Emerging roles of microRNAs in chronic pain

Neurochemistry International

Volumn 77, Issue , 2014, Pages 58-67

  Sakai, Atsushi ^a   Suzuki, Hidenori ^a  

^a NIPPON MEDICAL SCHOOL   (Japan)

Author keywords

Astrocyte; Cancer pain; Hyperexcitability; Inflammatory pain; Microglia; microRNA; Neuroinflammation; Neuropathic pain; Primary sensory neuron; Spinal cord

Indexed keywords

MICRORNA; MICRORNA 103; MICRORNA 124A; MICRORNA 146A; MICRORNA 1A 3P; MICRORNA 21; MICRORNA 7A; UNCLASSIFIED DRUG;

CENTRAL NERVOUS SYSTEM; CHRONIC PAIN; GENE EXPRESSION; GENETIC ASSOCIATION; GLIA CELL; HUMAN; INFLAMMATORY DISEASE; NEOPLASM; NERVE CELL; NONHUMAN; PERIPHERAL NERVE INJURY; PROTEIN EXPRESSION; REVIEW; SENSORY GANGLION; SOMATOSENSORY SYSTEM; SPINAL CORD INJURY; ANIMAL; BRAIN CHEMISTRY; GENETICS; METABOLISM; SPINAL CORD;

ANIMALS; BRAIN CHEMISTRY; CHRONIC PAIN; HUMANS; MICRORNAS; SPINAL CORD;

EID: 84907589170     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2014.05.010     Document Type: Review

References (106)

