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MicroRNA Changes in Preconditioning-Induced Neuroprotection

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Abstract

Preconditioning is a paradigm in which sublethal stress–prior to a more injurious insult–induces protection against injury. In the central nervous system (CNS), preconditioning against ischemic stroke is induced by short durations of ischemia, brief seizures, exposure to anesthetics, and other stresses. Increasing evidence supports the contribution of microRNAs (miRNAs) to the pathogenesis of cerebral ischemia and ischemic tolerance induced by preconditioning. Studies investigating miRNA changes induced by preconditioning have to date identified 562 miRNAs that change expression levels after preconditioning, and 15% of these changes were reproduced in at least one additional study. Of miRNAs assessed as changed by preconditioning in more than one study, about 40% changed in the same direction in more than one study. Most of the studies to assess the role of specific miRNAs in the neuroprotective mechanism of preconditioning were performed in vitro, with fewer studies manipulating individual miRNAs in vivo. Thus, while many miRNAs change in response to preconditioning stimuli, the mechanisms underlying their effects are not well understood. The data does suggest that miRNAs may play significant roles in preconditioning-induced neuroprotection. This review focuses on the current state of knowledge of the possible role of miRNAs in preconditioning-induced cerebral protection.

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References

  1. Dirnagl U, Becker K, Meisel A. Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. The Lancet Neurology. 2009;8(4):398–412. doi:10.1016/s1474-4422(09)70054-7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Dirnagl U, Meisel A. Endogenous neuroprotection: mitochondria as gateways to cerebral preconditioning? Neuropharmacology. 2008;55(3):334–44. doi:10.1016/j.neuropharm.2008.02.017.

    Article  CAS  PubMed  Google Scholar 

  3. McDonough A, Weinstein JR. Neuroimmune response in ischemic preconditioning. Neurotherapeutics: the journal of the American Society for Experimental NeuroTherapeutics. 2016;13(4):748–61. doi:10.1007/s13311-016-0465-z.

    Article  CAS  Google Scholar 

  4. Stevens SL, Vartanian KB, Stenzel-Poore MP. Reprogramming the response to stroke by preconditioning. Stroke. 2014;45(8):2527–31. doi:10.1161/STROKEAHA.114.002879.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Meller R, Thompson SJ, Lusardi TA, Ordonez AN, Ashley MD, Jessick V, et al. Ubiquitin proteasome-mediated synaptic reorganization: a novel mechanism underlying rapid ischemic tolerance. The Journal of neuroscience : the official journal of the Society for Neuroscience. 2008;28(1):50–9. doi:10.1523/jneurosci.3474-07.2008.

    Article  CAS  Google Scholar 

  6. Bhuiyan MI, Kim YJ. Mechanisms and prospects of ischemic tolerance induced by cerebral preconditioning. International neurourology journal. 2010;14(4):203–12. doi:10.5213/inj.2010.14.4.203.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Kaneko T, Yokoyama K, Makita K. Late preconditioning with isoflurane in cultured rat cortical neurones. Br J Anaesth. 2005;95(5):662–8. doi:10.1093/bja/aei228.

    Article  CAS  PubMed  Google Scholar 

  8. Stenzel-Poore MP, Stevens SL, King JS, Simon RP. Preconditioning reprograms the response to ischemic injury and primes the emergence of unique endogenous neuroprotective phenotypes: a speculative synthesis. Stroke. 2007;38(2 Suppl):680–5. doi:10.1161/01.STR.0000251444.56487.4c.

    Article  PubMed  Google Scholar 

  9. Kitagawa K, Matsumoto M, Tagaya M, Hata R, Ueda H, Niinobe M, et al. 'Ischemic tolerance' phenomenon found in the brain. Brain Res. 1990;528(1):21–4.

