Differences in enhancer activity in mouse and zebrafish reporter assays are often associated with changes in gene expression

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Ariza Cosano, Ana ^a   Visel, Axel ^b,c   Pennacchio, Len A ^b,c   Fraser, Hunter B ^d   Gómez Skarmeta, José L ^a   Irimia, Manuel ^d,e   Bessa, José ^a  

^a UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c DOE JOINT GENOME INSTITUTE   (United States)

^d STANFORD UNIVERSITY   (United States)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

Enhancers; Evolution; Trans changes; Trans evolution; Vertebrates

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSAY; CONTROLLED STUDY; DNA SEQUENCE; EMBRYO; ENHANCER REGION; GENE ACTIVITY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENETIC ASSOCIATION; GENETIC CODE; GENETIC CONSERVATION; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; PREVALENCE; REPORTER ASSAY; SPECIES DIFFERENCE; TISSUE SPECIFICITY; TRANSGENIC MOUSE; TRANSGENICS; VERTEBRATE; ZEBRA FISH;

ANIMALS; CONSERVED SEQUENCE; DNA PRIMERS; ENHANCER ELEMENTS, GENETIC; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; GENES, REPORTER; HUMANS; IN SITU HYBRIDIZATION; MICE; MICE, TRANSGENIC; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS; ZEBRAFISH;

ANIMALIA; DANIO RERIO; MUS MUSCULUS; VERTEBRATA;

EID: 84871117732     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-713     Document Type: Article

References (71)

1. King MC, Wilson AC. Evolution at two levels in humans and chimpanzees. Science 1975, 188:107-116. 10.1126/science.1090005, 1090005.
2. Halder G, Callaerts P, Gehring WJ. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 1995, 267:1788-1792. 10.1126/science.7892602, 7892602.
3. Carroll SB. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 2008, 134:25-36. 10.1016/j.cell.2008.06.030, 18614008.
4. Ronald J, Akey JM. The evolution of gene expression QTL in Saccharomyces cerevisiae. PLoS One 2007, 2:e678. 10.1371/journal.pone.0000678, 1925141, 17668057.
5. Ronald J, Brem RB, Whittle J, Kruglyak L. Local regulatory variation in Saccharomyces cerevisiae. PLoS Genet 2005, 1:e25. 10.1371/journal.pgen.0010025, 1189075, 16121257.
6. Wang D, Sung H-M, Wang T-Y, Huang C-J, Yang P, Chang T, Wang Y-C, Tseng D-L, Wu J-P, Lee T-C, Shih M-C, Li W-H. Expression evolution in yeast genes of single-input modules is mainly due to changes in trans-acting factors. Genome Res 2007, 17:1161-1169. 10.1101/gr.6328907, 1933509, 17615293.
7. Sung H-M, Wang T-Y, Wang D, Huang Y-S, Wu J-P, Tsai H-K, Tzeng J, Huang C-J, Lee Y-C, Yang P, Hsu J, Chang T, Cho C-Y, Weng L-C, Lee T-C, Chang T-H, Li W-H, Shih M-C. Roles of trans and cis variation in yeast intraspecies evolution of gene expression. Mol Biol Evol 2009, 26:2533-2538. 10.1093/molbev/msp171, 2767097, 19648464.
8. Tirosh I, Reikhav S, Levy AA, Barkai N. A yeast hybrid provides insight into the evolution of gene expression regulation. Science 2009, 324:659-662. 10.1126/science.1169766, 19407207.
9. Emerson JJ, Hsieh L-C, Sung H-M, Wang T-Y, Huang C-J, Lu HH-S, Lu M-YJ WS-H, Li W-H. Natural selection on cis and trans regulation in yeasts. Genome Res 2010, 20:826-836. 10.1101/gr.101576.109, 2877579, 20445163.
10. Wittkopp PJ, Haerum BK, Clark AG. Evolutionary changes in cis and trans gene regulation. Nature 2004, 430:85-88. 10.1038/nature02698, 15229602.
