The non-coding RNA BC1 regulates experience-dependent structural plasticity and learning

Victor Briz; Leonardo Restivo; Emanuela Pasciuto; Konrad Juczewski; Valentina Mercaldo; Adrian C Lo; Pieter Baatsen; Natalia V Gounko; Antonella Borreca; Tiziana Girardi; Rossella Luca; Julie Nys; Rogier B Poorthuis; Huibert D Mansvelder; Gilberto Fisone; Martine Ammassari-Teule; Lutgarde Arckens; Patrik Krieger; Rhiannon Meredith; Claudia Bagni

doi:10.1038/s41467-017-00311-2

The non-coding RNA BC1 regulates experience-dependent structural plasticity and learning

Victor Briz, Leonardo Restivo, Emanuela Pasciuto, Konrad Juczewski, Valentina Mercaldo, Adrian C Lo, Pieter Baatsen, Natalia V Gounko, Antonella Borreca, Tiziana Girardi, Rossella Luca, Julie Nys, Rogier B Poorthuis, Huibert D Mansvelder, Gilberto Fisone, Martine Ammassari-Teule, Lutgarde Arckens, Patrik Krieger, Rhiannon Meredith, Claudia Bagni

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

The brain cytoplasmic (BC1) RNA is a non-coding RNA (ncRNA) involved in neuronal translational control. Absence of BC1 is associated with altered glutamatergic transmission and maladaptive behavior. Here, we show that pyramidal neurons in the barrel cortex of BC1 knock out (KO) mice display larger excitatory postsynaptic currents and increased spontaneous activity in vivo. Furthermore, BC1 KO mice have enlarged spine heads and postsynaptic densities and increased synaptic levels of glutamate receptors and PSD-95. Of note, BC1 KO mice show aberrant structural plasticity in response to whisker deprivation, impaired texture novel object recognition and altered social behavior. Thus, our study highlights a role for BC1 RNA in experience-dependent plasticity and learning in the mammalian adult neocortex, and provides insight into the function of brain ncRNAs regulating synaptic transmission, plasticity and behavior, with potential relevance in the context of intellectual disabilities and psychiatric disorders.Brain cytoplasmic (BC1) RNA is a non-coding RNA that has been implicated in translational regulation, seizure, and anxiety. Here, the authors show that in the cortex, BC1 RNA is required for sensory deprivation-induced structural plasticity of dendritic spines, as well as for correct sensory learning and social behaviors.

Original language	English
Article number	293
Pages (from-to)	293
Journal	Nature Communications
Volume	8
Issue number	1
DOIs	https://doi.org/10.1038/s41467-017-00311-2
Publication status	Published - 17 Aug 2017

Funding

We are thankful to Eef Lemmens and Annick Crevoisier for excellent administrative support and to Jonathan Royaert, Karin Jonkers, Joanna Viguie and Nathalie Leysen for technical assistance with neuronal cultures and mouse colonies. We thank Frone Vandewiele for helping with the membrane fractionation experiments and Ria Van Laer for technical assistance with the CO histochemistry. We are grateful to Zsuzsanna Callaerts-Vegh, Hilde Brems and Rudi D’Hooge for valuable discussions of the behavioral experiments. Finally, we thank Eleonora Rosina, Marijke Laarakker, Martien Kas, Muna Hilal, Carl Petersen, Sermet Berat Semihcan for the preliminary electrophysiological and behavioral data and Egbert Welker and Tilmann Achsel for critical reading of the manuscript, constructive experimental suggestions and data analysis. The Nikon microscope used in this study was acquired through a Hercules Type 1 AKUL/09/037 to Wim Annaert. This work was supported by the Fonds Wetenschap-pelijk Onderzoek Vlaanderen (FWO G070511N10 and GO88415N), Telethon (GGP15257), Queen Elisabeth Foundation (FMRE), Solvay Price, VIB, NEURON ERA-NET and 51NF40-158776 NCCR Synapsy to C.B.; Dutch Medical Research Council, NWO ZonMW (# 91710372) to R.M.; EU-BrainTrain (FP7-People-ITN-2008-238055) to C.B. and R.M.; German Research Foundation (SFB 874/A9) to P.K. We are thankful to Eef Lemmens and Annick Crevoisier for excellent administrative support and to Jonathan Royaert, Karin Jonkers, Joanna Viguie and Nathalie Leysen for technical assistance with neuronal cultures and mouse colonies. We thank Frone Vandewiele for helping with the membrane fractionation experiments and Ria Van Laer for technical assistance with the CO histochemistry. We are grateful to Zsuzsanna Callaerts-Vegh, Hilde Brems and Rudi D'Hooge for valuable discussions of the behavioral experiments. Finally, we thank Eleonora Rosina, Marijke Laarakker, Martien Kas, Muna Hilal, Carl Petersen, Sermet Berat Semihcan for the preliminary electrophysiological and behavioral data and Egbert Welker and Tilmann Achsel for critical reading of the manuscript, constructive experimental suggestions and data analysis. The Nikon microscope used in this study was acquired through a Hercules Type 1 AKUL/09/037 to Wim Annaert. This work was supported by the Fonds Wetenschappelijk Onderzoek Vlaanderen (FWO G070511N10 and GO88415N), Telethon (GGP15257), Queen Elisabeth Foundation (FMRE), Solvay Price, VIB, NEURON ERANET and 51NF40-158776 NCCR Synapsy to C.B.; Dutch Medical Research Council, NWO ZonMW (# 91710372) to R.M.; EU-BrainTrain (FP7-People-ITN-2008-238055) to C.B. and R.M.; German Research Foundation (SFB 874/A9) to P.K.

