p53 Requires the Stress Sensor USF1 to Direct Appropriate Cell Fate Decision

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Cancer is a complex disease that is characterized by the sequential accumulation of genetic mutations. Exposure to environmental agents, such as solar ultraviolet, induces such alterations and thus contributes to the development of genomic instability. The tumor suppressor p53 has a central role in orchestrating cellular responses to genotoxic stress. In response to DNA-damage, p53 is stabilized and activated to direct cell fate decisions. Cells in which p53 stabilization is compromised become more vulnerable to mutagenic agents and hence the mutation rate increases, which promotes tumor development. Stabilization of p53 is thus a critical step towards cancer prevention. Using a genetic approach, we demonstrate that the ubiquitous transcription factor Upstream Stimulatory factor 1 (USF1) is required for immediate p53 stabilization and appropriate cell fate decisions following genotoxic stress. Furthermore, we show that this involves a novel function of USF1 that underscores its critical role as a stress sensor. The loss of USF1 expression should thus be considered as a potential initiator of tumorigenesis in the context of environmental insults.

Vyšlo v časopise: p53 Requires the Stress Sensor USF1 to Direct Appropriate Cell Fate Decision. PLoS Genet 10(5): e32767. doi:10.1371/journal.pgen.1004309
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004309

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Zdroje

1. HanahanD, WeinbergRA (2011) Hallmarks of cancer: the next generation. Cell 144 : 646–674.

2. LawrenceMS, StojanovP, PolakP, KryukovGV, CibulskisK, et al. (2013) Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 499 : 214–218.

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

4. OrenM (2003) Decision making by p53: life, death and cancer. Cell Death Differ 10 : 431–442.

5. BrugarolasJ, ChandrasekaranC, GordonJI, BeachD, JacksT, et al. (1995) Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 377 : 552–557.

6. DengC, ZhangP, HarperJW, ElledgeSJ, LederP (1995) Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 82 : 675–684.

7. HarperJW, AdamiGR, WeiN, KeyomarsiK, ElledgeSJ (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75 : 805–816.

8. FuchsSY, AdlerV, BuschmannT, WuX, RonaiZ (1998) Mdm2 association with p53 targets its ubiquitination. Oncogene 17 : 2543–2547.

9. KruseJP, GuW (2009) Modes of p53 regulation. Cell 137 : 609–622.

10. MeekDW, AndersonCW (2009) Posttranslational modification of p53: cooperative integrators of function. Cold Spring Harb Perspect Biol 1: a000950.

11. Gomez-LazaroM, Fernandez-GomezFJ, JordanJ (2004) p53: twenty five years understanding the mechanism of genome protection. J Physiol Biochem 60 : 287–307.

12. OlssonA, ManzlC, StrasserA, VillungerA (2007) How important are post-translational modifications in p53 for selectivity in target-gene transcription and tumour suppression? Cell Death Differ 14 : 1561–1575.

13. PietenpolJA, StewartZA (2002) Cell cycle checkpoint signaling: cell cycle arrest versus apoptosis. Toxicology 181–182 : 475–481.

14. CorreS, PrimotA, BaronY, Le SeyecJ, GodingC, et al. (2009) Target gene specificity of USF-1 is directed via p38-mediated phosphorylation-dependent acetylation. J Biol Chem 284 : 18851–18862.

15. CorreS, PrimotA, SviderskayaE, BennettDC, VaulontS, et al. (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.

16. GalibertMD, CarreiraS, GodingCR (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.

17. IkehataH, OnoT (2011) The mechanisms of UV mutagenesis. J Radiat Res 52 : 115–125.

18. NarayananDL, SaladiRN, FoxJL (2010) Ultraviolet radiation and skin cancer. Int J Dermatol 49 : 978–986.

19. RavanatJL, DoukiT, CadetJ (2001) Direct and indirect effects of UV radiation on DNA and its components. J Photochem Photobiol B 63 : 88–102.

20. ZaidiMR, DayCP, MerlinoG (2008) From UVs to metastases: modeling melanoma initiation and progression in the mouse. J Invest Dermatol 128 : 2381–2391.

