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Exostosin-1 Glycosyltransferase Regulates Endoplasmic Reticulum Architecture and Dynamics

Despoina Kerselidou, View ORCID ProfileBushra Saeed Dohai, David R. Nelson, Sarah Daakour, View ORCID ProfileNicolas De Cock, View ORCID ProfileDae-Kyum Kim, View ORCID ProfileJulien Olivet, Diana C. El Assal, Ashish Jaiswal, Deeya Saha, Charlotte Pain, Filip Matthijssens, Pierre Lemaitre, Michael Herfs, Julien Chapuis, Bart Ghesquiere, Didier Vertommen, Verena Kriechbaumer, Kèvin Knoops, Carmen Lopez-Iglesias, Marc van Zandvoort, View ORCID ProfileJean-Charles Lambert, View ORCID ProfileJulien Hanson, Christophe Desmet, Marc Thiry, View ORCID ProfileKyle J. Lauersen, Marc Vidal, Pieter Van Vlierberghe, Franck Dequiedt, Kourosh Salehi-Ashtiani, View ORCID ProfileJean-Claude Twizere
doi: https://doi.org/10.1101/2020.09.02.275925
Despoina Kerselidou
1Laboratory of Viral Interactomes, GIGA Institute, University of Liege, Liege, Belgium
2Laboratory of Gene expression and Cancer, GIGA Institute, University of Liege, Liege, Belgium
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Bushra Saeed Dohai
3Division of Science and Math, New York University Abu Dhabi, Abu Dhabi, UAE
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David R. Nelson
4Center for Genomics and Systems Biology (CGSB), New York University Abu Dhabi, Abu Dhabi, UAE
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Sarah Daakour
4Center for Genomics and Systems Biology (CGSB), New York University Abu Dhabi, Abu Dhabi, UAE
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Nicolas De Cock
5TERRA Teaching and Research Centre, University of Liege, Belgium
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Dae-Kyum Kim
6The Donnelly Centre, University of Toronto, Toronto, ON, Canada
7Department of Molecular Genetics, University of Toronto, Toronto, ON, Canada
8Lunenfeld Tanenbaum Research Institute, Mount Sinai Hospital, Toronto, ON, Canada
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Julien Olivet
1Laboratory of Viral Interactomes, GIGA Institute, University of Liege, Liege, Belgium
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Diana C. El Assal
3Division of Science and Math, New York University Abu Dhabi, Abu Dhabi, UAE
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Ashish Jaiswal
4Center for Genomics and Systems Biology (CGSB), New York University Abu Dhabi, Abu Dhabi, UAE
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Deeya Saha
1Laboratory of Viral Interactomes, GIGA Institute, University of Liege, Liege, Belgium
2Laboratory of Gene expression and Cancer, GIGA Institute, University of Liege, Liege, Belgium
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Charlotte Pain
9Plant Cell Biology, Biological and Medical Sciences, Oxford Brookes University, Oxford, UK
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Filip Matthijssens
10Department of Biomolecular Medicine and Center for Medical Genetics, Ghent University, Ghent, Belgium
11Cancer Research Institute Ghent (CRIG), Ghent, Belgium
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Pierre Lemaitre
12GIGA-I3 Unit, GIGA Institute, University of Liege, Belgium
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Michael Herfs
13GIGA-Cancer Unit, GIGA Institute, University of Liege, Belgium
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Julien Chapuis
14Laboratory of Excellence Distalz, INSERM Unit 1167, Pasteur Institute of Lille, Lille, France
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Bart Ghesquiere
15Metabolomics Expertise Center, Center for Cancer Biology, VIB Center for Cancer Biology, Leuven, Belgium
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Didier Vertommen
16de Duve Institute, Catholic University of Louvain, Brussels, Belgium
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Verena Kriechbaumer
9Plant Cell Biology, Biological and Medical Sciences, Oxford Brookes University, Oxford, UK
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Kèvin Knoops
17Microscopy CORE Lab, Maastricht Multimodal Molecular Imaging Institute, Maastricht University, Maastricht, the Netherlands
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Carmen Lopez-Iglesias
17Microscopy CORE Lab, Maastricht Multimodal Molecular Imaging Institute, Maastricht University, Maastricht, the Netherlands
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Marc van Zandvoort
18Department of Cell Biology, School for Cardiovascular Diseases (CARIM), School for Nutrition and Translational Research in Metabolism (NUTRIM), School for Mental health and Neuroscience (MHeNS), and School for Oncology and Developmental Biology (GROW), Maastricht University, Maastricht, the Netherlands
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Jean-Charles Lambert
14Laboratory of Excellence Distalz, INSERM Unit 1167, Pasteur Institute of Lille, Lille, France
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Julien Hanson
19GIGA-Molecular Pharmacology, University of Liege, Liege, Belgium
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Christophe Desmet
12GIGA-I3 Unit, GIGA Institute, University of Liege, Belgium
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Marc Thiry
20Laboratory of cell and tissue Biology, GIGA-Neurosciences, University of Liège, Liège, Belgium
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Kyle J. Lauersen
21Biological and Environmental Sciences and Engineering Division (BESE), King Abdullah University of Science and Technology (KAUST), Thuwal, Kingdom of Saudi Arabia
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Marc Vidal
22Center for Cancer Systems Biology (CCSB), Dana-Farber Cancer Institute, Boston, MA, USA
23Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, MA, USA
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  • For correspondence: marc_vidal@dfci.harvard.edu fdequiedt@uliege.be ksa3@nyu.edu jean-claude.twizere@uliege.be
Pieter Van Vlierberghe
10Department of Biomolecular Medicine and Center for Medical Genetics, Ghent University, Ghent, Belgium
11Cancer Research Institute Ghent (CRIG), Ghent, Belgium
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Franck Dequiedt
2Laboratory of Gene expression and Cancer, GIGA Institute, University of Liege, Liege, Belgium
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  • For correspondence: marc_vidal@dfci.harvard.edu fdequiedt@uliege.be ksa3@nyu.edu jean-claude.twizere@uliege.be
Kourosh Salehi-Ashtiani
3Division of Science and Math, New York University Abu Dhabi, Abu Dhabi, UAE
4Center for Genomics and Systems Biology (CGSB), New York University Abu Dhabi, Abu Dhabi, UAE
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  • For correspondence: marc_vidal@dfci.harvard.edu fdequiedt@uliege.be ksa3@nyu.edu jean-claude.twizere@uliege.be
Jean-Claude Twizere
1Laboratory of Viral Interactomes, GIGA Institute, University of Liege, Liege, Belgium
5TERRA Teaching and Research Centre, University of Liege, Belgium
22Center for Cancer Systems Biology (CCSB), Dana-Farber Cancer Institute, Boston, MA, USA
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  • For correspondence: marc_vidal@dfci.harvard.edu fdequiedt@uliege.be ksa3@nyu.edu jean-claude.twizere@uliege.be
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SUMMARY

