Cerebrospinal fluid proteomics define the natural history of autosomal dominant Alzheimer’s disease
Open accessAbstract
Alzheimer’s disease (AD) pathology develops many years before the onset of cognitive symptoms. Two pathological processes—aggregation of the amyloid-β (Aβ) peptide into plaques and the microtubule protein tau into neurofibrillary tangles (NFTs)—are hallmarks of the disease. However, other pathological brain processes are thought to be key disease mediators of Aβ plaque and NFT pathology. How these additional pathologies evolve over the course of the disease is currently unknown. Here we show that proteomic measurements in autosomal dominant AD cerebrospinal fluid (CSF) linked to brain protein coexpression can be used to characterize the evolution of AD pathology over a timescale spanning six decades. SMOC1 and SPON1 proteins associated with Aβ plaques were elevated in AD CSF nearly 30 years before the onset of symptoms, followed by changes in synaptic proteins, metabolic proteins, axonal proteins, inflammatory proteins and finally decreases in neurosecretory proteins. The proteome discriminated mutation carriers from noncarriers before symptom onset as well or better than Aβ and tau measures. Our results highlight the multifaceted landscape of AD pathophysiology and its temporal evolution. Such knowledge will be critical for developing precision therapeutic interventions and biomarkers for AD beyond those associated with Aβ and tau.
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Synapse degeneration occurs before neuron loss and long before disease diagnosis.
“Synapse degeneration is an insidious process, occurring before neuron loss and long before disease diagnosis 4,17 .”
From NAD+ hydrolase Sarm1 is a key driver of synapse degeneration and memory loss in Alzheimer’s disease (2025) · cites this paper as [17]
The Results section reports changes in proteins associated with synaptic and neuronal coexpression approximately 26–22 years before expected symptom onset, preceding later markers of neuronal loss. But these early protein changes do not establish synapse degeneration; the paper describes frank synaptic and neuronal loss together at a later stage. It also measures time relative to symptom onset, not disease diagnosis. (LLM, conf=0.84)
Experimental — accuracy not yet measuredAβ disrupts synaptic transmission and induces synapse loss.
“While Aβ disrupts synaptic transmission 32,34,35 and induces synapse loss 17”
From NAD+ hydrolase Sarm1 is a key driver of synapse degeneration and memory loss in Alzheimer’s disease (2025) · cites this paper as [17]
The Results section reports decreases in neuronal and neurosecretory proteins during the course of autosomal dominant Alzheimer’s disease, which the authors interpret as suggesting synaptic and neuronal loss. It does not establish that Aβ induces that loss. The cited paper is attached to the synapse-loss clause; the separate synaptic-transmission clause has other citations. (LLM, conf=0.82)
Experimental — accuracy not yet measured
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Self-citationSymptom onset in autosomal dominant Alzheimer disease A systematic review and meta-analysis
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Self-citationInhibition of endogenous blood glutamate oxaloacetate transaminase enhances the ischemic damage
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Self-citationGlia maturation factor-β: a potential therapeutic target in neurodegeneration and neuroinflammation
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Self-citationAutosomal dominant and sporadic late onset Alzheimer disease share a common in vivo pathophysiology.
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Self-citationLarge‐scale deep proteomic analysis in Alzheimer's disease brain regions across race and ethnicity
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Self-citationA hybrid multimodal machine learning model for Detecting Alzheimer's disease
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Bridging systemic metabolic dysfunction and Alzheimer’s disease: the liver interface
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Alzheimer disease seen through the lens of sex and gender
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Self-citationThe 2024 Report on the Human Proteome from the HUPO Human Proteome Project
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SMOC1 colocalizes with Alzheimer’s disease neuropathology and delays Aβ aggregation
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Heparin-enriched plasma proteome is significantly altered in Alzheimer’s disease
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Self-citationCerebrovascular disease emerges with age and Alzheimer’s disease in adults with Down syndrome
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Self-citationParvalbumin interneuron cell-to-network plasticity: mechanisms and therapeutic avenues
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Proteomic Insight Into Alzheimer's Disease Pathogenesis Pathways
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Self-citationPlasma and cerebrospinal fluid biomarkers in aged dogs with cognitive decline
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Self-citationAre oligodendrocytes the missing link in Alzheimer’s disease and related dementia research?
