Neural crest cell origin and signals for intrinsic neurogenesis in the mammalian respiratory tract

American Journal of Respiratory Cell and Molecular Biology

Volumn 44, Issue 3, 2011, Pages 293-301

  Langsdorf, Aliete ^a   Radzikinas, Kelsi ^a   Kroten, Amanda ^b   Jain, Sanjay ^b   Ai, Xingbin ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Extrinsic innervation; GDNF; Intrinsic neuron; Neural crest cell; Respiratory tract

Indexed keywords

PROTEIN RET;

ANIMAL TISSUE; ARTICLE; BRONCHUS; CELL LINEAGE; EMBRYO; INNERVATION; MAMMAL; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGAN CULTURE; RESPIRATORY SYSTEM; TRACHEA;

ALLELES; ANIMALS; DNA, COMPLEMENTARY; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; IMMUNOHISTOCHEMISTRY; MICE; MICE, TRANSGENIC; NEURAL CREST; NEUROGENESIS; NEURONS; NEURTURIN; PREGNANCY; PROTO-ONCOGENE PROTEINS C-RET; RESPIRATORY SYSTEM;

MAMMALIA;

EID: 79952210266     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2009-0462OC     Document Type: Article

References (47)

1. Loosli CG, Hung KS. Development of pulmonary innervation. In: Lenfant C, Hodson WA, editors. Development of the lung. Volume 6. New York: Dekker; 1977. pp. 269-306.
2. Sparrow MP, Weichselbaum M, McCray PB. Development of the innervation and airway smooth muscle in human fetal lung. Am J Respir Cell Mol Biol 1999;20:550-560. (Pubitemid 129495643)
3. Weichselbaum M, Sparrow MP. A confocal microscopic study of the formation of ganglia in the airways of fetal pig lung. Am J Respir Cell Mol Biol 1999;21:607-620. (Pubitemid 129586596)
4. Tollet J, Everett AW, Sparrow MP. Spatial and temporal distribution of nerves, ganglia, and smooth muscle during the early pseudoglandular stage of fetal mouse lung development. Dev Dyn 2001; 221:48-60.
5. Vaccaro R, Salvi EP, Renda T. Early development of chick embryo respiratory nervous system: an immunohistochemical study. Anat Embryol (Berl) 2006;211:345-354. (Pubitemid 44484312)
6. Burns AJ, Thapar N, Barlow AJ. Development of neural crest-derived intrinsic innervation of the human lung. Am J Respir Cell Mol Biol 2008;38:269-275. (Pubitemid 351567695)
7. Belvisi MG. Overview of the innervation of the lung. Curr Opin Pharmacol 2002;2:211-215. (Pubitemid 34594357)
8. Carr MJ, Undem BJ. Bronchopulmonary afferent nerves. Respirology 2003;8:291-301. (Pubitemid 37163114)
9. Widdicombe J. Lung afferent activity: implications for respiratory sensation. Respir Physiol Neurobiol 2009;167:2-8.
10. Cardoso WV, Lü J. Regulation of early lung morphogenesis: questions, facts and controversies. Development 2006;133:1611-1624. (Pubitemid 43810969)
11. Natarajan D, Marcos-Gutierrez C, Pachnis V, de Graaff E. Requirement of signalling by receptor tyrosine kinase RET for the directed migration of enteric nervous system progenitor cells during mammalian embryogenesis. Development 2002;129:5151-5160. (Pubitemid 35460679)
12. Tollet J, Everett AW, Sparrow MP. Migration of neural crest cells into and within the developing lung. Int J Dev Neurosci 2002;19:707.
13. Dey R, Hung KS. Development of innervation in the lung. In: McDonald J, editor. Lung growth and development. Volume 100. New York: Dekker; 1997. pp. 244-265.
14. Yntema CL, Hammond WS. The origin of intrinsic ganglia of trunk viscera from vagal neural crest in the chick embryo. J Comp Neurol 1954;101:515-541.
