Ribonucleotides in DNA: Origins, repair and consequences

DNA Repair

Volumn 19, Issue , 2014, Pages 27-37

  Williams, Jessica S ^a   Kunkel, Thomas A ^a  

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

Author keywords

DNA polymerase; DNA repair; DNA replication; Genome instability; Ribonucleotides

Indexed keywords

APRATAXIN; DNA; DNA POLYMERASE; DNA PRIMASE; DNA TOPOISOMERASE; GENOMIC DNA; PROTEIN; RIBONUCLEOTIDE; RNA; UNCLASSIFIED DRUG; RIBONUCLEASE H;

AICARDI GOUTIERES SYNDROME; APRAXIA; ARTICLE; ATAXIA; BACTERIUM; BIOLOGICAL ACTIVITY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA RNA HYBRIDIZATION; DNA SYNTHESIS; EXCISION REPAIR; GENE; GENOMIC INSTABILITY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; MATING TYPE; MATURATION; MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RIBONUCLEOTIDE EXCISION REPAIR; RNA REPAIR; SCHIZOSACCHAROMYCES POMBE; SICKLE CELL ANEMIA; STRESS; BACTERIA; GENETICS; METABOLISM; SACCHAROMYCES CEREVISIAE;

BACTERIA; DNA; DNA REPAIR; DNA REPLICATION; GENOMIC INSTABILITY; HUMANS; RIBONUCLEASE H; RIBONUCLEOTIDES; RNA; SACCHAROMYCES CEREVISIAE;

EID: 84902074659     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2014.03.029     Document Type: Article

References (105)

