The Genetic and Mechanistic Basis for Variation in Gene Regulation

PLoS Genetics

Volumn 11, Issue 1, 2015, Pages

  Pai, Athma A ^a   Pritchard, Jonathan K ^b   Gilad, Yoav ^c  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; CHROMATIN; MESSENGER RNA;

ARTICLE; BINDING SITE; GENE EXPRESSION; GENE INTERACTION; GENETIC ASSOCIATION; GENETIC CORRELATION; GENETIC REGULATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HUMAN; NONHUMAN; POSTTRANSCRIPTIONAL GENE SILENCING; PROTEIN BINDING; QUANTITATIVE ANALYSIS; QUANTITATIVE TRAIT LOCUS MAPPING; REGULATORY MECHANISM; SINGLE NUCLEOTIDE POLYMORPHISM; CHROMATIN; CHROMOSOME MAP; DNA METHYLATION; GENE EXPRESSION REGULATION; GENETICS; HUMAN GENOME; PHENOTYPE; QUANTITATIVE TRAIT LOCUS;

CHROMATIN; CHROMOSOME MAPPING; DNA METHYLATION; GENE EXPRESSION REGULATION; GENOME, HUMAN; GENOME-WIDE ASSOCIATION STUDY; HUMANS; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EID: 84924365586     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004857     Document Type: Article

References (63)

