MicroRNAs and synaptic plasticity-a mutual relationship

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1652, 2014, Pages

  Aksoy Aksel, Ayla ^a   Zampa, Federico ^a   Schratt, Gerhard ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

Cognition; Learning and memory; microRNA; Neurological disease; Neuronal activity; Synaptic plasticity

Indexed keywords

BRAIN; COGNITION; GENE EXPRESSION; LEARNING; MATURATION; PLASTICITY; RNA; RODENT; TURNOVER;

MICRORNA;

ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; BRAIN; COGNITION; EPILEPSY; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; HUMAN; METABOLISM; MOUSE; NERVE CELL PLASTICITY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BRAIN; COGNITION; EPILEPSY; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HUMANS; MICE; MICRORNAS; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY;

EID: 84906086720     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2013.0515     Document Type: Review

References (86)

1. Bartel DP. 2004 MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297. (doi:10.1016/S0092-8674(04)00045-5)
2. Kim VN, Han J, Siomi MC. 2009 Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10, 126-139. (doi:10.1038/nrm2632)
3. Meister G. 2013 Argonaute proteins: functional insights and emerging roles. Nat. Rev. Genet. 14, 447-459. (doi:10.1038/nrg3462)
4. Bartel DP. 2009 MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233. (doi:10. 1016/j.cell.2009.01.002)
5. Fabian MR, Sonenberg N, Filipowicz W. 2010 Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem. 79, 351-379. (doi:10.1146/annurev-biochem-060308-103103)
6. Ameres SL, Zamore PD. 2013 Diversifying microRNA sequence and function. Nat. Rev. Mol. Cell Biol. 14, 475-488. (doi:10.1038/nrm3611)
7. Ruegger S, Grosshans H. 2012 MicroRNA turnover: when, how, and why. Trends Biochem. Sci. 37, 436-446. (doi:10.1016/j.tibs.2012.07.002)
8. Davis BN, Hata A. 2009 Regulation of microRNA biogenesis: a miRiad of mechanisms. Cell Commun. Signal. 7, 18. (doi:10.1186/1478-811X-7-18)
9. Remenyi J et al. 2010 Regulation of the miR-212/ 132 locus by MSK1 and CREB in response to neurotrophins. Biochem. J. 428, 281-291. (doi:10. 1042/BJ20100024)
10. Vo N, Klein ME, Varlamova O, Keller DM, Yamamoto T, Goodman RH, Impey S. 2005 A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc. Natl Acad. Sci. USA 102, 16 426-16 431. (doi:10.1073/pnas. 0508448102)
11. Klein ME, Lioy DT, Ma L, Impey S, Mandel G, Goodman RH. 2007 Homeostatic regulation of MeCP2 expression by a CREB-induced microRNA. Nat. Neurosci. 10, 1513-1514. (doi:10.1038/ nn2010)
12. Wayman GA et al. 2008 An activity-regulated microRNA controls dendritic plasticity by downregulating p250GAP. Proc. Natl Acad. Sci. USA 105, 9093-9098. (doi:10.1073/pnas.0803072105)
13. Fiore R, Khudayberdiev S, Christensen M, Siegel G, Flavell SW, Kim TK, Greenberg ME, Schratt G. 2009 Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels. EMBO J. 28, 697-710. (doi:10.1038/emboj.2009.10)
14. Gao J et al. 2010 A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 466, 1105-1109. (doi:10.1038/nature09271)
15. Liu CM, Wang RY, Jiao ZX, Zhang BY, Zhou FQ. 2013 MicroRNA-138 and SIRT1 form a mutual negative feedback loop to regulate mammalian axon regeneration. Genes Dev. 27, 1473-1483. (doi:10. 1101/gad.209619.112)
16. Zovoilis A et al. 2011 microRNA-34c is a novel target to treat dementias. EMBO J. 30, 4299-4308. (doi:10.1038/emboj.2011.327)
17. Li X, Jin P. 2010 Roles of small regulatory RNAs in determining neuronal identity. Nat. Rev. Neurosci. 11, 329-338. (doi:10.1038/nrn2739)
