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Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Mini-Review Article

Noncoding RNAs: Novel Targets for Opioid Tolerance

Author(s): Meiling Deng and Wangyuan Zou*

Volume 21, Issue 5, 2023

Published on: 02 February, 2023

Page: [1202 - 1213] Pages: 12

DOI: 10.2174/1570159X21666221129122932

Price: $65

Abstract

As a global health problem, chronic pain is one of the leading causes of disability, and it imposes a huge economic and public health burden on families and society. Opioids represent the cornerstone of analgesic drugs. However, opioid tolerance caused by long-term application of opioids is a major factor leading to drug withdrawal, serious side effects caused by dose increases, and even the death of patients, placing an increasing burden on individuals, medicine, and society. Despite efforts to develop methods to prevent and treat opioid tolerance, no effective treatment has yet been found. Therefore, understanding the mechanism underlying opioid tolerance is crucial for finding new prevention and treatment strategies. Noncoding RNAs (ncRNAs) are important parts of mammalian gene transcriptomes, and there are thousands of unique noncoding RNA sequences in cells. With the rapid development of high-throughput genome technology, research on ncRNAs has become a hot topic in biomedical research. In recent years, studies have shown that ncRNAs mediate physiological and pathological processes, including chromatin remodeling, transcription, posttranscriptional modification and signal transduction, which are key regulators of physiological processes in developmental and disease environments and have become biomarkers and potential therapeutic targets for various diseases. An increasing number of studies have found that ncRNAs are closely related to the development of opioid tolerance. In this review, we have summarized the evidence that ncRNAs play an important role in opioid tolerance and that ncRNAs may be novel targets for opioid tolerance.

Keywords: Noncoding RNA, chronic pain, opioid tolerance, microRNA, long noncoding RNA, circRNA.

Graphical Abstract
[1]
Raja, S.N.; Carr, D.B.; Cohen, M.; Finnerup, N.B.; Flor, H.; Gibson, S.; Keefe, F.J.; Mogil, J.S.; Ringkamp, M.; Sluka, K.A.; Song, X.J.; Stevens, B.; Sullivan, M.D.; Tutelman, P.R.; Ushida, T.; Vader, K. The revised international association for the study of pain definition of pain: Concepts, challenges, and compromises. Pain, 2020, 161(9), 1976-1982.
[http://dx.doi.org/10.1097/j.pain.0000000000001939] [PMID: 32694387]
[2]
Mills, S.E.E.; Nicolson, K.P.; Smith, B.H. Chronic pain: A review of its epidemiology and associated factors in population-based studies. Br. J. Anaesth., 2019, 123(2), e273-e283.
[http://dx.doi.org/10.1016/j.bja.2019.03.023] [PMID: 31079836]
[3]
Ji, R.R.; Nackley, A.; Huh, Y.; Terrando, N.; Maixner, W. Neuroinflammation and central sensitization in chronic and widespread pain. Anesthesiology, 2018, 129(2), 343-366.
[http://dx.doi.org/10.1097/ALN.0000000000002130] [PMID: 29462012]
[4]
Colloca, L.; Ludman, T.; Bouhassira, D.; Baron, R.; Dickenson, A.H.; Yarnitsky, D.; Freeman, R.; Truini, A.; Attal, N.; Finnerup, N.B.; Eccleston, C.; Kalso, E.; Bennett, D.L.; Dworkin, R.H.; Raja, S.N. Neuropathic pain. Nat. Rev. Dis. Primers, 2017, 3(1), 17002.
[http://dx.doi.org/10.1038/nrdp.2017.2] [PMID: 28205574]
[5]
Failde, I.; Dueñas, M.; Ribera, M.V.; Gálvez, R.; Mico, J.A.; Salazar, A.; de Sola, H.; Pérez, C. Prevalence of central and peripheral neuropathic pain in patients attending pain clinics in Spain: Factors related to intensity of pain and quality of life. J. Pain Res., 2018, 11, 1835-1847.
[http://dx.doi.org/10.2147/JPR.S159729] [PMID: 30254486]
[6]
Song, G.; Yang, Z.; Guo, J.; Zheng, Y.; Su, X.; Wang, X. Interactions among lncRNAs/circRNAs, miRNAs, and mRNAs in neuropathic pain. Neurotherapeutics, 2020, 17(3), 917-931.
[http://dx.doi.org/10.1007/s13311-020-00881-y] [PMID: 32632773]
[7]
Liedgens, H.; Obradovic, M.; De Courcy, J.; Holbrook, T.; Jakubanis, R. A burden of illness study for neuropathic pain in Europe. Clinicoecon. Outcomes Res., 2016, 8, 113-126.
[PMID: 27217785]
[8]
Volkow, N.D.; McLellan, A.T. Opioid abuse in chronic pain — Misconceptions and mitigation strategies. N. Engl. J. Med., 2016, 374(13), 1253-1263.
[http://dx.doi.org/10.1056/NEJMra1507771] [PMID: 27028915]
[9]
Uniyal, A.; Gadepalli, A. Akhilesh; Tiwari, V. Underpinning the neurobiological intricacies associated with opioid tolerance. ACS Chem. Neurosci., 2020, 11(6), 830-839.
[http://dx.doi.org/10.1021/acschemneuro.0c00019] [PMID: 32083459]
[10]
Wu, S.; Marie Lutz, B.; Miao, X.; Liang, L.; Mo, K.; Chang, Y.J.; Du, P.; Soteropoulos, P.; Tian, B.; Kaufman, A.G.; Bekker, A.; Hu, Y.; Tao, Y.X. Dorsal root ganglion transcriptome analysis following peripheral nerve injury in mice. Mol. Pain, 2016, 12.
[http://dx.doi.org/10.1177/1744806916629048] [PMID: 27030721]
[11]
Andersen, R.E.; Lim, D.A. Forging our understanding of lncRNAs in the brain. Cell Tissue Res., 2018, 371(1), 55-71.
[http://dx.doi.org/10.1007/s00441-017-2711-z] [PMID: 29079882]
[12]
Shi, Z.; Pan, B.; Feng, S. The emerging role of long non‐coding RNA in spinal cord injury. J. Cell. Mol. Med., 2018, 22(4), 2055-2061.
[http://dx.doi.org/10.1111/jcmm.13515] [PMID: 29392896]
[13]
Matsui, M.; Corey, D.R. Non-coding RNAs as drug targets. Nat. Rev. Drug Discov., 2017, 16(3), 167-179.
[http://dx.doi.org/10.1038/nrd.2016.117] [PMID: 27444227]
[14]
Seruggia, D.; Josa, S.; Fernández, A.; Montoliu, L. The structure and function of the mouse tyrosinase locus. Pigment Cell Melanoma Res., 2021, 34(2), 212-221.
