Redox proteomics analysis of brains from subjects with amnestic mild cognitive impairment compared to brains from subjects with preclinical Alzheimer’s disease: Insights into memory loss in MCI
Abstract
Alzheimer's disease (AD) is a central nervous system disorder pathologically characterized by senile plaques, neurofibrillary tangles, and synapse loss. A small percentage of individuals with normal antemortem psychometric scores, after adjustments for age and education, meet the neuropathological criteria for amnestic mild cognitive impairment (MCI) or AD; these individuals have been termed 'preclinical' or 'asymptomatic' AD (PCAD). In this study, we employed the immunochemical slot-blot method and two-dimensional gel-based redox proteomics to observe differences in protein levels and oxidative modifications between groups with equal levels of AD pathology who differ in regards to clinical symptoms of memory impairment. Results of global oxidative stress measurements revealed significantly higher levels of protein carbonyls in the MCI inferior parietal lobule (IPL) relative to PCAD (and controls), despite equal levels of neuropathology. Proteomics analysis of the IPL revealed differences in protein levels and specific carbonylation that are consistent with preservation of memory in PCAD and apparent memory decline in MCI. Our data suggest that marked changes occur at the protein level in MCI that may cause or reflect memory loss and other AD symptoms.
Integrity signals
Registry
Cites
Statistics
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?
Both HSP70 and HSP90 are significantly carbonylated in MCI IPL.
“Both HSP70 and HSP90 are significantly carbonylated in MCI IPL [59,60]”
From Mitochondrial Oxidative and Nitrosative Stress and Alzheimer Disease (2020) · cites this paper as [60]
Cites
Mild cognitive impairment as a diagnostic entity
Petersen, R. C. (2004) · Journal of Internal Medicine · doi:10.1111/j.1365-2796.2004.01388.x · Cited by 7,864 · see citing works
Shankar, G. M., Li, S., Mehta, T. H., Garcia-Munoz, A., Shepardson, N. E., Smith, I., Brett, F. M., Farrell, M. A., Rowan, M. J., Lemere, C. A., et al. (2008) · Nature Medicine · doi:10.1038/nm1782 · Cited by 3,685 · see citing works
Amyloid β-peptide is produced by cultured cells during normal metabolism
Haass, C., Schlossmacher, M. G., Hung, A. Y., Vigo-Pelfrey, C., Mellon, A., Ostaszewski, B. L., Lieberburg, I., Koo, E. H., Schenk, D., Teplow, D. B., et al. (1992) · Nature · doi:10.1038/359322a0 · Cited by 1,921 · see citing works
Profound Loss of Layer II Entorhinal Cortex Neurons Occurs in Very Mild Alzheimer’s Disease
Gómez-Isla, T., Price, J. L., McKeel Jr., D. W., Morris, J. C., Growdon, J. H., & Hyman, B. T. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-14-04491.1996 · Cited by 1,796 · see citing works
Isolation and quantification of soluble Alzheimer's β-peptide from biological fluids
Seubert, P., Vigo-Pelfrey, C., Esch, F., Lee, M., Dovey, H., Davis, D., Sinha, S., Schiossmacher, M., Whaley, J., Swindlehurst, C., et al. (1992) · Nature · doi:10.1038/359325a0 · Cited by 1,731 · see citing works
Shankar, G. M., Bloodgood, B. L., Townsend, M., Walsh, D. M., Selkoe, D. J., & Sabatini, B. L. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4970-06.2007 · Cited by 1,592 · see citing works
Production of the Alzheimer Amyloid β Protein by Normal Proteolytic Processing
Shoji, M., Golde, T. E., Ghiso, J., Cheung, T. T., Estus, S., Shaffer, L. M., Cai, X.-D., McKay, D. M., Tintner, R., Frangione, B., et al. (1992) · Science · doi:10.1126/science.1439760 · Cited by 1,447 · see citing works
Excess brain protein oxidation and enzyme dysfunction in normal aging and in Alzheimer disease.
