Role of by-products of lipid oxidation in Alzheimer's disease brain: A focus on acrolein

Journal of Alzheimer's Disease

Volumn 21, Issue 3, 2010, Pages 741-756

  Singh, Manjeet ^a   Nam, Dang Thanh ^a   Arseneault, Madeleine ^a   Ramassamy, Charles ^a  

^a INRS INSTITUT ARMAND FRAPPIER   (Canada)

Author keywords

4 hydroxy nonenal; Arachidonic acid; docosahexaenoic acid; isoprostanes; neuroprostanes; oxidative stress; polyamines

Indexed keywords

4 HYDROXYNONENAL; ACROLEIN; GLUTATHIONE; HISTIDINE; ISOPROSTANE DERIVATIVE; MALONALDEHYDE; NEUROPROSTANE DERIVATIVE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; BRAIN LEVEL; HIPPOCAMPUS; HUMAN; LIPID OXIDATION; MILD COGNITIVE IMPAIRMENT; NEUROTOXICITY; NEUROTRANSMISSION; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; TEMPORAL CORTEX;

EID: 77957256030     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2010-100405     Document Type: Review

References (127)

1. Smith MA, Harris PL, Sayre LM, Perry G (1997) Iron accumulation in Alzheimer disease is a source of redoxgenerated free radicals. Proc Natl Acad Sci U S A 94, 98669868. (Pubitemid 27408156)
2. Sayre LM, Perry G, Smith MA (1999) Redox metals and neurodegenerative disease. Curr Opin Chem Biol 3, 220225. (Pubitemid 29145789)
3. Rhein V, Song X, Wiesner A, Ittner LM, Baysang G, Meier F, Ozmen L, Bluethmann H, Drose S, Brandt U, Savaskan E, Czech C, Gotz J, Eckert A (2009) Amyloidbeta and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer's diseasemice. ProcNatl Acad Sci U S A 106, 2005720062.
4. Aliev G, Palacios HH, Walrafen B, Lipsitt AE, Obrenovich ME, Morales L (2009) Brain mitochondria as a primary target in the development of treatment strategies for Alzheimer disease. Int J Biochem Cell Biol 41, 19892004.
5. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297, 353356. (Pubitemid 34790756)
6. Hardy J (2009) The amyloid hypothesis for Alzheimer's disease: A critical reappraisal. J Neurochem 110, 11291134.
7. Christen Y (2000) Oxidative stress and Alzheimer disease. Am J Clin Nutr 71, 621S629.S. (Pubitemid 30061247)
8. Sonnen JA, Breitner JC, LovellMA,Markesbery WR, Quinn JF,Montine TJ (2008) Free radicalmediated damage to brain in Alzheimer's disease and its transgenic mousemodels. Free Radic Biol Med 45, 219230.
9. MarkesberyWR, Kryscio RJ, LovellMA,Morrow JD (2005) Lipid peroxidation is an early event in the brain in amnestic mild cognitive impairment. Ann Neurol 58, 730735.
10. AnsariMA, Scheff SWOxidative stress in the progression of Alzheimer disease in the frontal cortex. J Neuropathol Exp Neurol 69, 155167.
11. Perluigi M, Sultana R, Cenini G, Di Domenico F, Memo M, Pierce WM, Coccia R, Butterfield DA (2009) Redox proteomics identification of 4hydroxynonenalmodified brain proteins in Alzheimer's disease: Role of lipid peroxidation in Alzheimer's disease pathogenesis. Proteomics Clin Appl 3, 682693.
12. Casadesus G, Smith MA, Basu S, Hua J, Capobianco DE, Siedlak SL, ZhuX, Perry G (2007) Increased isoprostane and prostaglandin are prominent in neurons inAlzheimer disease. Mol Neurodegener 2, 2. (Pubitemid 46698832)
13. Reed TT, Pierce WM, Markesbery WR, Butterfield DA (2009) Proteomic identification of HNEbound proteins in early Alzheimer disease: Insights into the role of lipid peroxidation in the progression of AD. Brain Res 1274, 6676.
