An impairment of long distance SOX10 regulatory elements underlies isolated hirschsprung disease

Human Mutation

Volumn 35, Issue 3, 2014, Pages 303-307

  Lecerf, Laure ^a,b   Kavo, Anthula ^a,b   Ruiz Ferrer, Macarena ^c,d   Baral, Viviane ^a,b   Watanabe, Yuli ^a,b   Chaoui, Asma ^a,b   Pingault, Veronique ^a,b   Borrego, Salud ^c,d   Bondurand, Nadege ^a,b  

^a INSERM U955   (France)

^b FACULTÉ DE MÉDECINE   (France)

^c HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

^d CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

Author keywords

Enteric nervous system; Hirschsprung; Neural crest; Regulatory elements; SOX10

Indexed keywords

TRANSCRIPTION FACTOR SOX10;

ALU SEQUENCE; ARTICLE; AUTOREGULATION; BINDING SITE; CHROMOSOME 22; COMPARATIVE GENOMIC HYBRIDIZATION; COPY NUMBER VARIATION; ENHANCER REGION; GENE DELETION; HIRSCHSPRUNG DISEASE; HUMAN; IN VITRO STUDY; POINT MUTATION; PRIORITY JOURNAL; REGULATORY SEQUENCE; REPORTER GENE; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALIA;

ENTERIC NERVOUS SYSTEM; HIRSCHSPRUNG; NEURAL CREST; REGULATORY ELEMENTS; SOX10;

BASE SEQUENCE; FEMALE; HUMANS; INFANT; MALE; MOLECULAR SEQUENCE DATA; POINT MUTATION; REGULATORY SEQUENCES, NUCLEIC ACID; SEQUENCE DELETION; SOXE TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS; WAARDENBURG SYNDROME;

EID: 84893947886     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.22499     Document Type: Article

References (25)

