MicroRNA-92 modulates K(+) Cl(-) co-transporter KCC2 expression in cerebellar granule neurons
J. Neurochem. (2010) 113, 591-600. MicroRNAs have been associated to fine-tuning spatial and temporal control of gene expression during neuronal development. The neuronal Cl(-) extruding, K(+)Cl(-) co-transporter 2 (KCC2) is known to play an important role in neuronal Cl(-) homeostasis and in determ...
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| creator | Barbato, Christian Ruberti, Francesca Pieri, Massimo Vilardo, Elisa Costanzo, Manuela Ciotti, Maria Teresa Zona, Cristina Cogoni, Carlo |
| description | J. Neurochem. (2010) 113, 591-600. MicroRNAs have been associated to fine-tuning spatial and temporal control of gene expression during neuronal development. The neuronal Cl(-) extruding, K(+)Cl(-) co-transporter 2 (KCC2) is known to play an important role in neuronal Cl(-) homeostasis and in determining the physiological response to activation of anion selective GABA receptors. Here we show that microRNA-92 is developmentally down-regulated during maturation of rat cerebellar granule neurons (CGNs) in vitro. Computational predictions suggest several high-ranking targets for microRNA-92 including the KCC2 gene. Consistently, the KCC2 protein levels were up-regulated in mature CGN in vitro and a functional association between microRNA-92 and KCC2 3′ untranslated region was established using luciferase assays. The generation of an inward directed Cl(-) electrochemical gradient, necessary for the hyperpolarizing effect of GABA, requires robust KCC2 expression in several neuronal types. Here we show that lentiviral-mediated microRNA-92 over-expression reduced KCC2 protein levels and positively shifted reversal potential of GABA induced Cl(-) currents in CGNs. In addition KCC2 re-expression reversed microRNA-92 electrophysiological phenotype. Consistently microRNA-92 inhibition induced both an increase of the level of KCC2 and a negative shift in GABA reversal potential. These findings introduce a new player in the developmental change of GABA from depolarization to hyperpolarization. |
| doi_str_mv | 10.1111/j.1471-4159.2009.06560.x |
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Neurochem. (2010) 113, 591-600. MicroRNAs have been associated to fine-tuning spatial and temporal control of gene expression during neuronal development. The neuronal Cl(-) extruding, K(+)Cl(-) co-transporter 2 (KCC2) is known to play an important role in neuronal Cl(-) homeostasis and in determining the physiological response to activation of anion selective GABA receptors. Here we show that microRNA-92 is developmentally down-regulated during maturation of rat cerebellar granule neurons (CGNs) in vitro. Computational predictions suggest several high-ranking targets for microRNA-92 including the KCC2 gene. Consistently, the KCC2 protein levels were up-regulated in mature CGN in vitro and a functional association between microRNA-92 and KCC2 3′ untranslated region was established using luciferase assays. The generation of an inward directed Cl(-) electrochemical gradient, necessary for the hyperpolarizing effect of GABA, requires robust KCC2 expression in several neuronal types. Here we show that lentiviral-mediated microRNA-92 over-expression reduced KCC2 protein levels and positively shifted reversal potential of GABA induced Cl(-) currents in CGNs. In addition KCC2 re-expression reversed microRNA-92 electrophysiological phenotype. Consistently microRNA-92 inhibition induced both an increase of the level of KCC2 and a negative shift in GABA reversal potential. These findings introduce a new player in the developmental change of GABA from depolarization to hyperpolarization.</description><identifier>ISSN: 0022-3042</identifier><identifier>EISSN: 1471-4159</identifier><identifier>DOI: 10.1111/j.1471-4159.2009.06560.x</identifier><identifier>PMID: 20050974</identifier><identifier>CODEN: JONRA9</identifier><language>eng</language><publisher>Oxford, UK: Oxford, UK : Blackwell Publishing Ltd</publisher><subject>3' Untranslated Regions - genetics ; Animals ; Biological and medical sciences ; Blotting, Northern ; Blotting, Western ; Cell physiology ; Cells, Cultured ; cerebellar granule neurons ; Cerebellum - cytology ; Cerebellum - growth & development ; Cerebellum - metabolism ; Cytoplasmic Granules - metabolism ; Degenerative and