The Transcription Factor TFII-I Promotes DNA Translesion Synthesis and Genomic Stability

English version České info

DNA translesion synthesis (TLS) allows the DNA replication machinery to replicate past damaged bases, thus increasing cellular tolerance for DNA damage and maintaining genomic stability. Suppression of TLS is expected to enhance the efficacy of the anti-cancer drug, cisplatin. TLS employs a special set of DNA polymerases, including Pol ζ. The TLS polymerases are also involved in somatic hypermutation and proper immune response in mammals. Thus, it is critical to understand the underlying mechanisms of TLS. In this study, we have discovered the transcription factor TFII-I as a new Pol ζ-binding protein in human cells. We show that TFII-I is indeed required for TLS and DNA damage tolerance. We further delineate the mechanism by which TFII-I contributes to TLS. Our study significantly advances the molecular understanding of TLS, and provides a fascinating example of component sharing among disparate nuclear processes. Finally, because one copy of the TFII-I gene is deleted in Williams-Beuren syndrome (WBS), our work implicates TLS deficiency as a potential causal factor of this human genetic disorder.

Vyšlo v časopise: The Transcription Factor TFII-I Promotes DNA Translesion Synthesis and Genomic Stability. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004419
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004419

Souhrn

Zdroje

1. SancarA, Lindsey-BoltzLA, Unsal-KacmazK, LinnS (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73: 39–85.

2. SaleJE, LehmannAR, WoodgateR (2012) Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nat Rev Mol Cell Biol 13: 141–152.

3. ZanH, KomoriA, LiZ, CeruttiA, SchafferA, et al. (2001) The translesion DNA polymerase zeta plays a major role in Ig and bcl-6 somatic hypermutation. Immunity 14: 643–653.

4. ZanH, ShimaN, XuZ, Al-QahtaniA, Evinger IiiAJ, et al. (2005) The translesion DNA polymerase theta plays a dominant role in immunoglobulin gene somatic hypermutation. EMBO J 24: 3757–3769.

5. SaribasakH, MaulRW, CaoZ, YangWW, SchentenD, et al. (2012) DNA polymerase zeta generates tandem mutations in immunoglobulin variable regions. J Exp Med 209: 1075–1081.

6. BerginkS, JentschS (2009) Principles of ubiquitin and SUMO modifications in DNA repair. Nature 458: 461–467.

7. GargP, BurgersPM (2005) Ubiquitinated proliferating cell nuclear antigen activates translesion DNA polymerases eta and REV1. Proc Natl Acad Sci U S A 102: 18361–18366.

8. WoodA, GargP, BurgersPM (2007) A ubiquitin-binding motif in the translesion DNA polymerase Rev1 mediates its essential functional interaction with ubiquitinated proliferating cell nuclear antigen in response to DNA damage. J Biol Chem 282: 20256–20263.

9. MurakumoY, OguraY, IshiiH, NumataS, IchiharaM, et al. (2001) Interactions in the error-prone postreplication repair proteins hREV1, hREV3, and hREV7. J Biol Chem 276: 35644–35651.

10. GuoC, FischhaberPL, Luk-PaszycMJ, MasudaY, ZhouJ, et al. (2003) Mouse Rev1 protein interacts with multiple DNA polymerases involved in translesion DNA synthesis. EMBO J 22: 6621–6630.

11. RossAL, SimpsonLJ, SaleJE (2005) Vertebrate DNA damage tolerance requires the C-terminus but not BRCT or transferase domains of REV1. Nucleic Acids Res 33: 1280–1289.

12. OhashiE, MurakumoY, KanjoN, AkagiJ, MasutaniC, et al. (2004) Interaction of hREV1 with three human Y-family DNA polymerases. Genes Cells 9: 523–531.

13. KosarekJN, WoodruffRV, Rivera-BegemanA, GuoC, D'SouzaS, et al. (2008) Comparative analysis of in vivo interactions between Rev1 protein and other Y-family DNA polymerases in animals and yeasts. DNA Repair (Amst) 7: 439–451.

