Oxidative stress, protein modification and Alzheimer disease

Brain Research Bulletin

Volumn 133, Issue , 2017, Pages 88-96

  Tramutola, A ^a   Lanzillotta, C ^a   Perluigi, M ^a   Butterfield, D Allan ^b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Alzheimer disease; ATP synthase; Glucose metabolism; Oxidative stress; Protein oxidation

Indexed keywords

PROTEOME; AMYLOID BETA PROTEIN; GLUCOSE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REACTIVE OXYGEN METABOLITE;

ALZHEIMER DISEASE; AUTOPSY; BRAIN FUNCTION; CELL CYCLE PROGRESSION; CELL STRUCTURE; ENERGY METABOLISM; GLUCOSE METABOLISM; HOMEOSTASIS; HUMAN; MILD COGNITIVE IMPAIRMENT; NERVE DEGENERATION; NEUROPATHOLOGY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; ANIMAL; BRAIN; DEGENERATIVE DISEASE; DISEASE EXACERBATION; DISEASE MODEL; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; PROTEIN DEGRADATION; PROTEIN PROCESSING;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GLUCOSE; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTON-TRANSLOCATING ATPASES; NEURODEGENERATIVE DISEASES; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; PROTEOMICS; REACTIVE OXYGEN SPECIES;

EID: 84981494654     PISSN: 03619230     EISSN: 18732747     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2016.06.005     Document Type: Review

References (90)

1. Aluise, C.D., Robinson, R.A., Beckett, T.L., Murphy, M.P., Cai, J., Pierce, W.M., Markesbery, W.R., Butterfield, D.A., Preclinical Alzheimer disease: brain oxidative stress, Abeta peptide and proteomics. Neurobiol. Dis. 39 (2010), 221–228.
2. Aluise, C.D., Robinson, R.A., Cai, J., Pierce, W.M., Markesbery, W.R., Butterfield, D.A., 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. Alzheimers Dis. 23 (2011), 257–269.
3. Andreadis, A., Brown, W.M., Kosik, K.S., Structure and novel exons of the human tau gene. Biochemistry 31 (1992), 10626–10633.
4. Assoc, A., Alzheimer's association report 2015 Alzheimer's disease facts and figures. Alzheimers Dement. 12 (2016), 1–81.
5. Barone, E., Di Domenico, F., Cassano, T., Arena, A., Tramutola, A., Lavecchia, M.A., Coccia, R., Butterfield, D.A., Perluigi, M., Impairment of biliverdin reductase-A promotes brain insulin resistance in Alzheimer disease: a new paradigm. Free Radic. Biol. Med. 91 (2016), 127–142.
6. Beckman, J.S., Protein tyrosine nitration and peroxynitrite. FASEB J., 16, 2002, 1144.
7. Boutte, A.M., Woltjer, R.L., Zimmerman, L.J., Stamer, S.L., Montine, K.S., Manno, M.V., Cimino, P.J., Liebler, D.C., Montine, T.J., Selectively increased oxidative modifications mapped to detergent-insoluble forms of Abeta and beta-III tubulin in Alzheimer's disease. FASEB J. 20 (2006), 1473–1483.
8. Braak, E., Braak, H., Alzheimer's disease: transiently developing dendritic changes in pyramidal cells of sector CA1 of the Ammon's horn. Acta Neuropathol. 93 (1997), 323–325.
9. Bradley, M.A., Markesbery, W.R., Lovell, M.A., Increased levels of 4-hydroxynonenal and acrolein in the brain in preclinical Alzheimer disease. Free Radic. Biol. Med. 48 (2010), 1570–1576.
10. Broniowska, K.A., Hogg, N., The chemical biology of S-nitrosothiols. Antioxid. Redox Signal. 17 (2012), 969–980.
11. Butterfield, D.A., Boyd-Kimball, D., The critical role of methionine 35 in Alzheimer's amyloid beta-peptide (1–42)-induced oxidative stress and neurotoxicity. Biochim. Biophys. Acta 1703 (2005), 149–156.