inherited degenerative diseases of the nervous system. Leukodystrophies. Prion diseases ; development ; Electrophysiology ; Fundamental and applied biological sciences. Psychology ; GABA ; gamma-Aminobutyric Acid - physiology ; Gene expression ; Gene Expression Regulation - physiology ; Genes, Reporter - genetics ; Genetic Vectors ; Genotype & phenotype ; K Cl- Cotransporters ; KCC2 ; Lentivirus - genetics ; Luciferases - genetics ; Medical sciences ; Membrane and intracellular transports ; microRNA ; MicroRNAs - antagonists & inhibitors ; MicroRNAs - pharmacology ; Molecular and cellular biology ; Neurochemistry ; Neurology ; Neurons ; Neurons - drug effects ; Neurons - metabolism ; Patch-Clamp Techniques ; Rats ; Rats, Wistar ; Ribonucleic acid ; RNA ; Signal transduction ; Symporters - antagonists & inhibitors ; Symporters - biosynthesis</subject><ispartof>Journal of neurochemistry, 2010-05, Vol.113 (3), p.591-600</ispartof><rights>2010 The Authors. Journal Compilation © 2010 International Society for Neurochemistry</rights><rights>2015 INIST-CNRS</rights><rights>Journal compilation © 2010 International Society for Neurochemistry</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5970-3946adcee49354766f0f926f59033f79339788b193bf6330e37f4f0f95cb802a3</citedby><cites>FETCH-LOGICAL-c5970-3946adcee49354766f0f926f59033f79339788b193bf6330e37f4f0f95cb802a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fj.1471-4159.2009.06560.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fj.1471-4159.2009.06560.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=22728121$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20050974$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Barbato, Christian</creatorcontrib><creatorcontrib>Ruberti, Francesca</creatorcontrib><creatorcontrib>Pieri, Massimo</creatorcontrib><creatorcontrib>Vilardo, Elisa</creatorcontrib><creatorcontrib>Costanzo, Manuela</creatorcontrib><creatorcontrib>Ciotti, Maria Teresa</creatorcontrib><creatorcontrib>Zona, Cristina</creatorcontrib><creatorcontrib>Cogoni, Carlo</creatorcontrib><title>MicroRNA-92 modulates K(+) Cl(-) co-transporter KCC2 expression in cerebellar granule neurons</title><title>Journal of neurochemistry</title><addtitle>J Neurochem</addtitle><description>J. Neurochem. (2010) 113, 591-600. MicroRNAs have been associated to fine-tuning spatial and temporal control of gene expression during neuronal development. The neuronal Cl(-) extruding, K(+)Cl(-) co-transporter 2 (KCC2) is known to play an important role in neuronal Cl(-) homeostasis and in determining the physiological response to activation of anion selective GABA receptors. Here we show that microRNA-92 is developmentally down-regulated during maturation of rat cerebellar granule neurons (CGNs) in vitro. Computational predictions suggest several high-ranking targets for microRNA-92 including the KCC2 gene. Consistently, the KCC2 protein levels were up-regulated in mature CGN in vitro and a functional association between microRNA-92 and KCC2 3′ untranslated region was established using luciferase assays. The generation of an inward directed Cl(-) electrochemical gradient, necessary for the hyperpolarizing effect of GABA, requires robust KCC2 expression in several neuronal types. Here we show that lentiviral-mediated microRNA-92 over-expression reduced KCC2 protein levels and positively shifted reversal potential of GABA induced Cl(-) currents in CGNs. In addition KCC2 re-expression reversed microRNA-92 electrophysiological phenotype. Consistently microRNA-92 inhibition induced both an increase of the level of KCC2 and a negative shift in GABA reversal potential. These findings introduce a new player in the developmental change of GABA from depolarization to hyperpolarization.