The role of neural activity in the migration and differentiation of enteric neuron precursors

Neurogastroenterology and Motility

Volumn 22, Issue 5, 2010, Pages

  Hao, M M ^a   Moore, R E ^a   Roberts, R R ^a   Nguyen, T ^a   Furness, J B ^a   Anderson, R B ^a   Young, H M ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Differentiation; Enteric nervous system; Migration; Neural activity; Neural crest; Neuronal nitric oxide synthase

Indexed keywords

CALBINDIN; CLOTRIMAZOLE; INTERMEDIATE CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; N(G) NITROARGININE; NEURONAL NITRIC OXIDE SYNTHASE; SNARE PROTEIN; TETANUS TOXIN; TETRODOTOXIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL MIGRATION; CELL SUBPOPULATION; CONTROLLED STUDY; EMBRYO; EXPLANT; FEMALE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTESTINE; INTESTINE INNERVATION; MALE; MOUSE; MOUSE EMBRYO; NERVE CELL DIFFERENTIATION; NERVE CELL INHIBITION; NERVE FIBER; NERVE POTENTIAL; NEURAL CREST CELL; NEURAL STEM CELL; NEUROTRANSMITTER RELEASE; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN ANALYSIS; TISSUE CULTURE;

ACTION POTENTIALS; ANIMALS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CELL DIFFERENTIATION; CELL MOVEMENT; ENTERIC NERVOUS SYSTEM; GASTROINTESTINAL TRACT; IMMUNOHISTOCHEMISTRY; MICE; NEURONS; NITRIC OXIDE SYNTHASE TYPE I; ORGAN CULTURE TECHNIQUES;

EID: 77950678459     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/j.1365-2982.2009.01462.x     Document Type: Article

References (76)

