Extensive evolutionary changes in regulatory element activity during human origins are associated with altered gene expression and positive selection

PLoS Genetics

Volumn 8, Issue 6, 2012, Pages

  Shibata, Yoichiro ^a   Sheffield, Nathan C ^a   Fedrigo, Olivier ^a   Babbitt, Courtney C ^a   Wortham, Matthew ^a   Tewari, Alok K ^a   London, Darin ^a   Song, Lingyun ^a   Lee, Bum Kyu ^b   Iyer, Vishwanath R ^b   Parker, Stephen C J ^c   Margulies, Elliott H ^c   Wray, Gregory A ^a   Furey, Terrence S ^d,e   Crawford, Gregory E ^a,f  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF NORTH CAROLINA   (United States)

^f DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE; DEOXYRIBONUCLEASE I; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BINDING SITE; BIOGENESIS; CELL LINEAGE; CELL SPECIFICITY; CHIMPANZEE; CONTROLLED STUDY; DNA BINDING; DNA LIBRARY; DNA METABOLISM; FIBROBLAST; GENE EXPRESSION REGULATION; GENE LOSS; GENE MAPPING; GENETIC ASSOCIATION; GENETIC CONSERVATION; GENETIC SELECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; MOLECULAR EVOLUTION; NONHUMAN; PHENOTYPE; PROMOTER REGION; REGULATORY SEQUENCE; SEQUENCE ANALYSIS; SPECIES DIFFERENTIATION; TRANSCRIPTION REGULATION; ANIMAL; CELL LINE; CHROMATIN; GENETIC TRANSCRIPTION; GENETICS; HUMAN GENOME; MUTATION; NUCLEOTIDE MOTIF; PRIMATE; SPECIES DIFFERENCE;

PAN; PRIMATES;

ANIMALS; BINDING SITES; CELL LINE; CHROMATIN; DEOXYRIBONUCLEASE I; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; GENOME, HUMAN; HUMANS; MUTATION; NUCLEOTIDE MOTIFS; PHENOTYPE; PRIMATES; REGULATORY SEQUENCES, NUCLEIC ACID; SELECTION, GENETIC; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84864073098     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002789     Document Type: Article

References (71)

