Gene expression differences among primates are associated with changes in a histone epigenetic modification

Genetics

Volumn 187, Issue 4, 2011, Pages 1225-1234

  Cain, Carolyn E ^a   Blekhman, Ran ^a,b,c   Marioni, John C ^a,d   Gilad, Yoav ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE;

ANIMAL CELL; ARTICLE; CHIMPANZEE; CONTROLLED STUDY; EPIGENETICS; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC CONSERVATION; GENETIC DIFFERENCE; HISTONE MODIFICATION; HUMAN; HUMAN CELL; LYMPHOBLASTOID CELL LINE; NONHUMAN; PRIMATE; PRIORITY JOURNAL; RHESUS MONKEY; SPECIES COMPARISON;

ANIMALS; CELL LINE; CHROMATIN IMMUNOPRECIPITATION; DNA METHYLATION; EPIGENESIS, GENETIC; EPIGENOMICS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC VARIATION; HISTONES; HUMANS; PRIMATES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION INITIATION SITE;

MACACA MULATTA; PAN; PRIMATES;

EID: 79955403252     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.110.126177     Document Type: Article

References (73)

1. Akey, J.M., S. Biswas, J.T. Leek and J.D. Storey, 2007 On the design and analysis of gene expression studies in human populations. Nat. Genet. 39: 807-808, author reply 808-809.
2. Alberts, B., A. Johnson, J. Lewis, M. Raff, K. Roberts et al., 2002 Molecular Biology of the Cell. Garland Science, New York.
3. Ashburner, M., C.A. Ball, J.A. Blake, D. Botstein, H. Butler et al., 2000 Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25: 25-29.
4. Babbitt, C.C., O. Fedrigo, A.D. Pfefferle, A.P. Boyle, J.E. Horvath et al., 2010a Both noncoding and protein-coding RNAs contribute to gene expression evolution in the primate brain. Genome Biol. Evol. 2: 67-79.
5. Babbitt, C.C., J.S. Silverman, R. Haygood, J.M. Reininga, M.V. Rockman et al., 2010b Multiple functional variants in cis modulate PDYN expression. Mol. Biol. Evol. 27: 465-479.
6. Backes, C., A. Keller, J. Kuentzer, B. Kneissl, N. Comtesse et al., 2007 GeneTrail-advanced gene set enrichment analysis. Nucleic Acids Res. 35: W186-W192.
7. Barreiro, L.B., and L. Quintana-Murci, 2010 From evolutionary genetics to human immunology: how selection shapes host defence genes. Nat. Rev. Genet. 11: 17-30.
8. Barski, A., S. Cuddapah, K. Cui, T.Y. Roh, D.E. Schones et al., 2007 High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837.
9. Bernstein, B.E., M. Kamal, K. Lindblad-Toh, S. Bekiranov, D.K. Bailey et al., 2005 Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120: 169-181.
10. Blekhman, R., A. Oshlack, A.E. Chabot, G.K. Smyth and Y. Gilad, 2008 Gene regulation in primates evolves under tissue-specific selection pressures. PLoS Genet. 4: e1000271.
11. Blekhman, R., A. Oshlack and Y. Gilad, 2009 Segmental duplications contribute to gene expression differences between humans and chimpanzees. Genetics 182: 627-630.
12. Blekhman, R., J. Marioni, P. Zumbo, M. Stephens and Y. Gilad, 2010 Sex-specific and lineage-specific alternative splicing in primates. Genome Res. 20: 180-189.
13. Bullaughey, K., C.I. Chavarria, G. Coop and Y. Gilad, 2009 Expression quantitative trait loci detected in cell lines are often present in primary tissues. Hum. Mol. Genet. 18: 4296-4303.
14. Busslinger, M., 2004 Transcriptional control of early B cell development. Annu. Rev. Immunol. 22: 55-79.
15. Cáceres, M., J. Lachuer, M.A. Zapala, J.C. Redmond, L. Kudo et al., 2003 Elevated gene expression levels distinguish human from non-human primate brains. Proc. Natl. Acad. Sci. USA 100: 13030-13035.