14. Sultana N (2009) Proteomics identification of carbonylated and HNEbound brain proteins in Alzheimer's disease. Methods Mol Biol 566, 123135.
15. Calingasan NY, Uchida KGibson GE (1999) Proteinbound acrolein: A novel marker of oxidative stress in Alzheimer's disease. J Neurochem 72, 751756. (Pubitemid 29055239)
16. Sayre LM, Zelasko DA, Harris PL, Perry G, Salomon RG, SmithMA (1997) 4Hydroxynonenalderived advanced lipid peroxidation end products are increased in Alzheimer's disease. J Neurochem 68, 20922097. (Pubitemid 27176147)
17. Montine KS, Olson SJ, Amarnath V, Whetsell WO, Jr., Graham DG, Montine TJ (1997) Immunohistochemical detection of 4hydroxy2nonenal adducts in Alzheimer's disease is associated with inheritance of APOE4. Am J Pathol 150, 437443. (Pubitemid 27073773)
18. Ramassamy C, Averill D, Beffert U, Bastianetto S, Theroux L, LussierCacan S, Cohn JS, Christen Y, Davignon J, Quirion R, Poirier J (1999) Oxidative damage and protection by antioxidants in the frontal cortex of Alzheimer's disease is related to the apolipoprotein E genotype. Free Radic Biol Med 27, 544553. (Pubitemid 29408640)
19. Ramassamy C, Averill D, Beffert U, Theroux L, LussierCacan S, Cohn JS, ChristenY, SchoofsA,Davignon J, Poirier J (2000) Oxidative insults are associated with apolipoprotein E genotype in Alzheimer's disease brain. Neurobiol Dis 7, 2337. (Pubitemid 30141817)
20. Markesbery WR, Lovell MA (1998) Fourhydroxynonenal, a product of lipid peroxidation, is increased in the brain in Alzheimer's disease. Neurobiol Aging 19, 3336. (Pubitemid 28167792)
21. Montine KS, Reich E, Neely MD, Sidell KR, Olson SJ, Markesbery WR, Montine TJ (1998) Distribution of reducible 4hydroxynonenal adduct immunoreactivity in Alzheimer disease is associated with APOE genotype. J Neuropathol Exp Neurol 57, 415425. (Pubitemid 28237325)
22. Tamagno E, Parola M, Bardini P, Piccini A, Borghi R, Guglielmotto M, Santoro G, Davit A, Danni O, Smith MA, Perry G, Tabaton M (2005) Betasite APP cleaving enzyme upregulation induced by 4hydroxynonenal is mediated by stressactivated protein kinases pathways. J Neurochem 92, 628636. (Pubitemid 40189465)
23. Tang SC, Lathia JD, Selvaraj PK, JoDG,MughalMR, Cheng A, Siler DA, Markesbery WR, Arumugam TV, Mattson MP (2008) Tolllike receptor4 mediates neuronal apoptosis induced by amyloid betapeptide and the membrane lipid peroxidation product 4hydroxynonenal. Exp Neurol 213, 114121.
24. PraticoD,UryuK, Leight S, Trojanoswki JQ, LeeVM(2001) Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis. J Neurosci 21, 41834187. (Pubitemid 32538543)
25. Bradley MA, Markesbery WR, Lovell MA (2010) Increased levels of 4hydroxynonenal and acrolein in the brain in preclinical Alzheimer's disease (PCAD). Free Radic Biol Med 48, 15701576.
26. Morrow JD, Hill KE, Burk RF, Nammour TM, Badr KF, Roberts LJ, 2nd (1990) A series of prostaglandin F2like compounds are produced in vivo in humans by a noncyclooxygenase, free radicalcatalyzed mechanism. Proc Natl Acad Sci U S A 87, 93839387.
