ESCRT machinery mediates selective microautophagy of endoplasmic reticulum

Schäfer, Jasmin; Schessner, Julia; Bircham, Peter W.; Funaya, Charlotta; Schaeff, Katharina; Ruffini, Giulia; Papagiannidis, Dimitrios; Knop, Michael; Fujimoto, Toyoshi; Schuck, Sebastian

doi:10.1101/661306

Cited by 9 publications

(7 citation statements)

References 76 publications

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“…Moreover, it may enable therapeutic intervention in diseases associated with ER overload and aberrant lipid metabolism, such as diabetes and obesity. Besides organelle biogenesis, lipin activity impacts autophagy, axon regeneration, myopathy, dystonia, and neurodegeneration (Zhang et al , 2014; Grillet et al , 2016; Zhang & Reue, 2017; Fanning et al , 2019; Yang et al , 2019; Schäfer et al , 2020). Further unraveling the regulation of lipin will therefore have implications for a large variety of cellular processes and associated diseases.…”

Section: Discussionmentioning

confidence: 99%

Ice2 promotes ER membrane biogenesis in yeast by inhibiting the conserved lipin phosphatase complex

et al. 2021

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Cells dynamically adapt organelle size to current physiological demand. Organelle growth requires membrane biogenesis and therefore needs to be coordinated with lipid metabolism. The endoplasmic reticulum (ER) can undergo massive expansion, but the underlying regulatory mechanisms are largely unclear. Here, we describe a genetic screen for factors involved in ER membrane expansion in budding yeast and identify the ER transmembrane protein Ice2 as a strong hit. We show that Ice2 promotes ER membrane biogenesis by opposing the phosphatidic acid phosphatase Pah1, called lipin in metazoa. Specifically, Ice2 inhibits the conserved Nem1-Spo7 complex and thus suppresses the dephosphorylation and activation of Pah1. Furthermore, Ice2 cooperates with the transcriptional regulation of lipid synthesis genes and helps to maintain cell homeostasis during ER stress. These findings establish the control of the lipin phosphatase complex as an important mechanism for regulating ER membrane biogenesis.

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Section: Discussionmentioning

confidence: 99%

Ice2 promotes ER membrane biogenesis in yeast by inhibiting the conserved lipin phosphatase complex

et al. 2021

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“…In general, MVB is involved in nonselective autophagy. Recent studies have determined that MVBs can also participate in selective autophagy processes, such as the Cvt (cytoplasm‐to‐vacuole targeting) pathway and ER‐phagy (Huang et al ., 2014; Schafer et al ., 2020). The study found that the homologue of mammalian autophagy receptor NBR1‐Nbr1 interacts with two cytoplasmic hydrolases, Lap2 and Ape2, in a similar way to that observed in the Cvt signalling pathway and promotes their transport to the vacuole in yeast, which is called NVT (Nbr1‐mediated vacuolar targeting).…”

Section: Introductionmentioning

confidence: 99%

“…NVT elements colocalize with ESCRTs in multivesicular bodies (MVBs) and rely on ubiquitination for transport (Liu et al ., 2015). In yeast, the deletion of ESCRT‐0, ‐I, ‐II or ‐III protein, Bro1 or Vps4 can reduce or block endoplasmic reticulum autophagy (Schafer et al ., 2020).…”

Section: Introductionmentioning

confidence: 99%

Endosomal sorting complexes required for transport‐0 (ESCRT‐0) are essential for fungal development, pathogenicity, autophagy and ER‐phagy in Magnaporthe oryzae

Sun

Qian

Liu

et al. 2021

Environmental Microbiology

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Magnaporthe oryzae is an important plant pathogen that causes rice blast. Hse1 and Vps27 are components of ESCRT-0 involved in the multivesicular body (MVB) sorting pathway and biogenesis. To date, the biological functions of ESCRT-0 in M. oryzae have not been determined. In this study, we identified and characterized Hse1 and Vps27 in M. oryzae. Disruption of MoHse1 and MoVps27 caused pleiotropic defects in growth, conidiation, sexual development and pathogenicity, thereby resulting in loss of virulence in rice and barley leaves. Disruption of MoHse1 and MoVps27 triggered increased lipidation of MoAtg8 and degradation of GFP-MoAtg8, indicating that ESCRT-0 is involved in the regulation of autophagy. ESCRT-0 was determined to interact with coat protein complex II (COPII), a regulator functioning in homeostasis of the endoplasmic reticulum (ER homeostasis), and disruption of MoHse1 and MoVps27 also blocked activation of the unfolded protein response (UPR) and autophagy of the endoplasmic reticulum (ER-phagy). Overall, our results indicate that ESCRT-0 plays critical roles in regulating fungal development, virulence, autophagy and ER-phagy in M. oryzae.

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“…ESCRT is involved in various cellular processes, including cytokinesis, plasma membrane repair, nuclear membrane repair, multivesicular body formation, vacuolar membrane repair, autophagosome formation, and microautophagy of the endoplasmic reticulum (11, 27, 28). Here, we find ESCRT in our screen for PMD response factors.…”

Section: Discussionmentioning

confidence: 99%

Plasma membrane damage limits replicative lifespan in yeast and induces premature senescence in human fibroblasts

Kono

Johmura

Moriyama

et al. 2021

Preprint

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Plasma membrane damage (PMD) occurs in all cell types due to environmental perturbation and cell-autonomous activities. However, cellular outcomes of PMD remain largely unknown except for recovery or death. Here, using yeast and human fibroblasts, we show that cellular senescence, irreversible cell cycle arrest contributing to organismal aging, is the third outcome of PMD. To identify the genes essential for PMD response, we performed a systematic yeast genome-wide screen. The screen identified 48 genes. The top hits in the screen are the endosomal sorting complexes required for transport (ESCRT) genes. Strikingly, the replicative lifespan regulator genes are enriched in our 48 hits, and indeed, PMD limits the replicative lifespan in budding yeast; the ESCRT activator AAA-ATPase VPS4-overexpression extends it. In normal human fibroblasts, PMD induces cellular senescence via p53. Our study demonstrates that PMD limits replicative lifespan in two different eukaryotic cell types and highlights an underappreciated but ubiquitous senescent cell subtype, namely PMD-dependent senescent cells.

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ESCRT machinery mediates selective microautophagy of endoplasmic reticulum

Cited by 9 publications

References 76 publications

Ice2 promotes ER membrane biogenesis in yeast by inhibiting the conserved lipin phosphatase complex

Ice2 promotes ER membrane biogenesis in yeast by inhibiting the conserved lipin phosphatase complex

Endosomal sorting complexes required for transport‐0 (ESCRT‐0) are essential for fungal development, pathogenicity, autophagy and ER‐phagy in Magnaporthe oryzae

Plasma membrane damage limits replicative lifespan in yeast and induces premature senescence in human fibroblasts

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