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Oxidative stress in Alzheimer disease and mild cognitive impairment: evidence from human data provided by redox proteomics

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Abstract

Alzheimer disease (AD) is a neurodegenerative disease with many known pathological features, yet there is still much debate into the exact cause and mechanisms for progression of this degenerative disorder. The amyloid-beta (Aβ)-induced oxidative stress hypothesis postulates that it is the oligomeric Aβ that inserts into membrane systems to initiate much of the oxidative stress observed in brain during the progression of the disease. In order to study the effects of oxidative stress on tissue from patients with AD and amnestic mild cognitive impairment (MCI), we have developed a method called redox proteomics that identifies specific brain proteins found to be selectively oxidized. Here, we discuss experimental findings of oxidatively modified proteins involved in three key cellular processes implicated in the pathogenesis of AD progression: energy metabolism, cell signaling and neurotransmission, as well as the proteasomal degradation pathways and antioxidant response systems. These proteomics studies conducted by our laboratory and others in the field shed light on the molecular changes imposed on the cells of AD and MCI brain, through the deregulated increase in oxidative/nitrosative stress inflicted by Aβ and mitochondrial dysfunction.

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Abbreviations

3NT:

3-Nitrotyrosine

AD:

Alzheimer disease

Aβ:

Amyloid-beta

CRMP2:

Collapsin response mediator protein-2

EAD:

Early-onset Alzheimer disease

ESI–MS/MS:

Electrospray ionization tandem mass spectrometry

FAD:

Familial Alzheimer disease

GSH:

Glutathione

HNE:

4-Hydroxynonenal

IPL:

Inferior parietal lobule

LAD:

Late-onset Alzheimer disease

MCI:

Mild cognitive impairment

NFT:

Neurofibrillary tangle

PC:

Protein carbonyl

PCAD:

Preclinical Alzheimer disease

PET:

Positron emission tomography

Pin1:

Peptidyl-prolyl cis/trans isomerase NIMA-interacting 1

PMI:

Postmortem interval

RNS:

Reactive nitrogen species

ROS:

Reactive oxygen species

SP:

Senile plaque

UCH L-1:

Ubiquitin carboxy-terminal hydrolase L-1

References

  • Aaronson RM, Graven KK, Tucci M, McDonald RJ, Farber HW (1995) Non-neuronal enolase is an endothelial hypoxic stress protein. J Biol Chem 270:27752–27757

    Article  CAS  PubMed  Google Scholar 

  • Adam-Vizi V (2005) Production of reactive oxygen species in brain mitochondria: contribution by electron transport chain and non-electron transport chain sources. Antioxid Redox Signal. doi:10.1089/ars.2005.7.1140

    PubMed  Google Scholar 

  • Aiken CT, Kaake RM, Wang X, Huang L (2011) Oxidative stress-mediated regulation of proteasome complexes. Mol Cell Proteomics R110:006924. doi:10.1074/mcp.M110.006924

    Google Scholar 

  • Aluise CD, Robinson RA, Cai J, Pierce WM, Markesbery WR, Butterfield DA (2011) 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. J Alzheimer’s Dis. doi:10.3233/JAD-2010-101083

    Google Scholar 

  • Andreadis A, Brown WM, Kosik KS (1992) Structure and novel exons of the human tau gene. Biochemistry 10626–10633

  • Bader Lange ML, St Clair D, Markesbery WR, Studzinski CM, Murphy MP, Butterfield DA (2010) Age-related loss of phospholipid asymmetry in APP(NLh)/APP(NLh) x PS-1(P264L)/PS-1(P264L) human double mutant knock-in mice: relevance to Alzheimer disease. Neurobiol Dis. doi:10.1016/j.nbd.2010.01.004

    PubMed Central  PubMed  Google Scholar 

  • Behl C, Moosmann B (2002) Oxidative nerve cell death in Alzheimer’s disease and stroke: antioxidants as neuroprotective compounds. Biol Chem. doi:10.1515/BC.2002.053

    PubMed  Google Scholar 

  • Ben-Nissan G, Sharon M (2014) Regulating the 20S proteasome ubiquitin-independent degradation pathway. Biomolecules. doi:10.3390/biom4030862

