Non-coding RNAs: the gatekeepers of neural network activity
Abstract
Non-coding RNAs have emerged as potent regulators of numerous cellular processes. In neurons and circuits, these molecules serve especially critical functions that ensure neural activity is maintained within appropriate physiological parameters. Their targets include synaptic proteins, ion channels, neurotransmitter receptors, and components of essential signaling cascades. Here, we discuss how several species of non-coding RNAs (ncRNAs) regulate intrinsic excitability and synaptic transmission, both during development and in mature circuits. Furthermore, we present the relationships between aberrant ncRNA expression and psychiatric disorders. The research presented here demonstrates how ncRNAs can be useful tools for elucidating fundamental neurobiology mechanisms and identifying the key molecular players.
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The importance of ncRNAs is becoming increasingly apparent, not only in alcohol dependence but in brain physiology in general.
“However, the importance of ncRNAs is becoming increasingly apparent, not only in alcohol dependence (36) , but in brain physiology in general (37) , and these RNAs were therefore included in our data.”
From Single cell transcriptome profiling of the human alcohol-dependent brain (2020) · cites this paper as [37]
Cites
Excitatory actions of gaba during development: the nature of the nurture
Ben-Ari, Y. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn920 · Cited by 2,448 · see citing works
A brain-specific microRNA regulates dendritic spine development
Schratt, G. M., Tuebing, F., Nigh, E. A., Kane, C. G., Sabatini, M. E., Kiebler, M., & Greenberg, M. E. (2006) · Nature · doi:10.1038/nature04367 · Cited by 1,786 · see citing works
How Inhibition Shapes Cortical Activity
Isaacson, J. S., & Scanziani, M. (2011) · Neuron · doi:10.1016/j.neuron.2011.09.027 · Cited by 1,678 · see citing works
Genome-wide association analysis identifies 13 new risk loci for schizophrenia
Multicenter Genetic Studies of Schizophrenia Consortium, Ripke, S., Psychosis Endophenotypes International Consortium, Wellcome Trust Case Control Consortium 2, O'Dushlaine, C., Chambert, K., Moran, J. L., Kähler, A. K., Akterin, S., Bergen, S. E., et al. (2013) · Nature Genetics · doi:10.1038/ng.2742 · Cited by 1,496 · see citing works
MAPK cascade signalling and synaptic plasticity
Thomas, G. M., & Huganir, R. L. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1346 · Cited by 1,454 · see citing works
Loss of a mammalian circular RNA locus causes miRNA deregulation and affects brain function
Piwecka, M., Glažar, P., Hernandez-Miranda, L. R., Memczak, S., Wolf, S. A., Rybak-Wolf, A., Filipchyk, A., Klironomos, F., Cerda Jara, C. A., Fenske, P., et al. (2017) · Science · doi:10.1126/science.aam8526 · Cited by 1,210 · see citing works
Mechanisms underlying spontaneous patterned activity in developing neural circuits
Blankenship, A. G., & Feller, M. B. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2759 · Cited by 851 · see citing works
Zoghbi, H. Y., & Bear, M. F. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a009886 · Cited by 797 · see citing works
Genome-wide changes in lncRNA, splicing, and regional gene expression patterns in autism
Parikshak, N. N., Swarup, V., Belgard, T. G., Irimia, M., Ramaswami, G., Gandal, M. J., Hartl, C., Leppa, V., Ubieta, L. D. L. T., Huang, J., et al. (2016) · Nature · doi:10.1038/nature20612 · Cited by 685 · see citing works
Silencing microRNA-134 produces neuroprotective and prolonged seizure-suppressive effects