1. B.T. Aldrich, E.P. Frakes, J. Kasuya, D.L. Hammond, and T. Kitamoto 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. L. Alvarez-Erviti, Y. Seow, H. Yin, C. Betts, S. Lakhal, and M.J.A. Wood Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes Nat. Biotechnol. 29 2011 341 345
3. M. Ammari, C. Jorgensen, and F. Apparailly Impact of microRNAs on the understanding and treatment of rheumatoid arthritis Curr. Opin. Rheumatol. 25 2013 225 233
4. A.V. Apkarian, J.A. Hashmi, and M.N. Baliki Pain and the brain: specificity and plasticity of the brain in clinical chronic pain Pain 152 2011 S49 S64
5. M. Arai, Y. Genda, M. Ishikawa, T. Shunsuke, T. Okabe, and A. Sakamoto The miRNA and mRNA changes in rat hippocampi after chronic constriction injury Pain Med. 14 2013 720 729
6. G. Bai, R. Ambalavanar, D. Wei, and D. Dessem Downregulation of selective microRNAs in trigeminal ganglion neurons following inflammatory muscle pain Mol. Pain 3 2007 15
7. K.K. Bali, D. Selvaraj, V.P. Satagopam, J. Lu, R. Schneider, and R. Kuner Genome-wide identification and functional analyses of microRNA signatures associated with cancer pain EMBO Mol. Med. 5 2013 1740 1758
8. M.N. Baliki, P.Y. Geha, H.L. Fields, and A.V. Apkarian Predicting value of pain and analgesia: nucleus accumbens response to noxious stimuli changes in the presence of chronic pain Neuron 66 2010 149 160
9. D.P. Bartel MicroRNAs: target recognition and regulatory functions Cell 136 2009 215 233
10. A.I. Basbaum, D.M. Bautista, G. Scherrer, and D. Julius Cellular and molecular mechanisms of pain Cell 139 2009 267 284
11. A.S. Beutler, and M. Reinhardt AAV for pain: steps towards clinical translation Gene Ther. 16 2009 461 469
12. O.G. Bhalala, L. Pan, V. Sahni, T.L. McGuire, K. Gruner, W.G. Tourtellotte, and J.A. Kessler microRNA-21 regulates astrocytic response following spinal cord injury J. Neurosci. 32 2012 17935 17947
13. O.G. Bhalala, M. Srikanth, and J.A. Kessler The emerging roles of microRNAs in CNS injuries Nat. Rev. Neurol. 9 2013 328 339
14. J.L. Bjersing, C. Lundborg, M.I. Bokarewa, and K. Mannerkorpi Profile of cerebrospinal microRNAs in fibromyalgia PLoS One 8 2013 e78762
15. T. Brandenburger, M. Castoldi, M. Brendel, H. Grievink, L. Schlösser, R. Werdehausen, I. Bauer, and H. Hermanns Expression of spinal cord microRNAs in a rat model of chronic neuropathic pain Neurosci. Lett. 506 2012 281 286
16. B. Buller, X. Liu, X. Wang, R.L. Zhang, L. Zhang, A. Hozeska-Solgot, M. Chopp, and Z.G. Zhang MicroRNA-21 protects neurons from ischemic death FEBS J. 277 2010 4299 4307
17. M.C. Bushnell, M. Čeko, and L.A. Low Cognitive and emotional control of pain and its disruption in chronic pain Nat. Rev. Neurosci. 14 2013 502 511
18. M. Chakrabarti, N.L. Banik, and S.K. Ray miR-7-1 potentiated estrogen receptor agonists for functional neuroprotection in VSC4.1 motoneurons Neuroscience 256 2014 322 333
19. E.K.L. Chan, A. Ceribelli, and M. Satoh MicroRNA-146a in autoimmunity and innate immune responses Ann. Rheum. Dis. 72 2013 ii90 ii95
20. H.P. Chen, W. Zhou, L.M. Kang, H. Yan, L. Zhang, B.H. Xu, and W.H. Cai Intrathecal miR-96 inhibits Nav1.3 expression and alleviates neuropathic pain in rat following chronic construction injury Neurochem. Res. 39 2014 76 83
