Antagomirs targeting microRNA-134 increase hippocampal pyramidal neuron spine volume in vivo and protect against pilocarpine-induced status epilepticus

Brain Structure and Function

Volumn 220, Issue 4, 2015, Pages 2387-2399

  Jimenez Mateos, Eva M ^a   Engel, Tobias ^a   Merino Serrais, Paula ^b   Fernaud Espinosa, Isabel ^b   Rodriguez Alvarez, Natalia ^a   Reynolds, James ^a   Reschke, Cristina R ^a   Conroy, Ronan M ^a   McKiernan, Ross C ^a   deFelipe, Javier ^b   Henshall, David C ^a  

^a ROYAL COLLEGE OF SURGEONS IN IRELAND   (Ireland)

^b INSTITUTO CAJAL   (Spain)

Author keywords

Anticonvulsant; Hippocampal sclerosis; Non coding RNA; RNA induced silencing complex; Status epilepticus; Temporal lobe epilepsy

Indexed keywords

ANTAGOMIR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; LIM KINASE 1; MICRORNA; MICRORNA 134; PILOCARPINE; UNCLASSIFIED DRUG; MIRN134 MICRORNA, MOUSE; OLIGONUCLEOTIDE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DENDRITIC SPINE; DRUG TARGETING; ELECTROCORTICOGRAPHY; EPILEPTIC STATE; GENE EXPRESSION; HIPPOCAMPUS; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SPINE; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; ELECTROENCEPHALOGRAPHY; GENE EXPRESSION REGULATION; GENETICS; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; NERVE CELL; NONPARAMETRIC TEST; PATHOLOGY; PHYSIOLOGY; SPATIAL MEMORY; STATUS EPILEPTICUS; TIME;

ANIMALIA; MUS;

ANIMALS; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; ELECTROENCEPHALOGRAPHY; GENE EXPRESSION REGULATION; HIPPOCAMPUS; INJECTIONS, INTRAVENTRICULAR; MALE; MICE; MICRORNAS; NEURONS; OLIGONUCLEOTIDES; PILOCARPINE; SPATIAL MEMORY; STATISTICS, NONPARAMETRIC; STATUS EPILEPTICUS; TIME FACTORS;

EID: 84933178818     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0798-5     Document Type: Article

References (61)

