The Cell Adhesion Molecule L1 Is Required for Chain Migration of Neural Crest Cells in the Developing Mouse Gut

Gastroenterology

Volumn 130, Issue 4, 2006, Pages 1221-1232

  Anderson, Richard B ^a   Turner, Kirsty N ^a   Nikonenko, Alexander G ^b   Hemperly, John ^c   Schachner, Melitta ^b   Young, Heather M ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c BD Technologies   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; CELL ADHESION MOLECULE; CELL ADHESION MOLECULE L1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOASSAY; CELL ACTIVITY; CELL MIGRATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; FEMALE; HIRSCHSPRUNG DISEASE; IN VITRO STUDY; IN VIVO STUDY; INTESTINE; INTESTINE INNERVATION; KNOCKOUT MOUSE; MICROSCOPY; MOUSE; NEURAL CREST CELL; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

EID: 33645998136     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2006.01.002     Document Type: Article

References (62)

1. Yntema C.L., and Hammond W.S. The origin of intrinsic ganglia of trunk viscera from vagal neural crest in the chick embryo. J Comp Neurol 101 (1954) 515-541
2. Le Douarin N.M., and Teillet M.A. The migration of neural crest cells to the wall of the digestive tract in avian embryo. J Embryol Exp Morphol 30 (1973) 31-48
3. Puri P., and Wester T. Experience with Swenson's operation. In: Holschneider A.M., and Puri P. (Eds). Hirschsprung's disease and allied disorders (2000), Harwood Academic Publishers, Amsterdam, The Netherlands Chapter 19.2.
4. Belknap W.M. The pathogenesis of Hirschsprung disease. Curr Opin Gastroenterol 18 (2002) 74-81
5. Gariepy C.E. Developmental disorders of the enteric nervous system. genetic and molecular bases. J Pediatr Gastroenterol Nutr 39 (2004) 5-11
6. Parisi M.A., and Kapur R.P. Genetics of Hirschsprung disease. Curr Opin Pediatr 12 (2000) 610-617
7. Badner J.A., Sieber W.K., Garver K.L., and Chakravarti A. A genetic study of Hirschsprung disease. Am J Hum Genet 46 (1990) 568-580
8. Bolk S., Pelet A., Hofstra R.M., Angrist M., Salomon R., Croaker D., Buys C.H., Lyonnet S., and Chakravarti A. 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 U S A 97 (2000) 268-273
9. Carrasquillo M.M., McCallion A.S., Puffenberger E.G., Kashuk C.S., Nouri N., and Chakravarti A. Genome-wide association study and mouse model identify interaction between RET and EDNRB pathways in Hirschsprung disease. Nat Genet 32 (2002) 237-244
10. McCallion A.S., Stames E., Conlon R.A., and Chakravarti A. Phenotype variation in two-locus mouse models of Hirschsprung disease. tissue-specific interaction between Ret and Ednrb. Proc Natl Acad Sci U S A 100 (2003) 1826-1831
11. Cantrell V.A., Owens S.E., Chandler R.L., Airey D.C., Bradley K.M., Smith J.R., and 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 13 (2004) 2289-2301
12. Kenwrick S., Watkins A., and De Angelis E. Neural cell recognition molecule L1. relating biological complexity to human disease mutations. Hum Mol Genet 9 (2000) 879-886
13. Okamoto N., Wada Y., and Goto M. Hydrocephalus and Hirschsprung's disease in a patient with a mutation of L1CAM. J Med Genet 34 (1997) 670-671
14. Hofstra R.M., Elfferich P., Osinga J., Verlind E., Fransen E., Lopez Pison J., de Die-Smulders C.E., Stolte-Dijkstra I., and Buys C.H. Hirschsprung disease and L1CAM. is the disturbed sex ratio caused by L1CAM mutations?. J Med Genet 39 (2002) E11