    Article  CAS  PubMed  Google Scholar 

  10. Barone FC, White RF, Spera PA, Ellison J, Currie RW, Wang X, et al. Ischemic preconditioning and brain tolerance: temporal histological and functional outcomes, protein synthesis requirement, and interleukin-1 receptor antagonist and early gene expression. Stroke. 1998;29(9):1937–50. discussion 50-1

    Article  CAS  PubMed  Google Scholar 

  11. Obrenovitch TP. Molecular physiology of preconditioning-induced brain tolerance to ischemia. Physiol Rev. 2008;88(1):211–47. doi:10.1152/physrev.00039.2006.

    Article  CAS  PubMed  Google Scholar 

  12. Stenzel-Poore MP, Stevens SL, Xiong Z, Lessov NS, Harrington CA, Mori M, et al. Effect of ischaemic preconditioning on genomic response to cerebral ischaemia: similarity to neuroprotective strategies in hibernation and hypoxia-tolerant states. Lancet (London, England). 2003;362(9389):1028–37. doi:10.1016/s0140-6736(03)14412-1.

    Article  CAS  Google Scholar 

  13. Stenzel-Poore MP, Stevens SL, Simon RP. Genomics of preconditioning. Stroke. 2004;35(11 Suppl 1):2683–6. doi:10.1161/01.STR.0000143735.89281.bb.

    Article  CAS  PubMed  Google Scholar 

  14. Garcia-Bonilla L, Benakis C, Moore J, Iadecola C, Anrather J. Immune mechanisms in cerebral ischemic tolerance. Front Neurosci. 2014;8:44. doi:10.3389/fnins.2014.00044.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Ambros V. The functions of animal microRNAs. Nature. 2004;431(7006):350–5. doi:10.1038/nature02871.

    Article  CAS  PubMed  Google Scholar 

  16. Ouyang YB, Stary CM, Yang GY, Giffard R. MicroRNAs: innovative targets for cerebral ischemia and stroke. Curr Drug Targets. 2013;14(1):90–101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Barwari T, Joshi A, Mayr M. MicroRNAs in cardiovascular disease. J Am Coll Cardiol. 2016;68(23):2577–84. doi:10.1016/j.jacc.2016.09.945.

    Article  CAS  PubMed  Google Scholar 

  18. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136(2):215–33. doi:10.1016/j.cell.2009.01.002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Place RF, Li LC, Pookot D, Noonan EJ, Dahiya R. MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc Natl Acad Sci U S A. 2008;105(5):1608–13. doi:10.1073/pnas.0707594105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Duursma AM, Kedde M, Schrier M, le Sage C, Agami R. MiR-148 targets human DNMT3b protein coding region. RNA (New York, NY). 2008;14(5):872–7. doi:10.1261/rna.972008.

    Article  CAS  Google Scholar 

  21. Cardoso AL, Guedes JR, de Lima MC. Role of microRNAs in the regulation of innate immune cells under neuroinflammatory conditions. Curr Opin Pharmacol. 2016;26:1–9. doi:10.1016/j.coph.2015.09.001.

    Article  CAS  PubMed  Google Scholar 

  22. Meza-Sosa KF, Pedraza-Alva G, Perez-Martinez L. MicroRNAs: key triggers of neuronal cell fate. Front Cell Neurosci. 2014;8:175. doi:10.3389/fncel.2014.00175.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Stappert L, Roese-Koerner B, Brustle O. The role of microRNAs in human neural stem cells, neuronal differentiation and subtype specification. Cell Tissue Res. 2015;359(1):47–64. doi:10.1007/s00441-014-1981-y.

    Article  CAS  PubMed  Google Scholar 

  24. Su W, Aloi MS, Garden GA. MicroRNAs mediating CNS inflammation: small regulators with powerful potential. Brain Behav Immun. 2016;52:1–8. doi:10.1016/j.bbi.2015.07.003.

    Article  PubMed  Google Scholar 

  25. Singh T, Jauhari A, Pandey A, Singh P, Pant AB, Parmar D, et al. Regulatory triangle of neurodegeneration, adult neurogenesis and microRNAs. CNS & neurological disorders drug targets. 2014;13(1):96–103.

