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01-12-2017 | Review

MicroRNA Changes in Preconditioning-Induced Neuroprotection

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

Published in: Translational Stroke Research | Issue 6/2017

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.

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMed

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.CrossRef

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.CrossRefPubMedPubMedCentral

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.CrossRef

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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 50-1CrossRefPubMed

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.CrossRefPubMed

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.CrossRef

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.CrossRefPubMed

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.CrossRefPubMedPubMedCentral

15.

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

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMed

18.

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

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.CrossRefPubMedPubMedCentral

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.CrossRef

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.CrossRefPubMed

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRef

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMedPubMedCentral

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.

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.CrossRefPubMedPubMedCentral

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.CrossRef

32.

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

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.CrossRefPubMedPubMedCentral

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.CrossRef

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.CrossRef

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.PubMedPubMedCentral

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMedPubMedCentral

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.CrossRef

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRef

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.CrossRefPubMed

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.CrossRef

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.CrossRefPubMedPubMedCentral

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.CrossRef

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.CrossRefPubMed

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.CrossRefPubMedPubMedCentral

53.

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

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

63.

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

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.CrossRefPubMed

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMed

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.

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.CrossRefPubMed

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.

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.CrossRefPubMed

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.

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.CrossRefPubMedPubMedCentral

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.CrossRef

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMed

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.CrossRefPubMed

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.CrossRefPubMed

83.

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

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMedPubMedCentral

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.CrossRef

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.CrossRef

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMedPubMedCentral

93.

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

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMedPubMedCentral

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.CrossRefPubMedPubMedCentral

98.

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

Title: MicroRNA Changes in Preconditioning-Induced Neuroprotection
Authors: Josh D. Bell
Jang-Eun Cho
Rona G. Giffard
Publication date: 01-12-2017
Publisher: Springer US
Published in: Translational Stroke Research / Issue 6/2017
Print ISSN: 1868-4483
Electronic ISSN: 1868-601X
DOI: https://doi.org/10.1007/s12975-017-0547-1

At a glance: The STEP trials

Springer Medicine

MicroRNA Changes in Preconditioning-Induced Neuroprotection

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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CCL11 (Eotaxin-1) Levels Predict Long-Term Functional Outcomes in Patients Following Ischemic Stroke

Annexin A2 Plus Low-Dose Tissue Plasminogen Activator Combination Attenuates Cerebrovascular Dysfunction After Focal Embolic Stroke of Rats

A Combination of Three Repurposed Drugs Administered at Reperfusion as a Promising Therapy for Postischemic Brain Injury

Novel Regenerative Therapies Based on Regionally Induced Multipotent Stem Cells in Post-Stroke Brains: Their Origin, Characterization, and Perspective

Infections Up to 76 Days After Stroke Increase Disability and Death

Preclinical and Clinical Evidence on Ipsilateral Corticospinal Projections: Implication for Motor Recovery