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A conserved membrane curvature-generating protein is crucial for autophagosome formation in fission yeast

Author

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  • Ning Wang

    (Harvard Medical School)

  • Yoko Shibata

    (Harvard Medical School)

  • Joao A. Paulo

    (Harvard Medical School)

  • Steven P. Gygi

    (Harvard Medical School)

  • Tom A. Rapoport

    (Harvard Medical School)

Abstract

Organelles are shaped by curvature-generating proteins, which include the reticulons and REEPs that are involved in forming the endoplasmic reticulum (ER). A conserved REEP subfamily differs from the ER-shaping REEPs in abundance and membrane topology and has unidentified functions. Here, we show that Rop1, the single member of this family in the fission yeast Schizosacharomyces pombe, is crucial for the macroautophagy of organelles and cytosolic proteins. Rop1 is needed for the formation of phagophores, cup-like structures consisting of two closely apposed membrane sheets that encapsulate cargo. It is recruited at early stages to phagophores and is required for their maturation into autophagosomes. Rop1 function relies on its ability to generate high membrane curvature and on its colocalization with the autophagy component Atg2 that is thought to reside at the phagophore rim. We propose that Rop1 facilitates the formation and growth of the double-membrane structure of the autophagosome.

Suggested Citation

  • Ning Wang & Yoko Shibata & Joao A. Paulo & Steven P. Gygi & Tom A. Rapoport, 2023. "A conserved membrane curvature-generating protein is crucial for autophagosome formation in fission yeast," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40530-4
    DOI: 10.1038/s41467-023-40530-4
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    References listed on IDEAS

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    1. Keisuke Mochida & Yu Oikawa & Yayoi Kimura & Hiromi Kirisako & Hisashi Hirano & Yoshinori Ohsumi & Hitoshi Nakatogawa, 2015. "Receptor-mediated selective autophagy degrades the endoplasmic reticulum and the nucleus," Nature, Nature, vol. 522(7556), pages 359-362, June.
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    3. Ning Wang & Lindsay D. Clark & Yuan Gao & Michael M. Kozlov & Tom Shemesh & Tom A. Rapoport, 2021. "Mechanism of membrane-curvature generation by ER-tubule shaping proteins," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    4. Keisuke Mochida & Akinori Yamasaki & Kazuaki Matoba & Hiromi Kirisako & Nobuo N. Noda & Hitoshi Nakatogawa, 2020. "Super-assembly of ER-phagy receptor Atg40 induces local ER remodeling at contacts with forming autophagosomal membranes," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    5. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
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    1. Yoko Shibata & Emily E. Mazur & Buyan Pan & Joao A. Paulo & Steven P. Gygi & Suyog Chavan & L. Sebastian Alexis Valerio & Jiuchun Zhang & Tom A. Rapoport, 2024. "The membrane curvature-inducing REEP1-4 proteins generate an ER-derived vesicular compartment," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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