A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis

Siegel G, Obernosterer G, Fiore R, Oehmen M, Bicker S, Christensen M, Khudayberdiev S, Leuschner PF, Busch CJL, Kane C, Huebel K, et al. (2009)
NATURE CELL BIOLOGY 11(6): 705-716.

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Abstract / Bemerkung
The microRNA pathway has been implicated in the regulation of synaptic protein synthesis and ultimately in dendritic spine morphogenesis, a phenomenon associated with long-lasting forms of memory. However, the particular microRNAs (miRNAs) involved are largely unknown. Here we identify specific miRNAs that function at synapses to control dendritic spine structure by performing a functional screen. One of the identified miRNAs, miR-138, is highly enriched in the brain, localized within dendrites and negatively regulates the size of dendritic spines in rat hippocampal neurons. miR-138 controls the expression of acyl protein thioesterase 1 (APT1), an enzyme regulating the palmitoylation status of proteins that are known to function at the synapse, including the alpha(13) subunits of G proteins (G alpha(13)). RNA-interference-mediated knockdown of APT1 and the expression of membrane-localized G alpha(13) both suppress spine enlargement caused by inhibition of miR-138, suggesting that APT1-regulated depalmitoylation of G alpha(13) might be an important downstream event of miR-138 function. Our results uncover a previously unknown miRNA-dependent mechanism in neurons and demonstrate a previously unrecognized complexity of miRNA-dependent control of dendritic spine morphogenesis.
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NATURE CELL BIOLOGY
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11
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6
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705-716
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Siegel G, Obernosterer G, Fiore R, et al. A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. NATURE CELL BIOLOGY. 2009;11(6):705-716.
Siegel, G., Obernosterer, G., Fiore, R., Oehmen, M., Bicker, S., Christensen, M., Khudayberdiev, S., et al. (2009). A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. NATURE CELL BIOLOGY, 11(6), 705-716. doi:10.1038/ncb1876
Siegel, G., Obernosterer, G., Fiore, R., Oehmen, M., Bicker, S., Christensen, M., Khudayberdiev, S., Leuschner, P. F., Busch, C. J. L., Kane, C., et al. (2009). A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. NATURE CELL BIOLOGY 11, 705-716.
Siegel, G., et al., 2009. A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. NATURE CELL BIOLOGY, 11(6), p 705-716.
G. Siegel, et al., “A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis”, NATURE CELL BIOLOGY, vol. 11, 2009, pp. 705-716.
Siegel, G., Obernosterer, G., Fiore, R., Oehmen, M., Bicker, S., Christensen, M., Khudayberdiev, S., Leuschner, P.F., Busch, C.J.L., Kane, C., Huebel, K., Dekker, F., Hedberg, C., Rengarajan, B., Drepper, C., Waldmann, H., Kauppinen, S., Greenberg, M.E., Draguhn, A., Rehmsmeier, M., Martinez, J., Schratt, G.M.: A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. NATURE CELL BIOLOGY. 11, 705-716 (2009).
Siegel, Gabriele, Obernosterer, Gregor, Fiore, Roberto, Oehmen, Martin, Bicker, Silvia, Christensen, Mette, Khudayberdiev, Sharof, Leuschner, Philipp F., Busch, Clara J. L., Kane, Christina, Huebel, Katja, Dekker, Frank, Hedberg, Christian, Rengarajan, Balamurugan, Drepper, Carsten, Waldmann, Herbert, Kauppinen, Sakari, Greenberg, Michael E., Draguhn, Andreas, Rehmsmeier, Marc, Martinez, Javier, and Schratt, Gerhard M. “A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis”. NATURE CELL BIOLOGY 11.6 (2009): 705-716.

