Development of Enteric Neuron Diversity

Overview

Journal J Cell Mol Med

Specialties Cell Biology
Molecular Biology

Date 2009 Jun 23

PMID 19538470

Citations 74

Authors

Marlene M Hao

Heather M Young

Affiliations

Soon will be listed here.

Abstract

The mature enteric nervous system (ENS) is composed of many different neuron subtypes and enteric glia, which all arise from the neural crest. How this diversity is generated from neural crest-derived cells is a central question in neurogastroenterology, as defects in these processes are likely to underlie some paediatric motility disorders. Here we review the developmental appearance (the earliest age at which expression of specific markers can be localized) and birthdates (the age at which precursors exit the cell cycle) of different enteric neuron subtypes, and their projections to some targets. We then focus on what is known about the mechanisms underlying the generation of enteric neuron diversity and axon pathfinding. Finally, we review the development of the ENS in humans and the etiologies of a number of paediatric motility disorders.

Citing Articles

Neuroimmune Crossroads: The Interplay of the Enteric Nervous System and Intestinal Macrophages in Gut Homeostasis and Disease.

Lou M, Heuckeroth R, Tjaden N Biomolecules. 2024; 14(9).

PMID: 39334870 PMC: 11430413. DOI: 10.3390/biom14091103.

Somatostatin-immunoreactive neurons of the rat gut during the development.

Emanuilov A, Budnik A, Masliukov P Histochem Cell Biol. 2024; 162(5):385-402.

PMID: 39153131 DOI: 10.1007/s00418-024-02322-9.

Spontaneous enteric nervous system activity generates contractile patterns prior to maturation of gastrointestinal motility.

Dershowitz L, Bueno Garcia H, Perley A, Coleman T, Kaltschmidt J Neurogastroenterol Motil. 2024; :e14890.

PMID: 39118231 PMC: 11806083. DOI: 10.1111/nmo.14890.

A novel method for culturing enteric neurons generates neurospheres containing functional myenteric neuronal subtypes.

Mandal A, Moneme C, Tewari B, Goldstein A, Sontheimer H, Cheng L J Neurosci Methods. 2024; 407:110144.

PMID: 38670535 PMC: 11144385. DOI: 10.1016/j.jneumeth.2024.110144.

Spatial gene expression profile of Wnt-signaling components in the murine enteric nervous system.

Scharr M, Hirt B, Neckel P Front Immunol. 2024; 15:1302488.

PMID: 38322254 PMC: 10846065. DOI: 10.3389/fimmu.2024.1302488.

References

Qian X, Shen Q, Goderie S, He W, Capela A, Davis A . Timing of CNS cell generation: a programmed sequence of neuron and glial cell production from isolated murine cortical stem cells. Neuron. 2000; 28(1):69-80. DOI: 10.1016/s0896-6273(00)00086-6. View

Sato Y, Heuckeroth R . Retinoic acid regulates murine enteric nervous system precursor proliferation, enhances neuronal precursor differentiation, and reduces neurite growth in vitro. Dev Biol. 2008; 320(1):185-98. PMC: 2586054. DOI: 10.1016/j.ydbio.2008.05.524. View

Goridis C, Rohrer H . Specification of catecholaminergic and serotonergic neurons. Nat Rev Neurosci. 2002; 3(7):531-41. DOI: 10.1038/nrn871. View

Hao M, Moore R, Roberts R, Nguyen T, Furness J, Anderson R . The role of neural activity in the migration and differentiation of enteric neuron precursors. Neurogastroenterol Motil. 2010; 22(5):e127-37. DOI: 10.1111/j.1365-2982.2009.01462.x. View

Manneschi L, Vannucchi M, Bechi P, Faussone-Pellegrini M . Neuron density and distribution of NADPH-diaphorase positive neurons in the human stomach. Neurosci Lett. 1998; 250(3):169-72. DOI: 10.1016/s0304-3940(98)00468-6. View

