Expression of Ret-, p75(NTR)-, phox2a-, phox2b-, and tyrosine hydroxylase-immunoreactivity by undifferentiated neural crest-derived cells and different classes of enteric neurons in the embryonic mouse gut

Developmental Dynamics

Volumn 216, Issue 2, 1999, Pages 137-152

  Young, H M ^a   Ciampoli, D ^a   Hsuan, J ^a   Canty, A J ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

CGRP; Mouse intestine; Nitric oxide synthase

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; NITRIC OXIDE SYNTHASE; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL SUBPOPULATION; EMBRYO DEVELOPMENT; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTESTINE INNERVATION; MOUSE; NEURAL CREST; NONHUMAN; PRIORITY JOURNAL; PROGENY; RECEPTOR AFFINITY; RECEPTOR BINDING; RECEPTOR DOWN REGULATION;

ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; CELL DIFFERENTIATION; DIGESTIVE SYSTEM; DOWN-REGULATION; DROSOPHILA PROTEINS; ENTERIC NERVOUS SYSTEM; ESOPHAGUS; HOMEODOMAIN PROTEINS; INTESTINE, LARGE; INTESTINE, SMALL; MICE; MICE, INBRED BALB C; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; NEURAL CREST; NEURONS; NITRIC OXIDE SYNTHASE; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-RET; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTOR, NERVE GROWTH FACTOR; TRANSCRIPTION FACTORS; TYROSINE 3-MONOOXYGENASE;

ANIMALIA;

EID: 0032822663     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0177(199910)216:2<137::AID-DVDY5>3.0.CO;2-6     Document Type: Article

References (54)