11. Wittkopp PJ, Haerum BK, Clark AG. Regulatory changes underlying expression differences within and between Drosophila species. Nat Genet 2008, 40:346-350. 10.1038/ng.77, 18278046.
12. Wilson MD, Barbosa-Morais NL, Schmidt D, Conboy CM, Vanes L, Tybulewicz VLJ, Fisher EMC, Tavaré S, Odom DT. Species-specific transcription in mice carrying human chromosome 21. Science 2008, 322:434-438. 10.1126/science.1160930, 18787134.
13. Sandelin A, Bailey P, Bruce S, Engström PG, Klos JM, Wasserman WW, Ericson J, Lenhard B. Arrays of ultraconserved non-coding regions span the loci of key developmental genes in vertebrate genomes. BMC Genomics 2004, 5:99. 10.1186/1471-2164-5-99, 544600, 15613238.
14. Shin JT, Priest JR, Ovcharenko I, Ronco A, Moore RK, Burns CG, MacRae CA. Human-zebrafish non-coding conserved elements act in vivo to regulate transcription. Nucleic Acids Res 2005, 33:5437-5445. 10.1093/nar/gki853, 1236720, 16179648.
15. Woolfe A, Goodson M, Goode DK, Snell P, McEwen GK, Vavouri T, Smith SF, North P, Callaway H, Kelly K, Walter K, Abnizova I, Gilks W, Edwards YJK, Cooke JE, Elgar G. Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol 2005, 3:e7. 10.1371/journal.pbio.0030007, 526512, 15630479.
16. Venkatesh B, Kirkness EF, Loh Y-H, Halpern AL, Lee AP, Johnson J, Dandona N, Viswanathan LD, Tay A, Venter JC, Strausberg RL, Brenner S. Ancient noncoding elements conserved in the human genome. Science 1892, 2006:314.
17. Allende ML, Manzanares M, Tena JJ, Feijóo CG, Gómez-Skarmeta JL. Cracking the genome's second code: enhancer detection by combined phylogenetic footprinting and transgenic fish and frog embryos. Methods 2006, 39:212-219. 10.1016/j.ymeth.2005.12.005, 16806968.
18. Pennacchio LA, Ahituv N, Moses AM, Prabhakar S, Nobrega MA, Shoukry M, Minovitsky S, Dubchak I, Holt A, Lewis KD, Plajzer-Frick I, Akiyama J, De Val S, Afzal V, Black BL, Couronne O, Eisen MB, Visel A, Rubin EM. In vivo enhancer analysis of human conserved non-coding sequences. Nature 2006, 444:499-502. 10.1038/nature05295, 17086198.
19. Navratilova P, Fredman D, Hawkins TA, Turner K, Lenhard B, Becker TS. Systematic human/zebrafish comparative identification of cis-regulatory activity around vertebrate developmental transcription factor genes. Dev Biol 2009, 327:526-540. 10.1016/j.ydbio.2008.10.044, 19073165.
20. De la Calle-Mustienes E, Feijóo CG, Manzanares M, Tena JJ, Rodríguez-Seguel E, Letizia A, Allende ML, Gómez-Skarmeta JL. A functional survey of the enhancer activity of conserved non-coding sequences from vertebrate Iroquois cluster gene deserts. Genome Res 2005, 15:1061-1072. 10.1101/gr.4004805, 1182218, 16024824.
21. Antonellis A, Huynh JL, Lee-Lin S-Q, Vinton RM, Renaud G, Loftus SK, Elliot G, Wolfsberg TG, Green ED, McCallion AS, Pavan WJ. Identification of neural crest and glial enhancers at the mouse Sox10 locus through transgenesis in zebrafish. PLoS Genet 2008, 4:e1000174. 10.1371/journal.pgen.1000174, 2518861, 18773071.
22. Jarinova O, Hatch G, Poitras L, Prudhomme C, Grzyb M, Aubin J, Bérubé-Simard F-A, Jeannotte L, Ekker M. Functional resolution of duplicated hoxb5 genes in teleosts. Development 2008, 135:3543-3553. 10.1242/dev.025817, 18832391.
