Tcof1 acts as a modifier of Pax3 during enteric nervous system development and in the pathogenesis of colonic aganglionosis

Human Molecular Genetics

Volumn 22, Issue 6, 2013, Pages 1206-1217

  Barlow, Amanda J ^a,b   Dixon, Jill ^c   Dixon, Michael ^c,d   Trainor, Paul A ^a,e  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TUBULIN; NUCLEAR PROTEIN; PROTEIN P75; PROTEIN RET; PROTEIN TCOF1; TRANSCRIPTION FACTOR PAX3; TRANSCRIPTION FACTOR SOX10; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; COLON AGANGLIONOSIS; CONTROLLED STUDY; EMBRYO; HAPLOINSUFFICIENCY; HETEROZYGOSITY; HIRSCHSPRUNG DISEASE; INTESTINE INNERVATION; LOSS OF FUNCTION MUTATION; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; COLON; ENTERIC NERVOUS SYSTEM; FEMALE; HIRSCHSPRUNG DISEASE; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, KNOCKOUT; NEURAL CREST; NUCLEAR PROTEINS; PAIRED BOX TRANSCRIPTION FACTORS; PHOSPHOPROTEINS;

EID: 84874551333     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds528     Document Type: Article

References (51)

1. Heanue, T.A. and Pachnis, V. (2007) Enteric nervous system development and Hirschsprung's disease: advances in genetic and stem cell studies. Nat. Rev. Neurosci., 8, 466-479.
2. Le Douarin, N.M. and Teillet, M.A. (1973) The migration of neural crest cells to the wall of the digestive tract in avian embryo. J. Embryol. Exp. Morphol., 30, 31-48.
3. Laranjeira, C. and Pachnis, V. (2009) Enteric nervous system development: recent progress and future challenges. Auton. Neurosci., 151, 61-69.
4. Amiel, J., Sproat-Emison, E., Garcia-Barcelo, M., Lantieri, F., Burzynski, G., Borrego, S., Pelet, A., Arnold, S., Miao, X., Griseri, P. et al. (2008) Hirschsprung disease, associated syndromes and genetics: a review. J. Med. Genet., 45, 1-14.
5. Belknap, W.M. (2002) The pathogenesis of Hirschsprung disease. Curr. Opin. Gastroenterol., 18, 74-81.
6. Parisi, M.A. and Kapur, R.P. (2000) Genetics of Hirschsprung disease. Curr. Opin. Pediatr., 12, 610-617.
7. Gershon, M.D. (1997) Genes and lineages in the formation of the enteric nervous system. Curr. Opin. Neurobiol., 7, 101-109.
8. Garcia-Barcelo, M.M., Tang, C.S., Ngan, E.S., Lui, V.C., Chen, Y., So, M.T., Leon, T.Y., Miao, X.P., Shum, C.K., Liu, F.Q. et al. (2009) Genome-wide association study identifies NRG1 as a susceptibility locus for Hirschsprung's disease. Proc. Natl Acad. Sci. USA, 106, 2694-2699.
9. Tang, C.S., Tang, W.K., So, M.T., Miao, X.P., Leung, B.M., Yip, B.H., Leon, T.Y., Ngan, E.S., Lui, V.C., Chen, Y. et al. (2011) Fine mapping of the NRG1 Hirschsprung's disease locus. PloS One., 6, e16181.
10. Wallace, A.S. and Anderson, R.B. (2011) Genetic interactions and modifier genes in Hirschsprung's disease. World J. Gastroenterol, 17, 4937-4944.
11. Pingault, V., Ente, D., Dastot-Le Moal, F., Goossens, M., Marlin, S. and Bondurand, N. (2010) Review and update of mutations causing Waardenburg syndrome. Hum. Mutat., 31, 391-406.
12. Baldwin, C.T., Hoth, C.F., Macina, R.A. and Milunsky, A. (1995) Mutations in PAX3 that cause Waardenburg syndrome type I: ten new mutations and review of the literature. Am. J. Med. Genet., 58, 115-122.
13. Hoth, C.F., Milunsky, A., Lipsky, N., Sheffer, R., Clarren, S.K. and Baldwin, C.T. (1993) Mutations in the paired domain of the human PAX3 gene cause Klein-Waardenburg syndrome (WS-III) as well as Waardenburg syndrome type I (WS-I). Am. J. Hum. Genet., 52, 455-462.
14. Tassabehji, M., Read, A.P., Newton, V.E., Harris, R., Balling, R., Gruss, P. and Strachan, T. (1992) Waardenburg's syndrome patients have mutations in the human homologue of the Pax-3 paired box gene. Nature, 355, 635-636.
15. Lang, D., Chen, F., Milewski, R., Li, J., Lu, M.M. and Epstein, J.A. (2000) Pax3 is required for enteric ganglia formation and functions with Sox10 to modulate expression of c-ret. J. Clin. Invest., 106, 963-971.
