Genome-wide identification of signaling center enhancers in the developing limb

Development (Cambridge)

Volumn 141, Issue 21, 2014, Pages 4194-4198

  Vandermeer, Julia E ^a   Smith, Robin P ^a   Jones, Stacy L ^a   Ahituv, Nadav ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

AER; Enhancer; Limb; Mouse; ZPA

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASSAY; CONTROLLED STUDY; DISSECTION; EMBRYO; ENHANCER REGION; FEMALE; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GENE SEQUENCE; GENOME; LIMB DEVELOPMENT; LIMB MALFORMATION; MALE; MOUSE; NONHUMAN; TRANSGENICS; ANIMAL; CYTOLOGY; ECTODERM; EMBRYOLOGY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETICS; LIMB BUD; METABOLISM; ORGANOGENESIS; PHYSIOLOGY; PREGNANCY;

SONIC HEDGEHOG PROTEIN;

ANIMALS; ECTODERM; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; LIMB BUDS; MICE; ORGANOGENESIS; PREGNANCY;

EID: 84908042311     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.110965     Document Type: Article

References (29)

1. Anderson, E., Peluso, S., Lettice, L. A. and Hill, R. E. (2012). Human limb abnormalities caused by disruption of hedgehog signaling. Trends Genet. 28, 364-373
2. Bell, S. M., Schreiner, C. M., Waclaw, R. R., Campbell, K., Potter, S. S. and Scott, W. J. (2003). Sp8 is crucial for limb outgrowth and neuropore closure. Proc. Natl. Acad. Sci. USA 100, 12195-12200
3. Cotney, J., Leng, J., Oh, S., DeMare, L. E., Reilly, S. K., Gerstein, M. B. and Noonan, J. P. (2012). Chromatin state signatures associated with tissue-specific gene expression and enhancer activity in the embryonic limb. Genome Res. 22, 1069-1080
4. Cotney, J., Leng, J., Yin, J., Reilly, S. K., DeMare, L. E., Emera, D., Ayoub, A. E., Rakic, P. and Noonan, J. P. (2013). The evolution of lineage-specific regulatory activities in the human embryonic limb. Cell 154, 185-196
5. Cretekos, C. J., Wang, Y., Green, E. D., Martin, J. F., Rasweiler, J. J. and Behringer, R. R. (2008). Regulatory divergence modifies limb length between mammals. Genes Dev. 22, 141-151
6. Creyghton, M. P., Cheng, A. W., Welstead, G. G., Kooistra, T., Carey, B. W., Steine, E. J., Hanna, J., Lodato, M. A., Frampton, G. M., Sharp, P. A. et al. (2010). Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. USA 107, 21931-21936
7. Dathe, K., Kjaer, K. W., Brehm, A., Meinecke, P., Nürnberg, P., Neto, J. C., Brunoni, D., Tommerup, N., Ott, C. E., Klopocki, E. et al. (2009). Duplications involving a conserved regulatory element downstream of BMP2 are associated with brachydactyly type A2 Am. J. Hum. Genet. 84, 483-492
8. Harfe, B. D., Scherz, P. J., Nissim, S., Tian, H., McMahon, A. P. and Tabin, C. J. (2004). Evidence for an Expansion-based temporal SHH gradient in specifying vertebrate digit identities. Cell 118, 517-528
9. Kothary, R., Clapoff, S., Darling, S., Perry, M. D., Moran, L. A. and Rossant, J. (1989). Inducible expression of an hsp68-lacZ hybrid gene in transgenic mice. Development 105, 707-714
10. Kurth, I., Klopocki, E., Stricker, S., van Oosterwijk, J., Vanek, S., Altmann, J., Santos, H. G., van Harssel, J. J. T., de Ravel, T., Wilkie, A. O. M. et al. (2009). Duplications of noncoding elements 5′ of SOX9 are associated with brachydactyly-anonychia. Nat. Genet. 41, 862-863
11. Langmead, B., Trapnell, C., Pop, M. and Salzberg, S. L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25