16. Carter, K.L., E. Cahir-McFarland and E. Kieff, 2002 Epstein- Barr virus-induced changes in B-lymphocyte gene expression. J. Virol. 76: 10427-10436.
17. Chabot, A., R.A. Shrit, R. Blekhman and Y. Gilad, 2007 Using reporter gene assays to identify cis regulatory differences between humans and chimpanzees. Genetics 176: 2069-2076.
18. Cheung, V.G., R.S. Spielman, K.G. Ewens, T.M. Weber, M. Morley et al., 2005 Mapping determinants of human gene expression by regional and genome-wide association. Nature 437: 365-1369.
19. Choy, E., R. Yelensky, S. Bonakdar, R.M. Plenge, R. Saxena et al., 2008 Genetic analysis of human traits in vitro: drug response and gene expression in lymphoblastoid cell lines. PLoS Genet. 4: e1000287.
20. Dimas, A. S., S. Deutsch, B. E. Stranger, S. B. Montgomery, C. Borel et al., 2009 Common regulatory variation impacts gene expression in a cell type-dependent manner. Science 325: 1246-1250.
21. Ding, J., J. E. Gudjonsson, L. Liang, P. E. Stuart, Y. Li et al., 2010 Gene expression in skin and lymphoblastoid cells: refined statistical method reveals extensive overlap in cis-eQTL signals. Am. J. Hum. Genet. 87: 779-789.
22. Dixon, A. L., L. Liang, M. F. Moffatt, W. Chen, S. Heath et al., 2007 A genome-wide association study of global gene expression. Nat. Genet. 39: 1202-1207.
23. Enard, W., P. Khaitovich, J. Klose, S. Zollner, F. Heissig et al., 2002 Intra- and interspecific variation in primate gene expression patterns. Science 296: 340-343.
24. Enard, W., A. Fassbender, F. Model, P. Adorjan, S. Paabo et al., 2004 Differences in DNA methylation patterns between humans and chimpanzees. Curr. Biol. 14: R148-R149.
25. Farcas, R., E. Schneider, K. Frauenknecht, I. Kondova, R. Bontrop et al., 2009 Differences in DNA methylation patterns and expression of the CCRK gene in human and nonhuman primate cortices. Mol. Biol. Evol. 26: 1379-1389.
26. Frazer, K. A., D. G. Ballinger, D. R. Cox, D. A. Hinds, L. L. Stuve et al., 2007 A second generation human haplotype map of over 3.1 million SNPs. Nature 449: 851-861.
27. Gama-Sosa, M. A., R. M. Midgett, V. A. Slagel, S. Githens, K. C. Kuo et al., 1983 Tissue-specific differences in DNA methylation in various mammals. Biochim. Biophys. Acta 740: 212-219.
28. Ge, B., D. K. Pokholok, T. Kwan, E. Grundberg, L. Morcos et al., 2009 Global patterns of cis variation in human cells revealed by high-density allelic expression analysis. Nat. Genet. 41: 1216-1222.
29. Gerber, M., and A. Shilatifard, 2003 Transcriptional elongation by RNA polymerase II and histone methylation. J. Biol. Chem. 278: 26303-26306.
30. Gilad, Y., A. Oshlack, G. K. Smyth, T. P. Speed and K. P. White, 2006 Expression profiling in primates reveals a rapid evolution of human transcription factors. Nature 440: 242-245.
31. Hampsey, M., and D. Reinberg, 2003 Tails of intrigue: phosphorylation of RNA polymerase II mediates histone methylation. Cell 113: 429-432.
32. Hannula, K., M. Lipsanen-Nyman, S. W. Scherer, C. Holmberg, P. Hoglund et al., 2001 Maternal and paternal chromosomes 7 show differential methylation of many genes in lymphoblast DNA. Genomics 73: 1-9.
33. Heintzman, N. D., R. K. Stuart, G. Hon, Y. Fu, C. W. Ching et al., 2007 Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 39: 311-318.