16. Lang, D. and Epstein, J.A. (2003) Sox10 and Pax3 physically interact to mediate activation of a conserved c-RET enhancer. Hum. Mol. Genet., 12, 937-945.
17. Leon, T.Y., Ngan, E.S., Poon, H.C., So, M.T., Lui, V.C., Tam, P.K. and Garcia-Barcelo, M.M. (2009) Transcriptional regulation of RET by Nkx2-1, Phox2b, Sox10, and Pax3. J. Pediatr. Surg., 44, 1904-1912.
18. Barlow, A.J., Dixon, J., Dixon, M. and Trainor, P.A. (2012) Balancing neural crest cell intrinsic processes with those of the microenvironment in Tcof1 haploinsufficient mice enables complete enteric nervous system formation. Hum. Mol. Genet., 21, 1782-1793.
19. Jones, N.C., Lynn, M.L., Gaudenz, K., Sakai, D., Aoto, K., Rey, J.P., Glynn, E.F., Ellington, L., Du, C., Dixon, J. et al. (2008) Prevention of the neurocristopathy Treacher Collins syndrome through inhibition of p53 function. Nat. Med., 14, 125-133.
20. Treacher Collins Syndrome Collaborative Group. (1996) Positional cloning of a gene involved in the pathogenesis of Treacher Collins syndrome. Nat. Genet., 12, 130-136.
21. Dixon, J., Jones, N.C., Sandell, L.L., Jayasinghe, S.M., Crane, J., Rey, J.P., Dixon, M.J. and Trainor, P.A. (2006) Tcof1/Treacle is required for neural crest cell formation and proliferation deficiencies that cause craniofacial abnormalities. Proc. Natl Acad. Sci. USA, 103, 13403-13408.
22. Pani, L., Horal, M. and Loeken, M.R. (2002) Rescue of neural tube defects in Pax-3-deficient embryos by p53 loss of function: implications for Pax-3- dependent development and tumorigenesis. Genes Dev., 16, 676-680.
23. Schuchardt, A., D'Agati, V., Larsson-Blomberg, L., Costantini, F. and Pachnis, V. (1994) Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature, 367, 380-383.
24. Auerbach, R. (1954) Analysis of the developmental effects of a lethal mutation in the house mouse. J. Exp. Zool., 127, 305-329.
25. Epstein, D.J., Vekemans, M. and Gros, P. (1991) Splotch (Sp2H), a mutation affecting development of the mouse neural tube, shows a deletion within the paired homeodomain of Pax3. Cell, 67, 767-774.
26. Epstein, D.J., Vogan, K.J., Trasler, D.G. and Gros, P. (1993) A mutation within intron 3 of the Pax-3 gene produces aberrantly spliced mRNA transcripts in the splotch (Sp) mouse mutant. Proc. Natl. Acad. Sci. USA, 90, 532-536.
27. Paratore, C., Eichenberger, C., Suter, U. and Sommer, L. (2002) Sox10 haploinsufficiency affects maintenance of progenitor cells in a mouse model of Hirschsprung disease. Hum. Mol. Genet., 11, 3075-3085.
28. Kim, J., Lo, L., Dormand, E. and Anderson, D.J. (2003) SOX10 maintains multipotency and inhibits neuronal differentiation of neural crest stem cells. Neuron, 38, 17-31.
29. Bondurand, N., Natarajan, D., Barlow, A., Thapar, N. and Pachnis, V. (2006) Maintenance of mammalian enteric nervous system progenitors by SOX10 and endothelin 3 signalling. Development, 133, 2075-2086.
30. Bondurand, N., Natarajan, D., Thapar, N., Atkins, C. and Pachnis, V. (2003) Neuron and glia generating progenitors of the mammalian enteric nervous system isolated from foetal and postnatal gut cultures. Development, 130, 6387-6400.
31. Durbec, P.L., Larsson-Blomberg, L.B., Schuchardt, A., Costantini, F. and Pachnis, V. (1996) Common origin and developmental dependence on c-ret of subsets of enteric and sympathetic neuroblasts. Development, 122, 349-358.
32. Morgan, S.C., Lee, H.Y., Relaix, F., Sandell, L.L., Levorse, J.M. and Loeken, M.R. (2008) Cardiac outflow tract septation failure in Pax3-deficient embryos is due to p53-dependent regulation of migrating cardiac neural crest. Mech. Dev., 125, 757-767.
33. Phelan, S.A., Ito, M. and Loeken, M.R. (1997) Neural tube defects in embryos of diabetic mice: role of the Pax-3 gene and apoptosis. Diabetes, 46, 1189-1197.
34. Underwood, T.J., Amin, J., Lillycrop, K.A. and Blaydes, J.P. (2007) Dissection of the functional interaction between p53 and the embryonic proto-oncoprotein PAX3. FEBS. Lett., 581, 5831-5835.