1. Ambros V (2004) The functions of animal microRNAs. Nature 431:350–355
2. Arellano JI, Benavides-Piccione R, Defelipe J, Yuste R (2007a) Ultrastructure of dendritic spines: correlation between synaptic and spine morphologies. Front Neurosci 1:131–143
3. Arellano JI, Espinosa A, Fairen A, Yuste R, DeFelipe J (2007b) Non-synaptic dendritic spines in neocortex. Neuroscience 145:464–469
4. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297
5. Ben-Ari Y (1985) Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 14:375–403
6. Blumcke I, Zuschratter W, Schewe JC, Suter B, Lie AA, Riederer BM, Meyer B, Schramm J, Elger CE, Wiestler OD (1999) Cellular pathology of hilar neurons in Ammon’s horn sclerosis. J Comp Neurol 414:437–453
7. Borges K, Gearing M, McDermott DL, Smith AB, Almonte AG, Wainer BH, Dingledine R (2003) Neuronal and glial pathological changes during epileptogenesis in the mouse pilocarpine model. Exp Neurol 182:21–34
8. Bramham CR (2008) Local protein synthesis, actin dynamics, and LTP consolidation. Curr Opin Neurobiol 18:524–531
9. Curia G, Longo D, Biagini G, Jones RS, Avoli M (2008) The pilocarpine model of temporal lobe epilepsy. J Neurosci Methods 172:143–157
10. Dogini DB, Avansini SH, Vieira AS, Lopes-Cendes I (2013) MicroRNA regulation and dysregulation in epilepsy. Front Cell Neurosci 7:172
11. Engel T, Sanz-Rodgriguez A, Jimenez-Mateos EM, Concannon CG, Jimenez-Pacheco A, Moran C, Mesuret G, Petit E, Delanty N, Farrell MA, O’Brien DF, Prehn JH, Lucas JJ, Henshall DC (2013) CHOP regulates the p53-MDM2 axis and is required for neuronal survival after seizures. Brain 136:577–592
12. Fabian MR, Sonenberg N, Filipowicz W (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79:351–379
13. Gao J, Wang WY, Mao YW, Graff J, Guan JS, Pan L, Mak G, Kim D, Su SC, Tsai LH (2010) A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 466:1105–1109
14. Gaughwin P, Ciesla M, Yang H, Lim B, Brundin P (2011) Stage-specific modulation of cortical neuronal development by Mmu-miR-134. Cereb Cortex 21:1857–1869
15. Guo D, Arnspiger S, Rensing NR, Wong M (2012) Brief seizures cause dendritic injury. Neurobiol Dis 45:348–355
16. Hering H, Sheng M (2001) Dendritic spines: structure, dynamics and regulation. Nat Rev Neurosci 2:880–888
17. 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
18. Im HI, Kenny PJ (2012) MicroRNAs in neuronal function and dysfunction. Trends Neurosci 35:325–334
19. Isokawa M, Levesque MF (1991) Increased NMDA responses and dendritic degeneration in human epileptic hippocampal neurons in slices. Neurosci Lett 132:212–216
20. Jimenez-Mateos EM, Henshall DC (2013) Epilepsy and microRNA. Neuroscience 238:218–229
21. Jimenez-Mateos EM, Bray I, Sanz-Rodriguez A, Engel T, McKiernan RC, Mouri G, Tanaka K, Sano T, Saugstad JA, Simon RP, Stallings RL, Henshall DC (2011) miRNA expression profile after status epilepticus and hippocampal neuroprotection by targeting miR-132. Am J Pathol 179:2519–2532
22. Jimenez-Mateos EM, Engel T, Merino-Serrais P, McKiernan RC, Tanaka K, Mouri G, Sano T, O’Tuathaigh C, Waddington JL, Prenter S, Delanty N, Farrell MA, O’Brien DF, Conroy RM, Stallings RL, Defelipe J, Henshall DC (2012) Silencing microRNA-134 produces neuroprotective and prolonged seizure-suppressive effects. Nat Med 18:1087–1094
23. Jimenez-Pacheco A, Mesuret G, Sanz-Rodriguez A, Tanaka K, Mooney C, Conroy R, Miras-Portugal MT, Diaz-Hernandez M, Henshall DC, Engel T (2013) Increased neocortical expression of the P2X7 receptor after status epilepticus and anticonvulsant effect of P2X7 receptor antagonist A-438079. Epilepsia 54:1551–1561
24. Kasai H, Fukuda M, Watanabe S, Hayashi-Takagi A, Noguchi J (2010) Structural dynamics of dendritic spines in memory and cognition. Trends Neurosci 33:121–129
25. Kosik KS (2006) The neuronal microRNA system. Nat Rev Neurosci 7:911–920
26. Koval ED, Shaner C, Zhang P, du Maine X, Fischer K, Tay J, Chau BN, Wu GF, Miller TM (2013) Method for widespread microRNA-155 inhibition prolongs survival in ALS-model mice. Hum Mol Genet 22:4127–4135
27. 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
28. Liu G, Gu B, He XP, Joshi RB, Wackerle HD, Rodriguiz RM, Wetsel WC, McNamara JO (2013) Transient inhibition of TrkB kinase after status epilepticus prevents development of temporal lobe epilepsy. Neuron 79:31–38
29. Loscher W, Brandt C (2010) Prevention or modification of epileptogenesis after brain insults: experimental approaches and translational research. Pharmacol Rev 62:668–700
30. Marchi N, Oby E, Batra A, Uva L, De Curtis M, Hernandez N, Van Boxel-Dezaire A, Najm I, Janigro D (2007) In vivo and in vitro effects of pilocarpine: relevance to ictogenesis. Epilepsia 48:1934–1946
