The Deubiquitinating Enzyme AMSH1 and the ESCRT-III Subunit VPS2.1 Are Required for Autophagic Degradation in<i>Arabidopsis</i>

Katsiarimpa, Anthi; Kalinowska, Kamila; Anzenberger, Franziska; Weis, Corina; Ostertag, M.; Tsutsumi, Chie; Schwechheimer, Claus; Brunner, Frédéric; Hückelhoven, Ralph; Isono, Erika

doi:10.1105/tpc.113.113399

Cited by 114 publications

(97 citation statements)

References 81 publications

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“…In mammalian cells, it has been found that autophagosomes can either fuse directly with lysosomes or fuse first with endosomes to form intermediate compartments called amphisomes, which subsequently fuse with the lysosome (6). In plants, the exact role of MVBs in autophagy remains elusive, even though a recent report has demonstrated a requirement for ESCRT-III in autophagic degradation (13). Because FREE1 is essential for the proper formation of MVBs, it is likely that loss of FREE1 might inhibit either the fusion of autophagosomes with MVBs or the fusion of amphisomes with vacuoles.…”

Section: Free1 Depletion Increases the Association Between Autophagosmentioning

confidence: 99%

“…New light has been thrown onto this situation through the discovery that ESCRT is also involved in autophagy. More and more studies on nematodes, flies, mammals, and even on plants provide evidence to support the conclusion that the inactivation of ESCRT machinery causes an accumulation of autophagosomes (9)(10)(11)(12)(13). Different models, such as the induction of autophagy or the disruption of autophagosome-endosome/lysosome fusion, have been proposed to explain the observation that autophagosomes accumulate in ESCRT-depleted cells (14,15).…”

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Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation

Gao

Zhuang

Cui

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

180

166

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Protein turnover can be achieved via the lysosome/vacuole and the autophagic degradation pathways. Evidence has accumulated revealing that efficient autophagic degradation requires functional endosomal sorting complex required for transport (ESCRT) machinery. However, the interplay between the ESCRT machinery and the autophagy regulator remains unclear. Here, we show that FYVE domain protein required for endosomal sorting 1 (FREE1), a recently identified plant-specific ESCRT component essential for multivesicular body (MVB) biogenesis and plant growth, plays roles both in vacuolar protein transport and autophagic degradation. FREE1 also regulates vacuole biogenesis in both seeds and vegetative cells of Arabidopsis. Additionally, FREE1 interacts directly with a unique plant autophagy regulator SH3 DOMAIN-CONTAINING PROTEIN2 and associates with the PI3K complex, to regulate the autophagic degradation in plants. Thus, FREE1 plays multiple functional roles in vacuolar protein trafficking and organelle biogenesis as well as in autophagic degradation via a previously unidentified regulatory mechanism of cross-talk between the ESCRT machinery and autophagy process. T he endosomal-lysosomal/vacuolar pathway is the primary catabolic system of eukaryotic cells that degrades extracellular and intracellular materials. Membrane proteins destined for degradation, such as misfolded proteins or endocytosed receptors, become tagged by ubiquitin for further sorting to the endosomal-lysosomal/vacuolar system for degradation (1). During this process, an evolutionarily conserved machinery called endosomal sorting complex required for transport (ESCRT), is responsible for sorting these ubiquitinated cargos into the intraluminal vesicles (ILVs) of prevacuolar compartments/multivesicular bodies (PVCs/MVBs), which subsequently fuse with vacuoles/lysosomes to deliver their contents into the lumen for proteolytic degradation (2, 3). Malfunction of the assembly or dissociation of the ESCRT machinery disrupts MVB formation and thus results in the accumulation of ubiquitinated membrane cargos (4, 5).Macroautophagy (hereafter as autophagy) is another highly conserved catabolic process, which converges on the endosomallysosomal/vacuolar pathway to deliver aberrant organelles, longlived proteins, and protein aggregates to the lysosome/vacuole via a unique structure termed the "autophagosome" (6). Morphologically different from MVBs, autophagosomes are characterized by a double membrane structure, which is initiated from the phagophore assembly site/preautophagosome site (PAS) (7). The proteins or organelles to be degraded are encapsulated by autophagosomes that fuse either directly with the vacuole/lysosome or with endosomes like MVBs for expansion/maturation to form amphisomes, which then fuse with vacuole/lysosome for degradation. A number of conserved autophagy-related gene (ATG) proteins have been identified as participating in the autophagy pathway in eukaryotic cells (8).Even though it is generally accepted that at least one population of...