Smith, C. D., Carney, J. M., Starke-Reed, P. E., Oliver, C. N., Stadtman, E. R., Floyd, R. A., & Markesbery, W. R. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.23.10540 · Cited by 1,296 · see citing works
Self-citationLi, S., Hong, S., Shepardson, N. E., Walsh, D. M., Shankar, G. M., & Selkoe, D. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.012 · Cited by 972 · see citing works
Oxidative damage in Alzheimer's
Smith, M. A., Perry, G. L., Richey, P. L., Sayrec, L. M., Anderson, V. E., Beal, M. F., & Kowall, N. W. (1996) · Nature · doi:10.1038/382120b0 · Cited by 897 · see citing works
In vitro aging of ß-amyloid protein causes peptide aggregation and neurotoxicity
Pike, C. J., Walencewicz, A. J., Glabe, C. G., & Cotman, C. W. (1991) · Brain Research · doi:10.1016/0006-8993(91)91553-d · Cited by 829 · see citing works
Neuropathology of nondemented aging: presumptive evidence for preclinical Alzheimer disease
Price, J. L., McKeel, D. W., Buckles, V. D., Roe, C. M., Xiong, C., Grundman, M., Hansen, L. A., Petersen, R. C., Parisi, J. E., Dickson, D. W., et al. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2009.04.002 · Cited by 661 · see citing works
Self-citationNeuron Number in the Entorhinal Cortex and CA1 in Preclinical Alzheimer Disease
Price, J. L., Ko, A. I., Wade, M. J., Tsou, S. K., McKeel, D. W., & Morris, J. C. (2001) · Archives of Neurology · doi:10.1001/archneur.58.9.1395 · Cited by 596 · see citing works
Castegna, A., Aksenov, M. Y., Thongboonkerd, V., Klein, J. B., Pierce, W. M. J., Booze, R. M., Markesbery, W. R., & Butterfield, D. A. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.01103.x · Cited by 581 · see citing works
Self-citationCastegna, A., Aksenov, M., Aksenova, M., Thongboonkerd, V., Klein, J. B., Pierce, W. M., Booze, R., Markesbery, W. R., & Butterfield, D. A. (2002) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(02)00914-0 · Cited by 581 · see citing works
Self-citationChoi, J., Levey, A. I., Weintraub, S. T., Rees, H. D., Gearing, M., Chin, L.-S., & Li, L. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m314124200 · Cited by 568 · see citing works
α-Enolase, a Novel Strong Plasmin(ogen) Binding Protein on the Surface of Pathogenic Streptococci
Pancholi, V., & Fischetti, V. A. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.23.14503 · Cited by 556 · see citing works
Aging renders the brain vulnerable to amyloid β-protein neurotoxicity
Guela, C., Wu, C.-K., Saroff, D., Lorenzo, A., Yuan, M., & Yankner, B. A. (1998) · Nature Medicine · doi:10.1038/nm0798-827 · Cited by 520 · see citing works
Protein oxidation in the brain in Alzheimer's disease
Aksenov, M. Y., Aksenova, M. V., Butterfield, D. A., Geddes, J. W., & Markesbery, W. R. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00580-7 · Cited by 503 · see citing works
Self-citationThe use of PET in Alzheimer disease
Nordberg, A. K., Rinne, J. O., Kadir, A., & Långström, B. (2010) · Nature Reviews Neurology · doi:10.1038/nrneurol.2009.217 · Cited by 451 · see citing works
Butterfield, D. A., Poon, H. F., St. Clair, D., Keller, J. N., Pierce, W. M., Klein, J. B., & Markesbery, W. R. (2006) · Neurobiology of Disease · doi:10.1016/j.nbd.2005.11.002 · Cited by 377 · see citing works
Self-citationRukhsana Sultana, A., Debra Boyd-kimball, A., Poon, H. F., Cai, J., Pierce, W. M. J., Klein, J. B., Merchant, M. L., Markesbery, W. R., & Butterfield, D. A. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.09.021 · Cited by 334 · see citing works
Self-citationHippocampal neurons in pre-clinical Alzheimer's disease.
West, M. J., Kawas, C. H., Stewart, W. F., Rudow, G. L., & Troncoso, J. C. (2004) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2003.12.005 · Cited by 317 · see citing works
Lipid peroxidation is an early event in the brain in amnestic mild cognitive impairment
Markesbery, W. R., Kryscio, R. J., Lovell, M. A., & Morrow, J. D. (2005) · Annals of Neurology · doi:10.1002/ana.20629 · Cited by 272 · see citing works
Self-citationStructural Analysis of α-Enolase
Subramanian, A. K., & Miller, D. M. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.8.5958 · Cited by 265 · see citing works
Reed, T., Perluigi, M., Sultana, R., Pierce, W. M., Klein, J. B., Turner, D. M., Coccia, R., Markesbery, W. R., & Butterfield, D. A. (2008) · Neurobiology of Disease · doi:10.1016/j.nbd.2007.12.007 · Cited by 257 · see citing works
Self-citationRukhsana Sultana, A., Debra Boyd-kimball, A., Poon, H. F., Cai, J., Pierce, W. M. J., Klein, J. B., Markesbery, W. R., Zhou, X. Z., Lu, K. P., & Butterfield, D. A. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.05.005 · Cited by 255 · see citing works
Self-citationButterfield, D. A., Reed, T., Perluigi, M., De Marco, C., Coccia, R., Cini, C., & Sultana, R. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2005.12.017 · Cited by 246 · see citing works
Self-citationOxidative damage in mild cognitive impairment and early Alzheimer's disease
Lovell, M. A., & Markesbery, W. R. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21346 · Cited by 245 · see citing works
Self-citationSmith, M. A., Sayre, L. M., Anderson, V. E., Harris, P. L. R., Beal, M. F., Kowall, N. W., & Perry, G. L. (1998) · Journal of Histochemistry & Cytochemistry · doi:10.1177/002215549804600605 · Cited by 222 · see citing works
Sultana, R., Perluigi, M., & Butterfield, D. A. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0517-0 · Cited by 215 · see citing works
Self-citationIacono (2009) · doi:10.1212/wnl.0b013e3181b01077 · Cited by 203 · see citing works
Self-citationOpii, W. O., Joshi, G., Head, E., Milgram, N. W., Muggenburg, B. A., Klein, J. B., Pierce, W. M., Cotman, C. W., & Butterfield, D. A. (2008) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.09.012 · Cited by 202 · see citing works
