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Original Research

Spinal TLR4/P2X7 Receptor-Dependent NLRP3 Inflammasome Activation Contributes to the Development of Tolerance to Morphine-Induced Antinociception

, , , , , , , , , , & ORCID Icon show all
Pages 571-582 | Published online: 24 Sep 2020

References

  • Williams JT, Ingram SL, Henderson G, et al. Regulation of mu-opioid receptors: desensitization,phosphorylation, internalization, and tolerance. Pharmacol Rev. 2013;65(1):223–254. doi:10.1124/pr.112.00594223321159
  • Bagley EE, Chieng BC, Christie MJ, et al. Opioid tolerance in periaqueductal gray neurons isolated from mice chronically treated with morphine. Br J Pharmacol. 2005;146(1):68–76. doi:10.1038/sj.bjp.070631515980868
  • Ueda H, Ueda M. Mechanisms underlying morphine analgesic tolerance and dependence. Front Biosci. 2009;14:5260–5272. doi:10.2741/3596
  • Eidson LN, Murphy AZ. Inflammatory mediators of opioid tolerance: implications for dependency and addiction. Peptides. 2019;115:51–58. doi:10.1016/j.peptides.2019.01.00330890355
  • Mika J, Wawrzczak-Bargiela A, Osikowicz M, et al. Attenuation of morphine tolerance by minocycline and pentoxifylline in naive and neuropathic mice. Brain Behav Immun. 2009;23(1):75–84. doi:10.1016/j.bbi.2008.07.00518684397
  • Leduc-Pessah H, Weilinger NL, Fan CY, et al. Site-specific regulation of P2X7 receptor function in microglia gates morphine analgesic tolerance. J Neurosci. 2017;37(42):10154–10172. doi:10.1523/jneurosci.0852-17.201728924009
  • Hameed H, Hameed M, Christo PJ. The effect of morphine on glial cells as a potential therapeutic target for pharmacological development of analgesic drugs. Curr Pain Headache Rep. 2010;14(2):96–104. doi:10.1007/s11916-010-0093-y20425198
  • Haque ME, Akther M, Jakaria M, et al. Targeting the microglial NLRP3 inflammasome and its role in Parkinson’s disease. Mov Disord. 2020;35(1):20–33. doi:10.1002/mds.2787431680318
  • Hung WL, Ho CT, Pan MH. Targeting the NLRP3 inflammasome in neuroinflammation: health promoting effects of dietary phytochemicals in neurological disorders. Mol Nutr Food Res. 2020;64(4):e1900550. doi:10.1002/mnfr.20190055031675164
  • Song L, Pei L, Yao S, et al. NLRP3 inflammasome in neurological diseases, from functions to therapies. Front Cell Neurosci. 2017:11. doi: 10.3389/fncel.2017.00063.28217083
  • Bauernfeind FG, Horvath G, Stutz A, et al. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol. 2009;183(2):787–791. doi:10.4049/jimmunol.090136319570822
  • Mariathasan S, Weiss DS, Newton K, et al. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature. 2006;440(7081):228–232. doi:10.1038/nature0451516407890
  • Muñoz-Planillo R, Kuffa P, Martínez-Colón G, et al. K+ efflux is the common trigger of NLRP3 inflammasome activation by bacterial toxins and particulate matter. Immunity. 2013;38(6):1142–1153. doi:10.1016/j.immuni.2013.05.01623809161
  • Heid ME, Keyel PA, Kamga C, et al. Mitochondrial reactive oxygen species induces NLRP3-dependent lysosomal damage and inflammasome activation. J Immunol. 2013;191(10):5230–5238. doi:10.4049/jimmunol.130149024089192
  • Cai Y, Kong H, Pan YB, et al. Procyanidins alleviates morphine tolerance by inhibiting activation of NLRP3 inflammasome in microglia. J Neuroinflammation. 2016;13(1):53. doi:10.1186/s12974-016-0520-z26931361
