The sacral neural crest contributes neurons and glia to the post-umbilical gut: Spatiotemporal analysis of the development of the enteric nervous system

Development

Volumn 125, Issue 21, 1998, Pages 4335-4347

  Burns, Alan J ^a   Le Douarin, Nicole M ^a  

^a CNRS   (France)

Author keywords

Avian; Enteric; Glia; Gut; Neural crest; Neuron

Indexed keywords

ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; COLON; EMBRYO; EMBRYO DEVELOPMENT; GANGLION; GLIA; INTESTINE INNERVATION; INTESTINE MUSCLE; NERVE CELL DIFFERENTIATION; NERVE PLEXUS; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST; NONHUMAN; PRIORITY JOURNAL; QUAIL; RECTUM; SACRUM; SEROSA; UMBILICUS; VAGUS NERVE;

ANIMALS; CARBOCYANINES; CELL MOVEMENT; CHICK EMBRYO; CHIMERA; COTURNIX; ENTERIC NERVOUS SYSTEM; FLUORESCENT DYES; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOHISTOCHEMISTRY; INTESTINES; MICROSCOPY, FLUORESCENCE; NADPH DEHYDROGENASE; NEURAL CREST; NEUROFILAMENT PROTEINS; NEUROGLIA; NEURONS; PHENOTYPE; SACRUM; VAGUS NERVE;

ANIMALIA; AVES; PHASIANIDAE; UMBILICUS;

EID: 0031794665     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (55)