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Evaluation of the Landscape of Pharmacodynamic Biomarkers in GM1 and GM2 Gangliosidosis
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15 years of longitudinal genetic, clinical, cognitive, imaging, and biochemical measures in DIAN
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Self-citationMulti-Omic Blood Biomarkers as Dynamic Risk Predictors in Late-Onset Alzheimer’s Disease
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- Authors
- Johnson, E. C. B., Bian, S., Haque, R. U., Carter, E. K., Watson, C. M., Gordon, B. A., Ping, L., Duong, D. M., Epstein, M. P., McDade, E., Barthélemy, N. R., Karch, C. M., Xiong, C., Cruchaga, C., Perrin, R. J., Wingo, A. P., Wingo, T. S., Chhatwal, J. P., Day, G. S., Noble, J. M., Berman, S. B., Martins, R., Graff-Radford, N. R., Schofield, P. R., Ikeuchi, T., Mori, H., Levin, J., Farlow, M., Lah, J. J., Haass, C., Jucker, M., Morris, J. C., Benzinger, T. L. S., Roberts, B. R., Bateman, R. J., Fagan, A. M., Seyfried, N. T., Levey, A. I., the Dominantly Inherited Alzheimer Network, Vöglein, J., Allegri, R., Mendez, P. C., Surace, E., Berman, S. B., Ikonomovic, S., Nadkarni, N., Lopera, F., Ramirez, L., Aguillon, D., Leon, Y., Ramos, C., Alzate, D., Baena, A., Londono, N., Moreno, S., Laske, C., Kuder-Buletta, E., Graber-Sultan, S., Preische, O., Hofmann, A., Kasuga, K., Niimi, Y., Ishii, K., Senda, M., Sanchez-Valle, R., Rosa-Neto, P., Fox, N., Cash, D., Lee, J.-H., Roh, J. H., Riddle, M., Menard, W., Bodge, C., Surti, M., Takada, L. T., Sanchez-Gonzalez, V. J., Orozco-Barajas, M., Goate, A., Renton, A., Esposito, B., Marsh, J., Cruchaga, C., Fernandez, V., Jerome, G., Herries, E., Llibre-Guerra, J., Brooks, W., Bechara, J., Hassenstab, J., Franklin, E., Chen, A., Chen, C., Flores, S., Friedrichsen, N., Hantler, N., Hornbeck, R., Jarman, S., Keefe, S., Koudelis, D., Massoumzadeh, P., McCullough, A., McKay, N., Nicklaus, J., Pulizos, C., Wang, Q., Mishall, S., Sabaredzovic, E., Deng, E., Candela, M., Smith, H., Hobbs, D., Scott, J., Wang, P., Xu, X., Li, Y., Gremminger, E., Ma, Y., Bui, R., Lu, R., Ortiz, A. L. S., Daniels, A., Courtney, L., Supnet-Bell, C., Xu, J., & Ringman, J.
- Affiliations
- Emory University (US)
- Washington University in St. Louis (US)
- Brigham and Women's Hospital (US)
- Mayo Clinic in Florida (US)
- Columbia University Irving Medical Center (US)
- Edith Cowan University (AU)
- UNSW Sydney (AU)
- Brain Research Institute, Niigata University (JP)
- Osaka Metropolitan University (JP)
- Ludwig-Maximilians-Universität München (DE)
- Indiana University Bloomington (US)
- German Center for Neurodegenerative Diseases (DE)
- Fundación para la Lucha contra las Enfermedades Neurológicas de la Infancia (AR)
- University of Pittsburgh (US)
- Universidad de Antioquia (CO)
- University of Tokyo Hospital (JP)
- Tokyo Metropolitan Institute of Gerontology (JP)
- Hospital Clínic de Barcelona (ES)
- UK Dementia Research Institute (GB)
- Korea University (KR)
- Brown University (US)
- Universidade de São Paulo (BR)
- Icahn School of Medicine at Mount Sinai (US)
- University of Southern California (US)
- Corresponding author
- Johnson, Erik C. B.
- ORCID
- Johnson, Erik C. B.
- Bian, Shijia
- Haque, Rafi U.
- Carter, E. Kathleen
- Watson, Caroline M.
- Gordon, Brian A.
- Ping, Lingyan
- Duong, Duc M.
- Epstein, Michael P.
- McDade, Eric
- Barthélemy, Nicolas R.
- Karch, Celeste M.
