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...
Gespeichert in:
Veröffentlicht in: | The FASEB journal 2017-12, Vol.31 (12), p.5332-5341 |
---|---|
Hauptverfasser: | , , , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
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 |
format | Article |
fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_1926687252</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1983928679</sourcerecordid><originalsourceid>FETCH-LOGICAL-c412R-54e9d24bede82baa78b50a5134b14127fd031045f96c0dacf867a6ccd067b7fd3</originalsourceid><addsrcrecordid>eNp90Utv1DAUBWALgei0sGSLLLFhk3LtJLYjVlAYKKqEVGAdOc4N4yGxg-1Q5d_Xw5SHWLCydP3pLM4h5AmDcwaNeDHszzkwCVCW_Poe2bC6hEIoAffJBlTDCyFKdUJOY9wDAAMmHpITrqRUjaw2ZL10CYPTI8XZph2OVlPr6Jvgo593dtS0t3Ee9UrD0tsJXdJhpcZPMyZ0BmnydPBhomZNPrs4WUMdphsfvkXqB5qCdvErunzeLZN29MfPFOsekQeDHiM-vnvPyJft288X74urj-8uL15dFaZi_LqoK2x6XnXYo-Kd1lJ1NeialVXHMpBDDyWDqh4aYaDXZlBCamFMD0J2-bc8I8-PuXPw3xeMqZ1sNDiO2qFfYssaLoSSvOaZPvuH7v1yKOegVNnwnN1kVRyVySXFgEM7BzvlWloG7WGTdti3fzbJ_uld6tJN2P_Wv0bI4OUR3NgR1_-ntdtPr_n2w1_xt_3ymy4</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1983928679</pqid></control><display><type>article</type><title>Internal epithelia in Drosophila display rudimentary competence to form cytoplasmic networks of transgenic human vimentin</title><source>Wiley Online Library</source><source>Alma/SFX Local Collection</source><creator>Gullmets, Josef ; Torvaldson, Elin ; Lindqvist, Julia ; Imanishi, Susumu Y. ; Taimen, Pekka ; Meinander, Annika ; Eriksson, John E.</creator><creatorcontrib>Gullmets, Josef ; Torvaldson, Elin ; Lindqvist, Julia ; Imanishi, Susumu Y. ; Taimen, Pekka ; Meinander, Annika ; Eriksson, John E.</creatorcontrib><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</description><identifier>ISSN: 0892-6638</identifier><identifier>EISSN: 1530-6860</identifier><identifier>DOI: 10.1096/fj.201700332R</identifier><identifier>PMID: 28778974</identifier><language>eng</language><publisher>United States: Federation of American Societies for Experimental Biology</publisher><subject>arthropod ; Arthropoda ; Arthropods ; Drosophila ; Epithelial cells ; evolution ; Filaments ; Insects ; Intermediate filaments ; lamin ; Lamins ; Lysates ; Mesenchyme ; Network formation ; Networks ; Nuclei ; Proteins ; Tissues ; Tropomyosin ; Vimentin</subject><ispartof>The FASEB journal, 2017-12, Vol.31 (12), p.5332-5341</ispartof><rights>FASEB</rights><rights>FASEB.</rights><rights>Copyright Federation of American Societies for Experimental Biology (FASEB) Dec 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c412R-54e9d24bede82baa78b50a5134b14127fd031045f96c0dacf867a6ccd067b7fd3</citedby><cites>FETCH-LOGICAL-c412R-54e9d24bede82baa78b50a5134b14127fd031045f96c0dacf867a6ccd067b7fd3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1096%2Ffj.201700332R$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1096%2Ffj.201700332R$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27903,27904,45553,45554</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28778974$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gullmets, Josef</creatorcontrib><creatorcontrib>Torvaldson, Elin</creatorcontrib><creatorcontrib>Lindqvist, Julia</creatorcontrib><creatorcontrib>Imanishi, Susumu Y.</creatorcontrib><creatorcontrib>Taimen, Pekka</creatorcontrib><creatorcontrib>Meinander, Annika</creatorcontrib><creatorcontrib>Eriksson, John E.</creatorcontrib><title>Internal epithelia in Drosophila display rudimentary competence to form cytoplasmic networks of transgenic human vimentin</title><title>The FASEB journal</title><addtitle>FASEB J</addtitle><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</description><subject>arthropod</subject><subject>Arthropoda</subject><subject>Arthropods</subject><subject>Drosophila</subject><subject>Epithelial cells</subject><subject>evolution</subject><subject>Filaments</subject><subject>Insects</subject><subject>Intermediate filaments</subject><subject>lamin</subject><subject>Lamins</subject><subject>Lysates</subject><subject>Mesenchyme</subject><subject>Network