1. Allan I. J. and Newgreen D. F. (1980). The origin and differentiation of enteric neurons of the intestine of the fow1 embryo. Am. J. Anat. 157, 137-154.
2. Altermatt H. J., Rodriguez M., Scheithauer B. W. and Lennon V. A. (1991). Paraneoplastic anti-purkinje and type I anti-neuronal nuclear antibodies bind selectively to central, peripheral and autonomic nervous system cells. Lab. Invest. 65, 412-420.
3. Arai H., Nakao K., Takaya K., Hosoda K., Ogawa Y., Nakanishi S. and Imura H. (1993). The human endothelin-B receptor gene. Structural organization and chromosomal assignment. J. Biol. Chem. 268, 3463-3470.
4. Baynash A. G., Hosoda K., Giaid A., Richardson J. A., Emoto N., Hammer R. E. and Yanagisawa M. (1994). Interaction of endothelin-3 with endothelin-B receptor is essential for development of epidermal melanocytes and enteric neurons. Cell 79, 1277-1285.
5. Catala M., Teillet M. A. and Le Douarin N. M. (1995). Organization and development of the tail bud analyzed with the quail-chick chimaera system. Mech. Dev. 51, 51-65.
6. Ciment G. and Weston J. A. (1983). Enteric neurogenesis by neural crest-derived branchial arch mesenchymal cells. Nature 305, 424-427.
7. Cochard P. and Le Douarin N. M. (1982). Development of the intrinsic innervation of the gut. Scand. J. Gastroenterol. Suppl. 71, 1-14.
8. Edery P., Attié T., Amiel J., Pelet A., Eng C., Hofstra R. M. W., Martelli H., Bidaud C., Munnich A. and Lyonnet S. (1996). Mutation of the endothelin-3 gene in the Waardenburg-Hirschsprung disease (Shah-Waardenburg syndrome). Nature Genet. 12, 442-444.
9. Epstein M. L., Mikawa T., Brown A. M. C. and McFarlin D. R. (1994). Mapping the origin of the avian enteric nervous system with a retroviral marker. Dev. Dyn. 201, 236-244.
10. Epstein M. L., Poulsen K. T. and Thiboldeaux R. (1991). Formation of ganglia in the gut of the chick embryo. J. Comp. Neurol. 307, 189-199.
11. Epstein M. L., Sherman D. and Gershon M. D. (1980). Development of serotonergic neurons in the chick duodenum. Dev. Biol. 77, 22-40.
12. Fairman C. L., Clagett-Dame M., Lennon V. A. and Epstein M. L. (1995). Appearance of neurons in the developing chick gut. Dev. Dyn. 204, 192-201.
13. Gershon M. D. (1997). Genes and lineages in the formation of the enteric nervous system. Curr. Opin. Neurobiol. 7, 101-109.
14. Gershon M. D., Epstein M. L. and Hegstrand L. (1980). Colonization of the chick gut by progenitors of enteric serotonergic neurons: distribution, differentiation and maturation within the gut. Dev. Biol. 77, 41-51.
15. Hamburger V. and Hamilton H. L. (1951). A series of normal stages in the development of chick embryo. J. Morphol. 88, 49-92.
16. Hearn C. J., Murphy M. and Newgreen D. (1998). GDNF and ET-3 differentially modulate the numbers of avian enteric neural crest cells and enteric neurons in vitro. Dev. Biol. 197, 93-105.
17. Hellmich H. L., Kos L., Cho E. S., Mahon K. A., Zimmer A. (1996). Embryonic expression of glial cell-line derived neurotrophic factor (GDNF) suggests multiple developmental roles in neural differentiation and epithelial-mesenchymal interactions. Mech. Dev. 54, 95-105.
18. Hosoda K., Hammer R. E., Richardson J. A., Greenstein-Baynash A., Cheung J. C., Giaid A. and Yanagisawa M. (1994). Targeted and natural (piebald-lethal) mutations of endothelin-B receptor gene produce megacolon associated with spotted coat color in mice. Cell 79, 1267-1276.
19. Lahav R., Ziller C., Dupin E. and Le Douarin N. M. (1996). Endothelin 3 promotes neural crest cell proliferation and mediates a vast increase in melanocyte number in culture. Proc. Natl. Acad. Sci. USA 93, 3892-3897.
20. Le Douarin N. M. and Dulac C. (1992). Influence of the environment on the development of the enteric nervous system from the neural crest. Advances in the Innervation of the Gastrointestinal Tract (ed. G. E. Holle et al.), pp 3-17. Amsterdam: Elsevier Science Publishers.
21. 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.
22. Le Douarin N. M. and Kalcheim C. (1998). The Neural Crest. Cambridge: Cambridge University Press. (In press).
23. Luider T. M., Peters-Van Der Sanden M. J. H., Molenaar J. C., Tibboel D., Van Derkamp A. W. M. and Meijers C. (1992). Characterization of HNK-1 antigens during the formation of the avian enteric nervous system. Development 115, 561-572.
24. Matini P., Mayer B. and Faussone-Pellegrini M. S. (1997). Neurochemical differentiation of rat enteric neurons during pre- and postnatal life. Cell Tiss. Res. 288, 11-23.
25. Meijers J. H., Tibboel D., Van Der Kamp A. W., Van Haperen-Heuts I. C. and Molenaar J. C. (1989). A model for aganglionosis in the chicken embryo. J. Pediatr. Surg. 24, 557-561.
26. Nataf V., Lecoin L., Eichmann A. and Le Douarin N. M. (1996). Endothelin-B receptor is expressed by neural crest cells in the avian embryo. Proc. Natl. Acad. Sci. USA 93, 9645-9650.
27. Nataf, V., Amemiya, A., Yanagisawa, M. and Le Douarin, N. M. (1998). The expression pattern of endothelin 3 in the avian embryo. Mech. Dev. 73, 217-220.
28. Newgreen D. F. and Hartley L. (1995). Extracellular matrix and adhesive molecules in the early development of the gut and its innervation in normal and spotting lethal rat embryos. Acta Anat. 154, 243-260.