[http://dx.doi.org/10.1111/pcmr.12942] [PMID: 33098271]
[15]
Li, Y.; Li, G.; Guo, X.; Yao, H.; Wang, G.; Li, C. Non-coding RNA in bladder cancer. Cancer Lett., 2020, 485, 38-44.
[http://dx.doi.org/10.1016/j.canlet.2020.04.023] [PMID: 32437725]
[16]
Statello, L.; Guo, C.J.; Chen, L.L.; Huarte, M. Gene regulation by long non-coding RNAs and its biological functions. Nat. Rev. Mol. Cell Biol., 2021, 22(2), 96-118.
[http://dx.doi.org/10.1038/s41580-020-00315-9] [PMID: 33353982]
[17]
Fukaya, T.; Tomari, Y. MicroRNAs mediate gene silencing via multiple different pathways in drosophila. Mol. Cell, 2012, 48(6), 825-836.
[http://dx.doi.org/10.1016/j.molcel.2012.09.024] [PMID: 23123195]
[18]
Hirota, K.; Miyoshi, T.; Kugou, K.; Hoffman, C.S.; Shibata, T.; Ohta, K. Stepwise chromatin remodelling by a cascade of transcription initiation of non-coding RNAs. Nature, 2008, 456(7218), 130-134.
[http://dx.doi.org/10.1038/nature07348] [PMID: 18820678]
[19]
Kleaveland, B.; Shi, C.Y.; Stefano, J.; Bartel, D.P. A network of noncoding regulatory RNAs acts in the mammalian brain. Cell, 2018, 174(2), 350-362.e17.
[http://dx.doi.org/10.1016/j.cell.2018.05.022] [PMID: 29887379]
[20]
Anastasiadou, E.; Jacob, L.S.; Slack, F.J. Non-coding RNA networks in cancer. Nat. Rev. Cancer, 2018, 18(1), 5-18.
[http://dx.doi.org/10.1038/nrc.2017.99] [PMID: 29170536]
[21]
Idda, M.L.; Munk, R.; Abdelmohsen, K.; Gorospe, M. Noncoding RNAs in Alzheimer’s disease. Wiley Interdiscip. Rev. RNA, 2018, 9(2)
[http://dx.doi.org/10.1002/wrna.1463] [PMID: 29327503]
[22]
Zhou, J.; Li, Z.; Wu, T.; Zhao, Q.; Zhao, Q.; Cao, Y. LncGBP9/miR-34a axis drives macrophages toward a phenotype conducive for spinal cord injury repair via STAT1/STAT6 and SOCS3. J. Neuroinflammation, 2020, 17(1), 134.
[http://dx.doi.org/10.1186/s12974-020-01805-5] [PMID: 32345320]
[23]
Lucas, T.; Bonauer, A.; Dimmeler, S. RNA therapeutics in cardiovascular disease. Circ. Res., 2018, 123(2), 205-220.
[http://dx.doi.org/10.1161/CIRCRESAHA.117.311311] [PMID: 29976688]
[24]
López-González, M.J.; Landry, M.; Favereaux, A. MicroRNA and chronic pain: From mechanisms to therapeutic potential. Pharmacol. Ther., 2017, 180, 1-15.
[http://dx.doi.org/10.1016/j.pharmthera.2017.06.001] [PMID: 28579386]
[25]
Huang, J.; Wang, J.; Guo, Q.; Zou, W. Emerging roles of microRNAs in morphine tolerance. J. Pain Res., 2019, 12, 1139-1147.
[http://dx.doi.org/10.2147/JPR.S187592] [PMID: 31114297]
[26]
Wood, E.J.; Lipovich, L. MicroRNAs in opioid addiction: elucidating evolution. Front. Genet., 2012, 3, 241.
[http://dx.doi.org/10.3389/fgene.2012.00241] [PMID: 23233859]
[27]
Levran, O.; Randesi, M.; Rotrosen, J.; Ott, J.; Adelson, M.; Kreek, M.J.A. 3′ UTR SNP rs885863, a cis-eQTL for the circadian gene VIPR2 and lincRNA 689, is associated with opioid addiction. PLoS One, 2019, 14(11), e0224399.
[http://dx.doi.org/10.1371/journal.pone.0224399] [PMID: 31689297]
[28]
Irie, T.; Shum, R.; Deni, I.; Hunkele, A.; Le Rouzic, V.; Xu, J.; Wilson, R.; Fischer, G.W.; Pasternak, G.W.; Pan, Y.X. Identification of abundant and evolutionarily conserved opioid receptor circular RNAs in the nervous system modulated by morphine. Mol. Pharmacol., 2019, 96(2), 247-258.
[http://dx.doi.org/10.1124/mol.118.113977] [PMID: 31243060]
[29]
Noh, K.M.; Hwang, J.Y.; Follenzi, A.; Athanasiadou, R.; Miyawaki, T.; Greally, J.M.; Bennett, M.V.L.; Zukin, R.S. Repressor element-1 silencing transcription factor (REST)-dependent epigenetic remodeling is critical to ischemia-induced neuronal death. Proc. Natl. Acad. Sci. USA, 2012, 109(16), E962-E971.
[http://dx.doi.org/10.1073/pnas.1121568109] [PMID: 22371606]
[30]
Harden, R.N. Chronic pain and opiates: A call for moderation. Arch. Phys. Med. Rehabil., 2008, 89(3)(Suppl. 1), S72-S76.
[http://dx.doi.org/10.1016/j.apmr.2007.12.013] [PMID: 18295654]
[31]
He, Y.; Wang, Z.J. Let-7 microRNAs and opioid tolerance. Front. Genet., 2012, 3, 110.
[http://dx.doi.org/10.3389/fgene.2012.00110] [PMID: 22737161]
[32]
Volkow, N.D.; Jones, E.B.; Einstein, E.B.; Wargo, E.M. Prevention and treatment of opioid misuse and addiction. JAMA Psychiatry, 2019, 76(2), 208-216.
[http://dx.doi.org/10.1001/jamapsychiatry.2018.3126] [PMID: 30516809]
[33]
Martyn, J.A.J.; Mao, J.; Bittner, E.A. Opioid tolerance in critical illness. N. Engl. J. Med., 2019, 380(4), 365-378.
[http://dx.doi.org/10.1056/NEJMra1800222] [PMID: 30673555]
[34]
Zachariou, V.; Bolanos, C.A.; Selley, D.E.; Theobald, D.; Cassidy, M.P.; Kelz, M.B.; Shaw-Lutchman, T.; Berton, O.; Sim-Selley, L.J.; Dileone, R.J.; Kumar, A.; Nestler, E.J. An essential role for ΔFosB in the nucleus accumbens in morphine action. Nat. Neurosci., 2006, 9(2), 205-211.
