Functional analysis of conserved non-coding regions around the short stature hox gene (shox) in whole Zebrafish embryos

PLoS ONE

Volumn 6, Issue 6, 2011, Pages

  Kenyon, Emma J ^a   McEwen, Gayle K ^b   Callaway, Heather ^c   Elgar, Greg ^d  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EMBRYO; ANIMAL TISSUE; ARTICLE; CONSERVED NON CODING ELEMENT; CONTROLLED STUDY; EMBRYO; ENHANCER REGION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOCUS; GENE SEQUENCE; GENE STRUCTURE; IN SITU HYBRIDIZATION; NONHUMAN; REGULATOR GENE; SHOX GENE; TISSUE DISTRIBUTION; ZEBRA FISH; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; DUPLICATE GENE; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PRENATAL DEVELOPMENT; PUFFER FISH; SEQUENCE ALIGNMENT;

CANIS FAMILIARIS; DANIO RERIO; DIDELPHIDAE; RODENTIA; TAKIFUGU;

GREEN FLUORESCENT PROTEIN; SHOX2 PROTEIN, ZEBRAFISH; SPACER DNA; TRANSCRIPTION FACTOR; ZEBRAFISH PROTEIN;

AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; DNA, INTERGENIC; EMBRYO, NONMAMMALIAN; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, DUPLICATE; GENETIC LOCI; GREEN FLUORESCENT PROTEINS; HUMANS; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; TAKIFUGU; TRANSCRIPTION FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 79959588043     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021498     Document Type: Article

References (39)