Self-citationIncreased levels of 4-hydroxynonenal and acrolein in the brain in preclinical Alzheimer disease
Bradley, M. A., Markesbery, W. R., & Lovell, M. A. (2010) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2010.02.016 · Cited by 193 · see citing works
Self-citationReed, T. T., Pierce, W. M., Markesbery, W. R., & Butterfield, D. A. (2009) · Brain Research · doi:10.1016/j.brainres.2009.04.009 · Cited by 190 · see citing works
Self-citationBlood-brain barrier disturbance in patients with Alzheimer's disease is related to vascular factors
Blennow, K., Wallin, A., Fredman, P., Karlsson, I., Gottfries, C. G., & Svennerholm, L. T. (2009) · Acta Neurologica Scandinavica · doi:10.1111/j.1600-0404.1990.tb01563.x · Cited by 185 · see citing works
An immunochemical study of the pyruvate dehydrogenase deficit in Alzheimer's disease brain
Sheu, K. R., Kim, Y., Blass, J. P., & Weksler, M. E. (1985) · Annals of Neurology · doi:10.1002/ana.410170505 · Cited by 180 · see citing works
Non-neuronal Enolase Is an Endothelial Hypoxic Stress Protein
Aaronson, R. M., Graven, K. K., Tucci, M., McDonald, R. J., & Farber, H. W. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.46.27752 · Cited by 155 · see citing works
Absence of cognitive impairment or decline in preclinical Alzheimer’s disease
Goldman, W. P., Price, J. L., Storandt, M., Grant, E., McKeel, D. W., Rubin, E. H., & Morris, J. C. (2001) · Neurology · doi:10.1212/wnl.56.3.361 · Cited by 143 · see citing works
Neuropathologic Studies of the Baltimore Longitudinal Study of Aging (BLSA)
O'Brien, R. J., Resnick, S. M., Zonderman, A. B., Ferrucci, L., Crain, B. J., Pletnikova, O., Rudow, G., Iacono, D., Riudavets, M. A., Driscoll, I., et al. (2009) · Journal of Alzheimer's Disease · doi:10.3233/jad-2009-1179 · Cited by 137 · see citing works
Brain protein and α‐ketoglutarate dehydrogenase complex activity in alzheimer‐s disease
Mastrogiacomo, F., LINDSAY, J. G., Bettendorff, L., Rice, J., & Kish, S. J. (1996) · Annals of Neurology · doi:10.1002/ana.410390508 · Cited by 132 · see citing works
Free radical damage, iron, and Alzheimer's disease
Smith, M. A., & Perry, G. L. (1995) · Journal of the Neurological Sciences · doi:10.1016/0022-510x(95)00213-l · Cited by 130 · see citing works
Sultana, R., Perluigi, M., Newman, S. F., Pierce, W. M., Cini, C., Coccia, R., & Butterfield, D. A. (2010) · Antioxidants & Redox Signaling · doi:10.1089/ars.2009.2810 · Cited by 125 · see citing works
Self-citationPlasminogen Binds Specifically to α‐Enolase on Rat Neuronal Plasma Membrane
Nakajima, K., Hamanoue, M., Takemoto, N., Hattori, T., Kato, K., & Kohsaka, S. (1994) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1994.63062048.x · Cited by 122 · see citing works
Schägger, H., & Ohm, T. G. (1995) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1995.tb20219.x · Cited by 117 · see citing works
Cloning and characterization of a human c-myc promoter-binding protein.
Ray, R. B., & Miller, D. M. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.4.2154 · Cited by 116 · see citing works
Rukhsana Sultana, A., Piroddi, M., Galli, F., & Butterfield, D. A. (2008) · Neurochemical Research · doi:10.1007/s11064-008-9593-0 · Cited by 115 · see citing works
Self-citationGanna Lyubartseva, A., Smith, J. L., Markesbery, W. R., & Lovell, M. A. (2009) · Brain Pathology · doi:10.1111/j.1750-3639.2009.00283.x · Cited by 103 · see citing works
Self-citationFluoride Exposure Attenuates Expression of Streptococcus pyogenes Virulence Factors
Thongboonkerd, V., Luengpailin, J., Cao, J., Pierce, W. M. J., Cai, J., Klein, J. B., & Doyle, R. J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m200746200 · Cited by 102 · see citing works
Self-citationZhang, D., Li, J., Costa, M., Gao, J., & Huang, C. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-0448 · Cited by 99 · see citing works
Neuronal Survival Factor from Bovine Brain Is Identical to Neuron‐Specific Enolase
Takei, N., Kondo, J., Nagaike, K., Ohsawa, K., Kato, K., & Kohsaka, S. (1991) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1991.tb08277.x · Cited by 98 · see citing works
Chandrasekaran, K., Hatanpaa, K., Rapoport, S., & Brady, D. (1997) · Brain Research. Molecular Brain Research · doi:10.1016/s0169-328x(96)00191-x · Cited by 95 · see citing works
Hattori, T., Takei, N., Mizuno, Y., Kato, K., & Kohsaka, S. (1995) · Neuroscience Research · doi:10.1016/0168-0102(94)00849-b · Cited by 94 · see citing works
Maki, M., Matsukawa, N., Yuasa, H., Otsuka, Y., Yamamoto, T., Akatsu, H., Okamoto, T., Ueda, R., & Ojika, K. (2002) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/61.2.176 · Cited by 83 · see citing works
Preclinical Alzheimer disease: Brain oxidative stress, Aβ peptide and proteomics
Aluise, C. D., Sowell, R. A., Beckett, T. L., Murphy, M. P., Cai, J., Pierce, W. M. J., Markesbery, W. R., & Butterfield, D. A. (2010) · Neurobiology of Disease · doi:10.1016/j.nbd.2010.04.011 · Cited by 83 · see citing works
Self-citationGeorge, A. J., Holsinger, R. M. D., McLean, C., Tan, S., Scott, H. S., Cardamone, T., Cappai, R., Masters, C. L., & Li, Q. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.03.014 · Cited by 69 · see citing works
Smith, M. A., Siedlak, S., Richey, P., Nagaraj, R., Elhammer, Å., & Perry, G. (1996) · Brain Research · doi:10.1016/0006-8993(95)01473-x · Cited by 58 · see citing works
牧, 美. (2002) · Medical Entomology and Zoology · Cited by 58 · see citing works
Hattori, T., Ohsawa, K., Mizuno, Y., Kato, K., & Kohsaka, S. (1994) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1994.1888 · Cited by 36 · see citing works
Plasmin Deficiency in Alzheimer’s Disease Brains: Causal or Casual?