    Article  Google Scholar 

  26. Lee ST, Chu K, Jung KH, Yoon HJ, Jeon D, Kang KM, et al. MicroRNAs induced during ischemic preconditioning. Stroke. 2010;41(8):1646–51. doi:10.1161/strokeaha.110.579649.

    Article  PubMed  Google Scholar 

  27. Ouyang YB, Giffard RG. MicroRNAs regulate the chaperone network in cerebral ischemia. Transl Stroke Res. 2013;4(6):693–703. doi:10.1007/s12975-013-0280-3.

    Article  CAS  PubMed  Google Scholar 

  28. Stary CM, Xu L, Sun X, Ouyang YB, White RE, Leong J, et al. MicroRNA-200c contributes to injury from transient focal cerebral ischemia by targeting Reelin. Stroke. 2015;46(2):551–6. doi:10.1161/strokeaha.114.007041.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Zeng L, Liu J, Wang Y, Wang L, Weng S, Tang Y, et al. MicroRNA-210 as a novel blood biomarker in acute cerebral ischemia. Frontiers in bioscience (Elite edition). 2011;3:1265–72.

    Google Scholar 

  30. Ziu M, Fletcher L, Rana S, Jimenez DF, Digicaylioglu M. Temporal differences in microRNA expression patterns in astrocytes and neurons after ischemic injury. PLoS One. 2011;6(2):e14724. doi:10.1371/journal.pone.0014724.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Dharap A, Bowen K, Place R, Li LC, Vemuganti R. Transient focal ischemia induces extensive temporal changes in rat cerebral microRNAome. Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism. 2009;29(4):675–87. doi:10.1038/jcbfm.2008.157.

    Article  CAS  Google Scholar 

  32. Saugstad JA. Non-coding RNAs in stroke and neuroprotection. Front Neurol. 2015;6:50. doi:10.3389/fneur.2015.00050.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Jimenez-Mateos EM. Role of microRNAs in innate neuroprotection mechanisms due to preconditioning of the brain. Front Neurosci. 2015;9:118. doi:10.3389/fnins.2015.00118.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Thompson JW, Dave KR, Young JI, Perez-Pinzon MA. Ischemic preconditioning alters the epigenetic profile of the brain from ischemic intolerance to ischemic tolerance. Neurotherapeutics : the journal of the American Society for Experimental NeuroTherapeutics. 2013;10(4):789–97. doi:10.1007/s13311-013-0202-9.

    Article  CAS  Google Scholar 

  35. Lusardi TA, Farr CD, Faulkner CL, Pignataro G, Yang T, Lan J, et al. Ischemic preconditioning regulates expression of microRNAs and a predicted target, MeCP2, in mouse cortex. Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism. 2010;30(4):744–56. doi:10.1038/jcbfm.2009.253.

    Article  CAS  Google Scholar 

  36. Dharap A, Vemuganti R. Ischemic pre-conditioning alters cerebral microRNAs that are upstream to neuroprotective signaling pathways. J Neurochem. 2010;113(6):1685–91. doi:10.1111/j.1471-4159.2010.06735.x.

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Hu K, Xie YY, Zhang C, Ouyang DS, Long HY, Sun DN, et al. MicroRNA expression profile of the hippocampus in a rat model of temporal lobe epilepsy and miR-34a-targeted neuroprotection against hippocampal neurone cell apoptosis post-status epilepticus. BMC Neurosci. 2012;13:115. doi:10.1186/1471-2202-13-115.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Buller B, Liu X, Wang X, Zhang RL, Zhang L, Hozeska-Solgot A, et al. MicroRNA-21 protects neurons from ischemic death. FEBS J. 2010;277(20):4299–307. doi:10.1111/j.1742-4658.2010.07818.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Moon JM, Xu L, Giffard RG. Inhibition of microRNA-181 reduces forebrain ischemia-induced neuronal loss. Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism. 2013;33(12):1976–82. doi:10.1038/jcbfm.2013.157.

