Increased miR-132-3p expression is associated with chronic neuropathic pain

Experimental Neurology

Volumn 283, Issue , 2016, Pages 276-286

  Leinders, M ^a,b   Uceyler N ^a   Pritchard, R A ^b   Sommer, C ^a   Sorkin, L S ^b  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

miR 132; neuroimmune; Neuropathic pain; PEAP; polyneuropathy; SNI

Indexed keywords

AMPA RECEPTOR; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; MICRORNA 132; MICRORNA 132 3P; UNCLASSIFIED DRUG; ACTIVATING TRANSCRIPTION FACTOR 3; ATF3 PROTEIN, RAT; LOCKED NUCLEIC ACID; MESSENGER RNA; MICRORNA; MIRN1323 MICRORNA, HUMAN; OLIGONUCLEOTIDE;

ADULT; AGED; ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL LEVEL; CHRONIC PAIN; CONTROLLED STUDY; DISEASE ASSOCIATION; EXPERIMENTAL PAIN TEST; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; HUMAN; HUMAN TISSUE; LEUKOCYTE; MAJOR CLINICAL STUDY; MALE; MICROGLIA; NERVE BIOPSY; NEUROIMMUNOLOGY; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; PAIN ASSESSMENT; PATHOPHYSIOLOGY; PERIPHERAL NEUROPATHY; PLACE ESCAPE AVOIDANCE PARADIGM; PRIORITY JOURNAL; RAT; SPINAL CORD; SPINAL GANGLION; SURAL NERVE; UPREGULATION; ANIMAL; AVOIDANCE BEHAVIOR; BLOOD; CHEMISTRY; CHRONIC DISEASE; COHORT ANALYSIS; DISEASE MODEL; DRUG EFFECT; GENETICS; METABOLISM; MIDDLE AGED; NEURALGIA; PAIN MEASUREMENT; PAIN THRESHOLD; PATHOLOGY; PHYSIOLOGY; VERY ELDERLY;

ACTIVATING TRANSCRIPTION FACTOR 3; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; AVOIDANCE LEARNING; CHRONIC DISEASE; COHORT STUDIES; DISEASE MODELS, ANIMAL; FEMALE; GANGLIA, SPINAL; HUMANS; LEUKOCYTES; MALE; MICRORNAS; MIDDLE AGED; NEURALGIA; OLIGONUCLEOTIDES; PAIN MEASUREMENT; PAIN THRESHOLD; RATS; RECEPTORS, AMPA; RNA, MESSENGER; UP-REGULATION;

EID: 84976650064     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2016.06.025     Document Type: Article

References (65)

