The DOI matches its Crossref record; 109 of the 111 references it cites were found in a registry or an index.
Reduction in mitochondrial superoxide dismutase modulates Alzheimer’s disease-like pathology and accelerates the onset of behavioral changes in human amyloid precursor protein transgenic mice
Open accessAbstract
Alzheimer's disease (AD) is associated with accumulations of amyloid-beta (Abeta) peptides, oxidative damage, mitochondrial dysfunction, neurodegeneration, and dementia. The mitochondrial antioxidant manganese superoxide dismutase-2 (Sod2) might protect against these alterations. To test this hypothesis, we inactivated one Sod2 allele (Sod2(+/-)) in human amyloid precursor protein (hAPP) transgenic mice, reducing Sod2 activity to approximately 50% of that in Sod2 wild-type (Sod2(+/+)) mice. A reduction in Sod2 activity did not obviously impair mice without hAPP/Abeta expression. In hAPP mice, however, it accelerated the onset of behavioral alterations and of deficits in prepulse inhibition of acoustic startle, a measure of sensorimotor gating. In these mice, it also worsened hAPP/Abeta-dependent depletion of microtubule-associated protein 2, a marker of neuronal dendrites. Sod2 reduction decreased amyloid plaques in the brain parenchyma but promoted the development of cerebrovascular amyloidosis, gliosis, and plaque-independent neuritic dystrophy. Sod2 reduction also increased the DNA binding activity of the transcription factor nuclear factor kappaB. These results suggest that Sod2 protects the aging brain against hAPP/Abeta-induced impairments. Whereas reductions in Sod2 would be expected to trigger or exacerbate neuronal and vascular pathology in AD, increasing Sod2 activity might be of therapeutic benefit.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“preserves synaptic integrity”
From The mitochondria-targeted antioxidant MitoQ prevents loss of spatial memory retention and early neuropathology in a transgenic mouse model of Alzheimer’s disease (2011) · cites this paper as Esposito et al., 2006
In the citing paper
“eliminates the earliest cognitive deficits in a transgenic mouse AD model”
From The mitochondria-targeted antioxidant MitoQ prevents loss of spatial memory retention and early neuropathology in a transgenic mouse model of Alzheimer’s disease (2011) · cites this paper as Esposito et al., 2006
In the citing paper
“reduction of mitochondrial superoxide dismutase (MnSOD) levels accelerates AD-like pathology in a transgenic mouse model of AD”
From The mitochondria-targeted antioxidant MitoQ prevents loss of spatial memory retention and early neuropathology in a transgenic mouse model of Alzheimer’s disease (2011) · cites this paper as Esposito et al., 2006
In the citing paper
“overexpression of MnSOD decreases Aβ-processing”
From The mitochondria-targeted antioxidant MitoQ prevents loss of spatial memory retention and early neuropathology in a transgenic mouse model of Alzheimer’s disease (2011) · cites this paper as Esposito et al., 2006
In the citing paper
“Elevated SOD expression is indicative of the high levels of oxidative stress associated with Aβ plaques in Alzheimer’s disease brains [21,48,80,104].”