Dotti, C. G., Galván, C. A., & Ledesma, M. D. (2004) · Neurodegenerative Diseases · doi:10.1159/000080987 · Cited by 24 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Oxidative stress and the amyloid beta peptide in Alzheimer’s disease
Cheignon, C., Tomas, M., Bonnefont-Rousselot, D., Faller, P., Hureau, C., & Collin, F. (2018) · Redox Biology · doi:10.1016/j.redox.2017.10.014 · Cited by 2,185 · see citing works
Free radicals and antioxidants: updating a personal view
Halliwell, B. B. (2012) · Nutrition Reviews · doi:10.1111/j.1753-4887.2012.00476.x · Cited by 918 · see citing works
Butterfield, D. A., Swomley, A. M., & Sultana, R. (2013) · Antioxidants & Redox Signaling · doi:10.1089/ars.2012.5027 · Cited by 526 · see citing works
Self-citationVerdile, G., Keane, K. N., Cruzat, V. F., Medic, S., Sabale, M., Rowles, J., Wijesekara, N., Martins, R. N., Fraser, P. E., & Newsholme, P. (2015) · Mediators of Inflammation · doi:10.1155/2015/105828 · Cited by 501 · see citing works
Sultana, R., Perluigi, M., & Butterfield, D. A. (2013) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2012.09.027 · Cited by 478 · see citing works
Self-citationNeuropathology of sporadic Parkinson's disease: Evaluation and changes of concepts
Jellinger, K. A. (2011) · Movement Disorders · doi:10.1002/mds.23795 · Cited by 448 · see citing works
Butterfield, D. A., Di Domenico, F., & Barone, E. (2014) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2014.06.010 · Cited by 402 · see citing works
Self-citationLipid peroxidation and neurodegenerative disease
Reed, T. T. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.06.027 · Cited by 380 · see citing works
Tramutola, A., Triplett, J. C., Di Domenico, F., Niedowicz, D. M., Murphy, M. P., Coccia, R., Perluigi, M., & Butterfield, D. A. (2015) · Journal of Neurochemistry · doi:10.1111/jnc.13037 · Cited by 347 · see citing works
Self-citationThe antioxidant paradox: less paradoxical now?
Halliwell, B. (2013) · British Journal of Clinical Pharmacology · doi:10.1111/j.1365-2125.2012.04272.x · Cited by 318 · see citing works
Oxidative stress, protein modification and Alzheimer disease
Tramutola, A., Lanzillotta, C., Perluigi, M., & Butterfield, D. A. (2017) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2016.06.005 · Cited by 303 · see citing works
Self-citationMarzia Perluigi, A., Domenico, F. D., & Butterfield, D. A. (2023) · Physiological Reviews · doi:10.1152/physrev.00030.2022 · Cited by 306 · see citing works
Self-citationThe role of type 2 diabetes in neurodegeneration
Verdile, G., Fuller, S. J., & Martins, R. N. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.04.008 · Cited by 276 · see citing works
Redox Proteomics: Chemical Principles, Methodological Approaches and Biological/Biomedical Promises
Bachi, A., Dalle‐Donne, I., & Scaloni, A. (2012) · Chemical Reviews · doi:10.1021/cr300073p · Cited by 262 · see citing works
Perluigi, M., Coccia, R., & Butterfield, D. A. (2012) · Antioxidants & Redox Signaling · doi:10.1089/ars.2011.4406 · Cited by 229 · see citing works
Self-citationClemente‐Suárez, V. J., Redondo-Flórez, L., Beltrán-Velasco, A. I., Ramos‐Campo, D. J., Belinchón-deMiguel, P., Martínez‐Guardado, I., Dalamitros, A. A., Sepulveda, R. A. Y., Martín-Rodríguez, A., & Tornero-Aguilera, J. F. (2023) · Biomedicines · doi:10.3390/biomedicines11092488 · Cited by 241 · see citing works
Oxidative Damage to RNA in Aging and Neurodegenerative Disorders
Nunomura, A., Moreira, P. I., Castellani, R. J., Lee, H., Zhu, X., Smith, M. A., & Perry, G. L. (2012) · Neurotoxicity Research · doi:10.1007/s12640-012-9331-x · Cited by 183 · see citing works
