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

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

doi:10.1002/neu.20223

Cited by 53 publications

(48 citation statements)

References 62 publications

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“…depressants, which have effects on several molecular pathways including enhancing 5-HT levels in the synapse, have been shown to induce transcription (Thakker-Varia et al, 2001;Alder et al, 2003;Alfonso et al, 2005;Yamada and Higuchi, 2005;Ring et al, 2006). BDNF upregulates several classes of genes including synaptic vesicle proteins and neuropeptides (Thakker-Varia et al, 2001;Alder et al, 2005;Ring et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

“…BDNF upregulates several classes of genes including synaptic vesicle proteins and neuropeptides (Thakker-Varia et al, 2001;Alder et al, 2005;Ring et al, 2006). Neuropeptides known to be induced by BDNF include, among others, VGF, NPY, SP, and Nociceptin (Nawa et al, 1994;Eagleson et al, 2001;Alder et al, 2003;Ring et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

“…To begin to elucidate mechanisms of BDNF as an antidepressant, we examined the transcriptional regulation by 5-HT of BDNFinduced genes (Alder et al, 2003;Ring et al, 2006). Genes previously identified as BDNF-regulated were selected for this analysis based on their categorization as either immediate-early genes (IEGs), synapse-associated markers, or neuropeptides.…”

Section: -Ht Regulates a Subset Of Bdnf-induced Genes Through An Indmentioning

confidence: 99%

“…We successfully used transcriptional profiling after neurotrophin treatment to identify novel roles for genes in neuronal function (Thakker-Varia et al, 2001;Alder et al, 2003). Among the many classes of genes induced by BDNF, our studies reveal that synaptic vesicle proteins and neuropeptides are important regulators of hippocampal function (Thakker-Varia et al, 2001;Alder et al, 2003Alder et al, , 2005Ring et al, 2006). We recently discovered a role for the neuropeptide VGF in mediating synaptic activity of hippocampal cells (Alder et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

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The Neuropeptide VGF Produces Antidepressant-Like Behavioral Effects and Enhances Proliferation in the Hippocampus

Krol²,

et al. 2007

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Brain-derived neurotrophic factor (BDNF) is upregulated in the hippocampus by antidepressant treatments, and BDNF produces antidepressant-like effects in behavioral models of depression. In our previous work, we identified genes induced by BDNF and defined their specific roles in hippocampal neuronal development and plasticity. To identify genes downstream of BDNF that may play roles in psychiatric disorders, we examined a subset of BDNF-induced genes also regulated by 5-HT (serotonin), which includes the neuropeptide VGF (nonacronymic). To explore the function of VGF in depression, we first investigated the expression of the neuropeptide in animal models of depression. VGF was downregulated in the hippocampus after both the learned helplessness and forced swim test (FST) paradigms. Conversely, VGF infusion in the hippocampus of mice subjected to FST reduced the time spent immobile for up to 6 d, thus demonstrating a novel role for VGF as an antidepressant-like agent. Recent evidence indicates that chronic treatment of rodents with antidepressants increases neurogenesis in the adult dentate gyrus and that neurogenesis is required for the behavioral effects of antidepressants. Our studies using

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: -Ht Regulates a Subset Of Bdnf-induced Genes Through An Indmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

The Neuropeptide VGF Produces Antidepressant-Like Behavioral Effects and Enhances Proliferation in the Hippocampus

Krol²,

et al. 2007

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“…Recent studies show that all of these neurotrophic factors, except GDNF, positively modulate behavioral sensitization, whereas GDNF itself has a negative effect (Pierce and Bari, 2001). Both BDNF application to hippocampal cultures (Ring et al, 2006) and CNTF application to striatal cultures (Buzas et al, 1999) induce the expression of mRNA for N/OFQ, suggesting that endogenous N/OFQ could mediate the effect of these factors on behavioral sensitization. This possibility remains to be tested.…”

Section: Role Of Endogenous N/ofq In Behavioral Sensitizationmentioning

confidence: 99%

Endogenous Nociceptin (Orphanin FQ) Suppresses Basal Hedonic State and Acute Reward Responses to Methamphetamine and Ethanol, but Facilitates Chronic Responses

