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miR-135a Regulates Synaptic Transmission and Anxiety-Like Behavior in Amygdala

Mannironi, Cecilia, Biundo, Antonio, Rajendran, Samyutha, De Vito, Francesca, Saba, Luana, Caioli, Silvia, Zona, Cristina, Ciotti, Teresa, Caristi, Silvana, Perlas, Emerald, Del Vecchio, Giorgia, Bozzoni, Irene, Rinaldi, Arianna, Mele, Andrea, Presutti, Carlo·2018·Molecular Neurobiology

Abstract

MicroRNAs are a class of non-coding RNAs with a growing relevance in the regulation of gene expression related to brain function and plasticity. They have the potential to orchestrate complex phenomena, such as the neuronal response to homeostatic challenges. We previously demonstrated the involvement of miR-135a in the regulation of early stress response. In the present study, we examine the role of miR-135a in stress-related behavior. We show that the knockdown (KD) of miR-135a in the mouse amygdala induces an increase in anxiety-like behavior. Consistently with behavioral studies, electrophysiological experiments in acute brain slices indicate an increase of amygdala spontaneous excitatory postsynaptic currents, as a result of miR-135a KD. Furthermore, we presented direct evidences, by in vitro assays and in vivo miRNA overexpression in the amygdala, that two key regulators of synaptic vesicle fusion, complexin-1 and complexin-2, are direct targets of miR-135a. In vitro analysis of miniature excitatory postsynaptic currents on miR-135a KD primary neurons indicates unpaired quantal excitatory neurotransmission. Finally, increased levels of complexin-1 and complexin-2 proteins were detected in the mouse amygdala after acute stress, accordingly to the previously observed stress-induced miR-135a downregulation. Overall, our results unravel a previously unknown miRNA-dependent mechanism in the amygdala for regulating anxiety-like behavior, providing evidences of a physiological…