From Centella Asiatica Improves Memory and Promotes Antioxidative Signaling in 5XFAD Mice (2019) · cites this paper as [104]
Citations
Cites
Free radicals in biology and medicine
Gutteridge, J. M. C. (1991) · General Pharmacology The Vascular System · doi:10.1016/0306-3623(91)90478-o · Cited by 17,178
Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat
Pellow, S., Chopin, P., File, S. E., & Briley, M. (1985) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(85)90031-7 · Cited by 5,822
Free radicals in biology and medicine
Halliwell, B. B., & Gutteridge, J. M. C. (1985) · Journal of Free Radicals in Biology & Medicine · doi:10.1016/0748-5514(85)90140-0 · Cited by 2,938
The use of a plus-maze to measure anxiety in the mouse
Lister, R. G. (1987) · Psychopharmacology · doi:10.1007/bf00177912 · Cited by 2,617
Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein
Games, D., Adams, D., Alessandrini, R., Barbour, R., Borthelette, P., Blackwell, C., Carr, T., Clemens, J., Donaldson, T., Gillespie, F., et al. (1995) · Nature · doi:10.1038/373523a0 · Cited by 2,516
Self-citationMucke, L., Masliah, E., Yu, G.-Q., Mallory, M., Rockenstein, E. M., Tatsuno, G., Hu, K., Kholodenko, D., Johnson-Wood, K., & McConlogue, L. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04050.2000 · Cited by 1,856
Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective
Tanzi, R. E., & Bertram, L. (2005) · Cell · doi:10.1016/j.cell.2005.02.008 · Cited by 1,849
Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase
Li, Y., Huang, T.-T., Carlson, E. J., Melov, S., Ursell, P. C., Olson, J. L., Noble, L. J., Yoshimura, M. P., Berger, C., Chan, P. H., et al. (1995) · Nature Genetics · doi:10.1038/ng1295-376 · Cited by 1,789
Frequency of Stages of Alzheimer-Related Lesions in Different Age Categories
Braak, H., & Braak, E. (1997) · Neurobiology of Aging · doi:10.1016/s0197-4580(97)00056-0 · Cited by 1,656
Mitochondrial abnormalities in Alzheimer's disease
Hirai, K., Aliev, G., Nunomura, A., Fujioka, H., Russell, R. L., Atwood, C. S., Johnson, A. B., Kress, Y., Vinters, H. V., Tabaton, M., et al. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-09-03017.2001 · Cited by 1,367
Flagged first, then by citations
2 of the 111 references couldn’t be matched to a known paper.
Research works printed but not linked: 10
- 10.1172/JCI200523269 · DOI · Paper page
- (1995), Mol Pharmacol, 48, 825
- (2003), Behav Pharmacol, 14, 419
- (1987), Psychopharmacology, 92, 180
- (1993), Am J Pathol, 142, 871
- (2000), CMAJ, 162, 65
- (1989), Prog Clin Biol Res, 317, 781
- (2000), Nature, 404, 352
- (1994), Mol Cell Biol, 14, 7377
- (1999), Ann NY Acad Sci, 903, 317
Cited by
Sorted by citations
Items 201–254 of 254
Memory Recovery Effect of a New Bioactive Innovative Combination in Rats with Experimental Dementia
Tancheva, L. P., Kalfin, R. E., Minchev, B., Uzunova, D. N., Tasheva, K. N., Tsvetanova, E. R., Georgieva, A. P., Alexandrova, A., Stefanova, M. O., Solak, A., et al. (2023) · Antioxidants · doi:10.3390/antiox12122050 · Cited by 7