Turner K, Schachner M, Anderson R . Cell adhesion molecule L1 affects the rate of differentiation of enteric neurons in the developing gut. Dev Dyn. 2009; 238(3):708-15. DOI: 10.1002/dvdy.21861. View

Moore M, Klein R, Farinas I, Sauer H, Armanini M, Phillips H . Renal and neuronal abnormalities in mice lacking GDNF. Nature. 1996; 382(6586):76-9. DOI: 10.1038/382076a0. View

Taguchi T, Suita S, Masumoto K, Nagasaki A . An abnormal distribution of C-kit positive cells in the normoganglionic segment can predict a poor clinical outcome in patients with Hirschsprung's disease. Eur J Pediatr Surg. 2005; 15(3):153-8. DOI: 10.1055/s-2005-837612. View

Rothman T, Gershon M . Phenotypic expression in the developing murine enteric nervous system. J Neurosci. 1982; 2(3):381-93. PMC: 6564326. View

10.

DAutreaux F, Morikawa Y, Cserjesi P, Gershon M . Hand2 is necessary for terminal differentiation of enteric neurons from crest-derived precursors but not for their migration into the gut or for formation of glia. Development. 2007; 134(12):2237-49. DOI: 10.1242/dev.003814. View

11.

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(10):2075-86. DOI: 10.1242/dev.02375. View

12.

Golden J, DeMaro J, Osborne P, Milbrandt J, Johnson Jr E . Expression of neurturin, GDNF, and GDNF family-receptor mRNA in the developing and mature mouse. Exp Neurol. 1999; 158(2):504-28. DOI: 10.1006/exnr.1999.7127. View

13.

Furness J, Jones C, Nurgali K, Clerc N . Intrinsic primary afferent neurons and nerve circuits within the intestine. Prog Neurobiol. 2004; 72(2):143-64. DOI: 10.1016/j.pneurobio.2003.12.004. View

14.

Heng J, Nguyen L, Castro D, Zimmer C, Wildner H, Armant O . Neurogenin 2 controls cortical neuron migration through regulation of Rnd2. Nature. 2008; 455(7209):114-8. DOI: 10.1038/nature07198. View

15.

Nagy N, Goldstein A . Endothelin-3 regulates neural crest cell proliferation and differentiation in the hindgut enteric nervous system. Dev Biol. 2006; 293(1):203-17. DOI: 10.1016/j.ydbio.2006.01.032. View

16.

Vohra B, Tsuji K, Nagashimada M, Uesaka T, Wind D, Fu M . Differential gene expression and functional analysis implicate novel mechanisms in enteric nervous system precursor migration and neuritogenesis. Dev Biol. 2006; 298(1):259-71. PMC: 1952185. DOI: 10.1016/j.ydbio.2006.06.033. View

17.

Wakamatsu Y, Maynard T, Weston J . Fate determination of neural crest cells by NOTCH-mediated lateral inhibition and asymmetrical cell division during gangliogenesis. Development. 2000; 127(13):2811-21. DOI: 10.1242/dev.127.13.2811. View

18.

Natarajan D, Grigoriou M, Atkins C, Pachnis V . Multipotential progenitors of the mammalian enteric nervous system capable of colonising aganglionic bowel in organ culture. Development. 1998; 126(1):157-68. DOI: 10.1242/dev.126.1.157. View

19.

Brehmer A, Schrodl F, Neuhuber W . Morphology of VIP/nNOS-immunoreactive myenteric neurons in the human gut. Histochem Cell Biol. 2005; 125(5):557-65. DOI: 10.1007/s00418-005-0107-8. View

20.

Barlow A, de Graaff E, Pachnis V . Enteric nervous system progenitors are coordinately controlled by the G protein-coupled receptor EDNRB and the receptor tyrosine kinase RET. Neuron. 2003; 40(5):905-16. DOI: 10.1016/s0896-6273(03)00730-x. View