29. Newgreen D. F., Powell M. E. and Moser B. (1990). Spatiotemporal changes in HNK-1/L2 glycoconjugates on avian embryo somite and neural crest cells. Dev. Biol. 139, 100-120.
30. Noden D, M. (1975). An analysis of migratory behavior of avian cephalic neural crest cells. Dev. Biol. 42, 106-130.
31. Pachnis V., Mankoo B., Costantini F. (1993). Expression of the c-ret protooncogene during mouse embryogenesis. Development 119, 1005-1017.
32. Pardanaud L., Altmann C., Kitos P., Dieterlen-Lièvre F. and Buck C. A. (1987). Vasculogenesis in the early quail blastodisc as studied with a monoclonal antibody recognizing endothelial cells. Development 100, 339-349.
33. Payette R. F., Bennett G. S. and Gershon M. D. (1984). Neurofilament expression in vagal neural crest-derived precursors of enteric neurons. Dev. Biol. 105, 273-287.
34. Payette R. F., Tennyson V. M., Pham T. D., Mawe G. M., Pomeranz H. D., Rothman T. P. and Gershon M. D. (1987). Origin and morphology of nerve fibers in the aganglionic colon of the lethal spotted (ls/ls) mutant mouse. J. Comp. Neurol. 257, 237-252.
35. Peters Van Der Sanden M. J. H., Kirby M. L., Gittenber Gerdegroot A., Tibboel D., Mulder M. P. and Meijers C. (1993). Ablation of various regions within the avian vagal neural crest has differential effects on ganglion formation in the foregut, midgut and hindgut. Dev. Dyn. 196, 183-194.
36. Pham T. D., Gershon M. D. and Rothman T. P. (1991). Time of origin of neurons in the murine enteric nervous system: sequence in relation to phenotype. J. Comp. Neurol. 314, 789-798.
37. Pichel J. G., Shen L. Y., Sheng H. Z., Granholm A. C., Drago J., Grinberg A., Lee E. J., Huang S. P., Saarma M., Hoffer B. J., Sariola H. and Westphal H. (1996). Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 382, 73-76.
38. Pomeranz H. D. and Gershon M. D. (1990). Colonization of the avian hindgut by cells derived from the sacral neural crest. Dev. Biol. 137, 378-394.
39. Pomeranz H. D., Rothman T. P. and Gershon M. D. (1991). Colonization of the post-umbilical bowel by cells derived from the sacral neural crest: direct tracing of cell migration using an intercalating probe and a replication-deficient retrovirus. Development 111, 647-655.
40. Puffenberger E. G., Hosoda K., Washington S. S., Nakao K., Dewit D., Yanagisawa M. and Chakravarti A. (1994). A missense mutation of the endothelin-B receptor gene in multigenic Hirschsprung's disease. Cell 79, 1257-1266.
41. Rong P. M., Ziller C., Pena-Melian A. and Le Douarin N. M. (1987). A monoclonal antibody specific for avian early myogenic cells and differentiated muscle. Dev. Biol. 122, 338-353.
42. Rothman T. P. and Gershon M. D. (1984). Regionally defective colonization of the terminal bowel by the precursors of enteric neurons in lethal spotted mutant mice. Neuroscience 12, 1293-1311.
43. Sanchez M. P., Silos-Santiago I., Frisen J., He B., Lira S. A. and Barbacid M. (1996). Renal agenesis and the absence of enteric neurons in mice lacking GDNF. Nature 382, 70-73.
44. 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.
45. Serbedzija G. N., Burgan S., Fraser S. E. and Bronner-Fraser M. (1991). Vital dye labelling demonstrates a sacral neural crest contribution to the enteric nervous system of chick and mouse embryos. Development 111, 857-866.
46. Smith J., Cochard P. and Le Douarin N. M. (1977). Development of choline acetyltransferase and cholinesterase activities in enteric ganglia derived from presumptive adrenergic and cholinergic levels of the neural crest. Cell Diff. 6, 199-216.
47. Teillet M.-A. (1978). Evolution of the lumbo-sacral neural crest in the avian embryo: origin and differentiation of the ganglionated nerve of Remak studied in interspecific quail-chick chimerae. Roux's Arch. Dev. Biol. 184, 251-268.
48. Tennyson V. M., Gershon M. D., Wade P. R., Crotty D. A. and Wolgemuth D. J. (1998). Fetal development of the enteric nervous system of transgenic mice that overexpress the Hoxa-4 gene. Dev. Dyn. 211, 269-291.
49. Tucker G. C., Aoyama H., Lipinski M., Tursz T. and Thiery J. P. (1984). Identical reactivity of monoclonal antibodies HNK-1 and NC-1: conservation in vertebrates on cells derived from the neural primordium and on some leukocytes. Cell Diff. 14, 223-230.
50. Tucker G. C., Ciment G. and Thiery J. P. (1986). Pathways of avian neural crest cell migration in the developing gut. Dev. Biol. 116, 439-450.
51. Vincent M. and Thiery J. P. (1984). A cell surface marker for neural crest and placodal cells: further evolution in peripheral and central nervous system. Dev. Biol. 103, 468-481.
52. Vincent M., Duband J. L. and Thiery J. P. (1983). A cell surface determinant expressed early on migrating avian neural crest cells. Dev. Brain Res. 9, 235-238.
53. Ward S. M., Xue C., Shuttleworth C. W. R., Bredt D. S., Snyder S. H. and Sanders K. M. (1992). NADPH-diaphorase and nitric oxide synthase colocalisation in enteric neurons of the canine proximal colon. Am. J. Physiol. 263, G277-G284.
54. Yntema C. L. and Hammond W. S. (1954). The origin of intrinsic ganglia of trunk viscera from vagal neural crest in the chick embryo. J. Comp. Neurol. 101, 515-541.
55. Yntema C. L. and Hammond W. S. (1955). Experiments on the origin and development of the sacral autonomic nerves in the chick embryo. J. Exp. Zool. 129, 375-414.