15. Parisi M.A., Kapur R.P., Neilson I., Hofstra R.M., Holloway L.W., Michaelis R.C., and Leppig K.A. Hydrocephalus and intestinal aganglionosis. is L1CAM a modifier gene in Hirschsprung disease?. Am J Med Genet 108 (2002) 51-56
16. Okamoto N., Del Maestro R., Valero R., Monros E., Poo P., Kanemura Y., and Yamasaki M. Hydrocephalus and Hirschsprung's disease with a mutation of L1CAM. J Hum Genet 49 (2004) 334-337
17. Brummendorf T., Kenwrick S., and Rathjen F.G. Neural cell recognition molecule L1. from cell biology to human hereditary brain malformations. Curr Opin Neurobiol 8 (1998) 87-97
18. Haspel J., and Grumet M. The L1CAM extracellular region. a multi-domain protein with modular and cooperative binding modes. Front Biosci 8 (2003) s1210-s1225
19. Lindner J., Rathjen F.G., and Schachner M. L1 mono- and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. Nature 305 (1983) 427-430
20. Demyanenko G.P., Shibata Y., and Maness P.F. Altered distribution of dopaminergic neurons in the brain of L1 null mice. Brain Res Dev Brain Res 126 (2001) 21-30
21. Thelen K., Kedar V., Panicker A.K., Schmid R.S., Midkiff B.R., and Maness P.F. The neural cell adhesion molecule L1 potentiates integrin-dependent cell migration to extracellular matrix proteins. J Neurosci 22 (2002) 4918-4931
22. Ohyama K., Kawano H., Asou H., Fukuda T., Oohira A., Uyemura K., and Kawamura K. Coordinate expression of L1 and 6B4 proteoglycan/phosphacan is correlated with the migration of mesencephalic dopaminergic neurons in mice. Brain Res Dev Brain Res 107 (1998) 219-226
23. Fushiki S., and Schachner M. Immunocytological localization of cell adhesion molecules L1 and N-CAM and the shared carbohydrate epitope L2 during development of the mouse neocortex. Brain Res 389 (1986) 153-167
24. Mechtersheimer S., Gutwein P., Agmon-Levin N., Stoeck A., Oleszewski M., Riedle S., Postina R., Fahrenholz F., Fogel M., Lemmon V., and Altevogt P. Ectodomain shedding of L1 adhesion molecule promotes cell migration by autocrine binding to integrins. J Cell Biol 155 (2001) 661-673
25. Gutwein P., Oleszewski M., Mechtersheimer S., Agmon-Levin N., Krauss K., and Altevogt P. Role of Src kinases in the ADAM-mediated release of L1 adhesion molecule from human tumor cells. J Biol Chem 275 (2000) 15490-15497
26. Enomoto H., Crawford P.A., Gorodinsky A., Heuckeroth R.O., Johnson Jr. E.M., and Milbrandt J. RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development 128 (2001) 3963-3974
27. Mercer E.H., Hoyle G.W., Kapur R.P., Brinster R.L., and Palmiter R.D. The dopamine beta-hydroxylase gene promoter directs expression of E. coli lacZ to sympathetic and other neurons in adult transgenic mice. Neuron 7 (1991) 703-716
28. Dahme M., Bartsch U., Martini R., Anliker B., Schachner M., and Mantei N. Disruption of the mouse L1 gene leads to malformations of the nervous system. Nat Genet 17 (1997) 346-349
29. Hearn C.J., Young H.M., Ciampoli D., Lomax A.E., and Newgreen D. Catenary cultures of embryonic gastrointestinal tract support organ morphogenesis, motility, neural crest cell migration, and cell differentiation. Dev Dyn 214 (1999) 239-247
30. Galko M.J., and Tessier-Lavigne M. Function of an axonal chemoattractant modulated by metalloprotease activity. Science 289 (2000) 1365-1367
31. Young H.M., Jones B.R., and McKeown S.J. The projections of early enteric neurons are influenced by the direction of neural crest cell migration. J Neurosci 22 (2002) 6005-6018
