RNase H and postreplication repair protect cells from ribonucleotides incorporated in DNA

Molecular Cell

Volumn 45, Issue 1, 2012, Pages 99-110

  Lazzaro, Federico ^a   Novarina, Daniele ^a   Amara, Flavio ^a   Watt, Danielle L ^b   Stone, Jana E ^b   Costanzo, Vincenzo ^c   Burgers, Peter M ^d   Kunkel, Thomas A ^b   Plevani, Paolo ^a   Muzi Falconi, Marco ^a  

^a UNIVERSITY OF MILAN   (Italy)

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

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DNA; DEOXYRIBONUCLEOTIDE; DNA POLYMERASE ZETA; GENOMIC DNA; RIBONUCLEASE H; RIBONUCLEASE H2; RIBONUCLEOTIDE; UNCLASSIFIED DRUG;

ARTICLE; CELL PROTECTION; CELL STRESS; CELL SURVIVAL; CONTROLLED STUDY; DNA REPAIR; DNA REPLICATION; DNA SYNTHESIS; GENE SWITCHING; NONHUMAN; YEAST CELL;

DNA; DNA REPAIR; DNA REPLICATION; GENOMIC INSTABILITY; PROLIFERATING CELL NUCLEAR ANTIGEN; RIBONUCLEASE H; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRESS, PHYSIOLOGICAL; UBIQUITINATION;

EID: 84855881475     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.12.019     Document Type: Article

References (50)