14. JohnsonRE, WashingtonMT, HaracskaL, PrakashS, PrakashL (2000) Eukaryotic polymerases iota and zeta act sequentially to bypass DNA lesions. Nature 406: 1015–1019.

15. ShacharS, ZivO, AvkinS, AdarS, WittschiebenJ, et al. (2009) Two-polymerase mechanisms dictate error-free and error-prone translesion DNA synthesis in mammals. EMBO J 28: 383–393.

16. LivnehZ, ZivO, ShacharS (2010) Multiple two-polymerase mechanisms in mammalian translesion DNA synthesis. Cell Cycle 9: 729–735.

17. WojtaszekJ, LeeCJ, D'SouzaS, MinesingerB, KimH, et al. (2012) Structural basis of Rev1-mediated assembly of a quaternary vertebrate translesion polymerase complex consisting of Rev1, heterodimeric polymerase (Pol) zeta, and Pol kappa. J Biol Chem 287: 33836–33846.

18. RoyAL, MalikS, MeisterernstM, RoederRG (1993) An alternative pathway for transcription initiation involving TFII-I. Nature 365: 355–359.

19. CheriyathV, RoyAL (2001) Structure-function analysis of TFII-I. Roles of the N-terminal end, basic region, and I-repeats. J Biol Chem 276: 8377–8383.

20. GilljamKM, FeyziE, AasPA, SousaMM, MullerR, et al. (2009) Identification of a novel, widespread, and functionally important PCNA-binding motif. J Cell Biol 186: 645–654.

21. RoyAL (2012) Biochemistry and biology of the inducible multifunctional transcription factor TFII-I: 10 years later. Gene 492: 32–41.

22. PoberBR (2010) Williams-Beuren syndrome. N Engl J Med 362: 239–252.

23. LucenaJ, PezziS, AsoE, ValeroMC, CarreiroC, et al. (2010) Essential role of the N-terminal region of TFII-I in viability and behavior. BMC Med Genet 11: 61.

24. LuoX, YuH (2008) Protein metamorphosis: the two-state behavior of Mad2. Structure 16: 1616–1625.

25. AravindL, KooninEV (1998) The HORMA domain: a common structural denominator in mitotic checkpoints, chromosome synapsis and DNA repair. Trends Biochem Sci 23: 284–286.

26. LuoX, FangG, ColdironM, LinY, YuH, et al. (2000) Structure of the Mad2 spindle assembly checkpoint protein and its interaction with Cdc20. Nat Struct Biol 7: 224–229.

27. LuoX, TangZ, RizoJ, YuH (2002) The Mad2 spindle checkpoint protein undergoes similar major conformational changes upon binding to either Mad1 or Cdc20. Mol Cell 9: 59–71.

28. LuoX, TangZ, XiaG, WassmannK, MatsumotoT, et al. (2004) The Mad2 spindle checkpoint protein has two distinct natively folded states. Nat Struct Mol Biol 11: 338–345.

29. ItohG, KannoS, UchidaKS, ChibaS, SuginoS, et al. (2011) CAMP (C13orf8, ZNF828) is a novel regulator of kinetochore-microtubule attachment. EMBO J 30: 130–144.

30. HaraK, HashimotoH, MurakumoY, KobayashiS, KogameT, et al. (2010) Crystal structure of human REV7 in complex with a human REV3 fragment and structural implication of the interaction between DNA polymerase zeta and REV1. J Biol Chem 285: 12299–12307.

31. KikuchiS, HaraK, ShimizuT, SatoM, HashimotoH (2012) Structural basis of recruitment of DNA polymerase zeta by interaction between REV1 and REV7 proteins. J Biol Chem 287: 33847–33852.

32. CheungHW, ChunAC, WangQ, DengW, HuL, et al. (2006) Inactivation of human MAD2B in nasopharyngeal carcinoma cells leads to chemosensitization to DNA-damaging agents. Cancer Res 66: 4357–4367.

