Fine tuning of craniofacial morphology by distant-acting enhancers

Science

Volumn 342, Issue 6157, 2013, Pages

  Attanasio, Catia ^a   Nord, Alex S ^a   Zhu, Yiwen ^a   Blow, Matthew J ^b   Li, Zirong ^c,g   Liberton, Denise K ^d   Morrison, Harris ^e   Plajzer Frick, Ingrid ^a   Holt, Amy ^a   Hosseini, Roya ^a   Phouanenavong, Sengthavy ^a   Akiyama, Jennifer A ^a   Shoukry, Malak ^a   Afzal, Veena ^a   Rubin, Edward M ^a,b   FitzPatrick, David R ^e,f   Ren, Bing ^c   Hallgrímsson, Benedikt ^d   Pennacchio, Len A ^a,b   Visel, Axel ^a,b  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b U S DEPARTMENT OF ENERGY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALGARY   (Canada)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

^f ROYAL HOSPITAL FOR SICK CHILDREN   (United Kingdom)

^g MILLIPORE CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEVELOPMENTAL BIOLOGY; GENE EXPRESSION; GENETICALLY MODIFIED ORGANISM; MORPHOLOGY; PROTEIN; SKULL; SPATIAL ANALYSIS;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CRANIOFACIAL DEVELOPMENT; CRANIOFACIAL MORPHOLOGY; EMBRYO DEVELOPMENT; ENHANCER REGION; GENE SEQUENCE; GENOME; HUMAN; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CONGENITAL MALFORMATION; CRANIOFACIAL MALFORMATION; FACE; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE TARGETING; GENETIC EPIGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; MAXILLOFACIAL DEVELOPMENT; MOUSE; PATHOLOGY; PHYSIOLOGY; SKULL; TRANSGENIC MOUSE;

MUS MUSCULUS;

ANIMALS; CRANIOFACIAL ABNORMALITIES; ENHANCER ELEMENTS, GENETIC; EPIGENESIS, GENETIC; FACE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE TARGETING; MAXILLOFACIAL DEVELOPMENT; MICE; MICE, TRANSGENIC; SEQUENCE DELETION; SKULL;

EID: 84886257610     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.1241006     Document Type: Article

References (61)

