dedon P.C., Begley T.J. A quantitative systems approach reveals dynamic control of tRNA modifications during cellular stress. PLoS Genet. 2010, 6:e1001247.
57. Mischo H.E., Gomez-Gonzalez B., Grzechnik P., Rondon A.G., Wei W., Steinmetz L., Aguilera A., Proudfoot N.J. Yeast Sen1 helicase protects the genome from transcription-associated instability. Mol. Cell 2011, 41:21-32.
58. Luke B., Lingner J. TERRA: telomeric repeat-containing RNA. EMBO J. 2009, 28:2503-2510.
59. Reddy K., Tam M., Bowater R.P., Barber M., Tomlinson M., Nichol Edamura K., Wang Y.H., Pearson C.E. Determinants of R-loop formation at convergent bidirectionally transcribed trinucleotide repeats. Nucleic Acids Res. 2011, 39:1749-1762.
60. Wongsurawat T., Jenjaroenpun P., Kwoh C.K., Kuznetsov V. Quantitative model of R-loop forming structures reveals a novel level of RNA-DNA interactome complexity. Nucleic Acids Res. 2012, 40:e16.
61. Coffin S.R., Hollis T., Perrino F.W. Functional consequences of the RNase H2A subunit mutations that cause Aicardi-Goutières syndrome. J. Biol. Chem. 2011, 286:16984-16991.
62. Crow Y.J., Rehwinkel J. Aicardi-Goutières syndrome and related phenotypes: linking nucleic acid metabolism with autoimmunity. Hum. Mol. Genet. 2009, 18:R130-R136.