</description><subject>3' Untranslated Regions - genetics</subject><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Blotting, Northern</subject><subject>Blotting, Western</subject><subject>Cell physiology</subject><subject>Cells, Cultured</subject><subject>cerebellar granule neurons</subject><subject>Cerebellum - cytology</subject><subject>Cerebellum - growth & development</subject><subject>Cerebellum - metabolism</subject><subject>Cytoplasmic Granules - metabolism</subject><subject>Degenerative and inherited degenerative diseases of the nervous system. Leukodystrophies. Prion diseases</subject><subject>development</subject><subject>Electrophysiology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>GABA</subject><subject>gamma-Aminobutyric Acid - physiology</subject><subject>Gene expression</subject><subject>Gene Expression Regulation - physiology</subject><subject>Genes, Reporter - genetics</subject><subject>Genetic Vectors</subject><subject>Genotype & phenotype</subject><subject>K Cl- Cotransporters</subject><subject>KCC2</subject><subject>Lentivirus - genetics</subject><subject>Luciferases - genetics</subject><subject>Medical sciences</subject><subject>Membrane and intracellular transports</subject><subject>microRNA</subject><subject>MicroRNAs - antagonists & inhibitors</subject><subject>MicroRNAs - pharmacology</subject><subject>Molecular and cellular biology</subject><subject>Neurochemistry</subject><subject>Neurology</subject><subject>Neurons</subject><subject>Neurons - drug effects</subject><subject>Neurons - metabolism</subject><subject>Patch-Clamp Techniques</subject><subject>Rats</subject><subject>Rats, Wistar</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Signal transduction</subject><subject>Symporters - antagonists & inhibitors</subject><subject>Symporters - biosynthesis</subject><issn>0022-3042</issn><issn>1471-4159</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkV1rFDEUhoModq3-BQ2C2CIznnxMPi68KIOfrRXUXkrIZJMyy-xkTXZw--_NuGsFbzQ3CZznPefkfRHCBGpSzstVTbgkFSeNrimArkE0AurdHbS4LdxFCwBKKwacHqEHOa8AiOCC3EdHRdOAlnyBvn3sXYqfL88qTfE6LqfBbn3G5ycvTnE7nFSn2MVqm-yYNzFtfcLnbUux322Sz7mPI-5H7HzynR8Gm_B1IafB49FPKY75IboX7JD9o8N9jK7evP7avqsuPr19355dVK7REiqmubBL5z3XrOFSiABBUxEaDYwFqRnTUqmOaNYFwRh4JgOfmcZ1Cqhlx-j5vu8mxe-Tz1uz7rObVxp9nLKRvMxRgqt_k4w1mkMjC_n0L3IVpzSWbxha7CZKAS-Q2kPFxJyTD2aT-rVNN4aAmaMyKzMnYuZEzByV-RWV2RXp40P_qVv75a3wdzYFeHYAbHZ2CMVa1-c_HJVUEUoK92rP_egHf_PfC5gPl-38Kvone32w0djrVGZcfaFAGBBFuVCM_QR28LPf</recordid><startdate>201005</startdate><enddate>201005</enddate><creator>Barbato, Christian</creator><creator>Ruberti, Francesca</creator><creator>Pieri, Massimo</creator><creator>Vilardo, Elisa</creator><creator>Costanzo, Manuela</creator><creator>Ciotti, Maria Teresa</creator><creator>Zona, Cristina</creator><creator>Cogoni, Carlo</creator><general>Oxford, UK : Blackwell Publishing Ltd</general><general>Blackwell Publishing Ltd</general><general>Wiley-Blackwell</general><scope>FBQ</scope><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>P64</scope><scope>7X8</scope><scope>7TM</scope></search><sort><creationdate>201005</creationdate><title>MicroRNA-92 modulates K(+) Cl(-) co-transporter KCC2 expression in cerebellar granule neurons</title><author>Barbato, Christian ; Ruberti, Francesca ; Pieri, Massimo ; Vilardo, Elisa ; Costanzo, Manuela ; Ciotti, Maria Teresa ; Zona, Cristina ; Cogoni, Carlo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5970-3946adcee49354766f0f926f59033f79339788b193bf6330e37f4f0f95cb802a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>3' Untranslated Regions - genetics</topic><topic>Animals</topic><topic>Biological and medical sciences</topic><topic>Blotting, Northern</topic><topic>Blotting, Western</topic><topic>Cell physiology</topic><topic>Cells, Cultured</topic><topic>cerebellar granule neurons</topic><topic>Cerebellum - cytology</topic><topic>Cerebellum - growth & development</topic><topic>Cerebellum - metabolism</topic><topic>Cytoplasmic Granules - metabolism</topic><topic>Degenerative and inherited degenerative diseases of the nervous system. Leukodystrophies. Prion diseases</topic><topic>development</topic><topic>Electrophysiology</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>GABA</topic><topic>gamma-Aminobutyric Acid - physiology</topic><topic>Gene expression</topic><topic>Gene Expression Regulation - physiology</topic><topic>Genes, Reporter - genetics</topic><topic>Genetic Vectors</topic><topic>Genotype & phenotype</topic><topic>K Cl- Cotransporters</topic><topic>KCC2</topic><topic>Lentivirus - genetics</topic><topic>Luciferases - genetics</topic><topic>Medical sciences</topic><topic>Membrane and intracellular transports</topic><topic>microRNA</topic><topic>MicroRNAs - antagonists & inhibitors</topic><topic>MicroRNAs - pharmacology</topic><topic>Molecular and cellular biology</topic><topic>Neurochemistry</topic><topic>Neurology</topic><topic>Neurons</topic><topic>Neurons - drug effects</topic><topic>Neurons - metabolism</topic><topic>Patch-Clamp