Nucleation of DNA repair factors by FOXA1 links DNA demethylation to transcriptional pioneering

Nature Genetics

Volumn 48, Issue 9, 2016, Pages 1003-1013

  Zhang, Yu ^a   Zhang, Di ^a   Li, Qian ^a   Liang, Jing ^a   Sun, Luyang ^a   Yi, Xia ^a   Chen, Zhe ^a   Yan, Ruorong ^a   Xie, Guojia ^a   Li, Wanjin ^a   Liu, Shumeng ^a   Xu, Bosen ^a   Li, Lei ^a   Yang, Jianguo ^a   He, Lin ^a   Shang, Yongfeng ^a,b  

^a Department of Biochemistry and Molecular BiologyCancer Hospital of Peking University   (China)

^b TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE BETA; DNA TOPOISOMERASE (ATP HYDROLYSING) B; ESTROGEN RECEPTOR ALPHA; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; KU ANTIGEN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; RECEPTOR INTERACTING PROTEIN 140; X BOX BINDING PROTEIN 1; XRCC1 PROTEIN; DNA LIGASE; ESTROGEN; FOXA1 PROTEIN, HUMAN;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DEMETHYLATION; DNA BINDING; DNA METHYLATION; DNA REPAIR; DNA TRANSCRIPTION; DOUBLE STRANDED DNA BREAK; ENHANCER REGION; EPIGENETICS; FEMALE; GENE MAPPING; GENE TARGETING; HUMAN; HUMAN CELL; MALE; NUCLEAR REPROGRAMMING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SINGLE STRANDED DNA BREAK; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HELA CELL LINE; MCF-7 CELL LINE; METABOLISM; NEOPLASM;

BINDING SITES; DNA METHYLATION; DNA POLYMERASE BETA; DNA REPAIR; DNA REPAIR ENZYMES; EPIGENOMICS; ESTROGENS; GENE EXPRESSION REGULATION, NEOPLASTIC; HELA CELLS; HEPATOCYTE NUCLEAR FACTOR 3-ALPHA; HUMANS; MCF-7 CELLS; NEOPLASMS; PROMOTER REGIONS, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84981214271     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3635     Document Type: Article

References (69)