32. Kapur R.P., Yost C., and Palmiter R.D. A transgenic model for studying development of the enteric nervous system in normal and aganglionic mice. Development 116 (1992) 167-175
33. Probstmeier R., Martini R., Tacke R., and Schachner M. Expression of the adhesion molecules L1, N-CAM and J1/tenascin during development of the murine small intestine. Differentiation 44 (1990) 42-55
34. Young H.M., Bergner A.J., Anderson R.B., Enomoto H., Milbrandt J., Newgreen D.F., and Whitington P.M. Dynamics of neural crest-derived cell migration in the embryonic mouse gut. Dev Biol 270 (2004) 455-473
35. Stewart A.L., Anderson R.B., and Young H.M. Characterization of lacZ-expressing cells in the gut of embryonic and adult DbetaH-nlacZ mice. J Comp Neurol 464 (2003) 208-219
36. Adcock K.H., Brown D.J., Shearer M.C., Shewan D., Schachner M., Smith G.M., Geller H.M., and Fawcett J.W. Axon behaviour at Schwann cell-astrocyte boundaries. manipulation of axon signalling pathways and the neural adhesion molecule L1 can enable axons to cross. Eur J Neurosci 20 (2004) 1425-1435
37. Anderson R.B., Cooper H.M., Jackson S.C., Seaman C., and Key B. DCC plays a role in navigation of forebrain axons across the ventral midbrain commissure in embryonic xenopus. Dev Biol 217 (2000) 244-253
38. Vutskits L., Djebbara-Hannas Z., Zhang H., Paccaud J.P., Durbec P., Rougon G., Muller D., and Kiss J.Z. PSA-NCAM modulates BDNF-dependent survival and differentiation of cortical neurons. Eur J Neurosci 13 (2001) 1391-1402
39. Conner P.J., Focke P.J., Noden D.M., and Epstein M.L. 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
40. Beer S., Oleszewski M., Gutwein P., Geiger C., and Altevogt P. Metalloproteinase-mediated release of the ectodomain of L1 adhesion molecule. J Cell Sci 112 (1999) 2667-2675
41. Hattori M., Osterfield M., and Flanagan J.G. Regulated cleavage of a contact-mediated axon repellent. Science 289 (2000) 1360-1365
42. Kajita M., Itoh Y., Chiba T., Mori H., Okada A., Kinoh H., and Seiki M. Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration. J Cell Biol 153 (2001) 893-904
43. Noe V., Fingleton B., Jacobs K., Crawford H.C., Vermeulen S., Steelant W., Bruyneel E., Matrisian L.M., and Mareel M. Release of an invasion promoter E-cadherin fragment by matrilysin and stromelysin-1. J Cell Sci 114 (2001) 111-118
44. Kalus I., Schnegelsberg B., Seidah N.G., Kleene R., and Schachner M. The proprotein convertase PC5A and a metalloprotease are involved in the proteolytic processing of the neural adhesion molecule L1. J Biol Chem 278 (2003) 10381-10388
45. Chalazonitis A., Rothman T.P., Chen J., and Gershon M.D. Age-dependent differences in the effects of GDNF and NT-3 on the development of neurons and glia from neural crest-derived precursors immunoselected from the fetal rat gut. expression of GFRalpha-1 in vitro and in vivo. Dev Biol 204 (1998) 385-406
46. Young H.M., Hearn C.J., Ciampoli D., Southwell B.R., Brunet J.F., and Newgreen D.F. A single rostrocaudal colonization of the rodent intestine by enteric neuron precursors is revealed by the expression of Phox2b, Ret, and p75 and by explants grown under the kidney capsule or in organ culture. Dev Biol 202 (1998) 67-84
47. Chazal G., Durbec P., Jankovski A., Rougon G., and Cremer H. Consequences of neural cell adhesion molecule deficiency on cell migration in the rostral migratory stream of the mouse. J Neurosci 20 (2000) 1446-1457