Jimenez-Mateos, E. M., Engel, T., Merino‐Serrais, P., McKiernan, R. C., Tanaka, K., Mouri, G., Sano, T., O’Tuathaigh, C. M. P., Waddington, J. L., Prenter, S., et al. (2012) · Nature Medicine · doi:10.1038/nm.2834 · Cited by 463 · see citing works
The splicing regulator Rbfox1 (A2BP1) controls neuronal excitation in the mammalian brain
Gehman, L. T., Stoilov, P., Maguire, J., Damianov, A., Lin, C.-H., Shiue, L., Ares, M., Mody, I., & Black, D. L. (2011) · Nature Genetics · doi:10.1038/ng.841 · Cited by 331 · see citing works
MicroRNA-128 Governs Neuronal Excitability and Motor Behavior in Mice
Tan, C. L., Plotkin, J. L., Venø, M. T., von Schimmelmann, M. J., Feinberg, P. A., Mann, S., Handler, A., Kjems, J., Surmeier, D. J., O’Carroll, D., et al. (2013) · Science · doi:10.1126/science.1244193 · Cited by 301 · see citing works
Cytoplasmic Rbfox1 Regulates the Expression of Synaptic and Autism-Related Genes
Lee, J.-A., Damianov, A., Lin, C.-H., Fontes, M., Parikshak, N. N., Anderson, E. S., Geschwind, D. H., Black, D. L., & Martin, K. C. (2016) · Neuron · doi:10.1016/j.neuron.2015.11.025 · Cited by 232 · see citing works
The schizophrenia risk gene product miR-137 alters presynaptic plasticity
Siegert, S., Seo, J., Kwon, E. J., Rudenko, A., Cho, S., Wang, W., Flood, Z., Martorell, A. J., Ericsson, M., Mungenast, A. E., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.4023 · Cited by 224 · see citing works
Genome-wide, integrative analysis implicates microRNA dysregulation in autism spectrum disorder
Wu, Y. E., Parikshak, N. N., Belgard, T. G., & Geschwind, D. H. (2016) · Nature Neuroscience · doi:10.1038/nn.4373 · Cited by 195 · see citing works
Activity-dependent spatially localized miRNA maturation in neuronal dendrites
Sambandan, S., Akbalık, G., Kochen, L., Rinne, J. S., Kahlstatt, J., Glock, C., Tushev, G., Alvarez‐Castelao, B., Heckel, A., & Schuman, E. M. (2017) · Science · doi:10.1126/science.aaf8995 · Cited by 179 · see citing works
Regulation of cell-type-specific transcriptomes by microRNA networks during human brain development
Nowakowski, T. J., Rani, N., Golkaram, M., Zhou, H. R., Alvarado, B., Huch, K., West, J. A., Leyrat, A., Pollen, A. A., Kriegstein, A. R., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0265-3 · Cited by 166 · see citing works
Loss of motoneuron-specific microRNA-218 causes systemic neuromuscular failure
Amin, N. D., Bai, G., Klug, J. R., Bonanomi, D., Pankratz, M. T., Gifford, W. D., Hinckley, C. A., Sternfeld, M. J., Driscoll, S. P., Dominguez, B., et al. (2015) · Science · doi:10.1126/science.aad2509 · Cited by 146 · see citing works
miR-183 cluster scales mechanical pain sensitivity by regulating basal and neuropathic pain genes
Peng, C., Li, L., Zhang, M.-D., Gonzales, C. B., Parisien, M., Belfer, I., Usoskin, D., Abdo, H., Furlan, A., Häring, M., et al. (2017) · Science · doi:10.1126/science.aam7671 · Cited by 142 · see citing works
Cheng, Y., Wang, Z., Tan, W., Wang, X., Li, Y., Bai, B., Li, Y., Zhang, S.-F., Yan, H., Chen, Z.-L., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0261-7 · Cited by 136 · see citing works
Specific disruption of thalamic inputs to the auditory cortex in schizophrenia models
Chun, S., Westmoreland, J. J., Bayazitov, I. T., Eddins, D. M., Pani, A. K., Smeyne, R. J., Yu, J., Blundon, J. A., & Zakharenko, S. S. (2014) · Science · doi:10.1126/science.1253895 · Cited by 123 · see citing works
Forrest, M. P., Zhang, H., Moy, W., McGowan, H., Leites, C., Dionisio, L. E., Xu, Z., Shi, J., Sanders, A. R., Greenleaf, W. J., et al. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.07.008 · Cited by 118 · see citing works