27. Roberts LJ, 2nd, Montine TJ, Markesbery WR, Tapper AR, Hardy P, Chemtob S, Dettbarn WD, Morrow JD (1998) Formation of isoprostanelike compounds (neuroprostanes) in vivo from docosahexaenoic acid. J Biol Chem 273, 1360513612. (Pubitemid 28268404)
28. Lawson JA, Rokach J, FitzGerald GA (1999) Isoprostanes: formation, analysis and use as indices of lipid peroxidation in vivo. J Biol Chem 274, 2444124444. (Pubitemid 129529317)
29. Milne GL, Yin H, Morrow JD (2008) Human biochemistry of the isoprostane pathway. J Biol Chem 283, 1553315537.
30. YinH,Morrow JD, Porter NA(2004) Identification of a novel class of endoperoxides from arachidonate autoxidation. J Biol Chem 279, 37663776. (Pubitemid 38140621)
31. NouroozZadeh J, Liu EH, Yhlen B, Anggard EE, Halliwell B (1999) F4isoprostanes as specific marker of docosahexaenoic acid peroxidation in Alzheimer's disease. J Neurochem 72, 734740. (Pubitemid 29055237)
32. Soderberg M, Edlund C, Kristensson K, Dallner G (1991) Fatty acid composition of brain phospholipids in aging and in Alzheimer's disease. Lipids 26, 421425.
33. Moore SA, Yoder E, Murphy S, Dutton GR, Spector AA (1991) Astrocytes, not neurons, produce docosahexaenoic acid (22:6 omega3) and arachidonic acid (20:4 omega6). J Neurochem 56, 518524. (Pubitemid 21901992)
34. Milne GL, Zanoni G, Porta A, Sasi S, Vidari G, Musiek ES, Freeman ML, Morrow JD (2004) The cyclopentenone product of lipid peroxidation, 15A2tisoprostane, is efficiently metabolized by HepG2 cells via conjugation with glutathione. Chem Res Toxicol 17, 1725. (Pubitemid 38134056)
35. Milne GL, Gao L, Porta A, Zanoni G, Vidari G, Morrow JD (2005) Identification of the major urinary metabolite of the highly reactive cyclopentenone isoprostane 15A( 2t)isoprostane in vivo. J Biol Chem 280, 2517825184. (Pubitemid 40934610)
36. Lovell MA, Xie C, Markesbery WR (1998) Decreased glutathione transferase activity in brain and ventricular fluid in Alzheimer's disease. Neurology 51, 15621566. (Pubitemid 28565232)
37. 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, 22152220. (Pubitemid 40036893)
38. Reich EE,Markesbery WR, Roberts LJ, 2nd, Swift LL,Morrow JD, Montine TJ (2001) Brain regional quantification of Fring and D/Ering isoprostanes and neuroprostanes in Alzheimer's disease. Am J Pathol 158, 293297. (Pubitemid 32096495)
39. Pratico D, Lee VMY, Trojanowski JQ, Rokach J, Fitzgerald GA (1998) Increased F2isoprostanes in Alzheimer's disease: evidence for enhanced lipid peroxidation in vivo. FASEB J 12, 17771783. (Pubitemid 28553673)
40. BernoudHubac N, Davies SS, Boutaud O, Montine TJ, Roberts LJ, 2nd (2001) Formation of highly reactive gammaketoaldehydes (neuroketals) as products of the neuroprostane pathway. J Biol Chem 276, 3096430970. (Pubitemid 37384959)
41. Montine TJ, Morrow JD (2005) Fatty acid oxidation in the pathogenesis of Alzheimer's disease. Am J Pathol 166, 12831289. (Pubitemid 40586500)
42. Esterbauer H, Schaur RJ, Zollner H (1991) Chemistry and biochemistry of 4hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 11, 81128. (Pubitemid 121003917)
43. Doorn JA, Petersen DR (2002) Covalent modification of amino acid nucleophiles by the lipid peroxidation products 4hydroxy2nonenal and 4oxo2nonenal. Chem Res Toxicol 15, 14451450.