23. Kleinjan DA, Bancewicz RM, Gautier P, Dahm R, Schonthaler HB, Damante G, Seawright A, Hever AM, Yeyati PL, Van Heyningen V, Coutinho P. Subfunctionalization of duplicated zebrafish pax6 genes by cis-regulatory divergence. PLoS Genet 2008, 4:e29. 10.1371/journal.pgen.0040029, 2242813, 18282108.
24. Strähle U, Rastegar S. Conserved non-coding sequences and transcriptional regulation. Brain Res Bull 2008, 75:225-230. 10.1016/j.brainresbull.2007.11.010, 18331875.
25. Ritter DI, Li Q, Kostka D, Pollard KS, Guo S, Chuang JH. The importance of being cis: evolution of orthologous fish and mammalian enhancer activity. Mol Biol Evol 2010, 27:2322-2332. 10.1093/molbev/msq128, 3107594, 20494938.
26. Visel A, Minovitsky S, Dubchak I, Pennacchio LA. VISTA enhancer browser-a database of tissue-specific human enhancers. Nucleic Acids Res 2007, 35:D88-D92. 10.1093/nar/gkl822, 1716724, 17130149.
27. Royo JL, Hidalgo C, Roncero Y, Seda MA, Akalin A, Lenhard B, Casares F, Gómez-Skarmeta JL. Dissecting the transcriptional regulatory properties of human chromosome 16 highly conserved non-coding regions. PLoS One 2011, 6:e24824. 10.1371/journal.pone.0024824, 3172297, 21935474.
28. Irie N, Kuratani S. Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis. Nat Commun 2011, 2:248. 3109953, 21427719.
29. Bessa J, Tena JJ, De la Calle-Mustienes E, Fernández-Miñán A, Naranjo S, Fernández A, Montoliu L, Akalin A, Lenhard B, Casares F, Gómez-Skarmeta JL. Zebrafish enhancer detection (ZED) vector: a new tool to facilitate transgenesis and the functional analysis of cis-regulatory regions in zebrafish. Dev Dyn 2009, 238:2409-2417. 10.1002/dvdy.22051, 19653328.
30. Navratilova P, Fredman D, Lenhard B, Becker TS. Regulatory divergence of the duplicated chromosomal loci sox11a/b by subpartitioning and sequence evolution of enhancers in zebrafish. Mol Genet Genomics 2010, 283:171-184. 10.1007/s00438-009-0503-1, 20039180.
31. Komisarczuk AZ, Kawakami K, Becker TS. Cis-regulation and chromosomal rearrangement of the fgf8 locus after the teleost/tetrapod split. Dev Biol 2009, 336:301-312. 10.1016/j.ydbio.2009.09.029, 19782672.
32. Naranjo S, Voesenek K, De la Calle-Mustienes E, Robert-Moreno A, Kokotas H, Grigoriadou M, Economides J, Van Camp G, Hilgert N, Moreno F, Alsina B, Petersen MB, Kremer H, Gómez-Skarmeta JL. Multiple enhancers located in a 1-Mb region upstream of POU3F4 promote expression during inner ear development and may be required for hearing. Hum Genet 2010, 128:411-419. 10.1007/s00439-010-0864-x, 2939330, 20668882.
33. Punnamoottil B, Herrmann C, Pascual-Anaya J, D'Aniello S, Garcia-Fernàndez J, Akalin A, Becker TS, Rinkwitz S. Cis-regulatory characterization of sequence conservation surrounding the Hox4 genes. Dev Biol 2010, 340:269-282. 10.1016/j.ydbio.2010.01.035, 20144609.
