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Single paternal Dexamethasone challenge programs offspring metabolism and reveals circRNAs as novel candidates in RNA-mediated inheritance

View ORCID ProfileKatharina Gapp, Guillermo Parada, Fridolin Gross, Alberto Corcoba, Evelyn Grau, Martin Hemberg, Johannes Bohacek, Eric A. Miska
doi: https://doi.org/10.1101/2021.02.10.429888
Katharina Gapp
1Gurdon Institute, University of Cambridge, Tennis Court Rd, Cambridge, CB2 1QN, UK.
2Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, CB10 1SA, UK
3Institute for Neuroscience, Department of Health Science Technology, ETH Zürich, Winterthurerstr. 190, 8057 Zürich, Switzerland
4Neuroscience Center Zurich, ETH Zurich and University of Zurich, Switzerland
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  • ORCID record for Katharina Gapp
Guillermo Parada
1Gurdon Institute, University of Cambridge, Tennis Court Rd, Cambridge, CB2 1QN, UK.
2Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, CB10 1SA, UK
5Department of Genetics, University of Cambridge, Downing Street, Cambridge, CB2 3EH, UK
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Fridolin Gross
3Institute for Neuroscience, Department of Health Science Technology, ETH Zürich, Winterthurerstr. 190, 8057 Zürich, Switzerland
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Alberto Corcoba
2Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, CB10 1SA, UK
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Evelyn Grau
2Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, CB10 1SA, UK
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Martin Hemberg
1Gurdon Institute, University of Cambridge, Tennis Court Rd, Cambridge, CB2 1QN, UK.
2Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, CB10 1SA, UK
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Johannes Bohacek
3Institute for Neuroscience, Department of Health Science Technology, ETH Zürich, Winterthurerstr. 190, 8057 Zürich, Switzerland
4Neuroscience Center Zurich, ETH Zurich and University of Zurich, Switzerland
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Eric A. Miska
1Gurdon Institute, University of Cambridge, Tennis Court Rd, Cambridge, CB2 1QN, UK.
2Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, CB10 1SA, UK
5Department of Genetics, University of Cambridge, Downing Street, Cambridge, CB2 3EH, UK
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Summary

Single traumatic events that elicit an exaggerated stress response can lead to the development of neuropsychiatric conditions. Studies in mice suggests germline RNA as a mediator of effects of chronic environmental exposures to the progeny. The effects of an acute paternal stress exposure on the germline and their potential consequences on offspring remain unknown. We find that acute administration of an agonist for the stress- sensitive Glucocorticoid receptor, using the common corticosteroid Dexamethasone, affects the RNA payload of post-meiotic transcriptionally silent, mature sperm as soon as 3 hours post exposure. It further impacts early embryonic transcriptional trajectories, as determined by single embryo sequencing, and metabolism in the offspring. Importantly, we show persistent regulation of tRNA fragments in sperm and the descendant 2-cell- embryos, suggesting actual transmission from sperm to embryo. Lastly, we unravel environmentally induced alterations in the previously underconsidered class of sperm circRNAs, and their targets in the early embryo, highlighting this class as a novel candidate in RNA-mediated inheritance.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • The revised version has clarified the relation of our findings in relation to previous findings. This is reflected in changes to the abstract but also to the discussion.

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-ND 4.0 International license.
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Posted March 10, 2021.
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Single paternal Dexamethasone challenge programs offspring metabolism and reveals circRNAs as novel candidates in RNA-mediated inheritance
Katharina Gapp, Guillermo Parada, Fridolin Gross, Alberto Corcoba, Evelyn Grau, Martin Hemberg, Johannes Bohacek, Eric A. Miska
bioRxiv 2021.02.10.429888; doi: https://doi.org/10.1101/2021.02.10.429888
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Single paternal Dexamethasone challenge programs offspring metabolism and reveals circRNAs as novel candidates in RNA-mediated inheritance
Katharina Gapp, Guillermo Parada, Fridolin Gross, Alberto Corcoba, Evelyn Grau, Martin Hemberg, Johannes Bohacek, Eric A. Miska
bioRxiv 2021.02.10.429888; doi: https://doi.org/10.1101/2021.02.10.429888

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