1. Crick F. Central dogma of molecular biology. Nature 1970, 227:561-563.
2. Cech T.R. The RNA worlds in context. Cold Spring Harbor Perspect. Biol. 2012, 4:a006742.
3. Li Y., Breaker R.R. Kinetics of RNA degradation by specific base catalysis of transesterification involving the 2'-hydroxyl group. J. Am. Chem. Soc. 1999, 121:5326-5372.
4. Egli M., Usman N., Rich A. Conformational influence of the ribose 2'-hydroxyl group: crystal structures of DNA-RNA chimeric duplexes. Biochemistry 1993, 32:3221-3237.
5. 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.
6. 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(CCGG) with a novel intermolecular G-center-dot-C base-paired quadruplet. J. Mol. Biol. 1994, 236:275-285.
7. DeRose E.F., Perera L., Murray M.S., Kunkel T.A., London R.E. Solution structure of the Dickerson DNA dodecamer containing a single ribonucleotide. Biochemistry 2012, 51:2407-2416.
8. Bessman M.J., Kornberg A., Lehman I.R., Simms E.S. Enzymic synthesis of deoxyribonucleic acid. Biochim. Biophys. Acta 1956, 21:197-198.
9. Kuchta R.D., Stengel G. Mechanism and evolution of DNA primases. Biochim. Biophys. Acta 2010, 1804:1180-1189.
10. Burgers P.M. Polymerase dynamics at the eukaryotic DNA replication fork. J. Biol. Chem. 2009, 284:4041-4045.
11. Zheng L., Shen B. Okazaki fragment maturation: nucleases take centre stage. J. Mol. Cell Biol. 2011, 3:23-30.
12. Balakrishnan L., Bambara R.A. Okazaki fragment metabolism. Cold Spring Harbor Perspect. Biol. 2013, 5:a010173.
13. Yeeles J.T., Poli J., Marians K.J., Pasero P. Rescuing stalled or damaged replication forks. Cold Spring Harbor Perspect. Biol. 2013, 5:a012815.
14. Pomerantz R.T., O'Donnell M. The replisome uses mRNA as a primer after colliding with RNA polymerase. Nature 2008, 456:762-766.
15. Wan L., Lou J., Xia Y., Su B., Liu T., Cui J., Sun Y., Lou H., Huang J. hPrimpol1/CCDC111 is a human DNA primase-polymerase required for the maintenance of genome integrity. EMBO Rep. 2013, 14:1104-1112.
16. Garcia-Gomez S., Reyes A., Martinez-Jimenez M.I., Chocron E.S., Mouron S., Terrados G., Powell C., Salido E., Mendez J., Holt I.J., Blanco L. PrimPol, an archaic primase/polymerase operating in human cells. Mol. Cell 2013, 52:541-553.
17. Bianchi J., Rudd S.G., Jozwiakowski S.K., Bailey L.J., Soura V., Taylor E., Stevanovic I., Green A.J., Stracker T.H., Lindsay H.D., Doherty A.J. PrimPol bypasses UV photoproducts during eukaryotic chromosomal DNA replication. Mol. Cell 2013, 52:566-573.
18. Mouron S., Rodriguez-Acebes S., Martinez-Jimenez M.I., Garcia-Gomez S., Chocron S., Blanco L., Mendez J. Repriming of DNA synthesis at stalled replication forks by human PrimPol. Nat. Struct. Mol. Biol. 2013, 20:1383-1389.
19. Gao G., Orlova M., Georgiadis M.M., Hendrickson W.A., Goff S.P. Conferring RNA polymerase activity to a DNA polymerase: a single residue in reverse transcriptase controls substrate selection. Proc. Nat. Acad. Sci. U.S.A. 1997, 94:407-411.
20. Joyce C.M. Choosing the right sugar: how polymerases select a nucleotide substrate. Proc. Nat. Acad. Sci. U.S.A. 1997, 94:1619-1622.
21. Shinkai A., Patel P.H., Loeb L.A. The conserved active site motif A of Escherichia coli DNA polymerase I is highly mutable. J. Biol. Chem. 2001, 276:18836-18842.
22. Gosavi R.A., Moon A.F., Kunkel T.A., Pedersen L.C., Bebenek K. The catalytic cycle for ribonucleotide incorporation by human DNA Pol lambda. Nucleic Acids Res. 2012, 40:7518-7527.
23. Brown J.A., Suo Z. Unlocking the sugar "steric gate" of DNA polymerases. Biochemistry 2011, 50:1135-1142.
24. Cavanaugh N.A., Beard W.A., Batra V.K., Perera L., Pedersen L.G., Wilson S.H. Molecular insights into DNA polymerase deterrents for ribonucleotide insertion. J. Biol. Chem. 2011, 286:31650-31660.
25. Kasiviswanathan R., Copeland W.C. Ribonucleotide discrimination and reverse transcription by the human mitochondrial DNA polymerase. J. Biol. Chem. 2011, 286:31490-31500.
26. Wang W., Wu E.Y., Hellinga H.W., Beese L.S. Structural factors that determine selectivity of a high fidelity DNA polymerase for deoxy-, dideoxy-, and ribonucleotides. J. Biol. Chem. 2012, 287:28215-28226.
27. Kunkel T.A. Evolving views of DNA replication (in)fidelity. Cold Spring Harbor Symp. Quant. Biol. 2009, 74:91-101.