34. Ragvin A, Moro E, Fredman D, Navratilova P, Drivenes T, Engström PG, Alonso ME, de La Calle Mustienes E, Skarmeta JLG, Tavares MJ, Casares F, Manzanares M, Van Heyningen V, Molven A, Njølstad PR, Argenton F, Lenhard B, Becker TS. Long-range gene regulation links genomic type 2 diabetes and obesity risk regions to HHEX, SOX4, and IRX3. Proc Natl Acad Sci U S A 2010, 107:775-780. 10.1073/pnas.0911591107, 2818943, 20080751.
35. Royo JL, Maeso I, Irimia M, Gao F, Peter IS, Lopes CS, D'Aniello S, Casares F, Davidson EH, Garcia-Fernández J, Gómez-Skarmeta JL. Transphyletic conservation of developmental regulatory state in animal evolution. Proc Natl Acad Sci U S A 2011, 108:14186-14191. 10.1073/pnas.1109037108, 3161536, 21844364.
36. Tena JJ, Alonso ME, De la Calle-Mustienes E, Splinter E, De Laat W, Manzanares M, Gómez-Skarmeta JL. An evolutionarily conserved three-dimensional structure in the vertebrate Irx clusters facilitates enhancer sharing and coregulation. Nat Commun 2011, 2:310.
37. Robert-moreno T, Naranjo S, De la Calle-Mustienes E, Gómez-Skarmeta JL, Alsina B. Characterization of New otic enhancers of the Pou3f4 gene reveal distinct signaling pathway regulation and spatio-temporal patterns. PLoS One 5:e15907.
38. Maeso I, Irimia M, Tena JJ, González-Pérez E, Tran D, Ravi V, Venkatesh B, Campuzano S, Gómez-Skarmeta JL, Garcia-Fernàndez J. An ancient genomic regulatory block conserved across bilaterians and its dismantling in tetrapods by retrogene replacement. Genome Res 2012, 22:642-655. 10.1101/gr.132233.111, 3317147, 22234889.
39. Irimia M, Royo JL, Burguera D, Maeso I, Gómez-Skarmeta JL, Garcia-Fernandez J. Comparative genomics of the Hedgehog loci in chordates and the origins of Shh regulatory novelties. Sci Rep 2012, 2:433. 3364491, 22666536.
40. Irimia M, Tena JJ, Alexis MS, Fernandez-Miñan A, Maeso I, Bogdanovic O, De la Calle-Mustienes E, Roy SW, Gómez-Skarmeta JL, Fraser HB. Extensive conservation of ancient microsynteny across metazoans due to cis-regulatory constraints. Genome Res 2012, 22:2356-2367. 10.1101/gr.139725.112, 22722344.
41. Ellingsen S, Laplante MA, König M, Kikuta H, Furmanek T, Hoivik EA, Becker TS. Large-scale enhancer detection in the zebrafish genome. Development 2005, 132:3799-3811. 10.1242/dev.01951, 16049110.
42. Nóbrega MA, Zhu Y, Plajzer-Frick I, Afzal V, Rubin EM. Megabase deletions of gene deserts result in viable mice. Nature 2004, 431:988-993. 10.1038/nature03022, 15496924.
43. Verma-Kurvari S, Savage T, Smith D, Johnson JE. Multiple elements regulate Mash1 expression in the developing CNS. Dev Biol 1998, 197:106-116. 10.1006/dbio.1998.8873, 9578622.
44. Lee AP, Brenner S, Venkatesh B. Mouse transgenesis identifies conserved functional enhancers and cis-regulatory motif in the vertebrate LIM homeobox gene Lhx2 locus. PLoS One 2011, 6:e20088. 10.1371/journal.pone.0020088, 3100342, 21629789.
45. Potvin E, Beuret L, Cadrin-Girard J-F, Carter M, Roy S, Tremblay M, Charron J. Cooperative action of multiple cis-acting elements is required for N-myc expression in branchial arches: specific contribution of GATA3. Mol Cell Biol 2010, 30:5348-5363. 10.1128/MCB.00353-09, 2976382, 20855530.
46. Wasserman NF, Aneas I, Nobrega MA. An 8q24 gene desert variant associated with prostate cancer risk confers differential in vivo activity to a MYC enhancer. Genome Res 2010, 20:1191-1197. 10.1101/gr.105361.110, 2928497, 20627891.
