Insight in the multilevel regulation of NER

Experimental Cell Research

Volumn 329, Issue 1, 2014, Pages 116-123

  Dijk, Madelon ^a   Typas, Dimitris ^a   Mullenders, Leon ^a   Pines, Alex ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

DNA damage response; Global genome nucleotide excision repair; Nucleotide excision repair; Post translational modifications; Transcription coupled nucleotide excision repair

Indexed keywords

CHAPERONE; POLY(ADENOSINE DIPHOSPHATE RIBOSE); RNA POLYMERASE; RNA POLYMERASE II; SCAFFOLD PROTEIN;

AGING; CANCER SUSCEPTIBILITY; CHROMATIN; DNA DAMAGE; DNA HELIX; ENZYME DEGRADATION; EXCISION REPAIR; GENOMIC INSTABILITY; MASS SPECTROMETRY; NERVE DEGENERATION; PREMATURITY; REGULATORY MECHANISM; REVIEW; UBIQUITINATION; ANIMAL; DNA REPAIR; GENETIC TRANSCRIPTION; GENETICS; HUMAN; PROTEIN PROCESSING;

ANIMALS; DNA REPAIR; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; TRANSCRIPTION, GENETIC;

EID: 84919390763     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.08.010     Document Type: Review

References (61)

1. Aamann M.D., Sorensen M.M., Hvitby C., Berquist B.R., Muftuoglu M., Tian J., de Souza-Pinto N.C., Scheibye-Knudsen M., Wilson D.M., Stevnsner T., Bohr V.A. Cockayne syndrome group B protein promotes mitochondrial DNA stability by supporting the DNA repair association with the mitochondrial membrane. FASEB J. 2010, 24:2334-2346.
2. Aboussekhra A., Biggerstaff M., Shivji M.K., Vilpo J.A., Moncollin V., Podust V.N., Protic M., Hubscher U., Egly J.M., Wood R.D. Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell 1995, 80:859-868.
3. Adam S., Polo S.E., Almouzni G. Transcription recovery after DNA damage requires chromatin priming by the H3.3 histone chaperone HIRA. Cell 2013, 155:94-106.
4. Auclair Y., Rouget R., Affar E.B., Drobetsky E.A. ATR kinase is required for global genomic nucleotide excision repair exclusively during S phase in human cells. Proc. Natl. Acad. Sci. USA 2008, 105:17896-17901.
5. Balajee A.S., May A., Dianov G.L., Friedberg E.C., Bohr V.A. Reduced RNA polymerase II transcription in intact and permeabilized Cockayne syndrome group B cells. Proc. Natl. Acad. Sci. USA 1997, 94:4306-4311.
6. Brooks P.J. Blinded by the UV light: how the focus on transcription-coupled NER has distracted from understanding the mechanisms of Cockayne syndrome neurologic disease. DNA Repair (Amst) 2013, 12:656-671.
7. Cleaver J.E. Photosensitivity syndrome brings to light a new transcription-coupled DNA repair cofactor. Nat. Genet. 2012, 44:477-478.
8. DiGiovanna J.J., Kraemer K.H. Shining a light on xeroderma pigmentosum. J. Invest. Dermatol. 2012, 132:785-796.
9. Dinant C., Ampatziadis-Michailidis G., Lans H., Tresini M., Lagarou A., Grosbart M., Theil A.F., van Cappellen W.A., Kimura H., Bartek J., Fousteri M., Houtsmuller A.B., Vermeulen W., Marteijn J.A. Enhanced chromatin dynamics by FACT promotes transcriptional restart after UV-induced DNA damage. Mol. Cell 2013, 51:469-479.
10. Duan M.R., Smerdon M.J. UV damage in DNA promotes nucleosome unwrapping. J. Biol. Chem. 2010, 285:26295-26303.
11. Epshtein V., Kamarthapu V., McGary K., Svetlov V., Ueberheide B., Proshkin S., Mironov A., Nudler E. UvrD facilitates DNA repair by pulling RNA polymerase backwards. Nature 2014, 505:372-377.