    PubMed Central  PubMed  Google Scholar 

  • Boyd-Kimball D, Mohmmad Abdul H, Reed T, Sultana R, Butterfield DA (2004) Role of phenylalanine 20 in Alzheimer’s amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity. Chem Res Toxicol. doi:10.1021/tx049796w

    PubMed  Google Scholar 

  • Braak H, Braak E (1997) Staging of Alzheimer-related cortical destruction. Int Psychogeriatr 257–261 (discussion 269–272)

  • Bradley MA, Markesbery WR, Lovell MA (2010) Increased levels of 4-hydroxynonenal and acrolein in the brain in preclinical Alzheimer disease. Free Rad Biol Med. doi:10.1016/j.freeradbiomed.2010.02.016

    PubMed Central  PubMed  Google Scholar 

  • Butterfield DA (2002) Amyloid beta-peptide (1–42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer’s disease brain. A review. Free Rad Res 36:1307–1313

    Article  CAS  Google Scholar 

  • Butterfield DA, Boyd-Kimball D (2005) The critical role of methionine 35 in Alzheimer’s amyloid beta-peptide (1-42)-induced oxidative stress and neurotoxicity. Biochim Biophys Acta. doi:10.1016/j.bbapap.2004.10.014

    Google Scholar 

  • Butterfield DA, Lange ML (2009) Multifunctional roles of enolase in Alzheimer’s disease brain: beyond altered glucose metabolism. J Neurochem. doi:10.1111/j.1471-4159.2009.06397.x

    PubMed Central  PubMed  Google Scholar 

  • Butterfield DA, Sultana R (2011) Methionine-35 of abeta(1-42): importance for oxidative stress in Alzheimer disease. J Amino Acids. doi:10.4061/2011/198430

    PubMed Central  PubMed  Google Scholar 

  • Butterfield DA, Drake J, Pocernich C, Castegna A (2001) Evidence of oxidative damage in Alzheimer’s disease brain: central role for amyloid beta-peptide. Trends Mol Med 7:548–554

    Article  CAS  PubMed  Google Scholar 

  • Butterfield DA, Poon HF, St Clair D, Keller JN, Pierce WM, Klein JB, Markesbery WR (2006) Redox proteomics identification of oxidatively modified hippocampal proteins in mild cognitive impairment: insights into the development of Alzheimer’s disease. Neurobiol Dis. doi:10.1016/j.nbd.2005.11.002

    Google Scholar 

  • Butterfield DA, Reed T, Newman SF, Sultana R (2007) Roles of amyloid beta-peptide-associated oxidative stress and brain protein modifications in the pathogenesis of Alzheimer’s disease and mild cognitive impairment. Free Rad Biol Med. doi:10.1016/j.freeradbiomed.2007.05.037

    Google Scholar 

  • Butterfield DA, Bader Lange ML, Sultana R (2010a) Involvements of the lipid peroxidation product, HNE, in the pathogenesis and progression of Alzheimer’s disease. Biochim Biophys Acta. doi:10.1016/j.bbalip.2010.02.005

    PubMed Central  PubMed  Google Scholar 

  • Butterfield DA, Galvan V, Lange MB, Tang H, Sowell RA, Spilman P, Bredesen DE (2010b) In vivo oxidative stress in brain of Alzheimer disease transgenic mice: Requirement for methionine 35 in amyloid beta-peptide of APP. Free Rad Biol Med. doi:10.1016/j.freeradbiomed.2009.10.035

    Google Scholar 

  • Butterfield DA, Perluigi M, Reed T, Muharib T, Hughes CP, Robinson RA, Sultana R (2012) Redox proteomics in selected neurodegenerative disorders: from its infancy to future applications. Antioxid Redox Signal. doi:10.1089/ars.2011.4109

    Google Scholar 

  • Butterfield DA, Swomley AM, Sultana R (2013) Amyloid beta-peptide (1-42)-induced oxidative stress in Alzheimer disease: importance in disease pathogenesis and progression. Antioxid Redox Signal. doi:10.1089/ars.2012.5027