12. Butterfield, D.A., Dalle-Donne, I., Redox proteomics. Antioxid. Redox Signal. 17 (2012), 1487–1489.
13. Butterfield, D.A., Kanski, J., Brain protein oxidation in age-related neurodegenerative disorders that are associated with aggregated proteins. Mech. Ageing Dev. 122 (2001), 945–962.
14. Butterfield, D.A., Lange, M.L., Multifunctional roles of enolase in Alzheimer's disease brain: beyond altered glucose metabolism. J. Neurochem. 111 (2009), 915–933.
15. Butterfield, D.A., Lauderback, C.M., Lipid peroxidation and protein oxidation in Alzheimer's disease brain: potential causes and consequences involving amyloid beta-peptide-associated free radical oxidative stress. Free Radic. Biol. Med. 32 (2002), 1050–1060.
16. Butterfield, D.A., Stadtman, E., Protein oxidation process ina ging brain. Adv. Cell Aging Gerontol. 2 (1997), 161–191.
17. Butterfield, D.A., Sultana, R., Redox proteomics: understanding oxidative stress in the progression of age-related neurodegenerative disorders. Expert Rev. Proteom. 5 (2008), 157–160.
18. Butterfield, D.A., Sultana, R., Methionine-35 of abeta(1–42): importance for oxidative stress in Alzheimer disease. J. Amino Acids, 2011, 2011, 198430.
19. Butterfield, D.A., Drake, J., Pocernich, C., Castegna, A., Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta-peptide. Trends Mol. Med. 7 (2001), 548–554.
20. Butterfield, D.A., Reed, T., Perluigi, M., De Marco, C., Coccia, R., Cini, C., Sultana, R., Elevated protein-bound levels of the lipid peroxidation product 4-hydroxy-2-nonenal, in brain from persons with mild cognitive impairment. Neurosci. Lett. 397 (2006), 170–173.
21. Butterfield, D.A., Reed, T., Newman, S.F., Sultana, R., Roles of amyloid beta-peptide-associated oxidative stress and brain protein modifications in the pathogenesis of Alzheimer's disease and mild cognitive impairment. Free Radic. Biol. Med. 43 (2007), 658–677.
22. Butterfield, D.A., Reed, T.T., Perluigi, M., De Marco, C., Coccia, R., Keller, J.N., Markesbery, W.R., Sultana, R., Elevated levels of 3-nitrotyrosine in brain from subjects with amnestic mild cognitive impairment: implications for the role of nitration in the progression of Alzheimer's disease. Brain Res. 1148 (2007), 243–248.
23. Butterfield, D.A., Bader Lange, M.L., Sultana, R., Involvements of the lipid peroxidation product, HNE, in the pathogenesis and progression of Alzheimer's disease. Biochim. Biophys. Acta 1801 (2010), 924–929.
24. Butterfield, D.A., Galvan, V., Lange, M.B., Tang, H., Sowell, R.A., Spilman, P., Fombonne, J., Gorostiza, O., Zhang, J., Sultana, R., Bredesen, D.E., In vivo oxidative stress in brain of Alzheimer disease transgenic mice: requirement for methionine 35 in amyloid beta-peptide of APP. Free Radic. Biol. Med. 48 (2010), 136–144.
25. Butterfield, D.A., Perluigi, M., Reed, T., Muharib, T., Hughes, C.P., Robinson, R.A., Sultana, R., Redox proteomics in selected neurodegenerative disorders: from its infancy to future applications. Antioxid. Redox Signal. 17 (2012), 1610–1655.
26. Butterfield, D.A., Swomley, A.M., Sultana, R., Amyloid beta-peptide (1–42)-induced oxidative stress in Alzheimer disease: importance in disease pathogenesis and progression. Antioxid. Redox Signal. 19 (2013), 823–835.
27. Butterfield, D.A., Di Domenico, F., Barone, E., Elevated risk of type 2 diabetes for development of Alzheimer disease: a key role for oxidative stress in brain. Biochim. Biophys. Acta 1842 (2014), 1693–1706.
