The importance of Being Cis: Evolution of Orthologous Fish and Mammalian enhancer activity

Molecular Biology and Evolution

Volumn 27, Issue 10, 2010, Pages 2322-2332

  Ritter, Deborah I ^a   Li, Qiang ^b   Kostka, Dennis ^c   Pollard, Katherine S ^c   Guo, Su ^b   Chuang, Jeffrey H ^a  

^a BOSTON COLLEGE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c GLADSTONE INSTITUTES   (United States)

Author keywords

cis; conserved noncoding elements; development; enhancer; evolution; expression; trans; transcription factor

Indexed keywords

TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; COMPARATIVE STUDY; CONSERVED NONCODING ELEMENT; CONTROLLED STUDY; EMBRYO; ENHANCER REGION; GENE EXPRESSION; GENE SEQUENCE; GENETIC CONSERVATION; MAMMAL; MOLECULAR EVOLUTION; MOUSE; MOUSE EMBRYO; NONHUMAN; ZEBRA FISH;

ANIMALS; CONSERVED SEQUENCE; DNA, INTERGENIC; ENHANCER ELEMENTS, GENETIC; EVOLUTION, MOLECULAR; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; HUMANS; MICE; ROC CURVE; TRANSCRIPTION FACTORS; ZEBRAFISH;

DANIO RERIO; MAMMALIA; VERTEBRATA;

EID: 77957225928     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msq128     Document Type: Article

References (47)