    PubMed Central  PubMed  Google Scholar 

  • Calabrese V, Lodi R, Tonon C, D’Agata V, Sapienza M, Scapagnini G, Butterfield DA (2005) Oxidative stress, mitochondrial dysfunction and cellular stress response in Friedreich’s ataxia. J Neurol Sci. doi:10.1016/j.jns.2005.03.012

    PubMed  Google Scholar 

  • Castegna A, Aksenov M, Thongboonkerd V, Klein JB, Pierce WM, Booze R, Butterfield DA (2002a) Proteomic identification of oxidatively modified proteins in Alzheimer’s disease brain. Part II: dihydropyrimidinase-related protein 2, alpha-enolase and heat shock cognate 71. J Neurochem 82:1524–1532

    Article  CAS  PubMed  Google Scholar 

  • Castegna A, Aksenov M, Aksenova M, Thongboonkerd V, Klein JB, Pierce WM, Butterfield DA (2002b) Proteomic identification of oxidatively modified proteins in Alzheimer’s disease brain. Part I: creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1. Free Rad Biol Med 33:562–571

    Article  CAS  PubMed  Google Scholar 

  • Castegna A, Thongboonkerd V, Klein JB, Lynn B, Markesbery WR, Butterfield DA (2003) Proteomic identification of nitrated proteins in Alzheimer’s disease brain. J Neurochem 1394–1401

  • Castegna A, Lauderback CM, Mohmmad-Abdul H, Butterfield DA (2004) Modulation of phospholipid asymmetry in synaptosomal membranes by the lipid peroxidation products, 4-hydroxynonenal and acrolein: implications for Alzheimer’s disease. Brain Res. doi:10.1016/j.brainres.2004.01.036

    PubMed  Google Scholar 

  • Cecarini V, Ding Q, Keller JN (2007) Oxidative inactivation of the proteasome in Alzheimer’s disease. Free Rad Res. doi:10.1080/10715760701286159

    Google Scholar 

  • Chen CH, Li W, Sultana R, You MH, Kondo A, Shahpasand K, Lu KP (2015) Pin1 cysteine-113 oxidation inhibits its catalytic activity and cellular function in Alzheimer’s disease. Neurobiol Dis. doi:10.1016/j.nbd.2014.12.027

    Google Scholar 

  • Choi J, Levey AI, Weintraub ST, Rees HD, Gearing M, Chin LS, Li L (2004) Oxidative modifications and down-regulation of ubiquitin carboxyl-terminal hydrolase L1 associated with idiopathic Parkinson’s and Alzheimer’s diseases. J Biol Chem. doi:10.1074/jbc.M314124200

    Google Scholar 

  • Dasuri K, Zhang L, Keller JN (2013) Oxidative stress, neurodegeneration, and the balance of protein degradation and protein synthesis. Free Rad Biol Med. doi:10.1016/j.freeradbiomed.2012.09.016

    PubMed Central  Google Scholar 

  • Dean RT, Fu S, Stocker R Davies MJ (1997) Biochemistry and pathology of radical-mediated protein oxidation. Biochem J 1–18

  • Driver JA, Lu KP (2010) Pin1: a new genetic link between Alzheimer’s disease, cancer and aging. Curr Aging Sci 3:158–165

    Article  CAS  PubMed  Google Scholar 

  • Dunlop RA, Brunk UT, Rodgers KJ (2009) Oxidized proteins: mechanisms of removal and consequences of accumulation. IUBMB life. doi:10.1002/iub.189

    PubMed  Google Scholar 

  • Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol. doi:10.1038/nrm1589

    PubMed  Google Scholar 

  • Feeney MB, Schoneich C (2012) Tyrosine modifications in aging. Antioxid Redox Signal. doi:10.1089/ars.2012.4595

    PubMed Central  PubMed  Google Scholar 

  • Forster F, Unverdorben P, Sledz P, Baumeister W (2013) Unveiling the long-held secrets of the 26S proteasome. Structure. doi:10.1016/j.str.2013.08.010

    PubMed  Google Scholar 

  • Friedland-Leuner K, Stockburger C, Denzer I, Eckert GP, Muller WE (2014) Mitochondrial dysfunction: cause and consequence of Alzheimer’s disease. Prog Mol Biol Transl Sci. doi:10.1016/B978-0-12-394625-6.00007-6

