Btn3 regulates the endosomal sorting function of the yeast Ent3 epsin, an adaptor for SNARE proteins

Morvan, Joëlle; Craene, Johan-Owen De; Rinaldi, Bruno; Addis, Vanessa; Misslin, Cédric; Friant, Sylvie

doi:10.1242/jcs.159699

Cited by 10 publications

(7 citation statements)

References 44 publications

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“…We find that Can1 transits through the TGN both in the presence and absence of glucose, and that TGN‐localised clathrin adaptors are important for vacuolar protein sorting in response to glucose (Can1, Mup1, Tat1, and Tat2) and substrate (Can1, Mup1). These findings are consistent with prior reports about the loss of the Gga proteins or their co‐factors on post‐endocytic traffic to the vacuole of plasma membrane proteins such as Tat1, Ste3, Fur4, Jen1, and Gap1 (Scott et al., 2004; Sipos et al., 2004; Becuwe and Leon, 2014; Morvan et al., 2015). The mechanistic explanation of these prior observations was initially unclear.…”

Section: Discussionsupporting

confidence: 92%

Plasma membrane to vacuole traffic induced by glucose starvation requires Gga2‐dependent sorting at the trans‐Golgi network

Buelto

Hung

Aoh

et al. 2020

Biology of the Cell

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Background Information. In the yeast Saccharomyces cerevisiae, acute glucose starvation induces rapid endocytosis followed by vacuolar degradation of many plasma membrane proteins. This process is essential for cell viability, but the regulatory mechanisms that control it remain poorly understood. Under normal growth conditions, a major regulatory decision for endocytic cargo occurs at the trans-Golgi network (TGN) where proteins can recycle back to the plasma membrane or can be recognized by TGN-localised clathrin adaptors that direct them towards the vacuole. However, glucose starvation reduces recycling and alters the localization and post-translational modification of TGN-localised clathrin adaptors. This raises the possibility that during glucose starvation endocytosed proteins are routed to the vacuole by a novel mechanism that bypasses the TGN or does not require TGN-localised clathrin adaptors. Results. Here, we investigate the role of TGN-localised clathrin adaptors in the traffic of several amino acid permeases, including Can1, during glucose starvation. We find that Can1 transits through the TGN after endocytosis in both starved and normal conditions. Can1 and other amino acid permeases require TGN-localised clathrin adaptors for maximal delivery to the vacuole. Furthermore, these permeases are actively sorted to the vacuole, because ectopically forced de-ubiquitination at the TGN results in the recycling of the Tat1 permase in starved cells. Finally, we report that the Mup1 permease requires the clathrin adaptor Gga2 for vacuolar delivery. In contrast, the clathrin adaptor protein complex AP-1 plays a minor role, potentially in retaining permeases in the TGN, but it is otherwise dispensable for vacuolar delivery. Conclusions and significance. This work elucidates one membrane trafficking pathway needed for yeast to respond to acute glucose starvation. It also reveals the functions of TGNlocalised clathrin adaptors in this process. Our results indicate that the same machinery is needed for vacuolar protein sorting at the GN in glucose starved cells as is needed in the presence of glucose. In addition, our findings provide further support for the model that the TGN is a transit point for many endocytosed proteins, and that Gga2 and AP-1 function in distinct pathways at the TGN.

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Section: Discussionsupporting

confidence: 92%

Plasma membrane to vacuole traffic induced by glucose starvation requires Gga2‐dependent sorting at the trans‐Golgi network

Buelto

Hung

Aoh

et al. 2020

Biology of the Cell

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“…Impaired membrane transport in the inner membrane system can be manifested as changes in the PM lipid organization and/or defects in the pH control. However, Apl2 and Apl1, subunits of the adaptor complexes AP-1 and AP-2, respectively, had little contribution to the void zone formation, presumably because these mutants had insignificant disruption of the membrane trafficking compared to the effects of ent3Δ, ent5Δ and gga1Δ gga2Δ (Yeung et al, 1999;Sakane et al, 2006;Morvan et al, 2015). Deletion of APL5, which encodes the subunit of AP-3 responsible for the transport from the Golgi to the vacuole (Dell'Angelica, 2009), slightly reduced void zone formation, suggesting the importance of the vacuolar functions for void zone formation.…”