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Section: Free1 Depletion Increases the Association Between Autophagosmentioning

confidence: 99%

mentioning

confidence: 95%

Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation

Gao

Zhuang

Cui

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

180

166

View full text Add to dashboard Cite

show abstract

“…One of these complexes, ESCRT-III, associates directly with endosomal membranes and is thought to mediate changes in the membrane architecture that ultimately lead to intraluminal vesicle scission (Schuh and Audhya, 2014). Studies with Drosophila melanogaster, Caenorhabditis elegans, plants, and mammalian cells showing that ESCRT mutants hyperaccumulate autophagosomes (Roudier et al, 2005;Filimonenko et al, 2007;Lee et al, 2007;Rusten et al, 2007;Rusten and Stenmark, 2009;Djeddi et al, 2012;Katsiarimpa et al, 2013) implied that the ESCRT machinery plays a role in autophagy. Given that the scission of nascent intraluminal vesicles at endosomes and the closure of phagophores into sealed autophagosomes are topologically similar, ESCRT proteins could participate directly in phagophore closure.…”

Section: Introductionmentioning

confidence: 99%

The Endosomal Protein CHARGED MULTIVESICULAR BODY PROTEIN1 Regulates the Autophagic Turnover of Plastids in Arabidopsis

et al. 2015

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Endosomal Sorting Complex Required for Transport (ESCRT)-III proteins mediate membrane remodeling and the release of endosomal intraluminal vesicles into multivesicular bodies. Here, we show that the ESCRT-III subunit paralogs CHARGED MULTIVESICULAR BODY PROTEIN1 (CHMP1A) and CHMP1B are required for autophagic degradation of plastid proteins in Arabidopsis thaliana. Similar to autophagy mutants, chmp1a chmp1b (chmp1) plants hyperaccumulated plastid components, including proteins involved in plastid division. The autophagy machinery directed the release of bodies containing plastid material into the cytoplasm, whereas CHMP1A and B were required for delivery of these bodies to the vacuole. Autophagy was upregulated in chmp1 as indicated by an increase in vacuolar green fluorescent protein (GFP) cleavage from the autophagic reporter GFP-ATG8. However, autophagic degradation of the stromal cargo RECA-GFP was drastically reduced in the chmp1 plants upon starvation, suggesting that CHMP1 mediates the efficient delivery of autophagic plastid cargo to the vacuole. Consistent with the compromised degradation of plastid proteins, chmp1 plastids show severe morphological defects and aberrant division. We propose that CHMP1 plays a direct role in the autophagic turnover of plastid constituents.

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“…The induction and conjugation machineries leading to ATG8 lipidation have been characterized 3 [35][36][37][38] , the different steps of the autophagic pathway are not resolved. Moreover, little information is presently available on the morphology of early autophagosomal structures 34 , and the subcellular distribution of the ATG5 complex or the site of autophagosome formation are currently unknown.…”

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confidence: 99%

ATG5 defines a phagophore domain connected to the endoplasmic reticulum during autophagosome formation in plants

Bars

Marion

Borgne³

et al. 2014

Nat Commun

126

103

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Autophagosomes are the organelles responsible for macroautophagy and arise, in yeast and animals, from the sealing of a cup-shaped double-membrane precursor, the phagophore. How the phagophore is generated and grows into a sealed autophagosome is still not clear in detail, and unknown in plants. This is due, in part, to the scarcity of structurally informative, real-time imaging data of the required protein machinery at the phagophore formation site. Here we find that in intact living Arabidopsis tissue, autophagy-related protein ATG5, which is essential for autophagosome formation, is present at the phagophore site from early, sub-resolution stages and later defines a torus-shaped structure on a flat cisternal early phagophore. Movement and expansion of this structure are accompanied by the underlying endoplasmic reticulum, suggesting tight connections between the two compartments. Detailed real-time and 3D imaging of the growing phagophore are leveraged to propose a model for autophagosome formation in plants.

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The Deubiquitinating Enzyme AMSH1 and the ESCRT-III Subunit VPS2.1 Are Required for Autophagic Degradation inArabidopsis

Cited by 114 publications

References 81 publications

Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation

Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation

The Endosomal Protein CHARGED MULTIVESICULAR BODY PROTEIN1 Regulates the Autophagic Turnover of Plastids in Arabidopsis

ATG5 defines a phagophore domain connected to the endoplasmic reticulum during autophagosome formation in plants

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