    PubMed  Google Scholar 

  • Glabe C (2001) Intracellular mechanisms of amyloid accumulation and pathogenesis in Alzheimer’s disease. J Mol Neurosci. doi:10.1385/JMN:17:2:137

    PubMed  Google Scholar 

  • Glabe CC (2005) Amyloid accumulation and pathogensis of Alzheimer’s disease: significance of monomeric, oligomeric and fibrillar Abeta. Sub-cell Biochem 38:167–177

    Article  CAS  Google Scholar 

  • Halliwell B (2012) Free radicals and antioxidants: updating a personal view. Nutr Rev. doi:10.1111/j.1753-4887.2012.00476.x

    PubMed  Google Scholar 

  • Halliwell B, Gutteridge JM (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 1–14

  • Hebert LE, Scherr PA, Bienias JL, Bennett DA, Evans DA (2003) Alzheimer disease in the US population: prevalence estimates using the 2000 census. Arch Neurol. doi:10.1001/archneur.60.8.1119

    Google Scholar 

  • Hernandez-Saavedra D, McCord JM (2007) Evolution and free radicals. Importance of oxidative stress in human pathology. Revista medica del Instituto Mexicano del Seguro Social 45:477–484

    PubMed  Google Scholar 

  • Hwang J, Winkler L, Kalejta RF (2011) Ubiquitin-independent proteasomal degradation during oncogenic viral infections. Biochim Biophys Acta. doi:10.1016/j.bbcan.2011.05.005

    Google Scholar 

  • Indo HP, Yen HC, Nakanishi I, Matsumoto K, Tamura M, Nagano Y, Majima HJ (2015) A mitochondrial superoxide theory for oxidative stress diseases and aging. J Clin Biochem Nutr. doi:10.3164/jcbn.14-42

    Google Scholar 

  • Ischiropoulos H (2009) Protein tyrosine nitration–an update. Arch Biochem Biophys. doi:10.1016/j.abb.2008.10.034

    PubMed  Google Scholar 

  • Jicha GA, Parisi JE, Dickson DW, Johnson K, Cha R, Ivnik RJ, Petersen RC (2006) Neuropathologic outcome of mild cognitive impairment following progression to clinical dementia. Arch Neurol. doi:10.1001/archneur.63.5.674

    Google Scholar 

  • Jung T, Hohn A, Grune T (2013) The proteasome and the degradation of oxidized proteins: Part II - protein oxidation and proteasomal degradation. Redox Biol. doi:10.1016/j.redox.2013.12.008

    Google Scholar 

  • Keeney JT, Swomley AM, Harris JL, Fiorini A, Mitov MI, Perluigi M, Butterfield DA (2012) Cell cycle proteins in brain in mild cognitive impairment: insights into progression to Alzheimer disease. Neurotox Res. doi:10.1007/s12640-011-9287-2

    PubMed  Google Scholar 

  • Kleiger G, Mayor T (2014) Perilous journey: a tour of the ubiquitin-proteasome system. Trends Cell Biol. doi:10.1016/j.tcb.2013.12.003

    PubMed Central  PubMed  Google Scholar 

  • Levine RL, Williams JA, Stadtman ER, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol 233:346–357

    Article  CAS  PubMed  Google Scholar 

  • Lin CH, Li HY, Lee YC, Calkins MJ, Lee KH, Yang CN, Lu PJ (2015) Landscape of Pin1 in the cell cycle. Exp Biol Med. doi:10.1177/1535370215570829

    Google Scholar 

  • Liu X, Miller MJ, Joshi MS, Thomas DD, Lancaster Jr JR (1998) Accelerated reaction of nitric oxide with O2 within the hydrophobic interior of biological membranes. Proc Natl Acad Sci USA 95:2175–2179

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lovell MA, Xie C, Markesbery WR (1998) Decreased glutathione transferase activity in brain and ventricular fluid in Alzheimer’s disease. Neurology 51:1562–1566

    Article  CAS  PubMed  Google Scholar 

  • Lovell MA, Xie C, Markesbery WR (2001) Acrolein is increased in Alzheimer’s disease brain and is toxic to primary hippocampal cultures. Neurobiol Aging 22:187–194

