Genetic interaction between Sox10 and Zfhx1b during enteric nervous system development

Developmental Biology

Volumn 341, Issue 2, 2010, Pages 416-428

  Stanchina, Laure ^a,b   Van de Putte, Tom ^c,d,e   Goossens, Michel ^a,b   Huylebroeck, Danny ^c,d   Bondurand, Nadege ^a,b  

^a INSERM U955   (France)

^b FACULTÉ DE MÉDECINE   (France)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^e TiGenix   (Belgium)

Author keywords

Differentiation; Enteric nervous system; Hirschsprung; Mowat Wilson; Neural crest; Sox10; Transcription factor; Waardenburg; Zeb2; Zfhx1b

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX10; UNCLASSIFIED DRUG; ZINC FINGER HOMEOBOX 1B; HOMEODOMAIN PROTEIN; REPRESSOR PROTEIN; SOX10 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX; ZEB2 PROTEIN, HUMAN;

ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; GENE INTERACTION; GENE MUTATION; INTESTINE INNERVATION; MOUSE; MOUSE MUTANT; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEM CELL; ANIMAL; ANIMAL EMBRYO; C3H MOUSE; CROSS BREEDING; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GLIA; HIRSCHSPRUNG DISEASE; HUMAN; METABOLISM; MUTATION; PRENATAL DEVELOPMENT;

ANIMALS; CROSSES, GENETIC; EMBRYO, MAMMALIAN; ENTERIC NERVOUS SYSTEM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HIRSCHSPRUNG DISEASE; HOMEODOMAIN PROTEINS; HUMANS; MICE; MICE, INBRED C3H; MICE, KNOCKOUT; MUTATION; NEUROGLIA; REPRESSOR PROTEINS; SOXE TRANSCRIPTION FACTORS; STEM CELLS;

EID: 77952304708     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.02.036     Document Type: Article

References (70)