Sakoori

Murphy

2007

Neuropsychopharmacol

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The opioid peptide nociceptin (orphanin FQ) suppresses drug reward, drug self-administration, and impedes some of the processes believed to underlie the transition to addiction. As virtually all previous studies have used administration of nociceptin receptor agonists to evaluate the role of nociceptin on addiction-like behavior, the current study used a pharmacological (nociceptin receptor antagonist) and genetic (nociceptin receptor knockout mice) approach to elucidate the role of endogenous nociceptin. The nociceptin receptor antagonist UFP-101 induced a modest place preference, and enhanced the conditioned place preference induced by methamphetamine. In agreement with this, nociceptin receptor knockout mice had slightly enhanced methamphetamine and ethanol conditioned place preferences compared to wild-type mice. This effect did not appear to depend on differences in learning ability, as nociceptin receptor knockout mice had slightly weaker-conditioned place aversions to lithium chloride, the k-opioid receptor agonist, U50488H, and the general opiate antagonist, naloxone. The development of behavioral sensitization to methamphetamine was lower in nociceptin receptor knockout mice, and attenuated by UFP-101 administration to wild-type mice. Additionally, ethanol consumption and preference in a two-bottle choice test was lower in nociceptin receptor knockout mice, though ethanol-stimulated locomotion was stronger. Whereas the rewarding effect of methamphetamine and ethanol following chronic treatment, as measured by place conditioning, strengthened in wild-type mice, this effect was absent in nociceptin receptor knockout mice. These results suggest that endogenous N/OFQ suppresses basal and drug-stimulated increases in hedonic state, and plays either a permissive or facilitatory role in the development of addiction.

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Neuropeptide orphanin FQ inhibits dendritic morphogenesis through activation of RhoA

Alder

Kallman

Palmieri

et al. 2013

Developmental Neurobiology

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Brain-derived neurotrophic factor (BDNF) plays a facilitatory role in neuronal development and promotion of differentiation. Mechanisms that oppose BDNF's stimulatory effects create balance and regulate dendritic growth. However, these mechanisms have not been studied. We have focused our studies on the BDNF-induced neuropeptide OrphaninFQ/ Nociceptin (OFQ); while BDNF is known to enhance synaptic activity, OFQ has opposite effects on activity, learning, and memory. We have now examined whether OFQ provides a balance to the stimulatory effects of BDNF on neuronal differentiation in the hippocampus. Golgi staining in OFQ knockout (KO) mice revealed an increase in primary dendrite length as well as spine density, suggesting that endogenous OFQ inhibits dendritic morphology. We have also used cultured hippocampal neurons to demonstrate that exogenous OFQ has an inhibitory effect on dendritic growth and that the neuropeptide alters the response to BDNF when pre-administered. To determine if BDNF and OFQ act in a feedback loop, we inhibited the actions of the BDNF and OFQ receptors, TrkB and NOP using ANA-12 and NOP KO mice respectively but our data suggest that the two factors do not act in a negative feedback loop. We found that the inhibition of dendritic morphology induced by OFQ is via enhanced RhoA activity. Finally, we have evidence that RhoA activation is required for the inhibitory effects of OFQ on dendritic morphology. Our results reveal basic mechanisms by which neurons not only regulate the formation of proper dendritic growth during development but also control plasticity in the mature nervous system.

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

Cited by 53 publications

References 62 publications

The Neuropeptide VGF Produces Antidepressant-Like Behavioral Effects and Enhances Proliferation in the Hippocampus

The Neuropeptide VGF Produces Antidepressant-Like Behavioral Effects and Enhances Proliferation in the Hippocampus

Endogenous Nociceptin (Orphanin FQ) Suppresses Basal Hedonic State and Acute Reward Responses to Methamphetamine and Ethanol, but Facilitates Chronic Responses

Neuropeptide orphanin FQ inhibits dendritic morphogenesis through activation of RhoA

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