    Article  CAS  Google Scholar 

  40. Ouyang YB, Lu Y, Yue S, Xu LJ, Xiong XX, White RE, et al. MiR-181 regulates GRP78 and influences outcome from cerebral ischemia in vitro and in vivo. Neurobiol Dis. 2012;45(1):555–63. doi:10.1016/j.nbd.2011.09.012.

    Article  CAS  PubMed  Google Scholar 

  41. Wang P, Liang J, Li Y, Li J, Yang X, Zhang X, et al. Down-regulation of miRNA-30a alleviates cerebral ischemic injury through enhancing beclin 1-mediated autophagy. Neurochem Res. 2014;39(7):1279–91. doi:10.1007/s11064-014-1310-6.

    Article  CAS  PubMed  Google Scholar 

  42. Wang P, Zhang N, Liang J, Li J, Han S, Li J. Micro-RNA-30a regulates ischemia-induced cell death by targeting heat shock protein HSPA5 in primary cultured cortical neurons and mouse brain after stroke. J Neurosci Res. 2015;93(11):1756–68. doi:10.1002/jnr.23637.

    Article  CAS  PubMed  Google Scholar 

  43. Wei N, Xiao L, Xue R, Zhang D, Zhou J, Ren H, et al. MicroRNA-9 mediates the cell apoptosis by targeting Bcl2l11 in ischemic stroke. Mol Neurobiol. 2015; doi:10.1007/s12035-015-9605-4.

  44. Zhou X, Su S, Li S, Pang X, Chen C, Li J, et al. MicroRNA-146a down-regulation correlates with neuroprotection and targets pro-apoptotic genes in cerebral ischemic injury in vitro. Brain Res. 2016;1648(Pt A):136–43. doi:10.1016/j.brainres.2016.07.034.

    Article  CAS  PubMed  Google Scholar 

  45. Duris K, Lipkova J. The role of microRNA in ischemic and hemorrhagic stroke. Current drug delivery 2016.

  46. Meng R, Ding Y, Asmaro K, Brogan D, Meng L, Sui M, et al. Ischemic conditioning is safe and effective for octo- and nonagenarians in stroke prevention and treatment. Neurotherapeutics : the journal of the American Society for Experimental NeuroTherapeutics. 2015;12(3):667–77. doi:10.1007/s13311-015-0358-6.

    Article  CAS  Google Scholar 

  47. Slagsvold KH, Moreira JB, Rognmo O, Hoydal M, Bye A, Wisloff U, et al. Remote ischemic preconditioning preserves mitochondrial function and activates pro-survival protein kinase Akt in the left ventricle during cardiac surgery: a randomized trial. Int J Cardiol. 2014;177(2):409–17. doi:10.1016/j.ijcard.2014.09.206.

    Article  PubMed  Google Scholar 

  48. Tian Y, Li H, Liu P, Xu JM, Irwin MG, Xia Z, et al. Captopril pretreatment produces an additive cardioprotection to isoflurane preconditioning in attenuating myocardial ischemia reperfusion injury in rabbits and in humans. Mediat Inflamm. 2015;2015:819232. doi:10.1155/2015/819232.

    Article  Google Scholar 

  49. Wang Y, Reis C, Applegate R 2nd, Stier G, Martin R, Zhang JH. Ischemic conditioning-induced endogenous brain protection: applications pre-, per- or post-stroke. Exp Neurol. 2015;272:26–40. doi:10.1016/j.expneurol.2015.04.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Guicciardi ME, Gores GJ. Life and death by death receptors. FASEB journal : official publication of the Federation of American Societies for Experimental Biology. 2009;23(6):1625–37. doi:10.1096/fj.08-111005.

    Article  CAS  Google Scholar 

  51. Urdinguio RG, Sanchez-Mut JV, Esteller M. Epigenetic mechanisms in neurological diseases: genes, syndromes, and therapies. The Lancet Neurology. 2009;8(11):1056–72. doi:10.1016/s1474-4422(09)70262-5.