1. Amiel J., Sproat-Emison E., Garcia-Barcelo M., Lantieri F., Burzynski G., Borrego S., Pelet A., Arnold S., Miao X., Griseri P., Brooks A.S., Antinolo G., de Pontual L., Clement-Ziza M., Munnich A., Kashuk C., West K., Wong K.K., Lyonnet S., Chakravarti A., Tam P.K., Ceccherini I., Hofstra R.M., Fernandez R. Hirschsprung disease, associated syndromes and genetics: a review. J. Med. Genet. 2008, 45:1-14.
2. Antonellis A., Bennett W.R., Menheniott T.R., Prasad A.B., Lee-Lin S.Q., Green E.D., Paisley D., Kelsh R.N., Pavan W.J., Ward A. Deletion of long-range sequences at Sox10 compromises developmental expression in a mouse model of Waardenburg-Shah (WS4) syndrome. Hum. Mol. Genet. 2006, 15:259-271.
3. Antonellis A., Huynh J.L., Lee-Lin S.Q., Vinton R.M., Renaud G., Loftus S.K., Elliot G., Wolfsberg T.G., Green E.D., McCallion A.S., Pavan W.J. Identification of neural crest and glial enhancers at the mouse Sox10 locus through transgenesis in zebrafish. PLoS Genet. 2008, 4:e1000174.
4. Barlow A., de Graaff E., Pachnis V. Enteric nervous system progenitors are coordinately controlled by the G protein-coupled receptor EDNRB and the receptor tyrosine kinase RET. Neuron. 2003, 40:905-916.
5. Bassez G., Camand O.J., Cacheux V., Kobetz A., Dastot-Le Moal F., Marchant D., Catala M., Abitbol M., Goossens M. Pleiotropic and diverse expression of ZFHX1B gene transcripts during mouse and human development supports the various clinical manifestations of the "Mowat-Wilson" syndrome. Neurobiol. Dis. 2004, 15:240-250.
6. Bondurand N., Natarajan D., Barlow A., Thapar N., Pachnis V. Maintenance of mammalian enteric nervous system progenitors by SOX10 and endothelin 3 signalling. Development 2006, 133:2075-2086.
7. Bondurand N., Natarajan D., Thapar N., Atkins C., Pachnis V. Neuron and glia generating progenitors of the mammalian enteric nervous system isolated from foetal and postnatal gut cultures. Development 2003, 130:6387-6400.
8. Bowles J., Schepers G., Koopman P. Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev. Biol. 2000, 227:239-255.
9. Britsch S., Goerich D.E., Riethmacher D., Peirano R.I., Rossner M., Nave K.A., Birchmeier C., Wegner M. The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev. 2001, 15:66-78.
10. Burns A.J., Douarin N.M. The sacral neural crest contributes neurons and glia to the post-umbilical gut: spatiotemporal analysis of the development of the enteric nervous system. Development 1998, 125:4335-4347.
11. Burns A.J., Thapar N. Advances in ontogeny of the enteric nervous system. Neurogastroenterol. Motil. 2006, 18:876-887.
12. Burzynski G., Shepherd I.T., Enomoto H. Genetic model system studies of the development of the enteric nervous system, gut motility and Hirschsprung's disease. Neurogastroenterol. Motil. 2009, 21:113-127.
13. Cacheux V., Dastot-Le Moal F., Kaariainen H., Bondurand N., Rintala R., Boissier B., Wilson M., Mowat D., Goossens M. Loss-of-function mutations in SIP1 Smad interacting protein 1 result in a syndromic Hirschsprung disease. Hum. Mol. Genet. 2001, 10:1503-1510.
14. Cantrell V.A., Owens S.E., Chandler R.L., Airey D.C., Bradley K.M., Smith J.R., Southard-Smith E.M. Interactions between Sox10 and EdnrB modulate penetrance and severity of aganglionosis in the Sox10Dom mouse model of Hirschsprung disease. Hum. Mol. Genet. 2004, 13:2289-2301.
15. Chalazonitis A., D'Autreaux F., Guha U., Pham T.D., Faure C., Chen J.J., Roman D., Kan L., Rothman T.P., Kessler J.A., Gershon M.D. Bone morphogenetic protein-2 and -4 limit the number of enteric neurons but promote development of a TrkC-expressing neurotrophin-3-dependent subset. J. Neurosci. 2004, 24:4266-4282.
16. Chalazonitis A., Pham T.D., Li Z., Roman D., Guha U., Gomes W., Kan L., Kessler J.A., Gershon M.D. Bone morphogenetic protein regulation of enteric neuronal phenotypic diversity: relationship to timing of cell cycle exit. J. Comp. Neurol. 2008, 509:474-492.
