L1cam acts as a modifier gene during enteric nervous system development

Neurobiology of Disease

Volumn 40, Issue 3, 2010, Pages 622-633

  Wallace, Adam S ^a   Schmidt, Claudia ^b   Schachner, Melitta ^c   Wegner, Michael ^b   Anderson, Richard B ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c UNIVERSITY OF HAMBURG   (Germany)

Author keywords

Cell migration; Development; Enteric nervous system; Hirschsprung's disease; Neural crest

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; NERVE CELL ADHESION MOLECULE L1; PROTEIN RET; TRANSCRIPTION FACTOR SOX10;

AGANGLIONOSIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; EMBRYO; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INTERACTION; GENE LOSS; INTESTINE INNERVATION; MOUSE; NERVE CELL NECROSIS; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST CELL; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CELL MOVEMENT; ENTERIC NERVOUS SYSTEM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; HIRSCHSPRUNG DISEASE; IMMUNOHISTOCHEMISTRY; MICE; MICE, MUTANT STRAINS; NEURAL CELL ADHESION MOLECULE L1; NEURAL CREST; NEUROGENESIS; PROTO-ONCOGENE PROTEINS C-RET; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SOXE TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 77957759545     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2010.08.006     Document Type: Article

References (57)

1. Amiel J., Sproat-Emison E., Garcia-Barcelo M., Lantieri F., Burzynski G., Borrego S., et al. Hirschsprung disease, associated syndromes and genetics: a review. J. Med. Genet. 2008, 45:1-14.
2. Anderson R.B. Matrix metalloproteinase-2 is involved in the migration and network formation of enteric neural crest-derived cells. Int. J. Dev. Biol. 2010, 54:63-69.
3. Anderson R.B., Bergner A.J., Taniguchi M., Fujisawa H., Forrai A., Robb L., et al. Effects of different regions of the developing gut on the migration of enteric neural crest-derived cells: a role for Sema3A, but not Sema3F. Dev. Biol. 2007, 305:287-299.
4. Anderson R.B., Newgreen D.F., Young H.M. Neural crest and the development of the enteric nervous system. Adv. Exp. Med. Biol. 2006, 589:181-196.
5. Anderson R.B., Stewart A.L., Young H.M. Phenotypes of neural-crest-derived cells in vagal and sacral pathways. Cell Tissue Res. 2006, 323:11-25.
6. Anderson R.B., Turner K.N., Nikonenko A.G., Hemperly J., Schachner M., Young H.M. The cell adhesion molecule l1 is required for chain migration of neural crest cells in the developing mouse gut. Gastroenterology 2006, 130:1221-1232.
7. Asai N., Fukuda T., Wu Z., Enomoto A., Pachnis V., Takahashi M., et al. Targeted mutation of serine 697 in the Ret tyrosine kinase causes migration defect of enteric neural crest cells. Development 2006, 133:4507-4516.
8. 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.
9. Belknap W.M. The pathogenesis of Hirschsprung disease. Curr. Opin. Gastroenterol. 2002, 18:74-81.
10. Bolk S., Pelet A., Hofstra R.M., Angrist M., Salomon R., Croaker D., et al. A human model for multigenic inheritance: phenotypic expression in Hirschsprung disease requires both the RET gene and a new 9q31 locus. Proc. Natl Acad. Sci. USA 2000, 97:268-273.
11. Britsch S., Goerich D.E., Riethmacher D., Peirano R.I., Rossner M., Nave K.A., et al. The transcription factor Sox10 is a key regulator of peripheral glial development. Genes Dev. 2001, 15:66-78.
12. Burns A.J., Le 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.
13. Cantrell V.A., Owens S.E., Chandler R.L., Airey D.C., Bradley K.M., Smith J.R., et al. 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.
14. Carrasquillo M.M., McCallion A.S., Puffenberger E.G., Kashuk C.S., Nouri N., Chakravarti A. Genome-wide association study and mouse model identify interaction between RET and EDNRB pathways in Hirschsprung disease. Nat. Genet. 2002, 32:237-244.