Section: Identification Of the Genes Required For The Formation Of The Void Zonementioning

confidence: 99%

Characterization of micron-scale protein-depleted plasma membrane domains in phosphatidylserine-deficient yeast cells

Mioka

Gao

Wang

et al. 2021

Journal of Cell Science

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Membrane phase separation to form micron-scale domains of lipids and proteins occurs in artificial membranes; however, a similar large-scale phase separation has not been reported in the plasma membrane of the living cells. We show here that a stable micron-scale protein-depleted region is generated in the plasma membrane of yeast mutants lacking phosphatidylserine at high temperatures. We named this region the ‘void zone’. Transmembrane proteins and certain peripheral membrane proteins and phospholipids are excluded from the void zone. The void zone is rich in ergosterol, and requires ergosterol and sphingolipids for its formation. Such properties are also found in the cholesterol-enriched domains of phase-separated artificial membranes, but the void zone is a novel membrane domain that requires energy and various cellular functions for its formation. The formation of the void zone indicates that the plasma membrane in living cells has the potential to undergo phase separation with certain lipid compositions. We also found that void zones were frequently in contact with vacuoles, in which a membrane domain was also formed at the contact site.

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“…Impaired membrane transport in the inner membrane system can be manifested as the changes in the plasma membrane lipid organization and/or defects in the pH control. However, Apl2 and Apl1, the subunits of the adaptor complexes AP-1 and AP-2, respectively, had little contribution to the void zone formation presumably because these mutants had insignificant disruption of the membrane trafficking compared to the effects of ent3 Δ, ent5 Δ and gga1 Δ gga2 Δ (Yeung et al, 1999; Sakane et al, 2006; Morvan et al, 2015). Deletion of APL5 , which encodes the subunit of AP-3 responsible for the transport from the Golgi to the vacuole (Dell’Angelica, 2009), slightly reduced the void zone formation, suggesting the importance of the vacuolar functions for the void zone formation.…”

Section: Resultsmentioning

confidence: 99%

Phosphatidylserine prevents the generation of a protein-free giant plasma membrane domain in yeast

Mioka

Gao

Wang

et al. 2020

Preprint

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Membrane phase separation accompanied with micron-scale domains of lipids and proteins occurs in artificial membranes; however, a similar large phase separation has not been reported in the plasma membrane of the living cells. We demonstrate here that a stable micron-scale protein-free region is generated in the plasma membrane of the yeast mutants lacking phosphatidylserine. We named this region the ″void zone″. Transmembrane proteins, peripheral membrane proteins, and certain phospholipids are excluded from the void zone. The void zone is rich in ergosterol and requires ergosterol and sphingolipids for its formation. These characteristics of the void zone are similar to the properties of the liquid-ordered domain caused by phase separation. We propose that phosphatidylserine prevents the formation of the void zone by preferentially interacting with ergosterol. We also found that void zones were frequently in contact with vacuoles, in which a membrane domain was also formed at the contact site.

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Btn3 regulates the endosomal sorting function of the yeast Ent3 epsin, an adaptor for SNARE proteins

Cited by 10 publications

References 44 publications

Plasma membrane to vacuole traffic induced by glucose starvation requires Gga2‐dependent sorting at the trans‐Golgi network

Plasma membrane to vacuole traffic induced by glucose starvation requires Gga2‐dependent sorting at the trans‐Golgi network

Characterization of micron-scale protein-depleted plasma membrane domains in phosphatidylserine-deficient yeast cells

Phosphatidylserine prevents the generation of a protein-free giant plasma membrane domain in yeast

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