Identification of Sox8 as a modifier gene in a mouse model of Hirschsprung disease reveals underlying molecular defect

Developmental Biology

Volumn 277, Issue 1, 2005, Pages 155-169

  Maka, Marzena ^a   Claus Stolt, C ^a   Wegner, Michael ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Enteric nervous system; High mobility group; Hirschsprung disease; Megacolon; Sox10; Sry

Indexed keywords

ALLELE; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DNA MODIFICATION; GENE FUNCTION; HETEROZYGOSITY; HIRSCHSPRUNG DISEASE; INTESTINE INNERVATION; MOUSE; MUTATION; NERVE CELL DIFFERENTIATION; NEURAL CREST; NEURAL CREST CELL; NONHUMAN; PRIORITY JOURNAL; RAT; REDUCTION;

EID: 9644277156     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2004.09.014     Document Type: Article

References (49)

1. M. Angrist, S. Bolk, M. Halushka, P.A. Lapchak, and A. Chakravarti Germline mutations in glial cell line-derived neurotropic factor (GDNF) and RET in a Hirschsprung disease patient Nat. Genet. 14 1996 341 344
2. A. Barlow, E. de Graaff, and V. Pachnis Enteric nervous system progenitors are coordinately controlled by the G protein-coupled receptor EDNRB and the receptor tyrosine kinase RET Neuron 40 2003 905 916
3. J. Bowles, G. Schepers, and P. Koopman Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators Dev. Biol. 227 2000 239 255
4. S. Britsch, D.E. Goerich, D. Riethmacher, R.I. Peirano, M. Rossner, K.A. Nave, C. Birchmeier, and M. Wegner The transcription factor Sox10 is a key regulator of peripheral glial development Genes Dev. 15 2001 66 78
5. A.J. Burns, D. Champeval, and N.M. Le Douarin Sacral neural crest cells colonise aganglionic hindgut in vivo but fail to compensate for lack of enteric ganglia Dev. Biol. 219 2000 30 43
6. V. Cacheux, F. Dastot-Le Moal, H. Kaariainen, N. Bondurand, R. Rintala, B. Boissier, M. Wilson, D. Mowat, and M. Goossens Loss-of-function mutations in SIP1 Smad interacting protein 1 result in a syndromic Hirschsprung disease Hum. Mol. Genet. 10 2001 1503 1510
7. M.-C. Chaboissier, A. Kobayashi, V.I.P. Vidal, S. Lützkendorf, H.J.G. van de Kant, M. Wegner, D.G. de Rooij, R.R. Behringer, and A. Schedl Functional analysis of Sox8 and Sox9 during sex determination in the mouse Development 131 2004 1891 1901
8. A. Chakravarti Hirschsprung disease C.R. Scriver A.L. Beaudet D. Valle W.S. Sly B. Childs K. Kinzler B. Vogelstein The Metabolic and Molecular Bases of Inherited Disease 2001 McGraw-Hill New York 6231 6255
9. M. Cheung, and J. Briscoe Neural crest development is regulated by the transcription factor Sox9 Development 130 2003 5681 5693
10. P.J. Conner, P.J. Focke, D.M. Noden, and M.L. Epstein Appearance of neurons and glia with respect to the wavefront during colonization of the avian gut by neural crest cells Dev. Dyn. 226 2003 91 98
11. P. Edery, S. Lyonnet, L.M. Mulligan, A. Pelet, E. Dow, L. Abel, S. Holder, C. Nihoul-Fekete, B.A. Ponder, and A. Munnich Mutations of the RET proto-oncogene in Hirschsprung's disease Nature 367 1994 378 380
12. P. Edery, T. Attie, J. Amiel, A. Pelet, C. Eng, R.M. Hofstra, H. Martelli, C. Bidaud, A. Munnich, and S. Lyonnet Mutation of the endothelin-3 gene in the Waardenburg-Hirschsprung disease (Shah-Waardenburg syndrome) Nat. Genet. 12 1996 442 444
13. J.W. Foster, M.A. Dominguez-Steglich, S. Guioli, C. Kwok, P.A. Weller, M. Stevanovic, J. Weissenbach, S. Mansour, I.D. Young, P.N. Goodfellow, J.D. Brook, and A.J. Schafer Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene Nature 372 1994 525 530