1. Robertson M, (2010) The evolution of gene regulation, the RNA universe, and the vexed questions of artefact and noise. BMC Biol 8: 97.
2. Olson MV, Varki A, (2003) Sequencing the chimpanzee genome: insights into human evolution and disease. Nat Rev Genet 4: 20-28.
3. Sholtis SJ, Noonan JP, (2010) Gene regulation and the origins of human biological uniqueness. Trends Genet 26: 110-118.
4. King MC, Wilson AC, (1975) Evolution at two levels in humans and chimpanzees. Science 188: 107-116.
5. Caceres M, Lachuer J, Zapala MA, Redmond JC, Kudo L, et al. (2003) Elevated gene expression levels distinguish human from non-human primate brains. Proc Natl Acad Sci U S A 100: 13030-13035.
6. Khaitovich P, Hellmann I, Enard W, Nowick K, Leinweber M, et al. (2005) Parallel patterns of evolution in the genomes and transcriptomes of humans and chimpanzees. Science 309: 1850-1854.
7. Gilad Y, Oshlack A, Smyth GK, Speed TP, White KP, (2006) Expression profiling in primates reveals a rapid evolution of human transcription factors. Nature 440: 242-245.
8. Enard W, Khaitovich P, Klose J, Zollner S, Heissig F, et al. (2002) Intra- and interspecific variation in primate gene expression patterns. Science 296: 340-343.
9. Blekhman R, Marioni JC, Zumbo P, Stephens M, Gilad Y, (2010) Sex-specific and lineage-specific alternative splicing in primates. Genome Res 20: 180-189.
10. Somel M, Franz H, Yan Z, Lorenc A, Guo S, et al. (2009) Transcriptional neoteny in the human brain. Proc Natl Acad Sci U S A 106: 5743-5748.
11. Xu AG, He L, Li Z, Xu Y, Li M, et al. (2010) Intergenic and repeat transcription in human, chimpanzee and macaque brains measured by RNA-Seq. PLoS Comput Biol 6: e1000843 doi:10.1371/journal.pcbi.1000843.
12. Babbitt CC, Fedrigo O, Pfefferle AD, Boyle AP, Horvath JE, et al. (2010) Both noncoding and protein-coding RNAs contribute to gene expression evolution in the primate brain. Genome Biol Evol 2: 67-79.
13. Carroll SB, (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134: 25-36.
14. Pollard KS, Salama SR, King B, Kern AD, Dreszer T, et al. (2006) Forces shaping the fastest evolving regions in the human genome. PLoS Genet 2: e168 doi:10.1371/journal.pgen.0020168.
15. Prabhakar S, Poulin F, Shoukry M, Afzal V, Rubin EM, et al. (2006) Close sequence comparisons are sufficient to identify human cis-regulatory elements. Genome Res 16: 855-863.
16. Haygood R, Fedrigo O, Hanson B, Yokoyama KD, Wray GA, (2007) Promoter regions of many neural- and nutrition-related genes have experienced positive selection during human evolution. Nat Genet 39: 1140-1144.
17. Boyle AP, Davis S, Shulha HP, Meltzer P, Margulies EH, et al. (2008) High-Resolution Mapping and Characterization of Open Chromatin across the Genome. Cell 132: 311-322.
18. Song L, Crawford GE, (2010) DNase-seq: a high-resolution technique for mapping active gene regulatory elements across the genome from mammalian cells. Cold Spring Harb Protoc 2010: pdb prot5384.
19. Consortium E, (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
20. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, et al. (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39: 311-318.
21. Xi H, Shulha HP, Lin JM, Vales TR, Fu Y, et al. (2007) Identification and characterization of cell type-specific and ubiquitous chromatin regulatory structures in the human genome. PLoS Genet 3: e136 doi:10.1371/journal.pgen.0030136.
22. Blekhman R, Oshlack A, Chabot AE, Smyth GK, Gilad Y, (2008) Gene regulation in primates evolves under tissue-specific selection pressures. PLoS Genet 4: e1000271 doi:10.1371/journal.pgen.1000271.
23. Hinrichs AS, Karolchik D, Baertsch R, Barber GP, Bejerano G, et al. (2006) The UCSC Genome Browser Database: update 2006. Nucleic Acids Res 34: D590-598.
24. Crawford GE, Davis S, Scacheri PC, Renaud G, Halawi MJ, et al. (2006) DNase-chip: a high-resolution method to identify DNase I hypersensitive sites using tiled microarrays. Nat Meth 3: 503-509.
25. Shibata Y, Crawford GE, (2009) Mapping regulatory elements by DNaseI hypersensitivity chip (DNase-Chip). Methods Mol Biol 556: 177-190.
26. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
27. Sabo PJ, Hawrylycz M, Wallace JC, Humbert R, Yu M, et al. (2004) Discovery of functional noncoding elements by digital analysis of chromatin structure. Proc Natl Acad Sci U S A 101: 16837-16842.
28. Sabo PJ, Kuehn MS, Thurman R, Johnson BE, Johnson EM, et al. (2006) Genome-scale mapping of DNase I sensitivity in vivo using tiling DNA microarrays. Nat Methods 3: 511-518.
29. Chang HY, Chi JT, Dudoit S, Bondre C, van de Rijn M, et al. (2002) Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci U S A 99: 12877-12882.
30. Rinn JL, Bondre C, Gladstone HB, Brown PO, Chang HY, (2006) Anatomic demarcation by positional variation in fibroblast gene expression programs. PLoS Genet 2: e119 doi:10.1371/journal.pgen.0020119.
31. Consortium E, (2011) A User's Guide to the Encyclopedia of DNA Elements (ENCODE). PLoS Biol 9: e1001046 doi:10.1371/journal.pbio.1001046.
32. Song L, Zhang Z, Grasfeder LL, Boyle AP, Giresi PG, et al. (2011) Open chromatin defined by DNaseI and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res 21: 1757-1767.
33. Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, et al. (2011) Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473: 43-49.
34. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, et al. (2010) GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol 28: 495-501.