  • Eidson LN, Murphy AZ. Blockade of Toll-like receptor 4 attenuates morphine tolerance and facilitates the pain relieving properties of morphine. J Neurosci. 2013;33(40):15952–15963. doi:10.1523/JNEUROSCI.1609-13.201324089500
  • Eidson LN, Inoue K, Young LJ, et al. Toll-like receptor 4 mediates morphine-induced neuroinflammation and tolerance via soluble tumor necrosis factor signaling. Neuropsychopharmacology. 2017;42(3):661–670. doi:10.1038/npp.2016.13127461080
  • Wang X, Loram LC, Ramos K, et al. Morphine activates neuroinflammation in a manner parallel to endotoxin. Proc Natl Acad Sci U S A. 2012;109(16):6325–6330. doi:10.1073/pnas.120013010922474354
  • Lewis SS, Hutchinson MR, Rezvani N, et al. Evidence that intrathecal morphine-3-glucuronide may cause pain enhancement via toll-like receptor 4/MD-2 and interleukin-1beta. Neuroscience. 2010;165(2):569–583. doi:10.1016/j.neuroscience.2009.10.01119833175
  • Tavakoli Dargani Z, Singla DK. Embryonic stem cell-derived exosomes inhibit doxorubicin-induced TLR4-NLRP3-mediated cell death-pyroptosis. Am J Physiol Heart Circ Physiol. 2019;317(2):H460H71. doi:10.1152/ajpheart.00056.201931172809
  • Fu S, Wang J, Hao C, et al. Tetramethylpyrazine ameliorates depression by inhibiting TLR4-NLRP3 inflammasome signal pathway in mice. Psychopharmacology. 2019;236(7):2173–2185. doi:10.1007/s00213-019-05210-630847567
  • Bhattacharya A. Recent advances in CNS P2X7 physiology and pharmacology: focus on neuropsychiatric disorders. Front Pharmacol. 2018;9:30. doi:10.3389/fphar.2018.0003029449810
  • Thawkar BS, Kaur G. Inhibitors of NF-kappaB and P2X7/NLRP3/Caspase 1 pathway in microglia: novel therapeutic opportunities in neuroinflammation induced early-stage Alzheimer’s disease. J Neuroimmunol. 2019;326:62–74. doi:10.1016/j.jneuroim.2018.11.01030502599
  • Faria RX, Freitas HR, Reis RAM. P2X7 receptor large pore signaling in avian Muller glial cells. J Bioenerg Biomembr. 2017;49(3):215–229. doi:10.1007/s10863-017-9717-928573491
  • Kelley N, Jeltema D, Duan Y, et al. The NLRP3 inflammasome: an overview of mechanisms of activation and regulation. Int J Mol Sci. 2019;20:13. doi:10.3390/ijms20133328
  • Kilkenny C, Browne W, Cuthill IC, et al. Animal research: reporting in vivo experiments–the ARRIVE guidelines. J Cereb Blood Flow Metab. 2011;31(4):991–993. doi:10.1038/jcbfm.2010.22021206507
  • Jiang W, Li M, He F, et al. Targeting the NLRP3 inflammasome to attenuate spinal cord injury in mice. J Neuroinflammation. 2017;14(1):207. doi:10.1186/s12974-017-0980-929070054
  • Yang F, Wang Z, Wei X, et al. NLRP3 deficiency ameliorates neurovascular damage in experimental ischemic stroke. J Cereb Blood Flow Metab. 2014;34(4):660–667. doi:10.1038/jcbfm.2013.24224424382
  • Geldhoff M, Mook-Kanamori BB, Brouwer MC, et al. Genetic variation in inflammasome genes is associated with outcome in bacterial meningitis. Immunogenetics. 2013;65(1):9–16. doi:10.1007/s00251-012-0653-x23053059
  • Bossu P, Ciaramella A, Salani F, et al. Interleukin-18, from neuroinflammation to Alzheimer’s disease. Curr Pharm Des. 2010;16(38):4213–4224. doi:10.2174/13816121079451914721184660
