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Biogenesis of RNA-containing extracellular vesicles at endoplasmic reticulum membrane contact sites

Bahnisikha Barman, Jie Ping, Evan Krystofiak, Ryan Allen, Nripesh Prasad, Kasey Vickers, James G. Patton, Qi Liu, Alissa M. Weaver
doi: https://doi.org/10.1101/2020.12.04.412379
Bahnisikha Barman
1Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN, USA
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Jie Ping
2Department of Biostatistics, Vanderbilt University Medical Center, Nashville, TN, USA
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Evan Krystofiak
3Vanderbilt University Cell Imaging Shared Resource, Nashville, TN, USA
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Ryan Allen
4Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
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Nripesh Prasad
5HudsonAlpha Institute for Biotechnology, Huntsville, AL, USA
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Kasey Vickers
4Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, USA
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James G. Patton
6Department of Biological Sciences, Vanderbilt University, Nashville, TN, USA
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Qi Liu
2Department of Biostatistics, Vanderbilt University Medical Center, Nashville, TN, USA
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Alissa M. Weaver
1Department of Cell and Developmental Biology, Vanderbilt University School of Medicine, Nashville, TN, USA
7Department of Pathology, Microbiology and Immunology, Vanderbilt University Medical, Center, USA
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  • For correspondence: Alissa.weaver@vanderbilt.edu
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Summary

RNA transferred via extracellular vesicles (EVs) can influence cell and tissue phenotypes; however, the biogenesis of RNA-containing EVs is poorly understood and even controversial. Here, we identify the conserved endoplasmic reticulum membrane contact site (MCS) linker protein VAP-A as a major regulator of the RNA and RNA-binding protein content of small and large EVs. We also identify a unique subpopulation of secreted small EVs that is highly enriched in RNA and regulated by VAP-A. Functional experiments revealed that VAP-A-regulated EVs are critical for the transfer of miR-100 between cells and for in vivo tumor formation. Lipid analysis of VAP-A-knockdown EVs revealed large alterations in lipids known to regulate EV biogenesis, including ceramides and cholesterol. Knockdown of VAP-A-binding ceramide and cholesterol transfer proteins CERT and ORP1L led to similar defects in biogenesis of RNA-containing EVs. We propose that lipid transfer at VAP-A-positive MCS drives biogenesis of a select RNA-containing EV population.

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 December 05, 2020.
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Biogenesis of RNA-containing extracellular vesicles at endoplasmic reticulum membrane contact sites
Bahnisikha Barman, Jie Ping, Evan Krystofiak, Ryan Allen, Nripesh Prasad, Kasey Vickers, James G. Patton, Qi Liu, Alissa M. Weaver
bioRxiv 2020.12.04.412379; doi: https://doi.org/10.1101/2020.12.04.412379
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Biogenesis of RNA-containing extracellular vesicles at endoplasmic reticulum membrane contact sites
Bahnisikha Barman, Jie Ping, Evan Krystofiak, Ryan Allen, Nripesh Prasad, Kasey Vickers, James G. Patton, Qi Liu, Alissa M. Weaver
bioRxiv 2020.12.04.412379; doi: https://doi.org/10.1101/2020.12.04.412379

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