Anti-interleukin-1β antibody prevents the occurrence of repeated restraint stress-induced alterations in synaptic transmission and long-term potentiation in the rat frontal cortex

Bobula, Bartosz; Sowa, Joanna; Hess, Grzegorz

doi:10.1016/j.pharep.2014.08.011

Cited by 12 publications

(14 citation statements)

References 42 publications

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“…It has been proposed that the reduced excitatory synaptic transmission in both hippocampus- and PFC-NAcc pathways, leading to a dysfunction of corticomesolimbic reward circuitry that underlies many of the symptoms of depression. 72 Consistently, optogenetic activation of the PFC-NAcc pathway inhibits neuropathic pain and the affective symptoms produced by SNI. 73 Several lines of evidence show that proinflammatory cytokines, including IL-1β and TNF-α, regulate synaptic strength also in a region-dependent manner.…”

Section: Discussionmentioning

confidence: 95%

“…69 The synaptic connection in this pathway is reduced by SNI. 70 In contrast, SNI potentiates the synaptic transmission between parabrachial nucleus-central nucleus of amygdala 71 and PFC, 69 leading to memory deficit and depressive behaviors. It has been proposed that the reduced excitatory synaptic transmission in both hippocampus-and PFC-NAcc pathways, leading to a dysfunction of corticomesolimbic reward circuitry that underlies many of the symptoms of depression.…”

Section: Il-1 Mechanism Of Mirror Pain After Snimentioning

confidence: 99%

“…76,77 While the cytokines at pathological concentration inhibit LTP in hippocampus [78][79][80] and in frontal cortex. 70 Taken together, peripheral nerve injury and the resultant upregulation of IL-1b may lead to the neuropathic pain, memory deficit, and depression-like behavior via the region-dependent changes in synaptic strength. As neuropathic pain was dissociated with STMD and depression-like behavior in SNI and IL-1b injected rats, we proposed that the changes of synaptic connections in different regions may be variable in a given animals.…”

Section: Il-1 Mechanism Of Mirror Pain After Snimentioning

confidence: 99%

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Interleukin-1β overproduction is a common cause for neuropathic pain, memory deficit, and depression following peripheral nerve injury in rodents

Gui

Xiao²,

Lin³

et al. 2016

Mol Pain

165

134

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BackgroundChronic pain is often accompanied by short-term memory deficit and depression. Currently, it is believed that short-term memory deficit and depression are consequences of chronic pain. Here, we test the hypothesis that the symptoms might be caused by overproduction of interleukin-1beta (IL-1β) in the injured nerve independent of neuropathic pain following spared nerve injury in rats and mice.ResultsMechanical allodynia, a behavioral sign of neuropathic pain, was not correlated with short-term memory deficit and depressive behavior in spared nerve injury rats. Spared nerve injury upregulated IL-1β in the injured sciatic nerve, plasma, and the regions in central nervous system closely associated with pain, memory and emotion, including spinal dorsal horn, hippocampus, prefrontal cortex, nucleus accumbens, and amygdala. Importantly, the spared nerve injury-induced memory deficits, depressive, and pain behaviors were substantially prevented by peri-sciatic administration of IL-1β neutralizing antibody in rats or deletion of IL-1 receptor type 1 in mice. Furthermore, the behavioral abnormalities induced by spared nerve injury were mimicked in naïve rats by repetitive intravenous injection of re combinant rat IL-1β (rrIL-1β) at a pathological concentration as determined from spared nerve injury rats. In addition, microglia were activated by both spared nerve injury and intravenous injection of rrIL-1β and the effect of spared nerve injury was substantially reversed by peri-sciatic administration of anti-IL-1β.ConclusionsNeuropathic pain was not necessary for the development of cognitive and emotional disorders, while the overproduction of IL-1β in the injured sciatic nerve following peripheral nerve injury may be a common mechanism underlying the generation of neuropathic pain, memory deficit, and depression.

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Section: Discussionmentioning

confidence: 95%

Section: Il-1 Mechanism Of Mirror Pain After Snimentioning

confidence: 99%

Section: Il-1 Mechanism Of Mirror Pain After Snimentioning

confidence: 99%

See 1 more Smart Citation

Interleukin-1β overproduction is a common cause for neuropathic pain, memory deficit, and depression following peripheral nerve injury in rodents

Gui

Xiao²,

Lin³

et al. 2016

Mol Pain

165

134

View full text Add to dashboard Cite

show abstract

“…Proving the pivotal role of microglia in vivo, for example, is challenging, as depletion of microglia, or inhibition of activation, may also target invading peripheral immune cells [30]. Similarly, whilst there are reports of increased IL1β production in the hippocampus after microglial activation [15, 16, 18, 19, 23], determining whether such a change is directly responsible for synaptic deficits is complicated by difficulty in targeting IL1β antagonising drugs or neutralising antibodies to the brain and maintaining their levels [31, 32]. As such, many studies seek to explore proposed mechanisms using primary culture models.…”

