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RESEARCH ARTICLE
Vps13 is required for timely removal of nurse cell corpses
Anita I. E. Faber, Marianne van der Zwaag, Hein Schepers, Ellie Eggens-Meijer, Bart Kanon, Carmen IJsebaart, Jeroen Kuipers, Ben N. G. Giepmans, Raimundo Freire, Nicola A. Grzeschik, Catherine Rabouille, Ody C. M. Sibon
Development 2020 147: dev191759 doi: 10.1242/dev.191759 Published 29 October 2020
Anita I. E. Faber
1Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, The University of Groningen, 9713 AV, Groningen, The Netherlands
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Marianne van der Zwaag
1Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, The University of Groningen, 9713 AV, Groningen, The Netherlands
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Hein Schepers
1Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, The University of Groningen, 9713 AV, Groningen, The Netherlands
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Ellie Eggens-Meijer
1Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, The University of Groningen, 9713 AV, Groningen, The Netherlands
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Bart Kanon
1Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, The University of Groningen, 9713 AV, Groningen, The Netherlands
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Carmen IJsebaart
1Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, The University of Groningen, 9713 AV, Groningen, The Netherlands
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  • ORCID record for Carmen IJsebaart
Jeroen Kuipers
1Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, The University of Groningen, 9713 AV, Groningen, The Netherlands
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Ben N. G. Giepmans
1Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, The University of Groningen, 9713 AV, Groningen, The Netherlands
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Raimundo Freire
2Unidad de Investigación/FIISC, Hospital Universitario de Canarias, Ofra s/n, La Cuesta, 38320 San Cristóbal de La Laguna, Tenerife, Spain
3Instituto de Tecnologías Biomédicas, Universidad de La Laguna, 38200 San Cristóbal de La Laguna, Tenerife, Spain
4Facultad de Ciencias de la Salud, Universidad Fernando Pessoa Canarias, 35450 Las Palmas de Gran Canaria, Spain
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Nicola A. Grzeschik
1Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, The University of Groningen, 9713 AV, Groningen, The Netherlands
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Catherine Rabouille
1Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, The University of Groningen, 9713 AV, Groningen, The Netherlands
5Hubrecht Institute, University of Utrecht, 3584 CT, Utrecht, The Netherlands
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Ody C. M. Sibon
1Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, The University of Groningen, 9713 AV, Groningen, The Netherlands
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  • ORCID record for Ody C. M. Sibon
  • For correspondence: o.c.m.sibon@umcg.nl

Handling Editor: Swathi Arur

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ABSTRACT

Programmed cell death and consecutive removal of cellular remnants is essential for development. During late stages of Drosophila melanogaster oogenesis, the small somatic follicle cells that surround the large nurse cells promote non-apoptotic nurse cell death, subsequently engulf them, and contribute to the timely removal of nurse cell corpses. Here, we identify a role for Vps13 in the timely removal of nurse cell corpses downstream of developmental programmed cell death. Vps13 is an evolutionarily conserved peripheral membrane protein associated with membrane contact sites and lipid transfer. It is expressed in late nurse cells, and persistent nurse cell remnants are observed when Vps13 is depleted from nurse cells but not from follicle cells. Microscopic analysis revealed enrichment of Vps13 in close proximity to the plasma membrane and the endoplasmic reticulum in nurse cells undergoing degradation. Ultrastructural analysis uncovered the presence of an underlying Vps13-dependent membranous structure in close association with the plasma membrane. The newly identified structure and function suggests the presence of a Vps13-dependent process required for complete degradation of bulky remnants of dying cells.

Footnotes

  • Competing interests

    O.C.M.S. is a co-inventor on three patent applications for the use of 4′-phosphopantetheine for Coenzyme A-linked disorders. O.C.M.S. serves as non-compensated executive for the Stichting Lepelaar and the Spoonbill Foundation, two not-for-profit organizations. All other authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: A.I.E.F., N.A.G., C.R., O.C.M.S.; Methodology: A.I.E.F., C.I., M.v.d.Z., H.S., E.E.-M., B.K., J.K., B.N.G.G., R.F., N.A.G.; Validation: A.I.E.F.; Formal analysis: A.I.E.F., C.I., M.v.d.Z., H.S., E.E.-M., B.K., R.F., N.A.G., O.C.M.S.; Investigation: A.I.E.F., C.I., M.v.d.Z., H.S., E.E.-M., B.K., R.F., N.A.G.; Data curation: A.I.E.F.; Writing - original draft: A.I.E.F., C.R., O.C.M.S.; Writing - review & editing: A.I.E.F., H.S., B.N.G.G., N.A.G., O.C.M.S.; Visualization: A.I.E.F., B.N.G.G., N.A.G., C.R.; Supervision: N.A.G., C.R., O.C.M.S.; Project administration: O.C.M.S.; Funding acquisition: O.C.M.S.

  • Funding

    This work was supported by a Nederlandse Organisatie voor Wetenschappelijk Onderzoek VICI grant (865.10.012) and a Nederlandse Organisatie voor Wetenschappelijk Onderzoek ALW Open grant (ALWOP.252) to O.C.M.S.

  • Supplementary information

    Supplementary information available online at https://dev.biologists.org/lookup/doi/10.1242/dev.191759.supplemental

  • Received April 20, 2020.
  • Accepted September 15, 2020.
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Keywords

  • Vps13
  • Programmed cell death (PCD)
  • Oogenesis
  • Endoplasmic reticulum
  • Death cell degradation
  • Membrane contact sites

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RESEARCH ARTICLE
Vps13 is required for timely removal of nurse cell corpses
Anita I. E. Faber, Marianne van der Zwaag, Hein Schepers, Ellie Eggens-Meijer, Bart Kanon, Carmen IJsebaart, Jeroen Kuipers, Ben N. G. Giepmans, Raimundo Freire, Nicola A. Grzeschik, Catherine Rabouille, Ody C. M. Sibon
Development 2020 147: dev191759 doi: 10.1242/dev.191759 Published 29 October 2020
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RESEARCH ARTICLE
Vps13 is required for timely removal of nurse cell corpses
Anita I. E. Faber, Marianne van der Zwaag, Hein Schepers, Ellie Eggens-Meijer, Bart Kanon, Carmen IJsebaart, Jeroen Kuipers, Ben N. G. Giepmans, Raimundo Freire, Nicola A. Grzeschik, Catherine Rabouille, Ody C. M. Sibon
Development 2020 147: dev191759 doi: 10.1242/dev.191759 Published 29 October 2020

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