21. BaronY, CorreS, MouchetN, VaulontS, PrinceS, et al. (2012) USF-1 is critical for maintaining genome integrity in response to UV-induced DNA photolesions. PLoS Genet 8: e1002470.

22. ReismanD, RotterV (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.

23. HaleTK, BraithwaiteAW (1995) Identification of an upstream region of the mouse p53 promoter critical for transcriptional expression. Nucleic Acids Res 23 : 663–669.

24. CampbellC, QuinnAG, AngusB, FarrPM, ReesJL (1993) Wavelength specific patterns of p53 induction in human skin following exposure to UV radiation. Cancer Res 53 : 2697–2699.

25. AuclairY, RougetR, Affar elB, DrobetskyEA (2008) ATR kinase is required for global genomic nucleotide excision repair exclusively during S phase in human cells. Proc Natl Acad Sci U S A 105 : 17896–17901.

26. BonnerWM, RedonCE, DickeyJS, NakamuraAJ, SedelnikovaOA, et al. (2008) GammaH2AX and cancer. Nat Rev Cancer 8 : 957–967.

27. JimenezGS, NisterM, StommelJM, BeecheM, BarcarseEA, et al. (2000) A transactivation-deficient mouse model provides insights into Trp53 regulation and function. Nat Genet 26 : 37–43.

28. LiG, MitchellDL, HoVC, ReedJC, TronVA (1996) Decreased DNA repair but normal apoptosis in ultraviolet-irradiated skin of p53-transgenic mice. Am J Pathol 148 : 1113–1123.

29. McCormickD, ChongH, HobbsC, DattaC, HallPA (1993) Detection of the Ki-67 antigen in fixed and wax-embedded sections with the monoclonal antibody MIB1. Histopathology 22 : 355–360.

30. AndorferP, SchwarzmayrL, RothenederH (2011) EAPP modulates the activity of p21 and Chk2. Cell Cycle 10 : 2077–2082.

31. Hyka-NouspikelN, DesmaraisJ, GokhalePJ, JonesM, MeuthM, et al. (2012) Deficient DNA damage response and cell cycle checkpoints lead to accumulation of point mutations in human embryonic stem cells. Stem Cells 30 : 1901–1910.

32. FerreonJC, LeeCW, AraiM, Martinez-YamoutMA, DysonHJ, et al. (2009) Cooperative regulation of p53 by modulation of ternary complex formation with CBP/p300 and HDM2. Proc Natl Acad Sci U S A 106 : 6591–6596.

33. ShiehSY, IkedaM, TayaY, PrivesC (1997) DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91 : 325–334.

34. ShiehSY, AhnJ, TamaiK, TayaY, PrivesC (2000) The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes Dev 14 : 289–300.

35. TaoW, LevineAJ (1999) P19(ARF) stabilizes p53 by blocking nucleo-cytoplasmic shuttling of Mdm2. Proc Natl Acad Sci U S A 96 : 6937–6941.

36. NakanishiM, NiidaH, MurakamiH, ShimadaM (2009) DNA damage responses in skin biology—implications in tumor prevention and aging acceleration. J Dermatol Sci 56 : 76–81.

37. JungHS, KimKS, ChungYJ, ChungHK, MinYK, et al. (2007) USF inhibits cell proliferation through delay in G2/M phase in FRTL-5 cells. Endocr J 54 : 275–285.

38. Loayza-PuchF, DrostJ, RooijersK, LopesR, ElkonR, et al. (2013) p53 induces transcriptional and translational programs to suppress cell proliferation and growth. Genome Biol 14: R32.

39. LuoX, SawadogoM (1996) Antiproliferative properties of the USF family of helix-loop-helix transcription factors. Proc Natl Acad Sci U S A 93 : 1308–1313.

40. DavisPL, MironA, AndersenLM, IglehartJD, MarksJR (1999) Isolation and initial characterization of the BRCA2 promoter. Oncogene 18 : 6000–6012.

41. GoueliBS, JanknechtR (2003) Regulation of telomerase reverse transcriptase gene activity by upstream stimulatory factor. Oncogene 22 : 8042–8047.

