Proteomic identification of specifically carbonylated brain proteins in APPNLh/APPNLh×PS-1P264L/PS-1P264L human double mutant knock-in mice model of Alzheimer disease as a function of age
Open accessAbstract
Alzheimer disease (AD) is the most common type of dementia and is characterized pathologically by the presence of neurofibrillary tangles (NFTs), senile plaques (SPs), and loss of synapses. The main component of SP is amyloid-beta peptide (Aβ), a 39 to 43 amino acid peptide, generated by the proteolytic cleavage of amyloid precursor protein (APP) by the action of beta- and gamma-secretases. The presenilins (PS) are components of the γ-secretase, which contains the protease active center. Mutations in PS enhance the production of the Aβ42 peptide. To date, more than 160 mutations in PS1 have been identified. Many PS mutations increase the production of the β-secretase-mediated C-terminal (CT) 99 amino acid-long fragment (CT99), which is subsequently cleaved by γ-secretase to yield Aβ peptides. Aβ has been proposed to induce oxidative stress and neurotoxicity. Previous studies from our laboratory and others showed an age-dependent increase in oxidative stress markers, loss of lipid asymmetry, and Aβ production and amyloid deposition in the brain of APP/PS1 mice. In the present study, we used APP (NLh)/APP(NLh) × PS-1(P246L)/PS-1(P246L) human double mutant knock-in APP/PS-1 mice to identify specific targets of brain protein carbonylation in an age-dependent manner. We found a number of proteins that are oxidatively modified in APP/PS1 mice compared to age-matched controls. The relevance of the identified proteins to the progression and pathogenesis of AD is discussed.
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ATP synthase is carbonylated in vivo by Aβ, significantly modified by HNE in MCI hippocampus and IPL, early AD IPL, and late AD IPL, and significantly nitrated in late AD hippocampus.
“The carbonylation of ATP synthase is induced in vivo by Aβ [73], and it is significantly modified by HNE in MCI hippocampus and IPL [56], early AD IPL [55], and late AD IPL [54] in addition to being significantly nitrated in late AD hippocampus [57].”
From Mitochondrial Oxidative and Nitrosative Stress and Alzheimer Disease (2020) · cites this paper as [73]
The Results and Discussion (page unavailable) report significant oxidation of ATP synthase α-chain in the knock-in mice at 12 and 15 months, when brain Aβ levels were higher. But the paper says this only suggests Aβ contributes to oxidation and explicitly calls the proposed route to ATP synthase carbonylation speculative; it does not establish that Aβ induces it in vivo. The HNE and nitration findings in the citing sentence are attached to other citations, not this source. (LLM, conf=0.87)
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Abdul, H. M., Rukhsana Sultana, A., Clair, D. K. S., Markesbery, W. R., & Butterfield, D. A. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2008.08.012 · Cited by 81 · see citing works
Self-citationOxidative inactivation of the proteasome in Alzheimer's disease
Cecarini, V., Ding, Q., & Keller, J. N. (2007) · Free Radical Research · doi:10.1080/10715760701286159 · Cited by 79 · see citing works
Increased cerebrospinal fluid cAMP levels in Alzheimer's disease
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Glucose intolerance, cognitive impairment and Alzheimer’s disease
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Rethinking Alzheimer's Disease Therapy: Are Mitochondria the Key?
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Increased cerebrospinal fluid pyruvate levels in Alzheimer's disease
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Neurabin Contributes to Hippocampal Long-Term Potentiation and Contextual Fear Memory
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Debra Boyd-kimball, A., Rukhsana Sultana, A., Poon, H. F., Abdul, H. M., Lynn, B. C., Klein, J. B., & Butterfield, D. A. (2005) · Journal of Neuroscience Research · doi:10.1002/jnr.20393 · Cited by 50 · see citing works
Self-citationLange, M. L. B., Clair, D. K. S., Markesbery, W. R., Studzinski, C. M., Murphy, M. P., & Butterfield, D. A. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2010.01.004 · Cited by 41 · see citing works
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Anti–γ-Enolase Autoimmune Retinopathy Manifesting in Early Childhood
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Butterfield, D. A., & Boyd-Kimball, D. (2018) · Journal of Alzheimer’s Disease · doi:10.3233/jad-170543 · Cited by 403 · see citing works
Self-citationButterfield, D. A. (2014) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2014.06.006 · Cited by 126 · see citing works
Self-citationRedox proteomics and amyloid β-peptide: Insights into Alzheimer disease
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Self-citationMitochondrial Oxidative and Nitrosative Stress and Alzheimer Disease
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“The carbonylation of ATP synthase is induced in vivo by Aβ [73], and it is significantly modified by HNE in MCI hippocampus and IPL [56], early AD IPL [55], and late AD IPL [54] in addition to being significantly nitrated in late AD hippocampus [57].”
BackgroundSelf-citationShen, L., Chen, C., Yang, A., Chen, Y., Liu, Q., & Ni, J. (2015) · Journal of Proteomics · doi:10.1016/j.jprot.2015.04.005 · Cited by 73 · see citing works
Zaręba-Kozioł, M., Szwajda, A., Dadlez, M., Wysłouch-Cieszyńska, A., & Lalowski, M. (2014) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m113.036079 · Cited by 39 · see citing works
- Authors
- Sultana, R., Robinson, R. A. S., Di Domenico, F., Abdul, H. M., Clair, D. K. S., Markesbery, W. R., Cai, J., Pierce, W. M., & Butterfield, D. A.
- Affiliations
- University of Kentucky (US)
- University of Louisville (US)
- Corresponding author
- Butterfield, D. Allan
- Venue
- Journal of Proteomics
- Publisher
- Elsevier BV
- Published
- 2011-10
- Volume
- 74
- Issue
- 11
- Pages
- 2430-2440
- ISSN
- 1874-3919 (ISSN-L)
- PMC
- PMC3199338
- OpenAlex
- W2090857379
- Cited by
- 41
- References
- 102
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 2 · 2023: 2 · 2021: 2 · 2020: 7 · 2018: 2 · 2016: 3 · 2015: 5 · 2014: 4 · 2013: 6 · 2012: 3
- FWCI
- 3.06
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Journal of Proteomics (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- IRIS Research product catalog (Sapienza University of Rome) (submittedVersion)
- Funders
- National Institute on Aging (P30AG028383, P01AG005119, R37AG013939, T32AG000260, P01AG021184, R01AG020243, AG0 5119, R01AG013939)
- National Institute of General Medical Sciences (R25GM067071)
- National Institute of Neurological Disorders and Stroke (R01NS064247)
- 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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Keywords
- Alzheimer's disease, protein carbonylation, oxidative stress, amyloid-beta, gamma-secretase, presenilin, brain proteome, lipid asymmetry, neurofibrillary tangles, amyloid plaques
- MeSH terms
- Age Factors, Alzheimer Disease, Animals, Brain, Brain Chemistry, Disease Models, Animal, Humans, Leucine, Male, Mice, Transgenic, Nerve Tissue Proteins, Proline, Amyloid beta-Protein Precursor, Protein Structure, Tertiary, Amino Acid Substitution, Proteomics, Protein Carbonylation, Mice, Presenilin-1, Gene Knock-In Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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