    Article  CAS  PubMed  Google Scholar 

  • Ma SL, Pastorino L, Zhou XZ, Lu KP (2012) Prolyl isomerase Pin1 promotes amyloid precursor protein (APP) turnover by inhibiting glycogen synthase kinase-3beta (GSK3beta) activity: novel mechanism for Pin1 to protect against Alzheimer disease. J Biol Chem. doi:10.1074/jbc.C111.298596

    Google Scholar 

  • Markesbery WR (1997) Oxidative stress hypothesis in Alzheimer’s disease. Free Rad Biol Med 23:134–147

    Article  CAS  PubMed  Google Scholar 

  • Markesbery WR, Kryscio RJ, Lovell MA, Morrow JD (2005) Lipid peroxidation is an early event in the brain in amnestic mild cognitive impairment. Ann Neurol. doi:10.1002/ana.20629

    Google Scholar 

  • McCarty MF (2006) Down-regulation of microglial activation may represent a practical strategy for combating neurodegenerative disorders. Med Hypotheses. doi:10.1016/j.mehy.2006.01.013

    Google Scholar 

  • Moh C, Kubiak JZ, Bajic VP, Zhu X, Smith MA, Lee HG (2011) Cell cycle deregulation in the neurons of Alzheimer’s disease. Result Probl Cell Differ. doi:10.1007/978-3-642-19065-0_23

    Google Scholar 

  • Moller MN, Li Q, Lancaster JR Jr, Denicola A (2007) Acceleration of nitric oxide autoxidation and nitrosation by membranes. IUBMB life. doi:10.1080/15216540701311147

    PubMed  Google Scholar 

  • Nakamura T, Prikhodko OA, Pirie E, Nagar S, Akhtar MW, Oh CK, Lipton SA (2015) Aberrant protein S-nitrosylation contributes to the pathophysiology of neurodegenerative diseases. Neurobiol Dis. doi:10.1016/j.nbd.2015.03.017

    Google Scholar 

  • Nourazarian AR, Kangari P, Salmaninejad A (2014) Roles of oxidative stress in the development and progression of breast cancer. Asian Pac J Cancer Prev 15:4745–4751

    Article  PubMed  Google Scholar 

  • Oddo S (2008) The ubiquitin-proteasome system in Alzheimer’s disease. J Cell Mol Med. doi:10.1111/j.1582-4934.2008.00276.x

    PubMed Central  PubMed  Google Scholar 

  • Olivieri G, Hess C, Savaskan E, Ly C, Meier F, Baysang G, Muller-Spahn F (2001) Melatonin protects SHSY5Y neuroblastoma cells from cobalt-induced oxidative stress, neurotoxicity and increased beta-amyloid secretion. J Pineal Res 31:320–325

    Article  CAS  PubMed  Google Scholar 

  • Perluigi M, Sultana R, Cenini G, Di Domenico F, Memo M, Pierce WM, Butterfield DA (2009) Redox proteomics identification of 4-hydroxynonenal-modified brain proteins in Alzheimer’s disease: Role of lipid peroxidation in Alzheimer’s disease pathogenesis. Proteomics Clin Appl. doi:10.1002/prca.200800161

    PubMed Central  PubMed  Google Scholar 

  • Perluigi M, Coccia R, Butterfield DA (2012) 4-Hydroxy-2-nonenal, a reactive product of lipid peroxidation, and neurodegenerative diseases: a toxic combination illuminated by redox proteomics studies. Antioxid Redox Signal. doi:10.1089/ars.2011.4406

    Google Scholar 

  • Perluigi M, Swomley AM, Butterfield DA (2014) Redox proteomics and the dynamic molecular landscape of the aging brain. Ageing Res Rev. doi:10.1016/j.arr.2013.12.005

    PubMed  Google Scholar 

  • Pickering AM, Davies KJ (2012) Degradation of damaged proteins: the main function of the 20S proteasome. Prog Mol Biol Transl Sci. doi:10.1016/B978-0-12-397863-9.00006-7

    PubMed Central  PubMed  Google Scholar 

  • Quintanilla RA, Munoz FJ, Metcalfe MJ, Hitschfeld M, Olivares G, Godoy JA, Inestrosa NC (2005) Trolox and 17beta-estradiol protect against amyloid beta-peptide neurotoxicity by a mechanism that involves modulation of the Wnt signaling pathway. J Biol Chem. doi:10.1074/jbc.M411936200