Brennan, G. P., Dey, D., Chen, Y., Patterson, K. P., Magnetta, E., Hall, A. M., Dubé, C. M., Mei, Y., & Baram, T. Z. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.02.042 · Cited by 114 · see citing works
Sakai, A., Saitow, F., Maruyama, M., Miyake, N., Miyake, K., Shimada, T., Okada, T., & Suzuki, H. (2017) · Nature Communications · doi:10.1038/ncomms16079 · Cited by 114 · see citing works
A coding-independent function of an alternative Ube3a transcript during neuronal development
Valluy, J., Bicker, S., Aksoy‐Aksel, A., Lackinger, M., Sumer, S., Fiore, R., Wüst, T., Seffer, D., Metge, F., Dieterich, C., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.3996 · Cited by 106 · see citing works
MicroRNA miR124 is required for the expression of homeostatic synaptic plasticity
Hou, Q., Ruan, H., Gilbert, J. P., Wang, G., Ma, Q., Yao, W., & Man, H. (2015) · Nature Communications · doi:10.1038/ncomms10045 · Cited by 103 · see citing works
Rbfox1 Regulates Synaptic Transmission through the Inhibitory Neuron-Specific vSNARE Vamp1
Vuong, C. K., Wei, W., Lee, J.-A., Lin, C.-H., Damianov, A., de la Torre-Ubieta, L., Halabi, R., Otis, K. O., Martin, K. C., O’Dell, T. J., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.03.008 · Cited by 102 · see citing works
Bellon, A., Iyer, A., Bridi, S., Lee, F. C. Y., Ovando‐Vázquez, C., Corradi, E., Longhi, S., Roccuzzo, M., Strohbuecker, S., Naik, S., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2016.12.093 · Cited by 99 · see citing works
MicroRNA-Mediated Downregulation of the Potassium Channel Kv4.2 Contributes to Seizure Onset
Groß, C., Yao, X., Engel, T., Tiwari, D., Xing, L., Rowley, S. D., Danielson, S. W., Thomas, K. T., Jimenez-Mateos, E. M., Schroeder, L. M., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.08.074 · Cited by 92 · see citing works
Regulation of Neuroregeneration by Long Noncoding RNAs
Perry, R. B., Hezroni, H., Goldrich, M. J., & Ulitsky, I. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.09.021 · Cited by 91 · see citing works
Functional Implications of miR-19 in the Migration of Newborn Neurons in the Adult Brain
Han, J., Kim, H. J., Schafer, S. T., Paquola, A. C. M., Clemenson, G. D., Toda, T., Oh, J., Pankonin, A. R., Lee, B. S., Johnston, S. T., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.05.034 · Cited by 89 · see citing works
A microRNA‐129‐5p/Rbfox crosstalk coordinates homeostatic downscaling of excitatory synapses
Rajman, M., Metge, F., Fiore, R., Khudayberdiev, S., Aksoy-Aksel, A., Bicker, S., Reschke, C. R., Raoof, R., Brennan, G., Delanty, N., et al. (2017) · EMBO Journal · doi:10.15252/embj.201695748 · Cited by 89 · see citing works
Lippi, G., Fernandes, C., Ewell, L. A., John, D., Romoli, B., Curia, G., Taylor, S. R., Frady, E. P., Jensen, A. B., Liu, J. C., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.11.017 · Cited by 85 · see citing works
A neuroprotective role for microRNA miR-1000 mediated by limiting glutamate excitotoxicity
Verma, P., Augustine, G. J., Ammar, M.-R., Tashiro, A., & Cohen, S. M. (2015) · Nature Neuroscience · doi:10.1038/nn.3935 · Cited by 83 · see citing works
miR-92a regulates expression of synaptic GluA1-containing AMPA receptors during homeostatic scaling
Letellier, M., Elramah, S., Mondin, M., Soula, A., Penn, A. C., Choquet, D., Landry, M., Thoumine, O. R., & Favereaux, A. (2014) · Nature Neuroscience · doi:10.1038/nn.3762 · Cited by 80 · see citing works
Reschke, C. R., Silva, L. F. A., Norwood, B. A., Senthilkumar, K., Morris, G., Sanz‐Rodriguez, A., Conroy, R. M., Costard, L. S., Neubert, V., Bauer, S., et al. (2016) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2016.11.002 · Cited by 78 · see citing works