1. Aldrich, B.T., Frakes, E.P., Kasuya, J., Hammond, D.L., Kitamoto, T., Changes in expression of sensory organ-specific microRNAs in rat dorsal root ganglia in association with mechanical hypersensitivity induced by spinal nerve ligation. Neuroscience 164 (2009), 711–723.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J., Basic local alignment search tool. J. Mol. Biol. 215 (1990), 403–410.
3. Andersen, H.H., Duroux, M., Gazerani, P., Serum MicroRNA Signatures in Migraineurs During Attacks and in Pain-Free Periods. Mol. Neurobiol. 53 (2016), 1494–1500.
4. Arai, M., Genda, Y., Ishikawa, M., Shunsuke, T., Okabe, T., Sakamoto, A., The miRNA and mRNA changes in rat hippocampi after chronic constriction injury. Pain Med. 14 (2013), 720–729.
5. Bai, G., Ambalavanar, R., Wei, D., Dessem, D., Downregulation of selective microRNAs in trigeminal ganglion neurons following inflammatory muscle pain. Mol. Pain, 3, 2007, 15.
6. Basbaum, A.I., Bautista, D.M., Scherrer, G., Julius, D., Cellular and molecular mechanisms of pain. Cell 139 (2009), 267–284.
7. Betel, D., Wilson, M., Gabow, A., Marks, D.S., Sander, C., The microRNA.org resource: targets and expression. Nucleic Acids Res. 36 (2008), D149–D153.
8. Beyer, C., Zampetaki, A., Lin, N.Y., Kleyer, A., Perricone, C., Iagnocco, A., Distler, A., Langley, S.R., Gelse, K., Sesselmann, S., Lorenzini, R., Niemeier, A., Swoboda, B., Distler, J.H., Santer, P., Egger, G., Willeit, J., Mayr, M., Schett, G., Kiechl, S., Signature of circulating microRNAs in osteoarthritis. Ann. Rheum. Dis., 74, 2015, e18.
9. Bjersing, J.L., Lundborg, C., Bokarewa, M.I., Mannerkorpi, K., Profile of cerebrospinal microRNAs in fibromyalgia. PLoS One, 8, 2013, e78762.
10. Bouhassira, D., Attal, N., Fermanian, J., Alchaar, H., Gautron, M., Masquelier, E., Rostaing, S., Lanteri-Minet, M., Collin, E., Grisart, J., Boureau, F., Development and validation of the Neuropathic Pain Symptom Inventory. Pain 108 (2004), 248–257.
11. Bredy, T.W., Lin, Q., Wei, W., Baker-Andresen, D., Mattick, J.S., MicroRNA regulation of neural plasticity and memory. Neurobiol. Learn. Mem. 96 (2011), 89–94.
12. Breivik, H., Collett, B., Ventafridda, V., Cohen, R., Gallacher, D., Survey of chronic pain in Europe: prevalence, impact on daily life, and treatment. Eur. J. Pain 10 (2006), 287–333.
13. Calin, G.A., Croce, C.M., MicroRNA signatures in human cancers. Nat. Rev. Cancer 6 (2006), 857–866.
14. Calvo, M., Dawes, J.M., Bennett, D.L., The role of the immune system in the generation of neuropathic pain. Lancet Neurol. 11 (2012), 629–642.
15. Chaplan, S.R., Bach, F.W., Pogrel, J.W., Chung, J.M., Yaksh, T.L., Quantitative assessment of tactile allodynia in the rat paw. J. Neurosci. Methods 53 (1994), 55–63.
16. Cheng, H.Y., Papp, J.W., Varlamova, O., Dziema, H., Russell, B., Curfman, J.P., Nakazawa, T., Shimizu, K., Okamura, H., Impey, S., Obrietan, K., microRNA modulation of circadian-clock period and entrainment. Neuron 54 (2007), 813–829.
17. Cogswell, J.P., Ward, J., Taylor, I.A., Waters, M., Shi, Y., Cannon, B., Kelnar, K., Kemppainen, J., Brown, D., Chen, C., Prinjha, R.K., Richardson, J.C., Saunders, A.M., Roses, A.D., Richards, C.A., Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways. J. Alzheimers Dis. 14 (2008), 27–41.
18. Decosterd, I., Woolf, C.J., Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87 (2000), 149–158.
19. Dirig, D.M., Salami, A., Rathbun, M.L., Ozaki, G.T., Yaksh, T.L., Characterization of variables defining hindpaw withdrawal latency evoked by radiant thermal stimuli. J. Neurosci. Methods 76 (1997), 183–191.
20. Dyck, P., Thomas, P., Engelstad, J., Peripheral Neuropathy. 2005, Elsevier Saunders, Philadelphia.
21. Edbauer, D., Neilson, J.R., Foster, K.A., Wang, C.F., Seeburg, D.P., Batterton, M.N., Tada, T., Dolan, B.M., Sharp, P.A., Sheng, M., Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron 65 (2010), 373–384.
22. Elramah, S., Landry, M., Favereaux, A., MicroRNAs regulate neuronal plasticity and are involved in pain mechanisms. Front. Cell. Neurosci., 8, 2014, 31.
