KDM5 Interacts with Foxo to Modulate Cellular Levels of Oxidative Stress

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Reactive oxygen species are essential signaling molecules within the cell. However, when levels of these reactive intermediates become too high (oxidative stress), they cause significant damage to proteins and DNA. It is therefore vitally important to understand how cells regulate genes required to limit oxidative stress. Here we describe a new role for the transcription co-factor KDM5 as an activator of genes that prevent oxidative stress. KDM5 activates these genes by interacting with the transcription factor Foxo and affecting its ability to be recruited to target promoters. Our data provide new insights into the mechanisms by which redox state is regulated, and into the multiple means by which KDM5 regulates gene expression.

Vyšlo v časopise: KDM5 Interacts with Foxo to Modulate Cellular Levels of Oxidative Stress. PLoS Genet 10(10): e32767. doi:10.1371/journal.pgen.1004676
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004676

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1. RothbartSB, StrahlBD (2014) Interpreting the language of histone and DNA modifications. Biochim Biophys Acta 1839: 627–43 doi: 10.1016/j.bbagrm.2014.03.001

2. MargueronR, ReinbergD (2010) Chromatin structure and the inheritance of epigenetic information. Nat Rev Genet 11: 285–296.

3. BlairLP, CaoJ, ZouMR, SayeghJ, YanQ (2011) Epigenetic Regulation by Lysine Demethylase 5 (KDM5) Enzymes in Cancer. Cancers (Basel) 3: 1383–1404.

4. SecombeJ, EisenmanRN (2007) The function and regulation of the JARID1 family of histone H3 lysine 4 demethylases - The Myc connection. Cell Cycle 6: 1324–1328.

5. Lopez-BigasN, KisielTA, DeWaalDC, HolmesKB, VolkertTL, et al. (2008) Genome-wide analysis of the H3K4 histone demethylase RBP2 reveals a transcriptional program controlling differentiation. Molecular Cell 31: 520–530.

6. ChristensenJ, AggerK, CloosPA, PasiniD, RoseS, et al. (2007) RBP2 belongs to a family of demethylases, specific for tri-and dimethylated lysine 4 on histone H3. Cell 128: 1063–1076.

7. KloseRJ, YanQ, TothovaZ, YamaneK, Erdjument-BromageH, et al. (2007) The Retinoblastoma binding protein RBP2 is a H3K4 demethylase. Cell 128: 889–900.

8. IwaseS, LanF, BaylissP, de la Torre-UbietaL, HuarteM, et al. (2007) The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 128: 1077–1088.

9. YamaneK, TateishiK, KloseRJ, FangJ, FabrizioLA, et al. (2007) PLU-1 is a H3K4 demethylase involved in transcriptional repression and breast cancer cell proliferation. Molecular Cell 25: 801–812.

10. LeeMG, NormanJ, ShilatifardA, ShiekhattarR (2007) Physical and functional association of a trimethyl H3K4 demethylase and RING6a/MBLR, a Polycomb-like protein. Cell 128: 877–887.

11. EissenbergJC, LeeMG, SchneiderJ, IlvarsonnA, ShiekhattarR, et al. (2007) The trithorax-group gene in Drosophila little imaginal discs encodes a trimethylated histone H3 Lys4 demethylase. Nature Structural & Molecular Biology 14: 344–346.

12. LeeN, ZhangJY, KloseRJ, Erdjument-BromageH, TempstP, et al. (2007) The trithorax-group protein Lid is a histone H3 trimethyl-Lys4 demethylase. Nature Structural & Molecular Biology 14: 341–343.

13. SecombeJ, LiL, CarlosLS, EisenmanRN (2007) The Trithorax group protein Lid is a trimethyl histone H3K4 demethylase required for dMyc-induced cell growth. Genes & Development 21: 537–551.

14. KloseRJ, ZhangY (2007) Regulation of histone methylation by demethylimination and demethylation. Nat Rev Mol Cell Biol 8: 307–318.

15. LiL, GreerC, EisenmanRN, SecombeJ (2010) Essential functions of the histone demethylase lid. PLoS Genet 6: e1001221.

16. CatchpoleS, Spencer-DeneB, HallD, SantangeloS, RosewellI, et al. (2011) PLU-1/JARID1B/KDM5B is required for embryonic survival and contributes to cell proliferation in the mammary gland and in ER+ breast cancer cells. Int J Oncol 38: 1267–1277.

