Home LiteratureArticle Details
PMID: 23911320 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Cooperativity and rapid evolution of cobound transcription factors in closely related mammals.

Cell ·Vol. 154 ·No. 3 ·2013-08-01 ·Pages 530-40

Stefflova K, Thybert D, Wilson MD, Streeter I, Aleksic J, Karagianni P, Brazma A, Adams DJ, Talianidis I, Marioni JC, Flicek P, Odom DT

Abstract

To mechanistically characterize the microevolutionary processes active in altering transcription factor (TF) binding among closely related mammals, we compared the genome-wide binding of three tissue-specific TFs that control liver gene expression in six rodents. Despite an overall fast turnover of TF binding locations between species, we identified thousands of TF regions of highly constrained TF binding intensity. Although individual mutations in bound sequence motifs can influence TF binding, most binding differences occur in the absence of nearby sequence variations. Instead, combinatorial binding was found to be significant for genetic and evolutionary stability; cobound TFs tend to disappear in concert and were sensitive to genetic knockout of partner TFs. The large, qualitative differences in genomic regions bound between closely related mammals, when contrasted with the smaller, quantitative TF binding differences among Drosophila species, illustrate how genome structure and population genetics together shape regulatory evolution.

MeSH Terms
Animals Drosophila/genetics Evolution, Molecular Liver/metabolism Mice/classification,genetics,metabolism Mice, Inbred Strains Mice, Knockout Rats/genetics Transcription Factors/genetics,metabolism
Chemicals
Transcription Factors
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Stefflova Klara
Cancer Research UK Cambridge Institute, Li Ka Shing Centre, University of Cambridge, Cambridge CB2 0RE, UK.
Thybert David
Wilson Michael D
Streeter Ian
Aleksic Jelena
Karagianni Panagiota
Brazma Alvis
Adams David J
Talianidis Iannis
Marioni John C
Flicek Paul
Odom Duncan T
References (63)
63 references, click to expand
  1. Chromatin accessibility pre-determines glucocorticoid receptor binding patterns.
    Nat Genet. 2011 Mar;43(3):264-8 PMID: 21258342
  2. Transcription factor AP1 potentiates chromatin accessibility and glucocorticoid receptor binding.
    Mol Cell. 2011 Jul 8;43(1):145-55 PMID: 21726817
  3. Searching for phylogenetic trees under the frequency parsimony criterion: an approximation using generalized parsimony.
    Syst Biol. 1997 Mar;46(1):211-5 PMID: 11975353
  4. Collaborative competition mechanism for gene activation in vivo.
    Mol Cell Biol. 2003 Mar;23(5):1623-32 PMID: 12588982
  5. Does positive selection drive transcription factor binding site turnover? A test with Drosophila cis-regulatory modules.
    PLoS Genet. 2011 Apr;7(4):e1002053 PMID: 21572512
  6. Core transcriptional regulatory circuitry in human hepatocytes.
    Mol Syst Biol. 2006;2:2006.0017 PMID: 16738562
  7. Genome-wide and phase-specific DNA-binding rhythms of BMAL1 control circadian output functions in mouse liver.
    PLoS Biol. 2011 Feb;9(2):e1000595 PMID: 21364973
  8. ChIP-seq: using high-throughput sequencing to discover protein-DNA interactions.
    Methods. 2009 Jul;48(3):240-8 PMID: 19275939
  9. Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages.
    Cell. 2012 Jan 20;148(1-2):335-48 PMID: 22244452
  10. Temporal coordination of gene networks by Zelda in the early Drosophila embryo.
    PLoS Genet. 2011 Oct;7(10):e1002339 PMID: 22028675
  11. Performance and scalability of discriminative metrics for comparative gene identification in 12 Drosophila genomes.
    PLoS Comput Biol. 2008 Apr 18;4(4):e1000067 PMID: 18421375
  12. Plasticity and expanding complexity of the hepatic transcription factor network during liver development.
    Genes Dev. 2006 Aug 15;20(16):2293-305 PMID: 16912278
  13. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding.
    Science. 2010 May 21;328(5981):1036-40 PMID: 20378774
  14. Heritable individual-specific and allele-specific chromatin signatures in humans.
