Alterations to the remote control of Shh gene expression cause congenital abnormalities

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1620, 2013, Pages

  Hill, Robert E ^a   Lettice, Laura A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Limb development; Long range regulation; Preaxial polydactyly; Shh

Indexed keywords

ABNORMALITY; GENE EXPRESSION; MUTATION; PARADIGM SHIFT;

EID: 84891377732     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0357     Document Type: Article

References (38)

1. Ovcharenko I, Loots GG, Nobrega MA, Hardison RC, Miller W, Stubbs L. 2005 Evolution and functional classification of vertebrate gene deserts. Genome Res. 15, 137-145. (doi:10.1101/gr.3015505)
2. Bernstein BE, Birney E, Dunham I, Green ED, Gunter C, Snyder M. 2012 An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74. (doi:10.1038/nature11247)
3. Jeong Y, Epstein DJ. 2003 Distinct regulators of Shh transcription in the floor plate and notochord indicate separate origins for these tissues in the mouse node. Development 130, 3891-3902. (doi:10.1242/dev.00590)
4. Jeong Y, El Jaick K, Roessler E, Muenke M, Epstein DJ. 2006 A functional screen for sonic hedgehog regulatory elements across a 1 Mb interval identifies long-range ventral forebrain enhancers. Development 133, 761-772. (doi:10.1242/dev.02239)
5. Lettice LA et al. 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. (doi:10.1093/ hmg/ddg180)
6. Sagai T, Amano T, Tamura M, Mizushina Y, Sumiyama K, Shiroishi T. 2009 A cluster of three long-range enhancers directs regional Shh expression in the epithelial linings. Development 136, 1665-1674. (doi:10.1242/dev.032714)
7. Sagai T, Hosoya M, Mizushina Y, Tamura M, Shiroishi T. 2005 Elimination of a long-range cis-regulatory module causes complete loss of limb-specific Shh expression and truncation of the mouse limb. Development 132, 797-803. (doi:10.1242/dev.01613)
8. Lettice LA, Hill AE, Devenney PS, Hill RE. 2008 Point mutations in a distant sonic hedgehog cis-regulator generate a variable regulatory output responsible for preaxial polydactyly. Hum. Mol. Genet. 17, 978-985. (doi:10.1093/hmg/ddm370)
9. Hill RE. 2007 How to make a zone of polarizing activity: insights into limb development via the abnormality preaxial polydactyly. Dev. Growth Differ. 49, 439-448. (doi:10.1111/j.1440-169X.2007.00943.x)
10. Dahn RD, Davis MC, Pappano WN, Shubin NH. 2007 Sonic hedgehog function in chondrichthyan fins and the evolution of appendage patterning. Nature 445, 311-314. (doi:10.1038/nature05436)
11. Belloni E et al. 1996 Identification of Sonic hedgehog as a candidate gene responsible for holoprosencephaly. Nat. Genet. 14, 353-356. (doi:10.1038/ng1196-353)
12. Kleinjan DJ, van Heyningen V. 1998 Position effect in human genetic disease. Hum. Mol. Genet. 7, 1611-1618. (doi:10.1093/hmg/7.10.1611)
13. Lettice LA et al. 2011 Enhancer-adoption as a mechanism of human developmental disease. Hum. Mutat. 32, 1492-1499. (doi:10.1002/humu.21615)
14. Anderson E, Peluso S, Lettice LA, Hill RE. 2012 Human limb abnormalities caused by disruption of hedgehog signaling. Trends Genet. 28, 364-373. (doi:10.1016/j.tig.2012.03.012)
15. Wieczorek D et al. 2010 A specific mutation in the distant sonic hedgehog (SHH) cis-regulator (ZRS) causes Werner mesomelic syndrome (WMS) while complete ZRS duplications underlie Haas type polysyndactyly and preaxial polydactyly (PPD) with or without triphalangeal thumb. Hum. Mutat. 31, 81-89. doi:10.1002/humu.21142)
16. Al-Qattan MM, Al Abdulkareem I, Al Haidan Y, Al Balwi M. 2012 A novel mutation in the SHH longrange regulator (ZRS) is associated with preaxial polydactyly, triphalangeal thumb, and severe radial ray deficiency. Am. J. Med. Genet. A 158A, 2610-2615. (doi:10.1002/ajmg.a.35584)
17. Albuisson J, Isidor B, Giraud M, Pichon O, Marsaud T, David A, Le Caignec C, Bezieau S. 2011 Identification of two novel mutations in Shh longrange regulator associated with familial pre-axial polydactyly. Clin. Genet. 79, 371-377. (doi:10. 1111/j.1399-0004.2010.01465.x)
18. Farooq M et al. 2010 Preaxial polydactyly/ triphalangeal thumb is associated with changed transcription factor-binding affinity in a family with a novel point mutation in the long-range cisregulatory element ZRS. Eur. J. Hum. Genet. 18, 733-736. (doi:10.1038/ejhg.2009.225)