47. Werner T, Hammer A, Wahlbuhl M, Bösl MR, Wegner M. Multiple conserved regulatory elements with overlapping functions determine Sox10 expression in mouse embryogenesis. Nucleic Acids Res 2007, 35:6526-6538. 10.1093/nar/gkm727, 2095789, 17897962.
48. May D, Blow MJ, Kaplan T, McCulley DJ, Jensen BC, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Afzal V, Simpson PC, Rubin EM, Black BL, Bristow J, Pennacchio LA, Visel A. Large-scale discovery of enhancers from human heart tissue. Nat Genet 2012, 44:89-93.
49. Visel A, Akiyama JA, Shoukry M, Afzal V, Rubin EM, Pennacchio LA. Functional autonomy of distant-acting human enhancers. Genomics 2009, 93:509-513. 10.1016/j.ygeno.2009.02.002, 2683195, 19268701.
50. Visel A, Blow MJ, Li Z, Zhang T, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F, Afzal V, Ren B, Rubin EM, Pennacchio LA. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009, 457:854-858. 10.1038/nature07730, 2745234, 19212405.
51. Kawakami K, Shima A, Kawakami N. Identification of a functional transposase of the Tol2 element, an Ac-like element from the Japanese medaka fish, and its transposition in the zebrafish germ lineage. Proc Natl Acad Sci U S A 2000, 97:11403-11408. 10.1073/pnas.97.21.11403, 17212, 11027340.
52. Royo JL, Bessa J, Hidalgo C, Fernández-Miñán A, Tena JJ, Roncero Y, Gómez-Skarmeta JL, Casares F. Identification and analysis of conserved cis-regulatory regions of the MEIS1 gene. PLoS One 2012, 7:e33617. 10.1371/journal.pone.0033617, 3308983, 22448256.
53. Narlikar L, Sakabe NJ, Blanski AA, Arimura FE, Westlund JM, Nobrega MA, Ovcharenko I. Genome-wide discovery of human heart enhancers. Genome Res 2010, 20:381-392. 10.1101/gr.098657.109, 2840982, 20075146.
54. McGaughey DM, McCallion AS. Efficient discovery of ASCL1 regulatory sequences through transgene pooling. Genomics 2010, 95:363-369. 10.1016/j.ygeno.2010.02.011, 2904508, 20206680.
55. Beermann F, Kaloulis K, Hofmann D, Murisier F, Bucher P, Trumpp A. Identification of evolutionarily conserved regulatory elements in the mouse Fgf8 locus. Genesis 2006, 44:1-6. 10.1002/gene.20177, 16397882.
56. Takahasi KR, Matsuo T, Takano-Shimizu-Kouno T. Two types of cis-trans compensation in the evolution of transcriptional regulation. Proc Natl Acad Sci U S A 2011, 108:15276-15281. 10.1073/pnas.1105814108, 3174679, 21876147.
57. Goncalves A, Leigh-Brown S, Thybert D, Stefflova K, Turro E, Flicek P, Brazma A, Odom DT, Marioni JC. Extensive compensatory cis-trans regulation in the evolution of mouse gene expression. Genome Res 2012, 22:2376-2384. 10.1101/gr.142281.112, 3514667, 22919075.
58. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn 1995, 203:253-310. 10.1002/aja.1002030302, 8589427.
59. Lee AP, Kerk SY, Tan YY, Brenner S, Venkatesh B. Ancient vertebrate conserved noncoding elements have been evolving rapidly in teleost fishes. Mol Biol Evol 2011, 28:1205-1215. 10.1093/molbev/msq304, 21081479.
60. Sprague J, Bayraktaroglu L, Clements D, Conlin T, Fashena D, Frazer K, Haendel M, Howe DG, Mani P, Ramachandran S, Schaper K, Segerdell E, Song P, Sprunger B, Taylor S, Van Slyke CE, Westerfield M. The zebrafish information network: the zebrafish model organism database. Nucleic Acids Res 2006, 34:D581-D585. 10.1093/nar/gkj086, 1347449, 16381936.