Swomley, A. M., & Butterfield, D. A. (2015) · Archives of Toxicology · doi:10.1007/s00204-015-1556-z · Cited by 171 · see citing works
Self-citationRedox Proteomics in Selected Neurodegenerative Disorders: From Its Infancy to Future Applications
Butterfield, D. A., Marzia Perluigi, A., Reed, T. T., Muharib, T., Hughes, C. P., Robinson, R. A. S., & Rukhsana Sultana, A. (2011) · Antioxidants and Redox Signaling · doi:10.1089/ars.2011.4109 · Cited by 167 · see citing works
Self-citationKeeney, J. T. R., Ren, X., Warrier, G., Noel, T. J., Powell, D. K., Brelsfoard, J., Rukhsana Sultana, A., Saatman, K. E., Clair, D. K. S., & Butterfield, D. A. (2018) · Oncotarget · doi:10.18632/oncotarget.25718 · Cited by 159 · see citing works
Self-citationNunomura, A., Tamaoki, T., Motohashi, N., Nakamura, M., McKeel, D. W., Tabaton, M., Lee, H., Smith, M. A., Perry, G. L., & Zhu, X. (2012) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0b013e318248e614 · Cited by 131 · see citing works
Gonos, E. S., Καπετάνου, Μ., Sereikaitė, J., Bartosz, G., Naparło, K., Grzesik, M., & Sadowska‐Bartosz, I. (2018) · Aging · doi:10.18632/aging.101450 · Cited by 133 · see citing works
Butterfield, D. A. (2014) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2014.06.006 · Cited by 126 · see citing works
Self-citationEpigenomics of Alzheimer's disease
Bennett, D. A., Yu, L., Yang, J., Srivastava, G. P., Aubin, C., & Jager, P. L. D. (2014) · Translational research · doi:10.1016/j.trsl.2014.05.006 · Cited by 124 · see citing works
Marzia Perluigi, A., Domenico, F. D., Barone, E., & Butterfield, D. A. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2021.04.025 · Cited by 121 · see citing works
Self-citationMoya‐Alvarado, G., Gershoni‐Emek, N., Perlson, E., & Bronfman, F. C. (2016) · Molecular & Cellular Proteomics · doi:10.1074/mcp.r115.053330 · Cited by 119 · see citing works
Di Domenico, F., Barone, E., Perluigi, M., & Butterfield, D. A. (2017) · Antioxidants & Redox Signaling · doi:10.1089/ars.2016.6759 · Cited by 114 · see citing works
Self-citationMass spectrometry and redox proteomics: Applications in disease
Butterfield, D. A., Gu, L., Domenico, F. D., & Robinson, R. A. S. (2013) · Mass Spectrometry Reviews · doi:10.1002/mas.21374 · Cited by 113 · see citing works
Self-citationButterfield, D. A., Domenico, F. D., Swomley, A. M., Head, E., & Marzia Perluigi, A. (2014) · Biochemical Journal · doi:10.1042/bj20140772 · Cited by 111 · see citing works
Self-citationNrf2/ARE Pathway Modulation by Dietary Energy Regulation in Neurological Disorders
Vasconcelos, A. R., dos Santos, N. B., Scavone, C., & Munhoz, C. D. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00033 · Cited by 112 · see citing works
Redox proteomics and amyloid β-peptide: Insights into Alzheimer disease
Butterfield, D. A., & Boyd‐Kimball, D. (2019) · Journal of Neurochemistry · doi:10.1111/jnc.14589 · Cited by 105 · see citing works
Self-citationThe diabetic brain and cognition
Riederer, P., Korczyn, A. D., Ali, S. S., Bajenaru, O. A., Choi, M. S., Chopp, M., Dobrota, V. Đ., Grünblatt, E., Jellinger, K. A., Kamal, M. A., et al. (2017) · Journal of Neural Transmission · doi:10.1007/s00702-017-1763-2 · Cited by 96 · see citing works
Mitochondrial Oxidative and Nitrosative Stress and Alzheimer Disease
Butterfield, D. A., & Boyd-Kimball, D. (2020) · Antioxidants · doi:10.3390/antiox9090818 · Cited by 85 · see citing works
“MnSOD is oxidatively modified by HNE in early AD IPL, resulting in a significant decrease in enzyme activity [55] and is also oxidatively modified by HNE in late AD IPL [54].”