Proteomic profiling of the insoluble fractions in the rat hippocampus post-propofol anesthesia
Zhang, X., Liu, Y., Feng, C., Yang, S., Wang, Y., Wu, A., & Yue, Y. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.08.025 · Cited by 8
Poorgholam, P., Yaghmaei, P., Noureddini, M., & Zahra, H. (2021) · Acta Neurobiologiae Experimentalis · doi:10.21307/ane-2021-013 · Cited by 8
Functional amyloid formation in LPS activated cells from invertebrates to vertebrates
Grimaldi, A., Tettamanti, G., Girardello, R., Pulze, L., Valvassori, R., Malagoli, D., Ottaviani, E., & de Eguileor, M. (2014) · Invertebrate survival journal · Cited by 7
Senolytics prevent age-associated changes in female mice brain
Faria, O. W., Soares, M. S. P., de Mello, J. E., Alvez, F. L., Luduvico, K. P., Garcia, D. N., Schneider, A., Masternak, M. M., Spanevello, R. M., & Stefanello, F. M. (2024) · Neuroscience Letters · doi:10.1016/j.neulet.2024.137730 · Cited by 6
Liu, J., Sun, S., & Chen, Y. (2024) · Journal of Alzheimer s Disease · doi:10.3233/jad-231278 · Cited by 6
Qin, S., Fang, J., He, X., Yu, G., Yi, F., & Zhu, G. (2024) · Biology · doi:10.3390/biology13070544 · Cited by 4
Thermal cycling-hyperthermia ameliorates Aβ25-35-induced cognitive impairment in C57BL/6 mice
Kuo, Y.-Y., Chen, W., Lin, G.-B., Chen, Y.-M., Liu, H.-H., & Chao, C.-Y. (2023) · Neuroscience Letters · doi:10.1016/j.neulet.2023.137337 · Cited by 4
Milham, L. T., Morris, G. P., Konen, L. M., Rentsch, P., Avgan, N., & Vissel, B. (2024) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1338065 · Cited by 4
Nguyen, H. V. M., Ran, Q., Salmon, A. B., Ahn, B., Chiao, Y. A., Bhaskaran, S., & Richardson, A. G. (2024) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2024.10.269 · Cited by 4
FOXG1 Improves Cognitive Function in Alzheimer's Disease by Promoting Endogenous Neurogenesis
Pan, W., Xu, L., Wang, Y., Wang, Y., Wang, J., Qian, X., Zhou, C., Wang, H. X., Fan, X., & Wang, J. (2025) · The FASEB Journal · doi:10.1096/fj.202403299rr · Cited by 5
Perez, C., & Felty, Q. H. (2022) · Microvascular Research · doi:10.1016/j.mvr.2022.104337 · Cited by 4
Cofilin-mediated neurodegeneration in alzheimer’s disease and other amyloidopathies
Maloney, M. T., & Bamburg, J. R. (2007) · Molecular Neurobiology · doi:10.1007/s12035-007-0009-y · Cited by 4
Superoxide Dismutase in Psychiatric Diseases
Djordjevic, V. (2022) · Biochemistry · doi:10.5772/intechopen.99847 · Cited by 5
Molecular Aspects of Memory Dysfunction in Alzheimer’s Disease
Chin, J., Roberson, E. D., & Mucke, L. (2008) · Elsevier eBooks · doi:10.1016/b978-012370509-9.00015-2 · Cited by 5
Effect of the Dimethoate Administration on a Scrapie Murine Model
Hortells, P., Monleón, E., Acín, C., Vargas, A., Ryffel, B., Cesbron, J.-Y., Badiola, J. J., & Monzón, M. (2008) · Zoonoses and Public Health · doi:10.1111/j.1863-2378.2008.01139.x · Cited by 3
Pozdnyakov, D. I., & Voronkov, A. V. (2020) · Pharmaceutical Sciences · doi:10.34172/ps.2020.92 · Cited by 3
How can We Target Oxidative Stress in the Treatment of Neurodegenerative Diseases?
