Expression of Ret-, p75NTR-, Phox2a-, Phox2b-, and tyrosine hydroxylase-immunoreactivity by undifferentiated neural crest-derived cells and different classes of enteric neurons in the embryonic mouse gut

Young, Heather M.; Ciampoli, D.; Hsuan, J. Justin; Canty, AJ

doi:10.1002/(sici)1097-0177(199910)216:2<137::aid-dvdy5>3.0.co;2-6

Cited by 170 publications

(181 citation statements)

References 51 publications

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“…We previously reported the presence of chains of enteric crest cells at the wavefront (Epstein et al, 1991), but the current study provides evidence that these chains constitute the primary pattern of organization at the leading edge as crest cells advance down the avian gut. Others have also seen enteric crest cells aligned in cords in chick (Newgreen et al, 1996) and mouse embryos (Young et al, 1998(Young et al, , 1999, although Young reported both single cells and chains of cells in advance of the wavefront, and Newgreen et al (1996) found strands of crest cells separated from the leading edge in chick. We rarely saw cells separated from the wavefront.…”

Section: Patterns Of Crest Cell Movementmentioning

confidence: 99%

“…Natarajan et al (1999) injected small numbers of dissociated crest cells into the mouse gut; these cells migrated and differentiated but were insufficient to form extensive neuronal networks. Because the number of single cells or cells in chains distinct from the wavefront seen by Newgreen et al (1996) and Young et al (1998Young et al ( , 1999 is small, it is unlikely that these mediate complete colonization of the gut. We postulate that the main mode of colonization at the wavefront of migration occurs by the extension of cords of cells.…”

Section: Patterns Of Crest Cell Movementmentioning

confidence: 99%

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Appearance of neurons and glia with respect to the wavefront during colonization of the avian gut by neural crest cells

Conner

Focke

Noden

et al. 2002

Developmental Dynamics

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The enteric nervous system is formed by neural crest cells that migrate, proliferate, and differentiate into neurons and glia distributed in ganglia along the gastrointestinal tract. In the developing embryo some enteric crest cells cease their caudal movements, whereas others continue to migrate. Subsequently, the enteric neurons form a reticular network of ganglia interconnected by axonal projections. We studied the developing avian gut to characterize the pattern of migration of the crest cells, and the relationship between migration and differentiation. Crest cells at the leading edge of the migratory front appear as strands of cells; isolated individual crest cells are rarely seen. In the foregut and midgut, these strands are located immediately beneath the serosa. In contrast, crest cells entering the colon appear first in the deeper submucosal mesenchyme and later beneath the serosa. As the neural crest wavefront passes caudally, the crest cell cords become highly branched, forming a reticular lattice that presages the mature organization of the enteric nervous system. Neurons and glia first appear within the strands at the advancing wavefront. Later neurons are consistently located at the nodes where branches of the lattice intersect. In the most rostral foregut and in the colon, some neurons initially appear in close association with extrinsic nerve fibers from the vagus and Remak's nerve, respectively. We conclude that crest cells colonize the gut as chains of cells and that, within these chains, both neurons and glia appear close to the wavefront. Developmental Dynamics 226:91-98, 2003.

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Section: Patterns Of Crest Cell Movementmentioning

confidence: 99%

Section: Patterns Of Crest Cell Movementmentioning

confidence: 99%

Appearance of neurons and glia with respect to the wavefront during colonization of the avian gut by neural crest cells

Conner

Focke

Noden

et al. 2002

Developmental Dynamics

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“…Immature neurons in the gut transiently express TH during midembryonic development (Teitelman et al, 1981;Baetge and Gershon, 1989;Baetge et al, 1990a,b;Young et al, 1999). These cells represent approximately 15% of neural crest-derived cells in the gut of E10.5 mice .…”

Section: Characterization Of Gfp + Neurons In the Gut Of Embryonic Thmentioning

confidence: 99%

“…While they are migrating along the gut, a sub-population (10%-20%) of ENCCs starts to express panneuronal markers including neurofilaments, Hu, Tuj1, and PGP9.5 and may be considered immature neurons (Baetge and Gershon, 1989;Fairman et al, 1995;Newgreen and Hartley, 1995;Young et al, 1999Young et al, , 2002Barlow et al, 2003;Conner et al, 2003;Kruger et al, 2003;Bondurand et al, 2006). Immature enteric neurons also transiently express the catecholamine synthetic enzyme, tyrosine hydroxylase (TH) (Teitelman, 1981;Baetge and Gershon, 1989;Baetge et al, 1990a,b;Young et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

