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Development of enteric neuron diversity.

Hao MM, Young HM - J. Cell. Mol. Med. (2009)

Bottom Line: 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.We then focus on what is known about the mechanisms underlying the generation of enteric neuron diversity and axon pathfinding.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy & Cell Biology, University of Melbourne, Parkville, Victoria, Australia.

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.

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Related in: MedlinePlus

(A1-3) Single optical section through a myenteric ganglion in wholemount preparation of colon from a 28-day-old mouse following immunostaining performed with the pan-neuronal marker, PGP9.5 (red) and the glial marker, S100β (blue). The nuclei had been stained using the nucleic acid stain, SYTO (green). The nuclei adjacent to the ganglion (asterisks) belong to fibroblasts, interstitial cells of Cajal or circular smooth muscle cells. (B) Wholemount preparation of colon from an E12.5 RetTGM mouse [219] in which the neural crest cells express GFP that had also been immunostained performed with the pan-neuronal marker, Tuj1. Tuj1+ cell bodies (open arrows) are intermingled with other crest-derived (GFP+) cells, and they project axon-like processes (arrows) in close association with migrating crest cells. (C) Wholemount preparation of colon from an E12.5 mouse following staining with the pan-neural crest cell marker, Phox2b (green), and NOS (red). Some of the NOS cell bodies (open arrow) give rise to axon-like processes (arrow) that project caudally. (D, E) Wholemount preparations of small intestine from E16.5 (D) and E18.5 (E) mice immunostained with the pan-neuronal marker, Hu (green), and the neuron subtype marker, NOS (red). NOS fibres (arrows) are present in the circular muscle of E18.5 mice (E), but not in E16.5 (D) mice. These fibres run perpendicular to the first nerve fibre tracts to form, which project longitudinally (see Fig. 2E). (F) Submucosal neurons in the small intestine of an E18.5 mouse immunostained for Hu (green) and NOS (red). Although only around 1% of submucosal neurons in adult mice express NOS [19], approximately 50% of submucosal neurons in late embryonic and early post-natal stages express NOS [78]. All scale bars except D, E = 25 μm; D, E = 50 μm.
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fig01: (A1-3) Single optical section through a myenteric ganglion in wholemount preparation of colon from a 28-day-old mouse following immunostaining performed with the pan-neuronal marker, PGP9.5 (red) and the glial marker, S100β (blue). The nuclei had been stained using the nucleic acid stain, SYTO (green). The nuclei adjacent to the ganglion (asterisks) belong to fibroblasts, interstitial cells of Cajal or circular smooth muscle cells. (B) Wholemount preparation of colon from an E12.5 RetTGM mouse [219] in which the neural crest cells express GFP that had also been immunostained performed with the pan-neuronal marker, Tuj1. Tuj1+ cell bodies (open arrows) are intermingled with other crest-derived (GFP+) cells, and they project axon-like processes (arrows) in close association with migrating crest cells. (C) Wholemount preparation of colon from an E12.5 mouse following staining with the pan-neural crest cell marker, Phox2b (green), and NOS (red). Some of the NOS cell bodies (open arrow) give rise to axon-like processes (arrow) that project caudally. (D, E) Wholemount preparations of small intestine from E16.5 (D) and E18.5 (E) mice immunostained with the pan-neuronal marker, Hu (green), and the neuron subtype marker, NOS (red). NOS fibres (arrows) are present in the circular muscle of E18.5 mice (E), but not in E16.5 (D) mice. These fibres run perpendicular to the first nerve fibre tracts to form, which project longitudinally (see Fig. 2E). (F) Submucosal neurons in the small intestine of an E18.5 mouse immunostained for Hu (green) and NOS (red). Although only around 1% of submucosal neurons in adult mice express NOS [19], approximately 50% of submucosal neurons in late embryonic and early post-natal stages express NOS [78]. All scale bars except D, E = 25 μm; D, E = 50 μm.

Mentions: The ENS is composed of a complex network of neurons plus an equal or higher number of enteric glial cells [1, 2]. Enteric neurons form complex circuits that regulate or control a variety of gut functions including motility, secretion, vascular tone and release of hormones. Although there is normally interplay between the ENS and the central nervous system (CNS), in most regions of the gas-trointestinal tract the ENS can function autonomously; the ENS has therefore been referred to as a ‘second brain’[3]. In mammals and birds, most enteric neurons are clustered in myenteric ganglia (Fig. 1A), which are located between the circular and longitudinal muscle layers, and in submucosal ganglia. In the intestine of smaller mammals, myenteric neurons are primarily involved in the regulation of gut motility and submucosal neurons are mostly involved in the regulation of secretion and vascular tone; in larger mammals, some submucosal neurons are also directly involved in motility reflexes [4].