23. Friedman, R.C., Farh, K.K., Burge, C.B., Bartel, D.P., Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19 (2009), 92–105.
24. Fuchs, P.N., McNabb, C.T., The place escape/avoidance paradigm: a novel method to assess nociceptive processing. J. Integr. Neurosci. 11 (2012), 61–72.
25. Gillardon, F., Mack, M., Rist, W., Schnack, C., Lenter, M., Hildebrandt, T., Hengerer, B., MicroRNA and proteome expression profiling in early-symptomatic alpha-synuclein(A30P)-transgenic mice. Proteomics Clin. Appl. 2 (2008), 697–705.
26. Hansen, K.F., Sakamoto, K., Wayman, G.A., Impey, S., Obrietan, K., Transgenic miR132 alters neuronal spine density and impairs novel object recognition memory. PLoS One, 5, 2010, e15497.
27. Hansen, K.F., Karelina, K., Sakamoto, K., Wayman, G.A., Impey, S., Obrietan, K., miRNA-132: a dynamic regulator of cognitive capacity. Brain Struct. Funct. 218 (2013), 817–831.
28. Haramati, S., Navon, I., Issler, O., Ezra-Nevo, G., Gil, S., Zwang, R., Hornstein, E., Chen, A., MicroRNA as repressors of stress-induced anxiety: the case of amygdalar miR-34. J. Neurosci. 31 (2011), 14191–14203.
29. Hartmann, B., Ahmadi, S., Heppenstall, P.A., Lewin, G.R., Schott, C., Borchardt, T., Seeburg, P.H., Zeilhofer, H.U., Sprengel, R., Kuner, R., The AMPA receptor subunits GluR-A and GluR-B reciprocally modulate spinal synaptic plasticity and inflammatory pain. Neuron 44 (2004), 637–650.
30. Hsu, S.D., Lin, F.M., Wu, W.Y., Liang, C., Huang, W.C., Chan, W.L., Tsai, W.T., Chen, G.Z., Lee, C.J., Chiu, C.M., Chien, C.H., Wu, M.C., Huang, C.Y., Tsou, A.P., Huang, H.D., miRTarBase: a database curates experimentally validated microRNA-target interactions. Nucleic Acids Res. 39 (2011), D163–D169.
31. Huttenhofer, A., Schattner, P., The principles of guiding by RNA: chimeric RNA-protein enzymes. Nat. Rev. Genet. 7 (2006), 475–482.
32. Imai, S., Saeki, M., Yanase, M., Horiuchi, H., Abe, M., Narita, M., Kuzumaki, N., Suzuki, T., Narita, M., Change in microRNAs associated with neuronal adaptive responses in the nucleus accumbens under neuropathic pain. J. Neurosci. 31 (2011), 15294–15299.
33. Ji, R.R., Berta, T., Nedergaard, M., Glia and pain: is chronic pain a gliopathy?. Pain 154:Suppl. 1 (2013), S10–S28.
34. Joilin, G., Guevremont, D., Ryan, B., Claudianos, C., Cristino, A.S., Abraham, W.C., Williams, J.M., Rapid regulation of microRNA following induction of long-term potentiation in vivo. Front. Mol. Neurosci., 7, 2014, 98.
35. Kimura, J., Electrodiagnosis in diseases of nerve and muscle: Principles and practice. 2001, Oxford University Press Third edition, New York.
36. Kuner, R., Central mechanisms of pathological pain. Nat. Med. 16 (2010), 1258–1266.
37. Kusuda, R., Cadetti, F., Ravanelli, M.I., Sousa, T.A., Zanon, S., De Lucca, F.L., Lucas, G., Differential expression of microRNAs in mouse pain models. Mol. Pain, 7, 2011, 17.
38. Lee, S.T., Chu, K., Im, W.S., Yoon, H.J., Im, J.Y., Park, J.E., Park, K.H., Jung, K.H., Lee, S.K., Kim, M., Roh, J.K., Altered microRNA regulation in Huntington's disease models. Exp. Neurol. 227 (2011), 172–179.
39. Malkmus, S.A., Yaksh, T.L., Intrathecal catheterization and drug delivery in the rat. Methods Mol. Med. 99 (2004), 109–121.
40. Marques-Rocha, J.L., Samblas, M., Milagro, F.I., Bressan, J., Martinez, J.A., Marti, A., Noncoding RNAs, cytokines, and inflammation-related diseases. FASEB J. 29 (2015), 3595–3611.
41. Mattick, J.S., RNA regulation: a new genetics?. Nat. Rev. Genet. 5 (2004), 316–323.
42. McMahon, S.B., Malcangio, M., Current challenges in glia-pain biology. Neuron 64 (2009), 46–54.
43. Miller, B.H., Zeier, Z., Xi, L., Lanz, T.A., Deng, S., Strathmann, J., Willoughby, D., Kenny, P.J., Elsworth, J.D., Lawrence, M.S., Roth, R.H., Edbauer, D., Kleiman, R.J., Wahlestedt, C., MicroRNA-132 dysregulation in schizophrenia has implications for both neurodevelopment and adult brain function. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 3125–3130.
44. O'Connor, R.M., Dinan, T.G., Cryan, J.F., Little things on which happiness depends: microRNAs as novel therapeutic targets for the treatment of anxiety and depression. Mol. Psychiatry 17 (2012), 359–376.
