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

  1. Kanella Prodromidou  Is a corresponding author
  2. Ioannis S Vlachos
  3. Maria Gaitanou
  4. Georgia Kouroupi
  5. Artemis G Hatzigeorgiou
  6. Rebecca Matsas  Is a corresponding author
  1. Hellenic Pasteur Institute, Greece
  2. Beth Israel Deaconess Medical Center, United States
  3. DIANA-Lab, University of Thessaly, Greece
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Cite this article as: eLife 2020;9:e50561 doi: 10.7554/eLife.50561

Abstract

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.

Data availability

Sequencing data have been deposited in GEO under accession code GSE101548. All data generated or analysed during this study are included in the manuscript and supporting files.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Kanella Prodromidou

    Neurobiology, Hellenic Pasteur Institute, Athens, Greece
    For correspondence
    kprodromidou@pasteur.gr
    Competing interests
    The authors declare that no competing interests exist.

  2. Ioannis S Vlachos

    Pathology, Beth Israel Deaconess Medical Center, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Maria Gaitanou

    Neurobiology, Hellenic Pasteur Institute, Athens, Greece
    Competing interests
    The authors declare that no competing interests exist.

  4. Georgia Kouroupi

    Neurobiology, Hellenic Pasteur Institute, Athens, Greece
    Competing interests
    The authors declare that no competing interests exist.

  5. Artemis G Hatzigeorgiou

    Department of Electrical & Computer Engineering, DIANA-Lab, University of Thessaly, Volos, Greece
    Competing interests
    The authors declare that no competing interests exist.

  6. Rebecca Matsas

    Neurobiology, Hellenic Pasteur Institute, Athens, Greece
    For correspondence
    rmatsa@pasteur.gr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4027-348X

Funding

Ministry of Education and Religious Affairs, Sport and Culture (Greek General Secreteriat for Research and Technology Grant EXCELLENCE 2272)

  • Rebecca Matsas

Ministry of Education and Religious Affairs, Sport and Culture (Greek General Secreteriat for Research and Technology Grant MIS 5002486)

  • Rebecca Matsas

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: All procedures for generation of human iPSCs were approved by the Scientific Council and Ethics Committee of Attikon University Hospital (Athens, Greece), which is one of the Mendelian forms of Parkinson's Disease clinical centers, and by the Hellenic Pasteur Institute Ethics Committee overlooking stem cell research. Informed consent was obtained from all donors before skin biopsy. Proc Natl Acad Sci U S A. 2017 May 2;114(18)

Reviewing Editor

  1. Marianne E Bronner, California Institute of Technology, United States

Publication history

  1. Received: July 26, 2019
  2. Accepted: May 21, 2020
  3. Accepted Manuscript published: May 27, 2020 (version 1)
  4. Version of Record published: June 15, 2020 (version 2)

Copyright

© 2020, Prodromidou et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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