48. Teddy J.M., and Kulesa P.M. In vivo evidence for short- and long-range cell communication in cranial neural crest cells. Development 131 (2004) 6141-6151
49. Chalazonitis A., Tennyson V.M., Kibbey M.C., Rothman T.P., and Gershon M.D. The alpha1 subunit of laminin-1 promotes the development of neurons by interacting with LBP110 expressed by neural crest-derived cells immunoselected from the fetal mouse gut. J Neurobiol 33 (1997) 118-138
50. Ikawa H., Kawano H., Takeda Y., Masuyama H., Watanabe K., Endo M., Yokoyama J., Kitajima M., Uyemura K., and Kawamura K. Impaired expression of neural cell adhesion molecule L1 in the extrinsic nerve fibers in Hirschsprung's disease. J Pediatr Surg 32 (1997) 542-545
51. Yoneda A., Wang Y., O'Briain D.S., and Puri P. Cell-adhesion molecules and fibroblast growth factor signalling in Hirschsprung's disease. Pediatr Surg Int 17 (2001) 299-303
52. Parisi M.A., Baldessari A.E., Iida M.H., Clarke C.M., Doggett B., Shirasawa S., and Kapur R.P. Genetic background modifies intestinal pseudo-obstruction and the expression of a reporter gene in Hox11L1-/- mice. Gastroenterology 125 (2003) 1428-1440
53. Burnett A.L., Nelson R.J., Calvin D.C., Liu J.X., Demas G.E., Klein S.L., Kriegsfeld L.J., Dawson V.L., Dawson T.M., and Snyder S.H. Nitric oxide-dependent penile erection in mice lacking neuronal nitric oxide synthase. Mol Med 2 (1996) 288-296
54. Casini G., Dal Monte M., Petrucci C., Gambellini G., Grouselle D., Allen J.P., Kreienkamp H.J., Richter D., Epelbaum J., and Bagnoli P. Altered morphology of rod bipolar cell axonal terminals in the retinas of mice carrying genetic deletion of somatostatin subtype receptor 1 or 2. Eur J Neurosci 19 (2004) 43-54
55. Coventry S., Yost C., Palmiter R.D., and Kapur R.P. Migration of ganglion cell precursors in the ileoceca of normal and lethal spotted embryos, a murine model for Hirschsprung disease. Lab Invest 71 (1994) 82-93
56. Kapur R.P., Sweetser D.A., Doggett B., Siebert J.R., and Palmiter R.D. Intercellular signals downstream of endothelin receptor-B mediate colonization of the large intestine by enteric neuroblasts. Development 121 (1995) 3787-3795
57. Kapur R.P., Livingston R., Doggett B., Sweetser D.A., Siebert J.R., and Palmiter R.D. Abnormal microenvironmental signals underlie intestinal aganglionosis in dominant megacolon mutant mice. Dev Biol 174 (1996) 360-369
58. Auricchio A., Griseri P., Carpentieri M.L., Betsos N., Staiano A., Tozzi A., Priolo M., Thompson H., Bocciardi R., Romeo G., Ballabio A., and Ceccherini I. Double heterozygosity for a RET substitution interfering with splicing and an EDNRB missense mutation in Hirschsprung disease. Am J Hum Genet 64 (1999) 1216-1221
59. Barlow A., de Graaff E., and Pachnis V. 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
60. Zhu L., Lee H.O., Jordan C.S., Cantrell V.A., Southard-Smith E.M., and Shin M.K. Spatiotemporal regulation of endothelin receptor-B by SOX10 in neural crest-derived enteric neuron precursors. Nat Genet 36 (2004) 732-737
61. Anderson R.B., Newgreen D.F., and Young H.M. Neural crest and development of the enteric nervous system. In: Saint-Jeannet J.P. (Ed). Neural crest induction and differentiation (2006), Landes Bioscience, Georgetown, TX
62. Pattyn A., Morin X., Cremer H., Goridis C., and Brunet J.F. Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 124 (1997) 4065-4075