The endoplasmic reticulum (ER) is a central eukaryotic organelle with a tubular network made of hairpin proteins linked by hydrolysis of GTP nucleotides. Among post-translational modifications initiated at the ER level, glycosylation is the most common reaction. However, our understanding of the impact of glycosylation on ER structure remains unclear. Here, we show that Exostosin-1 (EXT1) glycosyltransferase, an enzyme involved in N-glycosylation, is a key regulator of ER morphology and dynamics. We have integrated multi-omics data and super-resolution imaging to characterize the broad effect of EXT1 inactivation, including ER shape-dynamics-function relationships in mammalian cells. We have observed that, inactivating EXT1 induces cell enlargement and enhances metabolic switches such as protein secretion. In particular, suppressing EXT1 in mouse thymocytes causes developmental dysfunctions associated to ER network extension. Our findings suggest that EXT1 drives glycosylation reactions involving ER structural proteins and high-energy nucleotide sugars, which might also apply to other organelles.

Competing Interest Statement

The University of Liege filed a patent application relating to the use of cells knocked down for EXT1 expression in biopharmaceuticals production (European Patent Office - Priority filing referred as EP20158875).

Footnotes

  • ↵24 Lead contact

  • https://data.mendeley.com/datasets/y3h34szx5z/1

  • https://data.mendeley.com/datasets/2mfzds3mmv/1

  • https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE138030

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Exostosin-1 Glycosyltransferase Regulates Endoplasmic Reticulum Architecture and Dynamics
Despoina Kerselidou, Bushra Saeed Dohai, David R. Nelson, Sarah Daakour, Nicolas De Cock, Dae-Kyum Kim, Julien Olivet, Diana C. El Assal, Ashish Jaiswal, Deeya Saha, Charlotte Pain, Filip Matthijssens, Pierre Lemaitre, Michael Herfs, Julien Chapuis, Bart Ghesquiere, Didier Vertommen, Verena Kriechbaumer, Kèvin Knoops, Carmen Lopez-Iglesias, Marc van Zandvoort, Jean-Charles Lambert, Julien Hanson, Christophe Desmet, Marc Thiry, Kyle J. Lauersen, Marc Vidal, Pieter Van Vlierberghe, Franck Dequiedt, Kourosh Salehi-Ashtiani, Jean-Claude Twizere
bioRxiv 2020.09.02.275925; doi: https://doi.org/10.1101/2020.09.02.275925
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Exostosin-1 Glycosyltransferase Regulates Endoplasmic Reticulum Architecture and Dynamics
Despoina Kerselidou, Bushra Saeed Dohai, David R. Nelson, Sarah Daakour, Nicolas De Cock, Dae-Kyum Kim, Julien Olivet, Diana C. El Assal, Ashish Jaiswal, Deeya Saha, Charlotte Pain, Filip Matthijssens, Pierre Lemaitre, Michael Herfs, Julien Chapuis, Bart Ghesquiere, Didier Vertommen, Verena Kriechbaumer, Kèvin Knoops, Carmen Lopez-Iglesias, Marc van Zandvoort, Jean-Charles Lambert, Julien Hanson, Christophe Desmet, Marc Thiry, Kyle J. Lauersen, Marc Vidal, Pieter Van Vlierberghe, Franck Dequiedt, Kourosh Salehi-Ashtiani, Jean-Claude Twizere
bioRxiv 2020.09.02.275925; doi: https://doi.org/10.1101/2020.09.02.275925

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