Genome-Wide Location Analysis Reveals Distinct Transcriptional Circuitry by Paralogous Regulators Foxa1 and Foxa2
Gene duplication is a powerful driver of evolution. Newly duplicated genes acquire new roles that are relevant to fitness, or they will be lost over time. A potential path to functional relevance is mutation of the coding sequence leading to the acquisition of novel biochemical properties, as analyzed here for the highly homologous paralogs Foxa1 and Foxa2 transcriptional regulators. We determine by genome-wide location analysis (ChIP-Seq) that, although Foxa1 and Foxa2 share a large fraction of binding sites in the liver, each protein also occupies distinct regulatory elements in vivo. Foxa1-only sites are enriched for p53 binding sites and are frequently found near genes important to cell cycle regulation, while Foxa2-restricted sites show only a limited match to the forkhead consensus and are found in genes involved in steroid and lipid metabolism. Thus, Foxa1 and Foxa2, while redundant during development, have evolved divergent roles in the adult liver, ensuring the maintenance of both genes during evolution.
Vyšlo v časopise:
Genome-Wide Location Analysis Reveals Distinct Transcriptional Circuitry by Paralogous Regulators Foxa1 and Foxa2. PLoS Genet 8(6): e32767. doi:10.1371/journal.pgen.1002770
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002770
Souhrn
Gene duplication is a powerful driver of evolution. Newly duplicated genes acquire new roles that are relevant to fitness, or they will be lost over time. A potential path to functional relevance is mutation of the coding sequence leading to the acquisition of novel biochemical properties, as analyzed here for the highly homologous paralogs Foxa1 and Foxa2 transcriptional regulators. We determine by genome-wide location analysis (ChIP-Seq) that, although Foxa1 and Foxa2 share a large fraction of binding sites in the liver, each protein also occupies distinct regulatory elements in vivo. Foxa1-only sites are enriched for p53 binding sites and are frequently found near genes important to cell cycle regulation, while Foxa2-restricted sites show only a limited match to the forkhead consensus and are found in genes involved in steroid and lipid metabolism. Thus, Foxa1 and Foxa2, while redundant during development, have evolved divergent roles in the adult liver, ensuring the maintenance of both genes during evolution.
Zdroje
1. LevineMTjianR 2003 Transcription regulation and animal diversity. Nature 424 147 151
2. SinghLNHannenhalliS 2008 Functional diversification of paralogous transcription factors via divergence in DNA binding site motif and in expression. PLoS ONE 3 e2345doi:10.1371/journal.pone.0002345
3. DavidsonEH 2009 Network design principles from the sea urchin embryo. Curr Opin Genet Dev 19 535 540
4. BochkisIMSchugJRubinsNEChopraARO'MalleyBW 2009 Foxa2-Dependent Hepatic Gene Regulatory Networks Depend on Physiological State. Physiol Genomics
5. LeeCSFriedmanJRFulmerJTKaestnerKH 2005 The initiation of liver development is dependent on Foxa transcription factors. Nature 435 944 947
6. BochkisIMRubinsNEWhitePFurthEEFriedmanJR 2008 Hepatocyte-specific ablation of Foxa2 alters bile acid homeostasis and results in endoplasmic reticulum stress. Nat Med 14 828 836
7. KaestnerKH 2005 The making of the liver: developmental competence in foregut endoderm and induction of the hepatogenic program. Cell Cycle 4 1146 1148
8. LaiEPreziosoVRTaoWFChenWSDarnellJEJr 1991 Hepatocyte nuclear factor 3 alpha belongs to a gene family in mammals that is homologous to the Drosophila homeotic gene fork head. Genes Dev 5 416 427
9. ClarkKLHalayEDLaiEBurleySK 1993 Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature 364 412 420
10. QianXCostaRH 1995 Analysis of hepatocyte nuclear factor-3 beta protein domains required for transcriptional activation and nuclear targeting. Nucleic Acids Res 23 1184 1191