18. Krol J et al. 2010 Characterizing light-regulated retinal microRNAs reveals rapid turnover as a common property of neuronal microRNAs. Cell 141, 618-631. (doi:10.1016/j.cell.2010.03.039)
19. Mellios N et al. 2011 miR-132, an experiencedependent microRNA, is essential for visual cortex plasticity. Nat. Neurosci. 14, 1240-1242. (doi:10. 1038/nn.2909)
20. Tognini P, Putignano E, Coatti A, Pizzorusso T. 2011 Experience-dependent expression of miR-132 regulates ocular dominance plasticity. Nat. Neurosci. 14, 1237-1239. (doi:10.1038/nn.2920)
21. Cheng HY et al. 2007 microRNA modulation of circadian-clock period and entrainment. Neuron 54, 813-829. (doi:10.1016/j.neuron.2007.05.017)
22. Krol J, Loedige I, Filipowicz W. 2010 The widespread regulation of microRNA biogenesis, function and decay. Nat. Rev. Genet. 11, 597-610. (doi:10.1038/ nrg2843)
23. Siomi H, Siomi MC. 2010 Posttranscriptional regulation of microRNA biogenesis in animals. Mol. Cell 38, 323-332. (doi:10.1016/j.molcel.2010.03.013)
24. Herbert KM, Pimienta G, Degregorio SJ, Alexandrov A, Steitz JA. 2013 Phosphorylation of DGCR8 increases its intracellular stability and induces a progrowth miRNA profile. Cell Rep. 5, 1070-1081. (doi:10.1016/j.celrep.2013.10.017)
25. Han J et al. 2009 Posttranscriptional crossregulation between Drosha and DGCR8. Cell 136, 75-84. (doi:10.1016/j.cell.2008.10.053)
26. Triboulet R, Chang HM, Lapierre RJ, Gregory RI. 2009 Post-transcriptional control of DGCR8 expression by the microprocessor. RNA 15, 1005-1011. (doi:10.1261/rna.1591709)
27. Barad O, Mann M, Chapnik E, Shenoy A, Blelloch R, Barkai N, Hornstein E. 2012 Efficiency and specificity in microRNA biogenesis. Nat. Struct. Mol. Biol. 19, 650-652. (doi:10.1038/nsmb.2293)
28. Kye MJ, Neveu P, Lee YS, Zhou M, Steen JA, Sahin M, Kosik KS, Silva AJ. 2011 NMDA mediated contextual conditioning changes miRNA expression. PLoS ONE 6, e24682. (doi:10.1371/journal.pone. 0024682)
29. Lugli G, Larson J, Martone ME, Jones Y, Smalheiser NR. 2005 Dicer and eIF2c are enriched at postsynaptic densities in adult mouse brain and are modified by neuronal activity in a calpaindependent manner. J. Neurochem. 94, 896-905. (doi:10.1111/j.1471-4159.2005.03224.x)
30. Huang YW, Ruiz CR, Eyler EC, Lin K, Meffert MK. 2012 Dual regulation of miRNA biogenesis generates target specificity in neurotrophin-induced protein synthesis. Cell 148, 933-946. (doi:10.1016/ j.cell.2012.01.036)
31. Obernosterer G, Leuschner PJ, Alenius M, Martinez J. 2006 Post-transcriptional regulation of microRNA expression. RNA 12, 1161-1167. (doi:10.1261/rna. 2322506)
32. Bicker S, Khudayberdiev S, Weiss K, Zocher K, Baumeister S, Schratt G. 2013 The DEAH-box helicase DHX36 mediates dendritic localization of the neuronal precursor-microRNA-134. Genes Dev. 27, 991-996.
33. Park CS, Tang SJ. 2009 Regulation of microRNA expression by induction of bidirectional synaptic plasticity. J. Mol. Neurosci. 38, 50-56. (doi:10. 1007/s12031-008-9158-3)
34. van Spronsen M et al. 2013 Developmental and activity-dependent miRNA expression profiling in primary hippocampal neuron cultures. PLoS ONE 8, e74907. (doi:10.1371/journal.pone.0074907)
35. Wibrand K, Panja D, Tiron A, Ofte ML, Skaftnesmo KO, Lee CS, Pena JT, Tuschl T, Bramham CR. 2010 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, 636-645. (doi:10.1111/j.1460-9568.2010.07112.x)
36. Schratt GM, Tuebing F, Nigh EA, Kane CG, Sabatini ME, Kiebler M, Greenberg ME. 2006 A brain-specific microRNA regulates dendritic spine development. Nature 439, 283-289. (doi:10.1038/nature04367)
