Home LiteratureArticle Details
PMID: 26807951 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Epigenomic annotation of gene regulatory alterations during evolution of the primate brain.

Nature neuroscience ·Vol. 19 ·No. 3 ·2016-03-00 ·Pages 494-503

Vermunt MW, Tan SC, Castelijns B, Geeven G, Reinink P, de Bruijn E, Kondova I, Persengiev S, Netherlands Brain Bank, Bontrop R, Cuppen E, de Laat W, Creyghton MP

Abstract

Although genome sequencing has identified numerous noncoding alterations between primate species, which of those are regulatory and potentially relevant to the evolution of the human brain is unclear. Here we annotated cis-regulatory elements (CREs) in the human, rhesus macaque and chimpanzee genomes using chromatin immunoprecipitation followed by sequencing (ChIP-seq) in different anatomical regions of the adult brain. We found high similarity in the genomic positioning of rhesus macaque and human CREs, suggesting that the majority of these elements were already present in a common ancestor 25 million years ago. Most of the observed regulatory changes between humans and rhesus macaques occurred before the ancestral separation of humans and chimpanzees, leaving a modest set of regulatory elements with predicted human specificity. Our data refine previous predictions and hypotheses on the consequences of genomic changes between primate species and allow the identification of regulatory alterations relevant to the evolution of the brain.