45. Orlova, I.A., Alexander, G.M., Qureshi, R.A., Sacan, A., Graziano, A., Barrett, J.E., Schwartzman, R.J., Ajit, S.K., MicroRNA modulation in complex regional pain syndrome. J. Transl. Med., 9, 2011, 195.
46. Paraskevopoulou, M.D., Georgakilas, G., Kostoulas, N., Vlachos, I.S., Vergoulis, T., Reczko, M., Filippidis, C., Dalamagas, T., Hatzigeorgiou, A.G., DIANA-microT web server v5.0: service integration into miRNA functional analysis workflows. Nucleic Acids Res. 41 (2013), W169–W173.
47. Pauley, K.M., Satoh, M., Chan, A.L., Bubb, M.R., Reeves, W.H., Chan, E.K., Upregulated miR-146a expression in peripheral blood mononuclear cells from rheumatoid arthritis patients. Arthritis Res. Ther., 10, 2008, R101.
48. Ryan, M.M., Mason-Parker, S.E., Tate, W.P., Abraham, W.C., Williams, J.M., Rapidly induced gene networks following induction of long-term potentiation at perforant path synapses in vivo. Hippocampus 21 (2011), 541–553.
49. Ryan, M.M., Ryan, B., Kyrke-Smith, M., Logan, B., Tate, W.P., Abraham, W.C., Williams, J.M., Temporal profiling of gene networks associated with the late phase of long-term potentiation in vivo. PLoS One, 7, 2012, e40538.
50. Schratt, G., microRNAs at the synapse. Nat. Rev. Neurosci. 10 (2009), 842–849.
51. Soreq, H., Wolf, Y., NeurimmiRs: microRNAs in the neuroimmune interface. Trends Mol. Med. 17 (2011), 548–555.
52. Stein, C.A., Exploiting the potential of antisense: beyond phosphorothioate oligodeoxynucleotides. Chem. Biol. 3 (1996), 319–323.
53. Stein, C.A., The experimental use of antisense oligonucleotides: a guide for the perplexed. J. Clin. Invest. 108 (2001), 641–644.
54. Taganov, K.D., Boldin, M.P., Chang, K.J., Baltimore, D., NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 12481–12486.
55. Taves, S., Berta, T., Chen, G., Ji, R.R., Microglia and spinal cord synaptic plasticity in persistent pain. Neural Plast., 2013, 2013, 753656.
56. Tsang, J., Zhu, J., van Oudenaarden, A., MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol. Cell 26 (2007), 753–767.
57. Üçeyler, N., Rogausch, J.P., Toyka, K.V., Sommer, C., Differential expression of cytokines in painful and painless neuropathies. Neurology 69 (2007), 42–49.
58. Üçeyler, N., Riediger, N., Kafke, W., Sommer, C., Differential gene expression of cytokines and neurotrophic factors in nerve and skin of patients with peripheral neuropathies. J. Neurol. 262 (2015), 203–212.
59. Von Korff, M., Ormel, J., Keefe, F.J., Dworkin, S.F., Grading the severity of chronic pain. Pain 50 (1992), 133–149.
60. von Schack, D., Agostino, M.J., Murray, B.S., Li, Y., Reddy, P.S., Chen, J., Choe, S.E., Strassle, B.W., Li, C., Bates, B., Zhang, L., Hu, H., Kotnis, S., Bingham, B., Liu, W., Whiteside, G.T., Samad, T.A., Kennedy, J.D., Ajit, S.K., Dynamic changes in the microRNA expression profile reveal multiple regulatory mechanisms in the spinal nerve ligation model of neuropathic pain. PLoS One, 6, 2011, e17670.
61. Wang, W.X., Huang, Q., Hu, Y., Stromberg, A.J., Nelson, P.T., Patterns of microRNA expression in normal and early Alzheimer's disease human temporal cortex: white matter versus gray matter. Acta Neuropathol. 121 (2011), 193–205.
62. Wibrand, K., Panja, D., Tiron, A., Ofte, M.L., Skaftnesmo, K.O., Lee, C.S., Pena, J.T., Tuschl, T., Bramham, C.R., Differential regulation of mature and precursor microRNA expression by NMDA and metabotropic glutamate receptor activation during LTP in the adult dentate gyrus in vivo. Eur. J. Neurosci. 31 (2010), 636–645.
63. Wibrand, K., Pai, B., Siripornmongcolchai, T., Bittins, M., Berentsen, B., Ofte, M.L., Weigel, A., Skaftnesmo, K.O., Bramham, C.R., MicroRNA regulation of the synaptic plasticity-related gene Arc. PLoS One, 7, 2012, e41688.
64. Zhang, Z., Chang, H., Li, Y., Zhang, T., Zou, J., Zheng, X., Wu, J., MicroRNAs: potential regulators involved in human anencephaly. Int. J. Biochem. Cell Biol. 42 (2010), 367–374.
65. Zhang, R., Huang, M., Cao, Z., Qi, J., Qiu, Z., Chiang, L.Y., MeCP2 plays an analgesic role in pain transmission through regulating CREB / miR-132 pathway. Mol. Pain, 11, 2015, 19.