USF-1 Is Critical for Maintaining Genome Integrity in Response to UV-Induced DNA Photolesions

English version České info

An important function of all organisms is to ensure that their genetic material remains intact and unaltered through generations. This is an extremely challenging task since the cell's DNA is constantly under assault by endogenous and environmental agents. To protect against this, cells have evolved effective mechanisms to recognize DNA damage, signal its presence, and mediate its repair. While these responses are expected to be highly regulated because they are critical to avoid human diseases, very little is known about the regulation of the expression of genes involved in mediating their effects. The Nucleotide Excision Repair (NER) is the major DNA–repair process involved in the recognition and removal of UV-mediated DNA damage. Here we use a combination of in vitro and in vivo assays with an intermittent UV-irradiation protocol to investigate the regulation of key players in the DNA–damage recognition step of NER sub-pathways (TCR and GGR). We show an up-regulation in gene expression of CSA and HR23A, which are involved in TCR and GGR, respectively. Importantly, we show that this occurs through a p53 independent mechanism and that it is coordinated by the stress-responsive transcription factor USF-1. Furthermore, using a mouse model we show that the loss of USF-1 compromises DNA repair, which suggests that USF-1 plays an important role in maintaining genomic stability.

Vyšlo v časopise: USF-1 Is Critical for Maintaining Genome Integrity in Response to UV-Induced DNA Photolesions. PLoS Genet 8(1): e32767. doi:10.1371/journal.pgen.1002470
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002470

Souhrn

Zdroje

1. Le MayNMota-FernandesDVelez-CruzRIltisIBiardD 2010 NER factors are recruited to active promoters and facilitate chromatin modification for transcription in the absence of exogenous genotoxic attack. Mol Cell 38 54 66

2. NouspikelT 2009 DNA repair in mammalian cells: Nucleotide excision repair: variations on versatility. Cell Mol Life Sci 66 994 1009

3. SarasinAStaryA 2007 New insights for understanding the transcription-coupled repair pathway. DNA Repair (Amst) 6 265 269

4. SugasawaK 2010 Regulation of damage recognition in mammalian global genomic nucleotide excision repair. Mutat Res 685 29 37

5. TornalettiS 2009 DNA repair in mammalian cells: Transcription-coupled DNA repair: directing your effort where it's most needed. Cell Mol Life Sci 66 1010 1020

6. VolkerMMoneMJKarmakarPvan HoffenASchulW 2001 Sequential assembly of the nucleotide excision repair factors in vivo. Mol Cell 8 213 224

7. LaineJPEglyJM 2006 When transcription and repair meet: a complex system. Trends Genet 22 430 436

8. SugasawaKNgJMMasutaniCIwaiSvan der SpekPJ 1998 Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol Cell 2 223 232

9. YokoiMMasutaniCMaekawaTSugasawaKOhkumaY 2000 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 275 9870 9875

10. KusumotoRMasutaniCSugasawaKIwaiSArakiM 2001 Diversity of the damage recognition step in the global genomic nucleotide excision repair in vitro. Mutat Res 485 219 227

11. Al-SarrajADayRMThielG 2005 Specificity of transcriptional regulation by the zinc finger transcription factors Sp1, Sp3, and Egr-1. J Cell Biochem 94 153 167

12. CorreSPrimotASviderskayaEBennettDCVaulontS 2004 UV-induced expression of key component of the tanning process, the POMC and MC1R genes, is dependent on the p-38-activated upstream stimulating factor-1 (USF-1). J Biol Chem 279 51226 51233

13. ValletVSCasadoMHenrionAABucchiniDRaymondjeanM 1998 Differential roles of upstream stimulatory factors 1 and 2 in the transcriptional response of liver genes to glucose. J Biol Chem 273 20175 20179

14. PerdizDGrofPMezzinaMNikaidoOMoustacchiE 2000 Distribution and repair of bipyrimidine photoproducts in solar UV-irradiated mammalian cells. Possible role of Dewar photoproducts in solar mutagenesis. J Biol Chem 275 26732 26742

15. PfeiferGPYouYHBesaratiniaA 2005 Mutations induced by ultraviolet light. Mutat Res 571 19 31

16. LehmanTAModaliRBoukampPStanekJBennettWP 1993 p53 mutations in human immortalized epithelial cell lines. Carcinogenesis 14 833 839

17. LootsGGOvcharenkoI 2004 rVISTA 2.0: evolutionary analysis of transcription factor binding sites. Nucleic Acids Res 32 W217 221

18. SandelinAWassermanWWLenhardB 2004 ConSite: web-based prediction of regulatory elements using cross-species comparison. Nucleic Acids Res 32 W249 252

19. CorreSGalibertMD 2005 Upstream stimulating factors: highly versatile stress-responsive transcription factors. Pigment Cell Res 18 337 348