34. Karaman, M. W., M. L. Houck, L. G. Chemnick, S. Nagpal, D. Chawannakul et al., 2003 Comparative analysis of geneexpression patterns in human and African great ape cultured fibroblasts. Genome Res. 13: 1619-1630.
35. Karlic, R., H. R. Chung, J. Lasserre, K. Vlahovicek and M. Vingron, 2010 Histone modification levels are predictive for gene expression. Proc. Natl. Acad. Sci. USA 107: 2926-2931.
36. Khaitovich, P., B. Muetzel, X. She, M. Lachmann, I. Hellmann et al., 2004 Regional patterns of gene expression in human and chimpanzee brains. Genome Res. 14: 1462-1473.
37. Khaitovich, P., I. Hellmann, W. Enard, K. Nowick, M. Leinweber et al., 2005 Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science 309: 1850-1854.
38. Khaitovich, P., W. Enard, M. Lachmann and S. Paabo, 2006 Evolution of primate gene expression. Nat. Rev. Genet. 7: 693-702.
39. Kouzarides, T., 2007 Chromatin modifications and their function. Cell 128: 693-705.
40. Li, H., S. Ilin, W. Wang, E. M. Duncan, J. Wysocka et al., 2006 Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF. Nature 442: 91-95.
41. Li, H., J. Ruan and R. Durbin, 2008 Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res. 18: 1851-1858.
42. Loisel, D. A., M. V. Rockman, G. A. Wray, J. Altmann and S. C. Alberts, 2006 Ancient polymorphism and functional variation in the primate MHC-DQA1 59 cis-regulatory region. Proc. Natl. Acad. Sci. USA 103: 16331-16336.
43. Marioni, J. C., C. E. Mason, S. M. Mane, M. Stephens and Y. Gilad, 2008 RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res. 18: 1509-1517.
44. McManus, C. J., J. D. Coolon, M. O. Duff, J. Eipper-Mains, B. R. Graveley et al., 2010 Regulatory divergence in Drosophila revealed by mRNA-seq. Genome Res. 20: 816-825.
45. Moffatt, M. F., M. Kabesch, L. Liang, A. L. Dixon, D. Strachan et al., 2007 Genetic variants regulating ORMDL3 expression contribute to the risk of childhood asthma. Nature 448: 470-473.
46. Monks, S. A., A. Leonardson, H. Zhu, P. Cundiff, P. Pietrusiak et al., 2004 Genetic inheritance of gene expression in human cell lines. Am. J. Hum. Genet. 75: 1094-1105.
47. Morley, M., C. M. Molony, T. M. Weber, J. L. Devlin, K. G. Ewens et al., 2004 Genetic analysis of genome-wide variation in human gene expression. Nature 430: 743-747.
48. Ng, H. H., F. Robert, R. A. Young and K. Struhl, 2003 Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol. Cell 11: 709-719.
49. Nishioka, K., S. Chuikov, K. Sarma, H. Erdjument-Bromage, C. D. Allis et al., 2002 Set9, a novel histone H3 methyltransferase that facilitates transcription by precluding histone tail modifications required for heterochromatin formation. Genes Dev. 16: 479-489.
50. Nislow, C., E. Ray and L. Pillus, 1997 A yeast member of the trithorax family, functions in transcriptional silencing and diverse cellular processes. Mol. Biol. Cell 8: 2421-2436.
51. Odom, D. T., R. D. Dowell, E. S. Jacobsen, W. Gordon, T. W. Danford et al., 2007 Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nat. Genet. 39: 730-732.
52. Pokholok, D. K., C. T. Harbison, S. Levine, M. Cole, N. M. Hannett et al., 2005 Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122: 517-527.
53. Pollard, K. S., S. R. Salama, N. Lambert, M.A. Lambot, S. Coppens et al., 2006 An RNA gene expressed during cortical development evolved rapidly in humans. Nature 443: 167-172.
54. Prabhakar, S., A. Visel, J. A. Akiyama, M. Shoukry, K. D. Lewis et al., 2008 Human-specific gain of function in a developmental enhancer. Science 321: 1346-1350.
