The Intertwined Roles of Transcription and Repair Proteins

Molecular Cell

Volumn 52, Issue 3, 2013, Pages 291-302

  Fong, Yick W ^a   Cattoglio, Claudia ^a   Tjian, Robert ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLCYTOSINE; ACTIVATION INDUCED CYTIDINE DEAMINASE; DNA; DNA GLYCOSYLTRANSFERASE; ENDONUCLEASE; ENDONUCLEASE XPF; ENDONUCLEASE XPG; FANCONI ANEMIA GROUP D2 PROTEIN; FANCONI ANEMIA PROTEIN; HELICASE; HORMONE RECEPTOR; MESSENGER RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN; RETINOIC ACID; RETINOIC ACID RECEPTOR BETA; RETINOIC ACID RECEPTOR BETA 2; RNA POLYMERASE II; THYMINE DNA GLYCOSYLASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR IIH; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; XERODERMA PIGMENTOSUM GROUP C PROTEIN;

CELL RENEWAL; CELL SPECIFICITY; CELL TYPE; DNA DAMAGE; DNA END JOINING REPAIR; DNA METHYLATION; DNA REPAIR; DNA SEQUENCE; DOUBLE STRANDED DNA BREAK; EMBRYO DEVELOPMENT; EXCISION REPAIR; FIBROBLAST; GENE ACTIVATION; GENE EXPRESSION; GENE MUTATION; GENE TARGETING; HELA CELL; HUMAN; IN VITRO STUDY; MESSENGER RNA SYNTHESIS; NONHUMAN; NUCLEAR REPROGRAMMING; PROMOTER REGION; PROTEIN FUNCTION; RECOMBINATION REPAIR; REVIEW; SOMATIC CELL; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

EID: 84887151305     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2013.10.018     Document Type: Review

References (112)

1. Aguilera A. The connection between transcription and genomic instability. EMBO J. 2002, 21:195-201.
2. Aguilera A., García-Muse T. R loops: from transcription byproducts to threats to genome stability. Mol. Cell 2012, 46:115-124.
3. Apostolou E., Ferrari F., Walsh R.M., Bar-Nur O., Stadtfeld M., Cheloufi S., Stuart H.T., Polo J.M., Ohsumi T.K., Borowsky M.L., et al. Genome-wide chromatin interactions of the Nanog locus in pluripotency, differentiation, and reprogramming. Cell Stem Cell 2013, 12:699-712.
4. Araki M., Masutani C., Takemura M., Uchida A., Sugasawa K., Kondoh J., Ohkuma Y., Hanaoka F. Centrosome protein centrin 2/caltractin 1 is part of the xeroderma pigmentosum group C complex that initiates global genome nucleotide excision repair. J.Biol. Chem. 2001, 276:18665-18672.
5. Barreto G., Schäfer A., Marhold J., Stach D., Swaminathan S.K., Handa V., Döderlein G., Maltry N., Wu W., Lyko F., Niehrs C. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 2007, 445:671-675.
6. Bochkareva A., Yuzenkova Y., Tadigotla V.R., Zenkin N. Factor-independent transcription pausing caused by recognition of the RNA-DNA hybrid sequence. EMBO J. 2012, 31:630-639.
7. Bradsher J., Auriol J., Proietti de Santis L., Iben S., Vonesch J.L., Grummt I., Egly J.M. CSB is a component of RNA pol I transcription. Mol. Cell 2002, 10:819-829.
8. Burma S., Chen B.P., Murphy M., Kurimasa A., Chen D.J. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J.Biol. Chem. 2001, 276:42462-42467.
9. Camenisch U., Träutlein D., Clement F.C., Fei J., Leitenstorfer A., Ferrando-May E., Naegeli H. Two-stage dynamic DNA quality check by xeroderma pigmentosum group C protein. EMBO J. 2009, 28:2387-2399.
10. Chambers I., Colby D., Robertson M., Nichols J., Lee S., Tweedie S., Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 2003, 113:643-655.
11. Chen D., Lucey M.J., Phoenix F., Lopez-Garcia J., Hart S.M., Losson R., Buluwela L., Coombes R.C., Chambon P., Schär P., Ali S. T:G mismatch-specific thymine-DNA glycosylase potentiates transcription of estrogen-regulated genes through direct interaction with estrogen receptor alpha. J.Biol. Chem. 2003, 278:38586-38592.
