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Dystrophic neurites, which surround A\u03b2 plaques and accumulate phosphorylated tau and other proteins, may play a role in seeding and spreading of pathologic tau. Here, we investigate the novel hypothesis that improved membrane repair capacity decreases dystrophic neurite formation by protecting axons from A\u03b2-induced membrane damage. Using a ratiometric calcium sensor and a FRET-based calpain cleavage sensor, we demonstrate that dystrophic neurites in 5XFAD mice have elevated resting calcium levels and calpain activity because of putative membrane damage. Annexin A6, a plasma membrane repair in muscle and neurons, is present at plasma membrane of neurons and dystrophic neurites in murine and human brains. Overexpression of annexin A6 in brains of 5XFAD mice decreased size and quantity of dystrophic neurites and accumulation of phospho-tau181, an early biomarker of amyloid pathology. Phospho-tau231, another early amyloid biomarker, and phosphorylated of tau kinases, c-jun N-terminal\u00a0kinase (JNK) and Calmodulin Kinase II (CaMKII) accumulate in dystrophic neurites in the brains of amyloid pathology mice and humans with AD, suggesting that dystrophic neurites are sites of active tau phosphorylation. Overexpression of dominant-negative annexin A6 in 5XFAD mice increased dystrophic neurites and phospho-tau181. Intracerebral injection of recombinant annexin A6 in 5XFAD and APP-NLGF knock-in mice resulted in localization of recombinant A6 to membranes of dystrophic neurites, suggesting therapeutic potential of recombinant annexin A6 for AD. In conclusion, dystrophic neurites have A\u03b2-induced membrane damage characterized by calcium elevation, calpain activation, and accumulation of tau kinases and phosphorylated tau. Overexpression of annexin A6 reduces dystrophic neurites and phospho-tau accumulation, suggesting that annexin A6-mediated membrane repair may represent a novel therapeutic approach for AD.<\/jats:p>","DOI":"10.1007\/s00401-025-02888-1","type":"journal-article","created":{"date-parts":[[2025,5,24]],"date-time":"2025-05-24T02:37:04Z","timestamp":1748054224000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Annexin A6 membrane repair protein protects against amyloid-induced dystrophic neurites and tau phosphorylation in Alzheimer\u2019s disease model mice"],"prefix":"10.1007","volume":"149","author":[{"given":"Katherine R.","family":"Sadleir","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karen P.","family":"Gomez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Abigail E.","family":"Edwards","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Armana J.","family":"Patel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Makenna L.","family":"Ley","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ammaarah W.","family":"Khatri","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joanna","family":"Guo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shreya","family":"Mahesh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elyse A.","family":"Watkins","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jelena","family":"Popovic","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Devi Krishna Priya","family":"Karunakaran","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dmitry","family":"Prokopenko","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rudolph E.","family":"Tanzi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bernabe","family":"Bustos","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Steven J.","family":"Lubbe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexis R.","family":"Demonbruen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elizabeth M.","family":"McNally","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert","family":"Vassar","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2025,5,24]]},"reference":[{"key":"2888_CR1","unstructured":"(2023) The Alzheimer\u2019s Association, Alzheimer\u2019s Disease: Facts and Figures https:\/\/www.alz.org\/alzheimers-dementia\/facts-figures"},{"key":"2888_CR2","doi-asserted-by":"publisher","first-page":"1717","DOI":"10.1001\/jama.2021.3854","volume":"325","author":"GC Alexander","year":"2021","unstructured":"Alexander GC, Emerson S, Kesselheim AS (2021) Evaluation of aducanumab for alzheimer disease: scientific evidence and regulatory review involving efficacy, safety, and futility. 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