[http://dx.doi.org/10.1038/nn1636] [PMID: 16415864]
[35]
Renthal, W.; Carle, T.L.; Maze, I.; Covington, H.E., III; Truong, H.T.; Alibhai, I.; Kumar, A.; Montgomery, R.L.; Olson, E.N.; Nestler, E.J. Delta FosB mediates epigenetic desensitization of the c-fos gene after chronic amphetamine exposure. J. Neurosci., 2008, 28(29), 7344-7349.
[http://dx.doi.org/10.1523/JNEUROSCI.1043-08.2008] [PMID: 18632938]
[36]
Levran, O.; Correa da Rosa, J.; Randesi, M.; Rotrosen, J.; Adelson, M.; Kreek, M.J. A non-coding CRHR2 SNP rs255105, a cis-eQTL for a downstream lincRNA AC005154.6, is associated with heroin addiction. PLoS One, 2018, 13(6), e0199951.
[http://dx.doi.org/10.1371/journal.pone.0199951] [PMID: 29953524]
[37]
Chen, L.; Heikkinen, L.; Wang, C.; Yang, Y.; Sun, H.; Wong, G. Trends in the development of miRNA bioinformatics tools. Brief. Bioinform., 2019, 20(5), 1836-1852.
[http://dx.doi.org/10.1093/bib/bby054] [PMID: 29982332]
[38]
Hill, M.; Tran, N. miRNA interplay: Mechanisms and consequences in cancer. Dis. Model. Mech., 2021, 14(4), dmm047662.
[http://dx.doi.org/10.1242/dmm.047662] [PMID: 33973623]
[39]
Lu, T.X.; Rothenberg, M.E. MicroRNA. J. Allergy Clin. Immunol., 2018, 141(4), 1202-1207.
[http://dx.doi.org/10.1016/j.jaci.2017.08.034] [PMID: 29074454]
[40]
Ramanathan, S.; Shenoda, B.B.; Ajit, S.K. Overview of microRNA modulation in analgesic research; Curr Protoc Pharmacol, 2017, pp. 21-29.
[41]
Dai, Z.; Chu, H.; Ma, J.; Yan, Y.; Zhang, X.; Liang, Y. The regulatory mechanisms and therapeutic potential of MicroRNAs: From chronic pain to morphine tolerance. Front. Mol. Neurosci., 2018, 11, 80.
[http://dx.doi.org/10.3389/fnmol.2018.00080] [PMID: 29615865]
[42]
Krol, J.; Loedige, I.; Filipowicz, W. The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet., 2010, 11(9), 597-610.
[http://dx.doi.org/10.1038/nrg2843] [PMID: 20661255]
[43]
Zhang, T.J.; Qiu, Y.; Hua, Z. The emerging perspective of morphine tolerance: MicroRNAs. Pain Res. Manag., 2019, 2019, 1-8.
[http://dx.doi.org/10.1155/2019/9432965] [PMID: 31182985]
[44]
Nam, M.H.; Won, W.; Han, K.S.; Lee, C.J. Signaling mechanisms of μ-opioid receptor (MOR) in the hippocampus: disinhibition versus astrocytic glutamate regulation. Cell. Mol. Life Sci., 2021, 78(2), 415-426.
[http://dx.doi.org/10.1007/s00018-020-03595-8] [PMID: 32671427]
[45]
Koehl, A.; Hu, H.; Maeda, S.; Zhang, Y.; Qu, Q.; Paggi, J.M.; Latorraca, N.R.; Hilger, D.; Dawson, R.; Matile, H.; Schertler, G.F.X.; Granier, S.; Weis, W.I.; Dror, R.O.; Manglik, A.; Skiniotis, G.; Kobilka, B.K. Structure of the µ-opioid receptor–Gi protein complex. Nature, 2018, 558(7711), 547-552.
[http://dx.doi.org/10.1038/s41586-018-0219-7] [PMID: 29899455]
[46]
Lee, M.C.; Wanigasekera, V.; Tracey, I. Imaging opioid analgesia in the human brain and its potential relevance for understanding opioid use in chronic pain. Neuropharmacology, 2014, 84(100), 123-130.
[http://dx.doi.org/10.1016/j.neuropharm.2013.06.035] [PMID: 23891639]
[47]
Mercadante, S.; Arcuri, E.; Santoni, A. Opioid-induced tolerance and hyperalgesia. CNS Drugs, 2019, 33(10), 943-955.
[http://dx.doi.org/10.1007/s40263-019-00660-0] [PMID: 31578704]
[48]
Corder, G.; Tawfik, V.L.; Wang, D.; Sypek, E.I.; Low, S.A.; Dickinson, J.R.; Sotoudeh, C.; Clark, J.D.; Barres, B.A.; Bohlen, C.J.; Scherrer, G. Loss of μ opioid receptor signaling in nociceptors, but not microglia, abrogates morphine tolerance without disrupting analgesia. Nat. Med., 2017, 23(2), 164-173.
[http://dx.doi.org/10.1038/nm.4262] [PMID: 28092666]
[49]
He, Y.; Yang, C.; Kirkmire, C.M.; Wang, Z.J. Regulation of opioid tolerance by let-7 family microRNA targeting the mu opioid receptor. J. Neurosci., 2010, 30(30), 10251-10258.
[http://dx.doi.org/10.1523/JNEUROSCI.2419-10.2010] [PMID: 20668208]
[50]
Dum, J.; Meyer, G.; Höllt, V.; Herz, A. In vivo opiate binding unchanged in tolerant/dependent mice. Eur. J. Pharmacol., 1979, 58(4), 453-460.
[http://dx.doi.org/10.1016/0014-2999(79)90316-9] [PMID: 574455]
[51]
Rothman, R.B.; Danks, J.A.; Jacobson, A.E.; Burke, T.R., Jr; Rice, K.C.; Tortella, F.C.; Holaday, J.W. Morphine tolerance increases μ-noncompetative δ binding sites. Eur. J. Pharmacol., 1986, 124(1-2), 113-119.
[http://dx.doi.org/10.1016/0014-2999(86)90130-5] [PMID: 3013657]
[52]
Lu, Z.; Xu, J.; Xu, M.; Pasternak, G.W.; Pan, Y.X. Morphine regulates expression of μ-opioid receptor MOR-1A, an intron-retention carboxyl terminal splice variant of the μ-opioid receptor (OPRM1) gene via miR-103/miR-107. Mol. Pharmacol., 2014, 85(2), 368-380.
