Short increase of BDNF messenger RNA triggers kainic acid-induced neuronal hypertrophy in adult mice

Neurotrophin gene expression in adult brain varies according to physiological activity and following brain injury, suggesting a role in neuronal maintenance and plasticity. However, the exact roles and mechanisms of action of neurotrophins in the adult brain are still poorly understood. We have rece...

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Veröffentlicht in:Neuroscience 1996-06, Vol.72 (4), p.923-931
Hauptverfasser: Guilhem, D., Dreyfus, P.A., Makiura, Y., Suzuki, F., Onteniente, B.
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Dreyfus, P.A.
Makiura, Y.
Suzuki, F.
Onteniente, B.
description Neurotrophin gene expression in adult brain varies according to physiological activity and following brain injury, suggesting a role in neuronal maintenance and plasticity. However, the exact roles and mechanisms of action of neurotrophins in the adult brain are still poorly understood. We have recently demonstrated that neurons of the adult mouse dentate gyrus can develop a conspicuous morphogenetic response to intrahippocampal injection of kainic acid. This response is correlated with long-lasting overexpression of the brain-derived neurotrophic factor gene, suggesting a causal relationship between molecular and structural changes. To test this hypothesis, brain-derived neurotrophic factor messenger RNA were sequestered in vivo by administration of antisense oligodeoxynucleotides. When administered before 20 h post-kainate, antisense oligodeoxynucleotides totally prevented the kainate-induced neuronal hypertrophy, while sense or missense sequences had no effect. On the other hand, the hypertrophic response was observed when antisense administration was begun 24 h post-kainate, indicating an involvement of brain-derived neurotrophic factor messenger RNA in the initiation of structural changes, but not in their evolution. The hypertrophy was blocked by inhibition of tyrosine kinase activities by K252a, suggesting an involvement of Trk high affinity receptors. Administration of human recombinant brain-derived neurotrophic factor without previous treatment by kainate failed to induce any morphogenetic response. These results show that a short activation of the brain-derived neurotrophic factor gene can, in association with neuronal activation by kainate, trigger dramatic and long-lasting morphological changes in adult neurons. A physiological role of brain-derived neurotrophic factor in adult brain could therefore be to link, by autocrine/paracrine action, activation of glutamate receptors and neuronal morphological adaptive responses.
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On the other hand, the hypertrophic response was observed when antisense administration was begun 24 h post-kainate, indicating an involvement of brain-derived neurotrophic factor messenger RNA in the initiation of structural changes, but not in their evolution. The hypertrophy was blocked by inhibition of tyrosine kinase activities by K252a, suggesting an involvement of Trk high affinity receptors. Administration of human recombinant brain-derived neurotrophic factor without previous treatment by kainate failed to induce any morphogenetic response. These results show that a short activation of the brain-derived neurotrophic factor gene can, in association with neuronal activation by kainate, trigger dramatic and long-lasting morphological changes in adult neurons. 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On the other hand, the hypertrophic response was observed when antisense administration was begun 24 h post-kainate, indicating an involvement of brain-derived neurotrophic factor messenger RNA in the initiation of structural changes, but not in their evolution. The hypertrophy was blocked by inhibition of tyrosine kinase activities by K252a, suggesting an involvement of Trk high affinity receptors. Administration of human recombinant brain-derived neurotrophic factor without previous treatment by kainate failed to induce any morphogenetic response. These results show that a short activation of the brain-derived neurotrophic factor gene can, in association with neuronal activation by kainate, trigger dramatic and long-lasting morphological changes in adult neurons. 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Psychology</topic><topic>hippocampus</topic><topic>Hypertrophy</topic><topic>Indole Alkaloids</topic><topic>Injections, Intraventricular</topic><topic>Kainic Acid - pharmacology</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>mouse</topic><topic>Nerve Growth Factors - genetics</topic><topic>neuronal plasticity</topic><topic>Neuronal Plasticity - drug effects</topic><topic>Neurons - drug effects</topic><topic>Neurons - pathology</topic><topic>neurotrophin</topic><topic>Oligonucleotides, Antisense - pharmacology</topic><topic>Recombinant Proteins - pharmacology</topic><topic>RNA, Messenger - metabolism</topic><topic>Vertebrates: nervous system and sense organs</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Guilhem, D.</creatorcontrib><creatorcontrib>Dreyfus, P.A.</creatorcontrib><creatorcontrib>Makiura, Y.</creatorcontrib><creatorcontrib>Suzuki, F.</creatorcontrib><creatorcontrib>Onteniente, B.</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Guilhem, D.</au><au>Dreyfus, P.A.</au><au>Makiura, Y.</au><au>Suzuki, F.</au><au>Onteniente, B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Short increase of BDNF messenger RNA triggers kainic acid-induced neuronal hypertrophy in adult mice</atitle><jtitle>Neuroscience</jtitle><addtitle>Neuroscience</addtitle><date>1996-06-01</date><risdate>1996</risdate><volume>72</volume><issue>4</issue><spage>923</spage><epage>931</epage><pages>923-931</pages><issn>0306-4522</issn><eissn>1873-7544</eissn><coden>NRSCDN</coden><abstract>Neurotrophin gene expression in adult brain varies according to physiological activity and following brain injury, suggesting a role in neuronal maintenance and plasticity. However, the exact roles and mechanisms of action of neurotrophins in the adult brain are still poorly understood. We have recently demonstrated that neurons of the adult mouse dentate gyrus can develop a conspicuous morphogenetic response to intrahippocampal injection of kainic acid. This response is correlated with long-lasting overexpression of the brain-derived neurotrophic factor gene, suggesting a causal relationship between molecular and structural changes. To test this hypothesis, brain-derived neurotrophic factor messenger RNA were sequestered in vivo by administration of antisense oligodeoxynucleotides. When administered before 20 h post-kainate, antisense oligodeoxynucleotides totally prevented the kainate-induced neuronal hypertrophy, while sense or missense sequences had no effect. On the other hand, the hypertrophic response was observed when antisense administration was begun 24 h post-kainate, indicating an involvement of brain-derived neurotrophic factor messenger RNA in the initiation of structural changes, but not in their evolution. The hypertrophy was blocked by inhibition of tyrosine kinase activities by K252a, suggesting an involvement of Trk high affinity receptors. Administration of human recombinant brain-derived neurotrophic factor without previous treatment by kainate failed to induce any morphogenetic response. These results show that a short activation of the brain-derived neurotrophic factor gene can, in association with neuronal activation by kainate, trigger dramatic and long-lasting morphological changes in adult neurons. 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source MEDLINE; Elsevier ScienceDirect Journals Complete
subjects adult brain
Anatomy
Animals
Biological and medical sciences
Brain-Derived Neurotrophic Factor - genetics
Carbazoles - pharmacology
Central nervous system
Dentate Gyrus - pathology
Enzyme Inhibitors - pharmacology
Excitatory Amino Acid Agonists - pharmacology
Fundamental and applied biological sciences. Psychology
hippocampus
Hypertrophy
Indole Alkaloids
Injections, Intraventricular
Kainic Acid - pharmacology
Male
Mice
Mice, Inbred C57BL
mouse
Nerve Growth Factors - genetics
neuronal plasticity
Neuronal Plasticity - drug effects
Neurons - drug effects
Neurons - pathology
neurotrophin
Oligonucleotides, Antisense - pharmacology
Recombinant Proteins - pharmacology
RNA, Messenger - metabolism
Vertebrates: nervous system and sense organs
title Short increase of BDNF messenger RNA triggers kainic acid-induced neuronal hypertrophy in adult mice
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