eLife (Aug 2020)
A cross-kingdom conserved ER-phagy receptor maintains endoplasmic reticulum homeostasis during stress
- Madlen Stephani,
- Lorenzo Picchianti,
- Alexander Gajic,
- Rebecca Beveridge,
- Emilio Skarwan,
- Victor Sanchez de Medina Hernandez,
- Azadeh Mohseni,
- Marion Clavel,
- Yonglun Zeng,
- Christin Naumann,
- Mateusz Matuszkiewicz,
- Eleonora Turco,
- Christian Loefke,
- Baiying Li,
- Gerhard Dürnberger,
- Michael Schutzbier,
- Hsiao Tieh Chen,
- Alibek Abdrakhmanov,
- Adriana Savova,
- Khong-Sam Chia,
- Armin Djamei,
- Irene Schaffner,
- Steffen Abel,
- Liwen Jiang,
- Karl Mechtler,
- Fumiyo Ikeda,
- Sascha Martens,
- Tim Clausen,
- Yasin Dagdas
Affiliations
- Madlen Stephani
- ORCiD
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria
- Lorenzo Picchianti
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria; Research Institute of Molecular Pathology (IMP), Vienna BioCenter (VBC), Vienna, Austria
- Alexander Gajic
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria
- Rebecca Beveridge
- Research Institute of Molecular Pathology (IMP), Vienna BioCenter (VBC), Vienna, Austria
- Emilio Skarwan
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria
- Victor Sanchez de Medina Hernandez
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria
- Azadeh Mohseni
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria
- Marion Clavel
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria
- Yonglun Zeng
- School of Life Sciences, Centre for Cell and Developmental Biology and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, School of Life Sciences, New Territories, Shatin, China
- Christin Naumann
- Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, Halle, Germany
- Mateusz Matuszkiewicz
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria; Department of Plant Genetics, Breeding and Biotechnology, Warsaw University of Life Sciences-SGGW, Warsaw, Poland
- Eleonora Turco
- Department of Biochemistry and Cell Biology, Max Perutz Labs, University of Vienna, Vienna BioCenter (VBC), Vienna, Austria
- Christian Loefke
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria
- Baiying Li
- School of Life Sciences, Centre for Cell and Developmental Biology and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, School of Life Sciences, New Territories, Shatin, China
- Gerhard Dürnberger
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria; Research Institute of Molecular Pathology (IMP), Vienna BioCenter (VBC), Vienna, Austria
- Michael Schutzbier
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria; Research Institute of Molecular Pathology (IMP), Vienna BioCenter (VBC), Vienna, Austria
- Hsiao Tieh Chen
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria; School of Life Sciences, Centre for Cell and Developmental Biology and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, School of Life Sciences, New Territories, Shatin, China
- Alibek Abdrakhmanov
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria
- Adriana Savova
- Department of Biochemistry and Cell Biology, Max Perutz Labs, University of Vienna, Vienna BioCenter (VBC), Vienna, Austria
- Khong-Sam Chia
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria
- Armin Djamei
- ORCiD
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria
- Irene Schaffner
- BOKU Core Facility Biomolecular & Cellular Analysis, University of Natural Resources and Life Sciences, Vienna, Austria
- Steffen Abel
- Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, Halle, Germany
- Liwen Jiang
- School of Life Sciences, Centre for Cell and Developmental Biology and State Key Laboratory of Agrobiotechnology, The Chinese University of Hong Kong, School of Life Sciences, New Territories, Shatin, China
- Karl Mechtler
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria; Research Institute of Molecular Pathology (IMP), Vienna BioCenter (VBC), Vienna, Austria
- Fumiyo Ikeda
- ORCiD
- Department of Molecular and Cellular Biology, Medical Institute of Bioregulation, Kyushu University, Fukuoka, Japan; Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna BioCenter (VBC), Vienna, Austria
- Sascha Martens
- ORCiD
- Department of Biochemistry and Cell Biology, Max Perutz Labs, University of Vienna, Vienna BioCenter (VBC), Vienna, Austria
- Tim Clausen
- ORCiD
- Research Institute of Molecular Pathology (IMP), Vienna BioCenter (VBC), Vienna, Austria; Medical University of Vienna, Vienna, Austria
- Yasin Dagdas
- ORCiD
- Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna BioCenter (VBC), Vienna, Austria
- DOI
- https://doi.org/10.7554/eLife.58396
- Journal volume & issue
-
Vol. 9
Abstract
Eukaryotes have evolved various quality control mechanisms to promote proteostasis in the endoplasmic reticulum (ER). Selective removal of certain ER domains via autophagy (termed as ER-phagy) has emerged as a major quality control mechanism. However, the degree to which ER-phagy is employed by other branches of ER-quality control remains largely elusive. Here, we identify a cytosolic protein, C53, that is specifically recruited to autophagosomes during ER-stress, in both plant and mammalian cells. C53 interacts with ATG8 via a distinct binding epitope, featuring a shuffled ATG8 interacting motif (sAIM). C53 senses proteotoxic stress in the ER lumen by forming a tripartite receptor complex with the ER-associated ufmylation ligase UFL1 and its membrane adaptor DDRGK1. The C53/UFL1/DDRGK1 receptor complex is activated by stalled ribosomes and induces the degradation of internal or passenger proteins in the ER. Consistently, the C53 receptor complex and ufmylation mutants are highly susceptible to ER stress. Thus, C53 forms an ancient quality control pathway that bridges selective autophagy with ribosome-associated quality control in the ER.
Keywords
- selective autophagy
- er-phagy
- er-quality control
- ribosome stalling
- cargo receptor
- marchantia polymorpha