1. Adams A., Gottschling D.E., Stearns T., Kaiser C.A. Methods in yeast genetics: a Cold Spring Harbor Laboratory course manual 1998, Cold Spring Harbor Laboratory Press, Plainview, NY.
2. 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.
3. Ban C., Ramakrishnan B., Sundaralingam M. A single 2'-hydroxyl group converts B-DNA to A-DNA. Crystal structure of the DNA-RNA chimeric decamer duplex d(CCGGC)r(G)d(CCGG) with a novel intermolecular G-C base-paired quadruplet. J.Mol. Biol. 1994, 236:275-285.
4. Ban C., Ramakrishnan B., Sundaralingam M. Crystal structure of the highly distorted chimeric decamer r(C)d(CGGCGCCG)r(G).spermine complex-spermine binding to phosphate only and minor groove tertiary base-pairing. Nucleic Acids Res. 1994, 22:5466-5476.
5. Burgers P.M., Gerik K.J. Structure and processivity of two forms of Saccharomyces cerevisiae DNA polymerase delta. J.Biol. Chem. 1998, 273:19756-19762.
6. Cerritelli S.M., Crouch R.J. Ribonuclease H: the enzymes in eukaryotes. FEBS J. 2009, 276:1494-1505.
7. Cerritelli S.M., Frolova E.G., Feng C., Grinberg A., Love P.E., Crouch R.J. Failure to produce mitochondrial DNA results in embryonic lethality in Rnaseh1 null mice. Mol. Cell 2003, 11:807-815.
8. Chabes A., Stillman B. Constitutively high dNTP concentration inhibits cell cycle progression and the DNA damage checkpoint in yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 2007, 104:1183-1188.
9. Clark A.B., Lujan S.A., Kissling G.E., Kunkel T.A. Mismatch repair-independent tandem repeat sequence instability resulting ribonucleotide incorporation by DNA polymerase ε. DNA Repair (Amst.) 2011, 10:476-482.
10. Crow Y.J., Rehwinkel J. Aicardi-Goutieres syndrome and related phenotypes: linking nucleic acid metabolism with autoimmunity. Hum. Mol. Genet. 2009, 18(R2):R130-R136.
11. Crow Y.J., Leitch A., Hayward B.E., Garner A., Parmar R., Griffith E., Ali M., Semple C., Aicardi J., Babul-Hirji R., et al. Mutations in genes encoding ribonuclease H2 subunits cause Aicardi-Goutières syndrome and mimic congenital viral brain infection. Nat. Genet. 2006, 38:910-916.
12. Crow Y.J., Hayward B.E., Parmar R., Robins P., Leitch A., Ali M., Black D.N., van Bokhoven H., Brunner H.G., Hamel B.C., et al. Mutations in the gene encoding the 3'-5' DNA exonuclease TREX1 cause Aicardi-Goutières syndrome at the AGS1 locus. Nat. Genet. 2006, 38:917-920.
13. Egli M., Usman N., Rich A. Conformational influence of the ribose2'-hydroxyl group: crystal structures of DNA-RNA chimeric duplexes. Biochemistry 1993, 32:3221-3237.
14. Friedberg E.C., Walker G.C., Siede W. DNA repair and mutagenesis 1995, ASM Press, Washington, DC.
15. Gangavarapu V., Prakash S., Prakash L. Requirement of RAD52 group genes for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 2007, 27:7758-7764.
16. Garg P., Stith C.M., Majka J., Burgers P.M. Proliferating cell nuclear antigen promotes translesion synthesis by DNA polymerase ζ. J.Biol. Chem. 2005, 280:23446-23450.
17. Heller R.C., Marians K.J. Replisome assembly and the direct restart of stalled replication forks. Nat. Rev. Mol. Cell Biol. 2006, 7:932-943.
18. Huertas P., Aguilera A. Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol. Cell 2003, 12:711-721.
19. Ii M., Brill S.J. Roles of SGS1, MUS81, and RAD51 in the repair of lagging-strand replication defects in Saccharomyces cerevisiae. Curr. Genet. 2005, 48:213-225.
20. Jaishree T.N., van der Marel G.A., van Boom J.H., Wang A.H. Structural influence of RNA incorporation in DNA: quantitative nuclear magnetic resonance refinement of d(CG)r(CG)d(CG) and d(CG)r(C)d(TAGCG). Biochemistry 1993, 32:4903-4911.
21. Joyce C.M. Choosing the right sugar: how polymerases select a nucleotide substrate. Proc. Natl. Acad. Sci. USA 1997, 94:1619-1622.
22. 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.
23. Kokoska R.J., McCulloch S.D., Kunkel T.A. The efficiency and specificity of apurinic/apyrimidinic site bypass by human DNA polymerase eta and Sulfolobus solfataricus Dpo4. J.Biol. Chem. 2003, 278:50537-50545.
24. Lawrence C.W. Cellular roles of DNA polymerase zeta and Rev1 protein. DNA Repair (Amst.) 2002, 1:425-435.
25. Lawrence C.W., Hinkle D.C. DNA polymerase zeta and the control of DNA damage induced mutagenesis in eukaryotes. Cancer Surv. 1996, 28:21-31.
26. Lazzaro F., Giannattasio M., Puddu F., Granata M., Pellicioli A., Plevani P., Muzi-Falconi M. Checkpoint mechanisms at the intersection between DNA damage and repair. DNA Repair (Amst.) 2009, 8:1055-1067.
27. Leroy C., Mann C., Marsolier M.C. Silent repair accounts for cell cycle specificity in the signaling of oxidative DNA lesions. EMBO J. 2001, 20:2896-2906.
28. Muzi-Falconi M., Liberi G., Lucca C., Foiani M. Mechanisms controlling the integrity of replicating chromosomes in budding yeast. Cell Cycle 2003, 2:564-567.
29. Negrini S., Gorgoulis V.G., Halazonetis T.D. Genomic instability-an evolving hallmark of cancer. Nat. Rev. Mol. Cell Biol. 2010, 11:220-228.
30. Nelson J.R., Lawrence C.W., Hinkle D.C. Thymine-thymine dimer bypass by yeast DNA polymerase ζ. Science 1996, 272:1646-1649.
31. Nick McElhinny S.A., Ramsden D.A. Polymerase mu is a DNA-directed DNA/RNA polymerase. Mol. Cell. Biol. 2003, 23:2309-2315.
32. Nick McElhinny S.A., Kumar D., Clark A.B., Watt D.L., Watts B.E., Lundström E.B., Johansson E., Chabes A., Kunkel T.A. Genome instability due to ribonucleotide incorporation into DNA. Nat. Chem. Biol. 2010, 6:774-781.
33. Nick McElhinny S.A., Watts B.E., Kumar D., Watt D.L., Lundström 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. USA 2010, 107:4949-4954.
34. Petermann E., Orta M.L., Issaeva N., Schultz N., Helleday T. Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol. Cell 2010, 37:492-502.
35. Popoff S.C., Spira A.I., Johnson A.W., Demple B. Yeast structural gene (APN1) for the major apurinic endonuclease: homology to Escherichia coli endonuclease IV. Proc. Natl. Acad. Sci. USA 1990, 87:4193-4197.
36. Prakash S., Johnson R.E., Prakash L. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 2005, 74:317-353.
37. Pursell Z.F., Isoz I., Lundström E.B., Johansson E., Kunkel T.A. Yeast DNA polymerase epsilon participates in leading-strand DNA replication. Science 2007, 317:127-130.
38. 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., et al. Mutations involved in Aicardi-Goutières syndrome implicate SAMHD1 as regulator of the innate immune response. Nat. Genet. 2009, 41:829-832.
39. 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. USA 2002, 99:16654-16659.
40. Sabbioneda S., Bortolomai I., Giannattasio M., Plevani P., Muzi-Falconi M. Yeast Rev1 is cell cycle regulated, phosphorylated in response to DNA damage and its binding to chromosomes is dependent upon MEC1. DNA Repair (Amst.) 2007, 6:121-127.
41. Sekiguchi J., Shuman S. Site-specific ribonuclease activity of eukaryotic DNA topoisomerase I. Mol. Cell 1997, 1:89-97.
42. Stetson D.B., Ko J.S., Heidmann T., Medzhitov R. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 2008, 134:587-598.
43. Stone J.E., Kissling G.E., Lujan S.A., Rogozin I.B., Stith C.M., Burgers P.M., Kunkel T.A. Low-fidelity DNA synthesis by the L979F mutator derivative of Saccharomyces cerevisiae DNA polymerase zeta. Nucleic Acids Res. 2009, 37:3774-3787.
44. Ulrich H.D. Timing and spacing of ubiquitin-dependent DNA damage bypass. FEBS Lett. 2011, 585:2861-2867.
45. Ulrich H.D., Davies A.A. Invivo detection and characterization of sumoylation targets in Saccharomyces cerevisiae. Methods Mol. Biol. 2009, 497:81-103.
46. Wahl M.C., Sundaralingam M. B-form to A-form conversion by a 3'-terminal ribose: crystal structure of the chimera d(CCACTAGTG)r(G). Nucleic Acids Res. 2000, 28:4356-4363.
47. 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.
48. Yang Y.G., Lindahl T., Barnes D.E. Trex1 exonuclease degrades ssDNA to prevent chronic checkpoint activation and autoimmune disease. Cell 2007, 131:873-886.
49. Zhong X., Garg P., Stith C.M., Nick McElhinny S.A., Kissling G.E., Burgers P.M.J., Kunkel T.A. The fidelity of DNA synthesis by yeast DNA polymerase zeta alone and with accessory proteins. Nucleic Acids Res. 2006, 34:4731-4742.
50. Zhu H., Shuman S. Bacterial nonhomologous end joining ligases preferentially seal breaks with a 3'-OH monoribonucleotide. J.Biol. Chem. 2008, 283:8331-8339.