Funders	Funder number
Dutch Medical Research Council
FMRE
Fonds Wetenschap-pelijk Onderzoek Vlaanderen
NWO ZonMw	FP7-People-ITN-2008-238055, 91710372
Queen Elisabeth Foundation
Solvay Price
Seventh Framework Programme	238055
Deutsche Forschungsgemeinschaft	SFB 874/A9
ZonMw
Fondazione Telethon	GGP15257
Fonds Wetenschappelijk Onderzoek	GO88415N, G070511N10
Vlaams Instituut voor Biotechnologie
Neuron Nadační Fond Na Podporu Vědy	51NF40-158776

Keywords

Animals
Base Sequence
Cells, Cultured
Dendritic Spines
Excitatory Postsynaptic Potentials
In Situ Hybridization, Fluorescence
Journal Article
Learning
Male
Mice, Inbred C57BL
Mice, Knockout
Microscopy, Electron
Neocortex
Neuronal Plasticity
Pyramidal Cells
RNA, Small Cytoplasmic
Research Support, Non-U.S. Gov't
Sensory Deprivation
Sequence Homology, Nucleic Acid
Social Behavior
Synaptic Transmission
Vibrissae

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Briz, V., Restivo, L., Pasciuto, E., Juczewski, K., Mercaldo, V., Lo, A. C., Baatsen, P., Gounko, N. V., Borreca, A., Girardi, T., Luca, R., Nys, J., Poorthuis, R. B., Mansvelder, H. D., Fisone, G., Ammassari-Teule, M., Arckens, L., Krieger, P., Meredith, R., & Bagni, C. (2017). The non-coding RNA BC1 regulates experience-dependent structural plasticity and learning. Nature Communications, 8(1), 293. Article 293. https://doi.org/10.1038/s41467-017-00311-2

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abstract = "The brain cytoplasmic (BC1) RNA is a non-coding RNA (ncRNA) involved in neuronal translational control. Absence of BC1 is associated with altered glutamatergic transmission and maladaptive behavior. Here, we show that pyramidal neurons in the barrel cortex of BC1 knock out (KO) mice display larger excitatory postsynaptic currents and increased spontaneous activity in vivo. Furthermore, BC1 KO mice have enlarged spine heads and postsynaptic densities and increased synaptic levels of glutamate receptors and PSD-95. Of note, BC1 KO mice show aberrant structural plasticity in response to whisker deprivation, impaired texture novel object recognition and altered social behavior. Thus, our study highlights a role for BC1 RNA in experience-dependent plasticity and learning in the mammalian adult neocortex, and provides insight into the function of brain ncRNAs regulating synaptic transmission, plasticity and behavior, with potential relevance in the context of intellectual disabilities and psychiatric disorders.Brain cytoplasmic (BC1) RNA is a non-coding RNA that has been implicated in translational regulation, seizure, and anxiety. Here, the authors show that in the cortex, BC1 RNA is required for sensory deprivation-induced structural plasticity of dendritic spines, as well as for correct sensory learning and social behaviors.",