61. Blader P, Plessy C, Strähle U. Multiple regulatory elements with spatially and temporally distinct activities control neurogenin1 expression in primary neurons of the zebrafish embryo. Mech Dev 2003, 120:211-218. 10.1016/S0925-4773(02)00413-6, 12559493.
62. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, Clawson H, Spieth J, Hillier LW, Richards S, Weinstock GM, Wilson RK, Gibbs RA, Kent WJ, Miller W, Haussler D. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 2005, 15:1034-1050. 10.1101/gr.3715005, 1182216, 16024819.
63. Akalin A, Fredman D, Arner E, Dong X, Bryne JC, Suzuki H, Daub CO, Hayashizaki Y, Lenhard B. Transcriptional features of genomic regulatory blocks. Genome Biol 2009, 10:R38. 10.1186/gb-2009-10-4-r38, 2688929, 19374772.
64. Dong X, Fredman D, Lenhard B. Synorth: exploring the evolution of synteny and long-range regulatory interactions in vertebrate genomes. Genome Biol 2009, 10:R86. 10.1186/gb-2009-10-8-r86, 2745767, 19698106.
65. Finger JH, Smith CM, Hayamizu TF, McCright IJ, Eppig JT, Kadin JA, Richardson JE, Ringwald M. The mouse gene expression database (GXD): 2011 update. Nucleic Acids Res 2011, 39:D835-D841. 10.1093/nar/gkq1132, 3013713, 21062809.
66. Richardson L, Venkataraman S, Stevenson P, Yang Y, Burton N, Rao J, Fisher M, Baldock RA, Davidson DR, Christiansen JH. EMAGE mouse embryo spatial gene expression database: 2010 update. Nucleic Acids Res 2010, 38:D703-D709. 10.1093/nar/gkp763, 2808994, 19767607.
67. Diez-Roux G, Banfi S, Sultan M, Geffers L, Anand S, Rozado D, Magen A, Canidio E, Pagani M, Peluso I, Lin-Marq N, Koch M, Bilio M, Cantiello I, Verde R, De Masi C, Bianchi SA, Cicchini J, Perroud E, Mehmeti S, Dagand E, Schrinner S, Nürnberger A, Schmidt K, Metz K, Zwingmann C, Brieske N, Springer C, Hernandez AM, Herzog S, et al. A high-resolution anatomical atlas of the transcriptome in the mouse embryo. PLoS Biol 2011, 9:e1000582. 10.1371/journal.pbio.1000582, 3022534, 21267068.
68. Visel A, Thaller C, Eichele G. GenePaint.org: an atlas of gene expression patterns in the mouse embryo. Nucleic Acids Res 2004, 32:D552-D556. 10.1093/nar/gkh029, 308763, 14681479.
69. Bradford Y, Conlin T, Dunn N, Fashena D, Frazer K, Howe DG, Knight J, Mani P, Martin R, Moxon SAT, Paddock H, Pich C, Ramachandran S, Ruef BJ, Ruzicka L, Bauer Schaper H, Schaper K, Shao X, Singer A, Sprague J, Sprunger B, Van Slyke C, Westerfield M ZFIN. Enhancements and updates to the zebrafish model organism database. Nucleic Acids Res 2011, 39:D822-D829. 10.1093/nar/gkq1077, 3013679, 21036866.
70. Gawantka V, Delius H, Hirschfeld K, Blumenstock C, Niehrs C. Antagonizing the Spemann organizer: role of the homeobox gene Xvent-1. EMBO J 1995, 14:6268-6279. 394751, 8557046.
71. Tena JJ, Neto A, De la Calle-Mustienes E, Bras-Pereira C, Casares F, Gómez-Skarmeta JL. Odd-skipped genes encode repressors that control kidney development. Dev Biol 2007, 301:518-531. 10.1016/j.ydbio.2006.08.063, 17011543.