1. Borodinsky LN, Root CM, Cronin JA, Sann SB, Gu X, Spitzer NC. Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 2004 429 : 523 530.
2. Manent JB, Demarque M, Jorquera I et al. A noncanonical release of GABA and glutamate modulates neuronal migration. J Neurosci 2005 25 : 4755 4765.
3. Spitzer NC. Electrical activity in early neuronal development. Nature 2006 444 : 707 712.
4. Weissman TA, Riquelme PA, Ivic L, Flint AC, Kriegstein AR. Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 2004 43 : 647 661.
5. Raven MA, Orton NC, Nassar H et al. Early afferent signaling in the outer plexiform layer regulates development of horizontal cell morphology. J Comp Neurol 2008 506 : 745 758.
6. Zou D-J, Chesler A, Firestein S. How the olfactory bulb got its glomeruli: a just so story? Nat Rev Neurosci 2009 10 : 611 618.
7. Bolteus AJ, Bordey A. GABA release and uptake regulate neuronal precursor migration in the postnatal subventricular zone. J Neurosci 2004 24 : 7623 7631.
8. Bless EP, Walker HJ, Yu KW et al. Live view of gonadotropin-releasing hormone containing neuron migration. Endocrinology 2005 146 : 463 468.
9. Heng JI, Moonen G, Nguyen L. Neurotransmitters regulate cell migration in the telencephalon. Eur J Neurosci 2007 26 : 537 546.
10. Platel J-C, Dave KA, Bordey Al. Control of neuroblast production and migration by converging GABA and glutamate signals in the postnatal forebrain. J Physiol 2008 586 : 3739 3743.
11. Root CM, Velazquez-Ulloa NA, Monsalve GC, Minakova E, Spitzer NC. Embryonically expressed GABA and glutamate drive electrical activity regulating neurotransmitter specification. J Neurosci 2008 28 : 4777 4784.
12. Furness JB. The Enteric Nervous System
13. 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.
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. 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.
16. Baetge G, Gershon MD. Transient catecholaminergic (TC) cells in the vagus nerves and bowel of fetal mice: relationship to the development of enteric neurons. Dev Biol 1989 132 : 189 211.
17. Baetge G, Schneider KA, Gershon MD. Development and persistence of catecholaminergic neurons in cultured explants of fetal murine vagus nerves and bowel. Development 1990 110 : 689 701.
18. Young HM, Ciampoli D, Hsuan J, Canty AJ. 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. Dev Dyn 1999 216 : 137 152.
19. Young HM, Jones BR, McKeown SJ. The projections of early enteric neurons are influenced by the direction of neural crest cell migration. J Neurosci 2002 22 : 6005 6018.
20. Bondurand N, Natarajan D, Barlow A, Thapar N, Pachnis V. Maintenance of mammalian enteric nervous system progenitors by SOX10 and endothelin 3 signalling. Development 2006 133 : 2075 2086.
21. Barlow AJ, Wallace AS, Thapar N, Burns AJ. Critical numbers of neural crest cells are required in the pathways from the neural tube to the foregut to ensure complete enteric nervous system formation. Development 2008 135 : 1681 1691.
22. Stewart AL, Young HM, Popoff M, Anderson RB. Effects of pharmacological inhibition of small GTPases on axon extension and migration of enteric neural crest-derived cells. Dev Biol 2007 307 : 92 104.
23. Young HM. Functional development of the enteric nervous system - from migration to motility. Neurogastroenterol Motil 2008 20 (Suppl. 1 20 31.
24. Vohra BP, Tsuji K, Nagashimada M et al. Differential gene expression and functional analysis implicate novel mechanisms in enteric nervous system precursor migration and neuritogenesis. Dev Biol 2006 298 : 259 271.
25. Chevalier J, Derkinderen P, Gomes P et al. Activity-dependent regulation of tyrosine hydroxylase expression in the enteric nervous system. J Physiol 2008 586 : 1963 1975.
26. Enomoto H, Crawford PA, Gorodinsky A, Heuckeroth RO, Johnson EM Jr., Milbrandt J. RET signaling is essential for migration, axonal growth and axon guidance of developing sympathetic neurons. Development 2001 128 : 3963 3974.
27. Hearn CJ, Young HM, Ciampoli D, Lomax AE, Newgreen D. Catenary cultures of embryonic gastrointestinal tract support organ morphogenesis, motility, neural crest cell migration, and cell differentiation. Dev Dyn 1999 214 : 239 247.