    Google Scholar 

  • Rapoport SI (1999) In vivo PET imaging and postmortem studies suggest potentially reversible and irreversible stages of brain metabolic failure in Alzheimer’s disease. Eur Arch Psychiatry Clin Neurosci 893:46–55

    Article  Google Scholar 

  • Reed T, Perluigi M, Sultana R, Pierce WM, Klein JB, Turner DM, Butterfield DA (2008) Redox proteomic identification of 4-hydroxy-2-nonenal-modified brain proteins in amnestic mild cognitive impairment: insight into the role of lipid peroxidation in the progression and pathogenesis of Alzheimer’s disease. Neurobiol Dis. doi:10.1016/j.nbd.2007.12.007

    PubMed  Google Scholar 

  • Riederer IM, Schiffrin M, Kovari E, Bouras C, Riederer BM (2009) Ubiquitination and cysteine nitrosylation during aging and Alzheimer’s disease. Brain Res Bull. doi:10.1016/j.brainresbull.2009.04.018

    Google Scholar 

  • Sayre LM, Zelasko DA, Harris PL, Perry G, Salomon RG, Smith MA (1997) 4-Hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzheimer’s disease. J Neurochem 68:2092–2097

    Article  CAS  PubMed  Google Scholar 

  • Shinde UA, Mehta AA, Goyal RK (2000) Nitric oxide: a molecule of the millennium. Indian J Exp Biol 38:201–210

    CAS  PubMed  Google Scholar 

  • Stadtman ER, Levine RL (2000) Protein oxidation. Ann Ny Acad Sci 899:191–208

    Article  CAS  PubMed  Google Scholar 

  • Subramanian A, Miller DM (2000) Structural analysis of alpha-enolase. Mapping the functional domains involved in down-regulation of the c-myc protooncogene. J Biol Chem 275:5958–5965

    Article  CAS  PubMed  Google Scholar 

  • Sultana R, Butterfield DA (2004) Oxidatively modified GST and MRP1 in Alzheimer’s disease brain: implications for accumulation of reactive lipid peroxidation products. Neurochem Res 29:2215–2220

    Article  CAS  PubMed  Google Scholar 

  • Sultana R, Boyd-Kimball D, Poon HF, Cai J, Pierce WM, Klein JB, Butterfield DA (2006a) Redox proteomics identification of oxidized proteins in Alzheimer’s disease hippocampus and cerebellum: an approach to understand pathological and biochemical alterations in AD. Neurobiol Aging. doi:10.1016/j.neurobiolaging.2005.09.021

    Google Scholar 

  • Sultana R, Poon HF, Cai J, Pierce WM, Merchant M, Klein JB, Butterfield DA (2006b) Identification of nitrated proteins in Alzheimer’s disease brain using a redox proteomics approach. Neurobiol Dis. doi:10.1016/j.nbd.2005.10.004

    Google Scholar 

  • Sultana R, Boyd-Kimball D, Poon HF, Cai J, Pierce WM, Klein JB, Butterfield DA (2006c) Oxidative modification and down-regulation of Pin1 in Alzheimer’s disease hippocampus: a redox proteomics analysis. Neurobiol Aging. doi:10.1016/j.neurobiolaging.2005.05.005

    Google Scholar 

  • Sultana R, Reed T, Perluigi M, Coccia R, Pierce WM, Butterfield DA (2007) Proteomic identification of nitrated brain proteins in amnestic mild cognitive impairment: a regional study. J Cell Mol Med. doi:10.1111/j.1582-4934.2007.00065.x

    PubMed Central  PubMed  Google Scholar 

  • Sultana R, Perluigi M, Butterfield DA (2009) Oxidatively modified proteins in Alzheimer’s disease (AD), mild cognitive impairment and animal models of AD: role of Abeta in pathogenesis. Acta Neuropathol. doi:10.1007/s00401-009-0517-0

    PubMed Central  PubMed  Google Scholar 

  • Suzuki YJ, Carini M, Butterfield DA (2010) Protein carbonylation. Antioxid Redox Signal. doi:10.1089/ars.2009.2887