Development of enteric neuron diversity.

Hao MM, Young HM - J. Cell. Mol. Med. (2009)

(A1-3) Single optical section through a myenteric ganglion in wholemount preparation of colon from a 28-day-old mouse following immunostaining performed with the pan-neuronal marker, PGP9.5 (red) and the glial marker, S100β (blue). The nuclei had been stained using the nucleic acid stain, SYTO (green). The nuclei adjacent to the ganglion (asterisks) belong to fibroblasts, interstitial cells of Cajal or circular smooth muscle cells. (B) Wholemount preparation of colon from an E12.5 RetTGM mouse [219] in which the neural crest cells express GFP that had also been immunostained performed with the pan-neuronal marker, Tuj1. Tuj1+ cell bodies (open arrows) are intermingled with other crest-derived (GFP+) cells, and they project axon-like processes (arrows) in close association with migrating crest cells. (C) Wholemount preparation of colon from an E12.5 mouse following staining with the pan-neural crest cell marker, Phox2b (green), and NOS (red). Some of the NOS cell bodies (open arrow) give rise to axon-like processes (arrow) that project caudally. (D, E) Wholemount preparations of small intestine from E16.5 (D) and E18.5 (E) mice immunostained with the pan-neuronal marker, Hu (green), and the neuron subtype marker, NOS (red). NOS fibres (arrows) are present in the circular muscle of E18.5 mice (E), but not in E16.5 (D) mice. These fibres run perpendicular to the first nerve fibre tracts to form, which project longitudinally (see Fig. 2E). (F) Submucosal neurons in the small intestine of an E18.5 mouse immunostained for Hu (green) and NOS (red). Although only around 1% of submucosal neurons in adult mice express NOS [19], approximately 50% of submucosal neurons in late embryonic and early post-natal stages express NOS [78]. All scale bars except D, E = 25 μm; D, E = 50 μm.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4496134&req=5

fig01: (A1-3) Single optical section through a myenteric ganglion in wholemount preparation of colon from a 28-day-old mouse following immunostaining performed with the pan-neuronal marker, PGP9.5 (red) and the glial marker, S100β (blue). The nuclei had been stained using the nucleic acid stain, SYTO (green). The nuclei adjacent to the ganglion (asterisks) belong to fibroblasts, interstitial cells of Cajal or circular smooth muscle cells. (B) Wholemount preparation of colon from an E12.5 RetTGM mouse [219] in which the neural crest cells express GFP that had also been immunostained performed with the pan-neuronal marker, Tuj1. Tuj1+ cell bodies (open arrows) are intermingled with other crest-derived (GFP+) cells, and they project axon-like processes (arrows) in close association with migrating crest cells. (C) Wholemount preparation of colon from an E12.5 mouse following staining with the pan-neural crest cell marker, Phox2b (green), and NOS (red). Some of the NOS cell bodies (open arrow) give rise to axon-like processes (arrow) that project caudally. (D, E) Wholemount preparations of small intestine from E16.5 (D) and E18.5 (E) mice immunostained with the pan-neuronal marker, Hu (green), and the neuron subtype marker, NOS (red). NOS fibres (arrows) are present in the circular muscle of E18.5 mice (E), but not in E16.5 (D) mice. These fibres run perpendicular to the first nerve fibre tracts to form, which project longitudinally (see Fig. 2E). (F) Submucosal neurons in the small intestine of an E18.5 mouse immunostained for Hu (green) and NOS (red). Although only around 1% of submucosal neurons in adult mice express NOS [19], approximately 50% of submucosal neurons in late embryonic and early post-natal stages express NOS [78]. All scale bars except D, E = 25 μm; D, E = 50 μm.
Mentions: The ENS is composed of a complex network of neurons plus an equal or higher number of enteric glial cells [1, 2]. Enteric neurons form complex circuits that regulate or control a variety of gut functions including motility, secretion, vascular tone and release of hormones. Although there is normally interplay between the ENS and the central nervous system (CNS), in most regions of the gas-trointestinal tract the ENS can function autonomously; the ENS has therefore been referred to as a ‘second brain’[3]. In mammals and birds, most enteric neurons are clustered in myenteric ganglia (Fig. 1A), which are located between the circular and longitudinal muscle layers, and in submucosal ganglia. In the intestine of smaller mammals, myenteric neurons are primarily involved in the regulation of gut motility and submucosal neurons are mostly involved in the regulation of secretion and vascular tone; in larger mammals, some submucosal neurons are also directly involved in motility reflexes [4].

Bottom Line: 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.We then focus on what is known about the mechanisms underlying the generation of enteric neuron diversity and axon pathfinding.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy & Cell Biology, University of Melbourne, Parkville, Victoria, Australia.

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.

Show MeSH
Related in: MedlinePlus