    Article  CAS  PubMed  Google Scholar 

  52. Chen S, Guttridge DC, You Z, Zhang Z, Fribley A, Mayo MW, et al. Wnt-1 signaling inhibits apoptosis by activating beta-catenin/T cell factor-mediated transcription. J Cell Biol. 2001;152(1):87–96.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Li F, Chong ZZ, Maiese K. Winding through the WNT pathway during cellular development and demise. Histol Histopathol. 2006;21(1):103–24.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Sun M, Yamashita T, Shang J, Liu N, Deguchi K, Feng J, et al. Time-dependent profiles of microRNA expression induced by ischemic preconditioning in the gerbil hippocampus. Cell Transplant. 2015;24(3):367–76. doi:10.3727/096368915x686869.

    Article  PubMed  Google Scholar 

  55. Sun M, Yamashita T, Shang J, Liu N, Deguchi K, Liu W, et al. Acceleration of TDP43 and FUS/TLS protein expressions in the preconditioned hippocampus following repeated transient ischemia. J Neurosci Res. 2014;92(1):54–63. doi:10.1002/jnr.23301.

    Article  CAS  PubMed  Google Scholar 

  56. Liu C, Peng Z, Zhang N, Yu L, Han S, Li D, et al. Identification of differentially expressed microRNAs and their PKC-isoform specific gene network prediction during hypoxic pre-conditioning and focal cerebral ischemia of mice. J Neurochem. 2012;120(5):830–41. doi:10.1111/j.1471-4159.2011.07624.x.

    Article  CAS  PubMed  Google Scholar 

  57. Klein ME, Lioy DT, Ma L, Impey S, Mandel G, Goodman RH. Homeostatic regulation of MeCP2 expression by a CREB-induced microRNA. Nat Neurosci. 2007;10(12):1513–4. doi:10.1038/nn2010.

    Article  CAS  PubMed  Google Scholar 

  58. Hwang JY, Kaneko N, Noh KM, Pontarelli F, Zukin RS. The gene silencing transcription factor REST represses miR-132 expression in hippocampal neurons destined to die. J Mol Biol. 2014;426(20):3454–66. doi:10.1016/j.jmb.2014.07.032.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Lee YJ, Johnson KR, Hallenbeck JM. Global protein conjugation by ubiquitin-like-modifiers during ischemic stress is regulated by microRNAs and confers robust tolerance to ischemia. PLoS One. 2012;7(10):e47787. doi:10.1371/journal.pone.0047787.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Peng Z, Li J, Li Y, Yang X, Feng S, Han S, et al. Downregulation of miR-181b in mouse brain following ischemic stroke induces neuroprotection against ischemic injury through targeting heat shock protein A5 and ubiquitin carboxyl-terminal hydrolase isozyme L1. J Neurosci Res. 2013;91(10):1349–62. doi:10.1002/jnr.23255.

    Article  CAS  PubMed  Google Scholar 

  61. Choi AY, Choi JH, Yoon H, Hwang KY, Noh MH, Choe W, et al. Luteolin induces apoptosis through endoplasmic reticulum stress and mitochondrial dysfunction in neuro-2a mouse neuroblastoma cells. Eur J Pharmacol. 2011;668(1–2):115–26. doi:10.1016/j.ejphar.2011.06.047.

    Article  CAS  PubMed  Google Scholar 

  62. Yuan Y, Guo Q, Ye Z, Pingping X, Wang N, Song Z. Ischemic postconditioning protects brain from ischemia/reperfusion injury by attenuating endoplasmic reticulum stress-induced apoptosis through PI3K-Akt pathway. Brain Res. 2011;1367:85–93. doi:10.1016/j.brainres.2010.10.017.