28. Butterfield, D.A., Gu, L., Di Domenico, F., Robinson, R.A., Mass spectrometry and redox proteomics: applications in disease. Mass Spectrom. Rev. 33 (2014), 277–301.
29. Butterfield, D.A., Amyloid beta-peptide (1–42)-induced oxidative stress and neurotoxicity: implications for neurodegeneration in Alzheimer's disease brain. A review. Free Radic. Res. 36 (2002), 1307–1313.
30. Chen, Z., Zhong, C., Decoding Alzheimer's disease from perturbed cerebral glucose metabolism: implications for diagnostic and therapeutic strategies. Prog. Neurobiol. 108 (2013), 21–43.
31. Clark, T.A., Lee, H.P., Rolston, R.K., Zhu, X., Marlatt, M.W., Castellani, R.J., Nunomura, A., Casadesus, G., Smith, M.A., Lee, H.G., Perry, G., Oxidative stress and its implications for future treatments and management of Alzheimer disease. Int. J. Biomed. Sci. 6 (2010), 225–227.
32. De Felice, F.G., Vieira, M.N., Bomfim, T.R., Decker, H., Velasco, P.T., Lambert, M.P., Viola, K.L., Zhao, W.Q., Ferreira, S.T., Klein, W.L., Protection of synapses against Alzheimer's-linked toxins: insulin signaling prevents the pathogenic binding of Abeta oligomers. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 1971–1976.
33. Dean, R.T., Fu, S., Stocker, R., Davies, M.J., Biochemistry and pathology of radical-mediated protein oxidation. Biochem. J. 324:Pt. 1 (1997), 1–18.
34. Dildar, K., Sinem, F., Gokhan, E., Orhan, Y., Filiz, M., Serum nitrosative stress levels are increased in Alzheimer disease but not in vascular dementia. Alzheimer Dis. Assoc. Disord. 24 (2010), 194–197.
35. Gururaj, A., Barnes, C.J., Vadlamudi, R.K., Kumar, R., Regulation of phosphoglucomutase 1 phosphorylation and activity by a signaling kinase. Oncogene 23 (2004), 8118–8127.
36. Halliwell, B., Oxidative stress and neurodegeneration: where are we now?. J. Neurochem. 97 (2006), 1634–1658.
37. Hensley, K., Williamson, K.S., Floyd, R.A., Measurement of 3-nitrotyrosine and 5-nitro-gamma-tocopherol by high-performance liquid chromatography with electrochemical detection. Free Radic. Biol. Med. 28 (2000), 520–528.
38. Hoyer, S., Glucose metabolism and insulin receptor signal transduction in Alzheimer disease. Eur. J. Pharmacol. 490 (2004), 115–125.
39. Ischiropoulos, H., Beckman, J.S., Oxidative stress and nitration in neurodegeneration: cause effect, or association?. J. Clin. Invest. 111 (2003), 163–169.
40. Kim, T.S., Pae, C.U., Yoon, S.J., Jang, W.Y., Lee, N.J., Kim, J.J., Lee, S.J., Lee, C., Paik, I.H., Lee, C.U., Decreased plasma antioxidants in patients with Alzheimer's disease. Int. J. Geriatr. Psychiatry 21 (2006), 344–348.
41. Korolainen, M.A., Goldsteins, G., Alafuzoff, I., Koistinaho, J., Pirttila, T., Proteomic analysis of protein oxidation in Alzheimer's disease brain. Electrophoresis 23 (2002), 3428–3433.
42. Korolainen, M.A., Nyman, T.A., Nyyssonen, P., Hartikainen, E.S., Pirttila, T., Multiplexed proteomic analysis of oxidation and concentrations of cerebrospinal fluid proteins in Alzheimer disease. Clin. Chem. 53 (2007), 657–665.
43. Lambert, M.P., Barlow, A.K., Chromy, B.A., Edwards, C., Freed, R., Liosatos, M., Morgan, T.E., Rozovsky, I., Trommer, B., Viola, K.L., Wals, P., Zhang, C., Finch, C.E., Krafft, G.A., Klein, W.L., Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U. S. A. 95 (1998), 6448–6453.