17. AlbertM, SchmitzSU, KooistraSM, MalatestaM, Morales TorresC, et al. (2013) The histone demethylase Jarid1b ensures faithful mouse development by protecting developmental genes from aberrant H3K4me3. PLoS Genet 9: e1003461.

18. DiTacchioL, LeHD, VollmersC, HatoriM, WitcherM, et al. (2011) Histone lysine demethylase JARID1a activates CLOCK-BMAL1 and influences the circadian clock. Science 333: 1881–1885.

19. LeeN, Erdjument-BromageH, TempstP, JonesRS, ZhangY (2009) The H3K4 Demethylase Lid Associates with and Inhibits the Histone Deacetylase Rpd3. Molecular and Cellular Biology 29: 1401–1410.

20. BarrettA, SantangeloS, TanK, CatchpoleS, RobertsK, et al. (2007) Breast cancer associated transcriptional repressor PLU-1/JARID1B interacts directly with histone deacetylases. International Journal of Cancer 121: 265–275.

21. KleinBJ, PiaoL, XiY, Rincon-AranoH, RothbartSB, et al. (2014) The Histone-H3K4-Specific Demethylase KDM5B Binds to Its Substrate and Product through Distinct PHD Fingers. Cell Rep 6: 325–35 doi: 10.1016/j.celrep.2013.12.021

22. GildeaJJ, LopezR, ShearnA (2000) A screen for new trithorax group genes identified little imaginal discs, the Drosophila melanogaster homologue of human retinoblastoma binding protein 2. Genetics 156: 645–663.

23. RoeschA, Fukunaga-KalabisM, SchmidtEC, ZabierowskiSE, BraffordPA, et al. (2010) A temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growth. Cell 141: 583–594.

24. RoeschA, VulturA, BogeskiI, WangH, ZimmermannKM, et al. (2013) Overcoming Intrinsic Multidrug Resistance in Melanoma by Blocking the Mitochondrial Respiratory Chain of Slow-Cycling JARID1B(high) Cells. Cancer Cell 23: 811–825.

25. OutchkourovNS, MuinoJM, KaufmannK, van IjckenWF, Groot KoerkampMJ, et al. (2013) Balancing of histone H3K4 methylation states by the Kdm5c/SMCX histone demethylase modulates promoter and enhancer function. Cell Rep 3: 1071–1079.

26. BenevolenskayaEV (2007) Retinoblastoma binding protein 2 (RBP2) and differentiation. Biochemistry and Cell Biology-Biochimie Et Biologie Cellulaire 85: 523–523.

27. BenevolenskayaEV, MurrayHL, BrantonP, YoungRA, KaelinWG (2005) Binding of pRB to the PHD protein RBP2 promotes cellular differentiation. Molecular Cell 18: 623–635.

28. LinW, CaoJ, LiuJ, BeshiriML, FujiwaraY, et al. (2011) Loss of the retinoblastoma binding protein 2 (RBP2) histone demethylase suppresses tumorigenesis in mice lacking Rb1 or Men1. Proc Natl Acad Sci U S A 108: 13379–13386.

29. JensenLR, AmendeM, GurokU, MoserB, GimmelV, et al. (2005) Mutations in the JARID1C gene, which is involved in transcriptional regulation and chromatin remodeling, cause X-linked mental retardation. American Journal of Human Genetics 76: 227–236.

30. RujirabanjerdS, NelsonJ, TarpeyPS, HackettA, EdkinsS, et al. (2010) Identification and characterization of two novel JARID1C mutations: suggestion of an emerging genotype-phenotype correlation. Eur J Hum Genet 18: 330–335.

31. SantosC, Rodriguez-RevengaL, MadrigalI, BadenasC, PinedaM, et al. (2006) A novel mutation in JARID1C gene associated with mental retardation. Eur J Hum Genet 14: 583–586.

