Dynamic Partnership between TFIIH, PGC-1α and SIRT1 Is Impaired in Trichothiodystrophy

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In eukaryotes, the expression of genes encoding proteins requires the action of hundreds of factors, together with the RNA polymerase II. While these factors are timely and selectively required for the expression of a given gene, little is known about their partnership upon gene expression. Our results reveal a cooperation between different types of transcription factors, namely the general transcription factor TFIIH, the cofactor PGC-1α and the deacetylase SIRT1. Such partnership is however impaired when TFIIH is mutated, as observed in Trichothiodystrophy patients that develop premature ageing. These results thus shed light on the coordinated action of factors during transcription and allow us to better understand molecular deficiencies observed in many human diseases.

Vyšlo v časopise: Dynamic Partnership between TFIIH, PGC-1α and SIRT1 Is Impaired in Trichothiodystrophy. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004732
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004732

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Zdroje

1. BrivanlouAH, DarnellJEJr (2002) Signal transduction and the control of gene expression. Science 295 : 813–818.

2. ThomasMC, ChiangCM (2006) The general transcription machinery and general cofactors. Crit Rev Biochem Mol Biol 41 : 105–178.

3. JitrapakdeeS (2012) Transcription factors and coactivators controlling nutrient and hormonal regulation of hepatic gluconeogenesis. Int J Biochem Cell Biol 44 : 33–45.

4. MayrB, MontminyM (2001) Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol 2 : 599–609.

5. KooSH, FlechnerL, QiL, ZhangX, ScreatonRA, et al. (2005) The CREB coactivator TORC2 is a key regulator of fasting glucose metabolism. Nature 437 : 1109–1111.

6. ParkEA, RoeslerWJ, LiuJ, KlemmDJ, GurneyAL, et al. (1990) The role of the CCAAT/enhancer-binding protein in the transcriptional regulation of the gene for phosphoenolpyruvate carboxykinase (GTP). Mol Cell Biol 10 : 6264–6272.

7. SchmollD, WalkerKS, AlessiDR, GremplerR, BurchellA, et al. (2000) Regulation of glucose-6-phosphatase gene expression by protein kinase Balpha and the forkhead transcription factor FKHR. Evidence for insulin response unit-dependent and -independent effects of insulin on promoter activity. J Biol Chem 275 : 36324–36333.

8. HallRK, YamasakiT, KuceraT, Waltner-LawM, O'BrienR, et al. (2000) Regulation of phosphoenolpyruvate carboxykinase and insulin-like growth factor-binding protein-1 gene expression by insulin. The role of winged helix/forkhead proteins. J Biol Chem 275 : 30169–30175.

9. RheeJ, InoueY, YoonJC, PuigserverP, FanM, et al. (2003) Regulation of hepatic fasting response by PPARgamma coactivator-1alpha (PGC-1): requirement for hepatocyte nuclear factor 4alpha in gluconeogenesis. Proc Natl Acad Sci U S A 100 : 4012–4017.

10. ImaiE, StromstedtPE, QuinnPG, Carlstedt-DukeJ, GustafssonJA, et al. (1990) Characterization of a complex glucocorticoid response unit in the phosphoenolpyruvate carboxykinase gene. Mol Cell Biol 10 : 4712–4719.

11. SchoneveldOJ, GaemersIC, LamersWH (2004) Mechanisms of glucocorticoid signalling. Biochim Biophys Acta 1680 : 114–128.

12. YuberoP, HondaresE, CarmonaMC, RossellM, GonzalezFJ, et al. (2004) The developmental regulation of peroxisome proliferator-activated receptor-gamma coactivator-1alpha expression in the liver is partially dissociated from the control of gluconeogenesis and lipid catabolism. Endocrinology 145 : 4268–4277.

13. HerzogB, HallRK, WangXL, Waltner-LawM, GrannerDK (2004) Peroxisome proliferator-activated receptor gamma coactivator-1alpha, as a transcription amplifier, is not essential for basal and hormone-induced phosphoenolpyruvate carboxykinase gene expression. Mol Endocrinol 18 : 807–819.