1. Augello, M.A., Hickey, T.E. & Knudsen, K.E. FOXA1: master of steroid receptor function in cancer. EMBO J. 30, 3885-3894 (2011).
2. Katoh, M. & Katoh, M. Human FOX gene family (Review). Int. J. Oncol. 25, 1495-1500 (2004).
3. Wijchers, P.J., Burbach, J.P. & Smidt, M.P. In control of biology: of mice, men and Foxes. Biochem. J. 397, 233-246 (2006).
4. Carroll, J.S. et al. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122, 33-43 (2005).
5. Cirillo, L.A. et al. Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol. Cell 9, 279-289 (2002).
6. INK4a activation during cellular senescence. EMBO J. 32, 858-873 (2013).
7. Zaret, K.S. & Carroll, J.S. Pioneer transcription factors: establishing competence for gene expression. Genes Dev. 25, 2227-2241 (2011).
8. Lupien, M. et al. FoxA1 translates epigenetic signatures into enhancer-driven lineage-specifc transcription. Cell 132, 958-970 (2008).
9. Hurtado, A., Holmes, K.A., Ross-Innes, C.S., Schmidt, D. & Carroll, J.S. FOXA1 is a key determinant of estrogen receptor function and endocrine response. Nat. Genet. 43, 27-33 (2011).
10. Wang, D. et al. Reprogramming transcription by distinct classes of enhancers functionally defned by eRNA. Nature 474, 390-394 (2011).
11. Wang, Q. et al. Androgen receptor regulates a distinct transcription program in androgen-independent prostate cancer. Cell 138, 245-256 (2009).
12. Kong, S.L., Li, G., Loh, S.L., Sung, W.K. & Liu, E.T. Cellular reprogramming by the conjoint action of ERα, FOXA1, and GATA3 to a ligand-inducible growth state. Mol. Syst. Biol. 7, 526 (2011).
13. Cirillo, L.A. et al. Binding of the winged-helix transcription factor HNF3 to a linker histone site on the nucleosome. EMBO J. 17, 244-254 (1998).
14. Cirillo, L.A. & Zaret, K.S. An early developmental transcription factor complex that is more stable on nucleosome core particles than on free DNA. Mol. Cell 4, 961-969 (1999).
15. Clark, K.L., Halay, E.D., Lai, E. & Burley, S.K. Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature 364, 412-420 (1993).
16. Sérandour, A.A. et al. Epigenetic switch involved in activation of pioneer factor FOXA1-dependent enhancers. Genome Res. 21, 555-565 (2011).
17. Bartke, T. et al. Nucleosome-interacting proteins regulated by DNA and histone methylation. Cell 143, 470-484 (2010).
18. Bernstein, B.E., Meissner, A. & Lander, E.S. The mammalian epigenome. Cell 128, 669-681 (2007).
19. Wu, H. & Zhang, Y. Reversing DNA methylation: mechanisms, genomics, and biological functions. Cell 156, 45-68 (2014).
20. Wu, S.C. & Zhang, Y. Active DNA demethylation: many roads lead to Rome. Nat. Rev. Mol. Cell Biol. 11, 607-620 (2010).
21. Zhu, J.K. Active DNA demethylation mediated by DNA glycosylases. Annu. Rev. Genet. 43, 143-166 (2009).
22. Conticello, S.G. The AID/APOBEC family of nucleic acid mutators. Genome Biol. 9, 229 (2008).
23. Cortellino, S. et al. Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146, 67-79 (2011).
24. Rai, K. et al. DNA demethylation in zebrafsh involves the coupling of a deaminase, a glycosylase, and Gadd45. Cell 135, 1201-1212 (2008).
25. Maiti, A. & Drohat, A.C. Thymine DNA glycosylase can rapidly excise 5-formylcytosine and 5-carboxylcytosine: potential implications for active demethylation of CpG sites. J. Biol. Chem. 286, 35334-35338 (2011).
26. Dalton, S.R. & Bellacosa, A. DNA demethylation by TDG. Epigenomics 4, 459-467 (2012).
27. Shen, L. et al. Genome-wide analysis reveals TET-and TDG-dependent 5-methylcytosine oxidation dynamics. Cell 153, 692-706 (2013).
28. Lloyd, R.S. The initiation of DNA base excision repair of dipyrimidine photoproducts. Prog. Nucleic Acid Res. Mol. Biol. 62, 155-175 (1999).
29. Schärer, O.D. & Jiricny, J. Recent progress in the biology, chemistry and structural biology of DNA glycosylases. BioEssays 23, 270-281 (2001).
30. Whitehouse, C.J. et al. XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair. Cell 104, 107-117 (2001).
31. Ma, Y. et al. A biochemically defned system for mammalian nonhomologous DNA end joining. Mol. Cell 16, 701-713 (2004).
32. Ma, Y., Pannicke, U., Schwarz, K. & Lieber, M.R. Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 108, 781-794 (2002).
33. Burma, S. & Chen, D.J. Role of DNA-PK in the cellular response to DNA double-strand breaks. DNA Repair (Amst.) 3, 909-918 (2004).