28. DeLucia A.M., Grindley N.D., Joyce C.M. An error-prone family Y DNA polymerase (DinB homolog from Sulfolobus solfataricus) uses a 'steric gate' residue for discrimination against ribonucleotides. Nucleic Acids Res. 2003, 31:4129-4137.
29. Moon A.F., Garcia-Diaz M., Batra V.K., Beard W.A., Bebenek K., Kunkel T.A., Wilson S.H., Pedersen L.C. The X family portrait: structural insights into biological functions of X family polymerases. DNA Repair (Amst.) 2007, 6:1709-1725.
30. Kumar D., Viberg J., Nilsson A.K., Chabes A. Highly mutagenic and severely imbalanced dNTP pools can escape detection by the S-phase checkpoint. Nucleic Acids Res. 2010, 38:3975-3983.
31. Nick McElhinny S.A., Watts B., Kumar D., Watt D.L., Lundström E.-B., Burgers P.M.J., Johansson E., Chabes A., Kunkel T.A. Abundant ribonucleotide incorporation into DNA by yeast replicative polymerases. Proc. Nat. Acad. Sci. U.S.A. 2010, 107:4949-4954.
32. Traut T.W. Physiological concentrations of purines and pyrimidines. Mol. Cell. Biochem. 1994, 140:1-22.
33. Ferraro P., Franzolin E., Pontarin G., Reichard P., Bianchi V. Quantitation of cellular deoxynucleoside triphosphates. Nucleic Acids Res. 2010, 38:e85.
34. Nick McElhinny S.A., Ramsden D.A. Polymerase mu is a DNA-directed DNA/RNA polymerase. Mol. Cell. Biol. 2003, 23:2309-2315.
35. Kunkel T.A., Burgers P.M. Dividing the workload at a eukaryotic replication fork. Trends Cell Biol. 2008, 18:521-527.
36. Clausen A.R., Zhang S., Burgers P.M., Lee M.Y., Kunkel T.A. Ribonucleotide incorporation, proofreading and bypass by human DNA polymerase delta. DNA Repair (Amst.) 2013, 12:121-127.
37. Goksenin A.Y., Zahurancik W., LeCompte K.G., Taggart D.J., Suo Z., Pursell Z.F. Human DNA polymerase epsilon is able to efficiently extend from multiple consecutive ribonucleotides. J. Biol. Chem. 2012, 287:42675-42684.
38. Yao N.Y., Schroeder J.W., Yurieva O., Simmons L.A., O'Donnell M.E. Cost of rNTP/dNTP pool imbalance at the replication fork. Proc. Nat. Acad. Sci. U.S.A. 2013, 110:12942-12947.
39. Chabes A., Georgieva B., Domkin V., Zhao X., Rothstein R., Thelander L. Survival of DNA damage in yeast directly depends on increased dNTP levels allowed by relaxed feedback inhibition of ribonucleotide reductase. Cell 2003, 112:391-401.
40. Hakansson P., Hofer A., Thelander L. Regulation of mammalian ribonucleotide reduction and dNTP pools after DNA damage and in resting cells. J. Biol. Chem. 2006, 281:7834-7841.
41. Collins K., Greider C.W. Utilization of ribonucleotides and RNA primers by Tetrahymena telomerase. EMBO J. 1995, 14:5422-5432.
42. Boule J.B., Rougeon F., Papanicolaou C. Terminal deoxynucleotidyl transferase indiscriminately incorporates ribonucleotides and deoxyribonucleotides. J. Biol. Chem. 2001, 276:31388-31393.
43. Vaisman A., Kuban W., McDonald J.P., Karata K., Yang W., Goodman M.F., Woodgate R. Critical amino acids in Escherichia coli UmuC responsible for sugar discrimination and base-substitution fidelity. Nucleic Acids Res. 2012, 40:6144-6157.
44. 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.
45. Rydberg B., Game J. Excision of misincorporated ribonucleotides in DNA by RNase H (type 2) and FEN-1 in cell-free extracts. Proc. Nat. Acad. Sci. U.S.A. 2002, 99:16654-16659.
46. Cerritelli S.M., Crouch R.J. Ribonuclease H: the enzymes in eukaryotes. FEBS J. 2009, 276:1494-1505.
47. 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.
48. Miyabe I., Kunkel T.A., Carr A.M. The major roles of DNA polymerases epsilon and delta at the eukaryotic replication fork are evolutionarily conserved. PLoS Genet. 2011, 7:e1002407.
49. Lujan S.A., Williams J.S., Clausen A.R., Clark A.B., Kunkel T.A. Ribonucleotides are signals for mismatch repair of leading-strand replication errors. Mol. Cell 2013, 50:437-443.
50. Grossman L.I., Watson R., Vinograd J. The presence of ribonucleotides in mature closed-circular mitochondrial DNA. Proc. Nat. Acad. Sci. U.S.A. 1973, 70:3339-3343.
51. Reijns M.A., Rabe B., Rigby R.E., Mill P., Astell K.R., Lettice L.A., Boyle S., Leitch A., Keighren M., Kilanowski F., Devenney P.S., Sexton D., Grimes G., Holt I.J., Hill R.E., Taylor M.S., Lawson K.A., Dorin J.R., Jackson A.P. Enzymatic removal of ribonucleotides from DNA is essential for mammalian genome integrity and development. Cell 2012, 149:1008-1022.
52. Kunkel T.A. The high cost of living. American Association for Cancer Research Special Conference: endogenous sources of mutations, Fort Myers, Florida, USA, 11-15 November, 1998. Trends Genet. 1999, 15:93-94.
