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A dominant vimentin variant causes a rare syndrome with premature aging

A dominant vimentin variant causes a rare syndrome with premature aging
A dominant vimentin variant causes a rare syndrome with premature aging

Progeroid syndromes are a group of rare genetic disorders, which mimic natural aging. Unraveling the molecular defects in such conditions could impact our understanding of age-related syndromes such as Alzheimer's or cardiovascular diseases. Here we report a de novo heterozygous missense variant in the intermediate filament vimentin (c.1160 T > C; p.(Leu387Pro)) causing a multisystem disorder associated with frontonasal dysostosis and premature aging in a 39-year-old individual. Human vimentin p.(Leu387Pro) expression in zebrafish perturbed body fat distribution, and craniofacial and peripheral nervous system development. In addition, studies in patient-derived and transfected cells revealed that the variant affects vimentin turnover and its ability to form filaments in the absence of wild-type vimentin. Vimentin p.(Leu387Pro) expression diminished the amount of peripilin and reduced lipid accumulation in differentiating adipocytes, recapitulating key patient's features in vivo and in vitro. Our data highlight the function of vimentin during development and suggest its contribution to natural aging.

3T3-L1 Cells, Adipocytes/metabolism, Adiposity, Adult, Animals, Cells, Cultured, Genes, Dominant, Humans, Induced Pluripotent Stem Cells/metabolism, MCF-7 Cells, Male, Mice, Mutation, Neurogenesis, Perilipin-1/metabolism, Progeria/genetics, Vimentin/genetics, Zebrafish
1018-4813
1218-1230
Cogné, Benjamin
ed383adc-c639-4e1d-a093-2bcd93a2b032
Bouameur, Jamal-Eddine
0ff98713-ce3b-4ed2-a4f1-e2ff3b8f671a
Hayot, Gaëlle
d2a9f919-6f74-4229-9d60-b45af1ddbd7d
Latypova, Xenia
587e46d4-0efe-4176-a25b-04ee743b0a51
Pattabiraman, Sundararaghavan
a9f5aac6-6388-4b65-ba29-33aa47aad5a4
Caillaud, Amandine
43bd8c66-8d3e-49d4-920a-415a411710d8
Si-Tayeb, Karim
37a4fcc2-6148-45c3-92b3-8e71afb709ac
Besnard, Thomas
9f398811-9c9d-4593-8f09-548d3e04cbda
Küry, Sébastien
2701e591-2a45-492d-b35a-ce8ae4cd441a
Chariau, Caroline
23296a56-20cc-4562-9dcb-9057d18cc232
Gaignerie, Anne
64973600-eef8-4762-b69b-7fd3c8105d10
David, Laurent
a77108ec-3c59-4e99-b383-1ffca0a3c0d8
Bordure, Philippe
693d8e70-c23f-4194-ab92-627ea0f7b7e5
Kaganovich, Daniel
ebb13f4e-e925-4aef-88e7-ddc25ef52d8f
Bézieau, Stéphane
4b683def-53d9-45f0-8d2e-7efd0ad42e06
Golzio, Christelle
e4faeef7-c91f-4b2d-ae78-4934271f2cde
Magin, Thomas M
66b8a34b-282d-4f55-81a5-0aa47c524939
Isidor, Bertrand
b4213395-1009-4ff5-a9ba-9a41c503e6ec
Cogné, Benjamin
ed383adc-c639-4e1d-a093-2bcd93a2b032
Bouameur, Jamal-Eddine
0ff98713-ce3b-4ed2-a4f1-e2ff3b8f671a
Hayot, Gaëlle
d2a9f919-6f74-4229-9d60-b45af1ddbd7d
Latypova, Xenia
587e46d4-0efe-4176-a25b-04ee743b0a51
Pattabiraman, Sundararaghavan
a9f5aac6-6388-4b65-ba29-33aa47aad5a4
Caillaud, Amandine
43bd8c66-8d3e-49d4-920a-415a411710d8
Si-Tayeb, Karim
37a4fcc2-6148-45c3-92b3-8e71afb709ac
Besnard, Thomas
9f398811-9c9d-4593-8f09-548d3e04cbda
Küry, Sébastien
2701e591-2a45-492d-b35a-ce8ae4cd441a
Chariau, Caroline
23296a56-20cc-4562-9dcb-9057d18cc232
Gaignerie, Anne
64973600-eef8-4762-b69b-7fd3c8105d10
David, Laurent
a77108ec-3c59-4e99-b383-1ffca0a3c0d8
Bordure, Philippe
693d8e70-c23f-4194-ab92-627ea0f7b7e5
Kaganovich, Daniel
ebb13f4e-e925-4aef-88e7-ddc25ef52d8f
Bézieau, Stéphane
4b683def-53d9-45f0-8d2e-7efd0ad42e06
Golzio, Christelle
e4faeef7-c91f-4b2d-ae78-4934271f2cde
Magin, Thomas M
66b8a34b-282d-4f55-81a5-0aa47c524939
Isidor, Bertrand
b4213395-1009-4ff5-a9ba-9a41c503e6ec

