Lens development depends on a pair of highly conserved Sox21 regulatory elements

Developmental Biology

Volumn 365, Issue 1, 2012, Pages 310-318

  Pauls, Stefan ^a   Smith, Sarah F ^a   Elgar, Greg ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Conserved non coding elements; Enhancer; Lens; Sox21; Zebrafish

Indexed keywords

PROTEIN SOX21; TRANSCRIPTION FACTOR SOX; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BINDING SITE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMBRYO; EMBRYO DEVELOPMENT; ENHANCER REGION; EYE DEVELOPMENT; GENE EXPRESSION; GENE FUNCTION; GENE LOCUS; GENE REGULATORY NETWORK; GENE SEQUENCE; GENETIC CODE; GENETIC CONSERVATION; GENETIC LINKAGE; GENOME ANALYSIS; LENS DEVELOPMENT; LENS DISEASE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN FUNCTION; REGULATOR GENE; SOX21 GENE; VERTEBRATE; ZEBRA FISH;

DANIO RERIO; MAMMALIA; TETRAODONTIDAE; VERTEBRATA;

EID: 84862805898     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.02.025     Document Type: Article

References (46)

1. Abramoff M.D., Magelhaes P.J., Ram S.J. Image processing with ImageJ. Biophotonics Int. 2004, 11:7.
2. Ahituv N., Zhu Y., Visel A., Holt A., Afzal V., Pennacchio L.A., Rubin E.M. Deletion of ultraconserved elements yields viable mice. PLoS Biol. 2007, 5:e234.
3. Albert H., Dale E.C., Lee E., Ow D.W. Site-specific integration of DNA into wild-type and mutant lox sites placed in the plant genome. Plant J. 1995, 7:649-659.
4. Bejerano G., Pheasant M., Makunin I., Stephen S., Kent W.J., Mattick J.S., Haussler D. Ultraconserved elements in the human genome. Science 2004, 304:1321-1325.
5. Betancur P., Sauka-Spengler T., Bronner M. A Sox10 enhancer element common to the otic placode and neural crest is activated by tissue-specific paralogs. Development 2011, 138:3689-3698.
6. Chen X., Xu H., Yuan P., Fang F., Huss M., Vega V.B., Wong E., Orlov Y.L., Zhang W., Jiang J., Loh Y.H., Yeo H.C., Yeo Z.X., Narang V., Govindarajan K.R., Leong B., Shahab A., Ruan Y., Bourque G., Sung W.K., Clarke N.D., Wei C.L., Ng H.H. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008, 133:1106-1117.
7. Couronne O., Poliakov A., Bray N., Ishkhanov T., Ryaboy D., Rubin E., Pachter L., Dubchak I. Strategies and tools for whole-genome alignments. Genome Res. 2003, 13:73-80.
8. Cunningham D.D., Meng Z., Fritzsch B., Casey E.S. Cloning and developmental expression of the soxB2 genes, sox14 and sox21, during Xenopus laevis embryogenesis. Int. J. Dev. Biol. 2008, 52:999-1004.
9. Dahm R., Schonthaler H.B., Soehn A.S., van Marle J., Vrensen G.F. Development and adult morphology of the eye lens in the zebrafish. Exp. Eye Res. 2007, 85:74-89.
10. Fisher S., Grice E.A., Vinton R.M., Bessling S.L., Urasaki A., Kawakami K., McCallion A.S. Evaluating the biological relevance of putative enhancers using Tol2 transposon-mediated transgenesis in zebrafish. Nat. Protoc. 2006, 1:1297-1305.
11. Frankel N., Davis G.K., Vargas D., Wang S., Payre F., Stern D.L. Phenotypic robustness conferred by apparently redundant transcriptional enhancers. Nature 2010, 466:490-493.
12. Howard M.L., Davidson E.H. cis-Regulatory control circuits in development. Dev. Biol. 2004, 271:109-118.
13. Jeong Y., El-Jaick K., Roessler E., Muenke M., Epstein D.J. A functional screen for sonic hedgehog regulatory elements across a 1 Mb interval identifies long-range ventral forebrain enhancers. Development 2006, 133:761-772.