    Article  CAS  PubMed  Google Scholar 

  63. Ciechanover A, Brundin P. The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron. 2003;40(2):427–46.

    Article  CAS  PubMed  Google Scholar 

  64. Dennissen FJ, Kholod N, van Leeuwen FW. The ubiquitin proteasome system in neurodegenerative diseases: culprit, accomplice or victim? Prog Neurobiol. 2012;96(2):190–207. doi:10.1016/j.pneurobio.2012.01.003.

    Article  CAS  PubMed  Google Scholar 

  65. Papa L, Akinyi L, Liu MC, Pineda JA, Tepas JJ 3rd, Oli MW, et al. Ubiquitin C-terminal hydrolase is a novel biomarker in humans for severe traumatic brain injury. Crit Care Med. 2010;38(1):138–44. doi:10.1097/CCM.0b013e3181b788ab.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Ni M, Zhang Y, Lee AS. Beyond the endoplasmic reticulum: atypical GRP78 in cell viability, signalling and therapeutic targeting. The Biochemical journal. 2011;434(2):181–8. doi:10.1042/bj20101569.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Xu LJ, Ouyang YB, Xiong X, Stary CM, Giffard RG. Post-stroke treatment with miR-181 antagomir reduces injury and improves long-term behavioral recovery in mice after focal cerebral ischemia. Exp Neurol. 2015;264:1–7. doi:10.1016/j.expneurol.2014.11.007.

    Article  CAS  PubMed  Google Scholar 

  68. Shin JH, Park YM, Kim DH, Moon GJ, Bang OY, Ohn T, et al. Ischemic brain extract increases SDF-1 expression in astrocytes through the CXCR2/miR-223/miR-27b pathway. Biochim Biophys Acta. 2014;1839(9):826–36. doi:10.1016/j.bbagrm.2014.06.019.

    Article  CAS  PubMed  Google Scholar 

  69. Ardelt AA, Bhattacharyya BJ, Belmadani A, Ren D, Miller RJ. Stromal derived growth factor-1 (CXCL12) modulates synaptic transmission to immature neurons during post-ischemic cerebral repair. Exp Neurol. 2013;248:246–53. doi:10.1016/j.expneurol.2013.06.017.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Miller JT, Bartley JH, Wimborne HJ, Walker AL, Hess DC, Hill WD, et al. The neuroblast and angioblast chemotaxic factor SDF-1 (CXCL12) expression is briefly up regulated by reactive astrocytes in brain following neonatal hypoxic-ischemic injury. BMC Neurosci. 2005;6:63. doi:10.1186/1471-2202-6-63.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Xu WH, Yao XY, Yu HJ, Huang JW, Cui LY. Downregulation of miR-199a may play a role in 3-nitropropionic acid induced ischemic tolerance in rat brain. Brain Res. 2012;1429:116–23. doi:10.1016/j.brainres.2011.10.007.

    Article  CAS  PubMed  Google Scholar 

  72. Feng Y, Li W, Wang JQ. MicroRNA-33A expression is reduced in cerebral cortex in a rat model of ischemic tolerance. Cellular and molecular biology (Noisy-le-Grand, France). 2015;61(3):24–9.

    CAS  Google Scholar 

  73. Payne RS, Akca O, Roewer N, Schurr A, Kehl F. Sevoflurane-induced preconditioning protects against cerebral ischemic neuronal damage in rats. Brain Res. 2005;1034(1–2):147–52. doi:10.1016/j.brainres.2004.12.006.

    Article  CAS  PubMed  Google Scholar 

  74. Wang H, Lu S, Yu Q, Liang W, Gao H, Li P, et al. Sevoflurane preconditioning confers neuroprotection via anti-inflammatory effects. Frontiers in bioscience (Elite edition). 2011;3:604–15.

    Google Scholar 

  75. Yang Q, Dong H, Deng J, Wang Q, Ye R, Li X, et al. Sevoflurane preconditioning induces neuroprotection through reactive oxygen species-mediated up-regulation of antioxidant enzymes in rats. Anesth Analg. 2011;112(4):931–7. doi:10.1213/ANE.0b013e31820bcfa4.