  • Wilms H, Sievers J, Rickert U, et al. Dimethylfumarate inhibits microglial and astrocytic inflammation by suppressing the synthesis of nitric oxide, IL-1beta, TNF-alpha and IL-6 in an in-vitro model of brain inflammation. J Neuroinflammation. 2010;7:30. doi:10.1186/1742-2094-7-3020482831
  • DeLeo JA, Tanga FY, Tawfik VL. Neuroimmune activation and neuroinflammation in chronic pain and opioid tolerance/hyperalgesia. Neuroscientist. 2004;10(1):40–52. doi:10.1177/107385840325995014987447
  • Qu J, Tao XY, Teng P, et al. Blocking ATP-sensitive potassium channel alleviates morphine tolerance by inhibiting HSP70-TLR4-NLRP3-mediated neuroinflammation. J Neuroinflammation. 2017;14(1):228. doi:10.1186/s12974-017-0997-029178967
  • Liu Q, Su LY, Sun C, et al. Melatonin alleviates morphine analgesic tolerance in mice by decreasing NLRP3 inflammasome activation. Redox Biol. 2020;34:101560. doi:10.1016/j.redox.2020.10156032413745
  • Xie XJ, Ma LG, Xi K, et al. Effects of microRNA-223 on morphine analgesic tolerance by targeting NLRP3 in a rat model of neuropathic pain. Mol Pain. 2017;13:1744806917706582. doi:10.1177/174480691770658228580822
  • Zhang Y, Wang K, Lin M, et al. Inhibition of morphine tolerance by MrgC receptor via modulation of interleukin-1beta and matrix metalloproteinase 9 in dorsal root ganglia in rats. Eur J Pharmacol. 2017;815:10–17. doi:10.1016/j.ejphar.2017.10.01128993160
  • Qian J, Zhu Y, Bai L, et al. Chronic morphine-mediated upregulation of high mobility group box 1 in the spinal cord contributes to analgesic tolerance and hyperalgesia in rats. Neurotherapeutics. 2019. doi:10.1007/s13311-019-00800-w
  • Liang Y, Chu H, Jiang Y, et al. Morphine enhances IL-1β release through toll-like receptor 4-mediated endocytic pathway in microglia. Purinergic Signal. 2016;12(4):637–645. doi:10.1007/s11302-016-9525-427506813
  • Sutterwala FS, Haasken S, Cassel SL. Mechanism of NLRP3 inflammasome activation. Ann N Y Acad Sci. 2014;1319:82–95. doi:10.1111/nyas.1245824840700
  • Jiang S, Zhang Y, Zheng JH, et al. Potentiation of hepatic stellate cell activation by extracellular ATP is dependent on P2X7R-mediated NLRP3 inflammasome activation. Pharmacol Res. 2017;117:82–93. doi:10.1016/j.phrs.2016.11.04027940204
  • He Y, Taylor N, Fourgeaud L, et al. The role of microglial P2X7: modulation of cell death and cytokine release. J Neuroinflammation. 2017;14(1):135. doi:10.1186/s12974-017-0904-828716092
  • Kim EA, Cho CH, Kim J, et al. The azetidine derivative, KHG26792 protects against ATP-induced activation of NFAT and MAPK pathways through P2X7 receptor in microglia. Neurotoxicology. 2015;51:198–206. doi:10.1016/j.neuro.2015.10.01326522449
  • Bhattacharya A, Jones DNC. Emerging role of the P2X7-NLRP3-IL1beta pathway in mood disorders. Psychoneuroendocrinology. 2018;98:95–100. doi:10.1016/j.psyneuen.2018.08.01530121550
  • Chen ML, Cao H, Chu YX, et al. Role of P2X7 receptor-mediated IL-18/IL-18R signaling in morphine tolerance: multiple glial-neuronal dialogues in the rat spinal cord. J Pain. 2012;13(10):945–958. doi:10.1016/j.jpain.2012.06.00722968128
  • Zhou D, Chen ML, Zhang YQ, et al. Involvement of spinal microglial P2X7 receptor in generation of tolerance to morphine analgesia in rats. J Neurosci. 2010;30(23):8042–8047. doi:10.1523/JNEUROSCI.5377-09.201020534852