14. Jeong Y., Leskow F.C., El-Jaick K., Roessler E., Muenke M., Yocum A., Dubourg C., Li X., Geng X., Oliver G., Epstein D.J. Regulation of a remote Shh forebrain enhancer by the Six3 homeoprotein. Nat. Genet. 2008, 40:1348-1353.
15. Kamachi Y., Sockanathan S., Liu Q., Breitman M., Lovell-Badge R., Kondoh H. Involvement of SOX proteins in lens-specific activation of crystallin genes. EMBO J. 1995, 14:3510-3519.
16. Kamachi Y., Uchikawa M., Collignon J., Lovell-Badge R., Kondoh H. Involvement of Sox1, 2 and 3 in the early and subsequent molecular events of lens induction. Development 1998, 125:2521-2532.
17. Kawakami K., Takeda H., Kawakami N., Kobayashi M., Matsuda N., Mishina M. A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev. Cell 2004, 7:133-144.
18. Kiso M., Tanaka S., Saba R., Matsuda S., Shimizu A., Ohyama M., Okano H.J., Shiroishi T., Okano H., Saga Y. The disruption of Sox21-mediated hair shaft cuticle differentiation causes cyclic alopecia in mice. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:9292-9297.
19. Lakowski J., Majumder A., Lauderdale J.D. Mechanisms controlling Pax6 isoform expression in the retina have been conserved between teleosts and mammals. Dev. Biol. 2007, 307:498-520.
20. Lan X., Wen L., Li K., Liu X., Luo B., Chen F., Xie D., Kung H.F. Comparative analysis of duplicated sox21 genes in zebrafish. Dev. Growth Differ. 2011, 53:347-356.
21. Lee G., Saito I. Role of nucleotide sequences of loxP spacer region in Cre-mediated recombination. Gene 1998, 216:55-65.
22. Lee E.C., Yu D., Martinez de Velasco J., Tessarollo L., Swing D.A., Court D.L., Jenkins N.A., Copeland N.G. A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 2001, 73:56-65.
23. Loh Y.H., Wu Q., Chew J.L., Vega V.B., Zhang W., Chen X., Bourque G., George J., Leong B., Liu J., Wong K.Y., Sung K.W., Lee C.W., Zhao X.D., Chiu K.P., Lipovich L., Kuznetsov V.A., Robson P., Stanton L.W., Wei C.L., Ruan Y., Lim B., Ng H.H. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat. Genet. 2006, 38:431-440.
24. McEwen G.K., Goode D.K., Parker H.J., Woolfe A., Callaway H., Elgar G. Early evolution of conserved regulatory sequences associated with development in vertebrates. PLoS Genet. 2009, 5:e1000762.
25. Meng A., Tang H., Ong B.A., Farrell M.J., Lin S. Promoter analysis in living zebrafish embryos identifies a cis-acting motif required for neuronal expression of GATA-2. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:6267-6272.
26. Muller F., Williams D.W., Kobolak J., Gauvry L., Goldspink G., Orban L., Maclean N. Activator effect of coinjected enhancers on the muscle-specific expression of promoters in zebrafish embryos. Mol. Reprod. Dev. 1997, 47:404-412.
27. Nasevicius A., Ekker S.C. Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 2000, 26:216-220.
28. Nishiguchi S., Wood H., Kondoh H., Lovell-Badge R., Episkopou V. Sox1 directly regulates the gamma-crystallin genes and is essential for lens development in mice. Genes Dev. 1998, 12:776-781.
29. Nobrega M.A., Zhu Y., Plajzer-Frick I., Afzal V., Rubin E.M. Megabase deletions of gene deserts result in viable mice. Nature 2004, 431:988-993.
30. Pennacchio L.A., Ahituv N., Moses A.M., Prabhakar S., Nobrega M.A., Shoukry M., Minovitsky S., Dubchak I., Holt A., Lewis K.D., Plajzer-Frick I., Akiyama J., De Val S., Afzal V., Black B.L., Couronne O., Eisen M.B., Visel A., Rubin E.M. In vivo enhancer analysis of human conserved non-coding sequences. Nature 2006, 444:499-502.
