Selective inhibition of miR-92 in hippocampal neurons alters contextual fear memory

Hippocampus

Volumn 24, Issue 12, 2014, Pages 1458-1465

  Vetere, Gisella ^a,b   Barbato, Christian ^a   Pezzola, Silvia ^a   Frisone, Paola ^a   Aceti, Massimiliano ^b   Ciotti, Mariateresa ^a   Cogoni, Carlo ^c   Ammassari Teule, Martine ^a,b   Ruberti, Francesca ^a  

^a CNR   (Italy)

^b Fondazione Santa Lucia Via del Fosso di Fiorano   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Contextual fear conditioning; Dendritic spines; Hippocampus; MicroRNA; MiR 92

Indexed keywords

COTRANSPORTER; CPEB3 PROTEIN, MOUSE; CPEB3 PROTEIN, RAT; MEF2D PROTEIN, MOUSE; MEF2D PROTEIN, RAT; MICRORNA; MIRN92 MICRORNA, MOUSE; MIRN92 MICRORNA, RAT; MYOCYTE ENHANCER FACTOR 2; POTASSIUM-CHLORIDE SYMPORTERS; RNA BINDING PROTEIN;

ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; CONDITIONED REFLEX; DENDRITIC SPINE; FEAR; HIPPOCAMPUS; MEMORY; METABOLISM; NERVE CELL; PHYSIOLOGY; WISTAR RAT;

ANIMALS; CELLS, CULTURED; CONDITIONING, CLASSICAL; DENDRITIC SPINES; FEAR; HIPPOCAMPUS; MEF2 TRANSCRIPTION FACTORS; MEMORY; MICE, INBRED C57BL; MICRORNAS; NEURONS; RATS, WISTAR; RNA-BINDING PROTEINS; SYMPORTERS;

EID: 84910153513     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22326     Document Type: Article

References (27)