53. 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.
54. Garg P., Stith C.M., Sabouri N., Johansson E., Burgers P.M. Idling by DNA polymerase delta maintains a ligatable nick during lagging-strand DNA replication. Genes Dev. 2004, 18:2764-2773.
55. Williams J.S., Clausen A.R., Nick McElhinny S.A., Watts B.E., Johansson E., Kunkel T.A. Proofreading of ribonucleotides inserted into DNA by yeast DNA polymerase epsilon. DNA Repair (Amst.) 2012, 11:649-656.
56. Sparks J.L., Chon H., Cerritelli S.M., Kunkel T.A., Johansson E., Crouch R.J., Burgers P.M. RNase H2-initiated ribonucleotide excision repair. Mol. Cell 2012, 47:980-986.
57. Tumbale P., Williams J.S., Schellenberg M.J., Kunkel T.A., Williams R.S. Aprataxin resolves adenylated RNA-DNA junctions to maintain genome integrity. Nature 2014, 506:111-115.
58. Sekiguchi J., Shuman S. Site-specific ribonuclease activity of eukaryotic DNA topoisomerase I. Mol. Cell 1997, 1:89-97.
59. 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.
60. Williams J.S., Smith D.J., Marjavaara L., Lujan S.A., Chabes A., Kunkel T.A. Topoisomerase 1-mediated removal of ribonucleotides from nascent leading-strand DNA. Mol. Cell 2013, 49:1010-1015.
61. Vos S.M., Tretter E.M., Schmidt B.H., Berger J.M. All tangled up: how cells direct, manage and exploit topoisomerase function. Nat. Rev. Mol. Cell Biol. 2011, 12:827-841.
62. Phatnani H.P., Jones J.C., Greenleaf A.L. Expanding the functional repertoire of CTD kinase I and RNA polymerase II: novel phosphoCTD-associating proteins in the yeast proteome. Biochemistry 2004, 43:15702-15719.
63. Aguilera A., Garcia-Muse T. R loops: from transcription byproducts to threats to genome stability. Mol. Cell 2012, 46:115-124.
64. Aguilera A., Klein H.L. Genetic control of intrachromosomal recombination in Saccharomyces cerevisiae. I. Isolation and genetic characterization of hyper-recombination mutations. Genetics 1988, 119:779-790.
65. Arana M.E., Kerns R.T., Wharey L., Gerrish K.E., Bushel P.R., Kunkel T.A. Transcriptional responses to loss of RNase H2 in Saccharomyces cerevisiae. DNA Repair (Amst.) 2012, 11:933-941.
66. 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.
67. Kim N., Cho J.E., Li Y.C., Jinks-Robertson S. RNA:DNA hybrids initiate quasi-palindrome-associated mutations in highly transcribed yeast DNA. PLoS Genet. 2013, 9:e1003924.
68. Vaisman A., McDonald J.P., Huston D., Kuban W., Liu L., Van Houten B., Woodgate R. Removal of misincorporated ribonucleotides from prokaryotic genomes: an unexpected role for nucleotide excision repair. PLoS Genet. 2013, 9:e1003878.
69. McDonald J.P., Vaisman A., Kuban W., Goodman M.F., Woodgate R. Mechanisms employed by Escherichia coli to prevent ribonucleotide incorporation into genomic DNA by Pol V. PLoS Genet. 2012, 8:e1003030.
70. Vaisman A., McDonald J.P., Noll S., Huston D., Loeb G., Goodman M.F., Woodgate R. Investigating the mechanisms of ribonucleotide excision repair in Escherichia coli. Mutat. Res. 2014, 761:21-33.
71. Caldecott K.W. Molecular biology. Ribose-an internal threat to DNA. Science 2014, 343:260-261.
72. Hiller B., Achleitner M., Glage S., Naumann R., Behrendt R., Roers A. Mammalian RNase H2 removes ribonucleotides from DNA to maintain genome integrity. J. Exp. Med. 2012, 209:1419-1426.
73. Clausen A.R., Murray M.S., Passer A.R., Pedersen L.C., Kunkel T.A. Structure-function analysis of ribonucleotide bypass by B family DNA replicases. Proc. Nat. Acad. Sci. U.S.A. 2013, 110:16802-16807.
74. Storici F., Bebenek K., Kunkel T.A., Gordenin D.A., Resnick M.A. RNA-templated DNA repair. Nature 2007, 447:338-341.
75. 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.
76. 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.
77. Bermejo R., Lai M.S., Foiani M. Preventing replication stress to maintain genome stability: resolving conflicts between replication and transcription. Mol. Cell 2012, 45:710-718.
78. Stetson D.B., Ko J.S., Heidmann T., Medzhitov R. Trex1 prevents cell-intrinsic initiation of autoimmunity. Cell 2008, 134:587-598.
79. Balk B., Maicher A., Dees M., Klermund J., Luke-Glaser S., Bender K., Luke B. Telomeric RNA-DNA hybrids affect telomere-length dynamics and senescence. Nat. Struct. Mol. Biol. 2013, 20:1199-1205.