44. Uchida K (2003) 4Hydroxy2nonenal: A product and mediator of oxidative stress. Prog Lipid Res 42, 318343. (Pubitemid 36411689)
45. Zarkovic K (2003) 4hydroxynonenal and neurodegenerative diseases. Mol Aspects Med 24, 293303.
46. Williams TI, Lynn BC, Markesbery WR, Lovell MA (2006) Increased levels of 4hydroxynonenal and acrolein, neurotoxic markers of lipid peroxidation, in the brain in Mild Cognitive Impairment and early Alzheimer's disease. Neurobiol Aging 27, 10941099.
47. Fukuda M, Kanou F, Shimada N, Sawabe M, Saito Y, Murayama S,HashimotoM,MaruyamaN, IshigamiA(2009)Elevated levels of 4hydroxynonenalhistidine Michael adduct in the hippocampi of patients with Alzheimer's disease. Biomed Res 30, 227233.
48. Schmitt FA, Davis DG, Wekstein DR, Smith CD, Ashford JW,MarkesberyWR (2000) "Preclinical" AD revisited: neuropathology of cognitively normal older adults. Neurology 55, 370376.
49. Volkel W, Sicilia T, Pahler A, GsellW, Tatschner T, Jellinger K, Leblhuber F, Riederer P, Lutz WK, Gotz ME (2006) Increased brain levels of 4hydroxy2nonenal glutathione conjugates in severe Alzheimer's disease. Neurochem Int 48, 679686.
50. Picklo MJ, Olson SJ, Markesbery WR, Montine TJ (2001) Expression and activities of aldoketo oxidoreductases in Alzheimer disease. J Neuropathol Exp Neurol 60, 686695. (Pubitemid 32619791)
51. Reed T, Perluigi M, Sultana R, Pierce WM, Klein JB, Turner DM, Coccia R, Markesbery WR, Butterfield DA (2008) Redox proteomic identification of 4hydroxy2nonenalmodified 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, 107120.
52. Drake J, Petroze R, Castegna A, Ding Q, Keller JN, Markesbery WR, Lovell MA, Butterfield DA (2004) 4Hydroxynonenal oxidatively modifies histones: Implications for Alzheimer's disease. Neurosci Lett 356, 155158. (Pubitemid 38186675)
53. Liu X, Lovell MA, Lynn BC (2006) Detection and quantification of endogenous cyclic DNA adducts derived from trans4hydroxy2nonenal in human brain tissue by isotope dilution capillary liquid chromatography nanoelectrospray tandem mass spectrometry. Chem Res Toxicol 19, 710718. (Pubitemid 43800988)
54. Camandola S, Poli G, Mattson MP (2000) The lipid peroxidation product 4hydroxy2,3nonenal inhibits constitutive and inducible activity of nuclear factor kappa B in neurons. Brain Res Mol Brain Res 85, 5360. (Pubitemid 32056236)
55. Mark RJ, Lovell MA, Markesbery WR, Uchida K, Mattson MP (1997) A role for 4hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid betapeptide. J Neurochem 68, 255264. (Pubitemid 26427315)
56. Tamagno E, RobinoG,ObbiliA, Bardini P,AragnoM, Parola M, Danni O (2003) H2O2 and 4hydroxynonenal mediate amyloid betainduced neuronal apoptosis by activating JNKs and p38MAPK. Exp Neurol 180, 144155.
57. Keller JN,Mark RJ, Bruce AJ, Blanc E, Rothstein JD, Uchida K, Waeg G, Mattson MP (1997) 4Hydroxynonenal, an aldehydic product of membrane lipid peroxidation, impairs glutamate transport and mitochondrial function in synaptosomes. Neuroscience 80, 685696. (Pubitemid 27334614)
58. Cenini G, Sultana R, Memo M, Butterfield DA (2008) Elevated levels of proapoptotic p53 and its oxidative modification by the lipid peroxidation product, HNE, in brain from subjects with amnestic mild cognitive impairment and Alzheimer's disease. J Cell Mol Med 12, 987994. (Pubitemid 351718076)
59. Marchenko ND, Zaika A, Moll UM (2000) Death signalinduced localization of p53 protein to mitochondria. A potential role in apoptotic signaling. J Biol Chem 275, 1620216212. (Pubitemid 30366932)
60. Kruman I, BruceKeller AJ, Bredesen D, Waeg G, Mattson MP (1997) Evidence that 4hydroxynonenal mediates oxidative stressinduced neuronal apoptosis. J Neurosci 17, 50895100. (Pubitemid 27263822)
61. Uchida K, Kanematsu M, Morimitsu Y, Osawa T, Noguchi N, Niki E (1998) Acrolein is a product of lipid peroxidation reaction. Formation of free acrolein and its conjugate with lysine residues in oxidized low density lipoproteins. J Biol Chem 273, 1605816066. (Pubitemid 28311374)
62. Marnett LJ, Riggins JN,West JD (2003) Endogenous generation of reactive oxidants and electrophiles and their reactions with DNA and protein. J Clin Invest 111, 583593.
