Interleukin-10 of Red Nucleus Plays Anti-allodynia Effect in Neuropathic Pain Rats with Spared Nerve Injury

Overview

Journal Neurochem Res

Specialties Chemistry
Neurology

Date 2012 May 16

PMID 22584848

Citations 13

Authors

Zhi-Hong Wang

Xiao-Yan Zeng

Shui-Ping Han

Gui-Xiang Fan

Jun-Yang Wang

Affiliations

Soon will be listed here.

Abstract

Our previous studies have shown that pro-inflammatory cytokines tumor necrosis factor-alpha (TNF-α) and interleukin-1beta (IL-1β) in red nucleus (RN) are involved in the development of neuropathic pain and play facilitated roles on the mechanical allodynia induced by peripheral nerve injury. The current study was designed to evaluate the expression and effect of IL-10, an anti-inflammatory cytokine, in the RN of rats with spared nerve injury (SNI). Immunohistochemical staining results demonstrated when 3 weeks after SNI, the expression level of IL-10 in the contralateral RN of SNI rats was apparently higher than those of sham-operated and normal rats. To further study the effect of IL-10 in the development of neuropathic pain, different doses of IL-10 (1.0, 0.5 and 0.1 μg/μl) were microinjected respectively into the RN contralateral to the nerve injury side of SNI rats. Results demonstrated that higher doses of IL-10 (1.0 and 0.5 μg/μl) significantly attenuated the mechanical allodynia of neuropathic rats, while 0.1 μg/μl of IL-10 did not show any analgesic effect. These results suggest that IL-10 of RN participates in the development of neuropathic pain and plays inhibitory roles on the mechanical allodynia induced by SNI.

Citing Articles

Red Nucleus Interleukin-6 Evokes Tactile Allodynia in Male Rats Through Modulating Spinal Pro-inflammatory and Anti-inflammatory Cytokines.

Yang Q, Li H, Xia Y, Tian X, Feng F, Yang J Front Mol Neurosci. 2022; 15:820664.

PMID: 35465093 PMC: 9026175. DOI: 10.3389/fnmol.2022.820664.

Persistent pain induces mood problems and memory loss by the involvement of cytokines, growth factors, and supraspinal glial cells.

da Silva M, Guginski G, Sato K, Sanada L, Sluka K, Santos A Brain Behav Immun Health. 2021; 7:100118.

PMID: 34589875 PMC: 8474185. DOI: 10.1016/j.bbih.2020.100118.

Red nucleus IL-33 facilitates the early development of mononeuropathic pain in male rats by inducing TNF-α through activating ERK, p38 MAPK, and JAK2/STAT3.

Li H, Yang Q, Wang W, Tian X, Feng F, Zhang S J Neuroinflammation. 2021; 18(1):150.

PMID: 34225736 PMC: 8258957. DOI: 10.1186/s12974-021-02198-9.

Red nucleus structure and function: from anatomy to clinical neurosciences.

Basile G, Quartu M, Bertino S, Serra M, Boi M, Bramanti A Brain Struct Funct. 2020; 226(1):69-91.

PMID: 33180142 PMC: 7817566. DOI: 10.1007/s00429-020-02171-x.

Activation of GPR40 produces mechanical antiallodynia via the spinal glial interleukin-10/β-endorphin pathway.

Mao X, Wu H, Tang X, Ali U, Liu H, Wang Y J Neuroinflammation. 2019; 16(1):84.

PMID: 30981281 PMC: 6461825. DOI: 10.1186/s12974-019-1457-9.

References

Milligan E, Sloane E, Langer S, Hughes T, Jekich B, Frank M . Repeated intrathecal injections of plasmid DNA encoding interleukin-10 produce prolonged reversal of neuropathic pain. Pain. 2006; 126(1-3):294-308. DOI: 10.1016/j.pain.2006.07.009. View

Lavoie S, Drew T . Discharge characteristics of neurons in the red nucleus during voluntary gait modifications: a comparison with the motor cortex. J Neurophysiol. 2002; 88(4):1791-814. DOI: 10.1152/jn.2002.88.4.1791. View

Zimmermann M . Ethical guidelines for investigations of experimental pain in conscious animals. Pain. 1983; 16(2):109-110. DOI: 10.1016/0304-3959(83)90201-4. View

Wieseler-Frank J, Maier S, Watkins L . Central proinflammatory cytokines and pain enhancement. Neurosignals. 2005; 14(4):166-74. DOI: 10.1159/000087655. View

Muir G, Whishaw I . Red nucleus lesions impair overground locomotion in rats: a kinetic analysis. Eur J Neurosci. 2000; 12(3):1113-22. DOI: 10.1046/j.1460-9568.2000.00987.x. View

