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Title: Autophagic Degradation of the 26S Proteasome Is Mediated by the Dual ATG8/Ubiquitin Receptor RPN10 in Arabidopsis

Abstract

Autophagic turnover of intracellular constituents is critical for cellular housekeeping, nutrient recycling, and various aspects of growth and development in eukaryotes. In this paper, we show that autophagy impacts the other major degradative route involving the ubiquitin-proteasome system by eliminating 26S proteasomes, a process we termed proteaphagy. Using Arabidopsis proteasomes tagged with GFP, we observed their deposition into vacuoles via a route requiring components of the autophagy machinery. This transport can be initiated separately by nitrogen starvation and chemical or genetic inhibition of the proteasome, implying distinct induction mechanisms. Proteasome inhibition stimulates comprehensive ubiquitylation of the complex, with the ensuing proteaphagy requiring the proteasome subunit RPN10, which can simultaneously bind both ATG8 and ubiquitin. Finally and collectively, we propose that Arabidopsis RPN10 acts as a selective autophagy receptor that targets inactive 26S proteasomes by concurrent interactions with ubiquitylated proteasome subunits/targets and lipidated ATG8 lining the enveloping autophagic membranes.

Authors:
; ; ; ;
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1259320
Alternate Identifier(s):
OSTI ID: 1250268; OSTI ID: 1344491
Grant/Contract Number:  
FG02-88ER13968
Resource Type:
Published Article
Journal Name:
Molecular Cell
Additional Journal Information:
Journal Name: Molecular Cell Journal Volume: 58 Journal Issue: 6; Journal ID: ISSN 1097-2765
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Marshall, Richard S., Li, Faqiang, Gemperline, David C., Book, Adam J., and Vierstra, Richard D. Autophagic Degradation of the 26S Proteasome Is Mediated by the Dual ATG8/Ubiquitin Receptor RPN10 in Arabidopsis. United States: N. p., 2015. Web. doi:10.1016/j.molcel.2015.04.023.
Marshall, Richard S., Li, Faqiang, Gemperline, David C., Book, Adam J., & Vierstra, Richard D. Autophagic Degradation of the 26S Proteasome Is Mediated by the Dual ATG8/Ubiquitin Receptor RPN10 in Arabidopsis. United States. doi:10.1016/j.molcel.2015.04.023.
Marshall, Richard S., Li, Faqiang, Gemperline, David C., Book, Adam J., and Vierstra, Richard D. Mon . "Autophagic Degradation of the 26S Proteasome Is Mediated by the Dual ATG8/Ubiquitin Receptor RPN10 in Arabidopsis". United States. doi:10.1016/j.molcel.2015.04.023.
@article{osti_1259320,
title = {Autophagic Degradation of the 26S Proteasome Is Mediated by the Dual ATG8/Ubiquitin Receptor RPN10 in Arabidopsis},
author = {Marshall, Richard S. and Li, Faqiang and Gemperline, David C. and Book, Adam J. and Vierstra, Richard D.},
abstractNote = {Autophagic turnover of intracellular constituents is critical for cellular housekeeping, nutrient recycling, and various aspects of growth and development in eukaryotes. In this paper, we show that autophagy impacts the other major degradative route involving the ubiquitin-proteasome system by eliminating 26S proteasomes, a process we termed proteaphagy. Using Arabidopsis proteasomes tagged with GFP, we observed their deposition into vacuoles via a route requiring components of the autophagy machinery. This transport can be initiated separately by nitrogen starvation and chemical or genetic inhibition of the proteasome, implying distinct induction mechanisms. Proteasome inhibition stimulates comprehensive ubiquitylation of the complex, with the ensuing proteaphagy requiring the proteasome subunit RPN10, which can simultaneously bind both ATG8 and ubiquitin. Finally and collectively, we propose that Arabidopsis RPN10 acts as a selective autophagy receptor that targets inactive 26S proteasomes by concurrent interactions with ubiquitylated proteasome subunits/targets and lipidated ATG8 lining the enveloping autophagic membranes.},
doi = {10.1016/j.molcel.2015.04.023},
journal = {Molecular Cell},
number = 6,
volume = 58,
place = {United States},
year = {2015},
month = {6}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1016/j.molcel.2015.04.023

Citation Metrics:
Cited by: 57 works
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Works referencing / citing this record:

A facile forward-genetic screen for Arabidopsis autophagy mutants reveals twenty-one loss-of-function mutations disrupting six ATG genes
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Actin filaments are dispensable for bulk autophagy in plants
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Understanding and exploiting autophagy signaling in plants
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  • Batoko, Henri; Dagdas, Yasin; Baluska, Frantisek
  • Essays in Biochemistry, Vol. 61, Issue 6
  • DOI: 10.1042/ebc20170034

Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition)
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Dehydrin MtCAS31 promotes autophagic degradation under drought stress
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Autophagy in Plant: A New Orchestrator in the Regulation of the Phytohormones Homeostasis
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  • Gou, Wentao; Li, Xi; Guo, Shaoying
  • International Journal of Molecular Sciences, Vol. 20, Issue 12
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Cellular Responses to Proteasome Inhibition: Molecular Mechanisms and Beyond
journal, July 2019

  • Albornoz, Nicolas; Bustamante, Hianara; Soza, Andrea
  • International Journal of Molecular Sciences, Vol. 20, Issue 14
  • DOI: 10.3390/ijms20143379

Understanding and exploiting autophagy signaling in plants
journal, December 2017

  • Batoko, Henri; Dagdas, Yasin; Baluska, Frantisek
  • Essays in Biochemistry, Vol. 61, Issue 6
  • DOI: 10.1042/ebc20170034

Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition)
journal, January 2016


A facile forward-genetic screen for Arabidopsis autophagy mutants reveals twenty-one loss-of-function mutations disrupting six ATG genes
journal, February 2019


Actin filaments are dispensable for bulk autophagy in plants
journal, March 2019


Dehydrin MtCAS31 promotes autophagic degradation under drought stress
journal, July 2019


All roads lead to the vacuole—autophagic transport as part of the endomembrane trafficking network in plants
journal, November 2017

  • Kalinowska, Kamila; Isono, Erika
  • Journal of Experimental Botany, Vol. 69, Issue 6
  • DOI: 10.1093/jxb/erx395

Tuning the proteasome to brighten the end of the journey
journal, November 2016

  • Mayor, Thibault; Sharon, Michal; Glickman, Michael H.
  • American Journal of Physiology-Cell Physiology, Vol. 311, Issue 5
  • DOI: 10.1152/ajpcell.00198.2016

The Role and Regulation of Autophagy and the Proteasome During Aging and Senescence in Plants
journal, April 2019


Autophagy in Plant: A New Orchestrator in the Regulation of the Phytohormones Homeostasis
journal, June 2019

  • Gou, Wentao; Li, Xi; Guo, Shaoying
  • International Journal of Molecular Sciences, Vol. 20, Issue 12
  • DOI: 10.3390/ijms20122900

Cellular Responses to Proteasome Inhibition: Molecular Mechanisms and Beyond
journal, July 2019

  • Albornoz, Nicolas; Bustamante, Hianara; Soza, Andrea
  • International Journal of Molecular Sciences, Vol. 20, Issue 14
  • DOI: 10.3390/ijms20143379

Functional characterization of EI24-induced autophagy in the degradation of RING-domain E3 ligases
journal, August 2016