    Science. 2010 Apr 9;328(5975):235-9 PMID: 20299549
  15. Fast and accurate short read alignment with Burrows-Wheeler transform.
    Bioinformatics. 2009 Jul 15;25(14):1754-60 PMID: 19451168
  16. Evidence for redundancy but not trans factor-cis element coevolution in the regulation of Drosophila Yp genes.
    Genetics. 1999 Jun;152(2):605-16 PMID: 10353903
  17. Subspecific origin and haplotype diversity in the laboratory mouse.
    Nat Genet. 2011 May 29;43(7):648-55 PMID: 21623374
  18. Animal transcription networks as highly connected, quantitative continua.
    Dev Cell. 2011 Oct 18;21(4):611-26 PMID: 22014521
  19. Functional targets of the monogenic diabetes transcription factors HNF-1alpha and HNF-4alpha are highly conserved between mice and humans.
    Diabetes. 2009 May;58(5):1245-53 PMID: 19188435
  20. Developmental roles of 21 Drosophila transcription factors are determined by quantitative differences in binding to an overlapping set of thousands of genomic regions.
    Genome Biol. 2009;10(7):R80 PMID: 19627575
  21. Dindel: accurate indel calls from short-read data.
    Genome Res. 2011 Jun;21(6):961-73 PMID: 20980555
  22. The evolutionary significance of cis-regulatory mutations.
    Nat Rev Genet. 2007 Mar;8(3):206-16 PMID: 17304246
  23. Zelda binding in the early Drosophila melanogaster embryo marks regions subsequently activated at the maternal-to-zygotic transition.
    PLoS Genet. 2011 Oct;7(10):e1002266 PMID: 22028662
  24. Binding site turnover produces pervasive quantitative changes in transcription factor binding between closely related Drosophila species.
    PLoS Biol. 2010 Mar 23;8(3):e1000343 PMID: 20351773
  25. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data.
    Genome Res. 2010 Sep;20(9):1297-303 PMID: 20644199
  26. False positive peaks in ChIP-seq and other sequencing-based functional assays caused by unannotated high copy number regions.
    Bioinformatics. 2011 Aug 1;27(15):2144-6 PMID: 21690102
  27. Rapid evolution of cis-regulatory sequences via local point mutations.
    Mol Biol Evol. 2001 Sep;18(9):1764-70 PMID: 11504856
  28. Quantitative models of the mechanisms that control genome-wide patterns of transcription factor binding during early Drosophila development.
    PLoS Genet. 2011 Feb 03;7(2):e1001290 PMID: 21304941
  29. Common genetic variants account for differences in gene expression among ethnic groups.
    Nat Genet. 2007 Feb;39(2):226-31 PMID: 17206142
  30. MEME: discovering and analyzing DNA and protein sequence motifs.
    Nucleic Acids Res. 2006 Jul 1;34(Web Server issue):W369-73 PMID: 16845028
  31. High-throughput microbial population genomics using the Cortex variation assembler.
    Bioinformatics. 2013 Jan 15;29(2):275-6 PMID: 23172865
  32. TFBS: Computational framework for transcription factor binding site analysis.
    Bioinformatics. 2002 Aug;18(8):1135-6 PMID: 12176838
  33. A high-resolution map of human evolutionary constraint using 29 mammals.
    Nature. 2011 Oct 12;478(7370):476-82 PMID: 21993624
  34. Ubiquitous selective constraints in the Drosophila genome revealed by a genome-wide interspecies comparison.
    Genome Res. 2006 Jul;16(7):875-84 PMID: 16751341
  35. An integrated encyclopedia of DNA elements in the human genome.
    Nature. 2012 Sep 6;489(7414):57-74 PMID: 22955616
  36. DNA-binding specificities of human transcription factors.
    Cell. 2013 Jan 17;152(1-2):327-39 PMID: 23332764
  37. Nucleosome-mediated cooperativity between transcription factors.
    Proc Natl Acad Sci U S A. 2010 Dec 28;107(52):22534-9 PMID: 21149679
  38. Master transcription factors and mediator establish super-enhancers at key cell identity genes.
    Cell. 2013 Apr 11;153(2):307-19 PMID: 23582322
  39. Multiple regulatory elements in the murine stromelysin-3 promoter. Evidence for direct control by CCAAT/enhancer-binding protein beta and thyroid and retinoid receptors.
    J Biol Chem. 2000 Dec 22;275(51):39981-90 PMID: 10993903
  40. Effects of sequence variation on differential allelic transcription factor occupancy and gene expression.