35. Pond SL, Frost SD, Muse SV, (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21: 676-679.
36. Prabhakar S, Noonan JP, Paabo S, Rubin EM, (2006) Accelerated evolution of conserved noncoding sequences in humans. Science 314: 786.
37. Prabhakar S, Visel A, Akiyama JA, Shoukry M, Lewis KD, et al. (2008) Human-specific gain of function in a developmental enhancer. Science 321: 1346-1350.
38. Pollard KS, Salama SR, Lambert N, Lambot MA, Coppens S, et al. (2006) An RNA gene expressed during cortical development evolved rapidly in humans. Nature 443: 167-172.
39. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050.
40. Cooper GM, Stone EA, Asimenos G, Green ED, Batzoglou S, et al. (2005) Distribution and intensity of constraint in mammalian genomic sequence. Genome Res 15: 901-913.
41. Parker SC, Hansen L, Abaan HO, Tullius TD, Margulies EH, (2009) Local DNA topography correlates with functional noncoding regions of the human genome. Science 324: 389-392.
42. Bickel PJ, Boley N, Brown JB, Huang H, Zhang NR, (2010) Subsampling methods for genomic inference. The Annals of Applied Statistics 4: 1660-1697.
43. Graur D, Li W-H, (2000) Fundamentals of molecular evolution Sunderland, Mass. Sinauer Associates xiv, 481 p.
44. Bradley RK, Li XY, Trapnell C, Davidson S, Pachter L, et al. (2010) Binding site turnover produces pervasive quantitative changes in transcription factor binding between closely related Drosophila species. PLoS Biol 8: e1000343 doi:10.1371/journal.pbio.1000343.
45. Schmidt D, Wilson MD, Ballester B, Schwalie PC, Brown GD, et al. (2010) Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 328: 1036-1040.
46. Odom DT, Dowell RD, Jacobsen ES, Gordon W, Danford TW, et al. (2007) Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nat Genet 39: 730-732.
47. Mikkelsen TS, Xu Z, Zhang X, Wang L, Gimble JM, et al. (2010) Comparative epigenomic analysis of murine and human adipogenesis. Cell 143: 156-169.
48. McLean CY, Reno PL, Pollen AA, Bassan AI, Capellini TD, et al. (2011) Human-specific loss of regulatory DNA and the evolution of human-specific traits. Nature 471: 216-219.
49. Papadopoulou V, Postigo A, Sanchez-Tillo E, Porter AC, Wagner SD, (2010) ZEB1 and CtBP form a repressive complex at a distal promoter element of the BCL6 locus. Biochem J 427: 541-550.
50. Zhang CL, McKinsey TA, Lu JR, Olson EN, (2001) Association of COOH-terminal-binding protein (CtBP) and MEF2-interacting transcription repressor (MITR) contributes to transcriptional repression of the MEF2 transcription factor. J Biol Chem 276: 35-39.
51. Brawand D, Soumillon M, Necsulea A, Julien P, Csardi G, et al. (2011) The evolution of gene expression levels in mammalian organs. Nature 478: 343-348.
52. Wray GA, (2006) The evolution of embryonic gene expression in sea urchins. Integr Comp Biol 46: 233-242.
53. Orgogozo V, Muro NM, Stern DL, (2007) Variation in fiber number of a male-specific muscle between Drosophila species: a genetic and developmental analysis. Evol Dev 9: 368-377.
54. Degner JF, Pai AA, Pique-Regi R, Veyrieras JB, Gaffney DJ, et al. (2012) DNase I sensitivity QTLs are a major determinant of human expression variation. Nature 482: 390-394.
55. Holloway AK, Lawniczak MK, Mezey JG, Begun DJ, Jones CD, (2007) Adaptive gene expression divergence inferred from population genomics. PLoS Genet 3: e187 doi:10.1371/journal.pgen.0030187.
56. Good JM, Hayden CA, Wheeler TJ, (2006) Adaptive protein evolution and regulatory divergence in Drosophila. Mol Biol Evol 23: 1101-1103.
57. Cain CE, Blekhman R, Marioni JC, Gilad Y, (2011) Gene expression differences among primates are associated with changes in a histone epigenetic modification. Genetics 187: 1225-1234.
58. Shaulian E, Karin M, (2002) AP-1 as a regulator of cell life and death. Nat Cell Biol 4: E131-136.
59. Karamouzis MV, Konstantinopoulos PA, Papavassiliou AG, (2007) The activator protein-1 transcription factor in respiratory epithelium carcinogenesis. Mol Cancer Res 5: 109-120.
60. Eferl R, Wagner EF, (2003) AP-1: a double-edged sword in tumorigenesis. Nat Rev Cancer 3: 859-868.
61. Biddie SC, John S, Sabo PJ, Thurman RE, Johnson TA, et al. (2011) Transcription factor AP1 potentiates chromatin accessibility and glucocorticoid receptor binding. Mol Cell 43: 145-155.
62. Buck MJ, Nobel AB, Lieb JD, (2005) ChIPOTle: a user-friendly tool for the analysis of ChIP-chip data. Genome Biol 6: R97.
63. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
64. Boyle AP, Guinney J, Crawford GE, Furey TS, (2008) F-Seq: a feature density estimator for high-throughput sequence tags. Bioinformatics 24: 2537-2538.
65. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, et al. (2011) Integrative genomics viewer. Nat Biotechnol 29: 24-26.
66. Zhang J, Nielsen R, Yang Z, (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22: 2472-2479.
67. Wong WS, Nielsen R, (2004) Detecting selection in noncoding regions of nucleotide sequences. Genetics 167: 949-958.
68. Gilbert W, (1978) Why genes in pieces? Nature 271: 501.
69. Paten B, Herrero J, Beal K, Fitzgerald S, Birney E, (2008) Enredo and Pecan: genome-wide mammalian consistency-based multiple alignment with paralogs. Genome Res 18: 1814-1828.
70. Paten B, Herrero J, Fitzgerald S, Beal K, Flicek P, et al. (2008) Genome-wide nucleotide-level mammalian ancestor reconstruction. Genome Res 18: 1829-1843.
71. t Hoen PA, Ariyurek Y, Thygesen HH, Vreugdenhil E, Vossen RH, et al. (2008) Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucleic Acids Res 36: e141.