32. Santos-ReboucasCB, Fintelman-RodriguesN, JensenLR, KussAW, RibeiroMG, et al. (2011) A novel nonsense mutation in KDM5C/JARID1C gene causing intellectual disability, short stature and speech delay. Neurosci Lett 498: 67–71.

33. MartinI, GrotewielMS (2006) Oxidative damage and age-related functional declines. Mech Ageing Dev 127: 411–423.

34. PaganoG, CastelloG (2012) Oxidative stress and mitochondrial dysfunction in Down syndrome. Adv Exp Med Biol 724: 291–299.

35. VictorinoVJ, PizzattiL, MichellettiP, PanisC (2014) Oxidative Stress, Redox Signaling and Cancer Chemoresistance: Putting Together the Pieces of the Puzzle. Curr Med Chem 21: 3211–26.

36. ZidBM, RogersAN, KatewaSD, VargasMA, KolipinskiMC, et al. (2009) 4E-BP extends lifespan upon dietary restriction by enhancing mitochondrial activity in Drosophila. Cell 139: 149–160.

37. TelemanAA, ChenYW, CohenSM (2005) 4E-BP functions as a metabolic brake used under stress conditions but not during normal growth. Genes Dev 19: 1844–1848.

38. TettweilerG, MironM, JenkinsM, SonenbergN, LaskoPF (2005) Starvation and oxidative stress resistance in Drosophila are mediated through the eIF4E-binding protein, d4E-BP. Genes Dev 19: 1840–1843.

39. WoodZA, SchroderE, Robin HarrisJ, PooleLB (2003) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 28: 32–40.

40. RadyukSN, MichalakK, KlichkoVI, BenesJ, RebrinI, et al. (2009) Peroxiredoxin 5 confers protection against oxidative stress and apoptosis and also promotes longevity in Drosophila. Biochem J 419: 437–445.

41. TulsawaniR, KellyLS, FatmaN, ChhunchhaB, KuboE, et al. (2010) Neuroprotective effect of peroxiredoxin 6 against hypoxia-induced retinal ganglion cell damage. BMC Neurosci 11: 125.

42. MassudiH, GrantR, GuilleminGJ, BraidyN (2012) NAD+ metabolism and oxidative stress: the golden nucleotide on a crown of thorns. Redox Rep 17: 28–46.

43. WalkerDW, MuffatJ, RundelC, BenzerS (2006) Overexpression of a Drosophila homolog of apolipoprotein D leads to increased stress resistance and extended lifespan. Current Biology 16: 674–679.

44. WangMC, BohmannD, JasperH (2005) JNK extends life span and limits growth by antagonizing cellular and organism-wide responses to insulin signaling. Cell 121: 115–125.

45. LinYJ, SeroudeL, BenzerS (1998) Extended life-span and stress resistance in the Drosophila mutant methuselah. Science 282: 943–946.

46. SanchezD, Lopez-AriasB, TorrojaL, CanalI, WangX, et al. (2006) Loss of glial lazarillo, a homolog of apolipoprotein D, reduces lifespan and stress resistance in Drosophila. Current Biology 16: 680–686.

47. GreerC, LeeM, WesterhofM, MilhollandB, SpokonyR, et al. (2013) Myc-dependent genome instability and lifespan in Drosophila. PLoS One 8: e74641.

48. SlackC, GiannakouME, FoleyA, GossM, PartridgeL (2011) dFOXO-independent effects of reduced insulin-like signaling in Drosophila. Aging Cell 10: 735–748.

49. DengH (2014) Multiple roles of Nrf2-Keap1 signaling: regulation of development and xenobiotic response using distinct mechanisms. Fly (Austin) 8: 7–12.

50. HwangAB, JeongDE, LeeSJ (2012) Mitochondria and organismal longevity. Curr Genomics 13: 519–532.

51. GarciaAM, DerventziA, BusuttilR, CalderRB, PerezEJr, et al. (2007) A model system for analyzing somatic mutations in Drosophila melanogaster. Nat Methods 4: 401–403.

52. CalnanDR, BrunetA (2008) The FoxO code. Oncogene 27: 2276–2288.

53. JüngerMA, RintelenF, StockerH, WassermanJD, VeghM, et al. (2003) The Drosophila forkhead transcription factor FOXO mediates the reduction in cell number associated with reduced insulin signaling. J Biol 2: 20.

