Reactive oxygen species in diabetes-induced vascular damage, stroke, and Alzheimer's disease

Journal of Alzheimer's Disease

Volumn 16, Issue 4, 2009, Pages 775-785

  Muhammad, Sajjad ^a   Bierhaus, Angelika ^a   Schwaninger, Markus ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Antioxidants; Endothelial dysfunction; Mitochondrial dysfunction; Neurodegeneration; Oxidative stress

Indexed keywords

AMYLOID BETA PROTEIN; ANTIOXIDANT; CYCLOOXYGENASE 2; CYTOCHROME C; NITRIC OXIDE SYNTHASE; NONSTEROID ANTIINFLAMMATORY AGENT; PHOSPHOLIPASE A2; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SUPEROXIDE DISMUTASE;

ALZHEIMER DISEASE; BLOOD VESSEL INJURY; BRAIN ISCHEMIA; DIABETES MELLITUS; HUMAN; INFLAMMATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; STROKE; ANIMAL; METABOLISM; VASCULAR DISEASE;

ANIMALS; DIABETES MELLITUS; HUMANS; REACTIVE OXYGEN SPECIES; STROKE; VASCULAR DISEASES;

EID: 67649736148     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2009-0982     Document Type: Review

References (108)

1. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid [beta]-peptide. Nat Rev Mol Cell Biol 8, 101-112. (Pubitemid 46432529)
2. Alzheimer A (1907) Über eine eigenartige Erkrankung der Hirnrinde. Psychiatrie Pych Ger Med 65, 146-148.
3. Attems J (2005) Sporadic cerebral amyloid angiopathy: pathology, clinical implications, and possible pathomechanisms. Acta Neuropathol 110, 345-359.
4. Jellinger KA, Attems J (2007) Neuropathological evaluation of mixed dementia. J Neurol Sci 257, 80-87.
5. Johnson KA, Albert MS (2000) Perfusion abnormalities in prodromal AD. Neurobiol Aging 21, 289-292.
6. Iadecola C (2004) Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Rev Neurosci 5, 347-360. (Pubitemid 38568496)
7. Park L, Zhou P, Pitstick R, Capone C, Anrather J, Norris EH, Younkin L, Younkin S, Carlson G, McEwen BS, Iadecola C (2008) Nox2-derived radicals contribute to neurovascular and behavioral dysfunction in mice overexpressing the amyloid precursor protein. Proc Natl Acad Sci U S A 105, 1347-1352.
8. Biessels GJ, Staekenborg S, Brunner E, Brayne C, Scheltens P (2006) Risk of dementia in diabetes mellitus: a systematic review. Lancet Neurol 5, 64-74. (Pubitemid 41790697)
9. Halliwell B (2006) Oxidative stress and neurodegeneration: where are we now? J Neurochem 97, 1634-1658. (Pubitemid 43873658)
10. Bloch-Damti A, Bashan N (2005) Proposed mechanisms for the induction of insulin resistance by oxidative stress. Antioxid Redox Signal 7, 1553-1567. (Pubitemid 41767991)
11. Andrews ZB, Liu ZW, Walllingford N, Erion DM, Borok E, Friedman JM, Tschop MH, Shanabrough M, Cline G, Shulman GI, Coppola A, Gao XB, Horvath TL, Diano S (2008) UCP2 mediates ghrelin's action on NPY/AgRP neurons by lowering free radicals. Nature 454, 846-851.
12. Wang W, Fang H, Groom L, Cheng A, Zhang W, Liu J, Wang X, Li K, Han P, Zheng M, Yin J, Mattson MP, Kao JP, Lakatta EG, Sheu SS, Ouyang K, Chen J, Dirksen RT, Cheng H (2008) Superoxide flashes in single mitochondria. Cell 134, 279-290.
13. Bedard K, Krause K-H (2007) The NOX Family of ROS-Generating NADPH Oxidases: Physiology and Pathophysiology. Physiol Rev 87, 245-313. (Pubitemid 46209993)
14. Forstermann U, Munzel T (2006) Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation 113, 1708-1714. (Pubitemid 43754233)