MeSH Terms
Animals Brain/metabolism Chromatin Immunoprecipitation Epigenesis, Genetic/genetics Epigenomics Evolution, Molecular Humans Macaca mulatta/genetics Pan troglodytes/genetics Regulatory Elements, Transcriptional/genetics
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Vermunt Marit W
Hubrecht Institute-KNAW and University Medical Center Utrecht, Utrecht, the Netherlands.
Tan Sander C ORCID
Hubrecht Institute-KNAW and University Medical Center Utrecht, Utrecht, the Netherlands.
Castelijns Bas
Hubrecht Institute-KNAW and University Medical Center Utrecht, Utrecht, the Netherlands.
Geeven Geert
Hubrecht Institute-KNAW and University Medical Center Utrecht, Utrecht, the Netherlands.
Reinink Peter
Hubrecht Institute-KNAW and University Medical Center Utrecht, Utrecht, the Netherlands.
de Bruijn Ewart
Hubrecht Institute-KNAW and University Medical Center Utrecht, Utrecht, the Netherlands.
Kondova Ivanela
Biomedical Primate Research Center, Rijswijk, the Netherlands.
Persengiev Stephan
Biomedical Primate Research Center, Rijswijk, the Netherlands.
Netherlands Brain Bank
Bontrop Ronald
Biomedical Primate Research Center, Rijswijk, the Netherlands.
Cuppen Edwin ORCID
Hubrecht Institute-KNAW and University Medical Center Utrecht, Utrecht, the Netherlands.
de Laat Wouter
Hubrecht Institute-KNAW and University Medical Center Utrecht, Utrecht, the Netherlands.
Creyghton Menno P
Hubrecht Institute-KNAW and University Medical Center Utrecht, Utrecht, the Netherlands.
References (63)
63 references, click to expand
  1. Tissue-specific analysis of chromatin state identifies temporal signatures of enhancer activity during embryonic development.
    Nat Genet. 2012 Jan 08;44(2):148-56 PMID: 22231485
  2. A high-resolution map of human evolutionary constraint using 29 mammals.
    Nature. 2011 Oct 12;478(7370):476-82 PMID: 21993624
  3. Integrative analysis of 111 reference human epigenomes.
    Nature. 2015 Feb 19;518(7539):317-30 PMID: 25693563
  4. The evolutionary significance of cis-regulatory mutations.
    Nat Rev Genet. 2007 Mar;8(3):206-16 PMID: 17304246
  5. Discovery and characterization of chromatin states for systematic annotation of the human genome.
    Nat Biotechnol. 2010 Aug;28(8):817-25 PMID: 20657582
  6. Large-scale identification of coregulated enhancer networks in the adult human brain.
    Cell Rep. 2014 Oct 23;9(2):767-79 PMID: 25373911
  7. MYC and transcription elongation.
    Cold Spring Harb Perspect Med. 2014 Jan 01;4(1):a020990 PMID: 24384817
  8. Combinatorial patterns of histone acetylations and methylations in the human genome.
    Nat Genet. 2008 Jul;40(7):897-903 PMID: 18552846
  9. Fast gapped-read alignment with Bowtie 2.
    Nat Methods. 2012 Mar 04;9(4):357-9 PMID: 22388286
  10. Transcriptional amplification in tumor cells with elevated c-Myc.
    Cell. 2012 Sep 28;151(1):56-67 PMID: 23021215
  11. Contrasts between adaptive coding and noncoding changes during human evolution.
    Proc Natl Acad Sci U S A. 2010 Apr 27;107(17):7853-7 PMID: 20385805
  12. Human-chimpanzee differences in a FZD8 enhancer alter cell-cycle dynamics in the developing neocortex.
    Curr Biol. 2015 Mar 16;25(6):772-9 PMID: 25702574
  13. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence.
    Nat Rev Genet. 2011 Dec 06;13(1):59-69 PMID: 22143240
  14. Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain.
    J Comp Neurol. 2009 Apr 10;513(5):532-41 PMID: 19226510
  15. Sepsid even-skipped enhancers are functionally conserved in Drosophila despite lack of sequence conservation.
    PLoS Genet. 2008 Jun 27;4(6):e1000106 PMID: 18584029
  16. The NIH Roadmap Epigenomics Mapping Consortium.
    Nat Biotechnol. 2010 Oct;28(10):1045-8 PMID: 20944595
  17. Evolution of transcription factor binding in metazoans - mechanisms and functional implications.
    Nat Rev Genet. 2014 Apr;15(4):221-33 PMID: 24590227
  18. Enhancer evolution across 20 mammalian species.
    Cell. 2015 Jan 29;160(3):554-66 PMID: 25635462
  19. Large-scale imputation of epigenomic datasets for systematic annotation of diverse human tissues.
    Nat Biotechnol. 2015 Apr;33(4):364-76 PMID: 25690853
  20. Evolution at two levels in humans and chimpanzees.
    Science. 1975 Apr 11;188(4184):107-16 PMID: 1090005
  21. Java Treeview--extensible visualization of microarray data.
    Bioinformatics. 2004 Nov 22;20(17):3246-8 PMID: 15180930
  22. Histone H3K27ac separates active from poised enhancers and predicts developmental state.
    Proc Natl Acad Sci U S A. 2010 Dec 14;107(50):21931-6 PMID: 21106759
  23. A quantitative study of the human cerebellum with unbiased stereological techniques.
    J Comp Neurol. 1992 Dec 22;326(4):549-60 PMID: 1484123
  24. Mouse regulatory DNA landscapes reveal global principles of cis-regulatory evolution.
    Science. 2014 Nov 21;346(6212):1007-12 PMID: 25411453
  25. The Sequence Alignment/Map format and SAMtools.
    Bioinformatics. 2009 Aug 15;25(16):2078-9 PMID: 19505943
  26. ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia.
    Genome Res. 2012 Sep;22(9):1813-31 PMID: 22955991
  27. Shadow enhancers foster robustness of Drosophila gastrulation.
