An ultrastructural study of neurons and non-neuronal cells in the myenteric plexus of the rabbit colon

doi:10.1016/0306-4522(82)90037-9

Neuroscience

Volume 7, Issue 7, July 1982, Pages 1797-1806

https://doi.org/10.1016/0306-4522(82)90037-9 Get rights and content

Abstract

The myenteric plexus of the rabbit colon showed a degree of structural organization that was unusually high for the peripheral nervous system, providing a basis for the complex integrative activity which is known to occur. It resembled central nervous tissue in several respects: a wide range of neuron types was present; the proportion of glial cells to neurons was about 2:1; and there was a densely packed, avascular neuropil, not penetrated by connective tissue. Most neurons had at least one surface exposed to the extraganglionic space. Clear evidence was obtained for spontaneous neuronal degeneration. Three types of non-neuronal (glial) cells were observed: Type 1, which was most common, contained many 10 nm ‘gliofilaments’ and resembled enteric glial cells or astrocytes in the central nervous system; Type 2, composing about 5% of the glial cells, had few filaments; Type 3 was seen only rarely, had a small dark nucleus, little cytoplasm, may have been of extraganglionic origin and resembled microglia of the central nervous system. Fibroblast-like cells were also present in extraganglionic sites. Schwann cells could not be identified within the myenteric ganglia.

References (36)

DailW.G. et al.
Ultrastructure of adrenergic terminals and SIF cells in the superior cervical ganglion of the rabbit
Brain Res.
(1978)
FurnessJ.B. et al.
Types of nerves in the enteric nervous system
Neuroscience
(1980)
GabellaG.
Ultrastructure of the nerve plexuses of the mammalian intestine: the enteric glial cells
Neuroscience
(1981)
TaxiJ.
The chromaffin and chromaffin-like cells in the autonomic nervous system
Int. Rev. Cytol.
(1979)
VaughnJ.E. et al.
The morphology and development of neuroglial cells
BaumgartenH.G. et al.
Auerbach's plexus of mammals and man: electron microscopic identification of three different types of neuronal processes in myenteric ganglia of the large intestine from rhesus monkey, guinea-pigs and man
Z. Zellforsch. mikrosk. Anat.
(1970)
BurnstockG.
Interactions of cholinergic, adrenergic, purinergic and peptidergic neurons in the gut
BursztajnS. et al.
Discrimination between nicotinic receptors in vertebrate ganglia and skeletal muscle by alpha-bungarotoxin and cobra venoms
J. Physiol., Lond.
(1977)
CammermeyerJ.
The life history of the microglial cell: a light-microscopic study
Neurosci. Res.
(1970)
CookR.D. et al.
The ultrastructure of Auerbach's plexus in the guinea-pig—I. Neuronal elements
J. Neurocytol.
(1976)

CookR.D. et al.

The ultrastructure of Auerbach's plexus in the guinea-pig—II. Non-neuronal elements

J. Neurocytol.

(1976)

CostaM. et al.

Adrenergic innervation of the alimentary canal

Z. Zellforsch, mikrosk. Anat.

(1971)

GabellaG.

Glial cells in the myenteric plexus

Z. Natur-f.

(1971)

GabellaG.

Fine structure of the myenteric plexus in the guinea-pig ileum

J. Anat.

(1972)

GabellaG.

Structure of the Autonomic Nervous System

(1976)

GabellaG.

Innervation of the gastrointestinal tract.

Int. Rev. Cytol.

(1979)

GabellaG.

Structure of muscles and nerves in the gastrointestinal tract

GershonM.D. et al.