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author = "Victor Briz and Leonardo Restivo and Emanuela Pasciuto and Konrad Juczewski and Valentina Mercaldo and Lo, {Adrian C} and Pieter Baatsen and Gounko, {Natalia V} and Antonella Borreca and Tiziana Girardi and Rossella Luca and Julie Nys and Poorthuis, {Rogier B} and Mansvelder, {Huibert D} and Gilberto Fisone and Martine Ammassari-Teule and Lutgarde Arckens and Patrik Krieger and Rhiannon Meredith and Claudia Bagni",

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Briz, V, Restivo, L, Pasciuto, E, Juczewski, K, Mercaldo, V, Lo, AC, Baatsen, P, Gounko, NV, Borreca, A, Girardi, T, Luca, R, Nys, J, Poorthuis, RB, Mansvelder, HD, Fisone, G, Ammassari-Teule, M, Arckens, L, Krieger, P, Meredith, R & Bagni, C 2017, 'The non-coding RNA BC1 regulates experience-dependent structural plasticity and learning', Nature Communications, vol. 8, no. 1, 293, pp. 293. https://doi.org/10.1038/s41467-017-00311-2

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T1 - The non-coding RNA BC1 regulates experience-dependent structural plasticity and learning

AU - Briz, Victor

AU - Restivo, Leonardo

AU - Pasciuto, Emanuela

AU - Juczewski, Konrad

AU - Mercaldo, Valentina

AU - Lo, Adrian C

AU - Baatsen, Pieter

AU - Gounko, Natalia V

AU - Borreca, Antonella

AU - Girardi, Tiziana

AU - Luca, Rossella

AU - Nys, Julie

AU - Poorthuis, Rogier B

AU - Mansvelder, Huibert D

AU - Fisone, Gilberto

AU - Ammassari-Teule, Martine

AU - Arckens, Lutgarde

AU - Krieger, Patrik

AU - Meredith, Rhiannon

AU - Bagni, Claudia

PY - 2017/8/17

Y1 - 2017/8/17

N2 - The brain cytoplasmic (BC1) RNA is a non-coding RNA (ncRNA) involved in neuronal translational control. Absence of BC1 is associated with altered glutamatergic transmission and maladaptive behavior. Here, we show that pyramidal neurons in the barrel cortex of BC1 knock out (KO) mice display larger excitatory postsynaptic currents and increased spontaneous activity in vivo. Furthermore, BC1 KO mice have enlarged spine heads and postsynaptic densities and increased synaptic levels of glutamate receptors and PSD-95. Of note, BC1 KO mice show aberrant structural plasticity in response to whisker deprivation, impaired texture novel object recognition and altered social behavior. Thus, our study highlights a role for BC1 RNA in experience-dependent plasticity and learning in the mammalian adult neocortex, and provides insight into the function of brain ncRNAs regulating synaptic transmission, plasticity and behavior, with potential relevance in the context of intellectual disabilities and psychiatric disorders.Brain cytoplasmic (BC1) RNA is a non-coding RNA that has been implicated in translational regulation, seizure, and anxiety. Here, the authors show that in the cortex, BC1 RNA is required for sensory deprivation-induced structural plasticity of dendritic spines, as well as for correct sensory learning and social behaviors.

AB - The brain cytoplasmic (BC1) RNA is a non-coding RNA (ncRNA) involved in neuronal translational control. Absence of BC1 is associated with altered glutamatergic transmission and maladaptive behavior. Here, we show that pyramidal neurons in the barrel cortex of BC1 knock out (KO) mice display larger excitatory postsynaptic currents and increased spontaneous activity in vivo. Furthermore, BC1 KO mice have enlarged spine heads and postsynaptic densities and increased synaptic levels of glutamate receptors and PSD-95. Of note, BC1 KO mice show aberrant structural plasticity in response to whisker deprivation, impaired texture novel object recognition and altered social behavior. Thus, our study highlights a role for BC1 RNA in experience-dependent plasticity and learning in the mammalian adult neocortex, and provides insight into the function of brain ncRNAs regulating synaptic transmission, plasticity and behavior, with potential relevance in the context of intellectual disabilities and psychiatric disorders.Brain cytoplasmic (BC1) RNA is a non-coding RNA that has been implicated in translational regulation, seizure, and anxiety. Here, the authors show that in the cortex, BC1 RNA is required for sensory deprivation-induced structural plasticity of dendritic spines, as well as for correct sensory learning and social behaviors.

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KW - Base Sequence

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KW - Excitatory Postsynaptic Potentials

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KW - Journal Article

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The non-coding RNA BC1 regulates experience-dependent structural plasticity and learning

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Keywords

UN SDGs

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