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miR-124-regulated RhoG: A conductor of neuronal process complexity.
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MicroRNA-182 regulates amygdala-dependent memory formation.
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Role of microRNA-138 as a potential tumor suppressor in head and neck squamous cell carcinoma.
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Regulation of microRNA biogenesis and turnover by animals and their viruses.
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Context-specific microRNA function in developmental complexity.
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Comparison of microRNA expression in hippocampus and the marginal division (MrD) of the neostriatum in rats.
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microRNAs and the regulation of neuronal plasticity under stress conditions.
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Short-term recognition memory correlates with regional CNS expression of microRNA-138 in mice.
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Cardiotoxicity of mycotoxin citrinin and involvement of microRNA-138 in zebrafish embryos.
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Developmental and activity-dependent miRNA expression profiling in primary hippocampal neuron cultures.
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MicroRNAs in the pathophysiology and treatment of status epilepticus.
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A comprehensive characterization of the nuclear microRNA repertoire of post-mitotic neurons.
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Structural modulation of dendritic spines during synaptic plasticity.
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Differentiation of single cell derived human mesenchymal stem cells into cells with a neuronal phenotype: RNA and microRNA expression profile.
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MicroRNA networks direct neuronal development and plasticity.
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Inherited and de novo SHANK2 variants associated with autism spectrum disorder impair neuronal morphogenesis and physiology.
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Targeting microRNAs in neurons: tools and perspectives.
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Dopamine-regulated microRNA MiR-181a controls GluA2 surface expression in hippocampal neurons.
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Putting proteins in their place: palmitoylation in Huntington disease and other neuropsychiatric diseases.
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Expression profiling of synaptic microRNAs from the adult rat brain identifies regional differences and seizure-induced dynamic modulation.
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Post-transcriptional trafficking and regulation of neuronal gene expression.
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Regulation of the actin cytoskeleton in dendritic spines.
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G protein trafficking.
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Targeting protein lipidation in disease.
Resh MD., Trends Mol Med 18(4), 2012
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HuR protein attenuates miRNA-mediated repression by promoting miRISC dissociation from the target RNA.
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Non-coding RNAs--novel targets in neurotoxicity.
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MicroRNA dysregulation in neuropsychiatric disorders and cognitive dysfunction.
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Emerging role of neuronal exosomes in the central nervous system.
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Global Approaches to the Role of miRNAs in Drug-Induced Changes in Gene Expression.
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The Emerging Role of Non-Coding RNAs in Drug Addiction.
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Neurofibromin 1 is a miRNA target in neurons.
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Protein palmitoylation and pathogenesis in apicomplexan parasites.
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Neurodegeneration as an RNA disorder.
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Genetic correction of human induced pluripotent stem cells from patients with spinal muscular atrophy.
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MicroRNA expression changes during zebrafish development induced by perfluorooctane sulfonate.
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Identification and experimental validation of G protein alpha inhibiting activity polypeptide 2 (GNAI2) as a microRNA-138 target in tongue squamous cell carcinoma.
Jiang L, Dai Y, Liu X, Wang C, Wang A, Chen Z, Heidbreder CE, Kolokythas A, Zhou X., Hum Genet 129(2), 2011
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Human microRNAs miR-22, miR-138-2, miR-148a, and miR-488 are associated with panic disorder and regulate several anxiety candidate genes and related pathways.
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Dynamic palmitoylation and the role of DHHC proteins in T cell activation and anergy.
Ladygina N, Martin BR, Altman A., Adv Immunol 109(), 2011
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Ageing, neuronal connectivity and brain disorders: an unsolved ripple effect.
Bano D, Agostini M, Melino G, Nicotera P., Mol Neurobiol 43(2), 2011
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MicroRNA in central nervous system trauma and degenerative disorders.
Liu NK, Xu XM., Physiol Genomics 43(10), 2011
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MicroRNAs in addiction: adaptation's middlemen?
Li MD, van der Vaart AD., Mol Psychiatry 16(12), 2011
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Reversible inhibition of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling.
Muddashetty RS, Nalavadi VC, Gross C, Yao X, Xing L, Laur O, Warren ST, Bassell GJ., Mol Cell 42(5), 2011
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Up-regulation of microRNAs in brain of human alcoholics.
Lewohl JM, Nunez YO, Dodd PR, Tiwari GR, Harris RA, Mayfield RD., Alcohol Clin Exp Res 35(11), 2011
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MicroRNA-138 modulates DNA damage response by repressing histone H2AX expression.
Wang Y, Huang JW, Li M, Cavenee WK, Mitchell PS, Zhou X, Tewari M, Furnari FB, Taniguchi T., Mol Cancer Res 9(8), 2011
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microRNA-Seq reveals cocaine-regulated expression of striatal microRNAs.
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A study of neural-related microRNAs in the developing amphioxus.
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Review of MicroRNA Deregulation in Oral Cancer. Part I.
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The microRNA contribution to learning and memory.
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Understanding the functional significance of ghrelin processing and degradation.
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Axotomy-induced miR-21 promotes axon growth in adult dorsal root ganglion neurons.
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miR-124a is required for hippocampal axogenesis and retinal cone survival through Lhx2 suppression.
Sanuki R, Onishi A, Koike C, Muramatsu R, Watanabe S, Muranishi Y, Irie S, Uneo S, Koyasu T, Matsui R, Chérasse Y, Urade Y, Watanabe D, Kondo M, Yamashita T, Furukawa T., Nat Neurosci 14(9), 2011
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Targeting of the Arpc3 actin nucleation factor by miR-29a/b regulates dendritic spine morphology.
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NMDA mediated contextual conditioning changes miRNA expression.
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microRNA-34c is a novel target to treat dementias.
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., EMBO J 30(20), 2011
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miRNA Expression profile after status epilepticus and hippocampal neuroprotection by targeting miR-132.
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Abnormal microRNA expression in Ts65Dn hippocampus and whole blood: contributions to Down syndrome phenotypes.
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MicroRNA-138 suppresses epithelial-mesenchymal transition in squamous cell carcinoma cell lines.
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MicroRNAs in neural cell development and brain diseases.
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Defining larger roles for "tiny" RNA molecules: role of miRNAs in neurodegeneration research.
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Regulation of spine and synapse formation by activity-dependent intracellular signaling pathways.
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miR-138 might reverse multidrug resistance of leukemia cells.
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Subcellular targeting strategies for drug design and delivery.
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Spatially restricting gene expression by local translation at synapses.
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Understanding neuronal connectivity through the post-transcriptional toolkit.
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Genome-wide dissection of microRNA functions and cotargeting networks using gene set signatures.
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MicroRNAs in neuronal development, function and dysfunction.
Saba R, Schratt GM., Brain Res 1338(), 2010
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Mechanisms of translational regulation in synaptic plasticity.
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MicroRNA pathways in neural development and plasticity.
Vo NK, Cambronne XA, Goodman RH., Curr Opin Neurobiol 20(4), 2010
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MicroRNA miR-137 regulates neuronal maturation by targeting ubiquitin ligase mind bomb-1.
Smrt RD, Szulwach KE, Pfeiffer RL, Li X, Guo W, Pathania M, Teng ZQ, Luo Y, Peng J, Bordey A, Jin P, Zhao X., Stem Cells 28(6), 2010
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Identification and quantitative analyses of microRNAs located in the distal axons of sympathetic neurons.
Natera-Naranjo O, Aschrafi A, Gioio AE, Kaplan BB., RNA 16(8), 2010
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miRNA malfunction causes spinal motor neuron disease.
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The widespread regulation of microRNA biogenesis, function and decay.
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