54. PuigO, MarrMT, RuhfML, TjianR (2003) Control of cell number by Drosophila FOXO: downstream and feedback regulation of the insulin receptor pathway. Genes Dev 17: 2006–2020.

55. AlicN, AndrewsTD, GiannakouME, PapatheodorouI, SlackC, et al. (2011) Genome-wide dFOXO targets and topology of the transcriptomic response to stress and insulin signalling. Mol Syst Biol 7: 502.

56. BaiH, KangP, HernandezAM, TatarM (2013) Activin signaling targeted by insulin/dFOXO regulates aging and muscle proteostasis in Drosophila. PLoS Genet 9: e1003941.

57. TelemanAA, HietakangasV, SayadianAC, CohenSM (2008) Nutritional control of protein biosynthetic capacity by insulin via Myc in Drosophila. Cell Metab 7: 21–32.

58. KramerJM, DavidgeJT, LockyerJM, StaveleyBE (2003) Expression of Drosophila FOXO regulates growth and can phenocopy starvation. BMC Dev Biol 3: 5.

59. DaitokuH, SakamakiJ, FukamizuA (2011) Regulation of FoxO transcription factors by acetylation and protein-protein interactions. Biochim Biophys Acta 1813: 1954–1960.

60. WangB, MoyaN, NiessenS, HooverH, MihaylovaMM, et al. (2011) A hormone-dependent module regulating energy balance. Cell 145: 596–606.

61. MihaylovaMM, VasquezDS, RavnskjaerK, DenechaudPD, YuRT, et al. (2011) Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell 145: 607–621.

62. Lloret-LlinaresM, Perez-LluchS, RossellD, MoranT, Ponsa-CobasJ, et al. (2012) dKDM5/LID regulates H3K4me3 dynamics at the transcription-start site (TSS) of actively transcribed developmental genes. Nucleic Acids Research 40: 9493–505 doi: 10.1093/nar/gks773

63. LiX, FangP, MaiJ, ChoiET, WangH, et al. (2013) Targeting mitochondrial reactive oxygen species as novel therapy for inflammatory diseases and cancers. J Hematol Oncol 6: 19.

64. WangGG, SongJ, WangZ, DormannHL, CasadioF, et al. (2009) Haematopoietic malignancies caused by dysregulation of a chromatin-binding PHD finger. Nature 459: 847–851.

65. CaoJ, LiuZ, CheungWK, ZhaoM, ChenSY, et al. (2014) Histone demethylase RBP2 is critical for breast cancer progression and metastasis. Cell Rep 6: 868–877.

66. De FeliceC, SignoriniC, LeonciniS, PecorelliA, DurandT, et al. (2012) The role of oxidative stress in Rett syndrome: an overview. Ann N Y Acad Sci 1259: 121–135.

67. YanMH, WangX, ZhuX (2013) Mitochondrial defects and oxidative stress in Alzheimer disease and Parkinson disease. Free Radic Biol Med 62: 90–101.

68. HuZ, ChenL, ZhangJ, LiT, TangJ, et al. (2007) Structure, function, property, and role in neurologic diseases and other diseases of the sHsp22. J Neurosci Res 85: 2071–2079.

69. PattenDA, GermainM, KellyMA, SlackRS (2010) Reactive oxygen species: stuck in the middle of neurodegeneration. J Alzheimers Dis 20 Suppl 2: S357–367.

70. XuJ, DengX, DistecheCM (2008) Sex-Specific Expression of the X-Linked Histone Demethylase Gene Jarid1c in Brain. Plos One 3: e2553.

71. RiedelCG, DowenRH, LourencoGF, KirienkoNV, HeimbucherT, et al. (2013) DAF-16 employs the chromatin remodeller SWI/SNF to promote stress resistance and longevity. Nat Cell Biol 15: 491–501.

72. EberhardySR, FarnhamPJ (2002) Myc recruits P-TEFb to mediate the final step in the transcriptional activation of the cad promoter. Journal of Biological Chemistry 277: 40156–40162.

73. EberhardySR, FarnhamPJ (2002) Myc mediates activation of the cad promoter via a post-RNA polymerase II recruitment mechanism. Faseb Journal 16: A1–a1.