31. Perry M.W., Boettiger A.N., Bothma J.P., Levine M. Shadow enhancers foster robustness of Drosophila gastrulation. Curr. Biol. : CB 2010, 20:1562-1567.
32. Poitras L., Yu M., Lesage-Pelletier C., MacDonald R.B., Gagne J.-P., Hatch G., Kelly I., Hamilton S.P., Rubenstein J.L.R., Poirier G.G., Ekker M. An SNP in an ultraconserved regulatory element affects Dlx5/Dlx6 regulation in the forebrain. Development 2010, 137:3089-3097.
33. Rex M., Uwanogho D.A., Orme A., Scotting P.J., Sharpe P.T. cSox21 exhibits a complex and dynamic pattern of transcription during embryonic development of the chick central nervous system. Mech. Dev. 1997, 66:39-53.
34. Rimini R., Beltrame M., Argenton F., Szymczak D., Cotelli F., Bianchi M.E. Expression patterns of zebrafish sox11A, sox11B and sox21. Mech. Dev. 1999, 89:167-171.
35. Royo J.L., Maeso I., Irimia M., Gao F., Peter I.S., Lopes C.S., D'Aniello S., Casares F., Davidson E.H., Garcia-Fernandez J., Gomez-Skarmeta J.L. Transphyletic conservation of developmental regulatory state in animal evolution. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:14186-14191.
36. Sagai T., Hosoya M., Mizushina Y., Tamura M., Shiroishi T. Elimination of a long-range cis-regulatory module causes complete loss of limb-specific Shh expression and truncation of the mouse limb. Development 2005, 132:797-803.
37. Sagai T., Amano T., Tamura M., Mizushina Y., Sumiyama K., Shiroishi T. A cluster of three long-range enhancers directs regional Shh expression in the epithelial linings. Development 2009, 136:1665-1674.
38. Sandberg M., Kallstrom M., Muhr J. Sox21 promotes the progression of vertebrate neurogenesis. Nat. Neurosci. 2005, 8:995-1001.
39. Sandelin A., Alkema W., Engstrom P., Wasserman W.W., Lenhard B. JASPAR: an open-access database for eukaryotic transcription factor binding profiles. Nucleic Acids Res. 2004, 32:D91-D94.
40. Sandelin A., Bailey P., Bruce S., Engstrom P.G., Klos J.M., Wasserman W.W., 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.
41. Thisse C., Thisse B. High Resolution Whole-Mount In Situ Hybridization 1998, Univ. of Oregon Press, Eugene.
42. Uchikawa M., Kamachi Y., Kondoh H. Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors: their expression during embryonic organogenesis of the chicken. Mech. Dev. 1999, 84:103-120.
43. Uchikawa M., Ishida Y., Takemoto T., Kamachi Y., Kondoh H. Functional analysis of chicken Sox2 enhancers highlights an array of diverse regulatory elements that are conserved in mammals. Dev. Cell 2003, 4:509-519.
44. Venkatesh B., Kirkness E.F., Loh Y.H., Halpern A.L., Lee A.P., Johnson J., Dandona N., Viswanathan L.D., Tay A., Venter J.C., Strausberg R.L., Brenner S. Ancient noncoding elements conserved in the human genome. Science 2006, 314:1892.
45. Woolfe A., Goodson M., Goode D.K., Snell P., McEwen G.K., Vavouri T., Smith S.F., North P., Callaway H., Kelly K., Walter K., Abnizova I., Gilks W., Edwards Y.J., Cooke J.E., Elgar G. Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol. 2005, 3:e7.
46. Woolfe A., Goode D.K., Cooke J., Callaway H., Smith S., Snell P., McEwen G.K., Elgar G. CONDOR: a database resource of developmentally associated conserved non-coding elements. BMC Dev. Biol. 2007, 7:100.