Transcriptional profiling of brain-derived-neurotrophic factor-induced neuronal plasticity: A novel role for nociceptin in hippocampal neurite outgrowth

Robert H. Ring, Janet Alder Suss, Myles Fennell, Evguenia Kouranova, Ira B. Black, Smita Varia

Research output: Contribution to journalArticle

39 Citations (Scopus)

Abstract

Brain derived neurotrophic factor (BDNF) exhibits a sequence of actions on neurons ranging from acute enhancement of transmission to long-term promotion of neurite outgrowth and synaptogenesis associated with learning and memory. The manifold effects of BDNF on neuronal modifications may be mediated by genomic alterations. We previously found that BDNF treatment acutely increases transcription of the synaptic vesicle protein Rab3A, required for trophin-induced synaptic plasticity, as well as the peptide VGF, which increases during learning. To elucidate comprehensive transcriptional programs associated with short- and long-term BDNF exposure, we now examine mRNA abundance and complexity using Affymetrix GeneChips in cultured hippocampal neurons. Consistent with the modulation of synaptic plasticity, BDNF treatment (3-6 h) induced mRNAs encoding the synapse-associated proteins synaptojanin 2, neuronal pentraxin 1, septin 9, and ryanodine receptor 2. BDNF also induced expression of mRNAs encoding neuropeptides (6-12 h), including prepronociceptin, neuropeptide Y, and secretogranin. To determine whether these neuropeptides induced by BDNF mediate neuronal development, we examined their effects on hippocampal neurons. The four mature peptides derived from post-translational processing of the ppNociceptin propeptide induced the expression of several immediate early genes in hippocampal cultures, indicating neuronal activation. To examine the significance of activation, the effects of nociceptin (orphanin FQ) and nocistatin on neurite outgrowth were examined. Quantitative morphometric analysis revealed that nociceptin significantly increased both average neurite length and average number of neurites per neuron, while nocistatin had no effect on these parameters. These results reveal a novel role for nociceptin and suggest that these neuropeptide systems may contribute to the regulation of neuronal function by BDNF.

Original languageEnglish (US)
Pages (from-to)361-377
Number of pages17
JournalJournal of Neurobiology
Volume66
Issue number4
DOIs
StatePublished - Mar 1 2006

Fingerprint

Neuronal Plasticity
Brain-Derived Neurotrophic Factor
Neuropeptides
Neurons
Neurites
Messenger RNA
rab3A GTP-Binding Protein
Septins
Learning
Chromogranins
Ryanodine Receptor Calcium Release Channel
Immediate-Early Genes
nociceptin
Neuronal Outgrowth
Synaptic Vesicles
Neuropeptide Y
Synapses
Peptides

All Science Journal Classification (ASJC) codes

  • Cellular and Molecular Neuroscience
  • Neuroscience(all)

Keywords

  • BDNF
  • Microarray
  • Neurite outgrowth
  • Nociceptin
  • Synaptic plasticity

Cite this

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abstract = "Brain derived neurotrophic factor (BDNF) exhibits a sequence of actions on neurons ranging from acute enhancement of transmission to long-term promotion of neurite outgrowth and synaptogenesis associated with learning and memory. The manifold effects of BDNF on neuronal modifications may be mediated by genomic alterations. We previously found that BDNF treatment acutely increases transcription of the synaptic vesicle protein Rab3A, required for trophin-induced synaptic plasticity, as well as the peptide VGF, which increases during learning. To elucidate comprehensive transcriptional programs associated with short- and long-term BDNF exposure, we now examine mRNA abundance and complexity using Affymetrix GeneChips in cultured hippocampal neurons. Consistent with the modulation of synaptic plasticity, BDNF treatment (3-6 h) induced mRNAs encoding the synapse-associated proteins synaptojanin 2, neuronal pentraxin 1, septin 9, and ryanodine receptor 2. BDNF also induced expression of mRNAs encoding neuropeptides (6-12 h), including prepronociceptin, neuropeptide Y, and secretogranin. To determine whether these neuropeptides induced by BDNF mediate neuronal development, we examined their effects on hippocampal neurons. The four mature peptides derived from post-translational processing of the ppNociceptin propeptide induced the expression of several immediate early genes in hippocampal cultures, indicating neuronal activation. To examine the significance of activation, the effects of nociceptin (orphanin FQ) and nocistatin on neurite outgrowth were examined. Quantitative morphometric analysis revealed that nociceptin significantly increased both average neurite length and average number of neurites per neuron, while nocistatin had no effect on these parameters. These results reveal a novel role for nociceptin and suggest that these neuropeptide systems may contribute to the regulation of neuronal function by BDNF.",
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Transcriptional profiling of brain-derived-neurotrophic factor-induced neuronal plasticity : A novel role for nociceptin in hippocampal neurite outgrowth. / Ring, Robert H.; Suss, Janet Alder; Fennell, Myles; Kouranova, Evguenia; Black, Ira B.; Varia, Smita.

In: Journal of Neurobiology, Vol. 66, No. 4, 01.03.2006, p. 361-377.

Research output: Contribution to journalArticle

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