1. K. Christensen, K. Juel, A. M. Herskind, J. C. Murray, Long term follow up study of survival associated with cleft lip and palate at birth. BMJ 328, 1405 (2004). doi: 10.1136/bmj.38106.559120.7C; pmid: 15145797
2. G. L. Wehby, C. H. Cassell, The impact of orofacial clefts on quality of life and healthcare use and costs. Oral Dis. 16, 3-10 (2010). doi: 10.1111/j.1601-0825.2009.01588.x; pmid: 19656316
3. M. Kayser, P. M. Schneider, DNA-based prediction of human externally visible characteristics in forensics: Motivations, scientific challenges, and ethical considerations. Forensic Sci. Int. Genet. 3, 154-161 (2009). doi: 10.1016/j.fsigen.2009.01.012; pmid: 19414162
4. L. A. P. Kohn, The role of genetics in craniofacial morphology and growth. Annu. Rev. Anthropol. 20, 261-278 (1991). doi: 10.1146/annurev.an.20. 100191.001401
5. C. Manfredi, R. Martina, G. B. Grossi, M. Giuliani, Heritability of 39 orthodontic cephalometric parameters on MZ, DZ twins and MN-paired singletons. Am. J. Orthod. Dentofacial Orthop. 111, 44-51 (1997). doi: 10.1016/S0889- 5406(97)70301-9; pmid: 9009923
6. B. Johannsdottir, F. Thorarinsson, A. Thordarson, T. E. Magnusson, Heritability of craniofacial characteristics between parents and offspring estimated from lateral cephalograms. Am. J. Orthod. Dentofacial Orthop. 127, 200-207, quiz 260-261 (2005). doi: 10.1016/j.ajodo.2004.07.033; pmid: 15750539
7. I. Satokata, R. Maas, Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat. Genet. 6, 348-356 (1994). doi: 10.1038/ng0494-348; pmid: 7914451
8. M. J. van den Boogaard, M. Dorland, F. A. Beemer, H. K. van Amstel, MSX1 mutation is associated with orofacial clefting and tooth agenesis in humans. Nat. Genet. 24, 342-343 (2000). doi: 10.1038/74155; pmid: 10742093
9. S. Kondo et al., Mutations in IRF6 cause Van der Woude and popliteal pterygium syndromes. Nat. Genet. 32, 285-289 (2002). doi: 10.1038/ng985; pmid: 12219090
10. S. Suzuki et al., Mutations in BMP4 are associated with subepithelial, microform, and overt cleft lip. Am. J. Hum. Genet. 84, 406-411 (2009). doi: 10.1016/j.ajhg.2009.02.002; pmid: 19249007
11. M. J. Dixon, Treacher Collins syndrome. Hum. Mol. Genet. 5, 1391-1396 (1996). pmid: 8875242
12. S. B. Ng et al., Exome sequencing identifies MLL2 mutations as a cause of Kabuki syndrome. Nat. Genet. 42, 790-793 (2010). doi: 10.1038/ng.646; pmid: 20711175
13. S. B. Ng et al., Exome sequencing identifies the cause of a Mendelian disorder. Nat. Genet. 42, 30-35 (2010). doi: 10.1038/ng.499; pmid: 19915526
14. M. J. Dixon, M. L. Marazita, T. H. Beaty, J. C. Murray, Cleft lip and palate: Understanding genetic and environmental influences. Nat. Rev. Genet. 12, 167-178 (2011). doi: 10.1038/nrg2933; pmid: 21331089
15. S. Boehringer et al., Genetic determination of human facial morphology: Links between cleft-lips and normal variation. Eur. J. Hum. Genet. 19, 1192-1197 (2011). doi: 10.1038/ejhg.2011.110; pmid: 21694738
16. F. Liu et al., A genome-wide association study identifies five loci influencing facial morphology in Europeans. PLOS Genet. 8, e1002932 (2012). doi: 10.1371/journal.pgen.1002932; pmid: 23028347
17. L. Paternoster et al., Genome-wide association study of three-dimensional facial morphology identifies a variant in PAX3 associated with nasion position. Am. J. Hum. Genet. 90, 478-485 (2012). doi: 10.1016/j.ajhg.2011.12.021; pmid: 22341974
18. D. L. Stern, Evolutionary developmental biology and the problem of variation. Evolution 54, 1079-1091 (2000). pmid: 11005278
19. Y. Shen et al., A map of the cis-regulatory sequences in the mouse genome. Nature 488, 116-120 (2012). doi: 10.1038/nature11243; pmid: 22763441
20. J. Zhu et al., Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell 152, 642-654 (2013). doi: 10.1016/j.cell.2012.12.033; pmid: 23333102
21. A. Visel et al., ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457, 854-858 (2009). doi: 10.1038/nature07730; pmid: 19212405