14. YoonJC, PuigserverP, ChenG, DonovanJ, WuZ, et al. (2001) Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature 413 : 131–138.

15. RodgersJT, LerinC, HaasW, GygiSP, SpiegelmanBM, et al. (2005) Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434 : 113–118.

16. NemotoS, FergussonMM, FinkelT (2005) SIRT1 functionally interacts with the metabolic regulator and transcriptional coactivator PGC-1{alpha}. J Biol Chem 280 : 16456–16460.

17. CompeE, EglyJM (2012) TFIIH: when transcription met DNA repair. Nat Rev Mol Cell Biol 13 : 343–354.

18. CoinF, MarinoniJC, RodolfoC, FribourgS, PedriniAM, et al. (1998) Mutations in the XPD helicase gene result in XP and TTD phenotypes, preventing interaction between XPD and the p44 subunit of TFIIH. Nat Genet 20 : 184–188.

19. BradsherJ, CoinF, EglyJM (2000) Distinct roles for the helicases of TFIIH in transcript initiation and promoter escape. J Biol Chem 275 : 2532–2538.

20. LuH, ZawelL, FisherL, EglyJM, ReinbergD (1992) Human general transcription factor IIH phosphorylates the C-terminal domain of RNA polymerase II. Nature 358 : 641–645.

21. CompeE, DraneP, LaurentC, DiderichK, BraunC, et al. (2005) Dysregulation of the Peroxisome Proliferator-Activated Receptor Target Genes by XPD Mutations. Mol Cell Biol 25 : 6065–6076.

22. CompeE, MalerbaM, SolerL, MarescauxJ, BorrelliE, et al. (2007) Neurological defects in trichothiodystrophy reveal a coactivator function of TFIIH. Nat Neurosci 10 : 1414–1422.

23. BroughtonBC, SteingrimsdottirH, WeberCA, LehmanAR (1994) Mutations in the xeroderma pigmentosum group D DNA repair/transcription gene in patients with trichothiodystrophy. Nature gnetics 7 : 189–194.

24. de BoerJ, de WitJ, van SteegH, BergR, MorreauH, et al. (1998) A mouse model for the basal transcription/DNA repair syndrome trichothiodystrophy. Mol Cell 1(7): 981–990.

25. ItinPH, PittelkowMR (1990) Trichothiodystrophy: review of sulfur-deficient brittle hair syndromes and association with the ectodermal dysplasias. J Am Acad Dermatol 22 : 705–717.

26. FaghriS, TamuraD, KraemerKH, DigiovannaJJ (2008) Trichothiodystrophy: a systematic review of 112 published cases characterises a wide spectrum of clinical manifestations. J Med Genet 45 : 609–621.

27. LehmannAR, ArlettCF, BroughtonBC, HarcourtSA, SteingrimsdottirH, et al. (1988) Trichothiodystrophy, a human DNA repair disorder with heterogeneity in the cellular response to ultraviolet light. Cancer Res 48 : 6090–6096.

28. SokolovicM, SokolovicA, WehkampD, Ver Loren van ThemaatE, de WaartDR, et al. (2008) The transcriptomic signature of fasting murine liver. BMC Genomics 9 : 528.

29. MinassianC, AjzannayA, RiouJP, MithieuxG (1994) Investigation of the mechanism of glycogen rebound in the liver of 72-hour fasted rats. J Biol Chem 269 : 16585–16588.

30. PuigserverP, RheeJ, DonovanJ, WalkeyCJ, YoonJC, et al. (2003) Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1alpha interaction. Nature 423 : 550–555.

31. HerzigS, LongF, JhalaUS, HedrickS, QuinnR, et al. (2001) CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413 : 179–183.

32. BottaE, NardoT, LehmannAR, EglyJM, PedriniAM, et al. (2002) Reduced level of the repair/transcription factor TFIIH in trichothiodystrophy. Hum Mol Genet 11 : 2919–2928.

33. PuigserverP, WuZ, ParkCW, GravesR, WrightM, et al. (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92 : 829–839.

34. WuZ, PuigserverP, AnderssonU, ZhangC, AdelmantG, et al. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98 : 115–124.

