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We studied cholera toxin (CTx), which invades the ER and activates IRE1\u03b1 in host cells, to understand how unfolded proteins are recognized. Proximity labeling colocalized the enzymatic and metastable A1 segment of CTx (CTxA1) with IRE1\u03b1 in live cells, where we also found that CTx-induced IRE1\u03b1 activation enhanced toxicity. In vitro, CTxA1 bound the IRE1\u03b1 lumenal domain (IRE1\u03b1LD), but global unfolding was not required. Rather, the IRE1\u03b1LD recognized a seven-residue motif within an edge \u03b2-strand of CTxA1 that must locally unfold for binding. Binding mapped to a pocket on IRE1\u03b1LD normally occupied by a segment of the IRE1\u03b1 C-terminal flexible loop implicated in IRE1\u03b1 oligomerization. Mutation of the CTxA1 recognition motif blocked CTx-induced IRE1\u03b1 activation in live cells, thus linking the binding event with IRE1\u03b1 signal transduction and induction of the UPR.<\/jats:p>","DOI":"10.1083\/jcb.202402062","type":"journal-article","created":{"date-parts":[[2024,3,21]],"date-time":"2024-03-21T02:21:27Z","timestamp":1710987687000},"update-policy":"https:\/\/doi.org\/10.1083\/jcb.crossmarkpolicy","source":"Crossref","is-referenced-by-count":9,"title":["IRE1\u03b1 recognizes a structural motif in cholera toxin to activate an unfolded protein response"],"prefix":"10.1083","volume":"223","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0133-7209","authenticated-orcid":true,"given":"Mariska S.","family":"Simpson","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/00dvg7y05","id-type":"ROR","asserted-by":"publisher"}],"name":"Boston Children\u2019s Hospital 1 Division of Gastroenterology, Hepatology and Nutrition, , Boston MA, USA"},{"name":"Utrecht 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