Neural crest-derived proprioceptive neurons express nerve growth factor receptors but are not supported by nerve growth factor in culture

doi:10.1016/0306-4522(87)90004-2

Neuroscience

Volume 20, Issue 1, January 1987, Pages 37-46

https://doi.org/10.1016/0306-4522(87)90004-2 Get rights and content

Abstract

The neural crest-derived, first-order, sensory neurons of the embryonic chick trigeminal mesencephalic nucleus were grown in dissociated, glia-free culture. Whereas brain-derived neurotrophic factor promoted the survival and growth of the majority of these neurons (over 70% after 48 h incubation), nerve growth factor had no effect on their survival. The percentage survival in cultures supplemented with nerve growth factor at concentrations ranging from 0.2 to 625 ng/ml was only 2%, the same percentage survival as in control cultures. Furthermore, nerve growth factor did not change the dose-response of these neurons to brain-derived neurotrophic factor. Although nerve growth factor did not influence the survival of trigeminal mesencephalic neurons in culture, nerve growth factor specifically bound to the great majority of neurons growing in the presence of brain-derived neurotrophic factor. Autoradiographs of cultures incubated with iodinated nerve growth factor showed that the perikarya and processes of neurons were heavily labelled with silver grains.

These findings demonstrate the existence of a population of neural crest-derived sensory neurons which express nerve growth factor receptors but are not supported by nerve growth factor in culture.

Reference (68)

CarbonettoS. et al.
Localization of nerve growth factor bound to neurons growing nerve fibres in culture
Devl. Brain Res.
(1982)
DaviesA.M.
The survival and growth of embryonic proprioceptive neurons is promoted by a factor present in skeletal muscle
Devl Biol.
(1986)
DaviesA.M. et al.
Neural crest derived spinal and cranial sensory neurones are equally sensitive to NGF but differ in their response to tissue extracts
Devl Brain Res.
(1984)
DaviesA.M. et al.
The cranial sensory ganglia in culture: response of placode-derived and neural crest-derived neurons to nerve growth factor
Devl Biol.
(1985)
DaviesA.M. et al.
Influence of nerve growth factor on developing dorso-medial and ventro-lateral neurons of chick and mouse trigeminal ganglia
Int. J. devl Neurosci.
(1983)
Fontaine-PerusJ. et al.
Embryonic origin of substance P containing neurons in cranial and spinal sensory ganglia of the avian embryo
Devl Biol.
(1985)
FrazierW.A. et al.
Properties of the specific binding of [¹²⁵I]nerve growth factor responsive peripheral neurones
J. biol. Chem.
(1974)
GreeneL.A.
Quantitative in vitro studies on the nerve growth factor (NGF) requirement of neurons. II. Sensory neurons
Devl Biol.
(1977)
HayashiM. et al.
Nerve growth factor changes the relative levels of neuropeptides in developing sensory and sympathetic ganglia of the chick embryo
Devl Biol.
(1985)
HelkeC.J. et al.
Substance P as a baro- and chemoreceptor afferent neurotransmitter: immunocytochemical and immunochemical evidence in the rat
Peptides
(1980)

HopkinsW.G. et al.

Effect of nerve growth factor on intramuscular axons of neonatal mice

Neuroscience

(1984)

HosangM. et al.

Molecular characteristics of nerve growth factor receptors on PC12 cells

J. biol. Chem.

(1985)

JohnsonE.M. et al.

Characterisation of the effects of autoimmune nerve growth factor deprivation in the developing guinea pig

Neuroscience

(1983)

Le DouarinN.

A biological cell labelling technique and its use in experimental embryology

Devl Biol.

(1973)

LindsayR.M. et al.

Placodal sensory neurons in culture: nodose ganglion neurons are unresponsive to NGF, lack NGF receptors but are supported by a liver derived neurotrophic factor

Devl Biol.

(1985)

ManniE. et al.

Jaw muscle proprioception and mesencephalic trigeminal cells in birds

Expl Neurol.

(1965)

NodenD.M.

The control of avian cephalic neural crest cyto-differentiation. II. Neural Tissues

Devl Biol.

(1978)

RohrerH.