31. Marchi N, Johnson AJ, Puvenna V, Johnson HL, Tierney W, Ghosh C, Cucullo L, Fabene PF, Janigro D (2011) Modulation of peripheral cytotoxic cells and ictogenesis in a model of seizures. Epilepsia 52:1627–1634
32. McNeill E, Van Vactor D (2012) MicroRNAs shape the neuronal landscape. Neuron 75:363–379
33. Meller R, Thompson SJ, Lusardi TA, Ordonez AN, Ashley MD, Jessick V, Wang W, Torrey DJ, Henshall DC, Gafken PR, Saugstad JA, Xiong ZG, Simon RP (2008) Ubiquitin proteasome-mediated synaptic reorganization: a novel mechanism underlying rapid ischemic tolerance. J Neurosci 28:50–59
34. Meng Y, Zhang Y, Tregoubov V, Falls DL, Jia Z (2003) Regulation of spine morphology and synaptic function by LIMK and the actin cytoskeleton. Rev Neurosci 14:233–240
35. Merino-Serrais P, Knafo S, Alonso-Nanclares L, Fernaud-Espinosa I, Defelipe J (2011) Layer-specific alterations to CA1 dendritic spines in a mouse model of Alzheimer’s disease. Hippocampus 21:1037–1044
36. Mizrahi A, Crowley JC, Shtoyerman E, Katz LC (2004) High-resolution in vivo imaging of hippocampal dendrites and spines. J Neurosci 24:3147–3151
37. Morimoto K, Fahnestock M, Racine RJ (2004) Kindling and status epilepticus models of epilepsy: rewiring the brain. Prog Neurobiol 73:1–60
38. Mouri G, Jimenez-Mateos E, Engel T, Dunleavy M, Hatazaki S, Paucard A, Matsushima S, Taki W, Henshall DC (2008) Unilateral hippocampal CA3-predominant damage and short latency epileptogenesis after intra-amygdala microinjection of kainic acid in mice. Brain Res 1213:140–151
39. Muller M, Gahwiler BH, Rietschin L, Thompson SM (1993) Reversible loss of dendritic spines and altered excitability after chronic epilepsy in hippocampal slice cultures. Proc Natl Acad Sci USA 90:257–261
40. Olney JW, Fuller T, de Gubareff T (1979) Acute dendrotoxic changes in the hippocampus of kainate treated rats. Brain Res 176:91–100
41. Paul LA, Fried I, Watanabe K, Forsythe AB, Scheibel AB (1981) Structural correlates of seizure behavior in the mongolian gerbil. Science 213:924–926
42. 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
43. Peters A, Kaiserman-Abramof IR (1970) The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines. Am J Anat 127:321–355
44. Rensing N, Ouyang Y, Yang XF, Yamada KA, Rothman SM, Wong M (2005) In vivo imaging of dendritic spines during electrographic seizures. Ann Neurol 58:888–898
45. Risbud RM, Porter BE (2013) Changes in microRNA expression in the whole hippocampus and hippocampal synaptoneurosome fraction following pilocarpine induced status epilepticus. PLoS ONE 8:e53464
46. Rochefort NL, Konnerth A (2012) Dendritic spines: from structure to in vivo function. EMBO Rep 13:699–708
47. Saneyoshi T, Fortin DA, Soderling TR (2010) Regulation of spine and synapse formation by activity-dependent intracellular signaling pathways. Curr Opin Neurobiol 20:108–115
48. 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
49. Schikorski T, Stevens CF (2001) Morphological correlates of functionally defined synaptic vesicle populations. Nat Neurosci 4:391–395
50. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Prot 3:1101–1108
51. Schratt G (2009) microRNAs at the synapse. Nat Rev Neurosci 10:842–849
52. 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
53. Segal M (2010) Dendritic spines, synaptic plasticity and neuronal survival: activity shapes dendritic spines to enhance neuronal viability. Eur J Neurosci 31:2178–2184
54. Shorvon S, Ferlisi M (2011) The treatment of super-refractory status epilepticus: a critical review of available therapies and a clinical treatment protocol. Brain 134:2802–2818
55. Sierra-Paredes G, Oreiro-Garcia T, Nunez-Rodriguez A, Vazquez-Lopez A, Sierra-Marcuno G (2006) Seizures induced by in vivo latrunculin a and jasplakinolide microperfusion in the rat hippocampus. J Mol Neurosci 28:151–160
56. Wilcox KS, Dixon-Salazar T, Sills GJ, Ben-Menachem E, White HS, Porter RJ, Dichter MA, Moshe SL, Noebels JL, Privitera MD, Rogawski MA (2013) Issues related to development of new antiseizure treatments. Epilepsia 54(Suppl 4):24–34
57. Willmore LJ, Ballinger WE Jr, Boggs W, Sypert GW, Rubin JJ (1980) Dendritic alterations in rat isocortex within an iron-induced chronic epileptic focus. Neurosurgery 7:142–146
58. Wimmer ME, Hernandez PJ, Blackwell J, Abel T (2012) Aging impairs hippocampus-dependent long-term memory for object location in mice. Neurobiol Aging 33:2220–2224
59. Wong M, Guo D (2012) Dendritic spine pathology in epilepsy: cause or consequence? Neuroscience 251:141–150
60. Zeng LH, Xu L, Rensing NR, Sinatra PM, Rothman SM, Wong M (2007) Kainate seizures cause acute dendritic injury and actin depolymerization in vivo. J Neurosci 27:11604–11613
61. Zhou Q, Homma KJ, Poo MM (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44:749–757