Network Analysis of a Membrane-Enriched Brain Proteome across Stages of Alzheimer’s Disease
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Previous systems-based proteomic approaches have characterized alterations in protein co-expression networks of unfractionated asymptomatic (AsymAD) and symptomatic Alzheimer’s disease (AD) brains. However, it remains unclear how sample fractionation and sub-proteomic analysis influences the organization of these protein networks and their relationship to clinicopathological traits of disease. In this proof-of-concept study, we performed a systems-based sub-proteomic analysis of membrane-enriched post-mortem brain samples from pathology-free control, AsymAD, and AD brains (n = 6 per group). Label-free mass spectrometry based on peptide ion intensity was used to quantify the 18 membrane-enriched fractions. Differential expression and weighted protein co-expression network analysis (WPCNA) were then used to identify and characterize modules of co-expressed proteins most significantly altered between the groups. We identified a total of 27 modules of co-expressed membrane-associated proteins. In contrast to the unfractionated proteome, these networks did not map strongly to cell-type specific markers. Instead, these modules were principally organized by their associations with a wide variety of membrane-bound compartments and organelles. Of these, the mitochondrion was associated with the greatest number of modules, followed by modules linked to the cell surface compartment. In addition, we resolved networks with strong associations to the endoplasmic reticulum, Golgi apparatus, and other membrane-bound organelles. A total of 14 of the 27 modules demonstrated significant correlations with clinical and pathological AD phenotypes. These results revealed that the proteins within individual compartments feature a heterogeneous array of AD-associated expression patterns, particularly during the preclinical stages of disease. In conclusion, this systems-based analysis of the membrane-associated AsymAD brain proteome yielded a unique network organization highly linked to cellular compartmentalization. Further study of this membrane-associated proteome may reveal novel insight into the complex pathways governing the earliest stages of disease.
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Nearly a dozen network-based analyses of the AD proteome have been performed in the human brain, including the dorsolateral prefrontal cortex, temporal cortex, and other cortical regions heavily affected in AD.
“Nearly a dozen informative network-based analyses of the AD proteome have been performed in the human brain [62–64, 74, 78, 96, 104–108], including the dorsolateral prefrontal cortex (DLPFC), temporal cortex, and other cortical regions heavily affected in AD.”
From Systems-based proteomics to resolve the biology of Alzheimer’s disease beyond amyloid and tau (2021) · cites this paper as [105]
The global AD network proteome consistently demonstrates progressive downregulation of synaptic modules in asymptomatic and symptomatic AD brains, preserved across various cortical brain regions.
“This is reflected in the global AD network proteome, which consistently demonstrates the progressive downregulation of synaptic modules in asymptomatic and symptomatic AD brains, a finding that appears to be preserved across various cortical brain regions [62, 96, 105].”
From Systems-based proteomics to resolve the biology of Alzheimer’s disease beyond amyloid and tau (2021) · cites this paper as [105]
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Rathore, S., Dammer, E. B., Shantaraman, A., Wu, F., Duong, D. M., Fox, E. J., Johnson, E. C. B., Lah, J. J., Initiative, A. D. N., Seyfried, N. T., et al. (2025) · medRxiv · doi:10.1101/2025.10.24.25337921 · Cited by 1 · see citing works
Self-citationNeuroproteomics: How a Multitude of Proteins Reflect Brain Functions
Гомазков, О. А. (2021) · Biology Bulletin Reviews · doi:10.1134/s2079086421020043
Zlatic, S. A., Dammer, E. B., Crocker, A. J., Duong, D. M., Selfridge, J., Gadalla, K. K. E., Gokhale, A., Tobin, B. R., Wood, L. B., Zandl‐Lang, M., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.30.673242
Self-citationShantaraman, A., Dammer, E. B., Ugochukwu, O., Duong, D. M., Yin, L., Carter, E. K., Gearing, M., Chen-Plotkin, A., Lee, E. B., Trojanowski, J. Q., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26758102
Self-citationShantaraman, A., Dammer, E. B., Ugochukwu, O., Duong, D. M., Yin, L., Carter, E. K., Gearing, M., Chen-Plotkin, A., Lee, E. B., Trojanowski, J. Q., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26507275
Self-citationShantaraman, A., Dammer, E. B., Ugochukwu, O., Duong, D. M., Yin, L., Carter, E. K., Gearing, M., Chen-Plotkin, A., Lee, E. B., Trojanowski, J. Q., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26507230
Self-citationShantaraman, A., Dammer, E. B., Ugochukwu, O., Duong, D. M., Yin, L., Carter, E. K., Gearing, M., Chen-Plotkin, A., Lee, E. B., Trojanowski, J. Q., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26758099
Self-citation
- Authors
- Higginbotham, L., Dammer, E., Duong, D., Modeste, E., Montine, T., Lah, J., Levey, A., & Seyfried, N.
- Affiliations
- Emory University (US)
- Stanford Medicine (US)
- Corresponding author
- Seyfried, Nicholas
- ORCID
- Venue
- Proteomes
- Publisher
- MDPI AG
- Published
- 2019-08-27
- Volume
- 7
- Issue
- 3
- Pages
- 30
- ISSN
- 2227-7382 (ISSN-L)
- PMC
- PMC6789842
- OpenAlex
- W2970123842
- Cited by
- 32
- References
- 49
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 8 · 2023: 3 · 2022: 4 · 2021: 5 · 2020: 5
- FWCI
- 2.40
- Type
- journal article
- Language
- en
- Open access
- gold
- dx.doi.org
- Licence
- Locations
- Proteomes (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institute on Aging (R01AG053960, R01AG061800)
- National Instiute on Aging (R01AG057911)
- Accelerating Medicine Partnership for AD (U01AG046161)
- Emory Alzheimer's Disease Research Center (P50AG025688)
- NINDS Emory Neuroscience Core (P30NS055077)
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Keywords
- Alzheimer's disease, preclinical Alzheimer's disease, protein co-expression networks, postmortem brain, sample fractionation, mitochondrial proteins, cell surface proteins, membrane-bound organelles, endoplasmic reticulum, Golgi apparatus, differentially expressed proteins
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