1. Ahituv N, Zhu Y, Visel A, Holt A, Afzal V, Pennacchio L.A, Rubin EM. 2007. Deletion of ultraconserved elements yields viable mice. PLoS Biol. 5:e234.
2. Akalin A, Fredman D, Arner E, Dong X, Bryne J, Suzuki H, Daub C, Hayashizaki Y, Lenhard B. 2009. Transcriptional features of genomic regulatory blocks. Genome Biol. 10:R38.
3. Antonellis A, Huynh JL, Lee-Lin S-Q, et al. 2008. Identification of neural crest and glial enhancers at the mouse Sox10 locus through transgenesis in zebrafish. PLoS Genet. 4:e1000174.
4. Badis G, Chan ET, van Bakel H, et al. 2008. A Library of Yeast Transcription Factor Motifs Reveals a Widespread Function for Rsc3 in Targeting Nucleosome Exclusion at Promoters. Mol Cell. 32:878-887.
5. Bejerano G, Pheasant M, Makunin I, Stephen S, Kent WJ, Mattick JS, Haussler D. 2004. Ultraconserved elements in the human genome. Science 304:1321-1325.
6. Berger MF, Badis G, Gehrke AR, et al. 2008. Variation in Homeodomain DNA Binding Revealed by High-Resolution Analysis of Sequence Preferences. Cell 133:1266-1276.
7. Bessa J, Tenna JJ, de la Calle-Mustienes E, et al. 2009. Zebrafish enhancer detection (ZED) vector: a new tool to facilitate transgenesis and the functional analysis of cis-regulatory regions in zebrafish. Dev Dyn. 238:2409-2417.
8. Bird C, Stranger B, Liu M, Thomas D, Ingle C, Beazley C, Miller W, Hurles M, Dermitzakis E. 2007. Fast-evolving noncoding sequences in the human genome. Genome Biol. 8:R118.
9. Blair JE, Hedges SB. 2005. Molecular phylogeny and divergence times of deuterostome animals. Mol Biol Evol. 22:2275-2284.
10. Chan E, Quon G, Chua G, et al. 2009. Conservation of core gene expression in vertebrate tissues. J Biol. 8:33.
11. De La Calle-Mustienes E, Feijoo CG, Manzanares M, Tena JJ, Rodriguez-Seguel E, Letizia A, Allende ML, Gomez-Skarmeta JL. 2005. A functional survey of the enhancer activity of conserved non-coding sequences from vertebrate Iroquois cluster gene deserts. Genome Res. 15:1061-1072.
12. Engstrom P, Fredman D, Lenhard B. 2008. Ancora: a web resource for exploring highly conserved noncoding elements and their association with developmental regulatory genes. Genome Biol. 9:R34.
13. Fisher S, Grice EA, Vinton RM, Bessling SL, McCallion AS. 2006. Conservation of RET regulatory function from human to zebrafish without sequence similarity. Science 312:276-279.
14. Gehrig J, Reischl M, Kalmar E, Ferg M, Hadzhiev Y, Zaucker A, Song C, Schindler S, Liebel U, Muller F. 2009. Automated high-throughput mapping of promoter-enhancer interactions in zebrafish embryos. Nat Methods. 6:911-916.
15. Hare EE, Peterson BK, Iyer VN, Meier R, Eisen MB. 2008. Sepsid even-skipped enhancers are functionally conserved in drosophila despite lack of sequence conservation. PLoS Genet. 4:e1000106.
16. Jarinova O, Hatch G, Poitras L, Prudhomme C, Grzyb M, Aubin J, Bérubé-Simard FA, Jeannotte L, Ekker M. 2008. Functional resolution of duplicated hoxb5 genes in teleosts. Development 135(21):3543-3553.
17. Kikuta H, Laplante M, Navratilova P, et al. 2007. Genomic regulatory blocks encompass multiple neighboring genes and maintain conserved synteny in vertebrates. Genome Res. 17:545-555.
18. Kleinjan DA, Bancewicz RM, Gautier P, et al. 2008. Subfunctional-ization of duplicated zebrafish pax6 genes by cis-regulatory divergence. PLoS Genet. 4:e29.
19. Li Q, Ritter D, Yang N, Dong Z, Li H, Chuang JH, Guo S. 2009. A systematic approach to identify functional motifs within vertebrate developmental enhancers. Developmental Biol. 337:484-495.
20. McEwen GK, Goode DK, Parker HJ, Woolfe A, Callaway H, Elgar G. 2009. Early evolution of conserved regulatory sequences associated with development in vertebrates. PLoS Genet. 59:e1000762.
21. McGaughey DM, Vinton RM, Huynh J, Al-Saif A, Beer MA, McCallion AS. 2008. Metrics of sequence constraint overlook regulatory sequences in an exhaustive analysis at phox2b. Genome Res. 18:252-260.
22. Navratilova P, Fredman D, Hawkins TA, Turner K, Lenhard B, Becker TS. 2009. Systematic human/zebrafish comparative identification of cis-regulatory activity around vertebrate developmental transcription factor genes. Developmental Biol. 327:526-540.
23. Navratilova P, Fredman D, Lenhard B, Becker T. 2010. Regulatory divergence of the duplicated chromosomal loci sox11a/b by subpartitioning and sequence evolution of enhancers in zebra-fish. Mol Genet Genomics. 283:171.
24. Odom DT, Dowell RD, Jacobsen ES, Gordon W, Danford TW, MacIsaac KD, Rolfe PA, Conboy CM, Gifford DK, Fraenkel E. 2007. Tissue-specific transcriptional regulation has diverged significantly between human and mouse. Nat Genet. 39: 730-732.
25. Ovcharenko I, Nobrega MA, Loots GG, Stubbs L. 2004. ECR Browser: a tool for visualizing and accessing data from comparisons of multiple vertebrate genomes. Nucl Acids Res. 32:W280-W286.
26. Pennacchio LA, Ahituv N, Moses AM, et al. 2006. In vivo enhancer analysis of human conserved non-coding sequences. Nature 444:499.
27. Pennacchio LA, Loots GG, Nobrega MA, Ovcharenko I. 2007. Predicting tissue-specific enhancers in the human genome. Genome Res. 17:201-211.
28. Persampieri J, Ritter DI, Lees D, Lehoczky J, Li Q, Guo S, Chuang JH. 2008.cneViewer: a database of conserved non-coding elements for studies of tissue-specific gene regulation. Bioinformatics 24:2418-2419.
29. Pollard KS, Hubisz MJ, Rosenbloom KR, Siepel A. 2010. Detection of non-neutral substitution rates on mammalian phylogenies. Genome Res. 20:110-121.
30. Prabhakar S, Noonan JP, Paabo S, Rubin EM. 2006. Accelerated evolution of conserved noncoding sequences in humans. Science 314:786.
31. Prabhakar S, Visel A, Akiyama JA, et al. 2008. Human-specific gain of function in a developmental enhancer. Science 321:1346-1350.
32. R Development Core Team. 2005. R: a language and environment for statistical computing. Vienna, Austria. ISBN 3-900051-07-0, Available from http://www.R-project.org.
33. Rahmann S, Muller T, Vingron M. 2003. On the power of profiles for transcription factor binding site detection. Stat Appl Genet Mol Biol. 2.
34. Sandelin A, Wasserman WW. 2004. Constrained binding site diversity within families of transcription factors enhances pattern discovery bioinformatics. J Mol Biol. 338:207-215.
35. Sprague J, Bayraktaroglu L, Clements D, et al. 2006. The zebrafish information network: the zebrafish model organism database. Nucl Acids Res. 34:D581-D585.
36. Stephen S, Pheasant M, Makunin IV, Mattick JS. 2008. Large-scale appearance of ultraconserved elements in tetrapod genomes and slowdown of the Molecular Clock. Mol Biol Evol. 25: 402-408.
37. Strähle U, Rastegar S. 2008. Conserved non-coding sequences and transcriptional regulation. Brain Res Bull. 75:225.
38. Visel A, Blow MJ, Li Z, et al. 2009. ChiP-Seq accurately predicts tissue specificity of enhancers. Nature 454:854.
39. Visel A, Bristow J, Pennacchio LA. 2007. Enhancer identification through comparative genomics. Semin Cell Dev Biol. 18:140.
40. Visel A, Minovitsky S, Dubchak I, Pennacchio L. 2007. VISTA enhancer browser\a database of tissue-specific human enhancers. Nucl Acids Res. 35(Suppl 1):D88-D92.
41. Wang J, Lee AP, Kodzius R, Brenner S, Venkatesh B. 2009. Large number of ultraconserved elements were already present in the jawed vertebrate ancestor. Mol Biol Evol. 26:487-490.
42. Wasserman WW, Sandelin A. 2004. Applied bioinformatics for the identification of regulatory elements. Nat Rev Genet. 5: 276-287.
43. Wilson MD, Barbosa-Morais NL, Schmidt D, Conboy CM, Vanes L, Tybulewicz VLJ, Fisher EMC, Tavare S, Odom DT. 2008. Species-specific transcription in mice carrying human chromosome 21. Science 322:434-438.
44. Wittkopp PJ, Haerum BK, Clark AG. 2004. Evolutionary changes in cis and trans gene regulation. Nature 430:85.
45. Wolfe KH, Shields DC. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708.
46. Woolfe A, Goode D, Cooke J, Callaway H, Smith S, Snell P, McEwen G, Elgar G. 2007. CONDOR: a database resource of developmentally associated conserved non-coding elements. BMC Dev Biol. 7:100.
47. Woolfe A, Goodson M, Goode DK, et al. 2005. Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol. 3:e7.