1. Alves MM, Sribudiani Y, Brouwer RW, Amiel J, Antinolo G, Borrego S, Ceccherini I, Chakravarti A, Fernandez RM, Garcia-Barcelo MM, Griseri P, Lyonnet S, et al. 2013. Contribution of rare and common variants determine complex diseases-Hirschsprung disease as a model. Dev Biol 382:330-343.
2. Amiel J, Benko S, Gordon CT, Lyonnet S. 2010. Disruption of long-distance highly conserved noncoding elements in neurocristopathies. Ann N Y Acad Sci 1214:34-46.
3. Antonellis A, Huynh JL, Lee-Lin SQ, Vinton RM, Renaud G, Loftus SK, Elliot G, Wolfsberg TG, Green ED, McCallion AS, Pavan WJ. 2008. Identification of neural crest and glial enhancers at the mouse Sox10 locus through transgenesis in zebrafish. PLoS Genet 4:e1000174.
4. Baral V, Chaoui A, Watanabe Y, Goossens M, Attie-Bitach T, Marlin S, Pingault V, Bondurand N. 2012. Screening of MITF and SOX10 regulatory regions in Waardenburg syndrome type 2. PLoS One 7:e41927.
5. Betancur P, Bronner-Fraser M, Sauka-Spengler T. 2010. Genomic code for Sox10 activation reveals a key regulatory enhancer for cranial neural crest. Proc Natl Acad Sci USA 107:3570-3575.
6. Bondurand N, Dastot-Le Moal F, Stanchina L, Collot N, Baral V, Marlin S, Attie-Bitach T, Giurgea I, Skopinski L, Reardon W, Toutain A, Sarda P, et al. 2007. Deletions at the SOX10 gene locus cause Waardenburg syndrome types 2 and 4. Am J Hum Genet 81:1169-1185.
7. Bondurand N, Fouquet V, Baral V, Lecerf L, Loundon N, Goossens M, Duriez B, Labrune P, Pingault V. 2012. Alu-mediated deletion of SOX10 regulatory elements in Waardenburg syndrome type 4. Eur J Hum Genet 20:990-994.
8. Bondurand N, Girard M, Pingault V, Lemort N, Dubourg O, Goossens M. 2001. Human Connexin 32, a gap junction protein altered in the X-linked form of Charcot-Marie-Tooth disease, is directly regulated by the transcription factor SOX10. Hum Mol Genet 10:2783-2795.
9. Bondurand N, Pingault V, Goerich DE, Lemort N, Sock E, Le Caignec C, Wegner M, Goossens M. 2000. Interaction among SOX10, PAX3 and MITF, three genes altered in Waardenburg syndrome. Hum Mol Genet 9:1907-1917.
10. Bondurand N, Sham MH. 2013. The role of SOX10 during enteric nervous system development. Dev Biol 382: 330-343.
11. Borrego S, Ruiz-Ferrer M, Fernandez RM, Antinolo G. 2013. Hirschsprung's disease as a model of complex genetic etiology. Histol Histopathol 28:1117-1136.
12. de Pontual L, Pelet A, Clement-Ziza M, Trochet D, Antonarakis SE, Attie-Bitach T, Beales PL, Blouin JL, Dastot-Le Moal F, Dollfus H, Goossens M, Katsanis N, et al. 2007. Epistatic interactions with a common hypomorphic RET allele in syndromic Hirschsprung disease. Hum Mutat 28:790-796.
13. Emison ES, McCallion AS, Kashuk CS, Bush RT, Grice E, Lin S, Portnoy ME, Cutler DJ, Green ED, Chakravarti A. 2005. A common sex-dependent mutation in a RET enhancer underlies Hirschsprung disease risk. Nature 434:857-863.
14. Inoue K, Khajavi M, Ohyama T, Hirabayashi S, Wilson J, Reggin JD, Mancias P, Butler IJ, Wilkinson MF, Wegner M, Lupski JR. 2004. Molecular mechanism for distinct neurological phenotypes conveyed by allelic truncating mutations. Nat Genet 36:361-369.
15. Luzon-Toro B, Fernandez RM, Torroglosa A, de Agustin JC, Mendez-Vidal C, Segura DI, Antinolo G, Borrego S. 2013. Mutational spectrum of semaphorin 3A and semaphorin 3D genes in Spanish Hirschsprung patients. PLoS One 8:e54800.
16. Luzon-Toro B, Torroglosa A, Nunez-Torres R, Enguix-Riego MV, Fernandez RM, de Agustin JC, Antinolo G, Borrego S. 2012. Comprehensive analysis of NRG1 common and rare variants in Hirschsprung patients. PLoS One 7:e36524.
17. Obermayr F, Hotta R, Enomoto H, Young HM. 2013. Development and developmental disorders of the enteric nervous system. Nat Rev Gastroenterol Hepatol 10:43-57.
18. Pingault V, Bondurand N, Kuhlbrodt K, Goerich DE, Prehu MO, Puliti A, Herbarth B, Hermans-Borgmeyer I, Legius E, Matthijs G, Amiel J, Lyonnet S, et al. 1998. SOX10 mutations in patients with Waardenburg-Hirschsprung disease. Nat Genet 18:171-173.
19. Pingault V, Ente D, Dastot-Le Moal F, Goossens M, Marlin S, Bondurand N. 2010. Review and update of mutations causing Waardenburg syndrome. Hum Mutat 31:391-406.
20. Ruiz-Ferrer M, Torroglosa A, Luzon-Toro B, Fernandez RM, Antinolo G, Mulligan LM, Borrego S. 2011a. Novel mutations at RET ligand genes preventing receptor activation are associated to Hirschsprung's disease. J Mol Med (Berl) 89:471-480.
21. Ruiz-Ferrer M, Torroglosa A, Nunez-Torres R, de Agustin JC, Antinolo G, Borrego S. 2011b. Expression of PROKR1 and PROKR2 in human enteric neural precursor cells and identification of sequence variants suggest a role in HSCR. PLoS One 6:e23475.
22. Sanchez-Mejias A, Watanabe Y, M Fernandez R, Lopez-Alonso M, Antinolo G, Bondurand N, Borrego S. 2010. Involvement of SOX10 in the pathogenesis of Hirschsprung disease: report of a truncating mutation in an isolated patient. J Mol Med (Berl) 88:507-514.
23. Wahlbuhl M, Reiprich S, Vogl MR, Bosl MR, Wegner M. 2012. Transcription factor Sox10 orchestrates activity of a neural crest-specific enhancer in the vicinity of its gene. Nucleic Acids Res 40:88-101.
24. Werner T, Hammer A, Wahlbuhl M, Bosl MR, Wegner M. 2007. Multiple conserved regulatory elements with overlapping functions determine Sox10 expression in mouse embryogenesis. Nucleic Acids Res 35:6526-6538.
25. Yokota Y, Saito D, Tadokoro R, Takahashi Y. 2011. Genomically integrated transgenes are stably and conditionally expressed in neural crest cell-specific lineages. Dev Biol 353:382-395.