Akasaka, H., & Ruan, K. (2016) · Future Medicinal Chemistry · doi:10.4155/fmc-2016-0065 · Cited by 2
Ferjan, I., Kržan, M., Lipnik‐Štangelj, M., Žiberna, L., Stanovnik, L., & Černe, K. (2015) · Slovenian Medical Journal · doi:10.6016/zdravvestn.1360 · Cited by 2
Alzheimer disease models and human neuropathology: similarities and diVerences
Duyckaerts, C. J., Potier, M., & Delatour, B. (2008) · Cited by 2
Shoji, H., Hagihara, H., Graef, I. A., Crabtree, G. R., Huang, F. L., Frankland, P. W., & Miyakawa, T. (2025) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyaf062 · Cited by 1
Stover, K. R. (2015) · DalSpace (Dalhousie University) · Cited by 1
Zawia, N. H., & Cardozo‐Pelaez, F. (2010) · Humana Press eBooks · doi:10.1007/978-1-60761-602-3_22 · Cited by 1
Koo, J., & Cho, I. (2016) · Exercise Science · doi:10.15857/ksep.2016.25.1.18 · Cited by 1
Stephens, G. S., You, J. C., Fu, C.-H., & Chin, J. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21126-7 · Cited by 1
AFFINITY ENRICHMENT AND MASS SPECTROMETRIC QUANTITATION OF PROTEIN CARBONYLS
Narayanasamy, S. (2014) · VCU Scholars Compass (Virginia Commonwealth University) · doi:10.25772/1fpy-qq93 · Cited by 1
Superoxide Dismutase and Hippocampal Function: Age and Isozyme Matter
Hu, D., Klann, E., & Thiels, E. (2006) · Antioxidants and Redox Signaling · doi:10.1089/ars.2007.9.ft-5 · Cited by 1
Bhatnagar, D., Ladhe, S., & Kumar, D. (2023) · BENTHAM SCIENCE PUBLISHERS eBooks · doi:10.2174/9789815136142123010012 · Cited by 1
Redox-dependent synaptic clustering of gephyrin
Gehling, M.-T., Bruckisch, E. H. W., Eggersmann, F. R., Benting, K., Jacobs, L. H. C., Behrmann, E., Riemer, J., Kloppenburg, P., Liebsch, F., & Schwarz, G. (2026) · Nature Communications · doi:10.1038/s41467-026-77147-2 · Cited by 1
Mecanismos reparadores neuronales en la enfermedad de Alzheimer
Urdaneta, E., Barrenetxe, J., de Mera, R. M. M. F., & Jordán, J. (2006) · Revista Española de Geriatría y Gerontología · doi:10.1016/s0211-139x(06)73011-6 · Cited by 1
Pharmacology and Pathology of Superoxide Dismutases (SOD)
Jordán, J., Sáez-Atiénzar, S., Atienzar‐Aroca, S., Solesio, M. E., & Galindo, M. F. (2014) · Springer eBooks · doi:10.1007/978-3-642-30018-9_29 · Cited by 1
Developmental Lead Exposure, Epigentics and Late Onset Alzheimer's Disease
Zawia, N. H., & Basha, R. M. (2010) · doi:10.1002/9780470917060.ch9
Muthuswamy, A. (2008) · UKnowledge (University of Kentucky)
Rothenberg, K. G., Siedlak, S. L., Lee, H., Zhu, X., Perry, G. L., & Smith, M. A. (2011) · Future Neurology · doi:10.2217/fnl.10.81
Animal Models in Neuro Ophthalmology
Normando, E. M., Brodie, J. T., & Cordeiro, M. F. (2016) · Springer eBooks · doi:10.1007/978-3-319-24085-5_13
Animal Models of Metallic Dementia
Rodella, L. F. (2010) · Neuromethods · doi:10.1007/978-1-60761-898-0_34
Kwakye, G. F., & Bowman, A. B. (2009)
Salminen, L. E. (2016) · IRL - University of Missouri, St. Louis (University of Missouri–St. Louis)
Analysis of infectious diseases in conditional mouse mutants
Pisano, F. (2009) · Digitale Bibliothek Braunschweig (Verbundzentrale Göttingen (VZG)) · doi:10.24355/dbbs.084-201003241212-0
Smith, M. A., & Lee, H.-P. (2008) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.1126898.584128
Animal Models in Neuro Ophthalmology
Normando, E. M., & Cordeiro, M. F. (2020) · Springer eBooks · doi:10.1007/978-3-030-26269-3_19
Żulińska, S., Wieczorek, I., Wencel, P., Strosznajder, R. P., Sun, G., & Strosznajder, J. B. (2022) · Research Square · doi:10.21203/rs.3.rs-1481945/v1