15. Linder N, Rapola J, Raivio KO (1999) Cellular expression of xanthine oxidoreductase protein in normal human tissues. Lab Invest 79, 967-974. (Pubitemid 29400141)
16. Sundquist K, Li X (2006) Type 1 diabetes as a risk factor for stroke in men and women aged 15-49: a nationwide study from Sweden. Diabet Med 23, 1261-1267. (Pubitemid 44600592)
17. Kannel WB, McGee DL (1979) Diabetes and cardiovascular disease. The Framingham study. JAMA 241, 2035-2038. (Pubitemid 9228506)
18. Manson JE, Colditz GA, Stampfer MJ, Willett WC, Krolewski AS, Rosner B, Arky RA, Speizer FE, Hennekens CH (1991) A prospective study of maturity-onset diabetes mellitus and risk of coronary heart disease and stroke in women. Arch Intern Med 151, 1141-1147.
19. Kim BJ, Lee SH, Kang BS, Yoon BW, Roh JK (2008) Diabetes increases large artery diseases, but not small artery diseases in the brain. J Neurol 255, 1176-1181.
20. Gispen WH, Biessels GJ (2000) Cognition and synaptic plasticity in diabetes mellitus. Trends Neurosci 23, 542-549.
21. Ting HH, Timimi FK, Boles KS, Creager SJ, Ganz P, Creager MA (1996) Vitamin C improves endothelium-dependent vasodilation in patients with non-insulin-dependent diabetes mellitus. J Clin Invest 97, 22-28. (Pubitemid 26021690)
22. Beckman JS, Koppenol WH (1996) Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol Cell Physiol 271, C1424-1437.
23. Brownlee M (2001) Biochemistry and molecular cell biology of diabetic complications. Nature 414, 813-820. (Pubitemid 34000785)
24. Hink U, Li H, Mollnau H, Oelze M, Matheis E, Hartmann M, Skatchkov M, Thaiss F, Stahl RA, Warnholtz A, Meinertz T, Griendling K, Harrison DG, Forstermann U, Munzel T (2001) Mechanisms underlying endothelial dysfunction in diabetes mellitus. Circ Res 88, E14-22.
25. Butler R, Morris AD, Belch JJ, Hill A, Struthers AD (2000) Allopurinol normalizes endothelial dysfunction in type 2 diabetics with mild hypertension. Hypertension 35, 746-751. (Pubitemid 30165320)
26. Camici GG, Schiavoni M, Francia P, Bachschmid M, Martin- Padura I, Hersberger M, Tanner FC, Pelicci P, Volpe M, Anversa P, Luscher TF, Cosentino F (2007) Genetic deletion of p66(Shc) adaptor protein prevents hyperglycemia-induced endothelial dysfunction and oxidative stress. Proc Natl Acad Sci U S A 104, 5217-5222. (Pubitemid 47186202)
27. Pinton P, Rimessi A, Marchi S, Orsini F, Migliaccio E, Giorgio M, Contursi C, Minucci S, Mantovani F, Wieckowski MR, Del Sal G, Pelicci PG, Rizzuto R (2007) Protein kinase C beta and prolyl isomerase 1 regulate mitochondrial effects of the life-span determinant p66Shc. Science 315, 659-663. (Pubitemid 46214712)
28. Giorgio M, Migliaccio E, Orsini F, Paolucci D, Moroni M, Contursi C, Pelliccia G, Luzi L, Minucci S, Marcaccio M, Pinton P, Rizzuto R, Bernardi P, Paolucci F, Pelicci PG (2005) Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 122, 221-233. (Pubitemid 41032986)
29. Bierhaus A, Humpert PM, Morcos M, Wendt T, Chavakis T, Arnold B, Stern DM, Nawroth PP (2005) Understanding RAGE, the receptor for advanced glycation end products. J Mol Med 83, 876-886. (Pubitemid 41598688)
30. Soro-Paavonen A, Watson AM, Li J, Paavonen K, Koitka A, Calkin AC, Barit D, Coughlan MT, Drew BG, Lancaster GI, Thomas M, Forbes JM, Nawroth PP, Bierhaus A, Cooper ME, Jandeleit-Dahm KA (2008) Receptor for advanced glycation end products (RAGE) deficiency attenuates the development of atherosclerosis in diabetes. Diabetes 57, 2461-2469.