12. Fei J., Chen J. KIAA1530 protein is recruited by Cockayne syndrome complementation group protein A (CSA) to participate in transcription-coupled repair (TCR). J. Biol. Chem. 2012, 287:35118-35126.
13. Fei J., Kaczmarek N., Luch A., Glas A., Carell T., Naegeli H. Regulation of nucleotide excision repair by UV-DDB: prioritization of damage recognition to internucleosomal DNA. PLoS. Biol. 2011, 9:e1001183.
14. Fischer E.S., Scrima A., Bohm K., Matsumoto S., Lingaraju G.M., Faty M., Yasuda T., Cavadini S., Wakasugi M., Hanaoka F., Iwai S., Gut H., Sugasawa K., Thoma N.H. The molecular basis of CRL4DDB2/CSA ubiquitin ligase architecture, targeting, and activation. Cell 2011, 147:1024-1039.
15. Fousteri M., Vermeulen W., van Zeeland A.A., Mullenders L.H. Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol. Cell 2006, 23:471-482.
16. Ganesan A., Spivak G., Hanawalt P.C. Transcription-coupled DNA repair in prokaryotes. Prog. Mol. Biol. Transl. Sci. 2012, 110:25-40.
17. Green C.M., Almouzni G. Local action of the chromatin assembly factor CAF-1 at sites of nucleotide excision repair in vivo. EMBO J. 2003, 22:5163-5174.
18. Groisman R., Polanowska J., Kuraoka I., Sawada J., Saijo M., Drapkin R., Kisselev A.F., Tanaka K., Nakatani Y. The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 2003, 113:357-367.
19. Guerrero-Santoro J., Kapetanaki M.G., Hsieh C.L., Gorbachinsky I., Levine A.S., Rapic-Otrin V. The cullin 4B-based UV-damaged DNA-binding protein ligase binds to UV-damaged chromatin and ubiquitinates histone H2A. Cancer Res. 2008, 68:5014-5022.
20. Jagannathan M., Nguyen T., Gallo D., Luthra N., Brown G.W., Saridakis V., Frappier L. A role for USP7 in DNA replication. Mol. Cell Biol. 2014, 34:132-145.
21. Kapetanaki M.G., Guerrero-Santoro J., Bisi D.C., Hsieh C.L., Rapic-Otrin V., Levine A.S. The DDB1-CUL4ADDB2 ubiquitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A at UV-damaged DNA sites. Proc. Natl. Acad. Sci. USA 2006, 103:2588-2593.
22. Lake R.J., Fan H.Y. Structure, function and regulation of CSB: a multi-talented gymnast. Mech. Ageing Dev. 2013, 134:202-211.
23. Lake R.J., Geyko A., Hemashettar G., Zhao Y., Fan H.Y. UV-induced association of the CSB remodeling protein with chromatin requires ATP-dependent relief of N-terminal autorepression. Mol. Cell 2010, 37:235-246.
24. Luijsterburg M.S., Lindh M., Acs K., Vrouwe M.G., Pines A., van A.H., Mullenders L.H., Dantuma N.P. DDB2 promotes chromatin decondensation at UV-induced DNA damage. J. Cell Biol. 2012, 197:267-281.
25. Luijsterburg M.S., von B.G., Gourdin A.M., Politi A.Z., Mone M.J., Warmerdam D.O., Goedhart J., Vermeulen W., van D.R., Hofer T. Stochastic and reversible assembly of a multiprotein DNA repair complex ensures accurate target site recognition and efficient repair. J. Cell Biol. 2010, 189:445-463.
26. Mandemaker I., Vermeulen W., Marteijn J. Role of chromatin remodeling during the transcriptional restart upon DNA damage. Nucleus 2014, 5:203-210.
27. Menoni H., Hoeijmakers J.H., Vermeulen W. Nucleotide excision repair-initiating proteins bind to oxidative DNA lesions in vivo. J. Cell Biol. 2012, 199:1037-1046.
28. Moser J., Volker M., Kool H., Alekseev S., Vrieling H., Yasui A., van Zeeland A.A., Mullenders L.H. The UV-damaged DNA binding protein mediates efficient targeting of the nucleotide excision repair complex to UV-induced photo lesions. DNA Repair (Amst) 2005, 4:571-582.