[http://dx.doi.org/10.1124/mol.113.089292] [PMID: 24302561]
[53]
Lu, Z.; Xu, J.; Wang, Q.; Pan, Y.X. Morphine modulates the expression of mu‐opioid receptor exon 5‐associated full‐length C‐terminal splice variants by upregulating miR‐378a‐3p. FASEB J., 2020, 34(3), 4540-4556.
[http://dx.doi.org/10.1096/fj.201901879RR] [PMID: 31999011]
[54]
Tapocik, J.D.; Ceniccola, K.; Mayo, C.L.; Schwandt, M.L.; Solomon, M.; Wang, B.D.; Luu, T.V.; Olender, J.; Harrigan, T.; Maynard, T.M.; Elmer, G.I.; Lee, N.H. MicroRNAs are involved in the development of morphine-induced analgesic tolerance and regulate functionally relevant changes in serpini1. Front. Mol. Neurosci., 2016, 9, 20.
[http://dx.doi.org/10.3389/fnmol.2016.00020] [PMID: 27047334]
[55]
Vasudevan, S.; Tong, Y.; Steitz, J.A. Switching from repression to activation: MicroRNAs can up-regulate translation. Science, 2007, 318(5858), 1931-1934.
[http://dx.doi.org/10.1126/science.1149460] [PMID: 18048652]
[56]
Ørom, U.A.; Nielsen, F.C.; Lund, A.H. MicroRNA-10a binds the 5'UTR of ribosomal protein mRNAs and enhances their translation. Mol. Cell, 2008, 30(4), 460-471.
[http://dx.doi.org/10.1016/j.molcel.2008.05.001] [PMID: 18498749]
[57]
Jacobsen, A.; Wen, J.; Marks, D.S.; Krogh, A. Signatures of RNA binding proteins globally coupled to effective microRNA target sites. Genome Res., 2010, 20(8), 1010-1019.
[http://dx.doi.org/10.1101/gr.103259.109] [PMID: 20508147]
[58]
Wu, S.; Bono, J.; Tao, Y.X. Long noncoding RNA (lncRNA): A target in neuropathic pain. Expert Opin. Ther. Targets, 2019, 23(1), 15-20.
[http://dx.doi.org/10.1080/14728222.2019.1550075] [PMID: 30451044]
[59]
Li, J.; Qi, X.; Jiang, B.; Huang, T.; Luo, L.; Liu, S.; Yin, Z. Phosphorylated heat shock protein 27 inhibits lipopolysaccharide-induced inflammation in Thp1 cells by promoting TLR4 endocytosis, ubiquitination, and degradation. Inflammation, 2019, 42(5), 1788-1799.
[http://dx.doi.org/10.1007/s10753-019-01041-x] [PMID: 31201585]
[60]
Eidson, L.N.; Murphy, A.Z. Blockade of Toll-like receptor 4 attenuates morphine tolerance and facilitates the pain relieving properties of morphine. J. Neurosci., 2013, 33(40), 15952-15963.
[http://dx.doi.org/10.1523/JNEUROSCI.1609-13.2013] [PMID: 24089500]
[61]
Ye, E.A.; Steinle, J.J. miR-146a attenuates inflammatory pathways mediated by TLR4/NF- κ B and TNF α to protect primary human retinal microvascular endothelial cells grown in high glucose. Mediators Inflamm., 2016, 2016, 1-9.
[http://dx.doi.org/10.1155/2016/3958453] [PMID: 26997759]
[62]
Wang, X.; Yin, F.; Li, L.; Kong, H.; You, B.; Zhang, W.; Chen, S.; Peng, J. Intracerebroventricular injection of miR-146a relieves seizures in an immature rat model of lithium-pilocarpine induced status epilepticus. Epilepsy Res., 2018, 139, 14-19.
[http://dx.doi.org/10.1016/j.eplepsyres.2017.10.006] [PMID: 29144992]
[63]
Xie, Q.; Wei, W.; Ruan, J.; Ding, Y.; Zhuang, A.; Bi, X.; Sun, H.; Gu, P.; Wang, Z.; Fan, X. Effects of miR-146a on the osteogenesis of adipose-derived mesenchymal stem cells and bone regeneration. Sci. Rep., 2017, 7(1), 42840.
[http://dx.doi.org/10.1038/srep42840] [PMID: 28205638]
[64]
Wang, Y.; Jiang, W.; Xia, B.; Zhang, M.; Wang, Y. MicroRNA-146a attenuates the development of morphine analgesic tolerance in a rat model. Neurol. Res., 2020, 42(5), 415-421.
[http://dx.doi.org/10.1080/01616412.2020.1735818] [PMID: 32131713]
[65]
Huo, Y.; Zhang, K.; Zhang, T.; Han, Y.; Hu, Z. MiR-124-3p alleviates the dezocine tolerance against pain by regulating TRAF6 in a rat model. Neuroreport, 2021, 32(1), 44-51.
[http://dx.doi.org/10.1097/WNR.0000000000001559] [PMID: 33165190]
[66]
Jo, E.K.; Kim, J.K.; Shin, D.M.; Sasakawa, C. Molecular mechanisms regulating NLRP3 inflammasome activation. Cell. Mol. Immunol., 2016, 13(2), 148-159.
[http://dx.doi.org/10.1038/cmi.2015.95] [PMID: 26549800]
[67]
Grace, P.M.; Strand, K.A.; Galer, E.L.; Urban, D.J.; Wang, X.; Baratta, M.V.; Fabisiak, T.J.; Anderson, N.D.; Cheng, K.; Greene, L.I.; Berkelhammer, D.; Zhang, Y.; Ellis, A.L.; Yin, H.H.; Campeau, S.; Rice, K.C.; Roth, B.L.; Maier, S.F.; Watkins, L.R. Morphine paradoxically prolongs neuropathic pain in rats by amplifying spinal NLRP3 inflammasome activation. Proc. Natl. Acad. Sci. USA, 2016, 113(24), E3441-E3450.
[http://dx.doi.org/10.1073/pnas.1602070113] [PMID: 27247388]
[68]
Bauernfeind, F.; Rieger, A.; Schildberg, F.A.; Knolle, P.A.; Schmid-Burgk, J.L.; Hornung, V. NLRP3 inflammasome activity is negatively controlled by miR-223. J. Immunol., 2012, 189(8), 4175-4181.
[http://dx.doi.org/10.4049/jimmunol.1201516] [PMID: 22984082]
[69]
Yang, Z.; Zhong, L.; Xian, R.; Yuan, B. MicroRNA-223 regulates inflammation and brain injury via feedback to NLRP3 inflammasome after intracerebral hemorrhage. Mol. Immunol., 2015, 65(2), 267-276.