- Xiong, Chengjie
- Perrin, Richard J.
- Wingo, Aliza P.
- Wingo, Thomas S.
- Chhatwal, Jasmeer P.
- Day, Gregory S.
- Noble, James M.
- Martins, Ralph
- Schofield, Peter R.
- Ikeuchi, Takeshi
- Mori, Hiroshi
- Levin, Johannes
- Farlow, Martin
- Lah, James J.
- Haass, Christian
- Jucker, Mathias
- Morris, John C.
- Benzinger, Tammie L. S.
- Roberts, Blaine R.
- Bateman, Randall J.
- Fagan, Anne M.
- Seyfried, Nicholas T.
- Levey, Allan I.
- Vöglein, Jonathan
- Allegri, Ricardo
- Surace, Ezequiel
- Nadkarni, Neelesh
- Lopera, Francisco
- Aguillon, David
- Baena, Ana
- Laske, Christoph
- Kasuga, Kensaku
- Niimi, Yoshiki
- Ishii, Kenji
- Senda, Michio
- Fox, Nick
- Lee, Jae-Hong
- Roh, Jee Hoon
- Riddle, Meghan
- Takada, Leonel Tadao
- Goate, Alison
- Renton, Alan
- Marsh, Jacob
- Brooks, William
- Bechara, Jacob
- Hassenstab, Jason
- Franklin, Erin
- Chen, Allison
- Chen, Charles
- Flores, Shaney
- Hornbeck, Russ
- Keefe, Sarah
- Massoumzadeh, Parinaz
- McCullough, Austin
- McKay, Nicole
- Nicklaus, Joyce
- Wang, Qing
- Deng, Emily
- Smith, Hunter
- Hobbs, Diana
- Scott, Jalen
- Wang, Peter
- Li, Yan
- Ma, Yinjiao
- Bui, Ryan
- Lu, Ruijin
- Daniels, Alisha
- Xu, Jinbin
- Ringman, John
- Venue
- Nature Medicine
- Published
- 2023-08
- Volume
- 29
- Issue
- 8
- Pages
- 1979-1988
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- PMC
- PMC10427428
- OpenAlex
- W4385639069
- Cited by
- 170
- References
- 88
- Citations by year
- 2026: 44 · 2025: 64 · 2024: 55 · 2023: 6
- FWCI
- 30.19
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Nature Medicine (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion, cc-by)
- Open access LMU (Ludwid Maxmilian's Universitat Munchen) (submittedVersion, cc-by)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- DZNE Pub (submittedVersion, cc-by)
- Digital Commons@Becker (Washington University School of Medicine) (submittedVersion, cc-by)
- Australasian Journal of Paramedicine (submittedVersion, cc-by)
- Greater South Information System
- Funders
- Alzheimer's Association (SG-20-690363-DIAN)
- Emory University (U01AG061357)
- Washington University in St. Louis
- Fondation Brain Canada
- Japan Agency for Medical Research and Development (17929884, 22dk0207049h0003)
- Deutsche Forschungsgemeinschaft (HA1737/16‐1, EXC 2145, Koselleck Project HA1737/16-1, EXC 2145SyNergy, 390857198)
- Korea Health Industry Development Institute
- Deutsches Zentrum für Neurodegenerative Erkrankungen
- National Institutes of Health (1s10od025214-01, 1rf1ag071170-01)
- Canadian Institutes of Health Research
- Goizueta Business School, Emory University
- Instituto de Salud Carlos III
- National Institute on Aging (R01AG056533, RF1 AG071170, AG 024904, AG066444, UF1AG032438, U01AG061357, P01AG003991, U19AG032438, K08AG068604, P30AG066444, U19AG024904, R01AG072120, R01AG075827, P01AG026276, P30AG066511)
- National Institute of Neurological Disorders and Stroke (R01NS092865)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Cerebrospinal fluid and hydrocephalus
- Keywords
- autosomal dominant Alzheimer's disease, cerebrospinal fluid proteomics, natural history of disease, amyloid plaques, neurofibrillary tangles, SMOC1, SPON1, presymptomatic biomarkers, mutation carriers, synaptic proteins, neuroinflammation, disease progression
- MeSH terms
- Adult, Alzheimer Disease, Female, Humans, Male, Middle Aged, Mutation, Biomarkers, Osteonectin, Age of Onset, Proteomics
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