29. Nakazawa Y., Sasaki K., Mitsutake N., Matsuse M., Shimada M., Nardo T., Takahashi Y., Ohyama K., Ito K., Mishima H., Nomura M., Kinoshita A., Ono S., Takenaka K., Masuyama R., Kudo T., Slor H., Utani A., Tateishi S., Yamashita S., Stefanini M., Lehmann A.R., Yoshiura K., Ogi T. Mutations in UVSSA cause UV-sensitive syndrome and impair RNA polymerase IIo processing in transcription-coupled nucleotide-excision repair. Nat. Genet. 2012, 44:586-592.
30. Ng J.M., Vermeulen W., van der Horst G.T., Bergink S., Sugasawa K., Vrieling H., Hoeijmakers J.H. A novel regulation mechanism of DNA repair by damage-induced and RAD23-dependent stabilization of xeroderma pigmentosum group C protein. Genes Dev. 2003, 17:1630-1645.
31. Nicholson B., Suresh Kumar K.G. The multifaceted roles of USP7: new therapeutic opportunities. Cell Biochem. Biophys. 2011, 60:61-68.
32. Nishi R., Alekseev S., Dinant C., Hoogstraten D., Houtsmuller A.B., Hoeijmakers J.H., Vermeulen W., Hanaoka F., Sugasawa K. UV-DDB-dependent regulation of nucleotide excision repair kinetics in living cells. DNA Repair (Amst) 2009, 8:767-776.
33. Nudler E. RNA polymerase backtracking in gene regulation and genome instability. Cell 2012, 149:1438-1445.
34. Oksenych V., Zhovmer A., Ziani S., Mari P.O., Eberova J., Nardo T., Stefanini M., Giglia-Mari G., Egly J.M., Coin F. Histone methyltransferase DOT1L drives recovery of gene expression after a genotoxic attack. PLoS Genet. 2013, 9:e1003611.
35. Overmeer R.M., Moser J., Volker M., Kool H., Tomkinson A.E., van Zeeland A.A., Mullenders L.H., Fousteri M. Replication protein A safeguards genome integrity by controlling NER incision events. J. Cell Biol. 2011, 192:401-415.
36. Park J.S., Marr M.T., Roberts J.W. E. coli Transcription repair coupling factor (Mfd protein) rescues arrested complexes by promoting forward translocation. Cell 2002, 109:757-767.
37. Pines A., Vrouwe M.G., Marteijn J.A., Typas D., Luijsterburg M.S., Cansoy M., Hensbergen P., Deelder A., de G.A., Matsumoto S., Sugasawa K., Thoma N., Vermeulen W., Vrieling H., Mullenders L. PARP1 promotes nucleotide excision repair through DDB2 stabilization and recruitment of ALC1. J. Cell Biol. 2012, 199:235-249.
38. Polo S.E., Roche D., Almouzni G. New histone incorporation marks sites of UV repair in human cells. Cell 2006, 127:481-493.
39. Poulsen S.L., Hansen R.K., Wagner S.A., van C.L., van Belle G.J., Streicher W., Wikstrom M., Choudhary C., Houtsmuller A.B., Marteijn J.A., Bekker-Jensen S., Mailand N. RNF111/Arkadia is a SUMO-targeted ubiquitin ligase that facilitates the DNA damage response. J. Cell Biol. 2013, 201:797-807.
40. Povlsen L.K., Beli P., Wagner S.A., Poulsen S.L., Sylvestersen K.B., Poulsen J.W., Nielsen M.L., Bekker-Jensen S., Mailand N., Choudhary C. Systems-wide analysis of ubiquitylation dynamics reveals a key role for PAF15 ubiquitylation in DNA-damage bypass. Nat. Cell Biol. 2012, 14:1089-1098.
41. Puumalainen M.R., Lessel D., Ruthemann P., Kaczmarek N., Bachmann K., Ramadan K., Naegeli H. Chromatin retention of DNA damage sensors DDB2 and XPC through loss of p97 segregase causes genotoxicity. Nat. Commun. 2014, 5:3695.
42. Rapic-Otrin V., McLenigan M.P., Bisi D.C., Gonzalez M., Levine A.S. Sequential binding of UV DNA damage binding factor and degradation of the p48 subunit as early events after UV irradiation. Nucleic Acids Res. 2002, 30:2588-2598.