14. S.B. Gabriel, R. Salomon, A. Pelet, M. Angrist, J. Amiel, M. Fornage, T. Attie-Bitach, J.M. Olson, R. Hofstra, and C. Buys Segregation at three loci explains familial and population risk in Hirschsprung disease Nat. Genet. 31 2002 89 93
15. M.D. Gershon Lessons from genetically engineered animal models: II. Disorders of enteric neuronal development: insights from transgenic mice Am. J. Physiol. 277 1999 G262 G267
16. C. Hearn, and D. Newgreen Lumbo-sacral neural crest contributes to the avian enteric nervous system independently of vagal neural crest Dev. Dyn. 218 2000 525 530
17. B. Herbarth, V. Pingault, N. Bondurand, K. Kuhlbrodt, I. Hermans-Borgmeyer, A. Puliti, N. Lemort, M. Goossens, and M. Wegner Mutation of the Sry-related Sox10 gene in dominant megacolon, a mouse model for human Hirschsprung disease Proc. Natl. Acad. Sci. U. S. A. 95 1998 5161 5165
18. R.P. Kapur Early death of neural crest cells is responsible for total enteric aganglionosis in Sox10(Dom)/Sox10(Dom) mouse embryos Pediatr. Dev. Pathol. 2 1999 559 569
19. J. Kim, L. Lo, E. Dormand, and D.J. Anderson SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells Neuron 38 2003 17 31
20. G.M. Kruger, J.T. Mosher, Y.-W. Tsai, K.J. Yeager, T. Iwahita, C.E. Gariepy, and S.J. Morrison Temporally distinct requirements for endothelin receptor B in the generation and migration of gut neural crest stem cells Neuron 40 2003 917 929
21. K. Kuhlbrodt, B. Herbarth, E. Sock, J. Enderich, I. Hermans-Borgmeyer, and M. Wegner Cooperative function of POU proteins and Sox proteins in glial cells J. Biol. Chem. 273 1998 16050 16057
22. K. Kuhlbrodt, C. Schmidt, E. Sock, V. Pingault, N. Bondurand, M. Goossens, and M. Wegner Functional analysis of Sox10 mutations found in human Waardenburg-Hirschsprung patients J. Biol. Chem. 273 1998 23033 23038
23. N. Le Douarin, and C. Kalchheim The Neural Crest 1999 Cambridge University Press Cambridge, UK
24. D. Newgreen, and H.M. Young Enteric nervous system: development and developmental disturbances-Part 1 Pediatr. Dev. Pathol. 5 2002 224 247
25. C. Paratore, D.E. Goerich, U. Suter, M. Wegner, and L. Sommer Survival and glial fate acquisition of neural crest cells are regulated by an interplay between the transcription factor Sox10 and extrinsic combinatorial signaling Development 128 2001 3949 3961
26. C. Paratore, C. Eichenberger, U. Suter, and L. Sommer Sox10 haploinsufficiency affects maintenance of progenitor cells in a mouse model of Hirschsprung disease Hum. Mol. Genet. 11 2002 3075 3085
27. D. Pfeifer, F. Poulat, E. Holinski-Feder, F. Kooy, and G. Scherer The SOX8 gene is located within 700 kb of the tip of chromosome 16p and is deleted in a patient with ATR-16 syndrome Genomics 63 2000 108 116
28. V. Pingault, N. Bondurand, K. Kuhlbrodt, D.E. Goerich, M.-O. Prehu, A. Puliti, B. Herbarth, I. Hermans-Borgmeyer, E. Legius, G. Matthijs, J. Amiel, S. Lyonnet, I. Ceccherini, G. Romeo, J.C. Smith, A.P. Read, M. Wegner, and M. Goossens Sox10 mutations in patients with Waardenburg-Hirschsprung disease Nat. Genet. 18 1998 171 173
29. E.G. Puffenberger, K. Hosoda, S.S. Washington, K. Nakao, D. deWit, M. Yanagisawa, and A. Chakravarti A missense mutation of the endothelin-B receptor gene in multigenic Hirschsprung's disease Cell 79 1994 1257 1266
30. S. Rehberg, P. Lischka, G. Glaser, S. Stamminger, M. Wegner, and O. Rosorius Sox10 is an active nucleocytoplasmic shuttling protein and shuttling is required for Sox10-mediated transactivation Mol. Cell. Biol. 22 2002 5826 5834
31. R. Salomon, T. Attie, A. Pelet, C. Bidaud, C. Eng, J. Amiel, S. Sarnacki, O. Goulet, C. Ricour, and C. Nihoul-Fekete Germline mutations of the RET ligand GDNF are not sufficient to cause Hirschsprung disease Nat. Genet. 14 1996 345 347
