Change in Cerebrospinal Fluid Tau Microtubule Binding Region Detects Symptom Onset, Cognitive Decline, Tangles, and Atrophy in Dominantly Inherited Alzheimer's Disease

and the Dominantly Inherited Alzheimer Network, Kanta Horie, Yan Li, Nicolas Barthelemy, Brian Gordon, Jason Hassenstab, Tammie Benzinger, Anne Niven, John Morris, Celeste M. Karch, Chengjie Xiong, Ricardo Allegri, Patricio Chrem Mendez, Takeshi Ikeuchi, Kensaku Kasuga, James Noble, Martin Farlow, Jasmeer Chhatwal, Gregory Day, Peter R. SchofieldColin L. Masters, Johannes Levin, Mathias Jucker, Jae Hong Lee, Jee Hoon Roh, Chihiro Sato, Pallavi Sachdev, Akihiko Koyama, Larisa Reyderman, Randall J. Bateman, Eric McDade

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

Objective: Identifying cerebrospinal fluid measures of the microtubule binding region of tau (MTBR-tau) species that reflect tau aggregation could provide fluid biomarkers that track Alzheimer's disease related neurofibrillary tau pathological changes. We examined the cerebrospinal fluid (CSF) MTBR-tau species in dominantly inherited Alzheimer's disease (DIAD) mutation carriers to assess the association with Alzheimer's disease (AD) biomarkers and clinical symptoms. Methods: Cross-sectional and longitudinal CSF from 229 DIAD mutation carriers and 130 mutation non-carriers had sequential characterization of N-terminal/mid-domain phosphorylated tau (p-tau) followed by MTBR-tau species and tau positron emission tomography (tau PET), other soluble tau and amyloid biomarkers, comprehensive clinical and cognitive assessments, and brain magnetic resonance imaging of atrophy. Results: CSF MTBR-tau species located within the putative “border” region and one species corresponding to the “core” region of aggregates in neurofibrillary tangles (NFTs) increased during the presymptomatic stage and decreased during the symptomatic stage. The “border” MTBR-tau species were associated with amyloid pathology and CSF p-tau; whereas the “core” MTBR-tau species were associated stronger with tau PET and CSF measures of neurodegeneration. The ratio of the border to the core species provided a continuous measure of increasing amounts that tracked clinical progression and NFTs. Interpretation: Changes in CSF soluble MTBR-tau species preceded the onset of dementia, tau tangle increase, and atrophy in DIAD. The ratio of 4R-specific MTBR-tau (border) to the NFT (core) MTBR-tau species corresponds to the pathology of NFTs in DIAD and change with disease progression. The dynamics between different MTBR-tau species in the CSF may serve as a marker of tau-related disease progression and target engagement of anti-tau therapeutics. ANN NEUROL 2023;93:1158–1172.

Original languageEnglish
Pages (from-to)1158-1172
Number of pages15
JournalAnnals of neurology
Volume93
Issue number6
DOIs
StatePublished - Jun 2023

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