22. N. M. Young, H. J. Chong, D. Hu, B. Hallgrímsson, R. S. Marcucio, Quantitative analyses link modulation of sonic hedgehog signaling to continuous variation in facial growth and shape. Development 137, 3405-3409 (2010). doi: 10.1242/dev.052340; pmid: 20826528
23. M. Simões-Costa, M. E. Bronner, Insights into neural crest development and evolution from genomic analysis. Genome Res. 23, 1069-1080 (2013). doi: 10.1101/gr.157586.113; pmid: 23817048
24. S. Bagheri-Fam et al., Long-range upstream and downstream enhancers control distinct subsets of the complex spatiotemporal Sox9 expression pattern. Dev. Biol. 291, 382-397 (2006). doi: 10.1016/j.ydbio.2005.11.013; pmid: 16458883
25. P. Betancur, M. Bronner-Fraser, T. Sauka-Spengler, Genomic code for Sox10 activation reveals a key regulatory enhancer for cranial neural crest. Proc. Natl. Acad. Sci. U.S.A. 107, 3570-3575 (2010). doi: 10.1073/pnas.0906596107; pmid: 20139305
26. H. Yanagisawa, D. E. Clouthier, J. A. Richardson, J. Charité, E. N. Olson, Targeted deletion of a branchial arch-specific enhancer reveals a role of dHAND in craniofacial development. Development 130, 1069-1078 (2003). doi: 10.1242/dev.00337; pmid: 12571099
27. A. Rada-Iglesias et al., Epigenomic annotation of enhancers predicts transcriptional regulators of human neural crest. Cell Stem Cell 11, 633-648 (2012). doi: 10.1016/j.stem.2012.07.006; pmid: 22981823
28. M. H. Kaufman, The Atlas of Mouse Development (Academic Press, London, 1992).
29. W. Feng et al., Spatial and temporal analysis of gene expression during growth and fusion of the mouse facial prominences. PLOS ONE 4, e8066 (2009). doi: 10.1371/journal.pone.0008066; pmid: 20016822
30. Materials and methods are available as supplementary materials on Science Online.
31. M. J. Blow et al., ChIP-Seq identification of weakly conserved heart enhancers. Nat. Genet. 42, 806-810 (2010). doi: 10.1038/ng.650; pmid: 20729851
32. A. Visel et al., A high-resolution enhancer atlas of the developing telencephalon. Cell 152, 895-908 (2013). doi: 10.1016/j.cell.2012.12.041; pmid: 23375746
33. C. Y. McLean et al., GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495-501 (2010). doi: 10.1038/nbt.1630; pmid: 20436461
34. L. A. Pennacchio et al., In vivo enhancer analysis of human conserved non-coding sequences. Nature 444, 499-502 (2006). doi: 10.1038/nature05295; pmid: 17086198
35. J. Sharpe et al., Optical projection tomography as a tool for 3D microscopy and gene expression studies. Science 296, 541-545 (2002). doi: 10.1126/science.1068206; pmid: 11964482
36. N. D. Heintzman et al., Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459, 108-112 (2009). doi: 10.1038/nature07829; pmid: 19295514
37. L. Z. Holland et al., The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res. 18, 1100-1111 (2008). doi: 10.1101/gr.073676.107; pmid: 18562680
38. D. May et al., Large-scale discovery of enhancers from human heart tissue. Nat. Genet. 44, 89-93 (2012). doi: 10.1038/ng.1006; pmid: 22138689
39. A. Visel et al., Ultraconservation identifies a small subset of extremely constrained developmental enhancers. Nat. Genet. 40, 158-160 (2008). doi: 10.1038/ng.2007.55; pmid: 18176564
40. H. Hochheiser et al., The FaceBase Consortium: a comprehensive program to facilitate craniofacial research. Dev. Biol. 355, 175-182 (2011). doi: 10.1016/j.ydbio.2011.02.033; pmid: 21458441
41. S. Alappat, Z. Y. Zhang, Y. P. Chen, Msx homeobox gene family and craniofacial development. Cell Res. 13, 429-442 (2003). doi: 10.1038/sj.cr.7290185; pmid: 14728799
42. A. Visel, E. M. Rubin, L. A. Pennacchio, Genomic views of distant-acting enhancers. Nature 461, 199-205 (2009). doi: 10.1038/nature08451; pmid: 19741700
43. S. Birnbaum et al., Key susceptibility locus for nonsyndromic cleft lip with or without cleft palate on chromosome 8q24. Nat. Genet. 41, 473-477 (2009). doi: 10.1038/ng.333; pmid: 19270707