37. Sosanya NM, Huang PP, Cacheaux LP, Chen CJ, Nguyen K, Perrone-Bizzozero NI, Raab-Graham KF. 2013 Degradation of high affinity HuD targets releases Kv1.1 mRNA from miR-129 repression by mTORC1. J. Cell Biol. 202, 53-69. (doi:10.1083/jcb. 201212089)
38. Banerjee S, Neveu P, Kosik KS. 2009 A coordinated local translational control point at the synapse involving relief from silencing and MOV10 degradation. Neuron 64, 871-884. (doi:10.1016/j. neuron.2009.11.023)
39. Siegel G et al. 2009 A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nat. Cell Biol. 11, 705-716. (doi:10.1038/ncb1876)
40. Muddashetty RS, Nalavadi VC, Gross C, Yao X, Xing L, Laur O, Warren ST, Bassell GJ. 2011 Reversible inhibition of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling. Mol. Cell 42, 673-688. (doi:10.1016/j.molcel.2011. 05.006)
41. Edbauer D et al. 2010 Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron 65, 373-384. (doi:10.1016/j.neuron.2010.01.005)
42. Chen YL, Shen CK. 2013 Modulation of mGluRdependent MAP1B translation and AMPA receptor endocytosis by microRNA miR-146a-5p. J. Neurosci. 33, 9013-9020. (doi:10.1523/JNEUROSCI.5210-12. 2013)
43. Impey S et al. 2010 An activity-induced microRNA controls dendritic spine formation by regulating Rac1-PAK signaling. Mol. Cell Neurosci. 43, 146-156. (doi:10.1016/j.mcn.2009.10.005)
44. Garcia-Perez D, Saez-Belmonte F, Laorden ML, Nunez C, Milanes MV. 2013 Morphine administration modulates expression of Argonaute 2 and dopamine-related transcription factors involved in midbrain dopaminergic neurons function. Br. J. Pharmacol. 168, 1889-1901. (doi:10.1111/ bph.12083)
45. Smibert P, Yang JS, Azzam G, Liu JL, Lai EC. 2013 Homeostatic control of argonaute stability by microRNA availability. Nat. Struct. Mol. Biol. 20, 789-795. (doi:10.1038/nsmb.2606)
46. Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J. 2013 Natural RNA circles function as efficient microRNA sponges. Nature 495, 384-388. (doi:10.1038/nature11993)
47. Memczak S et al. 2013 Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495, 333-338. (doi:10.1038/nature11928)
48. Sekido R, Lovell-Badge R. 2008 Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453, 930-934. (doi:10.1038/nature06944)
49. Bak M, Silahtaroglu A, Moller M, Christensen M, Rath MF, Skryabin B, Tommerup N, Kauppinen S. 2008 MicroRNA expression in the adult mouse central nervous system. RNA 14, 432-444. (doi:10. 1261/rna.783108)
50. Olsen L, Klausen M, Helboe L, Nielsen FC, Werge T. 2009 MicroRNAs show mutually exclusive expression patterns in the brain of adult male rats. PLoS ONE 4, e7225. (doi:10.1371/journal.pone.0007225)
51. Juhila J, Sipila T, Icay K, Nicorici D, Ellonen P, Kallio A, Korpelainen E, Greco D, Hovatta I. 2011 MicroRNA expression profiling reveals miRNA families regulating specific biological pathways in mouse frontal cortex and hippocampus. PLoS ONE 6, e21495. (doi:10.1371/journal.pone.0021495)
52. Shinohara Y, Yahagi K, Kawano M, Nishiyori H, Kawazu C, Suzuki N, Manabe R, Hirase H. 2011 miRNA profiling of bilateral rat hippocampal CA3 by deep sequencing. Biochem. Biophys. Res. Commun. 409, 293-298. (doi:10.1016/j.bbrc.2011.05.004)
53. Lee K, Kim JH, Kwon OB, An K, Ryu J, Cho K, Suh YH, Kim HS. 2012 An activity-regulated microRNA, miR-188, controls dendritic plasticity and synaptic transmission by downregulating neuropilin-2. J. Neurosci. 32, 5678-5687. (doi:10.1523/ JNEUROSCI.6471-11.2012)
