Nerve growth factor expression in parasympathetic neurons: Regulation by sympathetic innervation

Wohaib Hasan, Peter G. Smith

Research output: Contribution to journalArticle

23 Citations (Scopus)

Abstract

Interactions between sympathetic and parasympathetic nerves are important in regulating visceral target function. Sympathetic nerves are closely apposed to, and form functional synapses with, parasympathetic axons in many effector organs. The molecular mechanisms responsible for these structural and functional interactions are unknown. We explored the possibility that Nerve Growth Factor (NGF) synthesis by parasympathetic neurons provides a mechanism by which sympathetic-parasympathetic interactions are established. Parasympathetic pterygopalatine ganglia NGF-gene expression was examined by in situ hybridization and protein content assessed by immunohistochemistry. Under control conditions, NGF mRNA was present in ≈60% and NGF protein was in 40% of pterygopalatine parasympathetic neurons. Peripheral parasympathetic axons identified by vesicular acetylcholine transporter-immunoreactivity also displayed NGF immunoreactivity. To determine if sympathetic innervation regulates parasympathetic NGF expression, the ipsilateral superior cervical ganglion was excised. Thirty days postsympathectomy, the numbers of NGF mRNA-positive neurons were decreased to 38% and NGF immunoreactive neurons to 15%. This reduction was due to a loss of sympathetic nerve impulse activity, as similar reductions were achieved when superior cervical ganglia were deprived of preganglionic afferent input for 40 days. These findings provide evidence that normally NGF is synthesized by parasympathetic neurons and transported anterogradely to fibre terminals, where it may be available to sympathetic axons. Parasympathetic NGF expression, in turn, is augmented by impulse activity within (and presumably transmitter release from) sympathetic axons. It is suggested that parasympathetic NGF synthesis and its modulation by sympathetic innervation provides a molecular basis for establishment and maintenance of autonomic axo-axonal synaptic interactions.

Original languageEnglish (US)
Pages (from-to)4391-4397
Number of pages7
JournalEuropean Journal of Neuroscience
Volume12
Issue number12
DOIs
StatePublished - 2000
Externally publishedYes

Fingerprint

Nerve Growth Factor
Neurons
Axons
Parasympathetic Ganglia
Superior Cervical Ganglion
Vesicular Acetylcholine Transport Proteins
Messenger RNA
Synapses
Action Potentials
In Situ Hybridization
Proteins
Immunohistochemistry
Maintenance
Gene Expression

Keywords

  • Decentralization
  • Immunohistochemistry
  • In situ hybridization
  • Pterygopalatine ganglion
  • Rat
  • Sympathectomy

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Nerve growth factor expression in parasympathetic neurons : Regulation by sympathetic innervation. / Hasan, Wohaib; Smith, Peter G.

In: European Journal of Neuroscience, Vol. 12, No. 12, 2000, p. 4391-4397.

Research output: Contribution to journalArticle

@article{bd8e96c446ac4a8da3413a5928d56eea,
title = "Nerve growth factor expression in parasympathetic neurons: Regulation by sympathetic innervation",
abstract = "Interactions between sympathetic and parasympathetic nerves are important in regulating visceral target function. Sympathetic nerves are closely apposed to, and form functional synapses with, parasympathetic axons in many effector organs. The molecular mechanisms responsible for these structural and functional interactions are unknown. We explored the possibility that Nerve Growth Factor (NGF) synthesis by parasympathetic neurons provides a mechanism by which sympathetic-parasympathetic interactions are established. Parasympathetic pterygopalatine ganglia NGF-gene expression was examined by in situ hybridization and protein content assessed by immunohistochemistry. Under control conditions, NGF mRNA was present in ≈60{\%} and NGF protein was in 40{\%} of pterygopalatine parasympathetic neurons. Peripheral parasympathetic axons identified by vesicular acetylcholine transporter-immunoreactivity also displayed NGF immunoreactivity. To determine if sympathetic innervation regulates parasympathetic NGF expression, the ipsilateral superior cervical ganglion was excised. Thirty days postsympathectomy, the numbers of NGF mRNA-positive neurons were decreased to 38{\%} and NGF immunoreactive neurons to 15{\%}. This reduction was due to a loss of sympathetic nerve impulse activity, as similar reductions were achieved when superior cervical ganglia were deprived of preganglionic afferent input for 40 days. These findings provide evidence that normally NGF is synthesized by parasympathetic neurons and transported anterogradely to fibre terminals, where it may be available to sympathetic axons. Parasympathetic NGF expression, in turn, is augmented by impulse activity within (and presumably transmitter release from) sympathetic axons. It is suggested that parasympathetic NGF synthesis and its modulation by sympathetic innervation provides a molecular basis for establishment and maintenance of autonomic axo-axonal synaptic interactions.",
keywords = "Decentralization, Immunohistochemistry, In situ hybridization, Pterygopalatine ganglion, Rat, Sympathectomy",
author = "Wohaib Hasan and Smith, {Peter G.}",
year = "2000",
doi = "10.1046/j.0953-816X.2000.01353.x",
language = "English (US)",
volume = "12",
pages = "4391--4397",
journal = "European Journal of Neuroscience",
issn = "0953-816X",
publisher = "Wiley-Blackwell",
number = "12",

}

TY - JOUR

T1 - Nerve growth factor expression in parasympathetic neurons

T2 - Regulation by sympathetic innervation

AU - Hasan, Wohaib

AU - Smith, Peter G.