1. Barbato C, Ruberti F, Pieri M, Vilardo E, Costanzo M, Ciotti MT, Zona C, Cogoni C. 2010. MicroRNA-92 modulates K(+) Cl(-) co-transporter KCC2 expression in cerebellar granule neurons. J Neurochem 113:591-600.
2. Bartel DP. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136:215-233.
3. Bian S, Hong J, Li Q, Schebelle L, Pollock A, Knauss JL, Garg V, Sun T. 2013. MicroRNA cluster miR-17-92 regulates neural stem cell expansion and transition to intermediate progenitors in the developing mouse neocortex. Cell Rep 3:1398-1406.
4. Chao HW, Tsai LY, Lu YL, Lin PY, Huang WH, Chou HJ, Lu WH, Lin HC, Lee PT, Huang YS. 2013. Deletion of CPEB3 enhances hippocampus-dependent memory via increasing expressions of PSD95 and NMDA receptors. J Neurosci 33:17008-17022.
5. Chen Z, Liang S, Zhao Y, Han Z. 2012. miR-92b regulates Mef2 levels through a negative-feedback circuit during Drosophila muscle development. Development 139:3543-3552.
6. Cole CJ, Mercaldo V, Restivo L, Yiu AP, Sekeres MJ, Han JH, Vetere G, Pekar T, Ross PJ, Neve RL, Frankland PW, Josselyn SA. 2012. MEF2 negatively regulates learning-induced structural plasticity and memory formation. Nat Neurosci 15:1255-1264.
7. Concepcion CP, Bonetti C, Ventura A. 2012. The microRNA-17-92 family of microRNA clusters in development and disease. Cancer J 18:262-267.
8. Flavell SW, Cowan CW, Kim TK, Greer PL, Lin Y, Paradis S, Griffith EC, Hu LS, Chen C, Greenberg ME. 2006. Activity-dependent regulation of MEF2 transcription factors suppresses excitatory synapse number. Science 311:1008-1012.
9. Fukushima H, Maeda R, Suzuki R, Suzuki A, Nomoto M, Toyoda H, Wu LJ, Xu H, Zhao MG, Ueda K, Kitamoto A, Mamiya N, Yoshida T, Homma S, Masushige S, Zhuo M, Kida S. 2008. Upregulation of calcium/calmodulin-dependent protein kinase IV improves memory formation and rescues memory loss with aging. J Neurosci 28:9910-9919.
10. Gao J, Wang WY, Mao YW, Gräff 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.
11. Griggs EM, Young EJ, Rumbaugh G, Miller CA. 2013. MicroRNA-182 regulates amygdala-dependent memory formation. J Neurosci 33:1734-1740.
12. He M, Liu Y, Wang X, Zhang MQ, Hannon GJ, Huang ZJ. 2012. Cell-type-based analysis of microRNA profiles in the mouse brain. Neuron 73:35-48.
13. Hu Z, Yu D, Gu QH, Yang Y, Tu K, Zhu J, Li Z. 2014. miR-191 and miR-135 are required for long-lasting spine remodelling associated with synaptic long-term depression. Nat Commun 5:3263.
14. Inukai S, de Lencastre A, Turner M, Slack F. 2012. Novel microRNAs differentially expressed during aging in the mouse brain. PLoS One 7:e40028.
15. Li H, Khirug S, Cai C, Ludwig A, Blaesse P, Kolikova J, Afzalov R, Coleman SK, Lauri S, Airaksinen MS, Keinänen K, Khiroug L, Saarma M, Kaila K, Rivera C. 2007. KCC2 interacts with the dendritic cytoskeleton to promote spine development. Neuron 56:1019-1033.
16. Lin Q, Wei W, Coelho CM, Li X, Baker-Andresen D, Dudley K, Ratnu VS, Boskovic Z, Kobor MS, Sun YE, Bredy TW. 2011. The brain-specific microRNA miR-128 regulates the formation of extinction memory. Nat Neurosci 14:1115-1117.
17. Maren S, Phan KL, Liberzon I. 2013. The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat Rev Neurosci 14:417-428.
18. McNeill E, Van Vactor D. 2012. MicroRNAs shape the neuronal landscape. Neuron 75:363-379.
19. Morgan M, Iaconcig A, Muro AF. 2010. CPEB2, CPEB3 and CPEB4 are coordinately regulated by miRNAs recognizing conserved binding sites in paralog positions of their 3′-UTRs. Nucleic Acids Res 38:7698-7710.
20. Nowakowski TJ, Fotaki V, Pollock A, Sun T, Pratt T, Price DJ. 2013. MicroRNA-92b regulates the development of intermediate cortical progenitors in embryonic mouse brain. Proc Natl Acad Sci U S A 110:7056-7061.
21. Perkins DO, Jeffries CD, Jarskog LF, Thomson JM, Woods K, Newman MA, Parker JS, Jin J, Hammond SM. 2007. microRNA expression in the prefrontal cortex of individuals with schizophrenia and schizoaffective disorder. Genome Biol 8:R27.
22. Restivo L, Vetere G, Bontempi B, Ammassari-Teule M. 2009. The formation of recent and remote memory is associated with time-dependent formation of dendritic spines in the hippocampus and anterior cingulate cortex. J Neurosci 29:8206-8214.
23. Soeter M, Kindt M. 2013. High trait anxiety: a challenge for disrupting fear memory reconsolidation. PLoS One 8:2013.
24. Tornberg J, Voikar V, Savilahti H, Rauvala H, Airaksinen MS. 2005. Behavioural phenotypes of hypomorphic KCC2-deficient mice. Eur J Neurosci 21:1327-1337.
25. 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.
26. Zhou Q, Homma KJ, Poo MM. 2004. Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44:749-757.
27. Zovoilis A, Agbemenyah HY, Agis-Balboa RC, Stilling RM, Edbauer D, Rao P, Farinelli L, Delalle I, Schmitt A, Falkai P, Bahari-Javan S, Burkhardt S, Sananbenesi F, Fischer A. 2011. microRNA-34c is a novel target to treat dementias. EMBO J 30:4299-4308.