Origins, migration and differentiation of glial cells in the insect enteric nervous system from a discrete set of glial precursors

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

The enteric nervous system (ENS) of the moth, Manduca sexta, consists of two primary cellular domains and their associated nerves. The neurons of the anterior domain occupy two small peripheral ganglia (the frontal and hypocerebral ganglia), while a second population of neurons occupies a branching nerve plexus (the enteric plexus) that spans the foregut-midgut boundary. Previously, we have shown these two regions arise by separate programs of neurogenesis: cells that form the anterior enteric ganglia are generated from three discrete proliferative zones that differentiate within the foregut epithelium. In contrast, the cells of the enteric plexus (the EP cells) emerge from a neurogenic placode within the posterior lip of the foregut. Both sets of neurons subsequently undergo an extended period of migration and reorganization to achieve their mature distributions. We now show that prior to the completion of neurogenesis, an additional class of precursor cells is generated from the three proliferative zones of the foregut. Coincident with the onset of neuronal migration, this precursor class enters a phase of enhanced mitotic activity, giving rise to a population of cells that continue to divide as the ENS matures. Using clonal analyses of individual precursors, we demonstrate that the progeny of these cells become distributed along the same pathways taken by the migratory neurons; subsequently, they contribute to an ensheathing layer around the branches of the enteric plexus and the enteric ganglia. We conclude that this additional precursor class, which shares a common developmental origin with the enteric neurons, gives rise to a distinct population of peripheral glial cells. Moreover, the distribution of enteric glial cells is achieved by their migration and differentiation along the same pathways that are formed during the preceding phases of neuronal migration.

Original languageEnglish (US)
Pages (from-to)59-74
Number of pages16
JournalDevelopment
Volume117
Issue number1
StatePublished - Jan 1993

Fingerprint

Enteric Nervous System
Neuroglia
Insects
Ganglia
Neurons
Neurogenesis
Population
Manduca
Moths
Lip
Epithelium

Keywords

  • Cell lineage
  • Enteric nervous system
  • Glial differentiation
  • Glial progenitor
  • Manduca sexta

ASJC Scopus subject areas

  • Cell Biology
  • Anatomy

Cite this

@article{82bb841f851d4237ab354cf764d2aeec,
title = "Origins, migration and differentiation of glial cells in the insect enteric nervous system from a discrete set of glial precursors",
abstract = "The enteric nervous system (ENS) of the moth, Manduca sexta, consists of two primary cellular domains and their associated nerves. The neurons of the anterior domain occupy two small peripheral ganglia (the frontal and hypocerebral ganglia), while a second population of neurons occupies a branching nerve plexus (the enteric plexus) that spans the foregut-midgut boundary. Previously, we have shown these two regions arise by separate programs of neurogenesis: cells that form the anterior enteric ganglia are generated from three discrete proliferative zones that differentiate within the foregut epithelium. In contrast, the cells of the enteric plexus (the EP cells) emerge from a neurogenic placode within the posterior lip of the foregut. Both sets of neurons subsequently undergo an extended period of migration and reorganization to achieve their mature distributions. We now show that prior to the completion of neurogenesis, an additional class of precursor cells is generated from the three proliferative zones of the foregut. Coincident with the onset of neuronal migration, this precursor class enters a phase of enhanced mitotic activity, giving rise to a population of cells that continue to divide as the ENS matures. Using clonal analyses of individual precursors, we demonstrate that the progeny of these cells become distributed along the same pathways taken by the migratory neurons; subsequently, they contribute to an ensheathing layer around the branches of the enteric plexus and the enteric ganglia. We conclude that this additional precursor class, which shares a common developmental origin with the enteric neurons, gives rise to a distinct population of peripheral glial cells. Moreover, the distribution of enteric glial cells is achieved by their migration and differentiation along the same pathways that are formed during the preceding phases of neuronal migration.",
keywords = "Cell lineage, Enteric nervous system, Glial differentiation, Glial progenitor, Manduca sexta",
author = "Philip Copenhaver",
year = "1993",
month = "1",
language = "English (US)",
volume = "117",
pages = "59--74",
journal = "Development (Cambridge)",
issn = "0950-1991",
publisher = "Company of Biologists Ltd",
number = "1",