28. Anderson RB, Turner KN, Nikonenko AG, Hemperly J, Schachner M, Young HM. The cell adhesion molecule L1 is required for chain migration of neural crest cells in the developing mouse gut. Gastroenterology 2006 130 : 1221 1232.
29. Roberts RR, Murphy JF, Young HM, Bornstein JC. Development of colonic motility in the neonatal mouse-studies using spatiotemporal maps. Am J Physiol Gastrointest Liver Physiol 2007 292 : G930 8.
30. Neylon CB, Nurgali K, Hunne B et al. Intermediate-conductance calcium-activated potassium channels in enteric neurones of the mouse: pharmacological, molecular and immunochemical evidence for their role in mediating the slow afterhyperpolarization. J Neurochem 2004 90 : 1414 1422.
31. Anderson RB, Bergner AJ, Taniguchi M 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.
32. Kapur RP, Yost C, Palmiter RD. A transgenic model for studying development of the enteric nervous system in normal and aganglionic mice. Development 1992 116 : 167 175.
33. Young HM, Newgreen D. Enteric neural crest-derived cells: origin, identification, migration, and differentiation. Anat Rec 2001 262 : 1 15.
34. Young HM, Bergner AJ, Anderson RB et al. Dynamics of neural crest-derived cell migration in the embryonic mouse gut. Dev Biol 2004 270 : 455 473.
35. Simpson MJ, Landman KA, Hughes BD, Newgreen DF. Cell proliferation drives neural crest cell invasion of the intestine. Dev Biol 2007 302 : 553 568.
36. Baetge G, Pintar JE, Gershon MD. Transiently catecholaminergic (TC) cells in the bowel of the fetal rat: precursors of noncatecholaminergic enteric neurons. Dev Biol 1990 141 : 353 380.
37. Fairman CL, Clagett-Dame M, Lennon VA, Epstein ML. Appearance of neurons in the developing chick gut. Dev Dyn 1995 204 : 192 201.
38. Newgreen DF, Hartley L. Extracellular matrix and adhesive molecules in the early development of the gut and its innervation in normal and spotting lethal rat embryos. Acta Anat (Basel) 1995 154 : 243 260.
39. Conner PJ, Focke PJ, Noden DM, Epstein ML. Appearance of neurons and glia with respect to the wavefront during colonization of the avian gut by neural crest cells. Dev Dyn 2003 226 : 91 8.
40. Sang Q, Young HM. Chemical coding of neurons in the myenteric plexus and external muscle of the small and large intestine of the mouse. Cell Tissue Res 1996 284 : 39 53.
41. Furness JB. Types of neurons in the enteric nervous system. J Auton Nerv Syst 2000 81 : 87 96.
42. Brookes SJ. Classes of enteric nerve cells in the guinea-pig small intestine. Anat Rec 2001 262 : 58 70.
43. Qu ZD, Thacker M, Castelucci P, Bagyanszki M, Epstein ML, Furness JB. Immunohistochemical analysis of neuron types in the mouse small intestine. Cell Tissue Res 2008 334 : 147 161.
44. Hao MM, Young HM. Development of enteric neuron diversity. J Cell Mol Med 2009 13 : 1193 1210.
45. Hao MM, Anderson RB, Kobayashi K, Whitington PM, Young HM. The migratory behavior of immature enteric neurons. Dev Neurobiol 2009 69 : 22 35.
46. Rothman TP, Gershon MD. Phenotypic expression in the developing murine enteric nervous system. J Neurosci 1982 2 : 381 393.
47. Branchek TA, Gershon MD. 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 1989 285 : 262 273.
48. Burns AJ, Pasricha PJ, Young HM. Enteric neural crest-derived cells and neural stem cells: biology and therapeutic potential. Neurogastroenterol Motil 2004 16 (Suppl. 1 3 7.
49. Heanue TA, Pachnis V. Expression profiling the developing mammalian enteric nervous system identifies marker and candidate Hirschsprung disease genes. Proc Natl Acad Sci USA 2006 103 : 6919 6924.
50. Woodward MN, Sidebotham EL, Connell MG et al. Analysis of the effects of endothelin-3 on the development of neural crest cells in the embryonic mouse gut. J Pediatr Surg 2003 38 : 1322 1328.
51. Holmberg A, Olsson C, Holmgren S. The effects of endogenous and exogenous nitric oxide on gut motility in zebrafish Danio rerio embryos and larvae. J Exp Biol 2006 209 : 2472 2479.
52. Olden T, Akhtar T, Beckman SA, Wallace KN. Differentiation of the zebrafish enteric nervous system and intestinal smooth muscle. Genesis 2008 46 : 484 498.