42. JaiswalAS, NarayanS (2001) Upstream stimulating factor-1 (USF1) and USF2 bind to and activate the promoter of the adenomatous polyposis coli (APC) tumor suppressor gene. J Cell Biochem 81 : 262–277.

43. KanayaT, KyoS, HamadaK, TakakuraM, KitagawaY, et al. (2000) Adenoviral expression of p53 represses telomerase activity through down-regulation of human telomerase reverse transcriptase transcription. Clin Cancer Res 6 : 1239–1247.

44. WuK, JiangSW, CouchFJ (2003) p53 mediates repression of the BRCA2 promoter and down-regulation of BRCA2 mRNA and protein levels in response to DNA damage. J Biol Chem 278 : 15652–15660.

45. IkehataH, OkuyamaR, OgawaE, NakamuraS, UsamiA, et al. (2010) Influences of p53 deficiency on the apoptotic response, DNA damage removal and mutagenesis in UVB-exposed mouse skin. Mutagenesis 25 : 397–405.

46. HuangLC, ClarkinKC, WahlGM (1996) Sensitivity and selectivity of the DNA damage sensor responsible for activating p53-dependent G1 arrest. Proc Natl Acad Sci U S A 93 : 4827–4832.

47. KuerbitzSJ, PlunkettBS, WalshWV, KastanMB (1992) Wild-type p53 is a cell cycle checkpoint determinant following irradiation. Proc Natl Acad Sci U S A 89 : 7491–7495.

48. Saldana-MeyerR, Recillas-TargaF (2011) Transcriptional and epigenetic regulation of the p53 tumor suppressor gene. Epigenetics 6 : 1068–1077.

49. HealyE, ReynoldsNJ, SmithMD, CampbellC, FarrPM, et al. (1994) Dissociation of erythema and p53 protein expression in human skin following UVB irradiation, and induction of p53 protein and mRNA following application of skin irritants. J Invest Dermatol 103 : 493–499.

50. LiuM, DhanwadaKR, BirtDF, HechtS, PellingJC (1994) Increase in p53 protein half-life in mouse keratinocytes following UV-B irradiation. Carcinogenesis 15 : 1089–1092.

51. GembarskaA, LucianiF, FedeleC, RussellEA, DewaeleM, et al. (2012) MDM4 is a key therapeutic target in cutaneous melanoma. Nat Med 18 : 1239–47.

52. JiZ, KumarR, TaylorM, RajaduraiA, Marzuka-AlcalaA, et al. (2013) Vemurafenib Synergizes with Nutlin-3 to Deplete Survivin and Suppress Melanoma Viability and Tumor Growth. Clin Cancer Res 19 : 4383–91.

53. LuM, BreyssensH, SalterV, ZhongS, HuY, et al. (2013) Restoring p53 function in human melanoma cells by inhibiting MDM2 and cyclin B1/CDK1-phosphorylated nuclear iASPP. Cancer Cell 23 : 618–633.

54. ChatterjeeTK, IdelmanG, BlancoV, BlomkalnsAL, PiegoreMGJr, et al. (2011) Histone deacetylase 9 is a negative regulator of adipogenic differentiation. J Biol Chem 286 : 27836–27847.

55. Crusselle-DavisVJ, VieiraKF, ZhouZ, AnantharamanA, BungertJ (2006) Antagonistic regulation of beta-globin gene expression by helix-loop-helix proteins USF and TFII-I. Mol Cell Biol 26 : 6832–6843.

56. HuangS, LiX, YusufzaiTM, QiuY, FelsenfeldG (2007) USF1 recruits histone modification complexes and is critical for maintenance of a chromatin barrier. Mol Cell Biol 27 : 7991–8002.

57. WangY, WongRH, TangT, HudakCS, YangD, et al. (2013) Phosphorylation and recruitment of BAF60c in chromatin remodeling for lipogenesis in response to insulin. Mol Cell 49 : 283–297.

58. WongRH, ChangI, HudakCS, HyunS, KwanHY, et al. (2009) A role of DNA-PK for the metabolic gene regulation in response to insulin. Cell 136 : 1056–1072.