44. Lamers, K.J., Vos, P., Verbeek, M.M., Rosmalen, F., van Geel, W.J., van Engelen, B.G., Protein S-100B neuron-specific enolase (NSE), myelin basic protein (MBP) and glial fibrillary acidic protein (GFAP) in cerebrospinal fluid (CSF) and blood of neurological patients. Brain Res. Bull. 61 (2003), 261–264.
45. Levine, R.L., Williams, J.A., Stadtman, E.R., Shacter, E., Carbonyl assays for determination of oxidatively modified proteins. Methods Enzymol. 233 (1994), 346–357.
46. Lopez-Sanchez, L.M., Corrales, F.J., Gonzalez, R., Ferrin, G., Munoz-Castaneda, J.R., Ranchal, I., Hidalgo, A.B., Briceno, J., Lopez-Cillero, P., Gomez, M.A., De La Mata, M., Muntane, J., Rodriguez-Ariza, A., Alteration of S-nitrosothiol homeostasis and targets for protein S-nitrosation in human hepatocytes. Proteomics 8 (2008), 4709–4720.
47. Lovell, M.A., Xie, C., Xiong, S., Markesbery, W.R., Protection against amyloid beta peptide and iron/hydrogen peroxide toxicity by alpha lipoic acid. J. Alzheimers Dis. 5 (2003), 229–239.
48. Maczurek, A., Hager, K., Kenklies, M., Sharman, M., Martins, R., Engel, J., Carlson, D.A., Munch, G., Lipoic acid as an anti-inflammatory and neuroprotective treatment for Alzheimer's disease. Adv. Drug Deliv. Rev. 60 (2008), 1463–1470.
49. Markesbery, W.R., Lovell, M.A., Four-hydroxynonenal a product of lipid peroxidation, is increased in the brain in Alzheimer's disease. Neurobiol. Aging 19 (1998), 33–36.
50. Masters, C.L., Simms, G., Weinman, N.A., Multhaup, G., McDonald, B.L., Beyreuther, K., Amyloid plaque core protein in Alzheimer disease and down syndrome. Proc. Natl. Acad. Sci. U. S. A. 82 (1985), 4245–4249.
51. Mecocci, P., MacGarvey, U., Beal, M.F., Oxidative damage to mitochondrial DNA is increased in Alzheimer's disease. Ann. Neurol. 36 (1994), 747–751.
52. Morris, J.C., Cummings, J., Mild cognitive impairment (MCI) represents early-stage Alzheimer's disease. J. Alzheimers Dis. 7 (2005), 235–239 (discussion 255–262).
53. Moskovitz, J., Maiti, P., Lopes, D.H., Oien, D.B., Attar, A., Liu, T., Mittal, S., Hayes, J., Bitan, G., Induction of methionine-sulfoxide reductases protects neurons from amyloid beta-protein insults in vitro and in vivo. Biochemistry 50 (2011), 10687–10697.
54. Newington, J.T., Harris, R.A., Cumming, R.C., Reevaluating metabolism in Alzheimer's disease from the perspective of the astrocyte-neuron lactate shuttle model. J. Neurodegener. Dis., 2013, 2013, 234572.
55. Newman, S.F., Sultana, R., Perluigi, M., Coccia, R., Cai, J., Pierce, W.M., Klein, J.B., Turner, D.M., Butterfield, D.A., An increase in S-glutathionylated proteins in the Alzheimer's disease inferior parietal lobule, a proteomics approach. J. Neurosci. Res. 85 (2007), 1506–1514.
56. Ohta, S., Ohsawa, I., Dysfunction of mitochondria and oxidative stress in the pathogenesis of Alzheimer's disease: on defects in the cytochrome c oxidase complex and aldehyde detoxification. J. Alzheimers Dis. 9 (2006), 155–166.
57. Oien, D.B., Moskovitz, J., Substrates of the methionine sulfoxide reductase system and their physiological relevance. Curr. Top. Dev. Biol. 80 (2008), 93–133.