Techniques</topic><topic>Rats</topic><topic>Rats, Wistar</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>Signal transduction</topic><topic>Symporters - antagonists & inhibitors</topic><topic>Symporters - biosynthesis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Barbato, Christian</creatorcontrib><creatorcontrib>Ruberti, Francesca</creatorcontrib><creatorcontrib>Pieri, Massimo</creatorcontrib><creatorcontrib>Vilardo, Elisa</creatorcontrib><creatorcontrib>Costanzo, Manuela</creatorcontrib><creatorcontrib>Ciotti, Maria Teresa</creatorcontrib><creatorcontrib>Zona, Cristina</creatorcontrib><creatorcontrib>Cogoni, Carlo</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Nucleic Acids Abstracts</collection><jtitle>Journal of neurochemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Barbato, Christian</au><au>Ruberti, Francesca</au><au>Pieri, Massimo</au><au>Vilardo, Elisa</au><au>Costanzo, Manuela</au><au>Ciotti, Maria Teresa</au><au>Zona, Cristina</au><au>Cogoni, Carlo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>MicroRNA-92 modulates K(+) Cl(-) co-transporter KCC2 expression in cerebellar granule neurons</atitle><jtitle>Journal of neurochemistry</jtitle><addtitle>J Neurochem</addtitle><date>2010-05</date><risdate>2010</risdate><volume>113</volume><issue>3</issue><spage>591</spage><epage>600</epage><pages>591-600</pages><issn>0022-3042</issn><eissn>1471-4159</eissn><coden>JONRA9</coden><abstract>J. Neurochem. (2010) 113, 591-600. MicroRNAs have been associated to fine-tuning spatial and temporal control of gene expression during neuronal development. The neuronal Cl(-) extruding, K(+)Cl(-) co-transporter 2 (KCC2) is known to play an important role in neuronal Cl(-) homeostasis and in determining the physiological response to activation of anion selective GABA receptors. Here we show that microRNA-92 is developmentally down-regulated during maturation of rat cerebellar granule neurons (CGNs) in vitro. Computational predictions suggest several high-ranking targets for microRNA-92 including the KCC2 gene. Consistently, the KCC2 protein levels were up-regulated in mature CGN in vitro and a functional association between microRNA-92 and KCC2 3′ untranslated region was established using luciferase assays. The generation of an inward directed Cl(-) electrochemical gradient, necessary for the hyperpolarizing effect of GABA, requires robust KCC2 expression in several neuronal types. Here we show that lentiviral-mediated microRNA-92 over-expression reduced KCC2 protein levels and positively shifted reversal potential of GABA induced Cl(-) currents in CGNs. In addition KCC2 re-expression reversed microRNA-92 electrophysiological phenotype. Consistently microRNA-92 inhibition induced both an increase of the level of KCC2 and a negative shift in GABA reversal potential. These findings introduce a new player in the developmental change of GABA from depolarization to hyperpolarization.</abstract><cop>Oxford, UK</cop><pub>Oxford, UK : Blackwell Publishing Ltd</pub><pmid>20050974</pmid><doi>10.1111/j.1471-4159.2009.06560.x</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | 3' Untranslated Regions - genetics Animals Biological and medical sciences Blotting, Northern Blotting, Western Cell physiology Cells, Cultured cerebellar granule neurons Cerebellum - cytology Cerebellum - growth & development Cerebellum - metabolism Cytoplasmic Granules - metabolism Degenerative and inherited degenerative diseases of the nervous system. Leukodystrophies. Prion diseases development Electrophysiology Fundamental and applied biological sciences. Psychology GABA gamma-Aminobutyric Acid - physiology Gene expression Gene Expression Regulation - physiology Genes, Reporter - genetics Genetic Vectors Genotype & phenotype K Cl- Cotransporters KCC2 Lentivirus - genetics Luciferases - genetics Medical sciences Membrane and intracellular transports microRNA MicroRNAs - antagonists & inhibitors MicroRNAs - pharmacology Molecular and cellular biology Neurochemistry Neurology Neurons Neurons - drug effects Neurons - metabolism Patch-Clamp Techniques Rats Rats, Wistar Ribonucleic acid RNA Signal transduction Symporters - antagonists & inhibitors Symporters - biosynthesis |
| title | MicroRNA-92 modulates K(+) Cl(-) co-transporter KCC2 expression in cerebellar granule neurons |
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