63. Tillian HM, Schauenstein E, Ertl A, Esterbauer H (1976) Therapeutic effects of cysteine adducts of alpha, betaunsaturated aldehydes on Ehrlich ascites tumor of mice. Eur J Cancer 12, 989993. (Pubitemid 8008904)
64. Gan JC, Ansari GA (1987) Plausible mechanism of inactivation of plasma alpha 1proteinase inhibitor by acrolein. Res Commun Chem Pathol Pharmacol 55, 419422.
65. Kehrer JP, Biswal SS (2000) The molecular effects of acrolein. Toxicol Sci 57, 615.
66. KawaguchiNiida M, Shibata N,Morikawa S, Uchida K, Yamamoto T, Sawada T, Kobayashi M (2006) Crotonaldehyde accumulates in glial cells of Alzheimer's disease brain. Acta Neuropathol 111, 422429.
67. Kuhla B, Haase C, Flach K, Luth HJ, Arendt T, Munch G (2007) Effect of pseudophosphorylation and crosslinking by lipid peroxidation and advanced glycation end product precursors on tau aggregation and filament formation. J Biol Chem 282, 69846991. (Pubitemid 47093635)
68. DiazHernandez M, Hernandez F, MartinAparicio E, GomezRamos P, Moran MA, Castano JG, Ferrer I, Avila J, Lucas JJ (2003) Neuronal induction of the immunoproteasome in Huntington's disease. J Neurosci 23, 1165311661. (Pubitemid 38021292)
69. MunozMontano JR,Moreno FJ, Avila J, DiazNido J (1997) Lithium inhibits Alzheimer's diseaselike tau protein phosphorylation in neurons. FEBS Lett 411, 183188. (Pubitemid 27301451)
70. Wolfle WT, Johnson RE, Minko IG, Lloyd RS, Prakash S, Prakash L (2005) Human DNA polymerase iota promotes replication through a ringclosed minorgroove adduct that adopts a syn conformation in DNA. Mol Cell Biol 25, 87488754. (Pubitemid 41369191)
71. Nath RG, Chung FL (1994) Detection of exocyclic 1,N2propanodeoxyguanosine adducts as common DNA lesions in rodents and humans. Proc Natl Acad Sci U S A 91, 74917495. (Pubitemid 24238210)
72. Nath RG, Ocando JE, Chung FL (1996) Detection of 1, N2propanodeoxyguanosine adducts as potential endogenous DNA lesions in rodent and human tissues. Cancer Res 56, 452456.
73. LiuX, LovellMA, LynnBC(2005)Development of amethod for quantification of acroleindeoxyguanosine adducts in DNA using isotope dilutioncapillary LC/MS/MS and its application to human brain tissue. Anal Chem 77, 59825989. (Pubitemid 41324300)
74. Chung FL, Young R, Hecht SS (1984) Formation of cyclic 1,N2propanodeoxyguanosine adducts inDNAupon reaction with acrolein or crotonaldehyde. Cancer Res 44, 990995. (Pubitemid 14152780)
75. Kozekov ID, Nechev LV, Moseley MS, Harris CM, Rizzo CJ, Stone MP, Harris TM(2003) DNA interchain crosslinks formed by acrolein and crotonaldehyde. J Am Chem Soc 125, 5061.