35. Maka, M., Stolt, C.C. and Wegner, M. (2005) Identification of Sox8 as a modifier gene in a mouse model of Hirschsprung disease reveals underlying molecular defect. Dev. Biol., 277, 155-169.
36. Stanchina, L., Baral, V., Robert, F., Pingault, V., Lemort, N., Pachnis, V., Goossens, M. and Bondurand, N. (2006) Interactions between Sox10, Edn3 and Ednrb during enteric nervous system and melanocyte development. Dev. Biol., 295, 232-249.
37. Wallace, A.S., Schmidt, C., Schachner, M., Wegner, M. and Anderson, R.B. (2010) L1cam acts as a modifier gene during enteric nervous system development. Neurobiol. Dis., 40, 622-633.
38. Wallace, A.S., Barlow, A.J., Navaratne, L., Delalande, J.M., Tauszig-Delamasure, S., Corset, V., Thapar, N. and Burns, A.J. (2009) Inhibition of cell death results in hyperganglionosis: implications for enteric nervous system development. Neurogastroenterol Motil., 21, 768-e49.
39. Barlow, A.J., Wallace, A.S., Thapar, N. and Burns, A.J. (2008) Critical numbers of neural crest cells are required in the pathways from the neural tube to the foregut to ensure complete enteric nervous system formation. Development, 135, 1681-1691.
40. Zhang, D., Brinas, I.M., Binder, B.J., Landman, K.A. and Newgreen, D.F. (2010) Neural crest regionalisation for enteric nervous system formation: implications for Hirschsprung's disease and stem cell therapy. Dev. Biol., 339, 280-294.
41. Stanchina, L., Van de Putte, T., Goossens, M., Huylebroeck, D. and Bondurand, N. (2010) Genetic interaction between Sox10 and Zfhx1b during enteric nervous system development. Dev. Biol., 341, 416-428.
42. Okamura, Y. and Saga, Y. (2008) Notch signaling is required for the maintenance of enteric neural crest progenitors. Development, 135, 3555- 3565.
43. Lei, J. and Howard, M.J. (2011) Targeted deletion of Hand2 in enteric neural precursor cells affects its functions in neurogenesis, neurotransmitter specification and gangliogenesis, causing functional aganglionosis. Development, 138, 4789-4800.
44. Mundell, N.A., Plank, J.L., LeGrone, A.W., Frist, A.Y., Zhu, L., Shin, M.K., Southard-Smith, E.M. and Labosky, P.A. (2012) Enteric nervous system specific deletion of Foxd3 disrupts glial cell differentiation and activates compensatory enteric progenitors. Dev. Biol., 363, 373-387.
45. Goulding, M.D., Chalepakis, G., Deutsch, U., Erselius, J.R. and Gruss, P. (1991) Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. EMBO J., 10, 1135-1147.
46. Conway, S.J., Henderson, D.J. and Copp, A.J. (1997) Pax3 is required for cardiac neural crest migration in the mouse: evidence from the splotch (Sp2H) mutant. Development, 124, 505-514.
47. Epstein, J.A., Li, J., Lang, D., Chen, F., Brown, C.B., Jin, F., Lu, M.M., Thomas, M., Liu, E., Wessels, A. et al. (2000) Migration of cardiac neural crest cells in Splotch embryos. Development, 127, 1869-1878.
48. Conway, S.J., Bundy, J., Chen, J., Dickman, E., Rogers, R. and Will, B.M. (2000) Decreased neural crest stem cell expansion is responsible for the conotruncal heart defects within the splotch (Sp(2H))/Pax3 mouse mutant. Cardiovasc. Res., 47, 314-328.
49. Lang, D., Lu, M.M., Huang, L., Engleka, K.A., Zhang, M., Chu, E.Y., Lipner, S., Skoultchi, A., Millar, S.E. and Epstein, J.A. (2005) Pax3 functions at a nodal point in melanocyte stem cell differentiation. Nature, 433, 884-887.
50. Kubic, J.D., Young, K.P., Plummer, R.S., Ludvik, A.E. and Lang, D. (2008) Pigmentation PAX-ways: the role of Pax3 in melanogenesis, melanocyte stem cell maintenance, and disease. Pigment Cell Melanoma Res., 21, 627-645.
51. Dixon, J., Brakebusch, C., Fassler, R. and Dixon, M.J. (2000) Increased levels of apoptosis in the prefusion neural folds underlie the craniofacial disorder, Treacher Collins syndrome. Hum. Mol. Genet., 9, 1473-1480.