44. E. Mangold et al., Genome-wide linkage scan of nonsyndromic orofacial clefting in 91 families of central European origin. Am. J. Med. Genet. A. 149A, 2680-2694 (2009). doi: 10.1002/ajmg.a.33136; pmid: 19938073
45. T. Nikopensius et al., Replication of novel susceptibility locus for nonsyndromic cleft lip with or without cleft palate on chromosome 8q24 in Estonian and Lithuanian patients. Am. J. Med. Genet. A. 149A, 2551-2553 (2009). doi: 10.1002/ajmg.a.33024; pmid: 19839039
46. T. H. Beaty et al., A genome-wide association study of cleft lip with and without cleft palate identifies risk variants near MAFB and ABCA4. Nat. Genet. 42, 525-529 (2010). doi: 10.1038/ng.580; pmid: 20436469
47. Q. Yuan, S. H. Blanton, J. T. Hecht, Association of ABCA4 and MAFB with non-syndromic cleft lip with or without cleft palate. Am. J. Med. Genet. A. 155A, 1469-1471 (2011). doi: 10.1002/ajmg.a.33940; pmid: 21567910
48. E. J. Leslie et al., Expression and mutation analyses implicate ARHGAP29 as the etiologic gene for the cleft lip with or without cleft palate locus identified by genome-wide association on chromosome 1p22. Birth Defects Res. A Clin. Mol. Teratol. 94, 934-942 (2012). doi: 10.1002/bdra.23076; pmid: 23008150
49. F. Rahimov et al., Disruption of an AP-2alpha binding site in an IRF6 enhancer is associated with cleft lip. Nat. Genet. 40, 1341-1347 (2008). doi: 10.1038/ng.242; pmid: 18836445
50. K. F. Oram, E. A. Carver, T. Gridley, Slug expression during organogenesis in mice. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 271, 189-191 (2003). doi: 10.1002/ar.a.10027; pmid: 12552634
51. T. A. Mitsiadis, I. Angeli, C. James, U. Lendahl, P. T. Sharpe, Role of Islet1 in the patterning of murine dentition. Development 130, 4451-4460 (2003). doi: 10.1242/dev.00631; pmid: 12900460
52. D. E. Lieberman, B. Hallgrímsson, W. Liu, T. E. Parsons, H. A. Jamniczky, Spatial packing, cranial base angulation, and craniofacial shape variation in the mammalian skull: Testing a new model using mice. J. Anat. 212, 720-735 (2008). doi: 10.1111/j.1469-7580.2008.00900.x; pmid: 18510502
53. B. Hallgrímsson, D. E. Lieberman, W. Liu, A. F. Ford-Hutchinson, F. R. Jirik, Epigenetic interactions and the structure of phenotypic variation in the cranium. Evol. Dev. 9, 76-91 (2007). doi: 10.1111/j.1525-142X.2006.00139. x; pmid: 17227368
54. S. A. Murray, K. F. Oram, T. Gridley, Multiple functions of Snail family genes during palate development in mice. Development 134, 1789-1797 (2007). doi: 10.1242/dev.02837; pmid: 17376812
55. E. Mangold, K. U. Ludwig, M. M. Nöthen, Breakthroughs in the genetics of orofacial clefting. Trends Mol. Med. 17, 725-733 (2011). doi: 10.1016/j.molmed.2011.07.007; pmid: 21885341
56. A. MacKenzie, L. Purdie, D. Davidson, M. Collinson, R. E. Hill, Two enhancer domains control early aspects of the complex expression pattern of Msx1. Mech. Dev. 62, 29-40 (1997). doi: 10.1016/S0925-4773(96)00646-6; pmid: 9106164
57. S. Yokoyama et al., A systems approach reveals that the myogenesis genome network is regulated by the transcriptional repressor RP58. Dev. Cell 17, 836-848 (2009). doi: 10.1016/j.devcel.2009.10.011; pmid: 20059953
58. B. Balczerski et al., Distinct spatiotemporal roles of hedgehog signalling during chick and mouse cranial base and axial skeleton development. Dev. Biol. 371, 203-214 (2012). doi: 10.1016/j.ydbio.2012.08.011; pmid: 23009899
59. A. Vaahtokari, T. Aberg, J. Jernvall, S. Keränen, I. Thesleff, The enamel knot as a signaling center in the developing mouse tooth. Mech. Dev. 54, 39-43 (1996). doi: 10.1016/0925-4773(95)00459-9; pmid: 8808404
60. E. Koyama et al., Polarizing activity, Sonic hedgehog, and tooth development in embryonic and postnatal mouse. Dev. Dyn. 206, 59-72 (1996). doi: 10.1002/(SICI)1097-0177(199605)206:1〈59::AID-AJA6〉3.0.CO;2-#; pmid: 9019247
61. A. S. Tucker et al., Conserved regulation of mesenchymal gene expression by Fgf-8 in face and limb development. Development 126, 221-228 (1999). pmid: 9847236