1. Wray GA, (2007) The evolutionary significance of cis-regulatory mutations. Nat Rev Genet 8: 206–216 Available: http://bejerano.stanford.edu/readings/public/
2. Carroll SB, (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134: 25–36 doi:10.1016/j.cell.2008.06.030
3. Cookson W, Liang L, Abecasis G, Moffatt M, Lathrop M, (2009) Mapping complex disease traits with global gene expression. Nat Rev Genet 10: 184–194 doi:10.1038/nrg2537
4. Montgomery SB, Dermitzakis ET, (2011) From expression QTLs to personalized transcriptomics. Nat Rev Genet 12: 277–282 doi:10.1038/nrg2969
5. Pickrell JK, (2014) Joint analysis of functional genomic data and genome-wide association studies of 18 human traits. Am J Hum Genet 94: 559–573 doi:10.1016/j.ajhg.2014.03.004
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 doi:10.1126/science.1108296
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 doi:10.1038/nature04559
8. Brem RB, Yvert G, Clinton R, Kruglyak L, (2002) Genetic Dissection of Transcriptional Regulation in Budding Yeast. Science 296: 752–755.
9. Schadt EE, Monks SA, Drake TA, Lusis AJ, Che N, et al. (2003) Genetics of gene expression surveyed in maize, mouse and man. Nature 422: 297–302 doi:10.1038/nature01434
10. Cheung VG, Conlin LK, Weber TM, Arcaro M, Jen K-Y, et al. (2003) Natural variation in human gene expression assessed in lymphoblastoid cells. Nat Genet 33: 422–425 doi:10.1038/ng1094
11. Veyrieras J-B, Kudaravalli S, Kim SY, Dermitzakis ET, Gilad Y, et al. (2008) High-resolution mapping of expression-QTLs yields insight into human gene regulation. PLoS Genet 4: e1000214 doi:10.1371/journal.pgen.1000214
12. Stranger BE, Nica AC, Forrest MS, Dimas A, Bird CP, et al. (2007) Population genomics of human gene expression. Nat Genet 39: 1217–1224 doi:10.1038/ng2142
13. Göring HHH, Curran JE, Johnson MP, Dyer TD, Charlesworth J, et al. (2007) Discovery of expression QTLs using large-scale transcriptional profiling in human lymphocytes. Nat Genet 39: 1208–1216 doi:10.1038/ng2119
14. Romero IG, Ruvinsky I, Gilad Y, (2012) Comparative studies of gene expression and the evolution of gene regulation. Nat Rev Genet 13: 505–516 doi:10.1038/nrg3229
15. Gaffney DJ, Veyrieras J-B, Degner JF, Roger P-R, Pai AA, et al. (2012) Dissecting the regulatory architecture of gene expression QTLs. Genome Biology 13: R7 doi:10.1186/gb-2012-13-1-r7
16. Kasowski M, Kyriazopoulou-Panagiotopoulou S, Grubert F, Zaugg JB, Kundaje A, et al. (2013) Extensive variation in chromatin states across humans. Science 342: 750–752 doi:10.1126/science.1242510
17. Kasowski M, Grubert F, Heffelfinger C, Hariharan M, Asabere A, et al. (2010) Variation in transcription factor binding among humans. Science 328: 232–235 doi:10.1126/science.1183621
18. 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 doi:10.1126/science.1186176
19. Degner JF, Pai AA, Pique-Regi R, Veyrieras J-B, Gaffney DJ, et al. (2012) DNase I sensitivity QTLs are a major determinant of human expression variation. Nature 482: 390–394 doi:10.1038/nature10808
20. Stefflova K, Thybert D, Wilson MD, Streeter I, Aleksic J, et al. (2013) Cooperativity and rapid evolution of cobound transcription factors in closely related mammals. Cell 154: 530–540 doi:10.1016/j.cell.2013.07.007
21. Bell JT, Pai AA, Pickrell JK, Gaffney DJ, Pique-Regi R, et al. (2011) DNA methylation patterns associate with genetic and gene expression variation in HapMap cell lines. Genome Biology 12: R10 doi:10.1186/gb-2011-12-1-r10
22. 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 doi:10.1534/genetics.110.126177
23. Pai AA, Bell JT, Marioni JC, Pritchard JK, Gilad Y, (2011) A genome-wide study of DNA methylation patterns and gene expression levels in multiple human and chimpanzee tissues. PLoS Genet 7: e1001316 doi:10.1371/journal.pgen.1001316
24. Kilpinen H, Waszak SM, Gschwind AR, Raghav SK, Witwicki RM, et al. (2013) Coordinated effects of sequence variation on DNA binding, chromatin structure, and transcription. Science 342: 744–747 doi:10.1126/science.1242463