1. Baetge G, Gershon MD. 1989. Transient catecholaminergic (TC) cells in the vagus nerves and bowel of fetal mice: relationship to the development of enteric neurons. Dev Biol 132:189-211.
2. Baetge G, Pintar JE, Gershon MD. 1990. Transiently catecholaminergic (TC) cells in the bowel of the fetal rat: precursors of noncatecholaminergic enteric neurons. Dev Biol 141:353-380.
3. Blaugrund E, Pham TD, Tennyson VM, Lo L, Sommer L, Anderson DJ, Gershon MD. 1996. Distinct subpopulations of enteric neuronal progenitors defined by time of development, sympathoadrenal lineage markers and Mash-1-dependence. Development 122:309-320.
4. Branchek TA, Gershon MD. 1989. Time course of expression of neuropeptide Y, calcitonin gene-related peptide, and NADPH diaphorase activity in neurons of the developing murine bowel and the appearance of 5-hydroxytryptamine in mucosal enterochromaffin cells. J Comp Neurol 285:262-273.
5. Burns AJ, Le Douarin NM. 1998. The sacral neural crest contributes neurons and glia to the post-umbilical gut: spatiotemporal analysis of the development of the enteric nervous system. Development 125:4335-4347.
6. Cacalano G, Farinas I, Wang LC, Hagler K, Forgie A, Moore M, Armanini M, Phillips H, Ryan AM, Reichardt LF, Hynes M, Davies A, Rosenthal A. 1998. GFRalpha1 is an essential receptor component for GDNF in the developing nervous system and kidney. Neuron 21:53-62.
7. Chalazonitis A, Rothman TP, Chen J, Lamballe F, Barbacid M, Gershon MD. 1994. Neurotrophin-3 induces neural crest-derived cells from fetal rat gut to develop in vitro as neurons or glia. J Neurosci 14:6571-6584.
8. Chalazonitis A, Tennyson VM, Kibbey MC, Rothman TP, Gershon MD. 1997. 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 33:118-138.
9. Chalazonitis A, Rothman TP, Chen J, Gershon MD. 1998. 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 204:385-406.
10. Cochard P, Goldstein M, Black IB. 1978. Ontogenetic appearance and disappearance of tyrosine hydroxylase and catecholamines. Proc Natl Acad Sci USA 75:2986-2990.
11. Durbec PL, Larsson-Blomberg LB, Schuchardt A, Costantini F, Pachnis V. 1996. Common origin and developmental dependence on c-ret of subsets of enteric and sympathetic neuroblasts. Development 122:349-358.
12. Enomoto H, Araki T, Jackman A, Heuckeroth RO, Snider WD, Johnson EM, Jr., Milbrandt J. 1998. GFR alpha1-deficient mice have deficits in the enteric nervous system and kidneys. Neuron 21:317-324.
13. Esteban I, Levanti B, Garcia-Suarez O, Germana G, Ciriaco E, Naves FJ, Vega JA. 1998. A neuronal subpopulation in the mammalian enteric nervous system expresses TrkA and TrkC neurotrophin receptor-like proteins. Anat Rec 251:360-370.
14. Fiorica-Howells E, Maroteaux L, Gershon MD. 1998. 5-HT2B receptors are expressed by neuronal precursors in the enteric nervous system of fetal mice and promote neuronal differentiation. Ann N Y Acad Sci 861:246.
15. Gariepy CE, Williams SC, Richardson JA, Hammer RE, Yanagisawa M. 1998. Transgenic expression of the endothelin-B receptor prevents congenital intestinal aganglionosis in a rat model of Hirschsprung disease. J Clin Invest 102:1092-1101.
16. Gershon MD. 1997. Genes and lineages in the formation of the enteric nervous system. Curr Opin Neurobiol 7:101-109.
17. Gershon MD, Rothman TP, Joh TH, Teitelman GN. 1984. Transient and differential expression of aspects of the catecholaminergic phenotype during development of the fetal bowel of rats and mice. J Neurosci 4:2269-2280.
18. Gershon MD, Chalazonitis A, Rothman TP. 1992. From neural crest to bowel: development of the enteric nervous system. J Neurobiol 24:199-214.
19. Goridis C, Brunet JF. 1999. Transcriptional control of neurotransmitter phenotype. Curr Opin Neurobiol 9:47-53.
20. Hearn CJ, Murphy M, 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.
21. Herbarth B, Pingault V, Bondurand N, Kuhlbrodt K, Hermans-Borgmeyer I, Puliti A, Lemort N, Goossens M, Wegner M. 1998. Mutation of the Sry-related Sox10 gene in Dominant megacolon, a mouse model for human Hirschsprung disease. Proc Natl Acad Sci USA 95:5161-5165.
22. Hirsch MR, Tiveron MC, Guillemot F, Brunet JF, Goridis C. 1998. Control of noradrenergic differentiation and Phox2a expression by MASH1 in the central and peripheral nervous system. Development 125:599-608.
23. Jonakait GM, Wolf J, Cochard P, Goldstein M, Black IB. 1979. Selective loss of noradrenergic phenotypic characters in neuroblasts of the rat embryo. Proc Natl Acad Sci USA 76:4683-4686.
24. Kapur RP, Yost C, Palmiter RD. 1992. A transgenic model for studying development of the enteric nervous system in normal and aganglionic mice. Development 116:167-175.
25. Lo L, Anderson DJ. 1995. Postmigratory neural crest cells expressing c-RET display restricted developmental and proliferative capacities. Neuron 15:527-539.
26. Lo L, Guillemot F, Joyner AL, Anderson DJ. 1994. MASH-1: a marker and a mutation for mammalian neural crest development. Perspect Dev Neurobiol 2:191-201.
27. Lo LC, Johnson JE, Wuenschell CW, Saito T, Anderson DJ. 1991. Mammalian achaete-scute homolog 1 is transiently expressed by spatially restricted subsets of early neuroepithelial and neural crest cells. Genes Dev 5:1524-1537.