12. Chevray P.M., Nathans D. Protein interaction cloning in yeast: identification of mammalian proteins that react with the leucine zipper of Jun. Proc. Natl. Acad. Sci. USA 1992, 89:5789-5793.
13. Ciccia A., Elledge S.J. The DNA damage response: making it safe to play with knives. Mol. Cell 2010, 40:179-204.
14. Citterio E., Van Den Boom V., Schnitzler G., Kanaar R., Bonte E., Kingston R.E., Hoeijmakers J.H., Vermeulen W. ATP-dependent chromatin remodeling by the Cockayne syndrome B DNA repair-transcription-coupling factor. Mol. Cell. Biol. 2000, 20:7643-7653.
15. Compe E., Egly J.M. TFIIH: when transcription met DNA repair. Nat. Rev. Mol. Cell Biol. 2012, 13:343-354.
16. Conticello S.G. The AID/APOBEC family of nucleic acid mutators. Genome Biol. 2008, 9:229.
17. Cortázar D., Kunz C., Saito Y., Steinacher R., Schär P. The enigmatic thymine DNA glycosylase. DNA Repair (Amst.) 2007, 6:489-504.
18. Cortázar D., Kunz C., Selfridge J., Lettieri T., Saito Y., MacDougall E., Wirz A., Schuermann D., Jacobs A.L., Siegrist F., et al. Embryonic lethal phenotype reveals a function of TDG in maintaining epigenetic stability. Nature 2011, 470:419-423.
19. Cortellino S., Xu J., Sannai M., Moore R., Caretti E., Cigliano A., Le Coz M., Devarajan K., Wessels A., Soprano D., et al. Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 2011, 146:67-79.
20. D'Alessio J.A., Wright K.J., Tjian R. Shifting players and paradigms in cell-specific transcription. Mol. Cell 2009, 36:924-931.
21. D'Andrea A.D., Grompe M. Molecular biology of Fanconi anemia: implications for diagnosis and therapy. Blood 1997, 90:1725-1736.
22. Deans A.J., West S.C. DNA interstrand crosslink repair and cancer. Nat. Rev. Cancer 2011, 11:467-480.
23. Diderich K., Alanazi M., Hoeijmakers J.H. Premature aging and cancer in nucleotide excision repair-disorders. DNA Repair (Amst.) 2011, 10:772-780.
24. Etchegaray J.P., Mostoslavsky R. eNERgizing pluripotent gene transcription. Cell Stem Cell 2011, 9:285-286.
25. Fong Y.W., Inouye C., Yamaguchi T., Cattoglio C., Grubisic I., Tjian R. A DNA repair complex functions as an Oct4/Sox2 coactivator in embryonic stem cells. Cell 2011, 147:120-131.
26. Fong Y.W., Cattoglio C., Yamaguchi T., Tjian R. Transcriptional regulation by coactivators in embryonic stem cells. Trends Cell Biol. 2012, 22:292-298.
27. Franchini D.M., Schmitz K.M., Petersen-Mahrt S.K. 5-Methylcytosine DNA demethylation: more than losing a methyl group. Annu. Rev. Genet. 2012, 46:419-441.
28. Francia S., Michelini F., Saxena A., Tang D., de Hoon M., Anelli V., Mione M., Carninci P., d'Adda di Fagagna F. Site-specific DICER and DROSHA RNA products control the DNA-damage response. Nature 2012, 488:231-235.
29. Frederico L.A., Kunkel T.A., Shaw B.R. A sensitive genetic assay for the detection of cytosine deamination: determination of rate constants and the activation energy. Biochemistry 1990, 29:2532-2537.
30. Gan W., Guan Z., Liu J., Gui T., Shen K., Manley J.L., Li X. R-loop-mediated genomic instability is caused by impairment of replication fork progression. Genes Dev. 2011, 25:2041-2056.
31. Gonzalez F., Georgieva D., Vanoli F., Shi Z.D., Stadtfeld M., Ludwig T., Jasin M., Huangfu D. Homologous recombination DNA repair genes play a critical role in reprogramming to a pluripotent state. Cell Rep. 2013, 3:651-660.