    Google Scholar 

  • Takei N, Kondo J, Nagaike K, Ohsawa K, Kato K, Kohsaka S (1991) Neuronal survival factor from bovine brain is identical to neuron-specific enolase. J Neurochem 57:1178–1184

    Article  CAS  PubMed  Google Scholar 

  • Tangvarasittichai S (2015) Oxidative stress, insulin resistance, dyslipidemia and type 2 diabetes mellitus. World J Diabetes. doi:10.4239/wjd.v6.i3.456

    PubMed Central  PubMed  Google Scholar 

  • Tu S, Okamoto S, Lipton SA, Xu H (2014) Oligomeric abeta-induced synaptic dysfunction in Alzheimer’s disease. Mol Neurodegener. doi:10.1186/1750-1326-9-48

    PubMed Central  PubMed  Google Scholar 

  • Uttara B, Singh AV, Zamboni P, Mahajan RT (2009) Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol. doi:10.2174/157015909787602823

    PubMed Central  PubMed  Google Scholar 

  • Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. doi:10.1016/j.biocel.2006.07.001

    PubMed  Google Scholar 

  • van der Lee R, Buljan M, Lang B, Weatheritt RJ, Daughdrill GW, Dunker AK, Babu MM (2014) Classification of intrinsically disordered regions and proteins. Chem Rev. doi:10.1021/cr400525m

    Google Scholar 

  • Walsh DM, Selkoe DJ (2004) Oligomers on the brain: the emerging role of soluble protein aggregates in neurodegeneration. Protein Pept Lett 11:213–228

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Kettenhofen NJ, Shiva S, Hogg N, Gladwin MT (2008) Copper dependence of the biotin switch assay: modified assay for measuring cellular and blood nitrosated proteins. Free Rad Biol Med. doi:10.1016/j.freeradbiomed.2007.12.032

    Google Scholar 

  • Wilkins HM, Carl SM, Greenlief AC, Festoff BW, Swerdlow RH (2014) Bioenergetic dysfunction and inflammation in Alzheimer’s disease: a possible connection. Front Aging Neurosci. doi:10.3389/fnagi.2014.00311

    PubMed Central  PubMed  Google Scholar 

  • Williamson KS, Gabbita SP, Mou S, West M, Pye QN, Markesbery WR, Hensley K (2002) The nitration product 5-nitro-gamma-tocopherol is increased in the Alzheimer brain. Nitric oxide Biol Chem. doi:10.1006/niox.2001.0399

    Google Scholar 

  • Xu W, Charles IG, Moncada S, Gorman P, Sheer D, Liu L, Emson P (1994) Mapping of the genes encoding human inducible and endothelial nitric oxide synthase (NOS2 and NOS3) to the pericentric region of chromosome 17 and to chromosome 7, respectively. Genomics. doi:10.1006/geno.1994.1286

    Google Scholar 

  • Yao Y, Zhukareva V, Sung S, Clark CM, Rokach J, Lee VM, Pratico D (2003) Enhanced brain levels of 8,12-iso-iPF2alpha-VI differentiate AD from frontotemporal dementia. Neurology 61:475–478

    Article  CAS  PubMed  Google Scholar 

  • Yatin SM, Varadarajan S, Link CD, Butterfield DA (1999) In vitro and in vivo oxidative stress associated with Alzheimer’s amyloid beta-peptide (1–42). Neurobiol Aging 20:325–330 (discussion 339–342)

    Article  CAS  PubMed  Google Scholar 

  • Yatin SM, Varadarajan S, Butterfield DA (2000) Vitamin E prevents Alzheimer’s amyloid beta-peptide (1–42)-induced neuronal protein oxidation and reactive oxygen species production. J Alzheimer’s Dis 123–131

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  1. Department of Chemistry and Sanders-Brown Center on Aging, University of Kentucky, Lexington, KY, 40506-0055, USA

    Aaron M. Swomley & D. Allan Butterfield

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Swomley, A.M., Butterfield, D. Oxidative stress in Alzheimer disease and mild cognitive impairment: evidence from human data provided by redox proteomics. Arch Toxicol 89, 1669–1680 (2015). https://doi.org/10.1007/s00204-015-1556-z

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