Peripheral nerve injury evokes disabilities and sensory dysfunction in a subpopulation of rats: a closer model to human chronic neuropathic pain?

Keay, Kevin A.; Monassi, Claudia Regina; Levison, Dane B.; Bandler, Richard

doi:10.1016/j.neulet.2003.12.010

Cited by 43 publications

(16 citation statements)

References 19 publications

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“…Experimental manipulations of rat sciatic nerve by chronic constriction injury (CCI) 24, 25 and its variant sciatic nerve entrapment (SNE) injury 26–28 have been shown to induce a painful neuropathy in the ipsilateral hindpaw. The intact DRG and nerve proximal to the site of constriction/entrapment provide a convenient model for molecular biological experiments.…”

Section: Resultsmentioning

confidence: 99%

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Aberrant plasticity of peripheral sensory axons in a painful neuropathy

Hirai

Mulpuri

Cheng

et al. 2017

Sci Rep

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Neuronal cells express considerable plasticity responding to environmental cues, in part, through subcellular mRNA regulation. Here we report on the extensive changes in distribution of mRNAs in the cell body and axon compartments of peripheral sensory neurons and the 3′ untranslated region (3′UTR) landscapes after unilateral sciatic nerve entrapment (SNE) injury in rats. Neuronal cells dissociated from SNE-injured and contralateral L4 and L5 dorsal root ganglia were cultured in a compartmentalized system. Axonal and cell body RNA samples were separately subjected to high throughput RNA sequencing (RNA-Seq). The injured axons exhibited enrichment of mRNAs related to protein synthesis and nerve regeneration. Lengthening of 3′UTRs was more prevalent in the injured axons, including the newly discovered alternative cleavage and polyadenylation of NaV1.8 mRNA. Alternative polyadenylation was largely independent from the relative abundance of axonal mRNAs; but they were highly clustered in functional pathways related to RNA granule formation in the injured axons. These RNA-Seq data analyses indicate that peripheral nerve injury may result in highly selective mRNA enrichment in the affected axons with 3′UTR alterations potentially contributing to the mechanism of neuropathic pain.

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Section: Resultsmentioning

confidence: 99%

“…Paired-end fastq sequence reads for each sample were aligned to the UCSC Rattus norvegicus reference genome rn5 using TopHat v1.3.0 24 integrated with Bowtie v0.12.7 25 on cloud computing, BaseSpace (Illumina, CA, USA). The resulting aligned reads were analyzed further by Cufflinks v1.0.3 26 .…”

Section: Methodsmentioning

confidence: 99%

Aberrant plasticity of peripheral sensory axons in a painful neuropathy

Hirai

Mulpuri

Cheng

et al. 2017

Sci Rep

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“…A recent longitudinal analysis demonstrated that chronic pain strongly predicts the development of more depressive symptoms in patients with pain compared with those without pain [6]. These epidemiological studies suggest that individual differences exist in the development of pain and depression comorbidities [1,2,[7][8][9]. Although pain and depression share biological pathways, the precise mechanisms underlying the comorbidity of pain and depression remain unknown.…”

Section: Introductionmentioning

confidence: 99%

Brain-derived neurotrophic factor-TrkB signaling in the medial prefrontal cortex plays a role in the anhedonia-like phenotype after spared nerve injury

Fang

Yang

et al. 2018

Eur Arch Psychiatry Clin Neurosci

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Although depressive symptoms including anhedonia (i.e., loss of pleasure) frequently accompany pain, little is known about the risk factors contributing to individual differences in pain-induced anhedonia. In this study, we examined if signaling of brain-derived neurotrophic factor (BDNF) and its receptor tropomyosin-receptor-kinase B (TrkB) contribute to individual differences in the development of neuropathic pain-induced anhedonia. Rats were randomly subjected to spared nerved ligation (SNI) or sham surgery. The SNI rats were divided into two groups based on the results of a sucrose preference test. Rats with anhedonia-like phenotype displayed lower tissue levels of BDNF in the medial prefrontal cortex (mPFC) compared with rats without anhedonia-like phenotype and sham-operated rats. In contrast, tissue levels of BDNF in the nucleus accumbens (NAc) of rats with an anhedonia-like phenotype were higher compared with those of rats without anhedonia-like phenotype and sham-operated rats. Furthermore, tissue levels of BDNF in the hippocampus, L2-5 spinal cord, muscle, and liver from both rats with or without anhedonia-like phenotype were lower compared with those of sham-operated rats. A single injection of 7,8-dihydroxyflavone (10 mg/kg; TrkB agonist), but not ANA-12 (0.5 mg/kg; TrkB antagonist), ameliorated reduced sucrose preference and reduced BDNF-TrkB signaling in the mPFC in the rats with anhedonia-like phenotype. These findings suggest that reduced BDNF-TrkB signaling in the mPFC might contribute to neuropathic pain-induced anhedonia, and that TrkB agonists could be potential therapeutic drugs for pain-induced anhedonia.

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“…High pain severity is associated with greater sleep impairment in comparison with low pain severity [30][31][32] . However, in previous studies, sleep disturbance has only been observed in a subset of animals [33][34][35][36][37][38] . These discrepancies may be due to the different designs: wire or wireless recording, recording periods, and pain stimuli.…”

Section: Discussionmentioning

confidence: 93%

Changes in Sleep Architecture under Sustained Pain in Adult Male Rats Subjected to Neonatal Short-Lasting Local Inflammatory Insult

et al. 2017

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Neonatal, short-lasting, local, nociceptive insult by carrageenan can cause long-term alterations in somatosensory and neurohumoral systems. We previously revealed hyporesponsiveness of the autonomic nervous system (ANS) after painful stimulation of adult rats in a neonatal carrageenan-induced pain model. Sleep disturbance has been highly correlated with pain and ANS activity. In the present study, adult rats that had received an intraplantar injection of carrageenan on postnatal day 1 were investigated to determine if there were alterations in their sleep architecture upon the stimulation of pain. Polysomnographic and heart rate variability recordings were carried out, with a wireless transmission of data, for 24 h under baseline conditions and after an intraplantar injection of complete Freund's adjuvant to induce sustained nociception. Increased active awake (AW) and decreased quiet sleep (QS) and paradoxical sleep (PS) times were noted in the control animals. In the carrageenan-treated rats, the AW time increased but with decreased alertness, as revealed by decreases in beta and increases in theta power. The QS time did not decrease. The PS time decreased during the first 12 h, then increased during the following 12 h, suggesting an early rebound of formerly deprived PS time. Sympathetic activation under sustained pain was not apparent in any stage of sleep in carrageenan-treated rats and was even suppressed in AW time. An impaired sympathetic reaction to pain may have contributed to the atypical changes in sleep architecture in these rats. In conclusion, pain in early life has a long-term effect on the cardiovascular-autonomic-electroencephalographic responses to pain later in life. The physiological relevance of these results remains undetermined.

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Peripheral nerve injury evokes disabilities and sensory dysfunction in a subpopulation of rats: a closer model to human chronic neuropathic pain?

Cited by 43 publications

References 19 publications

Aberrant plasticity of peripheral sensory axons in a painful neuropathy

Aberrant plasticity of peripheral sensory axons in a painful neuropathy

Brain-derived neurotrophic factor-TrkB signaling in the medial prefrontal cortex plays a role in the anhedonia-like phenotype after spared nerve injury

Changes in Sleep Architecture under Sustained Pain in Adult Male Rats Subjected to Neonatal Short-Lasting Local Inflammatory Insult

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