1. Shears DJ, Vassal HJ, Goodman FR, Palmer RW, Reardon W, et al. (1998) Mutation and deletion of the pseudoautosomal gene SHOX cause Leri-Weill Dyschondrosteosis. Nature Genetics 19: 70-73.
2. Rao E, Weiss B, Fukami1 M, Rump A, Niesler B, et al. (1997) Pseudoautosomal deletions encompassing a novel homeobox gene cause growth failure in idiopathic short stature and Turner syndrome. Nature Genetics 16: 54-63.
3. Ellison JW, Wardak Z, Young MF, Robey PG, Laig-Webster M, et al. (1997) PHOG, a Candidate Gene for Involvement in the Short Stature of Turner Syndrome. Human Molecular Genetics 6: 1341-1347.
4. Ogata T, Muroya K, Matsuo N, Shinohara O, Yorifuji T, et al. (2001) Turner syndrome and Xp deletions: clinical and molecular studies in 47 patients. Clin Endocrinol Metab 86: 5498-508.
5. Ross JL, Scott C Jr, Marttila P, Kowal K, Nass A, et al. (2001) Phenotypes Associated with SHOX Deficiency. The Journal of Clinical Endocrinology & Metabolism 86: 5674-5680.
6. Clement-Jones M, Schiller S, Rao E, Blaschke RJ, Zuniga A, et al. (2000) The short stature homeobox gene SHOX is involved in skeletal abnormalities in Turner syndrome. Human Mol Genet 9: 695-702.
7. Tiecke E, Bangs F, Blaschke R, Farrell ER, Rappold G, et al. (2006) Expression of the short stature homeobox gene Shox is restricted by proximal and distal signals in chick limb buds and affects the length of skeletal elements. Dev Biol 298: 585-96.
8. Clement-Jones M, Schiller S, Rao E, Blaschke RJ, Zuniga A, et al. (2000) The short stature homeobox gene SHOX is involved in skeletal abnormalities in Turner syndrome. Hum Mol Genet 9: 695-702.
9. Blaschke RJ, Monaghan AP, Schiller S, Schechinger B, Rao E, et al. (1998) SHOT, a SHOX-related homeobox gene, is implicated in craniofacial, brain, heart, and limb development. PNAS 95: 2406-2411.
10. Sabherwal N, Bangs F, Röth R, Weiss B, Jantz K, et al. (2007) Long-range conserved non-coding SHOX sequences regulate expression in developing chicken limb and are associated with short stature phenotypes in human patients. Hum Mol Genet 16: 210-222.
11. Brudno M, Do CB, Cooper GM, Kim MF, Davydov E, et al. (2003) LAGAN and Multi-LAGAN: efficient tools for large-scale multiple alignment of genomic DNA. Genome Res 13: 721-731.
12. Woolfe A, Goode DK, Cooke J, Callaway H, Smith S, et al. (2007) CONDOR: a database resource of developmentally associated conserved non-coding elements. BMC Dev Biol 7: 100-111.
13. Fried C, Prohaska SJ, Stadler PF, (2003) Independent Hox-cluster duplications in lampreys. J Exp Zool B Mol Dev Evol 299: 18-25.
14. McEwen GK, Woolfe A, Goode D, Vavouri T, Callaway H, et al. (2006) Ancient duplicated conserved noncoding elements in vertebrates: a genomic and functional analysis. Genome Res 16: 451-65.
15. Goode DK, Callaway HA, Cerda GA, Lewis KE, Elgar G, (2011) Minor change, major difference: divergent functions of highly conserved cis-regulatory elements subsequent to whole genome duplication events. Development 138: 879-884.
16. Grandel H, Schulte-Merker S, (1998) The development of the paired fins in the zebrafish (Danio rerio). Mech Dev 79: 99-120.
17. Dane PJ, Tucker JB, (1985) Modulation of epidermal cell shaping and extracellular matrix during caudal fin morphogenesis in the zebra fish Brachydanio rerio. J Embryol Exp Morphol 87: 145-161.
18. Krauss S, Concordet JP, Ingham PW, (1993) A functionally conserved homolog of the Drosophila segment polarity gene hh is expressed in tissues with polarizing activity in zebrafish embryos. Cell 75: 1431-1444.
19. Akimenko MA, Ekker M, (1995) Anterior duplication of the Sonic hedgehog expression pattern in the pectoral fin buds of zebrafish treated with retinoic acid. Dev Biol 170: 243-247.
20. Riddle RD, Johnson RL, Laufer E, Tabin C, (1993) Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75: 1401-1416.
21. Loomis CA, Harris E, Michaud J, Wurst W, Hanks M, et al. (1996) The mouse Engrailed-1 gene and ventral limb patterning. Nature 382: 360-363.
22. Riddle RD, Ensini M, Nelson C, Tsuchida T, Jessell TM, et al. (1995) Induction of the LIM homeobox gene Lmx1 by WNT7a establishes dorsoventral pattern in the vertebrate limb. Cell 83: 631-640.
23. Avaron F, Smith A, Akimenko MA, (2007) Shh and Gli Signalling and Development. Publisher: Springer New York DOI: 10.1007/978-0-387-39957-7 Copyright: 2007 ISBN: 978-0-387-39956-0 (Print 978-0-387-39957-7 (Online).
24. Freitas R, Zhang GJ, Cohn MJ, (2006) Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature 442: 1033-1037.
25. Gillis JA, Dahn RD, Shubin NH, (2009) Shared developmental mechanisms pattern the vertebrate gill arch and paired fin skeletons. PNAS 106: 5720-5724.
26. Spranger S, Schiller S, Jauch A, Wolff K, Rauterberg-Ruland I, et al. (1999) Léri-Weill syndrome as part of a contiguous gene syndrome at Xp22.3. Am J Med Genet 83: 367-371.
27. Robertson SP, Shears DJ, Oei P, Winter RM, Scambler PJ, et al. (2000) Homozygous deletion of SHOX in a mentally retarded male with Langer mesomelic dysplasia. J Med Genetics 37: 959-964.
28. Zinn AR, Wei F, Zhang L, Elder FF, Scott CI Jr, et al. (2002) Complete SHOX deficiency causes Langer mesomelic dysplasia. Am J Med Genet 110: 158-163.
29. Kozak M, (2001) Constraints on reinitiation of translation in mammals. Nucl Acids Res 29: 5226-5232.
30. Losson R, Lacroute F, (1979) Interference of nonsense mutations with eukaryotic messenger mRNA stability. Proc Natl Acad Sci U S A 76: 5134-5137.
31. Thisse B, Thisse C, (2004) Fast Release Clones: A High Throughput Expression Analysis. ZFIN Direct Data Submission. Zfin website. Available: http://zfin.org/cgi-bin/webdriver?MIval=aa-markerview.apg&OID=ZDB-GENE-040426-1457 Accessed 2011 Jun 7.
32. Blaschke RJ, Hahurij ND, Kuijper S, Just S, Wisse LJ, et al. (2007) Targeted mutation reveals essential functions of the homeodomain transcription factor Shox2 in sinoatrial and pacemaking development. Circulation 115: 1830-1838.
33. Vickerman L, Neufeld S, Cobb J, (2011) Shox2 function couples neural, muscular and skeletal development in the proximal forelimb. Dev Biol 350: 323-36.
34. Durand C, Bangs F, Signolet J, Decker E, Tickle C, et al. (2010) Enhancer elements upstream of the SHOX gene are active in the developing limb. Eur J Hum 18: 527-532.
35. Muller F, Williams DW, Kobolak J, Gauvry L, Goldspink G, et al. (1997) Activator effect of coinjected enhancers on the muscle-specific expression of promoters in zebrafish embryos. Mol Reprod Dev 47: 404-412.
36. Woolfe A, Goodson M, Goode DK, Snell P, McEwen GK, et al. (2005) Highly Conserved Non-Coding Sequences Are Associated with Vertebrate Development. PLoS Biol 3 (1): e7.
37. Thisse B, Thisse C, Zfin website Available: http://zfin.org/ZFIN/Methods/ThisseProtocol.html Accessed 2011 Jun 7.
38. Westerfield M, (2000) The zebrafish book: A guide for the laboratory use of zebrafish (Danio rerio). 4th ed Eugene (Oregon) University of Oregon Press.
39. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF, (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310.