}

TY - JOUR

T1 - Origins, migration and differentiation of glial cells in the insect enteric nervous system from a discrete set of glial precursors

AU - Copenhaver, Philip

PY - 1993/1

Y1 - 1993/1

N2 - The enteric nervous system (ENS) of the moth, Manduca sexta, consists of two primary cellular domains and their associated nerves. The neurons of the anterior domain occupy two small peripheral ganglia (the frontal and hypocerebral ganglia), while a second population of neurons occupies a branching nerve plexus (the enteric plexus) that spans the foregut-midgut boundary. Previously, we have shown these two regions arise by separate programs of neurogenesis: cells that form the anterior enteric ganglia are generated from three discrete proliferative zones that differentiate within the foregut epithelium. In contrast, the cells of the enteric plexus (the EP cells) emerge from a neurogenic placode within the posterior lip of the foregut. Both sets of neurons subsequently undergo an extended period of migration and reorganization to achieve their mature distributions. We now show that prior to the completion of neurogenesis, an additional class of precursor cells is generated from the three proliferative zones of the foregut. Coincident with the onset of neuronal migration, this precursor class enters a phase of enhanced mitotic activity, giving rise to a population of cells that continue to divide as the ENS matures. Using clonal analyses of individual precursors, we demonstrate that the progeny of these cells become distributed along the same pathways taken by the migratory neurons; subsequently, they contribute to an ensheathing layer around the branches of the enteric plexus and the enteric ganglia. We conclude that this additional precursor class, which shares a common developmental origin with the enteric neurons, gives rise to a distinct population of peripheral glial cells. Moreover, the distribution of enteric glial cells is achieved by their migration and differentiation along the same pathways that are formed during the preceding phases of neuronal migration.

AB - The enteric nervous system (ENS) of the moth, Manduca sexta, consists of two primary cellular domains and their associated nerves. The neurons of the anterior domain occupy two small peripheral ganglia (the frontal and hypocerebral ganglia), while a second population of neurons occupies a branching nerve plexus (the enteric plexus) that spans the foregut-midgut boundary. Previously, we have shown these two regions arise by separate programs of neurogenesis: cells that form the anterior enteric ganglia are generated from three discrete proliferative zones that differentiate within the foregut epithelium. In contrast, the cells of the enteric plexus (the EP cells) emerge from a neurogenic placode within the posterior lip of the foregut. Both sets of neurons subsequently undergo an extended period of migration and reorganization to achieve their mature distributions. We now show that prior to the completion of neurogenesis, an additional class of precursor cells is generated from the three proliferative zones of the foregut. Coincident with the onset of neuronal migration, this precursor class enters a phase of enhanced mitotic activity, giving rise to a population of cells that continue to divide as the ENS matures. Using clonal analyses of individual precursors, we demonstrate that the progeny of these cells become distributed along the same pathways taken by the migratory neurons; subsequently, they contribute to an ensheathing layer around the branches of the enteric plexus and the enteric ganglia. We conclude that this additional precursor class, which shares a common developmental origin with the enteric neurons, gives rise to a distinct population of peripheral glial cells. Moreover, the distribution of enteric glial cells is achieved by their migration and differentiation along the same pathways that are formed during the preceding phases of neuronal migration.

KW - Cell lineage

KW - Enteric nervous system

KW - Glial differentiation

KW - Glial progenitor

KW - Manduca sexta

UR - http://www.scopus.com/inward/record.url?scp=0027405793&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0027405793&partnerID=8YFLogxK

M3 - Article

VL - 117

SP - 59

EP - 74

JO - Development (Cambridge)

JF - Development (Cambridge)

SN - 0950-1991

IS - 1

ER -