32. Goodrich J.A., Tjian R. Unexpected roles for core promoter recognition factors in cell-type-specific transcription and gene regulation. Nat. Rev. 2010, 11:549-558.
33. Hanawalt P.C., Spivak G. Transcription-coupled DNA repair: two decades of progress and surprises. Nat. Rev. Mol. Cell Biol. 2008, 9:958-970.
34. He Y., Fang J., Taatjes D.J., Nogales E. Structural visualization of key steps in human transcription initiation. Nature 2013, 495:481-486.
35. Helmrich A., Ballarino M., Nudler E., Tora L. Transcription-replication encounters, consequences and genomic instability. Nat. Struct. Mol. Biol. 2013, 20:412-418.
36. Hoeijmakers J.H. Genome maintenance mechanisms for preventing cancer. Nature 2001, 411:366-374.
37. Hong H., Takahashi K., Ichisaka T., Aoi T., Kanagawa O., Nakagawa M., Okita K., Yamanaka S. Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 2009, 460:1132-1135.
38. Iacovoni J.S., Caron P., Lassadi I., Nicolas E., Massip L., Trouche D., Legube G. High-resolution profiling of gammaH2AX around DNA double strand breaks in the mammalian genome. EMBO J. 2010, 29:1446-1457.
39. Iben S., Tschochner H., Bier M., Hoogstraten D., Hozák P., Egly J.M., Grummt I. TFIIH plays an essential role in RNA polymerase I transcription. Cell 2002, 109:297-306.
40. Ito S., Kuraoka I., Chymkowitch P., Compe E., Takedachi A., Ishigami C., Coin F., Egly J.M., Tanaka K. XPG stabilizes TFIIH, allowing transactivation of nuclear receptors: implications for Cockayne syndrome in XP-G/CS patients. Mol. Cell 2007, 26:231-243.
41. Iyama T., Wilson D.M. DNA repair mechanisms in dividing and non-dividing cells. DNA Repair (Amst.) 2013, 12:620-636.
42. Jin S.G., Guo C., Pfeifer G.P. GADD45A does not promote DNA demethylation. PLoS Genet. 2008, 4:e1000013.
43. Ju B.G., Lunyak V.V., Perissi V., Garcia-Bassets I., Rose D.W., Glass C.K., Rosenfeld M.G. A topoisomerase IIbeta-mediated dsDNA break required for regulated transcription. Science 2006, 312:1798-1802.
44. Kamileri I., Karakasilioti I., Garinis G.A. Nucleotide excision repair: new tricks with old bricks. Trends Genet. 2012, 28:566-573.
45. Kamileri I., Karakasilioti I., Sideri A., Kosteas T., Tatarakis A., Talianidis I., Garinis G.A. Defective transcription initiation causes postnatal growth failure in a mouse model of nucleotide excision repair (NER) progeria. Proc. Natl. Acad. Sci. USA 2012, 109:2995-3000.
46. Kawamura T., Suzuki J., Wang Y.V., Menendez S., Morera L.B., Raya A., Wahl G.M., Izpisúa Belmonte J.C. Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature 2009, 460:1140-1144.
47. Khobta A., Epe B. Interactions between DNA damage, repair, and transcription. Mutat. Res. 2012, 736:5-14.
48. Kim N., Jinks-Robertson S. Transcription as a source of genome instability. Nat. Rev. 2012, 13:204-214.
49. King I.F., Yandava C.N., Mabb A.M., Hsiao J.S., Huang H.S., Pearson B.L., Calabrese J.M., Starmer J., Parker J.S., Magnuson T., et al. Topoisomerases facilitate transcription of long genes linked to autism. Nature 2013, 501:58-62.
50. Krasikova Y.S., Rechkunova N.I., Maltseva E.A., Pestryakov P.E., Petruseva I.O., Sugasawa K., Chen X., Min J.H., Lavrik O.I. Comparative analysis of interaction of human and yeast DNA damage recognition complexes with damaged DNA in nucleotide excision repair. J.Biol. Chem. 2013, 288:10936-10947.
51. Le May N., Egly J.M., Coin F. True lies: the double life of the nucleotide excision repair factors in transcription and DNA repair. J.Nucleic Acids 2010, 2010. 10.4061/2010/616342.