Non-neuronal cells from chick sympathetic and dorsal root sensory ganglia express catecholamine uptake and receptors for nerve growth factor during development

Devl Biol.

(1985)

RohrerH. et al.

Presence and disappearance of nerve growth factor receptors on sensory neurons in culture

Devl Biol.

(1982)

SchwartzJ.P. et al.

Nerve growth factor mediated increase of substance P content of chick embryo dorsal root ganglia

Brain Res.

(1979)

SutterA. et al.

Nerve growth factor receptors. Characterisation of two distinct classes of binding sites on chick embryo sensory ganglia cells

J. biol. Chem.

(1979)

BardeY.-A. et al.

Purification of a new neurotrophic factor from mammalian brain

EMBO J.

(1982)

BardeY.-A. et al.

New neurotrophic factors

Ann. Rev. Physiol.

(1983)

BocchiniV. et al.

The nerve growth factor purification as a 30,000 molecular weight protein

ChunL.L.Y. et al.

Role of nerve growth factor in the development of rat sympathetic neurons in vitro. I. Survival, growth and differentiation of catecholamine production

J. Cell Biol.

(1977)

ChunL.L.Y. et al.

Role of nerve growth factor in the development of rat sympathetic neurons in vitro. II. Development studies

J. Cell Biol.

(1977)

CowanW.M. et al.

Regressive events in neurogenesis

Science

(1984)

D'Amico-MartelA. et al.

Contributions of placodal and neural crest cells to avian cranial peripheral ganglia

Am. J. Anat.

(1983)

DaviesA.M. et al.

Relation of target encounter and neuronal death to nerve growth factor responsiveness in the developing mouse trigeminal ganglion

J. comp. Neurol.

(1984)

DaviesA.M. et al.

The response of chick sensory neuron to brain-derived neurotrophic factor

J. Neurosci.

(1986)

DaviesA.M. et al.

Different factors from the central nervous system and periphery regulate the survival of sensory neurones

Nature

(1986)

EbendalT. et al.

Effects of nerve growth factor on the embryo trigeminal ganglion in culture

Zoonooz

(1975)

EdgarD. et al.

The heparin-binding domain of laminin is responsible for its effects on neurite outgrowth and neuronal survival

EMBO J.

(1984)

GoedertM. et al.

Biochemical and anatomical effects of antibodies against nerve growth factor on developing rat sensory ganglia

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Neural crest-derived proprioceptive neurons express nerve growth factor receptors but are not supported by nerve growth factor in culture

Abstract

Devl. Brain Res.

Devl Biol.

Devl Brain Res.

Devl Biol.

Int. J. devl Neurosci.

Devl Biol.

J. biol. Chem.

Devl Biol.

Devl Biol.

Peptides

Neuroscience

J. biol. Chem.

Neuroscience

Devl Biol.

Devl Biol.

Expl Neurol.

Devl Biol.

Devl Biol.

Devl Biol.

Brain Res.

J. biol. Chem.

Purification of a new neurotrophic factor from mammalian brain

EMBO J.

New neurotrophic factors

Ann. Rev. Physiol.

The nerve growth factor purification as a 30,000 molecular weight protein

Role of nerve growth factor in the development of rat sympathetic neurons in vitro. I. Survival, growth and differentiation of catecholamine production

J. Cell Biol.

Role of nerve growth factor in the development of rat sympathetic neurons in vitro. II. Development studies

J. Cell Biol.

Regressive events in neurogenesis

Science

Contributions of placodal and neural crest cells to avian cranial peripheral ganglia

Am. J. Anat.

Relation of target encounter and neuronal death to nerve growth factor responsiveness in the developing mouse trigeminal ganglion

J. comp. Neurol.

The response of chick sensory neuron to brain-derived neurotrophic factor

J. Neurosci.

Different factors from the central nervous system and periphery regulate the survival of sensory neurones

Nature

Effects of nerve growth factor on the embryo trigeminal ganglion in culture

Zoonooz

The heparin-binding domain of laminin is responsible for its effects on neurite outgrowth and neuronal survival

EMBO J.

Biochemical and anatomical effects of antibodies against nerve growth factor on developing rat sensory ganglia