15. Catto-Smith A.G., Trajanovska M., Taylor R.G. Long-term continence after surgery for Hirschsprung's disease. J. Gastroenterol. Hepatol. 2007, 22:2273-2282.
16. de Graaff E., Srinivas S., Kilkenny C., D'Agati V., Mankoo B.S., Costantini F., et al. Differential activities of the RET tyrosine kinase receptor isoforms during mammalian embryogenesis. Genes Dev. 2001, 15:2433-2444.
17. de Pontual L., Zaghloul N.A., Thomas S., Davis E.E., McGaughey D.M., Dollfus H., et al. Epistasis between RET and BBS mutations modulates enteric innervation and causes syndromic Hirschsprung disease. Proc. Natl Acad. Sci. USA 2009, 106:13921-13926.
18. Druckenbrod N.R., Epstein M.L. Age-dependent changes in the gut environment restrict the invasion of the hindgut by enteric neural progenitors. Development 2009, 136:3195-3203.
19. Enomoto H., Crawford P.A., Gorodinsky A., Heuckeroth R.O., Johnson E.M., Milbrandt J. RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development 2001, 128:3963-3974.
20. Fu M., Chi Hang Lui V., Har Sham M., Nga Yin Cheung A., Kwong Hang Tam P. HOXB5 expression is spatially and temporarily regulated in human embryonic gut during neural crest cell colonization and differentiation of enteric neuroblasts. Dev. Dyn. 2003, 228:1-10.
21. Fu M., Sato Y., Lyons-Warren A., Zhang B., Kane M.A., Napoli J.L., et al. Vitamin A facilitates enteric nervous system precursor migration by reducing Pten accumulation. Development 2010, 137:631-640.
22. Gabriel S.B., Salomon R., Pelet A., Angrist M., Amiel J., Fornage M., et al. Segregation at three loci explains familial and population risk in Hirschsprung disease. Nat. Genet. 2002, 31:89-93.
23. Garcia-Barcelo M.M., Tang C.S., Ngan E.S., Lui V.C., Chen Y., So M.T., et al. Genome-wide association study identifies NRG1 as a susceptibility locus for Hirschsprung's disease. Proc. Natl Acad. Sci. USA 2009, 106:2694-2699.
24. Gianino S., Grider J.R., Cresswell J., Enomoto H., Heuckeroth R.O. GDNF availability determines enteric neuron number by controlling precursor proliferation. Development 2003, 130:2187-2198.
25. Griseri P., Vos Y., Giorda R., Gimelli S., Beri S., Santamaria G., et al. Complex pathogenesis of Hirschsprung's disease in a patient with hydrocephalus, vesico-ureteral reflux and a balanced translocation t(3;17)(p12;q11). Eur. J. Hum. Genet. 2009, 17:483-490.
26. Hofstra R.M., Elfferich P., Osinga J., Verlind E., Fransen E., Lopez Pison J., et al. Hirschsprung disease and L1CAM: is the disturbed sex ratio caused by L1CAM mutations?. J. Med. Genet. 2002, 39:E11.
27. 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(6):559-569.
28. Kapur R.P. Colonization of the murine hindgut by sacral crest-derived neural precursors: experimental support for an evolutionarily conserved model. Dev. Biol. 2000, 227:146-155.
29. Kenwrick S., Watkins A., De Angelis E. Neural cell recognition molecule L1: relating biological complexity to human disease mutations. Hum. Mol. Genet. 2000, 9:879-886.
30. 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.
31. Lang D., Epstein J.A. Sox10 and Pax3 physically interact to mediate activation of a conserved c-RET enhancer. Hum. Mol. Genet. 2003, 12:937-945.
32. Le Douarin N.M., Teillet M.A. The migration of neural crest cells to the wall of the digestive tract in avian embryo. J. Embryol. Exp. Morphol. 1973, 30:31-48.
33. 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.
34. McCallion A.S., Stames E., Conlon R.A., Chakravarti A. Phenotype variation in two-locus mouse models of Hirschsprung disease: tissue-specific interaction between Ret and Ednrb. Proc. Natl Acad. Sci. USA 2003, 100:1826-1831.
35. Newgreen D., Young H.M. Enteric nervous system: development and developmental disturbances-part 1. Pediatr. Dev. Pathol. 2002, 5:224-247.