52. Le May N., Mota-Fernandes D., Vélez-Cruz R., Iltis I., Biard D., Egly J.M. NER factors are recruited to active promoters and facilitate chromatin modification for transcription in the absence of exogenous genotoxic attack. Mol. Cell 2010, 38:54-66.
53. Le May N., Fradin D., Iltis I., Bougnères P., Egly J.M. XPG and XPF endonucleases trigger chromatin looping and DNA demethylation for accurate expression of activated genes. Mol. Cell 2012, 47:622-632.
54. Lemon B., Tjian R. Orchestrated response: a symphony of transcription factors for gene control. Genes Dev. 2000, 14:2551-2569.
55. Levine M., Tjian R. Transcription regulation and animal diversity. Nature 2003, 424:147-151.
56. Li X., Manley J.L. Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability. Cell 2005, 122:365-378.
57. Li X., Manley J.L. Cotranscriptional processes and their influence on genome stability. Genes Dev. 2006, 20:1838-1847.
58. Li H., Collado M., Villasante A., Strati K., Ortega S., Cañamero M., Blasco M.A., Serrano M. The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 2009, 460:1136-1139.
59. Lieber M.R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 2010, 79:181-211.
60. Lin Y., Wilson J.H. Nucleotide excision repair, mismatch repair, and R-loops modulate convergent transcription-induced cell death and repeat instability. PLoS ONE 2012, 7:e46807.
61. Lin C., Yang L., Tanasa B., Hutt K., Ju B.G., Ohgi K., Zhang J., Rose D.W., Fu X.D., Glass C.K., Rosenfeld M.G. Nuclear receptor-induced chromosomal proximity and DNA breaks underlie specific translocations in cancer. Cell 2009, 139:1069-1083.
62. Lindahl T., Barnes D.E. Repair of endogenous DNA damage. Cold Spring Harb. Symp. Quant. Biol. 2000, 65:127-133.
63. 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. Natl. Acad. Sci. USA 2011, 108:698-703.
64. Mandal P.K., Blanpain C., Rossi D.J. DNA damage response in adult stem cells: pathways and consequences. Nat. Rev. Mol. Cell Biol. 2011, 12:198-202.
65. Marión R.M., Strati K., Li H., Murga M., Blanco R., Ortega S., Fernandez-Capetillo O., Serrano M., Blasco M.A. A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 2009, 460:1149-1153.
66. Mellon I., Spivak G., Hanawalt P.C. Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell 1987, 51:241-249.
67. Michel M., Cramer P. Transitions for regulating early transcription. Cell 2013, 153:943-944.
68. Mischo H.E., Gómez-González B., Grzechnik P., Rondón 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.
69. Mitsui K., Tokuzawa Y., Itoh H., Segawa K., Murakami M., Takahashi K., Maruyama M., Maeda M., Yamanaka S. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 2003, 113:631-642.
70. Molina-Estevez F.J., Lozano M.L., Navarro S., Torres Y., Grabundzija I., Ivics Z., Samper E., Bueren J.A., Guenechea G. Impaired cell reprogramming in non-homologous end joining deficient cells. Stem Cells 2013, 31:1726-1730.
71. Montes de Oca R., Andreassen P.R., Margossian S.P., Gregory R.C., Taniguchi T., Wang X., Houghtaling S., Grompe M., D'Andrea A.D. Regulated interaction of the Fanconi anemia protein, FANCD2, with chromatin. Blood 2005, 105:1003-1009.
72. Müller F., Zaucker A., Tora L. Developmental regulation of transcription initiation: more than just changing the actors. Curr. Opin. Genet. Dev. 2010, 20:533-540.
73. Müller L.U., Milsom M.D., Harris C.E., Vyas R., Brumme K.M., Parmar K., Moreau L.A., Schambach A., Park I.H., London W.B., et al. Overcoming reprogramming resistance of Fanconi anemia cells. Blood 2012, 119:5449-5457.