Properties of the enteric nervous system: limitation of access of intravascular macromolecules to the myenteric plexus and muscularis externa

J. comp. Neurol.

(1978)

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Gabella was the first to label glia in the gut “enteric glial cells” (EGCs), in recognition that they were phenotypically distinct from Schwann cells (Gabella, 1981). He and others showed that many EGCs had small central perikarya and stellate processes, more similar in ultrastructure to astrocytes than Schwann cells (Gabella, 1971; Komuro et al., 1982). These morphological studies combined with the discovery that enteric glia expressed S100B and glial fibrillary acidic protein (GFAP) (Ferri et al., 1982; Jessen and Mirsky, 1983), molecular markers characteristic of astrocytes, led to the idea that enteric glia were the “astroglia” of the gut.
Glia, the non-neuronal cells of the nervous system, were long considered secondary cells only necessary for supporting the functions of their more important neuronal neighbors. Work by many groups over the past two decades has completely overturned this notion, revealing the myriad and vital functions of glia in nervous system development, plasticity, and health. The largest population of glia outside the brain is in the enteric nervous system, a division of the autonomic nervous system that constitutes a key node of the gut-brain axis. Here, we review the latest in the understanding of these enteric glia in mammals with a focus on their putative roles in human health and disease.
Evidence of a Myenteric Plexus Barrier and Its Macrophage-Dependent Degradation During Murine Colitis: Implications in Enteric Neuroinflammation
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Neuroinflammation in the gut is associated with many gastrointestinal (GI) diseases, including inflammatory bowel disease. In the brain, neuroinflammatory conditions are associated with blood-brain barrier (BBB) disruption and subsequent neuronal injury. We sought to determine whether the enteric nervous system is similarly protected by a physical barrier and whether that barrier is disrupted in colitis.
Confocal and electron microscopy were used to characterize myenteric plexus structure, and FITC-dextran assays were used to assess for presence of a barrier. Colitis was induced with dextran sulfate sodium, with co-administration of liposome-encapsulated clodronate to deplete macrophages.
We identified a blood-myenteric barrier (BMB) consisting of extracellular matrix proteins (agrin and collagen-4) and glial end-feet, reminiscent of the BBB, surrounded by a collagen-rich periganglionic space. The BMB is impermeable to the passive movement of 4 kDa FITC-dextran particles. A population of macrophages is present within enteric ganglia (intraganglionic macrophages [IGMs]) and exhibits a distinct morphology from muscularis macrophages, with extensive cytoplasmic vacuolization and mitochondrial swelling but without signs of apoptosis. IGMs can penetrate the BMB in physiological conditions and establish direct contact with neurons and glia. Dextran sulfate sodium-induced colitis leads to BMB disruption, loss of its barrier integrity, and increased numbers of IGMs in a macrophage-dependent process.
In intestinal inflammation, macrophage-mediated degradation of the BMB disrupts its physiological barrier function, eliminates the separation of the intra- and extra-ganglionic compartments, and allows inflammatory stimuli to access the myenteric plexus. This suggests a potential mechanism for the onset of neuroinflammation in colitis and other GI pathologies with acquired enteric neuronal dysfunction.
Enteric glial reactivity to systemic LPS administration: Changes in GFAP and S100B protein
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Citation Excerpt :
For over forty years, astrocytic characteristics have been recognized in the enteric glia cell (EGC) (Gabella, 1971, 1981). The similarities between astrocytes and the enteric glia have been demonstrated in both morphological (Gabella and Trigg, 1984; Hanani and Reichenbach, 1994; Komuro et al., 1982) and functional (Aube et al., 2006; Ferri et al., 1982; Hoff et al., 2008; Jessen and Mirsky, 1980, 1983; Kimball and Mulholland, 1996; Nasser et al., 2006a) aspects. Even in response to different insults, such as inflammation and infection, similarities are observed between the responses of the astrocytes and the enteric glia (Cabarrocas et al., 2003; Coelho-Aguiar et al., 2015).
Lipopolysaccharide (LPS) is used to induce inflammation and promotes nervous system activation. Different regions of the brain present heterogeneous glial responses; thus, in order to verify whether systemic LPS-induced inflammation affects the enteric glia differently across the intestinal segments, we evaluated the expressions of two glial activity markers, GFAP and S100B protein, in different intestine segments, at 1 h, 24 h and 7 days after acute systemic LPS administration (0.25 or 2.5 mg kg⁻¹) in rats. Histological inflammatory analysis indicated that the cecum was most affected when compared to the duodenum and proximal colon at the highest doses of LPS. LPS induced an increased S100B content after 24 h in all three regions, which decreased at 7 days after the highest dose in all regions. Moreover, at 24 h, this dose of LPS increased ex-vivo S100B secretion only in the cecum. The highest dose of LPS also increased GFAP in all regions at 24 h, but earlier in the cecum, where LPS-induced enteric S100B and GFAP alterations were dependent on dose, time and intestine region. No associated changes in serum S100B were observed. Our results indicate heterogeneous enteric glial responses to inflammatory insult, as observed in distinct brain areas.
Development of the Enteric Nervous System
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Development of the Enteric Nervous System
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Vasoactive intestinal peptide rescues cultured rat myenteric neurons from lipopolysaccharide induced cell death
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The role of the enteric nervous system in intestinal inflammation is not fully understood and the plethora of cellular activities concurrently ongoing in vivo renders intelligible studies difficult. In order to explore possible effects of bacterial lipopolysaccharide (LPS) on enteric neurons we utilised cultured myenteric neurons from rat small intestine. Exposure to LPS caused markedly reduced neuronal survival and increased neuronal expression of vasoactive intestinal peptide (VIP), while the expression of Toll-like receptor 4 (TLR4) was unchanged. TLR4 was expressed in approximately 35% of all myenteric neurons irrespective of if they were cultured in the presence or absence of LPS. In neurons cultured in medium, without LPS, 50% of all TLR4-immunoreactive neurons contained also VIP. Addition of LPS to the neuronal cultures markedly increased the proportion of TLR4-immunoreactive neurons also expressing VIP, while the proportion of TLR4 neurons devoid of VIP decreased. Simultaneous addition of LPS and VIP to the neuronal cultures resulted in a neuronal survival comparable to controls.
LPS recognition by myenteric neurons is mediated via TLR4 and causes neuronal cell death. Presence of VIP rescues the neurons from LPS-induced neurodegeneration.