58. Opii, W.O., Joshi, G., Head, E., Milgram, N.W., Muggenburg, B.A., Klein, J.B., Pierce, W.M., Cotman, C.W., Butterfield, D.A., Proteomic identification of brain proteins in the canine model of human aging following a long-term treatment with antioxidants and a program of behavioral enrichment: relevance to Alzheimer's disease. Neurobiol. Aging 29 (2008), 51–70.
59. Orosz, F., Olah, J., Ovadi, J., Triosephosphate isomerase deficiency: facts and doubts. IUBMB Life 58 (2006), 703–715.
60. Palmer, A.M., The activity of the pentose phosphate pathway is increased in response to oxidative stress in Alzheimer's disease. J. Neural Transm. 106 (1999), 317–328.
61. Pasinetti, G.M., Wang, J., Porter, S., Ho, L., Caloric intake, dietary lifestyles, macronutrient composition, and Alzheimer's disease dementia. Int. J. Alzheimers Dis., 2011, 2011, 806293.
62. Perluigi, M., Sultana, R., Cenini, G., Di Domenico, F., Memo, M., Pierce, W.M., Coccia, R., Butterfield, D.A., Redox proteomics identification of 4-hydroxynonenal-modified brain proteins in Alzheimer's disease: role of lipid peroxidation in Alzheimer's disease pathogenesis. Proteom. Clin. Appl. 3 (2009), 682–693.
63. Petersen, R.C., Doody, R., Kurz, A., Mohs, R.C., Morris, J.C., Rabins, P.V., Ritchie, K., Rossor, M., Thal, L., Winblad, B., Current concepts in mild cognitive impairment. Arch. Neurol. 58 (2001), 1985–1992.
64. Price, J.L., Morris, J.C., Tangles and plaques in nondemented aging and preclinical Alzheimer's disease. Ann. Neurol. 45 (1999), 358–368.
65. Ray, P.D., Huang, B.W., Tsuji, Y., Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal. 24 (2012), 981–990.
66. Reddy, V.P., Zhu, X., Perry, G., Smith, M.A., Oxidative stress in diabetes and Alzheimer's disease. J. Alzheimers Dis. 16 (2009), 763–774.
67. Reed, T., Perluigi, M., Sultana, R., Pierce, W.M., Klein, J.B., Turner, D.M., Coccia, R., Markesbery, W.R., Butterfield, D.A., 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. 30 (2008), 107–120.
68. Schopfer, F.J., Baker, P.R., Freeman, B.A., NO-dependent protein nitration: a cell signaling event or an oxidative inflammatory response?. Trends Biochem. Sci. 28 (2003), 646–654.
69. Selfridge, J.E., Lu, L.E.J., Swerdlow, R.H., Role of mitochondrial homeostasis and dynamics in Alzheimer's disease. Neurobiol. Dis. 51 (2013), 3–12.
70. Selkoe, D.J., Alzheimer's disease: genes, proteins, and therapy. Physiol. Rev. 81 (2001), 741–766.
71. Selkoe, D.J., Biochemistry and molecular biology of amyloid beta-protein and the mechanism of Alzheimer's disease. Handb. Clin. Neurol. 89 (2008), 245–260.
72. Seth, D., Stamler, J.S., The SNO-proteome: causation and classifications. Curr. Opin. Chem. Biol. 15 (2011), 129–136.
73. Smith, M.A., Sayre, L.M., Anderson, V.E., Harris, P.L., Beal, M.F., Kowall, N., Perry, G., Cytochemical demonstration of oxidative damage in Alzheimer disease by immunochemical enhancement of the carbonyl reaction with 2,4-dinitrophenylhydrazine. J. Histochem. Cytochem. 46 (1998), 731–735.
74. Stamler, J.S., Singel, D.J., Loscalzo, J., Biochemistry of nitric oxide and its redox-activated forms. Science 258 (1992), 1898–1902.
75. Stewart, A.G., Laming, E.M., Sobti, M., Stock, D., Rotary ATPases—dynamic molecular machines. Curr. Opin. Struct. Biol. 25 (2014), 40–48.