21. E.D. Crown The role of mitogen activated protein kinase signaling in microglia and neurons in the initiation and maintenance of chronic pain Exp. Neurol. 234 2012 330 339
22. A. de Chevigny, N. Coré, P. Follert, M. Gaudin, P. Barbry, C. Béclin, and H. Cremer miR-7a regulation of Pax6 controls spatial origin of forebrain dopaminergic neurons Nat. Neurosci. 15 2012 1120 1126
23. V. Deretic, T. Saitoh, and S. Akira Autophagy in infection, inflammation and immunity Nat. Rev. Immunol. 13 2013 722 737
24. M. Devor Sodium channels and mechanisms of neuropathic pain J. Pain 7 2006 S3 S12
25. R.H. Dworkin, A.B. O'Connor, J. Kent, S.C. Mackey, S.N. Raja, B.R. Stacey, R.M. Levy, M. Backonja, R. Baron, H. Harke, J.D. Loeser, R.D. Treede, D.C. Turk, and C.D. Wells Interventional management of neuropathic pain: NeuPSIG recommendations Pain 154 2013 2249 2261
26. A. Favereaux, O. Thoumine, R. Bouali-Benazzouz, V. Roques, M.A. Papon, S.A. Salam, G. Drutel, C. Léger, A. Calas, F. Nagy, and M. Landry Bidirectional integrative regulation of Cav1.2 calcium channel by microRNA miR-103: role in pain EMBO J. 30 2011 3830 3841
27. P. Fossat, E. Dobremez, R. Bouali-Benazzouz, A. Favereaux, S.S. Bertrand, K. Kilk, C. Léger, J.R. Cazalets, Ü. Langel, M. Landry, and F. Nagy Knockdown of L calcium channel subtypes: differential effects in neuropathic pain J. Neurosci. 30 2010 1073 1085
28. N.H. Fourie, R.M. Peace, S.K. Abey, L.B. Sherwin, B. Rahim-Williams, P.A. Smyser, J.W. Wiley, and W.A. Henderson Elevated circulating miR-150 and miR-342-3p in patients with irritable bowel syndrome Exp. Mol. Pathol. 96 2014 422 425
29. R.C. Friedman, K.K. Farh, C.B. Burge, and D.P. Bartel Most mammalian mRNAs are conserved targets of microRNAs Genome Res. 19 2009 92 105
30. S. Fujita, T. Ito, T. Mizutani, S. Minoguchi, N. Yamamichi, K. Sakurai, and H. Iba miR-21 gene expression triggered by AP-1 is sustained through a double-negative feedback mechanism J. Mol. Biol. 378 2008 492 504
31. Y. Genda, M. Arai, M. Ishikawa, S. Tanaka, T. Okabe, and A. Sakamoto MicroRNA changes in the dorsal horn of the spinal cord of rats with chronic constriction injury: a TaqMan® Low Density Array study Int. J. Mol. Med. 31 2013 129 137
32. S.M. Géranton, C. Morenilla-Palao, and S.P. Hunt A role for transcriptional repressor methyl-CpG-binding protein 2 and plasticity-related gene serum- and glucocorticoid-inducible kinase 1 in the induction of inflammatory pain states J. Neurosci. 27 2007 6163 6173
33. S.M. Géranton, V. Fratto, K.K. Tochiki, and S.P. Hunt Descending serotonergic controls regulate inflammation-induced mechanical sensitivity and methyl-CpG-binding protein 2 phosphorylation in the rat superficial dorsal horn Mol. Pain 4 2008 35
34. A.H. Gheinani, F.C. Burkhard, and K. Monastyrskaya Deciphering microRNA code in pain and inflammation: lessons from bladder pain syndrome Cell. Mol. Life Sci. 70 2013 3773 3789
35. J.R. Goss, D. Krisky, J. Wechuck, and D. Wolfe Herpes simplex virus-based nerve targeting gene therapy in pain management J. Pain Res. 7 2014 71 79
36. Y. He, C. Yang, C.M. Kirkmire, and Z.J. Wang Regulation of opioid tolerance by let-7 family microRNA targeting the μ opioid receptor J. Neurosci. 30 2010 10251 10258
37. Y. Hori, G. Goto, M. Arai-Iwasaki, M. Ishikawa, and A. Sakamoto Differential expression of rat hippocampal microRNAs in two rat models of chronic pain Int. J. Mol. Med. 32 2013 1287 1292
