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Phosphoribosyl ubiquitination of SNARE proteins regulates autophagy during Legionella infection

Title: Phosphoribosyl ubiquitination of SNARE proteins regulates autophagy during Legionella infection
Authors: Mukherjee,Rukmini; Bhattacharya,Anshu; Tomaskovic,Ines; Mello-Vieira,João; Brunstein,Melinda Elaine; Başoğlu,Marion; Veenendaal, Tineke; Bailey,Henry; Colby,Thomas; Misra,Mohit; Eimer,Stefan; Klumperman, Judith; Münch,Christian; Matic,Ivan; Dikic,Ivan; CMM Groep Klumperman; Cancer; CMM Sectie Celbiologie; Brain; Regenerative Medicine and Stem Cells
Publication Year: 2025
Subject Terms: Autophagy; Legionella pneumophila; Syntaxin17; Ubiquitin; Xenophagy; General Neuroscience; Molecular Biology; General Biochemistry,Genetics and Molecular Biology; General Immunology and Microbiology; Journal Article
Description: Legionella pneumophila is an intracellular pathogen that causes Legionnaires' disease. The bacteria release effector proteins, some of which remodel host autophagic-lysosomal pathways. One such effector is RavZ, which delipidates ATG8 proteins, making compromising autophagy in Legionella-infected cells. Here we show that SidE effectors also affect these pathways, by mediating phosphoribosyl-ubiquitination (PR-Ub) of the autophagic SNARE proteins STX17 and SNAP29. STX17 modification induces recruitment of STX17-positive membranes from the endoplasmic reticulum to Legionella-containing phagosomes, forming replicative vacuoles. Using proximity labeling, biochemistry and Legionella infection studies, we define a mechanism by which autophagy is hijacked by bacteria to recruit ER membranes to the bacterial vacuole, via a structure bearing autophagy markers but not fusing with lysosomes. Mass-spectrometric identification of PR-Ub sites and mutational studies show that phosphoribosyl-ubiquitination of STX17 alters its interaction with ATG14L, which causes ER membranes to be recruited to the bacterial vacuole in a PI3K-dependent manner. On the other hand, phosphoribosyl-ubiquitination of SNAP29 inhibits the formation of the autophagosomal SNARE complex (STX17-SNAP29-VAMP8) via steric hindrance, thus preventing the fusion of bacterial vacuoles with lysosomes.
Document Type: article in journal/newspaper
File Description: application/pdf
Language: English
ISSN: 0261-4189
Relation: https://dspace.library.uu.nl/handle/1874/466556
Availability: https://dspace.library.uu.nl/handle/1874/466556
Rights: info:eu-repo/semantics/OpenAccess
Accession Number: edsbas.1BD5585
Database: BASE