25. McVicker G, van de Geijn B, Degner JF, Cain CE, Banovich NE, et al. (2013) Identification of genetic variants that affect histone modifications in human cells. Science 342: 747–749 doi:10.1126/science.1242429
26. Pickrell JK, Marioni JC, Pai AA, Degner JF, Engelhardt BE, et al. (2010) Understanding mechanisms underlying human gene expression variation with RNA sequencing. Nature 464: 768–772 doi:10.1038/nature08872
27. Barbosa-Morais NL, Irimia M, Pan Q, Xiong HY, Gueroussov S, et al. (2012) The Evolutionary Landscape of Alternative Splicing in Vertebrate Species. Science 338: 1587–1593 doi:10.1126/science.1230612
28. Merkin J, Russell C, Chen P, Burge CB, (2012) Evolutionary Dynamics of Gene and Isoform Regulation in Mammalian Tissues. Science 338: 1593–1599 doi:10.1126/science.1228186
29. Yoon OK, Hsu TY, Im JH, Brem RB, (2012) Genetics and regulatory impact of alternative polyadenylation in human B-lymphoblastoid cells. PLoS Genet 8: e1002882 doi:10.1371/journal.pgen.1002882
30. Pai AA, Cain CE, Mizrahi-Man O, De Leon S, Lewellen N, et al. (2012) The contribution of RNA decay quantitative trait loci to inter-individual variation in steady-state gene expression levels. PLoS Genet 8: e1003000 doi:10.1371/journal.pgen.1003000
31. Wittkopp PJ, Kalay G, (2011) Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat Rev Genet 13: 59–69 doi:10.1038/nrg3095
32. Majewski J, Pastinen T, (2011) The study of eQTL variations by RNA-seq: from SNPs to phenotypes. Trends Genet 27: 72–79 doi:10.1016/j.tig.2010.10.006
33. Montgomery SB, Sammeth M, Gutierrez Arcelus M, Lach RP, Ingle C, et al. (2010) Transcriptome genetics using second generation sequencing in a Caucasian population. Nature 464: 773–777 doi:10.1038/nature08903
34. Lappalainen T, Sammeth M, Friedländer MR, 't Hoen PAC, Monlong J, et al. (2013) Transcriptome and genome sequencing uncovers functional variation in humans. Nature 501: 506–511 doi:10.1038/nature12531
35. Westra H-J, Peters MJ, Esko T, Yaghootkar H, Schurmann C, et al. (2013) Systematic identification of trans eQTLs as putative drivers of known disease associations. Nat Genet 45: 1238–1243 doi:10.1038/ng.2756
36. Battle A, Mostafavi S, Zhu X, Potash JB, Weissman MM, et al. (2013) Characterizing the genetic basis of transcriptome diversity through RNA-sequencing of 922 individuals. Genome Research 24: 14–24 doi:10.1101/gr.155192.113
37. Price AL, Helgason A, Thorleifsson G, McCarroll SA, Kong A, et al. (2011) Single-Tissue and Cross-Tissue Heritability of Gene Expression Via Identity-by-Descent in Related or Unrelated Individuals. PLoS Genet 7: e1001317 doi:10.1371/journal.pgen.1001317
38. Popadin K, Gutierrez Arcelus M, Dermitzakis ET, Antonarakis SE, (2013) Genetic and epigenetic regulation of human lincRNA gene expression. Am J Hum Genet 93: 1015–1026 doi:10.1016/j.ajhg.2013.10.022
39. Lu J, Clark AG, (2012) Impact of microRNA regulation on variation in human gene expression. Genome Research 22: 1243–1254 doi:10.1101/gr.132514.111
40. Gibbs JR, van der Brug MP, Hernandez DG, Traynor BJ, Nalls MA, et al. (2010) Abundant quantitative trait Loci exist for DNA methylation and gene expression in human brain. PLoS Genet 6: e1000952 doi:10.1371/journal.pgen.1000952
41. Zhang D, Cheng L, Badner JA, Chen C, Chen Q, et al. (2010) Genetic control of individual differences in gene-specific methylation in human brain. Am J Hum Genet 86: 411–419 doi:10.1016/j.ajhg.2010.02.005
42. Gamazon ER, Badner JA, Cheng L, Zhang C, Zhang D, et al. (2012) Enrichment of cis-regulatory gene expression SNPs and methylation quantitative trait loci among bipolar disorder susceptibility variants. Mol Psychiatry 18: 340–346 doi:10.1038/mp.2011.174
43. Mcdaniell R, Lee BK, Song L, Liu Z, Boyle AP, et al. (2010) Heritable Individual-Specific and Allele-Specific Chromatin Signatures in Humans. Science 328: 235–239 doi:10.1126/science.1184655
