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Whether and how PSGs and SV2 may coordinate other proteins for BoNT\/A recruitment and internalization remains unknown. Here, we demonstrate that the targeted endocytosis of BoNT\/A into synaptic vesicles (SVs) requires a tripartite surface nanocluster. Live\u2010cell super\u2010resolution imaging and electron microscopy of catalytically inactivated BoNT\/A wildtype and receptor\u2010binding\u2010deficient mutants in cultured hippocampal neurons demonstrated that BoNT\/A must bind coincidentally to a PSG and SV2 to target synaptic vesicles. We reveal that BoNT\/A simultaneously interacts with a preassembled PSG\u2010synaptotagmin\u20101 (Syt1) complex and SV2 on the neuronal plasma membrane, facilitating Syt1\u2010SV2 nanoclustering that controls endocytic sorting of the toxin into synaptic vesicles. Syt1 CRISPRi knockdown suppressed BoNT\/A\u2010 and BoNT\/E\u2010induced neurointoxication as quantified by SNAP\u201025 cleavage, suggesting that this tripartite nanocluster may be a unifying entry point for selected botulinum neurotoxins that hijack this for synaptic vesicle targeting.<\/jats:p>","DOI":"10.15252\/embj.2022112095","type":"journal-article","created":{"date-parts":[[2023,5,25]],"date-time":"2023-05-25T06:00:21Z","timestamp":1684994421000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":35,"title":["Presynaptic targeting of botulinum neurotoxin type A requires a tripartite PSG\u2010Syt1\u2010SV2 plasma membrane nanocluster for synaptic vesicle entry"],"prefix":"10.1038","volume":"42","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4533-0455","authenticated-orcid":false,"given":"Merja","family":"Joensuu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7025-7037","authenticated-orcid":false,"given":"Parnayan","family":"Syed","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1296-2023","authenticated-orcid":false,"given":"Saber H","family":"Saber","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2572-1774","authenticated-orcid":false,"given":"Vanessa","family":"Lanoue","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tristan P","family":"Wallis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James","family":"Rae","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4666-9255","authenticated-orcid":false,"given":"Ailisa","family":"Blum","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1604-0253","authenticated-orcid":false,"given":"Rachel S","family":"Gormal","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christopher","family":"Small","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shanley","family":"Sanders","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7495-1875","authenticated-orcid":false,"given":"Anmin","family":"Jiang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stefan","family":"Mahrhold","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nadja","family":"Krez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1762-160X","authenticated-orcid":false,"given":"Michael A","family":"Cousin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruby","family":"Cooper\u2010White","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Justin J","family":"Cooper\u2010White","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6070-3774","authenticated-orcid":false,"given":"Brett M","family":"Collins","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7494-5248","authenticated-orcid":false,"given":"Robert G","family":"Parton","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Giuseppe","family":"Balistreri","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0645-1641","authenticated-orcid":false,"given":"Andreas","family":"Rummel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6400-1107","authenticated-orcid":false,"given":"Fr\u00e9d\u00e9ric A","family":"Meunier","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2023,5,25]]},"reference":[{"key":"BFEMBJ2022112095_CR1","doi-asserted-by":"crossref","first-page":"858","DOI":"10.1016\/j.bbamcr.2014.11.014","volume":"1853","author":"S Aigal","year":"2015","unstructured":"Aigal S, Claudinon J, Romer W (2015) Plasma membrane reorganization: a glycolipid gateway for microbes. 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