formation</subject><subject>Networks</subject><subject>Nuclei</subject><subject>Proteins</subject><subject>Tissues</subject><subject>Tropomyosin</subject><subject>Vimentin</subject><issn>0892-6638</issn><issn>1530-6860</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><recordid>eNp90Utv1DAUBWALgei0sGSLLLFhk3LtJLYjVlAYKKqEVGAdOc4N4yGxg-1Q5d_Xw5SHWLCydP3pLM4h5AmDcwaNeDHszzkwCVCW_Poe2bC6hEIoAffJBlTDCyFKdUJOY9wDAAMmHpITrqRUjaw2ZL10CYPTI8XZph2OVlPr6Jvgo593dtS0t3Ee9UrD0tsJXdJhpcZPMyZ0BmnydPBhomZNPrs4WUMdphsfvkXqB5qCdvErunzeLZN29MfPFOsekQeDHiM-vnvPyJft288X74urj-8uL15dFaZi_LqoK2x6XnXYo-Kd1lJ1NeialVXHMpBDDyWDqh4aYaDXZlBCamFMD0J2-bc8I8-PuXPw3xeMqZ1sNDiO2qFfYssaLoSSvOaZPvuH7v1yKOegVNnwnN1kVRyVySXFgEM7BzvlWloG7WGTdti3fzbJ_uld6tJN2P_Wv0bI4OUR3NgR1_-ntdtPr_n2w1_xt_3ymy4</recordid><startdate>201712</startdate><enddate>201712</enddate><creator>Gullmets, Josef</creator><creator>Torvaldson, Elin</creator><creator>Lindqvist, Julia</creator><creator>Imanishi, Susumu Y.</creator><creator>Taimen, Pekka</creator><creator>Meinander, Annika</creator><creator>Eriksson, John E.</creator><general>Federation of American Societies for Experimental Biology</general><general>Federation of American Societies for Experimental Biology (FASEB)</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7QP</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>201712</creationdate><title>Internal epithelia in Drosophila display rudimentary competence to form cytoplasmic networks of transgenic human vimentin</title><author>Gullmets, Josef ; Torvaldson, Elin ; Lindqvist, Julia ; Imanishi, Susumu Y. ; Taimen, Pekka ; Meinander, Annika ; Eriksson, John E.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c412R-54e9d24bede82baa78b50a5134b14127fd031045f96c0dacf867a6ccd067b7fd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>arthropod</topic><topic>Arthropoda</topic><topic>Arthropods</topic><topic>Drosophila</topic><topic>Epithelial cells</topic><topic>evolution</topic><topic>Filaments</topic><topic>Insects</topic><topic>Intermediate filaments</topic><topic>lamin</topic><topic>Lamins</topic><topic>Lysates</topic><topic>Mesenchyme</topic><topic>Network formation</topic><topic>Networks</topic><topic>Nuclei</topic><topic>Proteins</topic><topic>Tissues</topic><topic>Tropomyosin</topic><topic>Vimentin</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gullmets, Josef</creatorcontrib><creatorcontrib>Torvaldson, Elin</creatorcontrib><creatorcontrib>Lindqvist, Julia</creatorcontrib><creatorcontrib>Imanishi, Susumu Y.</creatorcontrib><creatorcontrib>Taimen, Pekka</creatorcontrib><creatorcontrib>Meinander, Annika</creatorcontrib><creatorcontrib>Eriksson, John E.</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The FASEB journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gullmets, Josef</au><au>Torvaldson, Elin</au><au>Lindqvist, Julia</au><au>Imanishi, Susumu Y.</au><au>Taimen, Pekka</au><au>Meinander, Annika</au><au>Eriksson, John E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Internal epithelia in Drosophila display rudimentary competence to form cytoplasmic networks of transgenic human vimentin</atitle><jtitle>The FASEB journal</jtitle><addtitle>FASEB J</addtitle><date>2017-12</date><risdate>2017</risdate><volume>31</volume><issue>12</issue><spage>5332</spage><epage>5341</epage><pages>5332-5341</pages><issn>0892-6638</issn><eissn>1530-6860</eissn><abstract>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</abstract><cop>United States</cop><pub>Federation of American Societies for Experimental Biology</pub><pmid>28778974</pmid><doi>10.1096/fj.201700332R</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0892-6638 |
ispartof | The FASEB journal, 2017-12, Vol.31 (12), p.5332-5341 |
issn | 0892-6638 1530-6860 |
language | eng |
recordid | cdi_proquest_miscellaneous_1926687252 |
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 |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-24T16%3A23%3A28IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Internal%20epithelia%20in%20Drosophila%20display%20rudimentary%20competence%20to%20form%20cytoplasmic%20networks%20of%20transgenic%20human%20vimentin&rft.jtitle=The%20FASEB%20journal&rft.au=Gullmets,%20Josef&rft.date=2017-12&rft.volume=31&rft.issue=12&rft.spage=5332&rft.epage=5341&rft.pages=5332-5341&rft.issn=0892-6638&rft.eissn=1530-6860&rft_id=info:doi/10.1096/fj.201700332R&rft_dat=%3Cproquest_cross%3E1983928679%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1983928679&rft_id=info:pmid/28778974&rfr_iscdi=true |