76. 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, 187194. (Pubitemid 32162967)
77. Lovell MA, Xie C, Gabbita SP, Markesbery WR (2000) Decreased thioredoxin and increased thioredoxin reductase levels in Alzheimer's disease brain. Free Radic Biol Med 28, 418427. (Pubitemid 30110658)
78. Adams JD, Jr., Klaidman LK (1993) Acroleininduced oxygen radical formation. Free Radic Biol Med 15, 187193.
79. Ramana KV, Dixit BL, Srivastava S, Balendiran GK, Srivastava SK, Bhatnagar A (2000) Selective recognition of glutathiolated aldehydes by aldose reductase. Biochemistry 39, 1217212180.
80. Mitchell DY, Petersen DR (1989) Metabolism of the glutathioneacroleinadduct, S( 2aldehydoethyl) glutathione, by rat liver alcohol and aldehyde dehydrogenase. J Pharmacol Exp Ther 251, 193198.
81. Wang X, Sheikh S, Saigal D, Robinson L, Weiner H (1996) Heterotetramers of human liver mitochondrial (class 2) aldehyde dehydrogenase expressed in Escherichia coli. A model to study the heterotetramers expected to be found in Oriental people. J Biol Chem 271, 3117231178. (Pubitemid 26408559)
82. Wang B, Wang J, Zhou S, Tan S, He X, Yang Z, Xie YC, Li S, Zheng C, Ma X (2008) The association of mitochondrial aldehyde dehydrogenase gene (ALDH2) polymorphism with susceptibility to lateonset Alzheimer's disease in Chinese. J Neurol Sci 268, 172175.
83. Ohta S, Ohsawa I, Kamino K, Ando F, Shimokata H (2004) Mitochondrial ALDH2 deficiency as an oxidative stress. Ann N Y Acad Sci 1011, 3644. (Pubitemid 38608389)
84. Kamino K, Nagasaka K, Imagawa M, Yamamoto H, Yoneda H, Ueki A, Kitamura S, Namekata K, Miki T, Ohta S (2000) Deficiency in mitochondrial aldehyde dehydrogenase increases the risk for lateonset Alzheimer's disease in the Japanese population. Biochem Biophys Res Commun 273, 192196. (Pubitemid 30426885)
85. Ohta S, Ohsawa I (2006) 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, 155166. (Pubitemid 44078643)
86. Mitchell DY, Petersen DR (1988) Inhibition of rat liver aldehyde dehydrogenases by acrolein. Drug Metab Dispos 16, 3742. (Pubitemid 18057094)
87. Uchida K (1999) Current status of acrolein as a lipid peroxidation product. Trends Cardiovasc Med 9, 109113. (Pubitemid 30001888)
88. Pocernich CB, Butterfield DA (2003) Acrolein inhibits NADHlinked mitochondrial enzyme activity: Implications for Alzheimer's disease. Neurotox Res 5, 515520.
89. Ansari MA, Keller JN, Scheff SW (2008) Protective effect of Pycnogenol in human neuroblastoma SHSY5Y cells following acroleininduced cytotoxicity. Free Radic Biol Med 45, 15101519.
90. Mello CF, Sultana R, Piroddi M, Cai J, Pierce WM, Klein JB, Butterfield DA (2007) Acrolein induces selective protein carbonylation in synaptosomes. Neuroscience 147, 674679. (Pubitemid 46990643)
91. Jeong MS, Kang JH (2008) Acrolein, the toxic endogenous aldehyde, induces neurofilamentL aggregation. BMB Rep 41, 635639.