43. Robu M., Shah R.G., Petitclerc N., Brind'Amour J., Kandan-Kulangara F., Shah G.M. Role of poly(ADP-ribose) polymerase-1 in the removal of UV-induced DNA lesions by nucleotide excision repair. Proc. Natl. Acad. Sci. USA 2013, 110:1658-1663.
44. Rockx D.A., Mason R., van H.A., Barton M.C., Citterio E., Bregman D.B., van Zeeland A.A., Vrieling H., Mullenders L.H. UV-induced inhibition of transcription involves repression of transcription initiation and phosphorylation of RNA polymerase II. Proc. Natl. Acad. Sci. USA 2000, 97:10503-10508.
45. Sahoo M., Klumpp S. Backtracking dynamics of RNA polymerase: pausing and error correction. J. Phys. Condens. Matter 2013, 25:374104.
46. Scheibye-Knudsen M., Croteau D.L., Bohr V.A. Mitochondrial deficiency in Cockayne syndrome. Mech. Ageing Dev. 2013, 134:275-283.
47. Schwertman P., Lagarou A., Dekkers D.H., Raams A., van der Hoek A.C., Laffeber C., Hoeijmakers J.H., Demmers J.A., Fousteri M., Vermeulen W., Marteijn J.A. UV-sensitive syndrome protein UVSSA recruits USP7 to regulate transcription-coupled repair. Nat. Genet. 2012, 44:598-602.
48. Schwertman P., Vermeulen W., Marteijn J.A. UVSSA and USP7, a new couple in transcription-coupled DNA repair. Chromosoma 2013, 122:275-284.
49. Selby C.P., Sancar A. Molecular mechanism of transcription-repair coupling. Science 1993, 260:53-58.
50. Sheng Y., Saridakis V., Sarkari F., Duan S., Wu T., Arrowsmith C.H., Frappier L. Molecular recognition of p53 and MDM2 by USP7/HAUSP. Nat. Struct. Mol. Biol. 2006, 13:285-291.
51. Stevnsner T., Muftuoglu M., Aamann M.D., Bohr V.A. The role of Cockayne Syndrome group B (CSB) protein in base excision repair and aging. Mech. Ageing Dev. 2008, 129:441-448.
52. Stevnsner T., Nyaga S., de Souza-Pinto N.C., van der Horst G.T., Gorgels T.G., Hogue B.A., Thorslund T., Bohr V.A. Mitochondrial repair of 8-oxoguanine is deficient in Cockayne syndrome group B. Oncogene 2002, 21:8675-8682.
53. 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.
54. 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.
55. Toledo L.I., Altmeyer M., Rask M.B., Lukas C., Larsen D.H., Povlsen L.K., Bekker-Jensen S., Mailand N., Bartek J., Lukas J. ATR prohibits replication catastrophe by preventing global exhaustion of RPA. Cell 2013, 155:1088-1103.
56. Tsaalbi-Shtylik A., Moser J., Mullenders L.H., Jansen J.G., de W.N. Persistently stalled replication forks inhibit nucleotide excision repair in trans by sequestering Replication protein A. Nucleic Acids Res. 2014, 42:4406-4413.
57. van Gool A.J., Citterio E., Rademakers S., van O.R., Vermeulen W., Constantinou A., Egly J.M., Bootsma D., Hoeijmakers J.H. The Cockayne syndrome B protein, involved in transcription-coupled DNA repair, resides in an RNA polymerase II-containing complex. EMBO J. 1997, 16:5955-5965.
58. van H.A., Balajee A.S., van Zeeland A.A., Mullenders L.H. Nucleotide excision repair and its interplay with transcription. Toxicology 2003, 193:79-90.
59. Wang H., Zhai L., Xu J., Joo H.Y., Jackson S., Erdjument-Bromage H., Tempst P., Xiong Y., Zhang Y. Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol. Cell 2006, 22:383-394.
60. 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.
61. Zhang X., Horibata K., Saijo M., Ishigami C., Ukai A., Kanno S., Tahara H., Neilan E.G., Honma M., Nohmi T., Yasui A., Tanaka K. Mutations in UVSSA cause UV-sensitive syndrome and destabilize ERCC6 in transcription-coupled DNA repair. Nat. Genet. 2012, 44:593-597.