[http://dx.doi.org/10.1016/j.molimm.2014.12.018] [PMID: 25710917]
[70]
Xie, X.J.; Ma, L.G.; Xi, K.; Fan, D.M.; Li, J.G.; Zhang, Q.; Zhang, W. Effects of microRNA-223 on morphine analgesic tolerance by targeting NLRP3 in a rat model of neuropathic pain. Mol. Pain, 2017, 13.
[http://dx.doi.org/10.1177/1744806917706582] [PMID: 28580822]
[71]
Qi, J.; Rice, S.J.; Salzberg, A.C.; Runkle, E.A.; Liao, J.; Zander, D.S.; Mu, D. MiR-365 regulates lung cancer and developmental gene thyroid transcription factor 1. Cell Cycle, 2012, 11(1), 177-186.
[http://dx.doi.org/10.4161/cc.11.1.18576] [PMID: 22185756]
[72]
Sun, Z.; Yu, J.T.; Jiang, T.; Li, M.M.; Tan, L.; Zhang, Q.; Tan, L. Genome-wide microRNA profiling of rat hippocampus after status epilepticus induced by amygdala stimulation identifies modulators of neuronal apoptosis. PLoS One, 2013, 8(10), e78375.
[http://dx.doi.org/10.1371/journal.pone.0078375] [PMID: 24205215]
[73]
Wang, J.; Xu, W.; Zhong, T.; Song, Z.; Zou, Y.; Ding, Z.; Guo, Q.; Dong, X.; Zou, W. miR-365 targets β-arrestin 2 to reverse morphine tolerance in rats. Sci. Rep., 2016, 6(1), 38285.
[http://dx.doi.org/10.1038/srep38285] [PMID: 27922111]
[74]
Wu, X.P.; She, R.X.; Yang, Y.P.; Xing, Z.M.; Chen, H.W.; Zhang, Y.W. MicroRNA-365 alleviates morphine analgesic tolerance via the inactivation of the ERK/CREB signaling pathway by negatively targeting β-arrestin2. J. Biomed. Sci., 2018, 25(1), 10.
[http://dx.doi.org/10.1186/s12929-018-0405-9] [PMID: 29415719]
[75]
Robison, A.J. Emerging role of CaMKII in neuropsychiatric disease. Trends Neurosci., 2014, 37(11), 653-662.
[http://dx.doi.org/10.1016/j.tins.2014.07.001] [PMID: 25087161]
[76]
Wang, Z.J.; Tang, L.; Xin, L. Reversal of morphine antinociceptive tolerance by acute spinal inhibition of Ca2+/calmodulin-dependent protein kinase II. Eur. J. Pharmacol., 2003, 465(1-2), 199-200.
[http://dx.doi.org/10.1016/S0014-2999(03)01484-5] [PMID: 12650850]
[77]
Pan, Z.; Zhu, L.J.; Li, Y.Q.; Hao, L.Y.; Yin, C.; Yang, J.X.; Guo, Y.; Zhang, S.; Hua, L.; Xue, Z.Y.; Zhang, H.; Cao, J.L. Epigenetic modification of spinal miR-219 expression regulates chronic inflammation pain by targeting CaMKIIγ. J. Neurosci., 2014, 34(29), 9476-9483.
[http://dx.doi.org/10.1523/JNEUROSCI.5346-13.2014] [PMID: 25031391]
[78]
Wang, J.; Xu, W.; Shao, J.; He, Z.; Ding, Z.; Huang, J.; Guo, Q.; Zou, W. miR-219-5p targets CaMKIIγ to attenuate morphine tolerance in rats. Oncotarget, 2017, 8(17), 28203-28214.
[http://dx.doi.org/10.18632/oncotarget.15997] [PMID: 28423675]
[79]
Dziedzic, S.A.; Su, Z.; Jean Barrett, V.; Najafov, A.; Mookhtiar, A.K.; Amin, P.; Pan, H.; Sun, L.; Zhu, H.; Ma, A.; Abbott, D.W.; Yuan, J. ABIN-1 regulates RIPK1 activation by linking Met1 ubiquitylation with Lys63 deubiquitylation in TNF-RSC. Nat. Cell Biol., 2018, 20(1), 58-68.
[http://dx.doi.org/10.1038/s41556-017-0003-1] [PMID: 29203883]
[80]
Huang, J.; Liang, X.; Wang, J.; Kong, Y.; Zhang, Z.; Ding, Z.; Song, Z.; Guo, Q.; Zou, W. miR-873a-5p targets A20 to facilitate morphine tolerance in mice. Front. Neurosci., 2019, 13, 347.
[http://dx.doi.org/10.3389/fnins.2019.00347] [PMID: 31024249]
[81]
Bai, L.; Wang, X.; Li, Z.; Kong, C.; Zhao, Y.; Qian, J.L.; Kan, Q.; Zhang, W.; Xu, J.T. Upregulation of chemokine CXCL12 in the dorsal root ganglia and spinal cord contributes to the development and maintenance of neuropathic pain following spared nerve injury in rats. Neurosci. Bull., 2016, 32(1), 27-40.
[http://dx.doi.org/10.1007/s12264-015-0007-4] [PMID: 26781879]
[82]
Wilson, N.M.; Jung, H.; Ripsch, M.S.; Miller, R.J.; White, F.A. CXCR4 signaling mediates morphine-induced tactile hyperalgesia. Brain Behav. Immun., 2011, 25(3), 565-573.
[http://dx.doi.org/10.1016/j.bbi.2010.12.014] [PMID: 21193025]
[83]
Mei, H.X.; Zhou, M.H.; Zhang, X.W.; Huang, X.X.; Wang, Y.L.; Wang, P.F.; Zhan, G.H. Effects of miR-338 on morphine tolerance by targeting CXCR4 in a rat model of bone cancer pain. Biosci. Rep., 2017, 37(2), BSR20160517.
[http://dx.doi.org/10.1042/BSR20160517] [PMID: 28108674]
[84]
Krames, E.S. The role of the dorsal root ganglion in the development of neuropathic pain. Pain Med., 2014, 15(10), 1669-1685.
[http://dx.doi.org/10.1111/pme.12413] [PMID: 24641192]
[85]
Li, Q.; Zhao, X.; Zhong, L.J.; Yang, H.Y.; Wang, Q.; Pu, X.P. Effects of chronic morphine treatment on protein expression in rat dorsal root ganglia. Eur. J. Pharmacol., 2009, 612(1-3), 21-28.
[http://dx.doi.org/10.1016/j.ejphar.2009.03.049] [PMID: 19345208]
[86]
Dominguez, E.; Mauborgne, A.; Mallet, J.; Desclaux, M.; Pohl, M. SOCS3-mediated blockade of JAK/STAT3 signaling pathway reveals its major contribution to spinal cord neuroinflammation and mechanical allodynia after peripheral nerve injury. J. Neurosci., 2010, 30(16), 5754-5766.
