MicroRNA-934 is a novel primate-specific small non-coding RNA with neurogenic function during early development

Integrating differential RNA and miRNA expression during neuronal lineage induction of human embryonic stem cells we identified miR-934, a primate-specific miRNA that displays a stage-specific expression pattern during progenitor expansion and early neuron generation. We demonstrate the biological r...

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Main Authors: Kanella Prodromidou, Ioannis S Vlachos, Maria Gaitanou, Georgia Kouroupi, Artemis G Hatzigeorgiou, Rebecca Matsas
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/50561
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author Kanella Prodromidou
Ioannis S Vlachos
Maria Gaitanou
Georgia Kouroupi
Artemis G Hatzigeorgiou
Rebecca Matsas
author_facet Kanella Prodromidou
Ioannis S Vlachos
Maria Gaitanou
Georgia Kouroupi
Artemis G Hatzigeorgiou
Rebecca Matsas
author_sort Kanella Prodromidou
collection DOAJ
description Integrating differential RNA and miRNA expression during neuronal lineage induction of human embryonic stem cells we identified miR-934, a primate-specific miRNA that displays a stage-specific expression pattern during progenitor expansion and early neuron generation. We demonstrate the biological relevance of this finding by comparison with data from early to mid-gestation human cortical tissue. Further we find that miR-934 directly controls progenitor to neuroblast transition and impacts on neurite growth of newborn neurons. In agreement, miR-934 targets are involved in progenitor proliferation and neuronal differentiation whilst miR-934 inhibition results in profound global transcriptome changes associated with neurogenesis, axonogenesis, neuronal migration and neurotransmission. Interestingly, miR-934 inhibition affects the expression of genes associated with the subplate zone, a transient compartment most prominent in primates that emerges during early corticogenesis. Our data suggest that mir-934 is a novel regulator of early human neurogenesis with potential implications for a species-specific evolutionary role in brain function.
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spelling doaj.art-74d31c8439434485ac522ecb044ead932022-12-22T03:52:55ZengeLife Sciences Publications LtdeLife2050-084X2020-05-01910.7554/eLife.50561MicroRNA-934 is a novel primate-specific small non-coding RNA with neurogenic function during early developmentKanella Prodromidou0https://orcid.org/0000-0001-5721-9124Ioannis S Vlachos1Maria Gaitanou2Georgia Kouroupi3Artemis G Hatzigeorgiou4Rebecca Matsas5https://orcid.org/0000-0002-4027-348XLaboratory of Cellular and Molecular Neurobiology-Stem Cells, Department of Neurobiology, Hellenic Pasteur Institute, Athens, GreeceDepartment of Pathology, Beth Israel Deaconess Medical Center, Boston, United States; DIANA-Lab, Hellenic Pasteur Institute, Athens, Greece; Harvard Medical School, Boston, United States; Broad Institute of MIT and Harvard, Cambridge, United StatesLaboratory of Cellular and Molecular Neurobiology-Stem Cells, Department of Neurobiology, Hellenic Pasteur Institute, Athens, GreeceLaboratory of Cellular and Molecular Neurobiology-Stem Cells, Department of Neurobiology, Hellenic Pasteur Institute, Athens, GreeceDIANA-Lab, Hellenic Pasteur Institute, Athens, GreeceLaboratory of Cellular and Molecular Neurobiology-Stem Cells, Department of Neurobiology, Hellenic Pasteur Institute, Athens, GreeceIntegrating differential RNA and miRNA expression during neuronal lineage induction of human embryonic stem cells we identified miR-934, a primate-specific miRNA that displays a stage-specific expression pattern during progenitor expansion and early neuron generation. We demonstrate the biological relevance of this finding by comparison with data from early to mid-gestation human cortical tissue. Further we find that miR-934 directly controls progenitor to neuroblast transition and impacts on neurite growth of newborn neurons. In agreement, miR-934 targets are involved in progenitor proliferation and neuronal differentiation whilst miR-934 inhibition results in profound global transcriptome changes associated with neurogenesis, axonogenesis, neuronal migration and neurotransmission. Interestingly, miR-934 inhibition affects the expression of genes associated with the subplate zone, a transient compartment most prominent in primates that emerges during early corticogenesis. Our data suggest that mir-934 is a novel regulator of early human neurogenesis with potential implications for a species-specific evolutionary role in brain function.https://elifesciences.org/articles/50561early neuronsneuritogenesisPAX6doublecortinprogenitor cellneural induction
spellingShingle Kanella Prodromidou
Ioannis S Vlachos
Maria Gaitanou
Georgia Kouroupi
Artemis G Hatzigeorgiou
Rebecca Matsas
MicroRNA-934 is a novel primate-specific small non-coding RNA with neurogenic function during early development
eLife
early neurons
neuritogenesis
PAX6
doublecortin
progenitor cell
neural induction
title MicroRNA-934 is a novel primate-specific small non-coding RNA with neurogenic function during early development
title_full MicroRNA-934 is a novel primate-specific small non-coding RNA with neurogenic function during early development
title_fullStr MicroRNA-934 is a novel primate-specific small non-coding RNA with neurogenic function during early development
title_full_unstemmed MicroRNA-934 is a novel primate-specific small non-coding RNA with neurogenic function during early development
title_short MicroRNA-934 is a novel primate-specific small non-coding RNA with neurogenic function during early development
title_sort microrna 934 is a novel primate specific small non coding rna with neurogenic function during early development
topic early neurons
neuritogenesis
PAX6
doublecortin
progenitor cell
neural induction
url https://elifesciences.org/articles/50561
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AT mariagaitanou microrna934isanovelprimatespecificsmallnoncodingrnawithneurogenicfunctionduringearlydevelopment
AT georgiakouroupi microrna934isanovelprimatespecificsmallnoncodingrnawithneurogenicfunctionduringearlydevelopment
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