Long noncoding RNA GM12371 acts as a transcriptional regulator of synapse function
Raveendra, B., Swarnkar, S., Avchalumov, Y., Liu, X.-A., Grinman, E., Badal, K. K., Reich, A. M., Pascal, B. D., & Puthanveettil, S. V. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1722587115 · Cited by 74 · see citing works
Neurotransmitter Switching Regulated by miRNAs Controls Changes in Social Preference
Dulcis, D., Lippi, G., Stark, C. J., Do, L. H., Berg, D. K., & Spitzer, N. C. (2017) · Neuron · doi:10.1016/j.neuron.2017.08.023 · Cited by 67 · see citing works
Rehfeld, F., Maticzka, D., Grosser, S., Knauff, P., Eravci, M., Vida, I., Backofen, R., & Wulczyn, F. G. (2018) · Nature Communications · doi:10.1038/s41467-018-03681-3 · Cited by 67 · see citing works
Thomas, K. T., Anderson, B. R., Shah, N., Zimmer, S. E., Hawkins, D., Valdez‐Sinon, A. N., Gu, Q., & Bassell, G. J. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.06.038 · Cited by 57 · see citing works
MicroRNA‐92 modulates K(+) Cl(−) co‐transporter KCC2 expression in cerebellar granule neurons
Barbato, C., Ruberti, F., Pieri, M., Vilardo, E., Costanzo, M., Ciotti, M. T., Zona, C., & Cogoni, C. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06560.x · Cited by 44 · see citing works
MiR-980 Is a Memory Suppressor MicroRNA that Regulates the Autism-Susceptibility Gene A2bp1
Guven-Ozkan, T., Busto, G. U., Schutte, S. S., Cervantes-Sandoval, I., O’Dowd, D. K., & Davis, R. L. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.01.040 · Cited by 43 · see citing works
Koichiro, Tsujimura, K., Nakashima, H., & Nakashima, K. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.705749 · Cited by 43 · see citing works
miR-92 Suppresses Robo1 Translation to Modulate Slit Sensitivity in Commissural Axon Guidance
Yang, T., Huang, H., Shao, Q., Yee, S., Majumder, T., & Liu, G. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.08.021 · Cited by 40 · see citing works
Martinez-Moreno, M., O’Shea, T. M., Zepecki, J. P., Olaru, A., Ness, J. K., Langer, R., & Tapinos, N. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.07.068 · Cited by 37 · see citing works
A microRNA negative feedback loop downregulates vesicle transport and inhibits fear memory
Mathew, R. S., Tatarakis, A., Rudenko, A., Johnson‐Venkatesh, E., Yang, Y. J., Murphy, E. A., Todd, T. P., Schepers, S. T., Siuti, N., Martorell, A. J., et al. (2016) · eLife · doi:10.7554/elife.22467 · Cited by 36 · see citing works
A Rapid Induction Mechanism for Lin28a in Trophic Responses
Amen, A. M., Ruiz, C. R., Shi, J., Subramanian, M. P., Pham, D. L., & Meffert, M. K. (2017) · Molecular Cell · doi:10.1016/j.molcel.2016.12.025 · Cited by 32 · see citing works
Lisi, V., Singh, B., Giroux, M., Guzman, E., Painter, M. W., Cheng, Y., Huebner, E. A., Coppola, G., Costigan, M., Woolf, C. J., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.07.010 · Cited by 29 · see citing works
Zampa, F., Bicker, S., & Schratt, G. M. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00171 · Cited by 29 · see citing works
The dynamic recruitment of TRBP to neuronal membranes mediates dendritogenesis during development
Antoniou, A., Khudayberdiev, S., Idziak, A., Bicker, S., Jacob, R., & Schratt, G. M. (2017) · EMBO Reports · doi:10.15252/embr.201744853 · Cited by 27 · see citing works
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Single cell transcriptome profiling of the human alcohol-dependent brain
Brenner, E., Tiwari, G. R., Kapoor, M., Liu, Y., Brock, A., & Mayfield, R. D. (2020) · Human Molecular Genetics · doi:10.1093/hmg/ddaa038 · Cited by 118 · see citing works