38. G. Hu, H. Yao, A.D. Chaudhuri, M. Duan, S.V. Yelamanchili, H. Wen, P.D. Cheney, H.S. Fox, and S. Buch Exosome-mediated shuttling of microRNA-29 regulates HIV Tat and morphine-mediated neuronal dysfunction Cell Death Dis. 3 2012 e381
39. Y. Huang, Y.B. Yang, X.H. Zhang, X.L. Yu, Z.B. Wang, and X.C. Cheng MicroRNA-21 gene and cancer Med. Oncol. 30 2013 376
40. Y.B. Im, M.K. Jee, J.I. Choi, H.T. Cho, O.H. Kwon, and S.K. Kang Molecular targeting of NOX4 for neuropathic pain after traumatic injury of the spinal cord Cell Death Dis. 3 2012 e426
41. S. Imai, M. Saeki, M. Yanase, H. Horiuchi, M. Abe, M. Narita, N. Kuzumaki, T. Suzuki, and M. Narita Change in microRNAs associated with neuronal adaptive responses in the nucleus accumbens under neuropathic pain J. Neurosci. 31 2011 15294 15299
42. L.L. Isom, D.S. Ragsdale, K.S. De Jongh, R.E. Westenbroek, B.F.X. Reber, T. Scheuer, and W.A. Catterall Structure and function of the β2 subunit of brain sodium channels, a transmembrane glycoprotein with a CAM motif Cell 83 1995 433 442
43. R.R. Ji, and G. Strichartz Cell signaling and the genesis of neuropathic pain Sci. STKE 2004 2004 re14
44. R.R. Ji, T. Kohno, K.A. Moore, and C.J. Woolf Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci. 26 2003 696 705
45. R.R. Ji, T. Berta, and M. Nedergaard Glia and pain: is chronic pain a gliopathy? Pain 154 2013 S10 S28
46. E. Junn, K.W. Lee, B.S. Jeong, T.W. Chan, J.Y. Im, and M.M. Mouradian Repression of α-synuclein expression and toxicity by microRNA-7 Proc. Natl. Acad. Sci. USA 106 2009 13052 13057
47. Y. Kawasaki, Z.Z. Xu, X. Wang, J.Y. Park, Z.Y. Zhuang, P.H. Tan, Y.J. Gao, K. Roy, G. Corfas, E.H. Lo, and R.R. Ji Distinct roles of matrix metalloproteases in the early- and late-phase development of neuropathic pain Nat. Med. 14 2008 331 336
48. R. Kumarswamy, I. Volkmann, and T. Thum Regulation and function of miRNA-21 in health and disease RNA Biol. 8 2011 706 713
49. R. Kuner Central mechanisms of pathological pain Nat. Med. 16 2010 1258 1266
50. R. Kusuda, F. Cadetti, M.I. Ravanelli, T.A. Sousa, S. Zanon, F.L. De Lucca, and G. Lucas Differential expression of microRNAs in mouse pain models Mol. Pain 7 2011 17
51. K.L. Kynast, O.Q. Russe, C.V. Möser, G. Geisslinger, and E. Niederberger Modulation of central nervous system-specific microRNA-124a alters the inflammatory response in the formalin test in mice Pain 154 2013 368 376
52. X. Li, G. Gibson, J.S. Kim, J. Kroin, S. Xu, A.J. van Wijnen, and H.J. Im MicroRNA-146a is linked to pain-related pathophysiology of osteoarthritis Gene 480 2011 34 41
53. X. Li, J.S. Kroin, R. Kc, G. Gibson, D. Chen, G.T. Corbett, K. Pahan, S. Fayyaz, J.S. Kim, A.J. van Wijnen, J. Suh, S.G. Kim, and H.J. Im Altered spinal microRNA-146a and the microRNA-183 cluster contribute to osteoarthritic pain in knee joints J. Bone Miner. Res. 28 2013 2512 2522
54. C.R. Lin, K.H. Chen, C.H. Yang, H.Y. Huang, and S.M. Sheen-Chen Intrathecal miR-183 delivery suppresses mechanical allodynia in mononeuropathic rats Eur. J. Neurosci. 39 2014 1682 1689
55. N.K. Liu, X.F. Wang, Q.B. Lu, and X.M. Xu Altered microRNA expression following traumatic spinal cord injury Exp. Neurol. 219 2009 424 429