34. Kubota, Y. et al. Reconstitution of DNA base excision-repair with purifed human proteins: interaction between DNA polymerase β and the XRCC1 protein. EMBO J. 15, 6662-6670 (1996).
35. Caldecott, K.W., Aoufouchi, S., Johnson, P. & Shall, S. XRCC1 polypeptide interacts with DNA polymerase β and possibly poly (ADP-ribose) polymerase, and DNA ligase III is a novel molecular 'nick-sensor' in vitro. Nucleic Acids Res. 24, 4387-4394 (1996).
36. + into a nuclear signal. Genes Dev. 19, 1951-1967 (2005).
37. +-dependent modulation of chromatin structure and transcription by nucleosome binding properties of PARP-1. Cell 119, 803-814 (2004).
38. Krishnakumar, R. & Kraus, W.L. PARP-1 regulates chromatin structure and transcription through a KDM5B-dependent pathway. Mol. Cell 39, 736-749 (2010).
39. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
40. Ernst, J. & Kellis, M. ChromHMM: automating chromatin-state discovery and characterization. Nat. Methods 9, 215-216 (2012).
41. ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74 (2012).
42. Stadler, M.B. et al. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480, 490-495 (2011).
43. Serandour, A.A., Brown, G.D., Cohen, J.D. & Carroll, J.S. Development of an Illumina-based ChIP-exonuclease method provides insight into FoxA1-DNA binding properties. Genome Biol. 14, R147 (2013).
44. McLean, C.Y. et al. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495-501 (2010).
45. Menet, J.S., Pescatore, S. & Rosbash, M. CLOCK:BMAL1 is a pioneer-like transcription factor. Genes Dev. 28, 8-13 (2014).
46. Pihlajamaa, P. et al. Tissue-specifc pioneer factors associate with androgen receptor cistromes and transcription programs. EMBO J. 33, 312-326 (2014).
47. Sherwood, R.I. et al. Discovery of directional and nondirectional pioneer transcription factors by modeling DNase profle magnitude and shape. Nat. Biotechnol. 32, 171-178 (2014).
48. Malovannaya, A. et al. Analysis of the human endogenous coregulator complexome. Cell 145, 787-799 (2011).
49. Yu, M. et al. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell 149, 1368-1380 (2012).
50. Spruijt, C.G. et al. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell 152, 1146-1159 (2013).
51. Ooi, S.K. & Bestor, T.H. The colorful history of active DNA demethylation. Cell 133, 1145-1148 (2008).
52. Billaud, M. & Santoro, M. Is co-option a prevailing mechanism during cancer progression? Cancer Res. 71, 6572-6575 (2011).
53. Ziller, M.J. et al. Charting a dynamic DNA methylation landscape of the human genome. Nature 500, 477-481 (2013).
54. Vizcaíno, J.A. et al. 2016 update of the PRIDE database and its related tools. Nucleic Acids Res. 44, D1, D447-D456 (2016).
55. Johnson, W.E. et al. Model-based analysis of tiling-arrays for ChIP-chip. Proc. Natl. Acad. Sci. USA 103, 12457-12462 (2006).
56. Shang, Y., Hu, X., DiRenzo, J., Lazar, M.A. & Brown, M. Cofactor dynamics and suffciency in estrogen receptor-regulated transcription. Cell 103, 843-852 (2000).
57. Zhang, H. et al. Differential gene regulation by the SRC family of coactivators. Genes Dev. 18, 1753-1765 (2004).
58. Wang, Y. et al. LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 138, 660-672 (2009).
59. Frommer, M. et al. A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc. Natl. Acad. Sci. USA 89, 1827-1831 (1992).
60. Schmidt, D. et al. ChIP-seq: using high-throughput sequencing to discover protein-DNA interactions. Methods 48, 240-248 (2009).
61. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S.L. Ultrafast and memory-effcient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
62. Neph, S. et al. BEDOPS: high-performance genomic feature operations. Bioinformatics 28, 1919-1920 (2012).
63. Xi, Y. & Li, W. BSMAP: whole genome bisulfte sequence MAPping program. BMC Bioinformatics 10, 232 (2009).
64. Lister, R. et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462, 315-322 (2009).
65. Lawrence, M. et al. Software for computing and annotating genomic ranges. PLoS Comput. Biol. 9, e1003118 (2013).
66. R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2014).
67. Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer-Verlag, 2009).
68. Li, W. et al. Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature 498, 516-520 (2013).
69. Liu, Z. et al. Enhancer activation requires trans-recruitment of a mega transcription factor complex. Cell 159, 358-373 (2014).