[http://dx.doi.org/10.1523/JNEUROSCI.5007-09.2010] [PMID: 20410127]
[87]
Miao, L.; Liu, K.; Xie, M.; Xing, Y.; Xi, T. miR-375 inhibits Helicobacter pylori-induced gastric carcinogenesis by blocking JAK2–STAT3 signaling. Cancer Immunol. Immunother., 2014, 63(7), 699-711.
[http://dx.doi.org/10.1007/s00262-014-1550-y] [PMID: 24718681]
[88]
Li, H.; Tao, R.; Wang, J.; Xia, L. Upregulation of miR-375 level ameliorates morphine analgesic tolerance in mouse dorsal root ganglia by inhibiting the JAK2/STAT3 pathway. J. Pain Res., 2017, 10, 1279-1287.
[http://dx.doi.org/10.2147/JPR.S125264] [PMID: 28603428]
[89]
Mercer, T.R.; Dinger, M.E.; Mattick, J.S. Long non-coding RNAs: Insights into functions. Nat. Rev. Genet., 2009, 10(3), 155-159.
[http://dx.doi.org/10.1038/nrg2521] [PMID: 19188922]
[90]
Ransohoff, J.D.; Wei, Y.; Khavari, P.A. The functions and unique features of long intergenic non-coding RNA. Nat. Rev. Mol. Cell Biol., 2018, 19(3), 143-157.
[http://dx.doi.org/10.1038/nrm.2017.104] [PMID: 29138516]
[91]
Zhu, J.; Fu, H.; Wu, Y.; Zheng, X. Function of lncRNAs and approaches to lncRNA-protein interactions. Sci. China Life Sci., 2013, 56(10), 876-885.
[http://dx.doi.org/10.1007/s11427-013-4553-6] [PMID: 24091684]
[92]
Mercer, T.R.; Mattick, J.S. Structure and function of long noncoding RNAs in epigenetic regulation. Nat. Struct. Mol. Biol., 2013, 20(3), 300-307.
[http://dx.doi.org/10.1038/nsmb.2480] [PMID: 23463315]
[93]
Mercer, T.R.; Dinger, M.E.; Sunkin, S.M.; Mehler, M.F.; Mattick, J.S. Specific expression of long noncoding RNAs in the mouse brain. Proc. Natl. Acad. Sci. USA, 2008, 105(2), 716-721.
[http://dx.doi.org/10.1073/pnas.0706729105] [PMID: 18184812]
[94]
Holdt, L.M.; Hoffmann, S.; Sass, K.; Langenberger, D.; Scholz, M.; Krohn, K.; Finstermeier, K.; Stahringer, A.; Wilfert, W.; Beutner, F.; Gielen, S.; Schuler, G.; Gäbel, G.; Bergert, H.; Bechmann, I.; Stadler, P.F.; Thiery, J.; Teupser, D. Alu elements in ANRIL non-coding RNA at chromosome 9p21 modulate atherogenic cell functions through trans-regulation of gene networks. PLoS Genet., 2013, 9(7), e1003588.
[http://dx.doi.org/10.1371/journal.pgen.1003588] [PMID: 23861667]
[95]
Yang, Z.; Jiang, S.; Shang, J.; Jiang, Y.; Dai, Y.; Xu, B.; Yu, Y.; Liang, Z.; Yang, Y. LncRNA: Shedding light on mechanisms and opportunities in fibrosis and aging. Ageing Res. Rev., 2019, 52, 17-31.
[http://dx.doi.org/10.1016/j.arr.2019.04.001] [PMID: 30954650]
[96]
Jain, A.K.; Xi, Y.; McCarthy, R.; Allton, K.; Akdemir, K.C.; Patel, L.R.; Aronow, B.; Lin, C.; Li, W.; Yang, L.; Barton, M.C. LncPRESS1 Is a p53-regulated LncRNA that safeguards pluripotency by disrupting SIRT6-mediated de-acetylation of histone H3K56. Mol. Cell, 2016, 64(5), 967-981.
[http://dx.doi.org/10.1016/j.molcel.2016.10.039] [PMID: 27912097]
[97]
Kino, T.; Hurt, D.E.; Ichijo, T.; Nader, N.; Chrousos, G.P. Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor. Sci. Signal., 2010, 3(107), ra8.
[http://dx.doi.org/10.1126/scisignal.2000568] [PMID: 20124551]
[98]
Tripathi, V.; Ellis, J.D.; Shen, Z.; Song, D.Y.; Pan, Q.; Watt, A.T.; Freier, S.M.; Bennett, C.F.; Sharma, A.; Bubulya, P.A.; Blencowe, B.J.; Prasanth, S.G.; Prasanth, K.V. The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol. Cell, 2010, 39(6), 925-938.
[http://dx.doi.org/10.1016/j.molcel.2010.08.011] [PMID: 20797886]
[99]
Kumar, P.P.; Emechebe, U.; Smith, R.; Franklin, S.; Moore, B.; Yandell, M.; Lessnick, S.L.; Moon, A.M. Coordinated control of senescence by lncRNA and a novel T-box3 co-repressor complex. eLife, 2014, 3, e02805.
[http://dx.doi.org/10.7554/eLife.02805] [PMID: 24876127]
[100]
Gu, P.; Chen, X.; Xie, R.; Xie, W.; Huang, L.; Dong, W.; Han, J.; Liu, X.; Shen, J.; Huang, J.; Lin, T. A novel AR translational regulator lncRNA LBCS inhibits castration resistance of prostate cancer. Mol. Cancer, 2019, 18(1), 109.
[http://dx.doi.org/10.1186/s12943-019-1037-8] [PMID: 31221168]
[101]
Tay, Y.; Rinn, J.; Pandolfi, P.P. The multilayered complexity of ceRNA crosstalk and competition. Nature, 2014, 505(7483), 344-352.
[http://dx.doi.org/10.1038/nature12986] [PMID: 24429633]
[102]
Ma, J.; Pan, Z.Z. Contribution of brainstem GABAA synaptic transmission to morphine analgesic tolerance. Pain, 2006, 122(1), 163-173.
[http://dx.doi.org/10.1016/j.pain.2006.01.031] [PMID: 16527406]
[103]
Ahmadi, S.; Miraki, F.; Rostamzadeh, J. Association of morphine-induced analgesic tolerance with changes in gene expression of GluN1 and MOR1 in rat spinal cord and midbrain. Iran. J. Basic Med. Sci., 2016, 19(9), 924-931.
