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LncRNAs interacting with the translation machinery contribute to human neuronal differentiation

View ORCID ProfileKaterina Douka, View ORCID ProfileIsabel Birds, View ORCID ProfileDapeng Wang, Sophie Clayton, Abigail Byford, View ORCID ProfileElton J. R. Vasconcelos, View ORCID ProfileMary J. O’Connell, View ORCID ProfileJim Deuchars, View ORCID ProfileAdrian Whitehouse, View ORCID ProfileJulie L. Aspden
doi: https://doi.org/10.1101/2020.10.01.321919
Katerina Douka
1School of Molecular and Cellular Biology, Faculty of Biological Sciences, University of Leeds, LS2 9JT, UK
2LeedsOmics, University of Leeds, UK
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Isabel Birds
1School of Molecular and Cellular Biology, Faculty of Biological Sciences, University of Leeds, LS2 9JT, UK
2LeedsOmics, University of Leeds, UK
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Dapeng Wang
2LeedsOmics, University of Leeds, UK
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Sophie Clayton
1School of Molecular and Cellular Biology, Faculty of Biological Sciences, University of Leeds, LS2 9JT, UK
3School of Biomedical Sciences, Faculty of Biological Sciences, University of Leeds, LS2 9JT, UK
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Abigail Byford
1School of Molecular and Cellular Biology, Faculty of Biological Sciences, University of Leeds, LS2 9JT, UK
3School of Biomedical Sciences, Faculty of Biological Sciences, University of Leeds, LS2 9JT, UK
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Elton J. R. Vasconcelos
2LeedsOmics, University of Leeds, UK
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Mary J. O’Connell
5School of Life Sciences, Faculty of Medicine and Health Sciences, The University of Nottingham, Nottingham, NG7 2UH, UK
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Jim Deuchars
2LeedsOmics, University of Leeds, UK
3School of Biomedical Sciences, Faculty of Biological Sciences, University of Leeds, LS2 9JT, UK
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Adrian Whitehouse
1School of Molecular and Cellular Biology, Faculty of Biological Sciences, University of Leeds, LS2 9JT, UK
2LeedsOmics, University of Leeds, UK
4Astbury Centre for Structural Molecular Biology, University of Leeds, Leeds, LS2 9JT, UK
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Julie L. Aspden
1School of Molecular and Cellular Biology, Faculty of Biological Sciences, University of Leeds, LS2 9JT, UK
2LeedsOmics, University of Leeds, UK
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  • For correspondence: j.aspden@leeds.ac.uk
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Abstract

LncRNAs are less conserved, yet more tissue and developmental-stage specific than mRNAs and are particularly enriched in the nervous system of Drosophila melanogaster, mouse and human. The function of cytoplasmic lncRNAs and their potential translation remains poorly understood. Here we performed Poly-Ribo-Seq to understand the interaction of lncRNAs with the translation machinery and the functional consequences during neuronal differentiation of SH-SH5Y cells. We discovered 237 cytoplasmic lncRNAs upregulated during early neuronal differentiation, most of which are associated with polysome complexes. The majority are cytoplasmically enriched and are intergenic or anti-sense. In addition, we find 45 small ORFs in lncRNAs to be actively translated, 17 specifically upon differentiation. 11 of these smORFs exhibit high sequence conservation across Hominidae suggesting they are under strong selective constraint with putative function in this clade. We discover LINC01116 is induced upon differentiation and contains an 87 codon smORF, which we detect as translated, with increased ribosome profiling signal upon differentiation. The LINC01116 peptide exhibits a cytoplasmic distribution and is detected in neurites. Knockdown of LINC01116 results in significant reduction of neurite length in differentiated cells indicating it contributes to neuronal differentiation. Our findings indicate lncRNAs are a source of non-canonical peptides and contribute to neuronal function.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 06, 2020.
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LncRNAs interacting with the translation machinery contribute to human neuronal differentiation
Katerina Douka, Isabel Birds, Dapeng Wang, Sophie Clayton, Abigail Byford, Elton J. R. Vasconcelos, Mary J. O’Connell, Jim Deuchars, Adrian Whitehouse, Julie L. Aspden
bioRxiv 2020.10.01.321919; doi: https://doi.org/10.1101/2020.10.01.321919
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LncRNAs interacting with the translation machinery contribute to human neuronal differentiation
Katerina Douka, Isabel Birds, Dapeng Wang, Sophie Clayton, Abigail Byford, Elton J. R. Vasconcelos, Mary J. O’Connell, Jim Deuchars, Adrian Whitehouse, Julie L. Aspden
bioRxiv 2020.10.01.321919; doi: https://doi.org/10.1101/2020.10.01.321919

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