19. Furniss D, Lettice LA, Taylor IB, Critchley PS, Giele H, Hill RE, Wilkie AO. 2008 A variant in the sonic hedgehog regulatory sequence (ZRS) is associated with triphalangeal thumb and deregulates expression in the developing limb. Hum. Mol. Genet. 17, 2417-2423. (doi:10.1093/hmg/ddn141)
20. Gurnett CA, Bowcock AM, Dietz FR, Morcuende JA, Murray JC, Dobbs MB. 2007 Two novel point mutations in the long-range SHH enhancer in three families with triphalangeal thumb and preaxial polydactyly. Am. J. Med. Genet. A 143, 27-32. (doi:10.1002/ajmg.a.31563)
21. Semerci CN, Demirkan F, Ozdemir M, Biskin E, Akin B, Bagci H, Akarsu NA. 2009 Homozygous feature of isolated triphalangeal thumb-preaxial polydactyly linked to 7q36: no phenotypic difference between homozygotes and heterozygotes. Clin. Genet. 76, 85-90. (doi:10.1111/j.1399-0004.2009.01192.x)
22. Vandermeer JE, Afzal M, Alyas S, Haque S, Ahituv N, Malik S. 2012 A novel ZRS mutation in a Balochi tribal family with triphalangeal thumb, pre-axial polydactyly, post-axial polydactyly, and syndactyly. Am. J. Med. Genet. A 158A, 2031-2035. (doi:10.1002/ajmg.a.35473)
23. Zhao J, Ding J, Li Y, Ren K, Sha J, Zhu M, Gao X. 2009 HnRNP U mediates the long-range regulation of Shh expression during limb development. Hum. Mol. Genet. 18, 3090-3097. (doi:10.1093/hmg/ddp250)
24. Laurell T et al. 2012 A novel 13 base pair insertion in the sonic hedgehog ZRS limb enhancer (ZRS/LMBR1) causes preaxial polydactyly with triphalangeal thumb. Hum. Mutat. 33, 1063-1066. (doi:10.1002/humu.22097)
25. Sun M et al. 2008 Triphalangeal thumbpolysyndactyly syndrome and syndactyly type IV are caused by genomic duplications involving the longrange, limb-specific SHH enhancer. J. Med. Genet. 45 589-595. (doi:10.1136/jmg.2008.057646)
26. Klopocki E, Ott CE, Benatar N, Ullmann R, Mundlos S, Lehmann K. 2008 A microduplication of the long range SHH limb regulator (ZRS) is associated with triphalangeal thumb-polysyndactyly syndrome. J. Med. Genet. 45, 370-375. (doi:10.1136/jmg.2007.055699)
27. Klopocki E, Mundlos S. 2011 Copy-number variations, noncoding sequences, and human phenotypes. Annu. Rev. Genomics Hum. Genet. 12, 53-72. (doi:10.1146/annurev-genom-082410-101404)
28. Saunders JW, Gasseling MT. 1968 Ectodermal-mesenchymal interactions in the origin of limb symmetry. In Epithelial-mesenchymal interactions (eds R Fleischmeyer, RE Billingham), pp. 78-97. Baltimore, MD: Williams & Wilkins.
29. Blanc I, Bach A, Robert B. 2002 Unusual pattern of Sonic hedgehog expression in the polydactylous mouse mutant Hemimelic extra-toes. Int. J. Dev. Biol. 46, 969-974.
30. Sharpe J, Lettice L, Hecksher-Sorensen J, Fox M, Hill R, Krumlauf R. 1999 Identification of sonic hedgehog as a candidate gene responsible for the polydactylous mouse mutant Sasquatch. Curr. Biol. 9, 97-100. (doi:10.1016/S0960-9822(99)80022-0)
31. Masuya H, Sagai T, Wakana S, Moriwaki K, Shiroishi T. 1995 A duplicated zone of polarizing activity in polydactylous mouse mutants. Genes Dev. 9, 1645-1653. (doi:10.1101/gad.9.13.1645)
32. Lettice LA et al. 2012 Opposing functions of the ETS factor family define Shh spatial expression in limb buds and underlie polydactyly. Dev. Cell 22, 459-467. (doi:10.1016/j.devcel.2011.12.010)
33. Hollenhorst PC, Shah AA, Hopkins C, Graves BJ. 2007 Genome-wide analyses reveal properties of redundant and specific promoter occupancy within the ETS gene family. Genes Dev. 21, 1882-1894. (doi:10.1101/gad.1561707)
34. Mao J, McGlinn E, Huang P, Tabin CJ, McMahon AP. 2009 Fgf-dependent Etv4/5 activity is required for posterior restriction of sonic hedgehog and promoting outgrowth of the vertebrate limb. Dev. Cell 16, 600-606. (doi:10.1016/j.devcel. 2009.02.005)
35. Zhang Z, Verheyden JM, Hassell JA, Sun X. 2009 FGF-regulated Etv genes are essential for repressing Shh expression in mouse limb buds. Dev. Cell 16, 607-613. (doi:10.1016/j.devcel.2009.02.008)
36. Amano T, Sagai T, Tanabe H, Mizushina Y, Nakazawa H, Shiroishi T. 2009 Chromosomal dynamics at the Shh locus: limb bud-specific differential regulation of competence and active transcription. Dev. Cell 16, 47-57. (doi:10.1016/j.devcel.2008.11.011)
37. Qu S, Niswender KD, Ji Q, van der MR, Keeney D, Magnuson MA, Wisdom R. 1997 Polydactyly and ectopic ZPA formation in Alx-4 mutant mice. Development 124, 3999-4008.
38. Kim TK et al. 2010 Widespread transcription at neuronal activity-regulated enhancers. Nature 465, 182-187. (doi:10.1038/nature09033)