80. Askree S.H., Yehuda T., Smolikov S., Gurevich R., Hawk J., Coker C., Krauskopf A., Kupiec M., McEachern M.J. A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length. Proc. Nat. Acad. Sci. U.S.A. 2004, 101:8658-8663.
81. Huertas P., Aguilera A. Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol. Cell 2003, 12:711-721.
82. Chon H., Sparks J.L., Rychlik M., Nowotny M., Burgers P.M., Crouch R.J., Cerritelli S.M. RNase H2 roles in genome integrity revealed by unlinking its activities. Nucleic Acids Res. 2013, 41:3130-3143.
83. Cho J.E., Kim N., Li Y.C., Jinks-Robertson S. Two distinct mechanisms of Topoisomerase 1-dependent mutagenesis in yeast. DNA Repair (Amst.) 2013, 12:205-211.
84. Lippert M.J., Kim N., Cho J.E., Larson R.P., Schoenly N.E., O'Shea S.H., Jinks-Robertson S. Role for topoisomerase 1 in transcription-associated mutagenesis in yeast. Proc. Nat. Acad. Sci. U.S.A. 2011, 108:698-703.
85. Takahashi T., Burguiere-Slezak G., Van der Kemp P.A., Boiteux S. Topoisomerase 1 provokes the formation of short deletions in repeated sequences upon high transcription in Saccharomyces cerevisiae. Proc. Nat. Acad. Sci. U.S.A. 2011, 108:692-697.
86. 2 interaction network functions to suppress genome instability. Mol. Cell Biol. 2014, 34:1521-1534.
87. 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-Goutieres syndrome and mimic congenital viral brain infection. Nat. Genet. 2006, 38:910-916.
88. Iyama T., Wilson D.M. DNA repair mechanisms in dividing and non-dividing cells. DNA Repair (Amst.) 2013, 12:620-636.
89. Brawley O.W., Cornelius L.J., Edwards L.R., Gamble V.N., Green B.L., Inturrisi C., James A.H., Laraque D., Mendez M., Montoya C.J., Pollock B.H., Robinson L., Scholnik A.P., Schori M. National Institutes of Health Consensus Development Conference statement: hydroxyurea treatment for sickle cell disease. Ann. Intern. Med. 2008, 148:932-938.
90. Sayrac S., Vengrova S., Godfrey E.L., Dalgaard J.Z. Identification of a novel type of spacer element required for imprinting in fission yeast. PLoS Genet. 2011, 7:e1001328.
91. Dalgaard J.Z. Causes and consequences of ribonucleotide incorporation into nuclear DNA. Trends Genet. 2012, 28:592-597.
92. Nick McElhinny S.A., Kissling G.E., Kunkel T.A. Differential correction of lagging-strand replication errors made by DNA polymerases α and δ. Proc. Nat. Acad. Sci. U.S.A. 2010, 107:21070-21075.
93. Ghodgaonkar M.M., Lazzaro F., Olivera-Pimentel M., Artola-Boran M., Cejka P., Reijns M.A., Jackson A.P., Plevani P., Muzi-Falconi M., Jiricny J. Ribonucleotides misincorporated into DNA act as strand-discrimination signals in eukaryotic mismatch repair. Mol. Cell 2013, 50:323-332.
94. Nandakumar J., Podell E.R., Cech T.R. How telomeric protein POT1 avoids RNA to achieve specificity for single-stranded DNA. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:651-656.
95. 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.
96. Dunn K., Griffith J.D. The presence of RNA in a double helix inhibits its interaction with histone protein. Nucleic Acids Res. 1980, 8:555-566.
97. Hovatter K.R., Martinson H.G. Ribonucleotide-induced helical alteration in DNA prevents nucleosome formation. Proc. Nat. Acad. Sci. U.S.A. 1987, 84:1162-1166.
98. Pursell Z.F., Kunkel T.A. DNA polymerase epsilon: a polymerase of unusual size (and complexity). Prog. Nucleic Acid Res. Mol. Biol. 2008, 82:101-145.
99. Singh G., Klar A.J. Mutations in deoxyribonucleotide biosynthesis pathway cause spreading of silencing across heterochromatic barriers at the mating-type region of the fission yeast. Yeast 2008, 25:117-128.
100. Kupfer P.A., Leumann C.J. The chemical stability of abasic RNA compared to abasic DNA. Nucleic Acids Res. 2007, 35:58-68.
101. Bartlett E.J., Brissett N.C., Doherty A.J. Ribonucleolytic resection is required for repair of strand displaced nonhomologous end-joining intermediates. Proc. Nat. Acad. Sci. U.S.A. 2013, 110:E1984-E1991.
102. Vengrova S., Dalgaard J.Z. The wild-type Schizosaccharomyces pombe mat1 imprint consists of two ribonucleotides. EMBO Rep. 2006, 7:59-65.
103. Phizicky E.M., Schwartz R.C., Abelson J. Saccharomyces cerevisiae tRNA ligase. Purification of the protein and isolation of the structural gene. J. Biol. Chem. 1986, 261:2978-2986.
104. Vengrova S., Dalgaard J.Z. RNase-sensitive DNA modification(s) initiates S. pombe mating-type switching. Genes Dev. 2004, 18:794-804.
105. 32P-postlabeling. Mutat. Res. 1992, 275:355-366.