Cao, D.-W., Liu, M., Duan, R., Tao, Y.-F., Zhou, J., Fang, W., Zhu, J., Niu, L., & Sun, J. (2019) · Acta Pharmacologica Sinica · doi:10.1038/s41401-019-0284-y · Cited by 102 · see citing works
Rahmani, A., Saleki, K., Javanmehr, N., Javad, K., Saadat, P., & Nouri, H. R. (2020) · Ageing Research Reviews · doi:10.1016/j.arr.2020.101106 · Cited by 97 · see citing works
MicroRNA-218 instructs proper assembly of hippocampal networks
Taylor, S. R., Kobayashi, M., Vilella, A., Tiwari, D., Zolboot, N., Du, J. X., Spencer, K. R., Hartzell, A. L., Girgiss, C. B. L., Abaci, Y. T., et al. (2023) · eLife · doi:10.7554/elife.82729 · Cited by 15 · see citing works
microRNA Deficiency in VIP+ Interneurons Leads to Cortical Circuit Dysfunction
Qiu, F., Mao, X., Liu, P., Wu, J., Zhang, Y., Sun, D., Zhu, Y., Gong, L., Shao, M., Fan, K., et al. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz236 · Cited by 15 · see citing works
MicroRNA mechanisms instructing Purkinje cell specification
Zolboot, N., Xiao, Y., Du, J. X., Ghanem, M. M., Choi, S. Y., Junn, M. J., Zampa, F., Huang, Z., MacRae, I. J., & Lippi, G. (2023) · Neuron · doi:10.1016/j.neuron.2025.03.009 · Cited by 13 · see citing works
Vof-16 knockout improves the recovery from hypoxic-ischemic brain damage of neonatal rats
Tan, Y., Du, R., Su, Z., Xue, L., Liu, J., Zhang, B.-L., Huang, S.-J., Li, L.-J., Xiyang, Y., & Xiong, L. (2020) · Brain Research · doi:10.1016/j.brainres.2020.147070 · Cited by 8 · see citing works
Exosomes and Exosomal microRNAs in Age-associated Stroke
Wang, X., Fu, C. H., Zhu, X., Liu, J., Gong, X., Pan, Q., & Ma, X. (2021) · Current Vascular Pharmacology · doi:10.2174/1570161119666210208202621 · Cited by 6 · see citing works
Transcriptomic Evidence Reveals the Dysfunctional Mechanism of Synaptic Plasticity Control in ASD
Kong, C., Bing, Z., Yang, L., Huang, Z., Wang, W.-X., & Grebogi, C. (2024) · Genes · doi:10.3390/genes16010011 · Cited by 7 · see citing works
Expanding the AtLAS of non-coding RNA functions in the brain
Regier, M., & Shepherd, J. D. (2020) · Cell Research · doi:10.1038/s41422-020-0289-6 · Cited by 3 · see citing works
Editorial overview: Molecular neuroscience
Ryan, T. A., & Jin, Y. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2019.06.002 · Cited by 3 · see citing works
RNA on Display: Cell Surface RNA as a Novel Layer of Cellular Regulation
Chahal, S., Jose, P., Greasley, A., Vytlingam, K., Thapa, R. K., Pyne, H., Omar, A. A., & Zheng, X. (2026) · Research · doi:10.34133/research.1147 · Cited by 1 · see citing works
Kong, C., Bing, Z., Yang, L., Huang, Z., & Wang, W.-X. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.12.25.573326 · Cited by 1 · see citing works
- Authors
- Zampa, F., Hartzell, A. L., Zolboot, N., & Lippi, G.
- Affiliations
- Scripps Research Institute (US)
- Corresponding author
- Lippi, Giordano
- Venue
- Current Opinion in Neurobiology
- Publisher
- Elsevier BV
- Published
- 2019-08
- Volume
- 57
- Pages
- 54-61
- ISSN
- 0959-4388 (ISSN-L)
- OpenAlex
- W2913175443
- Cited by
- 13
- References
- 51
- Citations by year
- 2026: 1 · 2024: 1 · 2023: 3 · 2021: 1 · 2020: 4 · 2019: 3
- FWCI
- 0.27
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Current Opinion in Neurobiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Whitehall Foundation (2018-12-55)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
- Keywords
- non-coding RNA, neuronal network activity, intrinsic excitability, synaptic transmission, ion channels, neurotransmitter receptors, synaptic proteins, neural circuit development, mental illness
- MeSH terms
- Nerve Net, Neurons, Signal Transduction, Neural Networks, Computer, RNA, Untranslated
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