Selective regulation of nerve growth factor expression in developing cutaneous tissue by early sensory innervation

<p>Abstract</p> <p>Background</p> <p>In the developing vertebrate peripheral nervous system, the survival of sympathetic neurons and the majority of sensory neurons depends on a supply of nerve growth factor (NGF) from tissues they innervate. Although neurotrophic theor...

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Main Authors: Vizard Tom N, Spori Bodo, Wyatt Sean L, Davies Alun M
Format: Article
Language:English
Published: BMC 2011-04-01
Series:Neural Development
Online Access:http://www.neuraldevelopment.com/content/6/1/18
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author Vizard Tom N
Spori Bodo
Wyatt Sean L
Davies Alun M
author_facet Vizard Tom N
Spori Bodo
Wyatt Sean L
Davies Alun M
author_sort Vizard Tom N
collection DOAJ
description <p>Abstract</p> <p>Background</p> <p>In the developing vertebrate peripheral nervous system, the survival of sympathetic neurons and the majority of sensory neurons depends on a supply of nerve growth factor (NGF) from tissues they innervate. Although neurotrophic theory presupposes, and the available evidence suggests, that the level of NGF expression is completely independent of innervation, the possibility that innervation may regulate the timing or level of NGF expression has not been rigorously investigated in a sufficiently well-characterized developing system.</p> <p>Results</p> <p>To address this important question, we studied the influence of innervation on the regulation of NGF mRNA expression in the embryonic mouse maxillary process <it>in vitro </it>and <it>in vivo</it>. The maxillary process receives its innervation from predominantly NGF-dependent sensory neurons of the trigeminal ganglion and is the most densely innervated cutaneous territory with the highest levels of NGF in the embryo. When early, uninnervated maxillary processes were cultured alone, the level of NGF mRNA rose more slowly than in maxillary processes cultured with attached trigeminal ganglia. In contrast to the positive influence of early innervation on NGF mRNA expression, the levels of brain-derived neurotrophic factor (BDNF) mRNA and neurotrophin-3 (NT3) mRNA rose to the same extent in early maxillary processes grown with and without trigeminal ganglia. The level of NGF mRNA, but not BDNF mRNA or NT3 mRNA, was also significantly lower in the maxillary processes of <it>erbB3</it><sup>-/- </sup>mice, which have substantially fewer trigeminal neurons than wild-type mice.</p> <p>Conclusions</p> <p>This selective effect of initial innervation on target field NGF mRNA expression provokes a re-evaluation of a key assertion of neurotrophic theory that the level of NGF expression is independent of innervation.</p>
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spelling doaj.art-e89defcdb39848ca862094f04b8fa4752022-12-22T02:49:02ZengBMCNeural Development1749-81042011-04-01611810.1186/1749-8104-6-18Selective regulation of nerve growth factor expression in developing cutaneous tissue by early sensory innervationVizard Tom NSpori BodoWyatt Sean LDavies Alun M<p>Abstract</p> <p>Background</p> <p>In the developing vertebrate peripheral nervous system, the survival of sympathetic neurons and the majority of sensory neurons depends on a supply of nerve growth factor (NGF) from tissues they innervate. Although neurotrophic theory presupposes, and the available evidence suggests, that the level of NGF expression is completely independent of innervation, the possibility that innervation may regulate the timing or level of NGF expression has not been rigorously investigated in a sufficiently well-characterized developing system.</p> <p>Results</p> <p>To address this important question, we studied the influence of innervation on the regulation of NGF mRNA expression in the embryonic mouse maxillary process <it>in vitro </it>and <it>in vivo</it>. The maxillary process receives its innervation from predominantly NGF-dependent sensory neurons of the trigeminal ganglion and is the most densely innervated cutaneous territory with the highest levels of NGF in the embryo. When early, uninnervated maxillary processes were cultured alone, the level of NGF mRNA rose more slowly than in maxillary processes cultured with attached trigeminal ganglia. In contrast to the positive influence of early innervation on NGF mRNA expression, the levels of brain-derived neurotrophic factor (BDNF) mRNA and neurotrophin-3 (NT3) mRNA rose to the same extent in early maxillary processes grown with and without trigeminal ganglia. The level of NGF mRNA, but not BDNF mRNA or NT3 mRNA, was also significantly lower in the maxillary processes of <it>erbB3</it><sup>-/- </sup>mice, which have substantially fewer trigeminal neurons than wild-type mice.</p> <p>Conclusions</p> <p>This selective effect of initial innervation on target field NGF mRNA expression provokes a re-evaluation of a key assertion of neurotrophic theory that the level of NGF expression is independent of innervation.</p>http://www.neuraldevelopment.com/content/6/1/18
spellingShingle Vizard Tom N
Spori Bodo
Wyatt Sean L
Davies Alun M
Selective regulation of nerve growth factor expression in developing cutaneous tissue by early sensory innervation
Neural Development
title Selective regulation of nerve growth factor expression in developing cutaneous tissue by early sensory innervation
title_full Selective regulation of nerve growth factor expression in developing cutaneous tissue by early sensory innervation
title_fullStr Selective regulation of nerve growth factor expression in developing cutaneous tissue by early sensory innervation
title_full_unstemmed Selective regulation of nerve growth factor expression in developing cutaneous tissue by early sensory innervation
title_short Selective regulation of nerve growth factor expression in developing cutaneous tissue by early sensory innervation
title_sort selective regulation of nerve growth factor expression in developing cutaneous tissue by early sensory innervation
url http://www.neuraldevelopment.com/content/6/1/18
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AT sporibodo selectiveregulationofnervegrowthfactorexpressionindevelopingcutaneoustissuebyearlysensoryinnervation
AT wyattseanl selectiveregulationofnervegrowthfactorexpressionindevelopingcutaneoustissuebyearlysensoryinnervation
AT daviesalunm selectiveregulationofnervegrowthfactorexpressionindevelopingcutaneoustissuebyearlysensoryinnervation