BackgroundInfluentialSelf-citationMitochondrial Abnormalities in Alzheimer’s Disease
Silva, D. F., Selfridge, J. E., Lu, J., E, L., Cardoso, S. M., & Swerdlow, R. H. (2012) · Advances in Pharmacology · doi:10.1016/b978-0-12-394816-8.00003-9 · Cited by 86 · see citing works
Leuner, K., Stockburger, C., Denzer, I., Eckert, G. P., & Müller, W. E. (2014) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-394625-6.00007-6 · Cited by 84 · see citing works
Rukhsana Sultana, A., & Butterfield, D. A. (2012) · Journal of Alzheimer s Disease · doi:10.3233/jad-2012-129018 · Cited by 83 · see citing works
Self-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
Targeting Mitochondria in Alzheimer Disease: Rationale and Perspectives
Lanzillotta, C., Domenico, F. D., Marzia Perluigi, A., & Butterfield, D. A. (2019) · CNS Drugs · doi:10.1007/s40263-019-00658-8 · Cited by 72 · see citing works
Self-citationLiang, J., Wang, C., Zhang, H., Huang, J., Xie, J., & Chen, N. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.755665 · Cited by 66 · see citing works
Redox imbalance and morphological changes in skin fibroblasts in typical Rett syndrome
Signorini, C., Leoncini, S., De Felice, C., Pecorelli, A., Meloni, I., Ariani, F., Mari, F., Amabile, S., Paccagnini, E., Gentile, M., et al. (2014) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2014/195935 · Cited by 61 · see citing works
mTOR signaling as a molecular target for the alleviation of Alzheimer's disease pathogenesis
Rapaka, D., Bitra, V. R., Challa, S. R., & Adiukwu, P. C. (2022) · Neurochemistry International · doi:10.1016/j.neuint.2022.105311 · Cited by 65 · see citing works
Khan, H., Singh, T. G., Singh, R., & Abdel‐Daim, M. M. (2022) · Neurochemical Research · doi:10.1007/s11064-022-03598-w · Cited by 62 · see citing works
Redox proteomics and the dynamic molecular landscape of the aging brain
Marzia Perluigi, A., Swomley, A. M., & Butterfield, D. A. (2013) · Ageing Research Reviews · doi:10.1016/j.arr.2013.12.005 · Cited by 59 · see citing works
Self-citationKeeney, J. T. R., Swomley, A. M., Harris, J. L., Fiorini, A., Mitov, M. I., Marzia Perluigi, A., Rukhsana Sultana, A., & Butterfield, D. A. (2011) · Neurotoxicity Research · doi:10.1007/s12640-011-9287-2 · Cited by 56 · see citing works
Self-citationLoss of biliverdin reductase-A favors Tau hyper-phosphorylation in Alzheimer's disease
Sharma, N. K., Tramutola, A., Lanzillotta, C., Arena, A., Blarzino, C., Cassano, T., Butterfield, D. A., Domenico, F. D., Marzia Perluigi, A., & Barone, E. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.02.003 · Cited by 57 · see citing works
Self-citationPerspectives on Oxidative Stress in Alzheimer’s Disease and Predictions of Future Research Emphases
Butterfield, D. A. (2018) · Journal of Alzheimer s Disease · doi:10.3233/jad-179912 · Cited by 57 · see citing works
Self-citationSignorini, C., Felice, C. D., Durand, T., Oger, C., Galano, J., Leoncini, S., Pecorelli, A., Valacchi, G., Ciccoli, L., & Hayek, J. (2013) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2013/343824 · Cited by 53 · see citing works
Redox Homeostasis and Prospects for Therapeutic Targeting in Neurodegenerative Disorders
Akanji, M. A., Rotimi, D. E., Elebiyo, T. C., Awakan, O. J., & Adeyemı, O. S. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/9971885 · Cited by 52 · see citing works
Domenico, F. D., Rukhsana Sultana, A., Ferree, A. W., Smith, K., Barone, E., Marzia Perluigi, A., Coccia, R., Pierce, W. M. J., Cai, J., Mancuso, C., et al. (2012) · Antioxidants and Redox Signaling · doi:10.1089/ars.2011.4312 · Cited by 51 · see citing works
Self-citationWalia, V., Kaushik, D., Mittal, V., Kumar, K., Verma, R., Parashar, J., Akter, R., Rahman, M. H., Bhatia, S., Al-Harrasi, A., et al. (2022) · Molecular Neurobiology · doi:10.1007/s12035-021-02617-1 · Cited by 47 · see citing works
Early Molecular Changes in Alzheimer Disease: Can We Catch the Disease in its Presymptomatic Phase?
