Internal epithelia in Drosophila display rudimentary competence to form cytoplasmic networks of transgenic human vimentin

ABSTRACT Cytoplasmic intermediate filaments (cIFs) are found in all eumetazoans, except arthropods. To investigate the compatibility of cIFs in arthropods, we expressed human vimentin (hVim), a cIF with filament‐forming capacity in vertebrate cells and tissues, transgenically in Drosophila. Transgen...

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Veröffentlicht in:The FASEB journal 2017-12, Vol.31 (12), p.5332-5341
Hauptverfasser: Gullmets, Josef, Torvaldson, Elin, Lindqvist, Julia, Imanishi, Susumu Y., Taimen, Pekka, Meinander, Annika, Eriksson, John E.
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container_end_page 5341
container_issue 12
container_start_page 5332
container_title The FASEB journal
container_volume 31
creator Gullmets, Josef
Torvaldson, Elin
Lindqvist, Julia
Imanishi, Susumu Y.
Taimen, Pekka
Meinander, Annika
Eriksson, John E.
description ABSTRACT Cytoplasmic intermediate filaments (cIFs) are found in all eumetazoans, except arthropods. To investigate the compatibility of cIFs in arthropods, we expressed human vimentin (hVim), a cIF with filament‐forming capacity in vertebrate cells and tissues, transgenically in Drosophila. Transgenic hVim could be recovered from whole‐fly lysates by using a standard procedure for intermediate filament (IF) extraction. When this procedure was used to test for the possible presence of IF‐like proteins in flies, only lamins and tropomyosin were observed in IF‐enriched extracts, thereby providing biochemical reinforcement to the paradigm that arthropods lack cIFs. In Drosophila, transgenic hVim was unable to form filament networks in S2 cells and mesenchymal tissues; however, cage‐like vimentin structures could be observed around the nuclei in internal epithelia, which suggests that Dro‐sophila retains selective competence for filament formation. Taken together, our results imply that although the filament network formation competence is partially lost in Drosophila, a rudimentary filament network formation ability remains in epithelial cells. As a result of the observed selective competence for cIF assembly in Drosophila, we hypothesize that internal epithelial cIFs were the last cIFs to disappear from arthropods.—Gullmets, J., Torvaldson, E., Lindqvist, J., Imanishi, S. Y., Taimen, P., Meinander, A., Eriksson, J. E. Internal epithelia in Drosophila display rudimentary competence to form cytoplasmic networks of transgenic human vimentin. FASEB J. 31, 5332–5341 (2017). www.fasebj.org
doi_str_mv 10.1096/fj.201700332R
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To investigate the compatibility of cIFs in arthropods, we expressed human vimentin (hVim), a cIF with filament‐forming capacity in vertebrate cells and tissues, transgenically in Drosophila. Transgenic hVim could be recovered from whole‐fly lysates by using a standard procedure for intermediate filament (IF) extraction. When this procedure was used to test for the possible presence of IF‐like proteins in flies, only lamins and tropomyosin were observed in IF‐enriched extracts, thereby providing biochemical reinforcement to the paradigm that arthropods lack cIFs. In Drosophila, transgenic hVim was unable to form filament networks in S2 cells and mesenchymal tissues; however, cage‐like vimentin structures could be observed around the nuclei in internal epithelia, which suggests that Dro‐sophila retains selective competence for filament formation. Taken together, our results imply that although the filament network formation competence is partially lost in Drosophila, a rudimentary filament network formation ability remains in epithelial cells. As a result of the observed selective competence for cIF assembly in Drosophila, we hypothesize that internal epithelial cIFs were the last cIFs to disappear from arthropods.—Gullmets, J., Torvaldson, E., Lindqvist, J., Imanishi, S. Y., Taimen, P., Meinander, A., Eriksson, J. E. Internal epithelia in Drosophila display rudimentary competence to form cytoplasmic networks of transgenic human vimentin. 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source Wiley Online Library; Alma/SFX Local Collection
subjects arthropod
Arthropoda
Arthropods
Drosophila
Epithelial cells
evolution
Filaments
Insects
Intermediate filaments
lamin
Lamins
Lysates
Mesenchyme
Network formation
Networks
Nuclei
Proteins
Tissues
Tropomyosin
Vimentin
title Internal epithelia in Drosophila display rudimentary competence to form cytoplasmic networks of transgenic human vimentin
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