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Research Article
Concurrent depletion of Vps37 proteins evokes ESCRT-I destabilization and profound cellular stress responses
Krzysztof Kolmus, Purevsuren Erdenebat, Ewelina Szymańska, Blair Stewig, Krzysztof Goryca, Edyta Derezińska-Wołek, Anna Szumera-Ciećkiewicz, Marta Brewińska-Olchowik, Katarzyna Piwocka, Monika Prochorec-Sobieszek, Michał Mikula, Marta Miączyńska
Journal of Cell Science 2021 134: jcs250951 doi: 10.1242/jcs.250951 Published 8 January 2021
Krzysztof Kolmus
1Laboratory of Cell Biology, International Institute of Molecular and Cell Biology, 02-109 Warsaw, Poland
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  • ORCID record for Krzysztof Kolmus
Purevsuren Erdenebat
1Laboratory of Cell Biology, International Institute of Molecular and Cell Biology, 02-109 Warsaw, Poland
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  • ORCID record for Purevsuren Erdenebat
Ewelina Szymańska
1Laboratory of Cell Biology, International Institute of Molecular and Cell Biology, 02-109 Warsaw, Poland
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  • ORCID record for Ewelina Szymańska
Blair Stewig
1Laboratory of Cell Biology, International Institute of Molecular and Cell Biology, 02-109 Warsaw, Poland
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Krzysztof Goryca
2Department of Genetics, Maria Skłodowska-Curie National Research Institute of Oncology, 02-781 Warsaw, Poland
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Edyta Derezińska-Wołek
3Department of Pathology and Laboratory Medicine, Maria Skłodowska-Curie National Research Institute of Oncology, 02-781 Warsaw, Poland
4Department of Diagnostic Hematology, Institute of Hematology and Transfusion Medicine, 02-776 Warsaw, Poland
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  • ORCID record for Edyta Derezińska-Wołek
Anna Szumera-Ciećkiewicz
3Department of Pathology and Laboratory Medicine, Maria Skłodowska-Curie National Research Institute of Oncology, 02-781 Warsaw, Poland
4Department of Diagnostic Hematology, Institute of Hematology and Transfusion Medicine, 02-776 Warsaw, Poland
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  • ORCID record for Anna Szumera-Ciećkiewicz
Marta Brewińska-Olchowik
5Laboratory of Cytometry, Nencki Institute of Experimental Biology, 02-093 Warsaw, Poland
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Katarzyna Piwocka
5Laboratory of Cytometry, Nencki Institute of Experimental Biology, 02-093 Warsaw, Poland
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  • ORCID record for Katarzyna Piwocka
Monika Prochorec-Sobieszek
3Department of Pathology and Laboratory Medicine, Maria Skłodowska-Curie National Research Institute of Oncology, 02-781 Warsaw, Poland
4Department of Diagnostic Hematology, Institute of Hematology and Transfusion Medicine, 02-776 Warsaw, Poland
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Michał Mikula
2Department of Genetics, Maria Skłodowska-Curie National Research Institute of Oncology, 02-781 Warsaw, Poland
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Marta Miączyńska
1Laboratory of Cell Biology, International Institute of Molecular and Cell Biology, 02-109 Warsaw, Poland
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  • For correspondence: miaczynska@iimcb.gov.pl

Handling Editor: David Stephens

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ABSTRACT

Molecular details of how endocytosis contributes to oncogenesis remain elusive. Our in silico analysis of colorectal cancer (CRC) patients revealed stage-dependent alterations in the expression of 112 endocytosis-related genes. Among them, transcription of the endosomal sorting complex required for transport (ESCRT)-I component VPS37B was decreased in the advanced stages of CRC. Expression of other ESCRT-I core subunits remained unchanged in the investigated dataset. We analyzed an independent cohort of CRC patients, which also showed reduced VPS37A mRNA and protein abundance. Transcriptomic profiling of CRC cells revealed non-redundant functions of Vps37 proteins. Knockdown of VPS37A and VPS37B triggered p21 (CDKN1A)-mediated inhibition of cell proliferation and sterile inflammatory response driven by the nuclear factor (NF)-κB transcription factor and associated with mitogen-activated protein kinase signaling. Co-silencing of VPS37C further potentiated activation of these independently induced processes. The type and magnitude of transcriptional alterations correlated with the differential ESCRT-I stability upon individual and concurrent Vps37 depletion. Our study provides novel insights into cancer cell biology by describing cellular stress responses that are associated with ESCRT-I destabilization.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: K.K., E.S., M. Mikula, M. Miączyńska; Methodology: K.K., P.E., E.S., A.S.-C., E.D.-W., M.B.-O., M. Mikula; Formal analysis: K.K., P.E., B.S., E.S., K.G., A.S.-C., E.D.-W., M.B.-O., K.P., M.P.-S., M. Mikula, M. Miączyńska; Investigation: K.K., P.E., E.S., B.S., E.D.-W., M.B.-O.; Resources: M. Miączyńska; Data curation: K.K., K.G., K.P., M.P.-S., M. Mikula, M. Miączyńska; Writing - original draft: K.K., M. Miączyńska; Writing - review & editing: K.K., P.E., B.S., E.S., A.S.-C., M.B.-O., K.P., M.P.-S., M. Mikula, M. Miączyńska; Supervision: K.K., M. Miączyńska; Funding acquisition: M. Miączyńska.

  • Funding

    This study was financed by a TEAM grant (POIR.04.04.00-00-20CE/16-00), and K.P. was supported by a TEAM-TECH Core Facility Plus/2017–2/2 grant (POIR.04.04.00-00-23C2/17-00) – both grants are from the Fundacja na rzecz Nauki Polskiej co-financed by the European Union under the European Regional Development Fund. E.S. was supported by a Sonata grant (2016/21/D/NZ3/00637) from the Narodowe Centrum Nauki.

  • Data availability

    RNA-Seq datasets reported in this paper have been deposited to GEO under the accession number GSE152195.

  • Supplementary information

    Supplementary information available online at https://jcs.biologists.org/lookup/doi/10.1242/jcs.250951.supplemental

  • Received July 7, 2020.
  • Accepted November 9, 2020.
  • © 2021. Published by The Company of Biologists Ltd
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Keywords

  • ESCRT
  • Vps37
  • Tsg101
  • Colorectal cancer
  • Inflammation
  • Cell growth

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Research Article
Concurrent depletion of Vps37 proteins evokes ESCRT-I destabilization and profound cellular stress responses
Krzysztof Kolmus, Purevsuren Erdenebat, Ewelina Szymańska, Blair Stewig, Krzysztof Goryca, Edyta Derezińska-Wołek, Anna Szumera-Ciećkiewicz, Marta Brewińska-Olchowik, Katarzyna Piwocka, Monika Prochorec-Sobieszek, Michał Mikula, Marta Miączyńska
Journal of Cell Science 2021 134: jcs250951 doi: 10.1242/jcs.250951 Published 8 January 2021
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Research Article
Concurrent depletion of Vps37 proteins evokes ESCRT-I destabilization and profound cellular stress responses
Krzysztof Kolmus, Purevsuren Erdenebat, Ewelina Szymańska, Blair Stewig, Krzysztof Goryca, Edyta Derezińska-Wołek, Anna Szumera-Ciećkiewicz, Marta Brewińska-Olchowik, Katarzyna Piwocka, Monika Prochorec-Sobieszek, Michał Mikula, Marta Miączyńska
Journal of Cell Science 2021 134: jcs250951 doi: 10.1242/jcs.250951 Published 8 January 2021

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