Wirz, K. T. S., Keitel, S., Swaab, D. F., Verhaagen, J., & Bossers, K. (2013) · Journal of Alzheimer s Disease · doi:10.3233/jad-130920 · Cited by 47 · see citing works
Early intervention attenuates synaptic plasticity impairment and neuroinflammation in 5xFAD mice
Li, K., Wang, X., Jiang, Y., Zhang, X., Liu, Z., Yin, T., & Yang, Z. R. (2021) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2021.02.007 · Cited by 43 · see citing works
Al‐Ezzi, A. A. A., Arechavala, R. J., Butler, R., Nolty, A., Kang, J. J. H., Shinsuke Shimojo, A., Wu, D.-A. J., Fonteh, A. N., Kleinman, M. T., Kloner, R. A., et al. (2024) · Communications Biology · doi:10.1038/s42003-024-06673-w · Cited by 42 · see citing works
Postsynaptic Proteome of Non-Demented Individuals with Alzheimer’s Disease Neuropathology
Zolochevska, O., Bjorklund, N., Woltjer, R., Wiktorowicz, J. E., & Taglialatela, G. (2018) · Journal of Alzheimer’s Disease · doi:10.3233/jad-180179 · Cited by 42 · see citing works
Protein Oxidation in Aging and Alzheimer’s Disease Brain
Rukhsana Sultana, A., & Butterfield, D. A. (2024) · Antioxidants · doi:10.3390/antiox13050574 · Cited by 42 · see citing works
Self-citationZaręba-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
Triplett, J. C., Swomley, A. M., Cai, J., Klein, J. B., & Butterfield, D. A. (2015) · Journal of Alzheimer s Disease · doi:10.3233/jad-150417 · Cited by 39 · see citing works
Self-citationAlhibshi, A., Odawara, A., & Suzuki, I. (2019) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2018.12.005 · Cited by 38 · see citing works
Finelli, M. J. (2020) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2020.00254 · Cited by 37 · see citing works
Lanzillotta, C., Tramutola, A., Lanzillotta, S., Greco, V., Pagnotta, S. E., Sanchini, C., Angelantonio, S. D., Forte, E., Rinaldo, S., Paone, A., et al. (2024) · Redox Biology · doi:10.1016/j.redox.2024.103221 · Cited by 29 · see citing works
Self-citationMehan, S., Bhalla, S., Siddiqui, E. M., Sharma, N., Shandilya, A., & Khan, A. (2022) · Degenerative Neurological and Neuromuscular Disease · doi:10.2147/dnnd.s247153 · Cited by 29 · see citing works
Oxidative Stress in Brain in Amnestic Mild Cognitive Impairment
Butterfield, D. A. (2023) · Antioxidants · doi:10.3390/antiox12020462 · Cited by 28 · see citing works
Self-citationMitochondria as a target for neuroprotection: implications for Alzheimer´s disease
Cardoso, S., Seiça, R. M. F., & Moreira, P. I. (2016) · Expert Review of Neurotherapeutics · doi:10.1080/14737175.2016.1205488 · Cited by 27 · see citing works
Oba, K., Tamura, Y., Ishikawa, J., Suzuki, H., Fujiwara, Y., Tachibana, A., Kodera, R., Toyoshima, K., Chiba, Y., & Araki, A. (2022) · BMC Geriatrics · doi:10.1186/s12877-022-02948-1 · Cited by 26 · see citing works
Shen, L., Chen, Y., Yang, A., Chen, C., Liao, L., Li, S., Ying, M., Tian, J., Liu, Q., & Ni, J. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17040469 · Cited by 26 · see citing works
Risk Classification in Mild Cognitive Impairment Patients for Developing Alzheimer's Disease
Zhou, B., Initiative, T. A. D. N., Nakatani, E., Teramukai, S., Nagai, Y., & Fukushima, M. (2012) · Journal of Alzheimer s Disease · doi:10.3233/jad-2012-112117 · Cited by 22 · see citing works
Redox imbalance and metabolic defects in the context of Alzheimer disease
Domenico, F. D., Lanzillotta, C., & Marzia Perluigi, A. (2024) · FEBS Letters · doi:10.1002/1873-3468.14840 · Cited by 22 · see citing works
Muñoz, P., Ardiles, Á. O., Pérez-Espinosa, B., Núñez-Espinosa, C. A., Paula-Lima, A. C., González-Billault, C. E., & Espinosa‐Parrilla, Y. (2020) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2020.111250 · Cited by 19 · see citing works
Road to Alzheimer’s Disease: The Pathomechanism Underlying
Anand, R., Kaushal, A., Wani, W. Y., & Gill, K. D. (2011) · Pathobiology · doi:10.1159/000332218 · Cited by 15 · see citing works
Stepler, K. E., & Robinson, R. A. S. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-05542-4_1 · Cited by 15 · see citing works
Self-citationKim, W., Cho, S. B., Jung, H. Y., Yoo, D. Y., Oh, J. K., Choi, G.-M., Cho, T. G., Kim, D. W., Hwang, I. K., Choi, S. Y., et al. (2019) · Cells · doi:10.3390/cells8111370 · Cited by 14 · see citing works
4-Hydroxyhexenal (HHE) Impairs Glutamate Transport in Astrocyte Cultures
Lovell, M. A., Bradley‐Whitman, M. A., & Fister, S. X. (2012) · Journal of Alzheimer s Disease · doi:10.3233/jad-2012-120409 · Cited by 13 · see citing works
Sanders, O. D. (2022) · Journal of Alzheimer s Disease Reports · doi:10.3233/adr-220047 · Cited by 12 · see citing works
Bacchella, C., Dell’Acqua, S., Nicolis, S., Monzani, E., & Casella, L. (2021) · Inorganic Chemistry · doi:10.1021/acs.inorgchem.0c02243 · Cited by 12 · see citing works
Das, N. K., & Jana, C. K. (2015) · Free Radical Research · doi:10.3109/10715762.2015.1017477 · Cited by 11 · see citing works