    Curr Biol. 2010 Sep 14;20(17):1562-7 PMID: 20797865
  28. GREAT improves functional interpretation of cis-regulatory regions.
    Nat Biotechnol. 2010 May;28(5):495-501 PMID: 20436461
  29. Model-based analysis of ChIP-Seq (MACS).
    Genome Biol. 2008;9(9):R137 PMID: 18798982
  30. Epigenomic enhancer profiling defines a signature of colon cancer.
    Science. 2012 May 11;336(6082):736-9 PMID: 22499810
  31. Comparative primate genomics: emerging patterns of genome content and dynamics.
    Nat Rev Genet. 2014 May;15(5):347-59 PMID: 24709753
  32. Single-cell chromatin accessibility reveals principles of regulatory variation.
    Nature. 2015 Jul 23;523(7561):486-90 PMID: 26083756
  33. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding.
    Science. 2010 May 21;328(5981):1036-40 PMID: 20378774
  34. BEDTools: a flexible suite of utilities for comparing genomic features.
    Bioinformatics. 2010 Mar 15;26(6):841-2 PMID: 20110278
  35. Initial sequence of the chimpanzee genome and comparison with the human genome.
    Nature. 2005 Sep 1;437(7055):69-87 PMID: 16136131
  36. Accelerated evolution of conserved noncoding sequences in humans.
    Science. 2006 Nov 3;314(5800):786 PMID: 17082449
  37. Quantitative genome-wide enhancer activity maps for five Drosophila species show functional enhancer conservation and turnover during cis-regulatory evolution.
    Nat Genet. 2014 Jul;46(7):685-92 PMID: 24908250
  38. Evolution of transcriptional enhancers and animal diversity.
    Philos Trans R Soc Lond B Biol Sci. 2013 Nov 11;368(1632):20130017 PMID: 24218630
  39. Transcriptional enhancers: from properties to genome-wide predictions.
    Nat Rev Genet. 2014 Apr;15(4):272-86 PMID: 24614317
  40. A computational pipeline for comparative ChIP-seq analyses.
    Nat Protoc. 2011 Dec 15;7(1):45-61 PMID: 22179591
  41. Determining long-range chromatin interactions for selected genomic sites using 4C-seq technology: from fixation to computation.
    Methods. 2012 Nov;58(3):221-30 PMID: 22609568
  42. Enhancer divergence and cis-regulatory evolution in the human and chimp neural crest.
    Cell. 2015 Sep 24;163(1):68-83 PMID: 26365491
  43. 4C technology: protocols and data analysis.
    Methods Enzymol. 2012;513:89-112 PMID: 22929766
  44. Human-specific transcriptional networks in the brain.
    Neuron. 2012 Aug 23;75(4):601-17 PMID: 22920253
  45. The evolution of gene expression levels in mammalian organs.
    Nature. 2011 Oct 19;478(7369):343-8 PMID: 22012392
  46. A molecular timescale for vertebrate evolution.
    Nature. 1998 Apr 30;392(6679):917-20 PMID: 9582070
  47. Shadow enhancers as a source of evolutionary novelty.
    Science. 2008 Sep 5;321(5894):1314 PMID: 18772429
  48. A unique chromatin signature uncovers early developmental enhancers in humans.
    Nature. 2011 Feb 10;470(7333):279-83 PMID: 21160473
  49. Evolution of the neocortex: a perspective from developmental biology.
    Nat Rev Neurosci. 2009 Oct;10(10):724-35 PMID: 19763105
  50. Multiplex single cell profiling of chromatin accessibility by combinatorial cellular indexing.
    Science. 2015 May 22;348(6237):910-4 PMID: 25953818
  51. Cortical evolution: judge the brain by its cover.
    Neuron. 2013 Oct 30;80(3):633-47 PMID: 24183016
  52. Evolutionary and biomedical insights from the rhesus macaque genome.
    Science. 2007 Apr 13;316(5822):222-34 PMID: 17431167
  53. ChromHMM: automating chromatin-state discovery and characterization.
    Nat Methods. 2012 Feb 28;9(3):215-6 PMID: 22373907
  54. Evolution of genetic and genomic features unique to the human lineage.
    Nat Rev Genet. 2012 Dec;13(12):853-66 PMID: 23154808
  55. Conservation of RET regulatory function from human to zebrafish without sequence similarity.
    Science. 2006 Apr 14;312(5771):276-9 PMID: 16556802
  56. Cadm1-expressing synapses on Purkinje cell dendrites are involved in mouse ultrasonic vocalization activity.
    PLoS One. 2012;7(1):e30151 PMID: 22272290
  57. Mapping accessible chromatin regions using Sono-Seq.
    Proc Natl Acad Sci U S A. 2009 Sep 1;106(35):14926-31 PMID: 19706456
  58. Fast-evolving noncoding sequences in the human genome.
    Genome Biol. 2007;8(6):R118 PMID: 17578567
  59. Functional and mechanistic diversity of distal transcription enhancers.
    Cell. 2011 Feb 4;144(3):327-39 PMID: 21295696
  60. The evolution of lineage-specific regulatory activities in the human embryonic limb.
    Cell. 2013 Jul 3;154(1):185-96 PMID: 23827682
  61. Evolutionary genomics. Evolutionary changes in promoter and enhancer activity during human corticogenesis.
    Science. 2015 Mar 6;347(6226):1155-9 PMID: 25745175
  62. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.
    Genome Biol. 2014;15(12):550 PMID: 25516281
  63. A high-resolution enhancer atlas of the developing telencephalon.
    Cell. 2013 Feb 14;152(4):895-908 PMID: 23375746
Article Info
Journal
Nature neuroscience
Abbr.
Nat Neurosci
ISSN
1546-1726
Published
2016-03-00
Epub
2016-00-25
Pages
494-503
Language
English
Region
United States
NLM ID
9809671
Subset
IM
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]