31. Yan SD, Schmidt AM, Anderson GM, Zhang J, Brett J, Zou YS, Pinsky D, Stern D (1994) Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J Biol Chem 269, 9889-9897. (Pubitemid 24196599)
32. Wautier MP, Chappey O, Corda S, Stern DM, Schmidt AM, Wautier JL (2001) Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am J Physiol Endocrinol Metab 280, E685-694. (Pubitemid 32466835)
33. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404, 787-790. (Pubitemid 30212409)
34. Bierhaus A, Schiekofer S, Schwaninger M, Andrassy M, Humpert PM, Chen J, Hong M, Luther T, Henle T, Kloting I, Morcos M, Hofmann M, Tritschler H, Weigle B, Kasper M, Smith M, Perry G, Schmidt AM, Stern DM, Haring HU, Schleicher E, Nawroth PP (2001) Diabetes-associated sustained activation of the transcription factor nuclear factor-kappaB. Diabetes 50, 2792-2808. (Pubitemid 33733131)
35. Kanters E, Pasparakis M, Gijbels MJ, Vergouwe MN, Partouns-Hendriks I, Fijneman RJ, Clausen BE, Forster I, Kockx MM, Rajewsky K, Kraal G, Hofker MH, de Winther MP (2003) Inhibition of NF-kappaB activation in macrophages increases atherosclerosis in LDL receptor-deficient mice. J Clin Invest 112, 1176-1185. (Pubitemid 38056294)
36. Kempe S, Kestler H, Lasar A, Wirth T (2005) NF-kappaB controls the global pro-inflammatory response in endothelial cells: evidence for the regulation of a pro-atherogenic program. Nucleic Acids Res 33, 5308-5319. (Pubitemid 41487834)
37. de Winther MPJ, Kanters E, Kraal G, Hofker MH (2005) Nuclear Factor {kappa}B Signaling in Atherogenesis. Arterioscler Thromb Vasc Biol 25, 904-914. (Pubitemid 40627833)
38. Takada Y, Mukhopadhyay A, Kundu GC, Mahabeleshwar GH, Singh S, Aggarwal BB (2003) Hydrogen peroxide activates NF-kappa B through tyrosine phosphorylation of I kappa B alpha and serine phosphorylation of p65: evidence for the involvement of I kappa B alpha kinase and Syk protein-tyrosine kinase. J Biol Chem 278, 24233-24241. (Pubitemid 36830260)
39. Kamata H, Manabe T, Oka S, Kamata K, Hirata H (2002) Hydrogen peroxide activates IkappaB kinases through phosphorylation of serine residues in the activation loops. FEBS Lett 519, 231-237. (Pubitemid 34522025)
40. Enesa K, Ito K, Luong LA, Thorbjornsen I, Phua C, To Y, Dean J, Haskard DO, Boyle J, Adcock I, Evans PC (2008) Hydrogen Peroxide Prolongs Nuclear Localization of NF-{kappa}B in Activated Cells by Suppressing Negative Regulatory Mechanisms. J Biol Chem 283, 18582-18590.
41. Kassem-Moussa H, Graffagnino C (2002) Nonocclusion and Spontaneous Recanalization Rates in Acute Ischemic Stroke: A Review of Cerebral Angiography Studies. Arch Neurol 59, 1870-1873. (Pubitemid 35424643)
42. Hacke W, Donnan G, Fieschi C, Kaste M, von Kummer R, Broderick JP, Brott T, Frankel M, Grotta JC, Haley EC, Jr., Kwiatkowski T, Levine SR, Lewandowski C, Lu M, Lyden P, Marler JR, Patel S, Tilley BC, Albers G, Bluhmki E, Wilhelm M, Hamilton S (2004) Association of outcome with early stroke treatment: pooled analysis of ATLANTIS, ECASS, and NINDS rt-PA stroke trials. Lancet 363, 768-774.
43. Peters O, Back T, Lindauer U, Busch C, Megow D, Dreier J, Dirnagl U (1998) Increased Formation of Reactive Oxygen Species After Permanent and Reversible Middle Cerebral Artery Occlusion in the Rat. J Cereb Blood Flow Metab 18, 196-205. (Pubitemid 28082517)