17. Comijn J., Berx G., Vermassen P., Verschueren K., van Grunsven L., Bruyneel E., Mareel M., Huylebroeck D., van Roy F. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol. Cell 2001, 7:1267-1278.
18. Dastot-Le Moal F., Wilson M., Mowat D., Collot N., Niel F., Goossens M. ZFHX1B mutations in patients with Mowat-Wilson syndrome. Hum. Mutat. 2007, 28:313-321.
19. De Santa Barbara P., Williams J., Goldstein A.M., Doyle A.M., Nielsen C., Winfield S., Faure S., Roberts D.J. Bone morphogenetic protein signaling pathway plays multiple roles during gastrointestinal tract development. Dev. Dyn. 2005, 234:312-322.
20. Deal K.K., Cantrell V.A., Chandler R.L., Saunders T.L., Mortlock D.P., Southard-Smith E.M. Distant regulatory elements in a Sox10-beta GEO BAC transgene are required for expression of Sox10 in the enteric nervous system and other neural crest-derived tissues. Dev. Dyn. 2006, 235:1413-1432.
21. Delalande J.M., Guyote M.E., Smith C.M., Shepherd I.T. Zebrafish sip1a and sip1b are essential for normal axial and neural patterning. Dev. Dyn. 2008, 237:1060-1069.
22. Dutton J.R., Antonellis A., Carney T.J., Rodrigues F.S., Pavan W.J., Ward A., Kelsh R.N. An evolutionarily conserved intronic region controls the spatiotemporal expression of the transcription factor Sox10. BMC Dev. Biol. 2008, 8:105.
23. Eisaki A., Kuroda H., Fukui A., Asashima M. XSIP1, a member of two-handed zinc finger proteins, induced anterior neural markers in Xenopus laevis animal cap. Biochem. Biophys. Res. Commun. 2000, 271:151-157.
24. Espinosa-Parrilla Y., Amiel J., Auge J., Encha-Razavi F., Munnich A., Lyonnet S., Vekemans M., Attie-Bitach T. Expression of the SMADIP1 gene during early human development. Mech. Dev. 2002, 114:187-191.
25. Fu M., Vohra B.P., Wind D., Heuckeroth R.O. BMP signaling regulates murine enteric nervous system precursor migration, neurite fasciculation, and patterning via altered Ncam1 polysialic acid addition. Dev. Biol. 2006, 299:137-150.
26. Furness, J., 2006. The enteric nervous system.
27. Garavelli L., Zollino M., Mainardi P.C., Gurrieri F., Rivieri F., Soli F., Verri R., Albertini E., Favaron E., Zignani M., Orteschi D., Bianchi P., Faravelli F., Forzano F., Seri M., Wischmeijer A., Turchetti D., Pompilii E., Gnoli M., Cocchi G., Mazzanti L., Bergamaschi R., De Brasi D., Sperandeo M.P., Mari F., Uliana V., Mostardini R., Cecconi M., Grasso M., Sassi S., Sebastio G., Renieri A., Silengo M., Bernasconi S., Wakamatsu N., Neri G. Mowat-Wilson syndrome: facial phenotype changing with age: study of 19 Italian patients and review of the literature. Am. J. Med. Genet. 2009, 149A:417-426.
28. Gershon M.D.K., A.L., Wade P.R. Functional Anatomy of the Enteric Nervous System 1994, Raven Press, New York.
29. Goldstein A.M., Brewer K.C., Doyle A.M., Nagy N., Roberts D.J. BMP signaling is necessary for neural crest cell migration and ganglion formation in the enteric nervous system. Mech. Dev. 2005, 122:821-833.
30. Hao M.M., Young H.M. Development of enteric neuron diversity. J. Cell Mol. Med. 2009.
31. Heanue T.A., Pachnis V. Enteric nervous system development and Hirschsprung's disease: advances in genetic and stem cell studies. Nat. Rev. Neurosci. 2007, 8:466-479.
32. Herbarth B., Pingault V., Bondurand N., Kuhlbrodt K., Hermans-Borgmeyer I., Puliti A., Lemort N., Goossens M., Wegner M. Mutation of the Sry-related Sox10 gene in Dominant megacolon, a mouse model for human Hirschsprung disease. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:5161-5165.
33. Higashi Y., Maruhashi M., Nelles L., Van de Putte T., Verschueren K., Miyoshi T., Yoshimoto A., Kondoh H., Huylebroeck D. Generation of the floxed allele of the SIP1 (Smad-interacting protein 1) gene for Cre-mediated conditional knockout in the mouse. Genesis 2002, 32:82-84.
34. Honore S.M., Aybar M.J., Mayor R. Sox10 is required for the early development of the prospective neural crest in Xenopus embryos. Dev. Biol. 2003, 260:79-96.
