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Establishment of the phagophore–ERES membrane contact site initiates phagophore elongation

Rubén Gómez‐Sánchez, Sabrina Chumpen Ramirez, Prado Vargas Duarte, Yan Hu, Muriel Mari, Katharina Olschewski, Ralph Hardenberg, J. Christopher Fromme, Christian Ungermann, Fulvio Reggiori

2025Nature Structural & Molecular Biology11 citationsDOIOpen Access PDF

Abstract

The de novo generation of membrane contact sites (MCSs) between the phagophore and the endoplasmic reticulum exit sites (ERES) is important for the acquisition of the lipids necessary for phagophore elongation and autophagosome formation during autophagy. However, it is currently unclear how these MCSs are established. Here, we show that the TRAPPIII complex, the guanine nucleotide exchange factor of the Rab GTPase Ypt1, localizes to and regulates the formation of the MCS between the phagophore and the ERES. In particular, TRAPPIII and the lipid transfer protein Atg2 appear equally essential for the association of the phagophore with the ERES, TRAPPIII activation and Ypt1 activation onto the phagophore. Ypt1 redistributes over the entire surface of the phagophore and promotes its elongation through both stimulation of the local biosynthesis of phosphatidylinositol-3-phosphate and recruitment of the downstream effectors Atg18 and Atg21. Our data suggest that de novo generation of the phagophore–ER MCSs and subsequent Ypt1 activation initiates phagophore elongation. Gómez-Sánchez et al. show that generation of phagophore–endoplasmic reticulum exit sites (ERES) membrane contact sites, mediated by Atg2 and the TRAPPIII complex, triggers Ypt1 activation, which is a signal to initiate phagophore elongation.

Topics & Concepts

Cell biologyAutophagosomeRabGTPaseAutophagyEndoplasmic reticulumGuanine nucleotide exchange factorSmall GTPaseBiologyChemistrySignal transductionBiochemistryApoptosisAutophagy in Disease and TherapyCellular transport and secretionEndoplasmic Reticulum Stress and Disease
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