15. Le Douarin NM, Teillet MA. The migration of neural crest cells to the wall of the digestive tract in avian embryo. J Embryol Exp Morphol 1973;30:31-48.
16. Burns AJ, Le Douarin NM. 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. (Pubitemid 28528940)
17. Burns AJ, Delalande J. Neural crest cell origin for intrinsic ganglia of the developing chicken lung. Dev Biol 2005;277:63-79. (Pubitemid 39574254)
18. Baker CV, Bronner-Fraser M. Vertebrate cranial placodes I. Embryonic induction. Dev Biol 2001;232:1-61.
19. Moore MW, Klein RD, Fariñas I, Sauer H, Armanini M, Phillips H, Reichardt LF, Ryan AM, Carver-Moore K, Rosenthal A. Renal and neuronal abnormalities in mice lacking GDNF. Nature 1996;382:76-79. (Pubitemid 26243361)
20. Pichel JG, Shen L, Sheng HZ, Granholm AC, Drago J, Grinberg A, Lee EJ, Huang SP, Saarma M, Hoffer BJ, et al. Defects in enteric innervation and kidney development in mice lacking GDNF. Nature 1996;382:73-76.
21. Sanchez MP, Silos-Santiago I, Frisen J, He B, Lira SA, Barbacid M. Renal agenesis and the absence of enteric neurons in mice lacking GDNF. Nature 1996;382:70-73. (Pubitemid 26243359)
22. Yan H, Bergner AJ, Enomoto H, Milbrandt J, Newgreen DF, Young HM. Neural cells in the esophagus respond to glial cell line-derived neurotrophic factor and neurturin, and are RET-dependent. Dev Biol 2004;272:118-133. (Pubitemid 38887289)
23. Baloh RH, Enomoto H, Johnson EM Jr, Milbrandt J. The GDNF family ligands and receptors - implications for neural development. Curr Opin Neurobiol 2000;10:103-110. (Pubitemid 30102862)
24. Enomoto H. Regulation of neural development by glial cell line-derived neurotrophic factor family ligands. Anat Sci Int 2005;80:42-52. (Pubitemid 40425966)
25. Tollet J, Everett AW, Sparrow MP. Development of neural tissue and airway smooth muscle in fetal mouse lung explants. A role for glialderived neurotrophic factor in lung innervation. Am J Respir Cell Mol Biol 2002;26:420-429. (Pubitemid 34253926)
26. Danielian PS, Echelard Y, Vassileva G, McMahon AP. A 5.5-kb enhancer is both necessary and sufficient for regulation of Wnt-1 transcription in vivo. Dev Biol 1998;192:300-309. (Pubitemid 28066935)
27. Heuckeroth RO, Lampe PA, Johnson EM, Milbrandt J. Neurturin and GDNF promote proliferation and survival of enteric neuron and glial progenitors in vitro. Dev Biol 1998;200:116-129. (Pubitemid 28374697)
28. Jain S, Golden JP, Wozniak D, Pehek E, Johnson EM Jr, Milbrandt J. RET signaling is dispensable for maintenance of midbrain dopaminergic neurons in adult mice. J Neurosci 2006;26:11230-11238. (Pubitemid 44772210)
29. Park WY, Miranda B, Lebeche D, Hashimoto G, Cardoso WV. FGF-10 is a chemotactic factor for distal epithelial buds during lung development. Dev Biol 1998;201:125-134. (Pubitemid 28447208)
30. Ai X, Kitazawa T, Do AT, Kusche-Gullberg M, Labosky PA, Emerson CP Jr. Sulf1 and Sulf2 regulate heparan sulfate-dependent GDNF signaling for esophageal innervation. Development 2007;134:3327-3338. (Pubitemid 350018433)
31. Golden JP, DeMaro JA, Osborne PA, Milbrandt J, Johnson EM Jr. Expression of neurturin, GDNF, and GDNF family-receptor mRNA in the developing and mature mouse. Exp Neurol 1999;158:504-528.
32. Shepherd IT, Raper J. Collapsin-1/semaphorin D is a repellent for chick ganglion of Remak axons. Dev Biol 1999;212:42-53. (Pubitemid 29368335)