    Article  CAS  PubMed  Google Scholar 

  76. Yu Q, Chu M, Wang H, Lu S, Gao H, Li P, et al. Sevoflurane preconditioning protects blood-brain-barrier against brain ischemia. Frontiers in bioscience (Elite edition). 2011;3:978–88.

    Google Scholar 

  77. Cao L, Feng C, Li L, Zuo Z. Contribution of microRNA-203 to the isoflurane preconditioning-induced neuroprotection. Brain Res Bull. 2012;88(5):525–8. doi:10.1016/j.brainresbull.2012.05.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Shi H, Sun BL, Zhang J, Lu S, Zhang P, Wang H, et al. MiR-15b suppression of Bcl-2 contributes to cerebral ischemic injury and is reversed by sevoflurane preconditioning. CNS & neurological disorders drug targets. 2013;12(3):381–91.

    Article  CAS  Google Scholar 

  79. Li L, Zuo Z. Isoflurane postconditioning induces neuroprotection via Akt activation and attenuation of increased mitochondrial membrane permeability. Neuroscience. 2011;199:44–50. doi:10.1016/j.neuroscience.2011.10.022.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Sun Y, Li Y, Liu L, Wang Y, Xia Y, Zhang L, et al. Identification of miRNAs involved in the protective effect of sevoflurane preconditioning against hypoxic injury in PC12 cells. Cell Mol Neurobiol. 2015;35(8):1117–25. doi:10.1007/s10571-015-0205-7.

    Article  CAS  PubMed  Google Scholar 

  81. Das KP, Freudenrich TM, Mundy WR. Assessment of PC12 cell differentiation and neurite growth: a comparison of morphological and neurochemical measures. Neurotoxicol Teratol. 2004;26(3):397–406. doi:10.1016/j.ntt.2004.02.006.

    Article  CAS  PubMed  Google Scholar 

  82. Gozal E, Sachleben LR Jr, Rane MJ, Vega C, Gozal D. Mild sustained and intermittent hypoxia induce apoptosis in PC-12 cells via different mechanisms. Am J Physiol Cell Physiol. 2005;288(3):C535–42. doi:10.1152/ajpcell.00270.2004.

    Article  CAS  PubMed  Google Scholar 

  83. Jimenez-Mateos EM, Henshall DC. Seizure preconditioning and epileptic tolerance: models and mechanisms. Int J Physiol Pathophysiol pharmacol. 2009;1(2):180–91.

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Jimenez-Mateos EM, Bray I, Sanz-Rodriguez A, Engel T, McKiernan RC, Mouri G, et al. miRNA expression profile after status epilepticus and hippocampal neuroprotection by targeting miR-132. Am J Pathol. 2011;179(5):2519–32. doi:10.1016/j.ajpath.2011.07.036.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Edbauer D, Neilson JR, Foster KA, Wang CF, Seeburg DP, Batterton MN, et al. Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron. 2010;65(3):373–84. doi:10.1016/j.neuron.2010.01.005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Magill ST, Cambronne XA, Luikart BW, Lioy DT, Leighton BH, Westbrook GL, et al. MicroRNA-132 regulates dendritic growth and arborization of newborn neurons in the adult hippocampus. Proc Natl Acad Sci U S A. 2010;107(47):20382–7. doi:10.1073/pnas.1015691107.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. McKiernan RC, Jimenez-Mateos EM, Sano T, Bray I, Stallings RL, Simon RP, et al. Expression profiling the microRNA response to epileptic preconditioning identifies miR-184 as a modulator of seizure-induced neuronal death. Exp Neurol. 2012;237(2):346–54. doi:10.1016/j.expneurol.2012.06.029.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Frerichs KU, Hallenbeck JM. Hibernation in ground squirrels induces state and species-specific tolerance to hypoxia and aglycemia: an in vitro study in hippocampal slices. Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism. 1998;18(2):168–75. doi:10.1097/00004647-199802000-00007.