56. L.F. Lopez-Santiago, M. Pertin, X. Morisod, C. Chen, S. Hong, J. Wiley, I. Decosterd, and L.L. Isom Sodium channel β2 subunits regulate tetrodotoxin-sensitive sodium channels in small dorsal root ganglion neurons and modulate the response to pain J. Neurosci. 26 2006 7984 7994
57. L.A. McWilliams, B.J. Cox, and M.W. Enns Mood and anxiety disorders associated with chronic pain: an examination in a nationally representative sample Pain 106 2003 127 133
58. F. Meng, R. Henson, H. Wehbe-Janek, K. Ghoshal, S.T. Jacob, and T. Patel MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer Gastroenterology 133 2007 647 658
59. S. Montagner, E.M. Orlandi, S. Merante, and S. Monticelli The role of miRNAs in mast cells and other innate immune cells Immunol. Rev. 253 2013 12 24
60. L. Morel, M. Regan, H. Higashimori, S.K. Ng, C. Esau, S. Vidensky, J. Rothstein, and Y. Yang Neuronal exosomal miRNA-dependent translational regulation of astroglial glutamate transporter GLT1 J. Biol. Chem. 288 2013 7105 7116
61. S. Mullenbrock, J. Shah, and G.M. Cooper Global expression analysis identified a preferentially nerve growth factor-induced transcriptional program regulated by sustained mitogen-activated protein kinase/extracellular signal-regulated kinase (ERK) and AP-1 protein activation during PC12 cell differentiation J. Biol. Chem. 286 2011 45131 45145
62. K. Nakanishi, T. Nakasa, N. Tanaka, M. Ishikawa, K. Yamada, K. Yamasaki, N. Kamei, B. Izumi, N. Adachi, S. Miyaki, H. Asahara, and M. Ochi Responses of microRNAs 124a and 223 following spinal cord injury in mice Spinal Cord 48 2010 192 196
63. K. Obara, and Y. Ohsumi Atg14: a key player in orchestrating autophagy Int. J. Cell Biol. 2011 2011 713435
64. K. Obata, H. Yamanaka, K. Kobayashi, Y. Dai, T. Mizushima, H. Katsura, T. Fukuoka, A. Tokunaga, and K. Noguchi Role of mitogen-activated protein kinase activation in injured and intact primary afferent neurons for mechanical and heat hypersensitivity after spinal nerve ligation J. Neurosci. 24 2004 10211 10222
65. I.A. Orlova, G.M. Alexander, R.A. Qureshi, A. Sacan, A. Graziano, J.E. Barrett, R.J. Schwartzman, and S.K. Ajit MicroRNA modulation in complex regional pain syndrome J. Transl. Med. 9 2011 195
66. C.K. Park, Z.Z. Xu, T. Berta, Q. Han, G. Chen, X.J. Liu, and R.R. Ji Extracellular microRNAs activate nociceptor neurons to elicit pain via TLR7 and TRPA1 Neuron 82 2014 47 54
67. K.W. Poh, J.F. Yeo, and W.Y. Ong MicroRNA changes in the mouse prefrontal cortex after inflammatory pain Eur. J. Pain 15 2011 801.e1 801.e12
68. E.D. Ponomarev, T. Veremeyko, N. Barteneva, A.M. Krichevsky, and H.L. Weiner MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-α-PU.1 pathway Nat. Med. 17 2011 64 70
69. P. Rao, E. Benito, and A. Fischer MicroRNAs as biomarkers for CNS disease Front. Mol. Neurosci. 6 2013 39
70. A. Rebane, and C.A. Akdis MicroRNAs: essential players in the regulation of inflammation J. Allergy Clin. Immunol. 132 2013 15 26
71. J.B. Redell, J. Zhao, and P.K. Dash Altered expression of miRNA-21 and its targets in the hippocampus after traumatic brain injury J. Neurosci. Res. 89 2011 212 221
72. C.Y. Saab Pain-related changes in the brain: diagnostic and therapeutic potentials Trends Neurosci. 35 2012 629 637
73. A. Sakai, and H. Suzuki Nerve injury-induced upregulation of miR-21 in the primary sensory neurons contributes to neuropathic pain in rats Biochem. Biophys. Res. Commun. 435 2013 176 181