33. Young HM, Bergner AJ, Anderson RB, Enomoto H, Milbrandt J, Newgreen DF, Whitington PM. Dynamics of neural crest-derived cell migration in the embryonic mouse gut. Dev Biol 2004;270:455-473. (Pubitemid 38748565)
34. Sparrow MP, Lamb JP. Ontogeny of airway smooth muscle: structure, innervation, myogenesis and function in the fetal lung. Respir Physiol Neurobiol 2003;137:361-372. (Pubitemid 37153294)
35. Adriaensen D, Timmermans JP, Brouns I, Berthoud HR, Neuhuber WL, Scheuermann DW. Pulmonary intraepithelial vagal nodose afferent nerve terminals are confined to neuroepithelial bodies: an anterograde tracing and confocal microscopy study in adult rats. Cell Tissue Res 1998;293:395-405. (Pubitemid 28427322)
36. Pan J, Yeger H, Cutz E. Innervation of pulmonary neuroendocrine cells and neuroepithelial bodies in developing rabbit lung. J Histochem Cytochem 2004;52:379-389. (Pubitemid 38229103)
37. Brouns I, Oztay F, Pintelon I, Proost ID, Lembrechts R, Timmermans JP, Adriaensen D. Neurochemical pattern of the complex innervations of neuroepithelial bodies in mouse lungs. Histochem Cell Biol 2009;131:55-74.
38. Gianino S, Grider JR, Cresswell J, Enomoto H, Heuckeroth RO. GDNF availability determines enteric neuron number by controlling precursor proliferation. Development 2003;130:2187-2198. (Pubitemid 36656714)
39. Leitner ML, Wang LH, Osborne PA, Golden JP, Milbrandt J, Johnson EM Jr. Expression and function of GDNF family ligands and receptors in the carotid body. Exp Neurol 2005;191:S68-S79. (Pubitemid 40075412)
40. Paratcha G, Ledda F, Ibáñez CF. The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell 2003;113:867-879. (Pubitemid 36792031)
41. KagoshimaM, Ito T. Diverse gene expression and function of semaphorins in developing lung: positive and negative regulatory roles of semaphorins in lung branching morphogenesis. Genes Cells 2001;6:559-571.
42. Fu M, Lui VC, Sham MH, Pachnis V, Tam PK. Sonic Hedgehog regulates the proliferation, differentiation, and migration of enteric neural crest cells in gut. J Cell Biol 2004;166:673-684. (Pubitemid 39181005)
43. Young HM, Hearn CJ, Farlie PG, Canty AJ, Thomas PQ, Newgreen DF. GDNF is a chemoattractant for enteric neural cells. Dev Biol 2001;229:503-516. (Pubitemid 32108709)
44. Hoyle GW, Graham RM, Finkelstein JB, Nguyen KP, Gozal D, Friedman M. Hyperinnervation of the airways in transgenic mice overexpressing nerve growth factor. Am J Respir Cell Mol Biol 1998; 18:149-157. (Pubitemid 128355188)
45. García-Suárez O, Pérez-Pinera P, Laurà R, Germana A, Esteban I, Cabo R, Silos-Santiago I, Cobo JL, Vega JA. TrkB is necessary for the normal development of the lung. Respir Physiol Neurobiol 2009;167:281-291.
46. Erickson JT, Conover JC, Borday V, Champagnat J, Barbacid M, Yancopoulos G, Katz DM. Mice lacking brain-derived neurotrophic factor exhibit visceral sensory neuron losses distinct from mice lacking NT4 and display a severe developmental deficit in control of breathing. J Neurosci 1996;16:5361-5371. (Pubitemid 26277865)
47. Proost ID, Pintelon I, Wilkinson WJ, Goethals S, Brouns I, Nassauw LV, Riccardi D, Timmermans JP, Kemp PJ, Adriaensen D. Purinergic signaling in the pulmonary neuroepithelial body microenvironment unraveled by live cell imaging. FASEB J 2009;23:1153-1160.