Splicing variation of BMP2K balances abundance of COPII assemblies and autophagic degradation in erythroid cells

  1. Jaroslaw Cendrowski  Is a corresponding author
  2. Marta Kaczmarek
  3. Michał Mazur
  4. Katarzyna Kuzmicz-Kowalska
  5. Kamil Jastrzebski
  6. Marta Brewinska-Olchowik
  7. Agata Kominek
  8. Katarzyna Piwocka
  9. Marta Miaczynska  Is a corresponding author
  1. International Institute of Molecular and Cell Biology in Warsaw, Poland
  2. Nencki Institute of Experimental Biology, Polish Academy of Sciences, Poland

Abstract

Intracellular transport undergoes remodeling upon cell differentiation, which involves cell type-specific regulators. Bone morphogenetic protein 2-inducible kinase (BMP2K) has been potentially implicated in endocytosis and cell differentiation but its molecular functions remained unknown. We discovered that its longer (L) and shorter (S) splicing variants regulate erythroid differentiation in a manner unexplainable by their involvement in AP-2 adaptor phosphorylation and endocytosis. However, both variants interact with SEC16A and could localize to the juxtanuclear secretory compartment. Variant-specific depletion approach showed that BMP2K isoforms constitute a BMP2K-L/S regulatory system that controls the distribution of SEC16A and SEC24B as well as SEC31A abundance at COPII assemblies. Finally, we found L to promote and S to restrict autophagic degradation and erythroid differentiation. Hence, we propose that BMP2K-L and BMP2K-S differentially regulate abundance and distribution of COPII assemblies as well as autophagy, possibly thereby fine-tuning erythroid differentiation.

Data availability

The mass spectrometry proteomics data have been deposited to the ProteomeXchange Consortium via the PRIDE partner repository with the dataset identifier PXD013542

The following data sets were generated

Article and author information

Author details

  1. Jaroslaw Cendrowski

    Laboratory of Cell Biology, International Institute of Molecular and Cell Biology in Warsaw, Warsaw, Poland
    For correspondence
    jcendrowski@iimcb.gov.pl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8579-7279
  2. Marta Kaczmarek

    Laboratory of Cell Biology, International Institute of Molecular and Cell Biology in Warsaw, Warsaw, Poland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4939-6299
  3. Michał Mazur

    Laboratory of Cell Biology, International Institute of Molecular and Cell Biology in Warsaw, Warsaw, Poland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5087-4409
  4. Katarzyna Kuzmicz-Kowalska

    Laboratory of Cell Biology, International Institute of Molecular and Cell Biology in Warsaw, Warsaw, Poland
    Competing interests
    The authors declare that no competing interests exist.
  5. Kamil Jastrzebski

    Laboratory of Cell Biology, International Institute of Molecular and Cell Biology in Warsaw, Warsaw, Poland
    Competing interests
    The authors declare that no competing interests exist.
  6. Marta Brewinska-Olchowik

    Neurobiology Center, Nencki Institute of Experimental Biology, Polish Academy of Sciences, Warsaw, Poland
    Competing interests
    The authors declare that no competing interests exist.
  7. Agata Kominek

    Neurobiology Center, Nencki Institute of Experimental Biology, Polish Academy of Sciences, Warsaw, Poland
    Competing interests
    The authors declare that no competing interests exist.
  8. Katarzyna Piwocka

    Neurobiology Center, Nencki Institute of Experimental Biology, Polish Academy of Sciences, Warsaw, Poland
    Competing interests
    The authors declare that no competing interests exist.
  9. Marta Miaczynska

    Laboratory of Cell Biology, International Institute of Molecular and Cell Biology in Warsaw, Warsaw, Poland
    For correspondence
    miaczynska@iimcb.gov.pl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0031-5267

Funding

Narodowe Centrum Nauki (UMO-2011/02/A/NZ3/00149)

  • Jaroslaw Cendrowski
  • Katarzyna Kuzmicz-Kowalska
  • Kamil Jastrzebski
  • Marta Miaczynska

Fundacja na rzecz Nauki Polskiej (POIR.04.04.00-00-20CE/16-00)

  • Marta Kaczmarek
  • Kamil Jastrzebski
  • Marta Miaczynska

Fundacja na rzecz Nauki Polskiej (POIR.04.04.00-00-1C54/16-00)

  • Jaroslaw Cendrowski
  • Michał Mazur

Fundacja na rzecz Nauki Polskiej (POIR.04.04.00-00-23C2/17-00)

  • Katarzyna Piwocka

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2020, Cendrowski et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Jaroslaw Cendrowski
  2. Marta Kaczmarek
  3. Michał Mazur
  4. Katarzyna Kuzmicz-Kowalska
  5. Kamil Jastrzebski
  6. Marta Brewinska-Olchowik
  7. Agata Kominek
  8. Katarzyna Piwocka
  9. Marta Miaczynska
(2020)
Splicing variation of BMP2K balances abundance of COPII assemblies and autophagic degradation in erythroid cells
eLife 9:e58504.
https://doi.org/10.7554/eLife.58504

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https://doi.org/10.7554/eLife.58504