92. Nakamura Y, Hasimoto R, Kashiwagi Y, Miyamae Y, Shinosaki K, Nishikawa T, Hattori H, Kudo T, Takeda M (1997) Abnormal distribution of neurofilament L in neurons with Alzheimer's disease. Neurosci Lett 225, 201204. (Pubitemid 27191630)
93. Horton ND, Biswal SS, Corrigan LL, Bratta J, Kehrer JP (1999) Acrolein causes inhibitor kappaBindependent decreases in nuclear factor kappaB activation in human lung adenocarcinoma (A549) cells. J Biol Chem 274, 92009206. (Pubitemid 129517882)
94. Liu H, Wang H, Shenvi S, Hagen TM, Liu RM (2004) Glutathione metabolism during aging and in Alzheimer disease. Ann N Y Acad Sci 1019, 346349. (Pubitemid 38951332)
95. Klatt P, Lamas S (2000) Regulation of protein function by Sglutathiolation in response to oxidative and nitrosative stress. Eur J Biochem 267, 49284944. (Pubitemid 30641289)
96. Ziegler DM(1985) Role of reversible oxidationreduction of enzyme thiolsdisulfides in metabolic regulation. Annu Rev Biochem 54, 305329.
97. Thomas JA, PolandB,HonzatkoR(1995) Protein sulfhydryls and their role in the antioxidant function of protein Sthiolation. Arch Biochem Biophys 319, 19.
98. Newman SF, Sultana R, Perluigi M, Coccia R, Cai J, Pierce WM, Klein JB, Turner DM, Butterfield DA (2007) An increase in Sglutathionylated proteins in the Alzheimer's disease inferior parietal lobule, a proteomics approach. J Neurosci Res 85, 15061514. (Pubitemid 46724394)
99. Zhong L, Holmgren A (2000) Essential role of selenium in the catalytic activities of mammalian thioredoxin reductase revealed by characterization of recombinant enzymes with selenocysteine mutations. J Biol Chem 275, 1812118128. (Pubitemid 30414762)
100. Lee SR, BarNoy S, Kwon J, Levine RL, Stadtman TC, Rhee SG (2000) Mammalian thioredoxin reductase: oxidation of the Cterminal cysteine/ selenocysteine active site forms a thioselenide, and replacement of selenium with sulfur markedly reduces catalytic activity. Proc Natl Acad Sci U S A 97, 25212526. (Pubitemid 30159203)
101. Bjornstedt M, Hamberg M, Kumar S, Xue J, Holmgren A (1995) Human thioredoxin reductase directly reduces lipid hydroperoxides by NADPH and selenocystine strongly stimulates the reaction via catalytically generated selenols. J Biol Chem 270, 1176111764.
102. Das KC, LewisMolock Y, White CW (1997) Elevation of manganese superoxide dismutase gene expression by thioredoxin. Am J Respir Cell Mol Biol 17, 713726. (Pubitemid 127348662)
103. Nikitovic D, Holmgren A (1996) Snitrosoglutathione is cleaved by the thioredoxin system with liberation of glutathione and redox regulating nitric oxide. J Biol Chem 271, 1918019185. (Pubitemid 26271582)
104. Sun QA, Wu Y, Zappacosta F, Jeang KT, Lee BJ, Hatfield DL, Gladyshev VN (1999) Redox regulation of cell signaling by selenocysteine in mammalian thioredoxin reductases. J Biol Chem 274, 2452224530. (Pubitemid 129529330)
105. Park YS, Misonou Y, Fujiwara N, Takahashi M, Miyamoto Y, Koh YH, Suzuki K, Taniguchi N (2005) Induction of thioredoxin reductase as an adaptive response to acrolein in human umbilical vein endothelial cells. BiochemBiophys Res Commun 327, 10581065. (Pubitemid 40137976)
106. Yang X, Wu X, Choi YE, Kern JC, Kehrer JP (2004) Effect of acrolein and glutathione depleting agents on thioredoxin. Toxicology 204, 209218. (Pubitemid 39244081)
107. Akterin S, Cowburn RF, MirandaVizuete A, Jimenez A, Bogdanovic N, Winblad B, CedazoMinguez A (2006) Involvement of glutaredoxin1 and thioredoxin1 in betaamyloid toxicity and Alzheimer's disease. Cell Death Differ 13, 14541465. (Pubitemid 44210349)