20. CorreSPrimotABaronYLe SeyecJGodingC 2009 Target gene specificity of USF-1 is directed via p38-mediated phosphorylation-dependent acetylation. J Biol Chem 284 18851 18862

21. GalibertMDCarreiraSGodingCR 2001 The Usf-1 transcription factor is a novel target for the stress-responsive p38 kinase and mediates UV-induced Tyrosinase expression. Embo J 20 5022 5031

22. HollanderMCAlamoIJackmanJWangMGMcBrideOW 1993 Analysis of the mammalian gadd45 gene and its response to DNA damage. J Biol Chem 268 24385 24393

23. MouchetNAdamskiHBouvetRCorreSCourbebaisseY 2010 In vivo identification of solar radiation-responsive gene network: role of the p38 stress-dependent kinase. PLoS ONE 5 e10776 doi:10.1371/journal.pone.0010776

24. FousteriMMullendersLH 2008 Transcription-coupled nucleotide excision repair in mammalian cells: molecular mechanisms and biological effects. Cell Res 18 73 84

25. FousteriMVermeulenWvan ZeelandAAMullendersLH 2006 Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol Cell 23 471 482

26. van GoolAJCitterioERademakersSvan OsRVermeulenW 1997 The Cockayne syndrome B protein, involved in transcription-coupled DNA repair, resides in an RNA polymerase II-containing complex. Embo J 16 5955 5965

27. van HoffenANatarajanATMayneLVvan ZeelandAAMullendersLH 1993 Deficient repair of the transcribed strand of active genes in Cockayne's syndrome cells. Nucleic Acids Res 21 5890 5895

28. HoeijmakersJH 2009 DNA damage, aging, and cancer. N Engl J Med 361 1475 1485

29. AndressooJOHoeijmakersJH 2005 Transcription-coupled repair and premature ageing. Mutat Res 577 179 194

30. LiLLuXPetersonCLegerskiR 1997 XPC interacts with both HHR23B and HHR23A in vivo. Mutat Res 383 197 203

31. SugasawaKNgJMMasutaniCMaekawaTUchidaA 1997 Two human homologs of Rad23 are functionally interchangeable in complex formation and stimulation of XPC repair activity. Mol Cell Biol 17 6924 6931

32. OkudaYNishiRNgJMVermeulenWvan der HorstGT 2004 Relative levels of the two mammalian Rad23 homologs determine composition and stability of the xeroderma pigmentosum group C protein complex. DNA Repair (Amst) 3 1285 1295

33. HsiehHCHsiehYHHuangYHShenFCTsaiHN 2005 HHR23A, a human homolog of Saccharomyces cerevisiae Rad23, regulates xeroderma pigmentosum C protein and is required for nucleotide excision repair. Biochem Biophys Res Commun 335 181 187

34. NgJMVermeulenWvan der HorstGTBerginkSSugasawaK 2003 A novel regulation mechanism of DNA repair by damage-induced and RAD23-dependent stabilization of xeroderma pigmentosum group C protein. Genes Dev 17 1630 1645

35. MaduraKPrakashS 1990 Transcript levels of the Saccharomyes cerevisiae DNA repair gene RAD23 increase in response to UV light and in meiosis but remain constant in the mitotic cell cycle. Nucleic Acids Res 18 4737 4742

36. ReismanDRotterV 1993 The helix-loop-helix containing transcription factor USF binds to and transactivates the promoter of the p53 tumor suppressor gene. Nucleic Acids Res 21 345 350

37. TanTChuG 2002 p53 Binds and activates the xeroderma pigmentosum DDB2 gene in humans but not mice. Mol Cell Biol 22 3247 3254

38. IsmailPMLuTSawadogoM 1999 Loss of USF transcriptional activity in breast cancer cell lines. Oncogene 18 5582 5591

39. LandaIRuiz-LlorenteSMontero-CondeCInglada-PerezLSchiaviF 2009 The variant rs1867277 in FOXE1 gene confers thyroid cancer susceptibility through the recruitment of USF1/USF2 transcription factors. PLoS Genet 5 e1000637 doi:10.1371/journal.pgen.1000637

40. MajumderSGhoshalKLiZBoYJacobST 1999 Silencing of metallothionein-I gene in mouse lymphosarcoma cells by methylation. Oncogene 18 6287 6295

41. GalibertMDBaronY 2010 Identification of specific Protein/E-box-containing DNA complexes: lessons from the ubiquitously expressed USF transcription factors of the b-HLH-LZ super family. Methods in Molecular Biology 647

42. GalibertMDMiyagoeYMeoT 1993 E-box activator of the C4 promoter is related to but distinct from the transcription factor upstream stimulating factor. J Immunol 151 6099 6109

43. MetivierRGallaisRTiffocheCLe PeronCJurkowskaRZ 2008 Cyclical DNA methylation of a transcriptionally active promoter. Nature 452 45 50