33. McNallyK, NealJA, McManusTP, McCormickJJ, MaherVM (2008) hRev7, putative subunit of hPolzeta, plays a critical role in survival, induction of mutations, and progression through S-phase, of UV((254 nm))-irradiated human fibroblasts. DNA Repair (Amst) 7: 597–604.

34. JansenJG, Tsaalbi-ShtylikA, HendriksG, VerspuyJ, GaliH, et al. (2009) Mammalian polymerase zeta is essential for post-replication repair of UV-induced DNA lesions. DNA Repair (Amst) 8: 1444–1451.

35. SharmaS, HicksJK, ChuteCL, BrennanJR, AhnJY, et al. (2012) REV1 and polymerase zeta facilitate homologous recombination repair. Nucleic Acids Res 40: 682–691.

36. ParrisCN, SeidmanMM (1992) A signature element distinguishes sibling and independent mutations in a shuttle vector plasmid. Gene 117: 1–5.

37. ChimgeNO, MakeyevAV, RuddleFH, BayarsaihanD (2008) Identification of the TFII-I family target genes in the vertebrate genome. Proc Natl Acad Sci U S A 105: 9006–9010.

38. CicciaA, NimonkarAV, HuY, HajduI, AcharYJ, et al. (2012) Polyubiquitinated PCNA recruits the ZRANB3 translocase to maintain genomic integrity after replication stress. Mol Cell 47: 396–409.

39. MakarovaAV, StodolaJL, BurgersPM (2012) A four-subunit DNA polymerase zeta complex containing Pol delta accessory subunits is essential for PCNA-mediated mutagenesis. Nucleic Acids Res 40: 11618–11626.

40. JohnsonRE, PrakashL, PrakashS (2012) Pol31 and Pol32 subunits of yeast DNA polymerase delta are also essential subunits of DNA polymerase zeta. Proc Natl Acad Sci U S A 109: 12455–12460.

41. LeeYS, GregoryMT, YangW (2014) Human Pol zeta purified with accessory subunits is active in translesion DNA synthesis and complements Pol eta in cisplatin bypass. Proc Natl Acad Sci U S A 111: 2954–2959.

42. BruningJB, ShamooY (2004) Structural and thermodynamic analysis of human PCNA with peptides derived from DNA polymerase-delta p66 subunit and flap endonuclease-1. Structure 12: 2209–2219.

43. GuoC, SonodaE, TangTS, ParkerJL, BielenAB, et al. (2006) REV1 protein interacts with PCNA: significance of the REV1 BRCT domain in vitro and in vivo. Mol Cell 23: 265–271.

44. de GrooteFH, JansenJG, MasudaY, ShahDM, KamiyaK, et al. (2011) The Rev1 translesion synthesis polymerase has multiple distinct DNA binding modes. DNA Repair (Amst) 10: 915–925.

45. HoTV, GuainazziA, DerkuntSB, EnoiuM, ScharerOD (2011) Structure-dependent bypass of DNA interstrand crosslinks by translesion synthesis polymerases. Nucleic Acids Res 39: 7455–7464.

46. HaraK, ShimizuT, UnzaiS, AkashiS, SatoM, et al. (2009) Purification, crystallization and initial X-ray diffraction study of human REV7 in complex with a REV3 fragment. Acta Crystallogr Sect F Struct Biol Cryst Commun 65: 1302–1305.

47. HishikiA, ShimizuT, SerizawaA, OhmoriH, SatoM, et al. (2008) Crystallographic study of G178S mutant of human proliferating cell nuclear antigen. Acta Crystallogr Sect F Struct Biol Cryst Commun 64: 819–821.

48. UematsuN, WeteringsE, YanoK, Morotomi-YanoK, JakobB, et al. (2007) Autophosphorylation of DNA-PKCS regulates its dynamics at DNA double-strand breaks. J Cell Biol 177: 219–229.