44. Abramov AY, Scorziello A, Duchen MR (2007) Three Distinct Mechanisms Generate Oxygen Free Radicals in Neurons and Contribute to Cell Death during Anoxia and Reoxygenation. J Neurosci 27, 1129-1138. (Pubitemid 46203321)
45. Huang Z, Huang PL, Panahian N, Dalkara T, Fishman MC, Moskowitz MA (1994) Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 265, 1883-1885. (Pubitemid 24324247)
46. Iadecola C, Zhang F, Casey R, Clark HB, Ross ME (1996) Inducible nitric oxide synthase gene expression in vascular cells after transient focal cerebral ischemia. Stroke 27, 1373-1380. (Pubitemid 26286171)
47. Iadecola C, Zhang F, Casey R, Nagayama M, Ross ME (1997) Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene. J Neurosci 17, 9157-9164. (Pubitemid 27498443)
48. Pruss H, Prass K, Ghaeni L, Milosevic M, Muselmann C, Freyer D, Royl G, Reuter U, Baeva N, Dirnagl U, Meisel A, Priller J (2007) Inducible nitric oxide synthase does not mediate brain damage after transient focal cerebral ischemia in mice. J Cereb Blood Flow Metab 28, 526-539. (Pubitemid 351304264)
49. Lo EH, Hara H, Rogowska J, Trocha M, Pierce AR, Huang PL, Fishman MC, Wolf GL, Moskowitz MA (1996) Temporal correlation mapping analysis of the hemodynamic penumbra in mutant mice deficient in endothelial nitric oxide synthase gene expression. Stroke 27, 1381-1385. (Pubitemid 26286172)
50. Huang Z, Huang PL, Ma J, Meng W, Ayata C, Fishman MC, Moskowitz MA (1996) Enlarged infarcts in endothelial nitric oxide synthase knockout mice are attenuated by nitro- L-arginine. J Cereb Blood Flow Metab 16, 981-987. (Pubitemid 26292066)
51. Muralikrishna Adibhatla R, Hatcher JF (2006) Phospholipase A2, reactive oxygen species, and lipid peroxidation in cerebral ischemia. Free Radic Biol Med 40, 376-387. (Pubitemid 43139673)
52. Nagayama M, Niwa K, Nagayama T, Ross ME, Iadecola C (1999) The cyclooxygenase-2 inhibitor NS-398 ameliorates ischemic brain injury in wild-type mice but not in mice with deletion of the inducible nitric oxide synthase gene. J Cereb Blood Flow Metab 19, 1213-1219. (Pubitemid 30176449)
53. Nogawa S, Forster C, Zhang F, Nagayama M, Ross ME, Iadecola C (1998) Interaction between inducible nitric oxide synthase and cyclooxygenase-2 after cerebral ischemia. Proc Natl Acad Sci U S A 95, 10966-10971. (Pubitemid 28413177)
54. Kunz A, Anrather J, Zhou P, Orio M, Iadecola C (2006) Cyclooxygenase-2 does not contribute to postischemic production of reactive oxygen species. J Cereb Blood Flow Metab 27, 545-551.
55. Bianca VD, Dusi S, Bianchini E, Dal Pra I, Rossi F (1999) beta-amyloid activates the O-2 forming NADPH oxidase in microglia, monocytes, and neutrophils. Apossible inflammatory mechanism of neuronal damage in Alzheimer's disease. J Biol Chem 274, 15493-15499. (Pubitemid 129518900)
56. Kahles T, Luedike P, Endres M, Galla HJ, Steinmetz H, Busse R, Neumann-Haefelin T, Brandes RP (2007) NADPH oxidase plays a central role in blood-brain barrier damage in experimental stroke. Stroke 38, 3000-3006. (Pubitemid 350035696)
57. Walder CE, Green SP, Darbonne WC, Mathias J, Rae J, Dinauer MC, Curnutte JT, Thomas GR (1997) Ischemic stroke injury is reduced in mice lacking a functional NADPH oxidase. Stroke 28, 2252-2258. (Pubitemid 27497931)