44. Ernst J, Kellis M, (2012) ChromHMM: automating chromatin-state discovery and characterization. Nat Meth 9: 215–216 doi:10.1038/nmeth.1906
45. Ernst J, Kellis M, (2010) Discovery and characterization of chromatin states for systematic annotation of the human genome. Nature Biotechnology 28: 817–838 doi:10.1038/nbt.1662
46. White MA, Myers CA, Corbo JC, Cohen BA, (2013) Massively parallel in vivo enhancer assay reveals that highly local features determine the cis-regulatory function of ChIP-seq peaks. Proc Natl Acad Sci USA 110: 11952–11957 doi:10.1073/pnas.1307449110
47. Lalonde E, Ha KCH, Wang Z, Bemmo A, Kleinman CL, et al. (2011) RNA sequencing reveals the role of splicing polymorphisms in regulating human gene expression. Genome Research 21: 545–554 doi:10.1101/gr.111211.110
48. Wang L, Oberg AL, Asmann YW, Sicotte H, McDonnell SK, et al. (2009) Genome-wide transcriptional profiling reveals microRNA-correlated genes and biological processes in human lymphoblastoid cell lines. PLoS One 4: e5878 doi:10.1371/journal.pone.0005878
49. Dori-Bachash M, Shema E, Tirosh I, (2011) Coupled Evolution of Transcription and mRNA Degradation. PLoS Biol 9: e1001106 doi:10.1371/journal.pbio.1001106.g006
50. Wu L, Candille SI, Choi Y, Xie D, Jiang L, et al. (2013) Variation and genetic control of protein abundance in humans. Nature 499: 79–82 doi:10.1038/nature12223
51. Johansson Å, Enroth S, Palmblad M, Deelder AM, Bergquist J, et al. (2013) Identification of genetic variants influencing the human plasma proteome. Proc Natl Acad Sci USA 110: 4673–4678 doi:10.1073/pnas.1217238110
52. Albert FW, Treusch S, Shockley AH, Bloom JS, Kruglyak L, (2014) Genetics of single-cell protein abundance variation in large yeast populations. Nature 506: 494–497 doi:10.1038/nature12904
53. Khan Z, Ford MJ, Cusanovich DA, Mitrano A, Pritchard JK, et al. (2013) Primate transcript and protein expression levels evolve under compensatory selection pressures. Science 342: 1100–1104 doi:10.1126/science.1242379
54. Arbiza L, Gronau I, Aksoy BA, Hubisz MJ, Gulko B, et al. (2013) Genome-wide inference of natural selection on human transcription factor binding sites. Nat Genet 45: 723–729 doi:10.1038/ng.2658
55. Cusanovich DA, Pavlovic B, Pritchard JK, Gilad Y, (2014) The functional consequences of variation in transcription factor binding. PLoS Genet 10: e1004226 doi:10.1371/journal.pgen.1004226
56. Heinz S, Romanoski CE, Benner C, Allison KA, Kaikkonen MU, et al. (2013) Effect of natural genetic variation on enhancer selection and function. Nature 503: 487–492 doi:10.1038/nature12615
57. Lam EWF, Brosens JJ, Gomes AR, Koo C-Y, (2013) Forkhead box proteins: tuning forks for transcriptional harmony. Nature Reviews Cancer 13: 482–495 doi:doi:10.1038/nrc3539
58. Zaret KS, Carroll JS, (2011) Pioneer transcription factors: establishing competence for gene expression. Genes & Development 25: 2227–2241.
59. Struhl K, Segal E, (2013) Determinants of nucleosome positioning. Nature Structural & Molecular Biology 20: 267–273 doi:10.1038/nsmb.2506
60. Marchetto MCN, Narvaiza I, Denli AM, Benner C, Lazzarini TA, et al. (2013) Differential L1 regulation in pluripotent stem cells of humans and apes. Nature 503: 525–529 doi:10.1038/nature12686
61. Pfefferle LW, Wray GA, (2013) Insights from a Chimpanzee Adipose Stromal Cell Population: Opportunities for Adult Stem Cells to Expand Primate Functional Genomics. Genome Biology and Evolution 5: 1995–2005.
62. Lee JH, Park IH, Gao Y, Li JB, Li Z, et al. (2009) A Robust Approach to Identifying Tissue-Specific Gene Expression Regulatory Variants Using Personalized Human Induced Pluripotent Stem Cells. PLoS Genet 5: e1000718.
63. Schreiber J, Jenner RG, Murray HL, Gerber GK, Gifford DK, et al. (2006) Coordinated binding of NF-kappaB family members in the response of human cells to lipopolysaccharide. Proc Natl Acad Sci USA 103: 5899–5904 doi:10.1073/pnas.0510996103