53. Rothman TP, Nilaver G, Gershon MD. Colonization of the developing murine enteric nervous system and subsequent phenotypic expression by the precursors of peptidergic neruons. J Comp Neurol 1984 225 : 13 23.
54. Young HM, Torihashi S, Ciampoli D, Sanders KM. Identification of neurons that express stem cell factor in the mouse small intestine. Gastroenterology 1998 115 : 898 908.
55. Cochard P, Goldstein M, Black IB. Ontogenetic appearance and disappearance of tyrosine hydroxylase and catecholamines in the rat embryo. Proc Natl Acad Sci USA 1978 75 : 2986 2990.
56. Teitelman G, Baker H, Joh TH, Reis DJ. Appearance of catecholamine- synthesising enzymes during development of rat sympathetic nervous system: possible role of tissue environment. Proc Natl Acad Sci USA 1979 76 : 509 513.
57. Gershon MD, Rothman TP, Joh TH, Teitelman GN. Transient and differential expression of aspects of the catecholaminergic phenotype during development of the fetal bowel of rats and mice. J Neurosci 1984 4 : 2269 2280.
58. Behar TN, Schaffner AE, Scott CA, Greene CL, Barker JL. GABA receptor antagonists modulate postmitotic cell migration in slice cultures of embryonic rat cortex. Cereb Cortex 2000 10 : 899 909.
59. Behar TN, Smith SV, Kennedy RT, McKenzie JM, Maric I, Barker JL. GABA(B) receptors mediate motility signals for migrating embryonic cortical cells. Cereb Cortex 2001 11 : 744 753.
60. Maric D, Liu QY, Maric I et al. GABA expression dominates neuronal lineage progression in the embryonic rat neocortex and facilitates neurite outgrowth via GABA(A) autoreceptor/Cl- channels. J Neurosci 2001 21 : 2343 2360.
61. Bicker G. STOP and GO with NO: nitric oxide as a regulator of cell motility in simple brains. Bioessays 2005 27 : 495 505.
62. McCallion AS, Stames E, Conlon RA, 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.
63. Schiavo G, Benfenati F, Poulain B et al. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 1992 359 : 832 835.
64. McMahon HT, Ushkaryov YA, Edelmann L et al. Cellubrevin is a ubiquitous tetanus-toxin substrate homologous to a putative synaptic vesicle fusion protein. Nature 1993 364 : 346 349.
65. Tayeb MA, Skalski M, Cha MC, Kean MJ, Scaife M, Coppolino MG. Inhibition of SNARE-mediated membrane traffic impairs cell migration. Exp Cell Res 2005 305 : 63 73.
66. Proux-Gillardeaux V, Gavard J, Irinopoulou T, Mege RM, Galli T. Tetanus neurotoxin-mediated cleavage of cellubrevin impairs epithelial cell migration and integrin-dependent cell adhesion. Proc Natl Acad Sci USA 2005 102 : 6362 6367. (Pubitemid 40617448)
67. Haase A, Bicker G. Nitric oxide and cyclic nucleotides are regulators of neuronal migration in an insect embryo. Development 2003 130 : 3977 3987.
68. Knipp S, Bicker G. Regulation of enteric neuron migration by the gaseous messenger molecules CO and NO. Development 2009 136 : 85 93.
69. Goridis C, Rohrer H. Specification of catecholaminergic and serotonergic neurons. Nat Rev Neurosci 2002 3 : 531 541.
70. Flames N, Hobert O. Gene regulatory logic of dopamine neuron differentiation. Nature 2009 458 : 885 889.
71. Rossi J, Herzig KH, Voikar V, Hiltunen PH, Segerstrale M, Airaksinen MS. Alimentary tract innervation deficits and dysfunction in mice lacking GDNF family receptor alpha2. J Clin Invest 2003 112 : 707 716.
72. Chalazonitis A, Pham TD, Rothman TP et al. Neurotrophin-3 is required for the survival-differentiation of subsets of developing enteric neurons. J Neurosci 2001 21 : 5620 5636.
73. Turner KN, Schachner M, Anderson RB. Cell adhesion molecule L1 affects the rate of differentiation of enteric neurons in the developing gut. Dev Dyn 2009 238 : 708 715.
74. Chalazonitis A, Pham TD, Li Z et al. Bone morphogenetic protein regulation of enteric neuronal phenotypic diversity: relationship to timing of cell cycle exit. J Comp Neurol 2008 509 : 474 492.
75. Norris PJ, Charles IG, Scorer CA, Emson PC. Studies on the localization and expression of nitric oxide synthase using histochemical techniques. Histochem J 1995 27 : 745 756.
76. Young HM, Ciampoli D. Transient expression of neuronal nitric oxide synthase by neurons of the submucous plexus of the mouse small intestine. Cell Tissue Res 1998 291 : 395 401.