108. Kimes BW, Morris DR (1971) Preparation and stability of oxidized polyamines. Biochim Biophys Acta 228, 223234.
109. Tabor CW, Tabor H (1984) Polyamines. Annu Rev Biochem 53, 749790. (Pubitemid 14059150)
110. Yoneda Y, Ogita K (1991) Neurochemical aspects of the NmethylDaspartate receptor complex. Neurosci Res 10, 133.
111. Washburn MS, Dingledine R (1996) Block of alphaamino3hydroxy5methyl4isoxazolepropionic acid (AMPA) receptors by polyamines and polyamine toxins. J Pharmacol Exp Ther 278, 669678. (Pubitemid 27167033)
112. Fage D, Voltz C, Scatton B, Carter C (1992) Selective release of spermine and spermidine from the rat striatum by NmethylDaspartate receptor activation in vivo. J Neurochem 58, 21702175.
113. Harman RJ, Shaw GG (1981) The spontaneous and evoked release of spermine from rat brain in vitro. Br J Pharmacol 73, 165174. (Pubitemid 11104775)
114. Morrison LD, Kish SJ (1995) Brain polyamine levels are altered in Alzheimer's disease. Neurosci Lett 197, 58.
115. Bernstein HG, Muller M (1999) The cellular localization of the Lornithine decarboxylase/polyamine system in normal and diseased central nervous systems. Prog Neurobiol 57, 485505. (Pubitemid 29136677)
116. Seidl R, Beninati S, Cairns N, Singewald N, Risser D, Bavan H, Nemethova M, Lubec G (1996) Polyamines in frontal cortex of patients with Down syndrome and Alzheimer disease. Neurosci Lett 206, 193195. (Pubitemid 26094691)
117. Yatin SM, Yatin M, Varadarajan S, Ain KB, Butterfield DA (2001) Role of spermine in amyloid betapeptideassociated free radicalinduced neurotoxicity. J Neurosci Res 63, 395401. (Pubitemid 32183788)
118. LovellMA, Xie C,Markesbery WR (2000) Acrolein, a product of lipid peroxidation, inhibits glucose and glutamate uptake in primary neuronal cultures. Free Radic Biol Med 29, 714720.
119. Mattson MP, Mark RJ (1996) Excitotoxicity and excitoprotection in vitro. Adv Neurol 71, 1-30; discussion 30-35.
120. Takano K, Ogura M, Yoneda Y, Nakamura Y (2005) Oxidative metabolites are involved in polyamineinduced microglial cell death. Neuroscience 134, 11231131. (Pubitemid 41207365)
121. Mark RJ, Pang Z, Geddes JW, Uchida K, Mattson MP (1997) Amyloid betapeptide impairs glucose transport in hippocampal and cortical neurons: Involvement of membrane lipid peroxidation. J Neurosci 17, 10461054. (Pubitemid 27043963)
122. Masliah E, Alford M, Mallory M, Rockenstein E, Moechars D, Van Leuven F (2000) Abnormal glutamate transport function in mutant amyloid precursor protein transgenic mice. Exp Neurol 163, 381387. (Pubitemid 30399086)
123. Masliah E, Alford M, DeTeresa R, Mallory M, Hansen L (1996) Deficient glutamate transport is associated with neurodegeneration in Alzheimer's disease. Ann Neurol 40, 759766. (Pubitemid 26415188)
124. Saransaari P,Oja SS (1995)Agerelated changes in the uptake and release of glutamate and aspartate in the mouse brain. Mech Ageing Dev 81, 6171.
125. LoPachin RM, Barber DS (2006) Synaptic cysteine sulfhydryl groups as targets of electrophilic neurotoxicants. Toxicol Sci 94, 240255.
126. Coleman P, Federoff H, Kurlan R (2004) A focus on the synapse for neuroprotection in Alzheimer disease and other dementias. Neurology 63, 11551162. (Pubitemid 39350010)
127. Arakawa M, Ushimaru N, Osada N, Oda T, Ishige K, Ito Y (2006) Nacetylcysteine selectively protects cerebellar granule cells from 4hydroxynonenalinduced cell death. Neurosci Res 55, 255263. (Pubitemid 43766414)