Liu M, Liu X, Liu B . [The analgesic effect of red nucleus and strengthening effect thereof to the acupuncture analgesia]. Zhen Ci Yan Jiu. 1991; 16(1):48-53. View

Loram L, Harrison J, Sloane E, Hutchinson M, Sholar P, Taylor F . Enduring reversal of neuropathic pain by a single intrathecal injection of adenosine 2A receptor agonists: a novel therapy for neuropathic pain. J Neurosci. 2009; 29(44):14015-25. PMC: 2799253. DOI: 10.1523/JNEUROSCI.3447-09.2009. View

Zelenin P, Beloozerova I, Sirota M, Orlovsky G, Deliagina T . Activity of red nucleus neurons in the cat during postural corrections. J Neurosci. 2010; 30(43):14533-42. PMC: 2988228. DOI: 10.1523/JNEUROSCI.2991-10.2010. View

Jancalek R, Svizenska I, Klusakova I, Dubovy P . Bilateral changes of IL-10 protein in lumbar and cervical dorsal root ganglia following proximal and distal chronic constriction injury of peripheral nerve. Neurosci Lett. 2011; 501(2):86-91. DOI: 10.1016/j.neulet.2011.06.052. View

10.

Jancalek R, Dubovy P, Svizenska I, Klusakova I . Bilateral changes of TNF-alpha and IL-10 protein in the lumbar and cervical dorsal root ganglia following a unilateral chronic constriction injury of the sciatic nerve. J Neuroinflammation. 2010; 7:11. PMC: 2828436. DOI: 10.1186/1742-2094-7-11. View

11.

Saade N, Nasr I, Massaad C, Safieh-Garabedian B, Jabbur S, Kanaan S . Modulation of ultraviolet-induced hyperalgesia and cytokine upregulation by interleukins 10 and 13. Br J Pharmacol. 2000; 131(7):1317-24. PMC: 1572458. DOI: 10.1038/sj.bjp.0703699. View

12.

Yu C, Fairbanks C, Wilcox G, Yezierski R . Effects of agmatine, interleukin-10, and cyclosporin on spontaneous pain behavior after excitotoxic spinal cord injury in rats. J Pain. 2003; 4(3):129-40. DOI: 10.1054/jpai.2003.11. View

13.

Shimizu K, Guo W, Wang H, Zou S, Lagraize S, Iwata K . Differential involvement of trigeminal transition zone and laminated subnucleus caudalis in orofacial deep and cutaneous hyperalgesia: the effects of interleukin-10 and glial inhibitors. Mol Pain. 2009; 5:75. PMC: 2806354. DOI: 10.1186/1744-8069-5-75. View

14.

Sawada M, Suzumura A, Marunouchi T . Cytokine network in the central nervous system and its roles in growth and differentiation of glial and neuronal cells. Int J Dev Neurosci. 1995; 13(3-4):253-64. PMC: 7135063. DOI: 10.1016/0736-5748(94)00076-f. View

15.

Laughlin T, Bethea J, Yezierski R, Wilcox G . Cytokine involvement in dynorphin-induced allodynia. Pain. 2000; 84(2-3):159-67. DOI: 10.1016/s0304-3959(99)00195-5. View

16.

Ruohonen S, Jagodi M, Khademi M, Taskinen H, Ojala P, Olsson T . Contralateral non-operated nerve to transected rat sciatic nerve shows increased expression of IL-1beta, TGF-beta1, TNF-alpha, and IL-10. J Neuroimmunol. 2002; 132(1-2):11-7. DOI: 10.1016/s0165-5728(02)00281-3. View

17.

Sloane E, Soderquist R, Maier S, Mahoney M, Watkins L, Milligan E . Long-term control of neuropathic pain in a non-viral gene therapy paradigm. Gene Ther. 2009; 16(4):470-5. PMC: 2756299. DOI: 10.1038/gt.2009.21. View

18.

Ledeboer A, Jekich B, Sloane E, Mahoney J, Langer S, Milligan E . Intrathecal interleukin-10 gene therapy attenuates paclitaxel-induced mechanical allodynia and proinflammatory cytokine expression in dorsal root ganglia in rats. Brain Behav Immun. 2006; 21(5):686-98. PMC: 2063454. DOI: 10.1016/j.bbi.2006.10.012. View

19.

Jing Y, Wang J, Li X, Wang Z, Pei L, Pan M . Nerve growth factor of red nucleus involvement in pain induced by spared nerve injury of the rat sciatic nerve. Neurochem Res. 2009; 34(9):1612-8. DOI: 10.1007/s11064-009-9950-7. View

20.

Mizuno T, Sawada M, Marunouchi T, Suzumura A . Production of interleukin-10 by mouse glial cells in culture. Biochem Biophys Res Commun. 1994; 205(3):1907-15. DOI: 10.1006/bbrc.1994.2893. View