Scholes, H. M., Cryar, A., Kerr, F., Sutherland, D., Gethings, L. A., Vissers, J. P. C., Lees, J., Orengo, C. A., Partridge, L., & Thalassinos, K. (2020) · Scientific Reports · doi:10.1038/s41598-020-74748-9 · Cited by 10 · see citing works
Swomley, A. M., Triplett, J. C., Keeney, J. T. R., Warrier, G., Pearson, K. J., Mattison, J. A., de Cabo, R., Cai, J., Klein, J. B., & Butterfield, D. A. (2016) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2016.10.006 · Cited by 9 · see citing works
Self-citationEpigenomics of Alzheimer’s Disease
Bennett, D. A., Yu, L., Yang, J., Klein, H., & Jager, P. L. D. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-800802-7.00009-5 · Cited by 9 · see citing works
Neuropathological links between T2DM and LOAD: systematic review and meta-analysis
Lemche, E., Hortobágyi, T., Kiecker, C. M., & Turkheimer, F. (2025) · Physiological Reviews · doi:10.1152/physrev.00040.2024 · Cited by 8 · see citing works
Oxidative Stress in CD90+ T-cells of AβPP/PS-1 Transgenic Mice
Robinson, R. A. S., Cao, Z., & Williams, C. (2013) · Journal of Alzheimer s Disease · doi:10.3233/jad-130665 · Cited by 6 · see citing works
Self-citation3D-QSAR studies on lipid peroxidation inhibitory activity of chromone derivatives
Phosrithong, N., & Ungwitayatorn, J. (2016) · Medicinal Chemistry Research · doi:10.1007/s00044-016-1690-z · Cited by 6 · see citing works
Antioxidant Plant Polyphenols and Cognitive Disorders
Nowak, D. (2014) · Oxidative stress in applied basic research and clinical practice · doi:10.1007/978-1-4939-0440-2_26 · Cited by 5 · see citing works
Protein Carbonylation in Brains of Subjects with Selected Neurodegenerative Disorders
Reed, T. T., & Butterfield, D. A. (2017) · Wiley eBooks · doi:10.1002/9781119374947.ch8 · Cited by 3 · see citing works
Self-citationLanzillotta, S., Boccardi, V., Zulli, B., Napoli, A., Paolozzi, G., Angelini, R., Ruzicka, B., Fratini, F., Guazzarini, A. G., Scamosci, M., et al. (2026) · Neurobiology of Disease · doi:10.1016/j.nbd.2026.107291 · Cited by 2 · see citing works
Self-citationLipid Peroxidation and Age-Related Neurodegenerative Disorders
Spickett, C., & Forman, H. (2015) · CRC Press eBooks · doi:10.1201/b18138-21 · Cited by 2 · see citing works
Targeting Mitochondria and Redox Dyshomeostasis in Brain Ageing: An Update
Cardoso, S., & Moreira, P. I. (2021) · Healthy ageing and longevity · doi:10.1007/978-3-030-84965-8_8 · Cited by 2 · see citing works
Keeney, J. T. R. (2013) · UKnowledge (University of Kentucky) · Cited by 2 · see citing works
d’Avila, J. C. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-817780-8.00004-9 · Cited by 2 · see citing works
Hashemi, M., Azizi, M. R., & Hashemi, F. (2022) · Research Square · doi:10.21203/rs.3.rs-1693554/v1 · Cited by 2 · see citing works
Bezine, M. (2017) · theses.fr (ABES) · doi:10.70675/a634c389z7b07z4830zb56dzbf7b53a56944 · Cited by 1 · see citing works
Molecular changes during the development of Alzheimer's disease
Wirz, K. T. S. (2013) · Data Archiving and Networked Services (DANS)
The Link Between Diabetes, Glucose Control, and Alzheimer's Disease and Neurodegenerative Diseases
Verdile, G., Fraser, P. E., & Martins, R. N. (2019) · Wiley eBooks · doi:10.1002/9781119356752.ch4
Robinson, R. A. S. (2021) · ACS symposium series · doi:10.1021/bk-2021-1381.ch010
Self-citationFreyssin, A. (2020) · theses.fr (ABES) · doi:10.70675/0db2e37dz547bz4731z852dz9b843c062cba
- Authors
- Aluise, C. D., Robinson, R. A. S., Cai, J., Pierce, W. M., Markesbery, W. R., & Butterfield, D. A.
- Affiliations
- University of Kentucky (US)
- University of Louisville (US)
- Venue
- Journal of Alzheimer's Disease
- Publisher
- SAGE Publications
- Published
- 2011-02-26
- Volume
- 23
- Issue
- 2
- Pages
- 257-269
- ISSN
- 1387-2877 (ISSN-L)
- 1875-8908
- OpenAlex
- W1506952168
- Semantic Scholar
- d0361e0d178681fe934b682fb1a6622058b8a93a
- Cited by
- 94
- References
- 60
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 4 · 2023: 3 · 2022: 6 · 2021: 8 · 2020: 6 · 2019: 7 · 2018: 5 · 2017: 5 · 2016: 7 · 2015: 8 · 2014: 8 · 2013: 7 · 2012: 12
- FWCI
- 7.20
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Alzheimer s Disease (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Kentucky
- National Institutes of Health
- National Institute on Aging (P01AG005119, AG0 5119)
- NIH Clinical Center
- 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
- amnestic mild cognitive impairment, preclinical Alzheimer's disease
- MeSH terms
- Aged, 80 and over, Alzheimer Disease, Amnesia, Analysis of Variance, Brain, Cognition Disorders, Female, Humans, Male, Memory, Oxidation-Reduction, Mass Spectrometry, Blotting, Western, Electrophoresis, Gel, Two-Dimensional, Neurofibrillary Tangles, Oxidative Stress, Statistics, Nonparametric, Proteomics, Plaque, Amyloid
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