[PMID: 27803778]
[104]
Sepehrizadeh, Z.; Bahrololoumi Shapourabadi, M.; Ahmadi, S.; Hashemi Bozchlou, S.; Zarrindast, M.R.; Sahebgharani, M. Decreased AMPA GluR2, but not GluR3, mRNA expression in rat amygdala and dorsal hippocampus following morphine-induced behavioural sensitization. Clin. Exp. Pharmacol. Physiol., 2008, 35(11), 1321-1330.
[http://dx.doi.org/10.1111/j.1440-1681.2008.05004.x] [PMID: 18671727]
[105]
Shao, J.; Wang, J.; Huang, J.; Liu, C.; Pan, Y.; Guo, Q.; Zou, W. Identification of lncRNA expression profiles and ceRNA analysis in the spinal cord of morphine-tolerant rats. Mol. Brain, 2018, 11(1), 21.
[http://dx.doi.org/10.1186/s13041-018-0365-8] [PMID: 29636075]
[106]
Ammon-Treiber, S.; Höllt, V. Morphine-induced changes of gene expression in the brain. Addict. Biol., 2005, 10(1), 81-89.
[http://dx.doi.org/10.1080/13556210412331308994] [PMID: 15849022]
[107]
Ahmadi, S.; Zobeiri, M.; Mohammadi Talvar, S.; Masoudi, K.; Khanizad, A.; Fotouhi, S.; Bradburn, S. Differential expression of H19, BC1, MIAT1, and MALAT1 long non-coding RNAs within key brain reward regions after repeated morphine treatment. Behav. Brain Res., 2021, 414, 113478.
[http://dx.doi.org/10.1016/j.bbr.2021.113478] [PMID: 34302875]
[108]
Kennedy, N.M.; Schmid, C.L.; Ross, N.C.; Lovell, K.M.; Yue, Z.; Chen, Y.T.; Cameron, M.D.; Bohn, L.M.; Bannister, T.D. Optimization of a series of Mu Opioid Receptor (MOR) agonists with high g protein signaling bias. J. Med. Chem., 2018, 61(19), 8895-8907.
[http://dx.doi.org/10.1021/acs.jmedchem.8b01136] [PMID: 30199635]
[109]
Kibaly, C.; Lin, H.Y.; Loh, H.H.; Law, P.Y. Spinal or supraspinal phosphorylation deficiency at the MOR C-terminus does not affect morphine tolerance in vivo. Pharmacol. Res., 2017, 119, 153-168.
[http://dx.doi.org/10.1016/j.phrs.2017.01.033] [PMID: 28179123]
[110]
Deng, M.; Zhang, Z.; Xing, M.; Liang, X.; Li, Z.; Wu, J.; Jiang, S.; Weng, Y.; Guo, Q.; Zou, W. LncRNA MRAK159688 facilitates morphine tolerance by promoting REST-mediated inhibition of mu opioid receptor in rats. Neuropharmacology, 2022, 206, 108938.
[http://dx.doi.org/10.1016/j.neuropharm.2021.108938] [PMID: 34982972]
[111]
Qiu, Y.; Meng, L.; Di, C.; Huo, Y.; Yao, B.; Zhang, T.; Hua, Z. Exploration of the differentially expressed long noncoding RNAs and genes of morphine tolerance via bioinformatic analysis. J. Comput. Biol., 2019, 26(12), 1379-1393.
[http://dx.doi.org/10.1089/cmb.2019.0188] [PMID: 31290683]
[112]
Memczak, S.; Jens, M.; Elefsinioti, A.; Torti, F.; Krueger, J.; Rybak, A.; Maier, L.; Mackowiak, S.D.; Gregersen, L.H.; Munschauer, M.; Loewer, A.; Ziebold, U.; Landthaler, M.; Kocks, C.; le Noble, F.; Rajewsky, N. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature, 2013, 495(7441), 333-338.
[http://dx.doi.org/10.1038/nature11928] [PMID: 23446348]
[113]
Jeck, W.R.; Sorrentino, J.A.; Wang, K.; Slevin, M.K.; Burd, C.E.; Liu, J.; Marzluff, W.F.; Sharpless, N.E. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA, 2013, 19(2), 141-157.
[http://dx.doi.org/10.1261/rna.035667.112] [PMID: 23249747]
[114]
Guo, J.U.; Agarwal, V.; Guo, H.; Bartel, D.P. Expanded identification and characterization of mammalian circular RNAs. Genome Biol., 2014, 15(7), 409.
[http://dx.doi.org/10.1186/s13059-014-0409-z] [PMID: 25070500]
[115]
Zhang, X.O.; Dong, R.; Zhang, Y.; Zhang, J.L.; Luo, Z.; Zhang, J.; Chen, L.L.; Yang, L. Diverse alternative back-splicing and alternative splicing landscape of circular RNAs. Genome Res., 2016, 26(9), 1277-1287.
[http://dx.doi.org/10.1101/gr.202895.115] [PMID: 27365365]
[116]
Izuogu, O.G.; Alhasan, A.A.; Mellough, C.; Collin, J.; Gallon, R.; Hyslop, J.; Mastrorosa, F.K.; Ehrmann, I.; Lako, M.; Elliott, D.J.; Santibanez-Koref, M.; Jackson, M.S. Analysis of human ES cell differentiation establishes that the dominant isoforms of the lncRNAs RMST and FIRRE are circular. BMC Genomics, 2018, 19(1), 276.
[http://dx.doi.org/10.1186/s12864-018-4660-7] [PMID: 29678151]
[117]
Huang, C.; Liang, D.; Tatomer, D.C.; Wilusz, J.E. A length-dependent evolutionarily conserved pathway controls nuclear export of circular RNAs. Genes Dev., 2018, 32(9-10), 639-644.
[http://dx.doi.org/10.1101/gad.314856.118] [PMID: 29773557]
[118]
Zhou, W.Y.; Cai, Z.R.; Liu, J.; Wang, D.S.; Ju, H.Q.; Xu, R.H. Circular RNA: metabolism, functions and interactions with proteins. Mol. Cancer, 2020, 19(1), 172.
[http://dx.doi.org/10.1186/s12943-020-01286-3] [PMID: 33317550]
[119]
Chen, L.L. The expanding regulatory mechanisms and cellular functions of circular RNAs. Nat. Rev. Mol. Cell Biol., 2020, 21(8), 475-490.
[http://dx.doi.org/10.1038/s41580-020-0243-y] [PMID: 32366901]
[120]
Vo, J.N.; Cieslik, M.; Zhang, Y.; Shukla, S.; Xiao, L.; Zhang, Y.; Wu, Y.M.; Dhanasekaran, S.M.; Engelke, C.G.; Cao, X.; Robinson, D.R.; Nesvizhskii, A.I.; Chinnaiyan, A.M. The landscape of circular RNA in cancer. Cell, 2019, 176(4), 869-881.e13.