Section: Introductionmentioning

confidence: 99%

Lipopolysaccharide-induced neuroinflammation induces presynaptic disruption through a direct action on brain tissue involving microglia-derived interleukin 1 beta

Sheppard

Coleman

Durrant

2019

J Neuroinflammation

114

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Background Systemic inflammation has been linked to synapse loss and cognitive decline in human patients and animal models. A role for microglial release of pro-inflammatory cytokines has been proposed based on in vivo and primary culture studies. However, mechanisms are hard to study in vivo as specific microglial ablation is challenging and the extracellular fluid cannot be sampled without invasive methods. Primary cultures have different limitations as the intricate multicellular architecture in the brain is not fully reproduced. It is essential to confirm proposed brain-specific mechanisms of inflammatory synapse loss directly in brain tissue. Organotypic hippocampal slice cultures (OHSCs) retain much of the in vivo neuronal architecture, synaptic connections and diversity of cell types whilst providing convenient access to manipulate and sample the culture medium and observe cellular reactions. Methods OHSCs were generated from P6-P9 C57BL/6 mice. Inflammation was induced via addition of lipopolysaccharide (LPS), and cultures were analysed for changes in synaptic proteins, gene expression and protein secretion. Microglia were selectively depleted using clodronate, and the effect of IL1β was assessed using a specific neutralising monoclonal antibody. Results LPS treatment induced loss of the presynaptic protein synaptophysin without altering PSD95 or Aβ protein levels. Depletion of microglia prior to LPS application prevented the loss of synaptophysin, whilst microglia depletion after the inflammatory insult was partially effective, although less so than pre-emptive treatment, indicating a time-critical window in which microglia can induce synaptic damage. IL1β protein and mRNA were increased after LPS addition, with these effects also prevented by microglia depletion. Direct application of IL1β to OHSCs resulted in synaptophysin loss whilst pre-treatment with IL1β neutralising antibody prior to LPS addition prevented a significant loss of synaptophysin but may also impact basal synaptic levels. Conclusions The loss of synaptophysin in this system confirms LPS can act directly within brain tissue to disrupt synapses, and we show that microglia are the relevant cellular target when all major CNS cell types are present. By overcoming limitations of primary culture and in vivo work, our study strengthens the evidence for a key role of microglia-derived IL1β in synaptic dysfunction after inflammatory insult. Electronic supplementary material The online version of this article (10.1186/s12974-019-1490-8) contains supplementary material, which is available to authorized users.

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“…In "uninjured" brain, when pro and anti-inflammatory cytokines are expressed at low basal levels, they serve essential physiological role in the regulation of bidirectional glioneuronal communication and in modulation of synaptic plasticity [44,46]. The final downstream effect of cytokines on plasticity and neuronal survival depends on their synaptic concentration.…”

Section: Neuroinflammationmentioning

confidence: 99%

Disruption of Neurosynaptic Physiology and Neuron Network Dysfunction in Brain Disorders: An Environmental and Occupational Health Perspective

Pandey¹

2017

AND

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Networks of signaling cascades regulate synaptic transmission and morphology. Signaling molecules and their dynamics are subject to impact of environmental insults as well as genes predisposing to disease risks. Pollutants may impact brain through cellular, molecular and inflammatory pathways, causing direct damage or predisposing to damage by other insults, leading to diseases. Disruptions in structure and function of neurotransmission elements and protein networks contribute to pathogenesis of neuropsychiatric diseases. Different affected brain regions and/or synaptic connections between excitatory and inhibitory neurons charecterise specific clinical states. Functional identification of synaptic signaling networks and specific neuronal pathways would facilitate understanding of specific pathomechanisms relevant to preventive and corrective interventions. Physiology of neural networks and pathogenesis, therapeutics and prevention of diseases arising of their disruption, specially with environmental afflictions, deserve holistic and not fragmentary understanding. Present article attempts to present such diverse information with possible coherence to emphasize necessary address in contemporary medical teaching and continuing education for young researchers. The mounting challenge of prevention and management of pollution inflicted disruption of neurophysiology associated with brain dysfunction and diseases in contemporary world may be better addressed by integrated interdisciplinary understanding of the problems.

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Anti-interleukin-1β antibody prevents the occurrence of repeated restraint stress-induced alterations in synaptic transmission and long-term potentiation in the rat frontal cortex

Abstract: These data point to an involvement of peripherally produced IL-1β in mediating the influence of repeated restraint stress on the functions of the frontal cortex.

Cited by 12 publications

References 42 publications

Interleukin-1β overproduction is a common cause for neuropathic pain, memory deficit, and depression following peripheral nerve injury in rodents

Interleukin-1β overproduction is a common cause for neuropathic pain, memory deficit, and depression following peripheral nerve injury in rodents

Lipopolysaccharide-induced neuroinflammation induces presynaptic disruption through a direct action on brain tissue involving microglia-derived interleukin 1 beta

Disruption of Neurosynaptic Physiology and Neuron Network Dysfunction in Brain Disorders: An Environmental and Occupational Health Perspective

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