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Nerve Growth Factor Treatment Increases Brain-Derived Neurotrophic Factor Selectively in TrkA-Expressing Dorsal Root Ganglion Cells and in Their Central Terminations within the Spinal Cord

Using immunocytochemistry and in situ hybridization, we have examined the expression of brain-derived neurotrophic factor (BDNF) and of neurotrophin receptors in dorsal root ganglion cells. In the adult rat, BDNF mRNA and protein were found mainly in the subpopulation of cells that express the nerve...

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Published in:The Journal of neuroscience 1997-11, Vol.17 (21), p.8476-8490
Main Authors: Michael, G. J, Averill, S, Nitkunan, A, Rattray, M, Bennett, D. L. H, Yan, Q, Priestley, J. V
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Priestley, J. V
description Using immunocytochemistry and in situ hybridization, we have examined the expression of brain-derived neurotrophic factor (BDNF) and of neurotrophin receptors in dorsal root ganglion cells. In the adult rat, BDNF mRNA and protein were found mainly in the subpopulation of cells that express the nerve growth factor (NGF) receptor trkA and the neuropeptide calcitonin gene-related peptide (CGRP). NGF increased BDNF within the trkA/CGRP cells to the extent that almost 90% of trkA cells contained BDNF mRNA after intrathecal NGF treatment, and 80-90% of BDNF-expressing cells contained trkA. Non-trkA cells that expressed BDNF included some trkC cells and some small cells that labeled with the lectin Griffonia simplicifolia IB4, a marker for cells that do not express trks. However, very few trkB cells expressed either BDNF mRNA or protein, and NGF did not increase BDNF expression in non-trkA cells. BDNF protein was anterogradely transported both peripherally and centrally. The central transport resulted in BDNF immunoreactivity in CGRP containing terminal arbors in the dorsal horn of the spinal cord, and this immunoreactivity was increased by NGF treatment. Electron microscopic analysis revealed that the BDNF immunoreactivity was present in finely myelinated and unmyelinated axons and in axon terminals, where it was most concentrated over dense-cored vesicles. Our data do not support an autocrine or paracrine role for BDNF within normal dorsal root ganglia, but indicate that BDNF may act as an anterograde trophic messenger. NGF levels in the periphery could influence dorsal horn neurons via release of BDNF from primary afferents.
doi_str_mv 10.1523/jneurosci.17-21-08476.1997
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J ; Averill, S ; Nitkunan, A ; Rattray, M ; Bennett, D. L. H ; Yan, Q ; Priestley, J. V</creator><creatorcontrib>Michael, G. J ; Averill, S ; Nitkunan, A ; Rattray, M ; Bennett, D. L. H ; Yan, Q ; Priestley, J. V</creatorcontrib><description>Using immunocytochemistry and in situ hybridization, we have examined the expression of brain-derived neurotrophic factor (BDNF) and of neurotrophin receptors in dorsal root ganglion cells. In the adult rat, BDNF mRNA and protein were found mainly in the subpopulation of cells that express the nerve growth factor (NGF) receptor trkA and the neuropeptide calcitonin gene-related peptide (CGRP). NGF increased BDNF within the trkA/CGRP cells to the extent that almost 90% of trkA cells contained BDNF mRNA after intrathecal NGF treatment, and 80-90% of BDNF-expressing cells contained trkA. Non-trkA cells that expressed BDNF included some trkC cells and some small cells that labeled with the lectin Griffonia simplicifolia IB4, a marker for cells that do not express trks. However, very few trkB cells expressed either BDNF mRNA or protein, and NGF did not increase BDNF expression in non-trkA cells. BDNF protein was anterogradely transported both peripherally and centrally. The central transport resulted in BDNF immunoreactivity in CGRP containing terminal arbors in the dorsal horn of the spinal cord, and this immunoreactivity was increased by NGF treatment. Electron microscopic analysis revealed that the BDNF immunoreactivity was present in finely myelinated and unmyelinated axons and in axon terminals, where it was most concentrated over dense-cored vesicles. Our data do not support an autocrine or paracrine role for BDNF within normal dorsal root ganglia, but indicate that BDNF may act as an anterograde trophic messenger. NGF levels in the periphery could influence dorsal horn neurons via release of BDNF from primary afferents.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/jneurosci.17-21-08476.1997</identifier><identifier>PMID: 9334420</identifier><language>eng</language><publisher>United States: Soc Neuroscience</publisher><subject>Afferent Pathways - metabolism ; Animals ; Axonal Transport ; Brain-Derived Neurotrophic Factor - biosynthesis ; Brain-Derived Neurotrophic Factor - genetics ; Calcitonin Gene-Related Peptide - analysis ; Fluorescent Antibody Technique, Indirect ; Ganglia, Spinal - drug effects ; Ganglia, Spinal - metabolism ; Gene Expression Regulation - drug effects ; In Situ Hybridization, Fluorescence ; Injections, Intraperitoneal ; Injections, Spinal ; Male ; Microscopy, Electron ; Nerve Growth Factors - administration &amp; dosage ; Nerve Growth Factors - pharmacology ; Nerve Tissue Proteins - biosynthesis ; Nerve Tissue Proteins - genetics ; Proto-Oncogene Proteins - biosynthesis ; Proto-Oncogene Proteins - genetics ; Rats ; Rats, Wistar ; Receptor Protein-Tyrosine Kinases - analysis ; Receptor Protein-Tyrosine Kinases - biosynthesis ; Receptor Protein-Tyrosine Kinases - genetics ; Receptor, Ciliary Neurotrophic Factor ; Receptor, trkA ; Receptor, trkC ; Receptors, Nerve Growth Factor - analysis ; Receptors, Nerve Growth Factor - biosynthesis ; Receptors, Nerve Growth Factor - genetics ; RNA, Messenger - biosynthesis ; RNA, Messenger - genetics ; Spinal Cord - metabolism ; Stimulation, Chemical</subject><ispartof>The Journal of neuroscience, 1997-11, Vol.17 (21), p.8476-8490</ispartof><rights>Copyright © 1997 Society for Neuroscience 1997</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c509t-18a435f69d72960e1d29e32ed5d8c0cbe3aacd9b3b2fa758a68f4259bf33fa773</citedby><cites>FETCH-LOGICAL-c509t-18a435f69d72960e1d29e32ed5d8c0cbe3aacd9b3b2fa758a68f4259bf33fa773</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6573719/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6573719/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/9334420$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Michael, G. J</creatorcontrib><creatorcontrib>Averill, S</creatorcontrib><creatorcontrib>Nitkunan, A</creatorcontrib><creatorcontrib>Rattray, M</creatorcontrib><creatorcontrib>Bennett, D. L. H</creatorcontrib><creatorcontrib>Yan, Q</creatorcontrib><creatorcontrib>Priestley, J. V</creatorcontrib><title>Nerve Growth Factor Treatment Increases Brain-Derived Neurotrophic Factor Selectively in TrkA-Expressing Dorsal Root Ganglion Cells and in Their Central Terminations within the Spinal Cord</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>Using immunocytochemistry and in situ hybridization, we have examined the expression of brain-derived neurotrophic factor (BDNF) and of neurotrophin receptors in dorsal root ganglion cells. In the adult rat, BDNF mRNA and protein were found mainly in the subpopulation of cells that express the nerve growth factor (NGF) receptor trkA and the neuropeptide calcitonin gene-related peptide (CGRP). 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V</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Nerve Growth Factor Treatment Increases Brain-Derived Neurotrophic Factor Selectively in TrkA-Expressing Dorsal Root Ganglion Cells and in Their Central Terminations within the Spinal Cord</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>1997-11-01</date><risdate>1997</risdate><volume>17</volume><issue>21</issue><spage>8476</spage><epage>8490</epage><pages>8476-8490</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>Using immunocytochemistry and in situ hybridization, we have examined the expression of brain-derived neurotrophic factor (BDNF) and of neurotrophin receptors in dorsal root ganglion cells. In the adult rat, BDNF mRNA and protein were found mainly in the subpopulation of cells that express the nerve growth factor (NGF) receptor trkA and the neuropeptide calcitonin gene-related peptide (CGRP). NGF increased BDNF within the trkA/CGRP cells to the extent that almost 90% of trkA cells contained BDNF mRNA after intrathecal NGF treatment, and 80-90% of BDNF-expressing cells contained trkA. Non-trkA cells that expressed BDNF included some trkC cells and some small cells that labeled with the lectin Griffonia simplicifolia IB4, a marker for cells that do not express trks. However, very few trkB cells expressed either BDNF mRNA or protein, and NGF did not increase BDNF expression in non-trkA cells. BDNF protein was anterogradely transported both peripherally and centrally. The central transport resulted in BDNF immunoreactivity in CGRP containing terminal arbors in the dorsal horn of the spinal cord, and this immunoreactivity was increased by NGF treatment. Electron microscopic analysis revealed that the BDNF immunoreactivity was present in finely myelinated and unmyelinated axons and in axon terminals, where it was most concentrated over dense-cored vesicles. Our data do not support an autocrine or paracrine role for BDNF within normal dorsal root ganglia, but indicate that BDNF may act as an anterograde trophic messenger. NGF levels in the periphery could influence dorsal horn neurons via release of BDNF from primary afferents.</abstract><cop>United States</cop><pub>Soc Neuroscience</pub><pmid>9334420</pmid><doi>10.1523/jneurosci.17-21-08476.1997</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record>
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source PubMed Central
subjects Afferent Pathways - metabolism
Animals
Axonal Transport
Brain-Derived Neurotrophic Factor - biosynthesis
Brain-Derived Neurotrophic Factor - genetics
Calcitonin Gene-Related Peptide - analysis
Fluorescent Antibody Technique, Indirect
Ganglia, Spinal - drug effects
Ganglia, Spinal - metabolism
Gene Expression Regulation - drug effects
In Situ Hybridization, Fluorescence
Injections, Intraperitoneal
Injections, Spinal
Male
Microscopy, Electron
Nerve Growth Factors - administration & dosage
Nerve Growth Factors - pharmacology
Nerve Tissue Proteins - biosynthesis
Nerve Tissue Proteins - genetics
Proto-Oncogene Proteins - biosynthesis
Proto-Oncogene Proteins - genetics
Rats
Rats, Wistar
Receptor Protein-Tyrosine Kinases - analysis
Receptor Protein-Tyrosine Kinases - biosynthesis
Receptor Protein-Tyrosine Kinases - genetics
Receptor, Ciliary Neurotrophic Factor
Receptor, trkA
Receptor, trkC
Receptors, Nerve Growth Factor - analysis
Receptors, Nerve Growth Factor - biosynthesis
Receptors, Nerve Growth Factor - genetics
RNA, Messenger - biosynthesis
RNA, Messenger - genetics
Spinal Cord - metabolism
Stimulation, Chemical
title Nerve Growth Factor Treatment Increases Brain-Derived Neurotrophic Factor Selectively in TrkA-Expressing Dorsal Root Ganglion Cells and in Their Central Terminations within the Spinal Cord
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