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

75. DaitokuH, HattaM, MatsuzakiH, ArataniS, OhshimaT, et al. (2004) Silent information regulator 2 potentiates Foxo1-mediated transcription through its deacetylase activity. Proc Natl Acad Sci U S A 101: 10042–10047.

76. WatrobaM, MaslinskaD, MaslinskiS (2012) Current overview of functions of FoxO proteins, with special regards to cellular homeostasis, cell response to stress, as well as inflammation and aging. Adv Med Sci 57: 183–195.

77. GreerEL, MauresTJ, HauswirthAG, GreenEM, LeemanDS, et al. (2010) Members of the H3K4 trimethylation complex regulate lifespan in a germline-dependent manner in C. elegans. Nature 466: 383–387.

78. AlvaresSM, MayberryGA, JoynerEY, LakowskiB, AhmedS (2013) H3K4 demethylase activities repress proliferative and postmitotic aging. Aging Cell 13: 245–53 doi: 10.1111/acel.12166

79. OrrWC, RadyukSN, SohalRS (2013) Involvement of redox state in the aging of Drosophila melanogaster. Antioxid Redox Signal 19: 788–803.

80. PuigO, TijanR (2005) Transcriptional feedback control of insulin receptor by dFOXO/FOXO1. Genes & Development 19: 2435–2446.

81. GuW, RoederRG (1997) Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90: 595–606.

82. GuW, ShiXL, RoederRG (1997) Synergistic activation of transcription by CBP and p53. Nature 387: 819–823.

83. BoyesJ, ByfieldP, NakataniY, OgryzkoV (1998) Regulation of activity of the transcription factor GATA-1 by acetylation. Nature 396: 594–598.

84. MinKJ, YamamotoR, BuchS, PankratzM, TatarM (2008) Drosophila lifespan control by dietary restriction independent of insulin-like signaling. Aging Cell 7: 199–206.

85. ZaffranS, ChartierA, GallantP, AstierM, ArquierN, et al. (1998) A Drosophila RNA helicase gene, pitchoune, is required for cell growth and proliferation and is a potential target of d-Myc. Development 125: 3571–3584.

86. KanaoT, VenderovaK, ParkDS, UntermanT, LuB, et al. (2010) Activation of FoxO by LRRK2 induces expression of proapoptotic proteins and alters survival of postmitotic dopaminergic neuron in Drosophila. Hum Mol Genet 19: 3747–3758.

87. HurlinPJ, FoleyKP, AyerDE, EisenmanRN, HanahanD, et al. (1995) Regulation of Myc and Mad during epidermal differentiation and HPV-associated tumorigenesis. Oncogene 11: 2487–2501.

88. LivakKJ, SchmittgenTD (2001) Analysis of relative gene expression data using Real-Time quantitative PCR and the 2−DDC method. Methods 25: 402–408.

89. GronkeS, ClarkeDF, BroughtonS, AndrewsTD, PartridgeL (2010) Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLoS Genet 6: e1000857.

90. de HoonMJ, ImotoS, NolanJ, MiyanoS (2004) Open source clustering software. Bioinformatics 20: 1453–1454.

91. StoreyJD, TibshiraniR (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 100: 9440–9445.

92. StoreyJD, TibshiraniR (2003) Statistical methods for identifying differentially expressed genes in DNA microarrays. Methods Mol Biol 224: 149–157.

93. Huang daW, ShermanBT, ZhengX, YangJ, ImamichiT, et al. (2009) Extracting biological meaning from large gene lists with DAVID. Curr Protoc Bioinformatics Chapter 13: Unit 13 11.

94. Huang daW, ShermanBT, LempickiRA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44–57.

95. ZhengQ, WangXJ (2008) GOEAST: a web-based software toolkit for Gene Ontology enrichment analysis. Nucleic Acids Res 36: W358–363.

96. Pérez-LluchS, BlancoE, CarbonellA, RahaD, SnyderM, et al. (2011) Genome-wide chromatin occupancy analysis reveals a role for ASH2 in transcriptional pausing. Nucleic Acids Research 39: 4628–39 doi: 10.1093/nar/gkq1322