[http://dx.doi.org/10.1016/j.cell.2018.12.021] [PMID: 30735636]
[121]
Aufiero, S.; Reckman, Y.J.; Pinto, Y.M.; Creemers, E.E. Circular RNAs open a new chapter in cardiovascular biology. Nat. Rev. Cardiol., 2019, 16(8), 503-514.
[http://dx.doi.org/10.1038/s41569-019-0185-2] [PMID: 30952956]
[122]
Mehta, S.L.; Dempsey, R.J.; Vemuganti, R. Role of circular RNAs in brain development and CNS diseases. Prog. Neurobiol., 2020, 186, 101746.
[http://dx.doi.org/10.1016/j.pneurobio.2020.101746] [PMID: 31931031]
[123]
Kristensen, L.S.; Hansen, T.B.; Venø, M.T.; Kjems, J. Circular RNAs in cancer: Opportunities and challenges in the field. Oncogene, 2018, 37(5), 555-565.
[http://dx.doi.org/10.1038/onc.2017.361] [PMID: 28991235]
[124]
Weng, W.; Wei, Q.; Toden, S.; Yoshida, K.; Nagasaka, T.; Fujiwara, T.; Cai, S.; Qin, H.; Ma, Y.; Goel, A. Circular RNA ciRS-7—A promising prognostic biomarker and a potential therapeutic target in colorectal cancer. Clin. Cancer Res., 2017, 23(14), 3918-3928.
[http://dx.doi.org/10.1158/1078-0432.CCR-16-2541] [PMID: 28174233]
[125]
Smid, M.; Wilting, S.M.; Uhr, K.; Rodríguez-González, F.G.; de Weerd, V.; Prager-Van der Smissen, W.J.C.; van der Vlugt-Daane, M.; van Galen, A.; Nik-Zainal, S.; Butler, A.; Martin, S.; Davies, H.R.; Staaf, J.; van de Vijver, M.J.; Richardson, A.L.; MacGrogan, G.; Salgado, R.; van den Eynden, G.G.G.M.; Purdie, C.A.; Thompson, A.M.; Caldas, C.; Span, P.N.; Sweep, F.C.G.J.; Simpson, P.T.; Lakhani, S.R.; Van Laere, S.; Desmedt, C.; Paradiso, A.; Eyfjord, J.; Broeks, A.; Vincent-Salomon, A.; Futreal, A.P.; Knappskog, S.; King, T.; Viari, A.; Børresen-Dale, A.L.; Stunnenberg, H.G.; Stratton, M.; Foekens, J.A.; Sieuwerts, A.M.; Martens, J.W.M. The circular RNome of primary breast cancer. Genome Res., 2019, 29(3), 356-366.
[http://dx.doi.org/10.1101/gr.238121.118] [PMID: 30692147]
[126]
Kristensen, L.S.; Andersen, M.S.; Stagsted, L.V.W.; Ebbesen, K.K.; Hansen, T.B.; Kjems, J. The biogenesis, biology and characterization of circular RNAs. Nat. Rev. Genet., 2019, 20(11), 675-691.
[http://dx.doi.org/10.1038/s41576-019-0158-7] [PMID: 31395983]
[127]
Rybak-Wolf, A.; Stottmeister, C.; Glažar, P.; Jens, M.; Pino, N.; Giusti, S.; Hanan, M.; Behm, M.; Bartok, O.; Ashwal-Fluss, R.; Herzog, M.; Schreyer, L.; Papavasileiou, P.; Ivanov, A.; Öhman, M.; Refojo, D.; Kadener, S.; Rajewsky, N. Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Mol. Cell, 2015, 58(5), 870-885.
[http://dx.doi.org/10.1016/j.molcel.2015.03.027] [PMID: 25921068]
[128]
Xu, K.; Zhang, Y.; Li, J. Expression and function of circular RNAs in the mammalian brain. Cell. Mol. Life Sci., 2021, 78(9), 4189-4200.
[http://dx.doi.org/10.1007/s00018-021-03780-3] [PMID: 33558994]
[129]
Viswanath, O.; Urits, I.; Burns, J.; Charipova, K.; Gress, K.; McNally, A.; Urman, R.D.; Welschmeyer, A.; Berger, A.A.; Kassem, H.; Sanchez, M.G.; Kaye, A.D.; Eubanks, T.N.; Cornett, E.M.; Ngo, A.L. Central neuropathic mechanisms in pain signaling pathways: Current evidence and recommendations. Adv. Ther., 2020, 37(5), 1946-1959.
[http://dx.doi.org/10.1007/s12325-020-01334-w] [PMID: 32291648]
[130]
Pan, Z.; Li, G.F.; Sun, M.L.; Xie, L.; Liu, D.; Zhang, Q.; Yang, X.X.; Xia, S.; Liu, X.; Zhou, H.; Xue, Z.Y.; Zhang, M.; Hao, L.Y.; Zhu, L.J.; Cao, J.L. MicroRNA-1224 splicing circularRNA-Filip1l in an Ago2-dependent manner regulates chronic inflammatory pain via targeting Ubr5. J. Neurosci., 2019, 39(11), 2125-2143.
[http://dx.doi.org/10.1523/JNEUROSCI.1631-18.2018] [PMID: 30651325]
[131]
Zhang, S.B.; Lin, S.Y.; Liu, M.; Liu, C.C.; Ding, H.H.; Sun, Y.; Ma, C.; Guo, R.X.; Lv, Y.Y.; Wu, S.L.; Xu, T.; Xin, W.J. CircAnks1a in the spinal cord regulates hypersensitivity in a rodent model of neuropathic pain. Nat. Commun., 2019, 10(1), 4119.
[http://dx.doi.org/10.1038/s41467-019-12049-0] [PMID: 31511520]
[132]
Weng, Y.; Wu, J.; Li, L.; Shao, J.; Li, Z.; Deng, M.; Zou, W. Circular RNA expression profile in the spinal cord of morphine tolerated rats and screen of putative key circRNAs. Mol. Brain, 2019, 12(1), 79.
[http://dx.doi.org/10.1186/s13041-019-0498-4] [PMID: 31533844]
[133]
Xing, M.; Deng, M.; Shi, Y.; Dai, J.; Ding, T.; Song, Z.; Zou, W. Identification and characterization of N6-methyladenosine circular RNAs in the spinal cord of morphine-tolerant rats. Front. Neurosci., 2022, 16, 967768.
[http://dx.doi.org/10.3389/fnins.2022.967768] [PMID: 35992914]

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