35. Kapur R.P. Early death of neural crest cells is responsible for total enteric aganglionosis in Sox10(Dom)/Sox10(Dom) mouse embryos. Pediatr. Dev. Pathol. 1999, 2:559-569.
36. Katoh M. Integrative genomic analyses of ZEB2: transcriptional regulation of ZEB2 based on SMADs, ETS1, HIF1alpha, POU/OCT, and NF-kappaB. Int. J. Oncol. 2009, 34:1737-1742.
37. Kelsh R.N. Sorting out Sox10 functions in neural crest development. Bioessays 2006, 28:788-798.
38. Kim J., Lo L., Dormand E., Anderson D.J. SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron 2003, 38:17-31.
39. Kurtz A., Zimmer A., Schnutgen F., Bruning G., Spener F., Muller T. The expression pattern of a novel gene encoding brain-fatty acid binding protein correlates with neuronal and glial cell development. Development 1994, 120:2637-2649.
40. Lang D., Chen F., Milewski R., Li J., Lu M.M., Epstein J.A. Pax3 is required for enteric ganglia formation and functions with Sox10 to modulate expression of c-ret. J. Clin. Invest. 2000, 106:963-971.
41. Le Douarin N.M., Kalcheim C. The Neural Crest 1999, Cambridge University Press, Cambridge.
42. Maka M., Stolt C.C., Wegner M. Identification of Sox8 as a modifier gene in a mouse model of Hirschsprung disease reveals underlying molecular defect. Dev. Biol. 2005, 277:155-169.
43. Miquelajauregui A., Van de Putte T., Polyakov A., Nityanandam A., Boppana S., Seuntjens E., Karabinos A., Higashi Y., Huylebroeck D., Tarabykin V. Smad-interacting protein-1 (Zfhx1b) acts upstream of Wnt signaling in the mouse hippocampus and controls its formation. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:12919-12924.
44. Mollaaghababa R., Pavan W.J. The importance of having your SOX on: role of SOX10 in the development of neural crest-derived melanocytes and glia. Oncogene 2003, 22:3024-3034.
45. Nitta K.R., Takahashi S., Haramoto Y., Fukuda M., Tanegashima K., Onuma Y., Asashima M. The N-terminus zinc finger domain of Xenopus SIP1 is important for neural induction, but not for suppression of Xbra expression. Int. J. Dev. Biol. 2007, 51:321-325.
46. Nitta K.R., Tanegashima K., Takahashi S., Asashima M. XSIP1 is essential for early neural gene expression and neural differentiation by suppression of BMP signaling. Dev. Biol. 2004, 275:258-267.
47. Owens S.E., Broman K.W., Wiltshire T., Elmore J.B., Bradley K.M., Smith J.R., Southard-Smith E.M. Genome-wide linkage identifies novel modifier loci of aganglionosis in the Sox10Dom model of Hirschsprung disease. Hum. Mol. Genet. 2005, 14:1549-1558.
48. Paratore C., Eichenberger C., Suter U., Sommer L. Sox10 haploinsufficiency affects maintenance of progenitor cells in a mouse model of Hirschsprung disease. Hum. Mol. Genet. 2002, 11:3075-3085.
49. Pattyn A., Morin X., Cremer H., Goridis C., Brunet J.F. Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 1997, 124:4065-4075.
50. Postigo A.A. Opposing functions of ZEB proteins in the regulation of the TGFbeta/BMP signaling pathway. EMBO J. 2003, 22:2443-2452.
51. Postigo A.A., Dean D.C. Differential expression and function of members of the zfh-1 family of zinc finger/homeodomain repressors. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:6391-6396.
52. Seuntjens E., Nityanandam A., Miquelajauregui A., Debruyn J., Stryjewska A., Goebbels S., Nave K.A., Huylebroeck D., Tarabykin V. Sip1 regulates sequential fate decisions by feedback signaling from postmitotic neurons to progenitors. Nat. Neurosci. 2009.
53. Southard-Smith E.M., Kos L., Pavan W.J. Sox10 mutation disrupts neural crest development in Dom Hirschsprung mouse model. Nat. Genet. 1998, 18:60-64.
54. Stanchina L., Baral V., Robert F., Pingault V., Lemort N., Pachnis V., Goossens M., Bondurand N. Interactions between Sox10, Edn3 and Ednrb during enteric nervous system and melanocyte development. Dev. Biol. 2006, 295:232-249.
