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

被引:148
作者
Gui, Wen-Shan [1 ,2 ,3 ]
Wei, Xiao [1 ,2 ,3 ]
Mai, Chun-Lin [1 ,2 ,3 ]
Murugan, Madhuvika [4 ]
Wu, Long-Jun [4 ]
Xin, Wen-Jun [1 ,2 ,3 ]
Zhou, Li-Jun [1 ,2 ,3 ,4 ]
Liu, Xian-Guo [1 ,2 ,3 ]
机构
[1] Sun Yat Sen Univ, Zhongshan Sch Med, Dept Physiol, Guangzhou 510275, Guangdong, Peoples R China
[2] Sun Yat Sen Univ, Zhongshan Sch Med, Pain Res Ctr, Guangzhou 510275, Guangdong, Peoples R China
[3] Guangdong Prov Key Lab Brain Funct & Dis, Guangzhou, Guangdong, Peoples R China
[4] Rutgers State Univ, Dept Cell Biol & Neurosci, Piscataway, NJ USA
来源
MOLECULAR PAIN | 2016年 / 12卷
基金
中国国家自然科学基金;
关键词
Neuropathic pain; short-term memory deficit; depression; interleukin-1; beta; microglia; peripheral nerve injury; LONG-TERM POTENTIATION; NECROSIS-FACTOR-ALPHA; BLOOD-BRAIN-BARRIER; SPINAL DORSAL-HORN; SRC-FAMILY KINASES; MIRROR-IMAGE PAIN; WORKING-MEMORY; SYNAPTIC PLASTICITY; GROWTH-FACTOR; HIPPOCAMPAL NEUROGENESIS;
D O I
10.1177/1744806916646784
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
Background: Chronic 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-1 beta) in the injured nerve independent of neuropathic pain following spared nerve injury in rats and mice. Results: Mechanical 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-1 beta 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-1 beta 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 naive rats by repetitive intravenous injection of re combinant rat IL-1 beta (rrIL-1 beta) 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-1 beta and the effect of spared nerve injury was substantially reversed by peri-sciatic administration of anti-IL-1 beta. Conclusions: Neuropathic pain was not necessary for the development of cognitive and emotional disorders, while the overproduction of IL-1 beta in the injured sciatic nerve following peripheral nerve injury may be a common mechanism underlying the generation of neuropathic pain, memory deficit, and depression.
引用
收藏
页数:15
相关论文
共 78 条
  • [1] Chronic dizocilpine or apomorphine and development of neuropathy in two animal models II: Effects on brain cytokines and neurotrophins
    Al-Amin, Hassen
    Sarkis, Rani
    Atweh, Samir
    Jabbur, Suhayl
    Saade, Nayef
    [J]. EXPERIMENTAL NEUROLOGY, 2011, 228 (01) : 30 - 40
  • [2] Expression of IL-1β in supraspinal brain regions in rats with neuropathic pain
    Apkarian, A. Vania
    Lavarello, Simona
    Randolf, Anke
    Berra, Hector H.
    Chialvo, Dante R.
    Besedovsky, Hugo O.
    del Rey, Adriana
    [J]. NEUROSCIENCE LETTERS, 2006, 407 (02) : 176 - 181
  • [3] INDUCTION OF IMMUNE-SYSTEM MEDIATORS IN THE HIPPOCAMPAL-FORMATION IN ALZHEIMERS AND PARKINSONS DISEASES - SELECTIVE EFFECTS ON SPECIFIC INTERLEUKINS AND INTERLEUKIN RECEPTORS
    ARAUJO, DM
    LAPCHAK, PA
    [J]. NEUROSCIENCE, 1994, 61 (04) : 745 - 754
  • [4] IL-1β regulates blood-brain barrier permeability via reactivation of the hypoxia-angiogenesis program
    Argaw, Azeb Tadesse
    Zhang, Yueting
    Snyder, Brian J.
    Zhao, Meng-Liang
    Kopp, Natalya
    Lee, Sunhee C.
    Raine, Cedric S.
    Brosnan, Celia F.
    John, Gareth R.
    [J]. JOURNAL OF IMMUNOLOGY, 2006, 177 (08) : 5574 - 5584
  • [5] Passage of cytokines across the blood-brain barrier
    Banks, WA
    Kastin, AJ
    Broadwell, RD
    [J]. NEUROIMMUNOMODULATION, 1995, 2 (04) : 241 - 248
  • [6] Peripheral nerve injury and TRPV1-expressing primary afferent C-fibers cause opening of the blood-brain barrier
    Beggs, Simon
    Liu, Xue Jun
    Kwan, Chun
    Salter, Michael W.
    [J]. MOLECULAR PAIN, 2010, 6
  • [7] Chronic pain, chronic stress and depression: Coincidence or consequence?
    Blackburn-Munro, G
    Blackburn-Munro, RE
    [J]. JOURNAL OF NEUROENDOCRINOLOGY, 2001, 13 (12) : 1009 - 1023
  • [8] 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
    [J]. PHARMACOLOGICAL REPORTS, 2015, 67 (01) : 123 - 128
  • [9] Maternal Deprivation Is Associated With Sex-Dependent Alterations in Nociceptive Behavior and Neuroinflammatory Mediators in the Rat Following Peripheral Nerve Injury
    Burke, Nikita N.
    Llorente, Ricardo
    Marco, Eva M.
    Tong, Kezanne
    Finn, David P.
    Viveros, Maria-Paz
    Roche, Michelle
    [J]. JOURNAL OF PAIN, 2013, 14 (10) : 1173 - 1184
  • [10] Synapse rearrangements upon learning: from divergent-sparse connectivity to dedicated sub-circuits
    Caroni, Pico
    Chowdhury, Ananya
    Lahr, Maria
    [J]. TRENDS IN NEUROSCIENCES, 2014, 37 (10) : 604 - 614