    Genome Res. 2012 May;22(5):860-9 PMID: 22300769
  41. Distribution and intensity of constraint in mammalian genomic sequence.
    Genome Res. 2005 Jul;15(7):901-13 PMID: 15965027
  42. Combinatorial binding predicts spatio-temporal cis-regulatory activity.
    Nature. 2009 Nov 5;462(7269):65-70 PMID: 19890324
  43. The general affinity of lac repressor for E. coli DNA: implications for gene regulation in procaryotes and eucaryotes.
    Cell. 1975 Feb;4(2):107-11 PMID: 1092468
  44. GREAT improves functional interpretation of cis-regulatory regions.
    Nat Biotechnol. 2010 May;28(5):495-501 PMID: 20436461
  45. High conservation of transcription factor binding and evidence for combinatorial regulation across six Drosophila species.
    Nat Genet. 2011 May;43(5):414-20 PMID: 21478888
  46. Hepatocyte nuclear factor 4alpha (nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis.
    Mol Cell Biol. 2001 Feb;21(4):1393-403 PMID: 11158324
  47. Transposable elements have rewired the core regulatory network of human embryonic stem cells.
    Nat Genet. 2010 Jul;42(7):631-4 PMID: 20526341
  48. Disruption of hepatic C/EBPalpha results in impaired glucose tolerance and age-dependent hepatosteatosis.
    J Biol Chem. 2004 Oct 22;279(43):44740-8 PMID: 15292250
  49. Mitogen-activated protein kinase-mediated disruption of enhancer-promoter communication inhibits hepatocyte nuclear factor 4alpha expression.
    Mol Cell Biol. 2006 Oct;26(19):7017-29 PMID: 16980607
  50. Evolution of genome content: population dynamics of transposable elements in flies and humans.
    Methods Mol Biol. 2012;855:361-83 PMID: 22407716
  51. Genome sequence of the Brown Norway rat yields insights into mammalian evolution.
    Nature. 2004 Apr 1;428(6982):493-521 PMID: 15057822
  52. Variation in transcription factor binding among humans.
    Science. 2010 Apr 9;328(5975):232-5 PMID: 20299548
  53. What fraction of the human genome is functional?
    Genome Res. 2011 Nov;21(11):1769-76 PMID: 21875934
  54. Cohesin regulates tissue-specific expression by stabilizing highly occupied cis-regulatory modules.
    Genome Res. 2012 Nov;22(11):2163-75 PMID: 22780989
  55. DNA regions bound at low occupancy by transcription factors do not drive patterned reporter gene expression in Drosophila.
    Proc Natl Acad Sci U S A. 2012 Dec 26;109(52):21330-5 PMID: 23236164
  56. Bias in phylogenetic estimation and its relevance to the choice between parsimony and likelihood methods.
    Syst Biol. 2001 Aug;50(4):525-39 PMID: 12116651
  57. HOT regions function as patterned developmental enhancers and have a distinct cis-regulatory signature.
    Genes Dev. 2012 May 1;26(9):908-13 PMID: 22499593
  58. The role of chromatin accessibility in directing the widespread, overlapping patterns of Drosophila transcription factor binding.
    Genome Biol. 2011;12(4):R34 PMID: 21473766
  59. Analysis of variation at transcription factor binding sites in Drosophila and humans.
    Genome Biol. 2012 Sep 28;13(9):R49 PMID: 22950968
  60. Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures.
    Nature. 2007 Nov 8;450(7167):219-32 PMID: 17994088
  61. A tamoxifen-inducible chimeric Cre recombinase specifically effective in the fetal and adult mouse liver.
    Hepatology. 2002 May;35(5):1072-81 PMID: 11981757
  62. Mouse genomic variation and its effect on phenotypes and gene regulation.
    Nature. 2011 Sep 14;477(7364):289-94 PMID: 21921910
  63. Initial sequencing and comparative analysis of the mouse genome.
    Nature. 2002 Dec 5;420(6915):520-62 PMID: 12466850
Article Info
Journal
Cell
Abbr.
Cell
ISSN
1097-4172
DOI
10.1016/j.cell.2013.07.007
Published
2013-08-01
Pages
530-40
Language
English
Region
United States
NLM ID
0413066
PMCID
PMC3732390
Subset
IM
Grants
European Research Council · 202218 · International
Cancer Research UK · A10185 · United Kingdom
Cancer Research UK · 13031 · United Kingdom
Wellcome Trust · 095908 · United Kingdom
Cancer Research UK · 15603 · United Kingdom
External Links
PubMed source DOI: 10.1016/j.cell.2013.07.007 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2