54. Hansen KF, Sakamoto K, Wayman GA, Impey S, Obrietan K. 2010 Transgenic miR132 alters neuronal spine density and impairs novel object recognition memory. PLoS ONE 5, e15497. (doi:10.1371/journal. pone.0015497)
55. Babiarz JE, Hsu R, Melton C, Thomas M, Ullian EM, Blelloch R. 2011 A role for noncanonical microRNAs in the mammalian brain revealed by phenotypic differences in Dgcr8 versus Dicer1 knockouts and small RNA sequencing. RNA 17, 1489-1501. (doi:10.1261/rna.2442211)
56. Konopka Wet al. 2010 MicroRNA loss enhances learning and memory in mice. J. Neurosci. 30, 14 835-14 842. (doi:10.1523/JNEUROSCI.3030-10.2010)
57. Christensen M, Larsen LA, Kauppinen S, Schratt G. 2010 Recombinant adeno-associated virus-mediated microRNA delivery into the postnatal mouse brain reveals a role for miR-134 in dendritogenesis in vivo. Front. Neural Circuits 3, 16. (doi:10.3389/ neuro.04.016.2009)
58. Jimenez-Mateos EM et al. 2012 Silencing microRNA-134 produces neuroprotective and prolonged seizure-suppressive effects. Nat. Med. 18, 1087-1094. (doi:10.1038/nm.2834)
59. Tognini P, Pizzorusso T. 2012 MicroRNA212/132 family: molecular transducer of neuronal function and plasticity. Int. J. Biochem. Cell Biol. 44, 6-10. (doi:10.1016/j.biocel.2011.10.015)
60. Nudelman AS, DiRocco DP, Lambert TJ, Garelick MG, Le J, Nathanson NM, Storm DR. 2010 Neuronal activity rapidly induces transcription of the CREBregulated microRNA-132, in vivo. Hippocampus 20, 492-498. (doi:10.1002/hipo.20646)
61. Wang RY, Phang RZ, Hsu PH, Wang WH, Huang HT, Liu IY. 2013 In vivo knockdown of hippocampal miR-132 expression impairs memory acquisition of trace fear conditioning. Hippocampus 23, 625-633. (doi:10.1002/hipo.22123)
62. Hansen KF, Karelina K, Sakamoto K, Wayman GA, Impey S, Obrietan K. 2013 miRNA-132: a dynamic regulator of cognitive capacity. Brain Struct. Funct. 218, 817-831. (doi:10.1007/s00429-012-0431-4)
63. Scott HL et al. 2012 MicroRNA-132 regulates recognition memory and synaptic plasticity in the perirhinal cortex. Eur. J. Neurosci. 36, 2941-2948. (doi:10.1111/j.1460-9568.2012.08220.x)
64. Remenyi J et al. 2013 miR-132/212 knockout mice reveal roles for these miRNAs in regulating cortical synaptic transmission and plasticity. PLoS ONE 8, e62509. (doi:10.1371/journal.pone.0062509)
65. Zhao YN, Li WF, Li F, Zhang Z, Dai YD, Xu AL, Qi C, Gao JM, Gao J. 2013 Resveratrol improves learning and memory in normally aged mice through microRNA-CREB pathway. Biochem. Biophys. Res. Commun. 435, 597-602. (doi:10.1016/j.bbrc.2013. 05.025)
66. Yang Y et al. 2012 EPAC null mutation impairs learning and social interactions via aberrant regulation of miR-124 and Zif268 translation. Neuron 73, 774-788. (doi:10.1016/j.neuron.2012. 02.003)
67. Rajasethupathy P, Fiumara F, Sheridan R, Betel D, Puthanveettil SV, Russo JJ, Sander C, Tuschl T, Kandel E. 2009 Characterization of small RNAs in aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. Neuron 63, 803-817. (doi:10.1016/j.neuron.2009.05.029)
68. Ai J et al. 2013 MicroRNA-195 protects against dementia induced by chronic brain hypoperfusion via its anti-amyloidogenic effect in rats. J. Neurosci. 33, 3989-4001. (doi:10.1523/JNEUROSCI.1997-12.2013)
69. Lee ST et al. 2012 miR-206 regulates brain-derived neurotrophic factor in Alzheimer disease model. Ann. Neurol. 72, 269-277. (doi:10.1002/ana.23588)
70. Griggs EM, Young EJ, Rumbaugh G, Miller CA. 2013 MicroRNA-182 regulates amygdala-dependent memory formation. J. Neurosci. 33, 1734-1740. (doi:10.1523/JNEUROSCI.2873-12.2013)