Cogné, Benjamin, Bouameur, Jamal-Eddine, Hayot, Gaëlle, Latypova, Xenia, Pattabiraman, Sundararaghavan, Caillaud, Amandine, Si-Tayeb, Karim, Besnard, Thomas, Küry, Sébastien, Chariau, Caroline, Gaignerie, Anne, David, Laurent, Bordure, Philippe, Kaganovich, Daniel, Bézieau, Stéphane, Golzio, Christelle, Magin, Thomas M and Isidor, Bertrand (2020) A dominant vimentin variant causes a rare syndrome with premature aging. European Journal of Human Genetics, 28 (9), 1218-1230. (doi:10.1038/s41431-020-0583-2).

Record type: Article

Abstract

Progeroid syndromes are a group of rare genetic disorders, which mimic natural aging. Unraveling the molecular defects in such conditions could impact our understanding of age-related syndromes such as Alzheimer's or cardiovascular diseases. Here we report a de novo heterozygous missense variant in the intermediate filament vimentin (c.1160 T > C; p.(Leu387Pro)) causing a multisystem disorder associated with frontonasal dysostosis and premature aging in a 39-year-old individual. Human vimentin p.(Leu387Pro) expression in zebrafish perturbed body fat distribution, and craniofacial and peripheral nervous system development. In addition, studies in patient-derived and transfected cells revealed that the variant affects vimentin turnover and its ability to form filaments in the absence of wild-type vimentin. Vimentin p.(Leu387Pro) expression diminished the amount of peripilin and reduced lipid accumulation in differentiating adipocytes, recapitulating key patient's features in vivo and in vitro. Our data highlight the function of vimentin during development and suggest its contribution to natural aging.

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More information

Accepted/In Press date: 17 January 2020
e-pub ahead of print date: 17 February 2020
Published date: September 2020
Keywords: 3T3-L1 Cells, Adipocytes/metabolism, Adiposity, Adult, Animals, Cells, Cultured, Genes, Dominant, Humans, Induced Pluripotent Stem Cells/metabolism, MCF-7 Cells, Male, Mice, Mutation, Neurogenesis, Perilipin-1/metabolism, Progeria/genetics, Vimentin/genetics, Zebrafish

Identifiers

Local EPrints ID: 474840
URI: http://eprints.soton.ac.uk/id/eprint/474840
ISSN: 1018-4813
PURE UUID: 88e347d4-d07b-461b-8f33-087a8dbd30b5
ORCID for Daniel Kaganovich: ORCID iD orcid.org/0000-0003-2398-1596

Catalogue record

Date deposited: 03 Mar 2023 17:45
Last modified: 17 Mar 2024 04:17

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Contributors

Author: Benjamin Cogné
Author: Jamal-Eddine Bouameur
Author: Gaëlle Hayot
Author: Xenia Latypova
Author: Sundararaghavan Pattabiraman
Author: Amandine Caillaud
Author: Karim Si-Tayeb
Author: Thomas Besnard
Author: Sébastien Küry
Author: Caroline Chariau
Author: Anne Gaignerie
Author: Laurent David
Author: Philippe Bordure
Author: Daniel Kaganovich ORCID iD
Author: Stéphane Bézieau
Author: Christelle Golzio
Author: Thomas M Magin
Author: Bertrand Isidor

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