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  1. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297 · DOI
  2. Krol J, Loedige I, Filipowicz W (2010) The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet. doi: 10.1038/nrg2843 · DOI · Paper page
  3. Eichhorn SW, Guo H, McGeary SE et al (2014) mRNA destabilization is the dominant effect of mammalian MicroRNAs by the time substantial repression ensues. Mol Cell 56:104–115. doi: 10.1016/j.molcel.2014.08.028 · DOI · Paper page
  4. Kosik KS (2006) The neuronal microRNA system. Nat Rev Neurosci 7:911–920. doi: 10.1038/nrn2037 · DOI
  5. Schratt G (2009) microRNAs at the synapse. Nat Rev Neurosci 10:842–849. doi: 10.1038/nrn2763 · DOI · Paper page
  6. Siegel G, Saba R, Schratt G (2011) microRNAs in neurons: manifold regulatory roles at the synapse. Curr Opin Genet Dev 21:491–497. doi: 10.1016/j.gde.2011.04.008 · DOI
  7. van Spronsen M, van Battum EY, Kuijpers 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.s002 · DOI
  8. Ashraf SI, McLoon AL, Sclarsic SM, Kunes S (2006) Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 124:191–205. doi: 10.1016/j.cell.2005.12.017 · DOI
  9. Capitano F, Camon J, Ferretti V et al (2015) microRNAs modulate spatial memory in the hippocampus and in the ventral striatum in a region-specific manner. Mol Neurobiol. doi: 10.1007/s12035-015-9398-5 · DOI
  10. Capitano F, Camon J, Licursi V et al (2016) MicroRNA-335-5p modulates spatial memory and hippocampal synaptic plasticity. Neurobiol Learn Mem 139:63–68. doi: 10.1016/j.nlm.2016.12.019 · DOI
  11. Dias BG, Goodman JV, Ahluwalia R et al (2014) Amygdala-dependent fear memory consolidation via miR-34a and notch signaling. Neuron 83:906–918. doi: 10.1016/j.neuron.2014.07.019 · DOI
  12. Volk N, Paul ED, Haramati S et al (2014) MicroRNA-19b associates with Ago2 in the amygdala following chronic stress and regulates the adrenergic receptor beta 1. J Neurosci 34:15070–15082. doi: 10.1523/JNEUROSCI.0855-14.2014 · DOI
  13. Issler O, Haramati S, Paul ED et al (2014) MicroRNA 135 is essential for chronic stress resiliency, antidepressant efficacy, and intact serotonergic activity. Neuron 83:344–360. doi: 10.1016/j.neuron.2014.05.042 · DOI · Paper page
  14. Mannironi C, Camon J, De Vito F et al (2013) Acute stress alters amygdala microRNA miR-135a and miR-124 expression: inferences for corticosteroid dependent stress response. PLoS One 8:e73385. doi: 10.1371/journal.pone.0073385 · DOI
  15. Meerson A, Cacheaux L, Goosens KA et al (2010) Changes in brain MicroRNAs contribute to cholinergic stress reactions. J Mol Neurosci 40:47–55. doi: 10.1007/s12031-009-9252-1 · DOI
  16. Rinaldi A, Vincenti S, De Vito F et al (2010) Behav Brain Res 208:265–269. doi: 10.1016/j.bbr.2009.11.012 · DOI
  17. Malan-Müller S, Hemmings SMJ, Seedat S (2012) Big effects of small RNAs: a review of MicroRNAs in anxiety. Mol Neurobiol 47:726–739. doi: 10.1007/s12035-012-8374-6 · DOI
  18. Davidson RJ, Abercrombie H, Nitschke JB, Putnam K (1999) Regional brain function, emotion and disorders of emotion. Curr Opin Neurobiol 9:228–234 · DOI
  19. Jiang L, Role LW (2008) Facilitation of cortico-amygdala synapses by nicotine: activity-dependent modulation of glutamatergic transmission. J Neurophysiol 99:1988–1999. doi: 10.1152/jn.00933.2007 · DOI
  20. Haramati S, Navon I, Issler O et al (2011) microRNA as repressors of stress-induced anxiety: the case of amygdala miR-34. J Neurosci 31:14191–14203. doi: 10.1523/JNEUROSCI.1673-11.2011 · DOI · Paper page
  21. Vetere G, Barbato C, Pezzola S et al (2014) Selective inhibition of miR-92 in hippocampal neurons alters contextual fear memory. Hippocampus 24:1458–1465. doi: 10.1002/hipo.22326 · DOI · Paper page
  22. Li X, Khanna A, Li N, Wang E (2011) Circulatory miR-34a as an RNA-based, noninvasive biomarker for brain aging. Aging (Albany NY) · DOI
  23. Elmén J, Lindow M, Schütz S et al (2008) LNA-mediated microRNA silencing in non-human primates. Nature 452:896–899. doi: 10.1038/nature06783 · DOI · Paper page
  24. Kocerha J, Faghihi MA, Lopez-Toledano MA et al (2009) MicroRNA-219 modulates NMDA receptor-mediated neurobehavioral dysfunction. Proc Natl Acad Sci 106:3507–3512. doi: 10.1073/pnas.0805854106 · DOI
  25. Jimenez-Mateos EM, Bray I, Sanz-Rodriguez A 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 · DOI
  26. Zovoilis A, Agbemenyah HY, Agis-Balboa RC et al (2011) microRNA-34c is a novel target to treat dementias. EMBO J 30:4299–4308. doi: 10.1038/emboj.2011.327 · DOI · Paper page
  27. Brose N (2008) For better or for worse: complexins regulate SNARE function and vesicle fusion. Traffic 9:1403–1413. doi: 10.1111/j.1600-0854.2008.00758.x · DOI
  28. Maximov A, Tang J, Yang X et al (2009) Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science 323:516–521. doi: 10.1126/science.1166505 · DOI
  29. McMahon HT, Missler M, Li C, Sudhof TC (1995) Complexins: cytosolic proteins that regulate SNAP receptor function. Cell 83(1):111–119 · DOI
  30. Hu Z, Yu D, Gu Q et al (2014) miR-191 and miR-135 are required for long-lasting spine remodelling associated with synaptic long-term depression. Nat Comms. doi: 10.1038/ncomms4263 · DOI
  31. Peña CJ, Bagot RC, Labonté B, Nestler EJ (2014) Epigenetic signaling in psychiatric disorders. J Mol Biol 426:3389–3412. doi: 10.1016/j.jmb.2014.03.016 · DOI · Paper page
  32. Tye KM, Prakash R, Kim S-Y et al (2011) Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471:358–362. doi: 10.1038/nature09820 · DOI · Paper page
  33. Hubert GW, Li C, Rainnie DG, Muly EC (2013) Effects of stress on AMPA receptor distribution and function in the basolateral amygdala. Brain Struct Funct 219:1169–1179. doi: 10.1007/s00429-013-0557-z · DOI
  34. de Kloet ER, Joëls M, Holsboer F (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6:463–475. doi: 10.1038/nrn1683 · DOI · Paper page
  35. Zhou H, Guo W, Zhao Y et al (2014) MicroRNA-135a acts as a putative tumor suppressor by directly targeting very low density lipoprotein receptor in human gallbladder cancer. Cancer Sci 105:956–965. doi: 10.1111/cas.12463 · DOI
  36. Kroiss A, Vincent S, Decaussin-Petrucci M et al (2015) Androgen-regulated microRNA-135a decreases prostate cancer cell migration and invasion through downregulating ROCK1 and ROCK2. Oncogene 34:2846–2855. doi: 10.1038/onc.2014.222 · DOI
  37. Hemmesi K, Squadrito ML, Mestdagh P, Conti V, Cominelli M, Piras IS, Sergi LS, Piccinin S et al (2015) miR-135a inhibits cancer stem cell-driven medulloblastoma development by directly repressing Arhgef6 expression. Stem Cells 33:1377–1389. doi: 10.1002/stem.1958 · DOI
  38. Chang S, Reim K, Pedersen M et al (2015) Complexin stabilizes newly primed synaptic vesicles and prevents their premature fusion at the mouse calyx of held synapse. J Neurosci 35:8272–8290. doi: 10.1523/JNEUROSCI.4841-14.2015 · DOI
  39. Brose N (2008) Altered complexin expression in psychiatric and neurological disorders: cause or consequence? Mol Cells 25:7–19 · DOI
  40. Heegde ter F, De Rijk RH, Vinkers CH (2015) The brain mineralocorticoid receptor and stress resilience. Psychoneuroendocrinology 52:92–110. doi: 10.1016/j.psyneuen.2014.10.022 · DOI · Paper page

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Metadata

Authors
Mannironi, C., Biundo, A., Rajendran, S., De Vito, F., Saba, L., Caioli, S., Zona, C., Ciotti, T., Caristi, S., Perlas, E., Del Vecchio, G., Bozzoni, I., Rinaldi, A., Mele, A., & Presutti, C.
Venue
Molecular Neurobiology
Published
2017-05-09
Volume
55
Issue
4
Pages
3301-3315
ISSN
  • 0893-7648
  • 1559-1182
Cited by
49
References
7
Language
en
Funders
  • Filas (Project F57I12000110009)
  • ERC-2013 (AdG 340172-MUNCODD)
  • Arisla (full grant 2014 “RNA circuitries in Amyotrophic Lateral Sclerosis pathogenesis”)

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