55. Redon, R., S. Ishikawa, K. R. Fitch, L. Feuk, G. H. Perry et al., 2006 Global variation in copy number in the human genome. Nature 444: 444-454.
56. Rockman, M. V., M. W. Hahn, N. Soranzo, F. Zimprich, D. B. Goldstein et al., 2005 Ancient and recent positive selection transformed opioid cis-regulation in humans. PLoS Biol. 3: e387.
57. Roh, T. Y., G. Wei, C. M. Farrell and K. Zhao, 2007 Genome-wide prediction of conserved and nonconserved enhancers by histone acetylation patterns. Genome Res. 17: 74-81.
58. Ruthenburg, A. J., C. D. Allis and J. Wysocka, 2007 Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol. Cell 25: 15-30.
59. Santos-Rosa, H., R. Schneider, A. J. Bannister, J. Sherriff, B. E. Bernstein et al., 2002 Active genes are tri-methylated at K4 of histone H3. Nature 419: 407-411.
60. Schneider, R., A. J. Bannister, F. A. Myers, A. W. Thorne, C. Crane-Robinson et al., 2004 Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat. Cell Biol. 6: 73-77.
61. Schübeler, D., D. M. MacAlpine, D. Scalzo, C. Wirbelauer, C. Kooperberg et al., 2004 The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 18: 1263-1271.
62. Stranger, B. E., M. S. Forrest, A. G. Clark, M. J. Minichiello, S. Deutsch et al., 2005 Genome-wide associations of gene expression variation in humans. PLoS Genet. 1: e78.
63. Stranger, B. E., A. C. Nica, M. S. Forrest, A. Dimas, C. P. Bird et al., 2007 Population genomics of human gene expression. Nat. Genet. 39: 1217-1224.
64. Verlaan, D. J., B. Ge, E. Grundberg, R. Hoberman, K. C. Lam et al., 2009 Targeted screening of cis-regulatory variation in human haplotypes. Genome Res. 19: 118-127.
65. Veyrieras, J. B., S. Kudaravalli, S. Y. Kim, E. T. Dermitzakis, Y. Gilad et al., 2008 High-resolution mapping of expression- QTLs yields insight into human gene regulation. PLoS Genet. 4: e1000214.
66. Wang, P., C. Lin, E. R. Smith, H. Guo, B. W. Sanderson et al., 2009 Global analysis of H3K4 methylation defines MLL family member targets and points to a role for MLL1-mediated H3K4 methylation in the regulation of transcriptional initiation by RNA polymerase II. Mol. Cell. Biol. 29: 6074-6085.
67. Warner, L. R., C. C. Babbitt, A. E. Primus, T. F. Severson, R. Haygood et al., 2009 Functional consequences of genetic variation in primates on tyrosine hydroxylase (TH) expression in vitro. Brain Res. 1288: 1-8.
68. Wilson, M. D., N. L. Barbosa-Morais, D. Schmidt, C. M. Conboy, L. Vanes et al., 2008 Species-specific transcription in mice carrying human chromosome 21. Science 322: 434-438.
69. Wysocka, J., T. Swigut, H. Xiao, T. A. Milne, S. Y. Kwon et al., 2006 A PHD finger of NURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 442: 86-90.
70. Zegerman, P., B. Canas, D. Pappin and T. Kouzarides, 2002 Histone H3 lysine 4 methylation disrupts binding of nucleosome remodeling and deacetylase (NuRD) repressor complex. J. Biol. Chem. 277: 11621-11624.
71. Zeller, T., P. Wild, S. Szymczak, M. Rotival, A. Schillert et al., 2010 Genetics and beyond-the transcriptome of human monocytes and disease susceptibility. PLoS One 5: e10693.
72. Zhang, X., Y. V. Bernatavichute, S. Cokus, M. Pellegrini and S. E. Jacobsen, 2009 Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol. 10: R62.
73. Zhang, Y., T. Liu, C. A. Meyer, J. Eeckhoute, D. S. Johnson et al., 2008 Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9: R137.