28. Lo L, Sommer L, Anderson DJ. 1997. MASH1 maintains competence for BMP2-induced neuronal differentiation in post-migratory neural crest cells. Curr Biol 7:440-450.
29. Lo L, Tiveron MC, Anderson DJ. 1998. MASH1 activates expression of the paired homeodomain transcription factor Phox2a, and couples pan-neuronal and subtype-specific components of autonomic neuronal identity. Development 125:609-620.
30. Moore MW, Klein RD, Farinas I, Sauer H, Armanini M, Phillips H, Reichardt LF, Ryan AM, Carver-Moore K, Rosenthal A. 1996. Renal and neuronal abnormalities in mice lacking GDNF. Nature 382: 76-79.
31. Morin X, Cremer H, Hirsch MR, Kapur RP, Goridis C, Brunet JF. 1997. Defects in sensory and autonomic ganglia and absence of locus coeruleus in mice deficient for the homeobox gene Phox2a. Neuron 18:411-423
32. Natarajan D, Grigoriou M, Marcos-Gutierrez CV, Atkins C, Pachnis V. 1999. Multipotential progenitors of the mammalian enteric nervous system capable of colonising aganglionic bowel in organ culture. Development 126:157-168.
33. Pachnis V, Mankoo B, Costantini F. 1993. Expression of the c-ret proto-oncogene during mouse embryogenesis. Development 119: 1005-1017.
34. Pachnis V, Durbec P, Taraviras S, Grigoriou M, Natarajan D. III. 1998. Role Of the RET signal transduction pathway in development of the mammalian enteric nervous system. Am J Physiol 275:G183-186.
35. Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF. 1997. Expression and interactions of the two closely related homeobox genes Phox2a and Phox2b during neurogenesis. Development 124:4065-4075.
36. Pattyn A, Morin X, Cremer H, Goridis C, Brunet JF. 1999. The homeobox gene Phox2b is essential for the development of autonomic neural crest derivatives. Nature 399:366-370.
37. Pichel JG, Shen L, Sheng HZ, Granholm AC, Drago J, Grinberg A, Lee EJ, Huang SP, Saarma M, Hoffer BJ, Sariola H, Westphal H. 1996. Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 382:73-76.
38. Rothman TP, Gershon MD. 1982. Phenotypic expression in the developing murine enteric nervous system. J Neurosci 2:381-393.
39. Sanchez MP, Silos-Santiago I, Frisen J, He B, Lira SA, Barbacid M. 1996. Renal agenesis and the absence of enteric neurons in mice lacking GDNF. Nature 382:70-73.
40. Sang Q, Young HM. 1996. Chemical coding of neurons in the myenteric plexus and external muscle of the small and large intestine of the mouse. Cell Tissue Res 284:39-53.
41. Sang Q, Young HM. 1997. Development of nicotinic receptor clusters and innervation accompanying the change in muscle phenotype in the mouse esophagus. J Comp Neurol 386:119-136.
42. Schuchardt A, D'Agati V, Larsson-Blomberg L, Costantini F, Pachnis V. 1994. Defects in the kidney and enteric nervous system of mice lacking the tyrosine kinase receptor Ret [see comments]. Nature 367:380-383.
43. Southard-Smith EM, Kos L, Pavan WJ. 1998. Sox10 mutation disrupts neural crest development in Dom Hirschsprung mouse model. Nat Genet 18:60-64.
44. Taraviras S, Pachnis V. 1999. Development of the enteric nervous system. Curr Opin Gen Dev 9:321-327.
45. Taraviras S, Marcos-Gutierrez CV, Durbec P, Jani H, Grigoriou M, Sukumaran M, Wang LC, Hynes M, Raisman G, Pachnis V. 1999. Signalling by the RET receptor tyrosine kinase and its role in the development of the mammalian enteric nervous system. Development 126:2785-2797.
46. Teitelman G, Job TH, Reis DJ. 1978. Transient expression of a noradrenergic phenotype in cells of the rat embryonic gut. Brain Res 158:229-234.
47. Teitelman G, Gershon MD, Rothman TP, Job TH, Reis DJ. 1981. Proliferation and distribution of cells that transiently express a catecholamine phenotype during development in mice and rats. Dev Biol 86:348-355.
48. Thieler K. The house mouse: atlas of embryonic development. New York:Springer-Verlag, 1989.
49. Tiveron MC, Hirsch MR, Brunet JF. 1996. The expression pattern of the transcription factor Phox2 delineates synaptic pathways of the autonomic nervous system. J Neurosci 16:7649-7660.
50. Tsuzuki T, Takahashi M, Asai N, Iwashita T, Matsuyama M, Asai J. 1995. Spatial and temporal expression of the ret proto-oncogene product in embryonic, infant, and adult rat tissues. Oncogene 10:191-198.
51. van Doorninck JH, van der Wees J, Karis A, Goedknegt E, Engel JD, Coesmans M, Rutteman M, Grosveld F, De Zeeuw CI. 1999. GATA-3 is involved in the development of serotonergic neurons in the caudal raphe nuclei. J Neurosci 19:RC12.
52. Watanabe Y, Harada T, Ito T, Ishiguro Y, Ando H, Seo T, Kobayashi S, Takahashi M, Nimura Y. 1997. ret Proto-oncogene product is a useful marker of lineage determination in the development of the enteric nervous system in rats. J Pediatr Surg 32:28-33.
53. Wu JJ, Chen JX, Rothman TP, Gershon MD. 1999. Inhibition of in vitro enteric neuronal development by endothelin-3: mediation by endothelin B receptors. Development 126:1161-1173.
54. Young HM, Hearn CJ, Ciampoli D, Southwell BR, Brunet JF, Newgreen DF. 1998. 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 202:67-84.