PY - 2000

Y1 - 2000

N2 - Interactions between sympathetic and parasympathetic nerves are important in regulating visceral target function. Sympathetic nerves are closely apposed to, and form functional synapses with, parasympathetic axons in many effector organs. The molecular mechanisms responsible for these structural and functional interactions are unknown. We explored the possibility that Nerve Growth Factor (NGF) synthesis by parasympathetic neurons provides a mechanism by which sympathetic-parasympathetic interactions are established. Parasympathetic pterygopalatine ganglia NGF-gene expression was examined by in situ hybridization and protein content assessed by immunohistochemistry. Under control conditions, NGF mRNA was present in ≈60% and NGF protein was in 40% of pterygopalatine parasympathetic neurons. Peripheral parasympathetic axons identified by vesicular acetylcholine transporter-immunoreactivity also displayed NGF immunoreactivity. To determine if sympathetic innervation regulates parasympathetic NGF expression, the ipsilateral superior cervical ganglion was excised. Thirty days postsympathectomy, the numbers of NGF mRNA-positive neurons were decreased to 38% and NGF immunoreactive neurons to 15%. This reduction was due to a loss of sympathetic nerve impulse activity, as similar reductions were achieved when superior cervical ganglia were deprived of preganglionic afferent input for 40 days. These findings provide evidence that normally NGF is synthesized by parasympathetic neurons and transported anterogradely to fibre terminals, where it may be available to sympathetic axons. Parasympathetic NGF expression, in turn, is augmented by impulse activity within (and presumably transmitter release from) sympathetic axons. It is suggested that parasympathetic NGF synthesis and its modulation by sympathetic innervation provides a molecular basis for establishment and maintenance of autonomic axo-axonal synaptic interactions.

AB - Interactions between sympathetic and parasympathetic nerves are important in regulating visceral target function. Sympathetic nerves are closely apposed to, and form functional synapses with, parasympathetic axons in many effector organs. The molecular mechanisms responsible for these structural and functional interactions are unknown. We explored the possibility that Nerve Growth Factor (NGF) synthesis by parasympathetic neurons provides a mechanism by which sympathetic-parasympathetic interactions are established. Parasympathetic pterygopalatine ganglia NGF-gene expression was examined by in situ hybridization and protein content assessed by immunohistochemistry. Under control conditions, NGF mRNA was present in ≈60% and NGF protein was in 40% of pterygopalatine parasympathetic neurons. Peripheral parasympathetic axons identified by vesicular acetylcholine transporter-immunoreactivity also displayed NGF immunoreactivity. To determine if sympathetic innervation regulates parasympathetic NGF expression, the ipsilateral superior cervical ganglion was excised. Thirty days postsympathectomy, the numbers of NGF mRNA-positive neurons were decreased to 38% and NGF immunoreactive neurons to 15%. This reduction was due to a loss of sympathetic nerve impulse activity, as similar reductions were achieved when superior cervical ganglia were deprived of preganglionic afferent input for 40 days. These findings provide evidence that normally NGF is synthesized by parasympathetic neurons and transported anterogradely to fibre terminals, where it may be available to sympathetic axons. Parasympathetic NGF expression, in turn, is augmented by impulse activity within (and presumably transmitter release from) sympathetic axons. It is suggested that parasympathetic NGF synthesis and its modulation by sympathetic innervation provides a molecular basis for establishment and maintenance of autonomic axo-axonal synaptic interactions.

KW - Decentralization

KW - Immunohistochemistry

KW - In situ hybridization

KW - Pterygopalatine ganglion

KW - Rat

KW - Sympathectomy

UR - http://www.scopus.com/inward/record.url?scp=0034502446&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0034502446&partnerID=8YFLogxK

U2 - 10.1046/j.0953-816X.2000.01353.x

DO - 10.1046/j.0953-816X.2000.01353.x

M3 - Article

C2 - 11122349

AN - SCOPUS:0034502446

VL - 12

SP - 4391

EP - 4397

JO - European Journal of Neuroscience

JF - European Journal of Neuroscience

SN - 0953-816X

IS - 12

ER -