35. SanoM, IzumiY, HeleniusK, AsakuraM, RossiDJ, et al. (2007) Menage-a-Trois 1 Is Critical for the Transcriptional Function of PPARgamma Coactivator 1. Cell Metab 5 : 129–142.

36. HaigisMC, SinclairDA (2010) Mammalian sirtuins: biological insights and disease relevance. Annual review of pathology 5 : 253–295.

37. SolomonJM, PasupuletiR, XuL, McDonaghT, CurtisR, et al. (2006) Inhibition of SIRT1 catalytic activity increases p53 acetylation but does not alter cell survival following DNA damage. Molecular and cellular biology 26 : 28–38.

38. DubaeleS, Proietti De SantisL, BienstockRJ, KerielA, StefaniniM, et al. (2003) Basal transcription defect discriminates between xeroderma pigmentosum and trichothiodystrophy in XPD patients. Mol Cell 11 : 1635–1646.

39. GuzderSN, SungP, BaillyV, PrakashL, PrakashS (1994) RAD25 is a DNA helicase required for DNA repair and RNA polymerase II transcription. Nature 369 : 578–581.

40. MorelandRJ, TirodeF, YanQ, ConawayJW, EglyJM, et al. (1999) A role for the TFIIH XPB DNA helicase in promoter escape by RNA polymerase II. J Biol Chem 274 : 22127–22130.

41. OksenychV, de JesusBB, ZhovmerA, EglyJM, CoinF (2009) Molecular insights into the recruitment of TFIIH to sites of DNA damage. EMBO J 28 : 2971–2980.

42. FanL, ArvaiAS, CooperPK, IwaiS, HanaokaF, et al. (2006) Conserved XPB core structure and motifs for DNA unwinding: implications for pathway selection of transcription or excision repair. Mol Cell 22 : 27–37.

43. KerielA, StaryA, SarasinA, Rochette-EglyC, EglyJM (2002) XPD mutations prevent TFIIH-dependent transactivation by nuclear receptors and phosphorylation of RARalpha. Cell 109 : 125–135.

44. SasakiT, MaierB, KoclegaKD, ChruszczM, GlubaW, et al. (2008) Phosphorylation regulates SIRT1 function. PLoS One 3: e4020.

45. Gerhart-HinesZ, DominyJEJr, BlattlerSM, JedrychowskiMP, BanksAS, et al. (2011) The cAMP/PKA pathway rapidly activates SIRT1 to promote fatty acid oxidation independently of changes in NAD(+). Molecular cell 44 : 851–863.

46. HoutkooperRH, PirinenE, AuwerxJ (2012) Sirtuins as regulators of metabolism and healthspan. Nature reviews Molecular cell biology 13 : 225–238.

47. ChalkiadakiA, GuarenteL (2012) Sirtuins mediate mammalian metabolic responses to nutrient availability. Nature reviews Endocrinology 8 : 287–296.

48. BrunetA, SweeneyLB, SturgillJF, ChuaKF, GreerPL, et al. (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303 : 2011–2015.

49. MottaMC, DivechaN, LemieuxM, KamelC, ChenD, et al. (2004) Mammalian SIRT1 represses forkhead transcription factors. Cell 116 : 551–563.

50. Velez-Cruz R, Zadorin AS, Coin F, Egly JM (2012) Sirt1 suppresses RNA synthesis after UV irradiation in combined xeroderma pigmentosum group D/Cockayne syndrome (XP-D/CS) cells. Proc Natl Acad Sci U S A.

51. KamiyaA, KinoshitaT, ItoY, MatsuiT, MorikawaY, et al. (1999) Fetal liver development requires a paracrine action of oncostatin M through the gp130 signal transducer. EMBO J 18 : 2127–2136.

52. KinoshitaT, SekiguchiT, XuMJ, ItoY, KamiyaA, et al. (1999) Hepatic differentiation induced by oncostatin M attenuates fetal liver hematopoiesis. Proc Natl Acad Sci U S A 96 : 7265–7270.

53. UedaT, CompeE, CatezP, KraemerKH, EglyJM (2009) Both XPD alleles contribute to the phenotype of compound heterozygote xeroderma pigmentosum patients. J Exp Med 206 : 3031–3046.