71. Lin Q et al. 2011 The brain-specific microRNA miR-128b regulates the formation of fear-extinction memory. Nat. Neurosci. 14, 1115-1117. (doi:10. 1038/nn.2891)
72. Stark KL et al. 2008 Altered brain microRNA biogenesis contributes to phenotypic deficits in a 22q11-deletion mouse model. Nat. Genet. 40, 751-760. (doi:10.1038/ng.138)
73. Hsu R, Schofield CM, Dela Cruz CG, Jones-Davis DM, Blelloch R, Ullian EM. 2012 Loss of microRNAs in pyramidal neurons leads to specific changes in inhibitory synaptic transmission in the prefrontal cortex. Mol. Cell Neurosci. 50, 283-292. (doi:10. 1016/j.mcn.2012.06.002)
74. Ouchi Y, Banno Y, Shimizu Y, Ando S, Hasegawa H, Adachi K, Iwamoto T. 2013 Reduced adult hippocampal neurogenesis and working memory deficits in the Dgcr8-deficient mouse model of 22q11.2 deletion-associated schizophrenia can be rescued by IGF2. J. Neurosci. 33, 9408-9419. (doi:10.1523/JNEUROSCI.2700-12.2013)
75. Fenelon K, Mukai J, Xu B, Hsu PK, Drew LJ, Karayiorgou M, Fischbach GD, Macdermott AB, Gogos JA. 2011 Deficiency of Dgcr8, a gene disrupted by the 22q11.2 microdeletion, results in altered short-term plasticity in the prefrontal cortex. Proc. Natl Acad. Sci. USA 108, 4447-4452. (doi:10. 1073/pnas.1101219108)
76. Xu B, Hsu PK, Stark KL, Karayiorgou M, Gogos JA. 2013 Derepression of a neuronal inhibitor due to miRNA dysregulation in a schizophrenia-related microdeletion. Cell 152, 262-275. (doi:10.1016/j. cell.2012.11.052)
77. Davis TH, Cuellar TL, Koch SM, Barker AJ, Harfe BD, McManus MT, Ullian EM. 2008 Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J. Neurosci. 28, 4322-4330. (doi:10.1523/JNEUROSCI.4815-07.2008)
78. Pichardo-Casas I et al. 2012 Expression profiling of synaptic microRNAs from the adult rat brain identifies regional differences and seizure-induced dynamic modulation. Brain Res. 1436, 20-33. (doi:10.1016/j.brainres.2011.12.001)
79. Liu DZ, Tian Y, Ander BP, Xu H, Stamova BS, Zhan X, Turner RJ, Jickling G, Sharp FR. 2010 Brain and blood microRNA expression profiling of ischemic stroke, intracerebral hemorrhage, and kainate seizures. J. Cereb. Blood Flow Metab. 30, 92-101. (doi:10.1038/jcbfm.2009.186)
80. Jimenez-Mateos EM, Henshall DC. 2013 Epilepsy and microRNA. Neuroscience 238, 218-229. (doi:10.1016/j.neuroscience.2013.02.027)
81. Jimenez-Mateos EM et al. 2011 miRNA expression profile after status epilepticus and hippocampal neuroprotection by targeting miR-132. Am. J. Pathol. 179, 2519-2532. (doi:10.1016/j. ajpath.2011.07.036)
82. Sano T, Reynolds JP, Jimenez-Mateos EM, Matsushima S, Taki W, Henshall DC. 2012 MicroRNA-34a upregulation during seizure-induced neuronal death. Cell Death Dis. 3, e287. (doi:10. 1038/cddis.2012.23)
83. Peng J, Omran A, Ashhab MU, Kong H, Gan N, He F, Yin F. 2013 Expression patterns of miR-124, miR-134, miR-132, and miR-21 in an immature rat model and children with mesial temporal lobe epilepsy. J. Mol. Neurosci. 50, 291-297. (doi:10. 1007/s12031-013-9953-3)
84. Hu K et al. 2012 MicroRNA expression profile of the hippocampus in a rat model of temporal lobe epilepsy and miR-34a-targeted neuroprotection against hippocampal neurone cell apoptosis poststatus epilepticus. BMC Neurosci. 13, 115. (doi:10. 1186/1471-2202-13-115)
85. Hu K, Zhang C, Long L, Long X, Feng L, Li Y, Xiao B. 2011 Expression profile of microRNAs in rat hippocampus following lithium-pilocarpine-induced status epilepticus. Neurosci. Lett. 488, 252-257. (doi:10.1016/j.neulet.2010.11.040)
86. Tan CL et al. 2013 MicroRNA-128 governs neuronal excitability and motor behavior in mice. Science 342, 1254-1258. (doi:10.1126/science. 1244193)