36. Newgreen D., Young H.M. Enteric nervous system: development and developmental disturbances-part 2. Pediatr. Dev. Pathol. 2002, 5:329-349.
37. Okamoto N., Del Maestro R., Valero R., Monros E., Poo P., Kanemura Y., et al. Hydrocephalus and Hirschsprung's disease with a mutation of L1CAM. J. Hum. Genet. 2004, 49:334-337.
38. Owens S.E., Broman K.W., Wiltshire T., Elmore J.B., Bradley K.M., Smith J.R., et al. Genome-wide linkage identifies novel modifier loci of aganglionosis in the Sox10Dom model of Hirschsprung disease. Hum. Mol. Genet. 2005, 14:1549-1558.
39. Parisi M.A., Kapur R.P. Genetics of Hirschsprung disease. Curr. Opin. Pediatr. 2000, 12:610-617.
40. Parisi M.A., Kapur R.P., Neilson I., Hofstra R.M., Holloway L.W., Michaelis R.C., et al. Hydrocephalus and intestinal aganglionosis: is L1CAM a modifier gene in Hirschsprung disease?. Am. J. Med. Genet. 2002, 108:51-56.
41. Peirano R.I., Goerich D.E., Riethmacher D., Wegner M. Protein zero gene expression is regulated by the glial transcription factor Sox10. Mol. Cell. Biol. 2000, 20:3198-3209.
42. Pichel J.G., Shen L., Sheng H.Z., Granholm A.C., Drago J., Grinberg A., et al. Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 1996, 382:73-76.
43. Roberts R.R., Bornstein J.C., Bergner A.J., Young H.M. Disturbances of colonic motility in mouse models of Hirschsprung's disease. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 294:G996-G1008.
44. Sanchez-Mejias A., Watanabe Y., Fernandez M., Lopez-Alonso M., Antinolo G., Bondurand N., et al. Involvement of SOX10 in the pathogenesis of Hirschsprung disease: report of a truncating mutation in an isolated patient. J. Mol. Med. 2010.
45. Schuchardt A., D'Agati V., Larsson-Blomberg L., Costantini F., Pachnis V. Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret. Nature 1994, 367:380-383.
46. Simpson M.J., Zhang D.C., Mariani M., Landman K.A., Newgreen D.F. Cell proliferation drives neural crest cell invasion of the intestine. Dev. Biol. 2007, 302:553-568.
47. 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.
48. Stanchina L., Baral V., Robert F., Pingault V., Lemort N., Pachnis V., et al. Interactions between Sox10, Edn3 and Ednrb during enteric nervous system and melanocyte development. Dev. Biol. 2006, 295:232-249.
49. Stewart A.L., Anderson R.B., Young H.M. Characterization of lacZ-expressing cells in the gut of embryonic and adult DbetaH-nlacZ mice. J. Comp. Neurol. 2003, 464:208-219.
50. Tannuri A.C., Tannuri U., Romao R.L. Transanal endorectal pull-through in children with Hirschsprung's disease-technical refinements and comparison of results with the Duhamel procedure. J. Pediatr. Surg. 2009, 44:767-772.
51. Turner K.N., Schachner M., Anderson R.B. Cell adhesion molecule L1 affects the rate of differentiation of enteric neurons in the developing gut. Dev. Dyn. 2009, 238:708-715.
52. Uesaka T., Nagashimada M., Yonemura S., Enomoto H. Diminished Ret expression compromises neuronal survival in the colon and causes intestinal aganglionosis in mice. J. Clin. Invest. 2008, 118:1890-1898.
53. Wallace A.S., Burns A.J. Development of the enteric nervous system, smooth muscle and interstitial cells of Cajal in the human gastrointestinal tract. Cell Tissue Res. 2005, 319:367-382.
54. Yntema C.L., Hammond W.S. The origin of intrinsic ganglia of trunk viscera from vagal neural crest in the chick embryo. J. Comp. Neurol. 1954, 101:515-541.
55. Young H.M., Bergner A.J., Anderson R.B., Enomoto H., Milbrandt J., Newgreen D.F., et al. Dynamics of neural crest-derived cell migration in the embryonic mouse gut. Dev. Biol. 2004, 270:455-473.
56. Young H.M., Newgreen D. Enteric neural crest-derived cells: origin, identification, migration, and differentiation. Anat. Rec. 2001, 262:1-15.
57. 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.