11. PaniLOverdierDGPorcellaAQianXLaiE 1992 Hepatocyte nuclear factor 3 beta contains two transcriptional activation domains, one of which is novel and conserved with the Drosophila fork head protein. Mol Cell Biol 12 3723 3732
12. WolfrumCBesserDLucaEStoffelM 2003 Insulin regulates the activity of forkhead transcription factor Hnf-3beta/Foxa-2 by Akt-mediated phosphorylation and nuclear/cytosolic localization. Proc Natl Acad Sci U S A 100 11624 11629
13. NockAAscanoJMJonesTBarreroMJSugiyamaN 2009 Identification of DNA-dependent protein kinase as a cofactor for the forkhead transcription factor FoxA2. J Biol Chem 284 19915 19926
14. LiZWhitePTutejaGRubinsNSackettS 2009 Foxa1 and Foxa2 regulate bile duct development in mice. J Clin Invest 119 1537 1545
15. TutejaGWhitePSchugJKaestnerKH 2009 Extracting transcription factor targets from ChIP-Seq data. Nucleic Acids Res 37 e113
16. LupienMEeckhouteJMeyerCAWangQZhangY 2008 FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 132 958 970
17. RobertsonAGBilenkyMTamAZhaoYZengT 2008 Genome-wide relationship between histone H3 lysine 4 mono- and tri-methylation and transcription factor binding. Genome Res 18 1906 1917
18. Portales-CasamarEThongjueaSKwonATArenillasDZhaoX 2010 JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res 38 D105 110
19. MatysVKel-MargoulisOVFrickeELiebichILandS 2006 TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res 34 D108 110
20. GaoNLe LayJQinWDolibaNSchugJ 2010 Foxa1 and Foxa2 maintain the metabolic and secretory features of the mature beta-cell. Mol Endocrinol 24 1594 1604
21. McPhersonLALoktevAVWeigelRJ 2002 Tumor suppressor activity of AP2alpha mediated through a direct interaction with p53. J Biol Chem 277 45028 45033
22. HurtadoAHolmesKARoss-InnesCSSchmidtDCarrollJS 2012 FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat Genet 43 27 33
23. LiZTutejaGSchugJKaestnerKH 2012 Foxa1 and Foxa2 are essential for sexual dimorphism in liver cancer. Cell 148 72 83
24. NguyenTTChoKStrattonSABartonMC 2005 Transcription factor interactions and chromatin modifications associated with p53-mediated, developmental repression of the alpha-fetoprotein gene. Mol Cell Biol 25 2147 2157
25. TaubeJHAlltonKDuncanSAShenLBartonMC 2010 Foxa1 functions as a pioneer transcription factor at transposable elements to activate Afp during differentiation of embryonic stem cells. J Biol Chem 285 16135 16144
26. MeulmeesterETen DijkeP 2011 The dynamic roles of TGF-beta in cancer. J Pathol 223 205 218
27. GaoNZhangJRaoMACaseTCMirosevichJ 2003 The role of hepatocyte nuclear factor-3 alpha (Forkhead Box A1) and androgen receptor in transcriptional regulation of prostatic genes. Mol Endocrinol 17 1484 1507
28. SunQYuXDegraffDJMatusikRJ 2009 Upstream stimulatory factor 2, a novel FoxA1-interacting protein, is involved in prostate-specific gene expression. Mol Endocrinol 23 2038 2047
29. GriffinMJWongRHPandyaNSulHS 2007 Direct interaction between USF and SREBP-1c mediates synergistic activation of the fatty-acid synthase promoter. J Biol Chem 282 5453 5467
30. PetersonRSClevidenceDEYeHCostaRH 1997 Hepatocyte nuclear factor-3 alpha promoter regulation involves recognition by cell-specific factors, thyroid transcription factor-1, and autoactivation. Cell Growth Differ 8 69 82
31. BesnardVWertSEHullWMWhitsettJA 2004 Immunohistochemical localization of Foxa1 and Foxa2 in mouse embryos and adult tissues. Gene Expr Patterns 5 193 208
32. BehrRBrestelliJFulmerJTMiyawakiNKleymanTR 2004 Mild nephrogenic diabetes insipidus caused by Foxa1 deficiency. J Biol Chem 279 41936 41941
33. LaganiereJDebloisGLefebvreCBatailleARRobertF 2005 From the Cover: Location analysis of estrogen receptor alpha target promoters reveals that FOXA1 defines a domain of the estrogen response. Proc Natl Acad Sci U S A 102 11651 11656
34. CarrollJSLiuXSBrodskyASLiWMeyerCA 2005 Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122 33 43