59. SuiG, Affar elB, ShiY, BrignoneC, WallNR, et al. (2004) Yin Yang 1 is a negative regulator of p53. Cell 117 : 859–872.

60. YanC, LuD, HaiT, BoydDD (2005) Activating transcription factor 3, a stress sensor, activates p53 by blocking its ubiquitination. EMBO J 24 : 2425–2435.

61. BuschmannT, LinY, AithmittiN, FuchsSY, LuH, et al. (2001) Stabilization and activation of p53 by the coactivator protein TAFII31. J Biol Chem 276 : 13852–13857.

62. QyangY, LuoX, LuT, IsmailPM, KrylovD, et al. (1999) Cell-type-dependent activity of the ubiquitous transcription factor USF in cellular proliferation and transcriptional activation. Mol Cell Biol 19 : 1508–1517.

63. ChangD, ChenF, ZhangF, McKayBC, LjungmanM (1999) Dose-dependent effects of DNA-damaging agents on p53-mediated cell cycle arrest. Cell Growth Differ 10 : 155–162.

64. PezzolesiMG, ZbukKM, WaiteKA, EngC (2007) Comparative genomic and functional analyses reveal a novel cis-acting PTEN regulatory element as a highly conserved functional E-box motif deleted in Cowden syndrome. Hum Mol Genet 16 : 1058–1071.

65. IsmailPM, LuT, SawadogoM (1999) Loss of USF transcriptional activity in breast cancer cell lines. Oncogene 18 : 5582–5591.

66. ChangJT, YangHT, WangTC, ChengAJ (2005) Upstream stimulatory factor (USF) as a transcriptional suppressor of human telomerase reverse transcriptase (hTERT) in oral cancer cells. Mol Carcinog 44 : 183–192.

67. Cleary SP, Jeck WR, Zhao X, Kuichen Selitsky SR, et al.. (2013) Identification of driver genes in hepatocellular carcinoma by exome sequencing. Hepatology.

68. KrauthammerM, KongY, HaBH, EvansP, BacchiocchiA, et al. (2012) Exome sequencing identifies recurrent somatic RAC1 mutations in melanoma. Nat Genet 44 : 1006–1014.

69. MorinRD, MungallK, PleasanceE, MungallAJ, GoyaR, et al. (2013) Mutational and structural analysis of diffuse large B-cell lymphoma using whole genome sequencing. Blood 122 : 1256–65.

70. ZeilingerS, KuhnelB, KloppN, BaurechtH, KleinschmidtA, et al. (2013) Tobacco smoking leads to extensive genome-wide changes in DNA methylation. PLoS One 8: e63812.

71. BussiereFI, MichelV, MemetS, AveP, VivasJR, et al. (2010) H. pylori-induced promoter hypermethylation downregulates USF1 and USF2 transcription factor gene expression. Cell Microbiol 12 : 1124–1133.

72. WeiJ, NagyTA, VilgelmA, ZaikaE, OgdenSR, et al. (2010) Regulation of p53 tumor suppressor by Helicobacter pylori in gastric epithelial cells. Gastroenterology 139 : 1333–1343.

73. ValletVS, CasadoM, HenrionAA, BucchiniD, RaymondjeanM, et al. (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.

74. LichtiU, AndersJ, YuspaSH (2008) Isolation and short-term culture of primary keratinocytes, hair follicle populations and dermal cells from newborn mice and keratinocytes from adult mice for in vitro analysis and for grafting to immunodeficient mice. Nat Protoc 3 : 799–810.

75. KernSE, PietenpolJA, ThiagalingamS, SeymourA, KinzlerKW, et al. (1992) Oncogenic forms of p53 inhibit p53-regulated gene expression. Science 256 : 827–830.

76. SaitoS, GoodarziAA, HigashimotoY, NodaY, Lees-MillerSP, et al. (2002) ATM mediates phosphorylation at multiple p53 sites, including Ser(46), in response to ionizing radiation. J Biol Chem 277 : 12491–12494.