76. Sultana, R., Boyd-Kimball, D., Poon, H.F., Cai, J., Pierce, W.M., Klein, J.B., Merchant, M., Markesbery, W.R., Butterfield, D.A., 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 27 (2006), 1564–1576.
77. Sultana, R., Perluigi, M., Butterfield, D.A., Redox proteomics identification of oxidatively modified proteins in Alzheimer's disease brain and in vivo and in vitro models of AD centered around Abeta(1–42). J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 833 (2006), 3–11.
78. Sultana, R., Perluigi, M., Butterfield, D.A., Oxidatively modified proteins in Alzheimer's disease (AD), mild cognitive impairment and animal models of AD: role of Abeta in pathogenesis. Acta Neuropathol. 118 (2009), 131–150.
79. Sultana, R., Mecocci, P., Mangialasche, F., Cecchetti, R., Baglioni, M., Butterfield, D.A., Increased protein and lipid oxidative damage in mitochondria isolated from lymphocytes from patients with Alzheimer's disease: insights into the role of oxidative stress in Alzheimer's disease and initial investigations into a potential biomarker for this dementing disorder. J. Alzheimers Dis. 24 (2011), 77–84.
80. Sultana, R., Baglioni, M., Cecchetti, R., Cai, J., Klein, J.B., Bastiani, P., Ruggiero, C., Mecocci, P., Butterfield, D.A., Lymphocyte mitochondria: toward identification of peripheral biomarkers in the progression of Alzheimer disease. Free Radic. Biol. Med. 65 (2013), 595–606.
81. Suzuki, Y.J., Carini, M., Butterfield, D.A., Protein carbonylation. Antioxid. Redox Signal. 12 (2010), 323–325.
82. Swomley, A.M., Forster, S., Keeney, J.T., Triplett, J., Zhang, Z., Sultana, R., Butterfield, D.A., Abeta, oxidative stress in Alzheimer disease: evidence based on proteomics studies. Biochim. Biophys. Acta 1842 (2014), 1248–1257.
83. Terni, B., Boada, J., Portero-Otin, M., Pamplona, R., Ferrer, I., Mitochondrial ATP-synthase in the entorhinal cortex is a target of oxidative stress at stages I/II of Alzheimer's disease pathology. Brain Pathol. 20 (2010), 222–233.
84. Tiwari, V., Patel, A.B., Pyruvate carboxylase and pentose phosphate fluxes are reduced in AbetaPP-PS1 mouse model of Alzheimer's disease: a (1)(3)C NMR study. J. Alzheimers Dis. 41 (2014), 387–399.
85. Varadarajan, S., Kanski, J., Aksenova, M., Lauderback, C., Butterfield, D.A., Different mechanisms of oxidative stress and neurotoxicity for Alzheimer's A beta(1–42) and A beta(25–35). J. Am. Chem. Soc. 123 (2001), 5625–5631.
86. Yatin, S.M., Varadarajan, S., Link, C.D., Butterfield, D.A., In vitro and in vivo oxidative stress associated with Alzheimer's amyloid beta-peptide (1–42). Neurobiol. Aging 20 (1999), 325–330 (discussion 339–342).
87. Yeo, W.S., Lee, S.J., Lee, J.R., Kim, K.P., Nitrosative protein tyrosine modifications: biochemistry and functional significance. BMB Rep. 41 (2008), 194–203.
88. Zahid, S., Khan, R., Oellerich, M., Ahmed, N., Asif, A.R., Differential S-nitrosylation of proteins in Alzheimer's disease. Neuroscience 256 (2014), 126–136.
89. Zhang, Z., Wu, S., Stenoien, D.L., Pasa-Tolic, L., High-throughput proteomics. Annu. Rev. Anal. Chem. (Palo Alto Calif.) 7 (2014), 427–454.
90. Zhao, Y., Zhao, B., Oxidative stress and the pathogenesis of Alzheimer's disease. Oxid. Med. Cell. Longev., 2013, 2013, 316523.