    Article  CAS  Google Scholar 

  89. Lee YJ, Miyake S, Wakita H, McMullen DC, Azuma Y, Auh S, et al. Protein SUMOylation is massively increased in hibernation torpor and is critical for the cytoprotection provided by ischemic preconditioning and hypothermia in SHSY5Y cells. Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism. 2007;27(5):950–62. doi:10.1038/sj.jcbfm.9600395.

    Article  CAS  Google Scholar 

  90. Lee YJ, Castri P, Bembry J, Maric D, Auh S, Hallenbeck JM. SUMOylation participates in induction of ischemic tolerance. J Neurochem. 2009;109(1):257–67. doi:10.1111/j.1471-4159.2009.05957.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Lee YJ, Mou Y, Maric D, Klimanis D, Auh S, Hallenbeck JM. Elevated global SUMOylation in Ubc9 transgenic mice protects their brains against focal cerebral ischemic damage. PLoS One. 2011;6(10):e25852. doi:10.1371/journal.pone.0025852.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Wu J, Bao J, Kim M, Yuan S, Tang C, Zheng H, et al. Two miRNA clusters, miR-34b/c and miR-449, are essential for normal brain development, motile ciliogenesis, and spermatogenesis. Proc Natl Acad Sci U S A. 2014;111(28):E2851–7. doi:10.1073/pnas.1407777111.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Mouradian MM. MicroRNAs in Parkinson's disease. Neurobiol Dis. 2012;46(2):279–84. doi:10.1016/j.nbd.2011.12.046.

    Article  CAS  PubMed  Google Scholar 

  94. Liu L, Liu L, Shi J, Tan M, Xiong J, Li X, et al. MicroRNA-34b mediates hippocampal astrocyte apoptosis in a rat model of recurrent seizures. BMC Neurosci. 2016;17(1):56. doi:10.1186/s12868-016-0291-6.

    Article  PubMed  PubMed Central  Google Scholar 

  95. Witwer KW, Halushka MK. Towards the promise of microRNAs - enhancing reproducibility and rigor in microRNA research. RNA Biol. 2016; doi:10.1080/15476286.2016.1236172.

  96. Mayya VK, Duchaine TF. On the availability of microRNA-induced silencing complexes, saturation of microRNA-binding sites and stoichiometry. Nucleic Acids Res. 2015;43(15):7556–65. doi:10.1093/nar/gkv720.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Aagaard L, Rossi JJ. RNAi therapeutics: principles, prospects and challenges. Adv Drug Deliv Rev. 2007;59(2–3):75–86. doi:10.1016/j.addr.2007.03.005.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Greenberg DS, Soreq H. MicroRNA therapeutics in neurological disease. Curr Pharm Des. 2014;20(38):6022–7.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was funded by R01 NS 084396, R01 NS 053898, and R01 NS 080177 to Dr. Rona G. Giffard Ph.D. M.D.

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Author notes

  1. Josh D. Bell and Jang-Eun Cho contributed equally to this work.

Authors and Affiliations

  1. Department of Anesthesiology, Perioperative and Pain Medicine, Stanford University School of Medicine, Stanford, CA, USA

    Josh D. Bell, Jang-Eun Cho & Rona G. Giffard

  2. Department of Anesthesia, University of Toronto, Toronto, Ontario, Canada

    Josh D. Bell

  3. Department of Anesthesiology and Pain Medicine, Anam Hospital, Korea University College of Medicine, Seoul, Republic of Korea

    Jang-Eun Cho

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  1. Josh D. Bell
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  2. Jang-Eun Cho
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  3. Rona G. Giffard
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Correspondence to Rona G. Giffard.

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Bell, J.D., Cho, JE. & Giffard, R.G. MicroRNA Changes in Preconditioning-Induced Neuroprotection. Transl. Stroke Res. 8, 585–596 (2017). https://doi.org/10.1007/s12975-017-0547-1

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  • DOI: https://doi.org/10.1007/s12975-017-0547-1

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