Kuo, Y.-Y., Chen, W., Lin, G.-B., Chen, Y.-M., Liu, H.-H., & Chao, C.-Y. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.07.22.500895
Żulińska, S., Wencel, P., Wieczorek, I., Strosznajder, R. P., & Strosznajder, J. B. (2023) · Research Square · doi:10.21203/rs.3.rs-2976047/v1
Antioxidants as Adjuncts to Conventional Therapies Against Oxidative Stress
Ahmed, A., Saleem, M. A., Afzaal, M., Ali, S. W., Nadeem, M., & Majeed, N. (2023) · Food bioactive ingredients · doi:10.1007/978-3-031-41188-5_9
Farnum, Z., Mani, R., Bindoff, A. D., Wilson, R., Fiotakis, A., Stephens, J., Cho, H., Mackay‐Sim, A., & Sinclair, D. (2024) · Journal of Neurochemistry · doi:10.1111/jnc.16263
Animal Models in Neuro Ophthalmology
Normando, E. M., Sher, A., Patel, R. P., Arora, N., & Cordeiro, M. F. (2025) · Springer eBooks · doi:10.1007/978-3-031-72156-4_19
Maladies neurodégénératives et stress oxydant
Lévy, E. (2020) · theses.fr (ABES) · doi:10.70675/75371581z194fz4cb4zb457z91bf72dc0320 · Cited by 4
Ansari, S., Khali, A., Joshi, B. C., & Uniyal, S. (2026) · Physiological Mini Reviews · doi:10.2174/0116695410415209251114033740
Acylglycerol Kinase Inhibition Restores Mitophagy and Alleviates Alzheimer's Disease Pathology
Li, W., Yu, X., Guo, C., Huang, Y., Wei, Z., Liu, Y., Wang, J., Liu, R., Ji, W., Duan, Q., et al. (2026) · MedComm · doi:10.1002/mco2.70863
Distinct sources and effects of mitochondrial reactive oxygen species
Barnett, D., Booraem, C., Orr, A. G., & Orr, A. L. (2026) · Molecular Cell · doi:10.1016/j.molcel.2026.07.009
Redox imbalance and epigenetic reprogramming underlie polysubstance-induced neuronal dysfunction
Chennakesavan, K., Hammond, H. R., Kalaisejiane, N., Devan, S., Karnati, A., Eans, S. O., Williams, A. K., McLaughlin, J. P., & Samikkannu, T. (2026) · Pharmacological Research · doi:10.1016/j.phrs.2026.109703
Metadata
- Authors
- Esposito, L., Raber, J., Kekonius, L., Yan, F., Yu, G.-Q., Bien-Ly, N., Puoliväli, J., Scearce-Levie, K., Masliah, E., & Mucke, L.
- Affiliations
- University of California, San Francisco (US)
- University of California San Diego (US)
- Gladstone Institutes (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-05-10
- Volume
- 26
- Issue
- 19
- Pages
- 5167-5179
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6674260
- OpenAlex
- W2109187744
- Cited by
- 254
- References
- 111
- Citations by year
- 2026: 5 · 2025: 6 · 2024: 9 · 2023: 12 · 2022: 14 · 2021: 16 · 2020: 18 · 2019: 8 · 2018: 11 · 2017: 13 · 2016: 13 · 2015: 16 · 2014: 16 · 2013: 10 · 2012: 12
- FWCI
- 10.60
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (AG‐022074, AG011385)
- National Institute on Aging (AG011385, AG022074, P01AG022074)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › 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 › Mitochondrial Function and Pathology
- Keywords
- Alzheimer's disease, manganese superoxide dismutase, amyloid precursor protein transgenic mice, amyloid-beta, mitochondrial dysfunction, oxidative stress, prepulse inhibition, sensorimotor gating, MAP2, dendritic degeneration, gliosis, neuritic dystrophy, nuclear factor-kappaB, behavioral deficits, neuroprotection
- MeSH terms
- Superoxide Dismutase 2, Alzheimer Disease, Animals, Mental Disorders, Enzyme Activation, Humans, Mice, Transgenic, Mitochondria, Receptors, Cell Surface, Superoxide Dismutase, Amyloid beta-Protein Precursor, Mice, Protease Nexins
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.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