74. A. Sakai, F. Saitow, N. Miyake, K. Miyake, T. Shimada, and H. Suzuki miR-7a alleviates the maintenance of neuropathic pain through regulation of neuronal excitability Brain 136 2013 2738 2750
75. D. Sayed, and M. Abdellatif MicroRNAs in development and disease Physiol. Rev. 91 2011 827 887
76. S.D. Selcuklu, M.T.A. Donoghue, and C. Spillane miR-21 as a key regulator of oncogenic processes Biochem. Soc. Trans. 37 2009 918 925
77. Aα-1receptor subunit down-regulation in adult spinal cord following neonatal cystitis-induced chronic visceral pain in rats Pain 154 2013 59 70
78. Y. Shi, X. Zhang, X. Tang, P. Wang, H. Wang, and Y. Wang MiR-21 is continually elevated long-term in the brain after exposure to ionizing radiation Radiat. Res. 177 2012 124 128
79. G. Shi, J. Shi, K. Liu, N. Liu, Y. Wang, Z. Fu, J. Ding, L. Jia, and W. Yuan Increased miR-195 aggravates neuropathic pain by inhibiting autophagy following peripheral nerve injury Glia 61 2013 504 512
80. J. Smythies, and L. Edelstein Transsynaptic modality codes in the brain: possible involvement of synchronized spike timing, microRNAs, exosomes and epigenetic processes Front. Integr. Neurosci. 6 2012 126
81. R.E. Sorge, T. Trang, R. Dorfman, S.B. Smith, S. Beggs, J. Ritchie, J.S. Austin, D.V. Zaykin, H.V. Meulen, M. Costigan, T.A. Herbert, M. Yarkoni-Abitbul, D. Tichauer, J. Livneh, E. Gershon, M. Zheng, K. Tan, S.L. John, G.D. Slade, J. Jordan, C.J. Woolf, G. Peltz, W. Maixner, L. Diatchenko, Z. Seltzer, M.W. Salter, and J.S. Mogil Genetically determined P2X7 receptor pore formation regulates variability in chronic pain sensitivity Nat. Med. 18 2012 595 599
82. P.L. Stemkowski, and P.A. Smith Sensory neurons, ion channels, inflammation and the onset of neuropathic pain Can. J. Neurol. Sci. 39 2012 416 435
83. E.R. Strickland, M.A. Hook, S. Balaraman, J.R. Huie, J.W. Grau, and R.C. Miranda MicroRNA dysregulation following spinal cord contusion: implications for neural plasticity and repair Neuroscience 186 2011 146 160
84. I.T. Strickland, L. Richards, F.E. Holmes, D. Wynick, J.B. Uney, and L.F. Wong Axotomy-induced miR-21 promotes axon growth in adult dorsal root ganglion neurons PLoS One 6 2011 e23423
85. K. Takasu, A. Sakai, H. Hanawa, T. Shimada, and H. Suzuki Overexpression of GDNF in the uninjured DRG exerts analgesic effects on neuropathic pain following segmental spinal nerve ligation in mice J. Pain 12 2011 1130 1139
86. S. Tam Tam, I. Bastian, X.F. Zhou, H.M. Vander, M.Z. Michael, I.L. Gibbins, and R.V. Haberberger MicroRNA-143 expression in dorsal root ganglion neurons Cell Tissue Res. 346 2011 163 173
87. A.J. Todd Neuronal circuitry for pain processing in the dorsal horn Nat. Rev. Neurosci. 11 2010 823 836
88. L. Vannucci, M. Lai, F. Chiuppesi, L. Ceccherini-Nelli, and M. Pistello Viral vectors: a look back and ahead on gene transfer technology New Microbiol. 36 2013 1 22
89. D. von Schack, M.J. Agostino, B.S. Murray, Y. Li, P.S. Reddy, J. Chen, S.E. Choe, B.W. Strassle, C. Li, B. Bates, L. Zhang, H. Hu, S. Kotnis, B. Bingham, W. Liu, G.T. Whiteside, T.A. Samad, J.D. Kennedy, and S.K. Ajit 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
90. Z. Wang MiRNA in the regulation of ion channel/transporter expression Compr. Physiol. 3 2013 599 653