12. Larkins, C. E., Aviles, G. D. G., East, M. P., Kahn, R. A. and Caspary, T. (2011). Arl13b regulates ciliogenesis and the dynamic localization of Shh signaling proteins. Mol. Biol. Cell 22, 4694-4703
13. Lettice, L. A., Heaney, S. J. H., Purdie, L. A., Li, L., de Beer, P., Oostra, B. A., Goode, D., Elgar, G., Hill, R. E. and de Graaff, E. (2003). A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum. Mol. Genet. 12, 1725-1735
14. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G. and Durbin, R. (2009). The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078-2079
15. McLean, C. Y., Bristor, D., Hiller, M., Clarke, S. L., Schaar, B. T., Lowe, C. B., Wenger, A. M. and Bejerano, G. (2010). GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495-501
16. Moore, K. L. and Persaud, T. V. N. (1998). The Developing Human: Clinically Oriented Embryology, 6th edn. Philadelphia: Saunders.
17. Nagy, A., Gertsenstein, M., Vintersten, K. and Behringer, R. (2002). Manipulating the Mouse Embryo: A Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
18. Pennacchio, L. A., Ahituv, N., Moses, A. M., Prabhakar, S., Nobrega, M. A., Shoukry, M., Minovitsky, S., Dubchak, I., Holt, A., Lewis, K. D. et al. (2006). In vivo enhancer analysis of human conserved non-coding sequences. Nature 444, 499-502
19. Quinlan, A. R. and Hall, I. M. (2010). BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841-842
20. Rada-Iglesias, A., Bajpai, R., Prescott, S., Brugmann, S. A., Swigut, T. and Wysocka, J. (2012). Epigenomic annotation of enhancers predicts transcriptional regulators of human neural crest. Cell Stem Cell 11, 633-648
21. Rock, J. R., Lopez, M. C., Baker, H. V. and Harfe, B. D. (2007). Identification of genes expressed in the mouse limb using a novel ZPA microarray approach. Gene Expr. Patterns 8, 19-26
22. Stoller, J. Z., Degenhardt, K. R., Huang, L., Zhou, D. D., Lu, M. M. and Epstein, J. A. (2008). Cre reporter mouse expressing a nuclear localized fusion of GFP and β-galactosidase reveals new derivatives of Pax3-expressing precursors. Genesis 46, 200-204
23. Sun, X., Lewandoski, M., Meyers, E. N., Liu, Y.-H., Maxson, R. E. and Martin, G. R. (2000). Conditional inactivation of Fgf4 reveals complexity of signalling during limb bud development. Nat. Genet. 25, 83-86
24. VanderMeer, J. E. and Ahituv, N. (2011). cis-regulatory mutations are a genetic cause of human limb malformations. Dev. Dyn. 240, 920-930
25. Visel, A., Minovitsky, S., Dubchak, I. and Pennacchio, L. A. (2007). VISTA Enhancer Browser–a database of tissue-specific human enhancers. Nucleic Acids Res. 35, D88-D92
26. Visel, A., Blow, M. J., Li, Z., Zhang, T., Akiyama, J. A., Holt, A., Plajzer-Frick, I., Shoukry, M., Wright, C., Chen, F. et al. (2009). ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457, 854-858
27. Xu, X., Weinstein, M., Li, C., Naski, M., Cohen, R. I., Ornitz, D. M., Leder, P. and Deng, C. (1998). Fibroblast growth factor receptor 2 (FGFR2)-mediated reciprocal regulation loop between FGF8 and FGF10 is essential for limb induction. Development 125, 753-765
28. Zang, C., Schones, D. E., Zeng, C., Cui, K., Zhao, K. and Peng, W. (2009). A clustering approach for identification of enriched domains from histone modification ChIP-Seq data. Bioinformatics 25, 1952-1958
29. Zeller, R., López-Ríos, J. and Zuniga, A. (2009). Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat.Rev.Genet. 10, 845-858.