74. Näär A.M., Lemon B.D., Tjian R. Transcriptional coactivator complexes. Annu. Rev. Biochem. 2001, 70:475-501.
75. Nardulli A.M., Shapiro D.J. DNA bending by nuclear receptors. Receptor 1993, 3:247-255.
76. Nudler E. RNA polymerase backtracking in gene regulation and genome instability. Cell 2012, 149:1438-1445.
77. Park E., Kim H., Kim J.M., Primack B., Vidal-Cardenas S., Xu Y., Price B.D., Mills A.A., D'Andrea A.D. FANCD2 activates transcription of TAp63 and suppresses tumorigenesis. Mol. Cell 2013, 50:908-918.
78. Perillo B., Ombra M.N., Bertoni A., Cuozzo C., Sacchetti S., Sasso A., Chiariotti L., Malorni A., Abbondanza C., Avvedimento E.V. DNA oxidation as triggered by H3K9me2 demethylation drives estrogen-induced gene expression. Science 2008, 319:202-206.
79. Phillips-Cremins J.E., Sauria M.E., Sanyal A., Gerasimova T.I., Lajoie B.R., Bell J.S., Ong C.T., Hookway T.A., Guo C., Sun Y., et al. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 2013, 153:1281-1295.
80. Polo J.M., Anderssen E., Walsh R.M., Schwarz B.A., Nefzger C.M., Lim S.M., Borkent M., Apostolou E., Alaei S., Cloutier J., et al. Amolecular roadmap of reprogramming somatic cells into iPS cells. Cell 2012, 151:1617-1632.
81. Rahmouni A.R., Wells R.D. Direct evidence for the effect of transcription on local DNA supercoiling invivo. J.Mol. Biol. 1992, 223:131-144.
82. Reaban M.E., Lebowitz J., Griffin J.A. Transcription induces the formation of a stable RNA.DNA hybrid in the immunoglobulin alpha switch region. J.Biol. Chem. 1994, 269:21850-21857.
83. Robinson C.E., Wu X., Morris D.C., Gimble J.M. DNA bending is induced by binding of the peroxisome proliferator-activated receptor gamma 2 heterodimer to its response element in the murine lipoprotein lipase promoter. Biochem. Biophys. Res. Commun. 1998, 244:671-677.
84. Roeder R.G. Transcriptional regulation and the role of diverse coactivators in animal cells. FEBS Lett. 2005, 579:909-915.
85. Roy R., Chun J., Powell S.N. BRCA1 and BRCA2: different roles in a common pathway of genome protection. Nat. Rev. Cancer 2012, 12:68-78.
86. Sancar A., Lindsey-Boltz L.A., Unsal-Kaçmaz K., Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 2004, 73:39-85.
87. Saxowsky T.T., Doetsch P.W. RNA polymerase encounters with DNA damage: transcription-coupled repair or transcriptional mutagenesis?. Chem. Rev. 2006, 106:474-488.
88. Schaeffer L., Roy R., Humbert S., Moncollin V., Vermeulen W., Hoeijmakers J.H., Chambon P., Egly J.M. DNA repair helicase: a component of BTF2 (TFIIH) basic transcription factor. Science 1993, 260:58-63.
89. Schmitz K.M., Schmitt N., Hoffmann-Rohrer U., Schäfer A., Grummt I., Mayer C. TAF12 recruits Gadd45a and the nucleotide excision repair complex to the promoter of rRNA genes leading to active DNA demethylation. Mol. Cell 2009, 33:344-353.
90. Shen L., Wu H., Diep D., Yamaguchi S., D'Alessio A.C., Fung H.L., Zhang K., Zhang Y. Genome-wide analysis reveals TET- and TDG-dependent 5-methylcytosine oxidation dynamics. Cell 2013, 153:692-706.
91. Shimizu Y., Uchimura Y., Dohmae N., Saitoh H., Hanaoka F., Sugasawa K. Stimulation of DNA glycosylase activities by XPC protein complex: roles of protein-protein interactions. J.Nucleic Acids 2010, 2010. 10.4061/2010/805698.
92. Song C.X., Szulwach K.E., Dai Q., Fu Y., Mao S.Q., Lin L., Street C., Li Y., Poidevin M., Wu H., et al. Genome-wide profiling of 5-formylcytosine reveals its roles in epigenetic priming. Cell 2013, 153:678-691.
93. Sugasawa K., Okamoto T., Shimizu Y., Masutani C., Iwai S., Hanaoka F. A multistep damage recognition mechanism for global genomic nucleotide excision repair. Genes Dev. 2001, 15:507-521.