32. G.E. Schepers, M. Bullejos, B.M. Hosking, and P. Koopman Cloning and characterisation of the sry-related transcription factor gene sox8 Nucleic Acids Res. 28 2000 1473 1480
33. G. Schepers, M. Wilson, D. Wilhelm, and P. Koopman Sox8 is expressed during testis differentiation in mice and synergizes with SF1 to activate the AMH promoter in vitro J. Biol. Chem. 278 2003 28101 28108
34. K. Schmidt, G. Glaser, A. Wernig, M. Wegner, and O. Rosorius Sox8 is a specific marker for muscle satellite cells and inhibits myogenesis J. Biol. Chem. 278 2003 29769 29775
35. A. Schuchardt, V. D'Agati, L. Larsson-Blomberg, F. Costantini, and V. Pachnis Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret Nature 367 1994 380 383
36. M.K. Shin, J.M. Levorse, R.S. Ingram, and S.M. Tilghman The temporal requirement for endothelin receptor-B signalling during neural crest development Nature 402 1999 496 501
37. E. Sock, K. Schmidt, I. Hermanns-Borgmeyer, M.R. Bösl, and M. Wegner Idiopathic weight reduction in mice deficient in the high-mobility-group transcription factor Sox8 Mol. Cell. Biol. 21 2001 6951 6959
38. E. Sonnenberg-Riethmacher, M. Miehe, C.C. Stolt, D.E. Goerich, M. Wegner, and D. Riethmacher Development and degeneration of dorsal root ganglia in the absence of the HMG-domain transcription factor Sox10 Mech. Dev. 109 2001 253 265
39. E.M. Southard-Smith, L. Kos, and W.J. Pavan Sox10 mutation disrupts neural crest development in Dom Hirschsprung mouse model Nat. Genet. 18 1998 60 64
40. E.M. Southard-Smith, M. Angrist, J.S. Ellison, R. Agarwala, A.D. Baxevanis, A. Chakravarti, and W.J. Pavan The Sox10(Dom) mouse: modeling the genetic variation of Waardenburg-Shah (WS4) syndrome Genome Res. 9 1999 215 225
41. C.C. Stolt, S. Rehberg, M. Ader, P. Lommes, D. Riethmacher, M. Schachner, U. Bartsch, and M. Wegner Terminal differentiation of myelin-forming oligodendrocytes depends on the transcription factor Sox10 Genes Dev. 16 2002 165 170
42. C.C. Stolt, P. Lommes, E. Sock, M.-C. Chaboissier, A. Schedl, and M. Wegner The Sox9 transcription factor determines glial fate choice in the developing spinal cord Genes Dev. 17 2003 1677 1689
43. C.C. Stolt, P. Lommes, R.P. Friedrich, and M. Wegner Transcription factors Sox8 and Sox10 perform non-equivalent roles during oligodendrocyte development despite functional redundancy Development 131 2004 2349 2358
44. T. Wagner, J. Wirth, J. Meyer, B. Zabel, M. Held, J. Zimmer, J. Pasantes, F.D. Bricarelli, J. Keutel, E. Hustert, U. Wolf, N. Tommerup, W. Schempp, and G. Scherer Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene Sox9 Cell 79 1994 1111 1120
45. N. Wakamatsu, Y. Yamada, K. Yamada, T. Ono, N. Nomura, H. Taniguchi, H. Kitoh, N. Mutoh, T. Yamanaka, K. Mushiake, K. Kato, S. Sonta, and M. Nagaya Mutations in SIP1, encoding Smad interacting protein-1, cause a form of Hirschsprung disease Nat. Genet. 27 2001 369 370
46. M. Wegner From head to toes: the multiple facets of Sox proteins Nucleic Acids Res. 27 1999 1409 1420
47. C.L. Yntema, and W.S. Hammond The origin of intrinsic ganglia of trunk viscera from vagal neural crest in the chick embryo J. Comp. Neurol. 1954 515 541
48. H.M. Young, and D. Newgreen Enteric neural crest-derived cells: origin, identification, migration and differentiation Anat. Rec. 262 2001 1 15
49. H.M. Young, A.J. Bergner, and T. Müller Acquisition of neuronal and glial markers by neural crest-derived cells in the mouse intestine J. Comp. Neurol. 456 2003 1 11