35. ZhangLRubinsNEAhimaRSGreenbaumLEKaestnerKH 2005 Foxa2 integrates the transcriptional response of the hepatocyte to fasting. Cell Metab 2 141 148
36. NoshiroMUsuiEKawamotoTKuboHFujimotoK 2007 Multiple mechanisms regulate circadian expression of the gene for cholesterol 7alpha-hydroxylase (Cyp7a), a key enzyme in hepatic bile acid biosynthesis. J Biol Rhythms 22 299 311
37. Kohler S, Cirillo LA Stable chromatin binding prevents FoxA acetylation, preserving FoxA chromatin remodeling. J Biol Chem 285 464 472
38. CirilloLALinFRCuestaIFriedmanDJarnikM 2002 Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol Cell 9 279 289
39. WederellEDBilenkyMCullumRThiessenNDagpinarM 2008 Global analysis of in vivo Foxa2-binding sites in mouse adult liver using massively parallel sequencing. Nucleic Acids Res 36 4549 4564
40. OdomDTDowellRDJacobsenESNekludovaLRolfePA 2006 Core transcriptional regulatory circuitry in human hepatocytes. Mol Syst Biol 2: 2006 0017
41. Rada-IglesiasAWallermanOKochCAmeurAEnrothS 2005 Binding sites for metabolic disease related transcription factors inferred at base pair resolution by chromatin immunoprecipitation and genomic microarrays. Hum Mol Genet 14 3435 3447
42. OdomDTDowellRDJacobsenESGordonWDanfordTW 2007 Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nat Genet 39 730 732
43. WangQLiWZhangYYuanXXuK 2009 Androgen receptor regulates a distinct transcription program in androgen-independent prostate cancer. Cell 138 245 256
44. GaoNLeLayJVatamaniukMZRieckSFriedmanJR 2008 Dynamic regulation of Pdx1 enhancers by Foxa1 and Foxa2 is essential for pancreas development. Genes Dev 22 3435 3448
45. YeDZKaestnerKH 2009 Foxa1 and Foxa2 control the differentiation of goblet and enteroendocrine L- and D-cells in mice. Gastroenterology 137 2052 2062
46. HuaSKittlerRWhiteKP 2009 Genomic antagonism between retinoic acid and estrogen signaling in breast cancer. Cell 137 1259 1271
47. EeckhouteJCarrollJSGeistlingerTRTorres-ArzayusMIBrownM 2006 A cell-type-specific transcriptional network required for estrogen regulation of cyclin D1 and cell cycle progression in breast cancer. Genes Dev 20 2513 2526
48. LeeKCCroweAJBartonMC 1999 p53-mediated repression of alpha-fetoprotein gene expression by specific DNA binding. Mol Cell Biol 19 1279 1288
49. NaqviAHoffmanTADeRiccoJKumarAKimCS 2010 A single-nucleotide variation in a p53-binding site affects nutrient-sensitive human SIRT1 expression. Hum Mol Genet 19 4123 4133
50. Wesierska-GadekJRanftlerCSchmidG 2005 Physiological ageing: role of p53 and PARP-1 tumor suppressors in the regulation of terminal senescence. J Physiol Pharmacol 56 77 88
51. MayeurGLKungWJMartinezAIzumiyaCChenDJ 2005 Ku is a novel transcriptional recycling coactivator of the androgen receptor in prostate cancer cells. J Biol Chem 280 10827 10833
52. PavriRLewisBKimTKDilworthFJErdjument-BromageH 2005 PARP-1 determines specificity in a retinoid signaling pathway via direct modulation of mediator. Mol Cell 18 83 96
53. KaestnerKHKatzJLiuYDruckerDJSchutzG 1999 Inactivation of the winged helix transcription factor HNF3alpha affects glucose homeostasis and islet glucagon gene expression in vivo. Genes Dev 13 495 504
54. SharovAAKoMS 2009 Exhaustive search for over-represented DNA sequence motifs with CisFinder. DNA Res 16 261 273
55. Thomas-ChollierMSandOTuratsinzeJVJankyRDefranceM 2008 RSAT: regulatory sequence analysis tools. Nucleic Acids Res 36 W119 127
56. CarlsonJMChakravartyADeZielCEGrossRH 2007 SCOPE: a web server for practical de novo motif discovery. Nucleic Acids Res 35 W259 264
57. LarkinMABlackshieldsGBrownNPChennaRMcGettiganPA 2007 Clustal W and Clustal X version 2.0. Bioinformatics 23 2947 2948
58. MarstrandTTFrellsenJMoltkeIThiimMValenE 2008 Asap: a framework for over-representation statistics for transcription factor binding sites. PLoS ONE 3e1623doi:10.1371/journal.pone.0001623
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 6
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