94. Sugasawa K., Okuda Y., Saijo M., Nishi R., Matsuda N., Chu G., Mori T., Iwai S., Tanaka K., Tanaka K., Hanaoka F. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 2005, 121:387-400.
95. Svejstrup J.Q. Mechanisms of transcription-coupled DNA repair. Nat. Rev. Mol. Cell Biol. 2002, 3:21-29.
96. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
97. 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. Natl. Acad. Sci. USA 2011, 108:692-697.
98. Um S., Harbers M., Benecke A., Pierrat B., Losson R., Chambon P. Retinoic acid receptors interact physically and functionally with the T:G mismatch-specific thymine-DNA glycosylase. J.Biol. Chem. 1998, 273:20728-20736.
99. Utikal J., Polo J.M., Stadtfeld M., Maherali N., Kulalert W., Walsh R.M., Khalil A., Rheinwald J.G., Hochedlinger K. Immortalization eliminates a roadblock during cellular reprogramming into iPS cells. Nature 2009, 460:1145-1148.
100. Venema J., van Hoffen A., Natarajan A.T., van Zeeland A.A., Mullenders L.H. The residual repair capacity of xeroderma pigmentosum complementation group C fibroblasts is highly specific for transcriptionally active DNA. Nucleic Acids Res. 1990, 18:443-448.
101. Vissers J.H., van Lohuizen M., Citterio E. The emerging role of Polycomb repressors in the response to DNA damage. J.Cell Sci. 2012, 125:3939-3948.
102. Wahba L., Gore S.K., Koshland D. The homologous recombination machinery modulates the formation of RNA-DNA hybrids and associated chromosome instability. eLife 2013, 2:e00505.
103. Wang Q.E., Zhu Q., Wani G., El-Mahdy M.A., Li J., Wani A.A. DNA repair factor XPC is modified by SUMO-1 and ubiquitin following UV irradiation. Nucleic Acids Res. 2005, 33:4023-4034.
104. Wei W., Ba Z., Gao M., Wu Y., Ma Y., Amiard S., White C.I., Rendtlew Danielsen J.M., Yang Y.G., Qi Y. A role for small RNAs in DNA double-strand break repair. Cell 2012, 149:101-112.
105. Wei Z., Gao F., Kim S., Yang H., Lyu J., An W., Wang K., Lu W. Klf4 organizes long-range chromosomal interactions with the oct4 locus in reprogramming and pluripotency. Cell Stem Cell 2013, 13:36-47.
106. Wu S.C., Zhang Y. Active DNA demethylation: many roads lead to Rome. Nat. Rev. Mol. Cell Biol. 2010, 11:607-620.
107. Yamamoto K.N., Kobayashi S., Tsuda M., Kurumizaka H., Takata M., Kono K., Jiricny J., Takeda S., Hirota K. Involvement of SLX4 in interstrand cross-link repair is regulated by the Fanconi anemia pathway. Proc. Natl. Acad. Sci. USA 2011, 108:6492-6496.
108. Yokoi M., Masutani C., Maekawa T., Sugasawa K., Ohkuma Y., Hanaoka F. The xeroderma pigmentosum group C protein complex XPC-HR23B plays an important role in the recruitment of transcription factor IIH to damaged DNA. J.Biol. Chem. 2000, 275:9870-9875.
109. Yu K., Chedin F., Hsieh C.L., Wilson T.E., Lieber M.R. R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nat. Immunol. 2003, 4:442-451.
110. Yüce O., West S.C. Senataxin, defective in the neurodegenerative disorder ataxia with oculomotor apraxia 2, lies at the interface of transcription and the DNA damage response. Mol. Cell. Biol. 2013, 33:406-417.
111. Zhang H., Jiao W., Sun L., Fan J., Chen M., Wang H., Xu X., Shen A., Li T., Niu B., et al. Intrachromosomal looping is required for activation of endogenous pluripotency genes during reprogramming. Cell Stem Cell 2013, 13:30-35.
112. Ziller M.J., Gu H., Müller F., Donaghey J., Tsai L.T., Kohlbacher O., DeJager P.L., Rosen E.D., Bennett D.A., Bernstein B.E., et al. Charting a dynamic DNA methylation landscape of the human genome. Nature 2013, 500:477-481.