91. L. Wang, M. Chopp, A. Szalad, Y. Zhang, X. Wang, R.L. Zhang, X.S. Liu, L. Jia, and Z.G. Zhang The role of miR-146a in dorsal root ganglia neurons of experimental diabetic peripheral neuropathy Neuroscience 259 2013 155 163
92. S.G. Waxman, and G.W. Zamponi Regulating excitability of peripheral afferents: emerging ion channel targets Nat. Neurosci. 17 2014 153 163
93. S.G. Waxman, J.D. Kocsis, and J.A. Black Type III sodium channel mRNA is expressed in embryonic but not adult spinal sensory neurons, and is reexpressed following axotomy J. Neurophysiol. 72 1994 466 470
94. H.L. Willemen, X.J. Huo, Q.L. Mao-Ying, J. Zijlstra, C.J. Heijnen, and A. Kavelaars MicroRNA-124 as a novel treatment for persistent hyperalgesia J. Neuroinflammation 9 2012 143
95. D. Wu, M. Raafat, E. Pak, S. Hammond, and A.K. Murashov MicroRNA machinery responds to peripheral nerve lesion in an injury-regulated pattern Neuroscience 190 2011 386 397
96. H. Xin, Y. Li, B. Buller, M. Katakowski, Y. Zhang, X. Wang, X. Shang, Z.G. Zhang, and M. Chopp Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth Stem Cells 30 2012 1556 1564
97. J.T. Xu, H.Y. Tu, W.J. Xin, X.G. Liu, G.H. Zhang, and C.H. Zhai Activation of phosphatidylinositol 3-kinase and protein kinase B/Akt in dorsal root ganglia and spinal cord contributes to the neuropathic pain induced by spinal nerve ligation in rats Exp. Neurol. 206 2007 269 279
98. Y. Xu, L. Li, X. Xiang, H. Wang, W. Cai, J. Xie, Y. Han, S. Bao, and Q. Xie Three common functional polymorphisms in microRNA encoding genes in the susceptibility to hepatocellular carcinoma: a systematic review and meta-analysis Gene 527 2013 584 593
99. B. Yu, S. Zhou, T. Qian, Y. Wang, F. Ding, and X. Gu Altered microRNA expression following sciatic nerve resection in dorsal root ganglia of rats Acta Biochim. Biophys. Sin. (Shanghai) 43 2011 909 915
100. B. Yu, S. Zhou, Y. Wang, G. Ding, F. Ding, and X. Gu Profile of microRNAs following rat sciatic nerve injury by deep sequencing: implication for mechanisms of nerve regeneration PLoS One 6 2011 e24612
101. C. Yu, W.P. Chen, and X.H. Wang MicroRNA in osteoarthritis J. Int. Med. Res. 39 2011 1 9
102. M. Yunta, M. Nieto-Díaz, F.J. Esteban, M. Caballero-López, R. Navarro-Ruíz, D. Reigada, D.W. Pita-Thomas, Á. del Águila, T. Muñoz-Galdeano, and R.M. Maza MicroRNA dysregulation in the spinal cord following traumatic injury PLoS One 7 2012 e34534
103. H.Y. Zhang, S.J. Zheng, J.H. Zhao, W. Zhao, L.F. Zheng, D. Zhao, J.M. Li, X.F. Zhang, Z.B. Chen, and X.N. Yi MicroRNAs 144, 145, and 214 are down-regulated in primary neurons responding to sciatic nerve transection Brain Res. 1383 2011 62 70
104. J. Zhao, M.C. Lee, A. Momin, C.M. Cendan, S.T. Shepherd, M.D. Baker, C. Asante, L. Bee, A. Bethry, J.R. Perkins, M.A. Nassar, B. Abrahamsen, A. Dickenson, B.S. Cobb, M. Merkenschlager, and J.N. Wood Small RNAs control sodium channel expression, nociceptor excitability, and pain thresholds J. Neurosci. 30 2010 10860 10871
105. S. Zhou, B. Yu, T. Qian, D. Yao, Y. Wang, F. Ding, and X. Gu Early changes of microRNAs expression in the dorsal root ganglia following rat sciatic nerve transection Neurosci. Lett. 494 2011 89 93
106. S. Zhou, D. Shen, Y. Wang, L. Gong, X. Tang, B. Yu, X. Gu, and F. Ding microRNA-222 targeting PTEN promotes neurite outgrowth from adult dorsal root ganglion neurons following sciatic nerve transection PLoS One 7 2012 e44768