55. Van de Putte T., Francis A., Nelles L., van Grunsven L.A., Huylebroeck D. Neural crest-specific removal of Zfhx1b in mouse leads to a wide range of neurocristopathies reminiscent of Mowat-Wilson syndrome. Hum. Mol. Genet. 2007, 16:1423-1436.
56. Van de Putte T., Maruhashi M., Francis A., Nelles L., Kondoh H., Huylebroeck D., Higashi Y. Mice lacking ZFHX1B, the gene that codes for Smad-interacting protein-1, reveal a role for multiple neural crest cell defects in the etiology of Hirschsprung disease-mental retardation syndrome. Am. J. Hum. Genet. 2003, 72:465-470.
57. van Grunsven L.A., Michiels C., Van de Putte T., Nelles L., Wuytens G., Verschueren K., Huylebroeck D. Interaction between Smad-interacting protein-1 and the corepressor C-terminal binding protein is dispensable for transcriptional repression of E-cadherin. J. Biol. Chem. 2003, 278:26135-26145.
58. van Grunsven L.A., Schellens A., Huylebroeck D., Verschueren K. SIP1 (Smad interacting protein 1) and deltaEF1 (delta-crystallin enhancer binding factor) are structurally similar transcriptional repressors. J. Bone Joint Surg. Am. 2001, 83-A(Suppl 1):S40-S47.
59. van Grunsven L.A., Taelman V., Michiels C., Verstappen G., Souopgui J., Nichane M., Moens E., Opdecamp K., Vanhomwegen J., Kricha S., Huylebroeck D., Bellefroid E.J. XSip1 neuralizing activity involves the co-repressor CtBP and occurs through BMP dependent and independent mechanisms. Dev. Biol. 2007, 306:34-49.
60. Vandewalle C., Comijn J., De Craene B., Vermassen P., Bruyneel E., Andersen H., Tulchinsky E., Van Roy F., Berx G. SIP1/ZEB2 induces EMT by repressing genes of different epithelial cell-cell junctions. Nucleic Acids Res. 2005, 33:6566-6578.
61. Verschueren K., Remacle J.E., Collart C., Kraft H., Baker B.S., Tylzanowski P., Nelles L., Wuytens G., Su M.T., Bodmer R., Smith J.C., Huylebroeck D. SIP1, a novel zinc finger/homeodomain repressor, interacts with Smad proteins and binds to 5'-CACCT sequences in candidate target genes. J. Biol. Chem. 1999, 274:20489-20498.
62. Wakamatsu N., Yamada Y., Yamada K., Ono T., Nomura N., Taniguchi H., Kitoh H., Mutoh N., Yamanaka T., Mushiake K., Kato K., Sonta S., Nagaya M. Mutations in SIP1, encoding Smad interacting protein-1, cause a form of Hirschsprung disease. Nat. Genet. 2001, 27:369-370.
63. Wegner M. From head to toes: the multiple facets of Sox proteins. Nucleic Acids Res. 1999, 27:1409-1420.
64. Wegner M. Secrets to a healthy Sox life: lessons for melanocytes. Pigment Cell Res. 2005, 18:74-85.
65. Wegner M. All purpose Sox: the many roles of Sox proteins in gene expression. Int. J. Biochem. Cell Biol. 2009.
66. Werner T., Hammer A., Wahlbuhl M., Bosl M.R., Wegner M. Multiple conserved regulatory elements with overlapping functions determine Sox10 expression in mouse embryogenesis. Nucleic Acids Res. 2007, 35:6526-6538.
67. Wilson M., Koopman P. Matching SOX: partner proteins and co-factors of the SOX family of transcriptional regulators. Curr. Opin. Genet. Dev. 2002, 12:441-446.
68. Young H.M., Bergner A.J., Muller T. Acquisition of neuronal and glial markers by neural crest-derived cells in the mouse intestine. J. Comp. Neurol. 2003, 456:1-11.
69. Zhu L., Lee H.O., Jordan C.S., Cantrell V.A., Southard-Smith E.M., Shin M.K. Spatiotemporal regulation of endothelin receptor-B by SOX10 in neural crest-derived enteric neuron precursors. Nat. Genet. 2004, 36:732-737.
70. Zweier C., Thiel C.T., Dufke A., Crow Y.J., Meinecke P., Suri M., Ala-Mello S., Beemer F., Bernasconi S., Bianchi P., Bier A., Devriendt K., Dimitrov B., Firth H., Gallagher R.C., Garavelli L., Gillessen-Kaesbach G., Hudgins L., Kaariainen H., Karstens S., Krantz I., Mannhardt A., Medne L., Mucke J., Kibaek M., Krogh L.N., Peippo M., Rittinger O., Schulz S., Schelley S.L., Temple I.K., Dennis N.R., Van der Knaap M.S., Wheeler P., Yerushalmi B., Zenker M., Seidel H., Lachmeijer A., Prescott T., Kraus C., Lowry R.B., Rauch A. Clinical and mutational spectrum of Mowat-Wilson syndrome. Eur. J. Med. Genet. 2005, 48:97-111.