“…Immature enteric neurons also transiently express the catecholamine synthetic enzyme, tyrosine hydroxylase (TH) (Teitelman, 1981;Baetge and Gershon, 1989;Baetge et al, 1990a,b;Young et al, 1999). In our previous time-lapse study using embryonic mice in which all ENCCs express GFP, we examined the phenotype of individual cells close to the migratory wavefront (Young et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

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The migratory behavior of immature enteric neurons

Hao

Anderson

Kobayashi

et al. 2008

Developmental Neurobiology

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While they are migrating caudally along the developing gut, around 10%-20% of enteric neural crest-derived cells start to express pan-neuronal markers and tyrosine hydroxylase (TH). We used explants of gut from embryonic TH-green fluorescence protein (GFP) mice and time-lapse microscopy to examine whether these immature enteric neurons migrate and their mode of migration. In the gut of E10.5 and E11.5 TH-GFP mice, around 50% of immature enteric neurons (GFP + cells) migrated, with an average speed of around 15 lm/h. This is slower than the speed at which the population of enteric neural crest-derived cells advances along the developing gut, and hence neuronal differentiation seems to slow, but not necessarily halt, the caudal migration of enteric neural crest cells. Most migrating immature enteric neurons migrated caudally by extending a long-leading process followed by translocation of the cell body. This mode of migration is different from that of non-neuronal enteric neural crestderived cells and neural crest cells in other locations, but resembles that of migrating neurons in many regions of the developing central nervous system (CNS). In migrating immature enteric neurons, a swelling often preceded the movement of the nucleus in the direction of the leading process. However, the centrosomal marker, pericentrin, was not localized to either the leading process or swelling. This seems to be the first detailed report of neuronal migration in the developing mammalian peripheral nervous system. ' 2008 Wiley Periodicals, Inc. Develop Neurobiol 69: 22-35, 2009

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Synapse formation during neuron differentiation: An in situ study of the myenteric plexus during murine embryonic life

Vannucchi¹,

Faussone–Pellegrini²

2000

J. Comp. Neurol.

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Ultrastructural steps characterizing synapse formation in vivo and appearance in neuroblasts of properties suggestive of synaptic function acquisition have scarcely been studied. Synapse formation and proteosynthetic apparatus organization were thus studied under transmission electron microscope in mouse myenteric neurons from embryonic day 12.5 (E12.5) until birth. Expression of Ret and p75(NTR), markers of neural crest cells, as well as that of neuron-specific enolase (NSE), synaptophysin (SY), and synaptosomal-associated protein (SNAP), markers of synaptic function acquisition, were immunohistochemically evaluated. At E12.5 many cells were Ret- and p75(NTR)-immunoreactive (IR), whereas a few were NSE-IR and had neuronal ultrastructural characteristics. Two types of contacts between poorly or nondifferentiated cells and axons of presumed extrinsic (synapse-like contacts) or local (immature synapses) origin were identified, along with SY-IR elements. By E16. 5, many cells had developed a proteosynthetic apparatus, synapse-like contacts were no longer present, and immature synapses were gradually differentiating. Concurrently, there was an increase in NSE-IR cells, some of which were also SNAP-IR, and in SY-IR varicosities. At E18.5, ultrastructurally mature neurons and synapses had increased in number as had NSE-IR and SNAP-IR cells and SY-IR varicosities. These data indicate that 1) one type of contact (synapse-like) is present at E12.5 between very immature cells and presumed vagal fibers, with a possible transient role for the onset of the differentiative process of these cells; and 2) another type of contact (typical synapses) lasts until E18.5, with a similar but long-lasting role that progressively shifts to the classical function (neurotransmission) as the synapse matures and the embryo reaches the day of birth.

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Expression of Ret-, p75NTR-, Phox2a-, Phox2b-, and tyrosine hydroxylase-immunoreactivity by undifferentiated neural crest-derived cells and different classes of enteric neurons in the embryonic mouse gut

Cited by 170 publications

References 51 publications

Appearance of neurons and glia with respect to the wavefront during colonization of the avian gut by neural crest cells

Appearance of neurons and glia with respect to the wavefront during colonization of the avian gut by neural crest cells

The migratory behavior of immature enteric neurons

Synapse formation during neuron differentiation: An in situ study of the myenteric plexus during murine embryonic life

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