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^*: Present address: Department of Anatomy, Ehime University School of Medicine, Shigenobu, Ehime, Japan.

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An ultrastructural study of neurons and non-neuronal cells in the myenteric plexus of the rabbit colon

Abstract

Brain Res.

Neuroscience

Neuroscience

Int. Rev. Cytol.

Auerbach's plexus of mammals and man: electron microscopic identification of three different types of neuronal processes in myenteric ganglia of the large intestine from rhesus monkey, guinea-pigs and man

Z. Zellforsch. mikrosk. Anat.

Interactions of cholinergic, adrenergic, purinergic and peptidergic neurons in the gut

Discrimination between nicotinic receptors in vertebrate ganglia and skeletal muscle by alpha-bungarotoxin and cobra venoms

J. Physiol., Lond.

The life history of the microglial cell: a light-microscopic study

Neurosci. Res.

The ultrastructure of Auerbach's plexus in the guinea-pig—I. Neuronal elements

J. Neurocytol.

The ultrastructure of Auerbach's plexus in the guinea-pig—II. Non-neuronal elements

J. Neurocytol.

Adrenergic innervation of the alimentary canal

Z. Zellforsch, mikrosk. Anat.

Glial cells in the myenteric plexus

Z. Natur-f.

Fine structure of the myenteric plexus in the guinea-pig ileum

J. Anat.

Structure of the Autonomic Nervous System

Innervation of the gastrointestinal tract.

Int. Rev. Cytol.

Structure of muscles and nerves in the gastrointestinal tract

Properties of the enteric nervous system: limitation of access of intravascular macromolecules to the myenteric plexus and muscularis externa

J. comp. Neurol.