58. Yenari MA, Xu L, Tang XN, Qiao Y, Giffard RG (2006) Microglia potentiate damage to blood-brain barrier constituents: improvement by minocycline in vivo and in vitro. Stroke 37, 1087-1093.
59. Hong H, Zeng JS, Kreulen DL, Kaufman DI, Chen AF (2006) Atorvastatin protects against cerebral infarction via inhibition of NADPH oxidase-derived superoxide in ischemic stroke. Am J Physiol Heart Circ Physiol 291, H2210-2215. (Pubitemid 44776647)
60. Muhammad S, Barakat W, Stoyanov S, Murikinati S, Yang H, Tracey KJ, Bendszus M, Rossetti G, Nawroth P, Bierhaus A, Schwaninger M (2008) The HMGB1 receptor RAGE mediates ischemic brain damage. J Neurosci 28, 12023-12031.
61. Zhang Y, Wang H, Li J, Jimenez DA, Levitan ES, Aizenman E, Rosenberg PA (2004) Peroxynitrite-induced neuronal apoptosis is mediated by intracellular zinc release and 12- lipoxygenase activation. J Neurosci 24, 10616-10627. (Pubitemid 39557634)
62. Chan PH (2005) Mitochondrial dysfunction and oxidative stress as determinants of cell death/survival in stroke. Ann N Y Acad Sci 1042, 203-209. (Pubitemid 40967640)
63. Crack PJ, Taylor JM, Ali U, Mansell A, Hertzog PJ (2006) Potential contribution of NF-kappaB in neuronal cell death in the glutathione peroxidase-1 knockout mouse in response to ischemia-reperfusion injury. Stroke 37, 1533-1538. (Pubitemid 44305738)
64. Huang CY, Fujimura M, Noshita N, Chang YY, Chan PH (2001) SOD1 down-regulates NF-kappaB and c-Myc expression in mice after transient focal cerebral ischemia. J Cereb Blood Flow Metab 21, 163-173. (Pubitemid 32143978)
65. Herrmann O, Baumann B, De Lorenzi R, Muhammad S, Zhang W, Kleesiek J, Malfertheiner M, Köhrmann M, Potrovita I, Maegele I, Beyer C, Burke JR, Hasan MT, Bujard H, Wirth T, Pasparakis M, Schwaninger M (2005) IKK mediates ischemia-induced neuronal cell death. Nat Med 11, 1322-1329. (Pubitemid 41752913)
66. Schneider A, Martin-Villalba A, Weih F, Vogel J, Wirth T, Schwaninger M (1999) NF-kappaB is activated and promotes cell death in focal cerebral ischemia. Nat Med 5, 554-559. (Pubitemid 29220215)
67. Ridder DA, Schwaninger M (2008) NF-kappaB signaling in cerebral ischemia. Neuroscience, in press.
68. Mattson MP, Meffert MK (2006) Roles for NF-kappaB in nerve cell survival, plasticity, and disease. Cell Death Differ 13, 852-860.
69. Kawase M, Murakami K, Fujimura M, Morita-Fujimura Y, Gasche Y, Kondo T, Scott RW, Chan PH (1999) Exacerbation of delayed cell injury after transient global ischemia in mutant mice with CuZn superoxide dismutase deficiency. Stroke 30, 1962-1968. (Pubitemid 29411842)
70. Kondo T, Reaume AG, Huang TT, Carlson E, Murakami K, Chen SF, Hoffman EK, Scott RW, Epstein CJ, Chan PH (1997) Reduction of CuZn-superoxide dismutase activity exacerbates neuronal cell injury and edema formation after transient focal cerebral ischemia. J Neurosci 17, 4180-4189. (Pubitemid 27220609)
71. Kondo T, Reaume AG, Huang TT, Murakami K, Carlson E, Chen S, Scott RW, Epstein CJ, Chan PH (1997) Edema for mation exacerbates neurological and histological outcomes after focal cerebral ischemia in CuZn-superoxide dismutase gene knockout mutant mice. Acta Neurochir Suppl 70, 62-64. (Pubitemid 127502052)
72. Fujimura M, Tominaga T, Chan PH (2005) Neuroprotective effect of an antioxidant in ischemic brain injury: involvement of neuronal apoptosis. Neurocrit Care 2, 59-66. (Pubitemid 40404630)
73. He YY, Hsu CY, Ezrin AM, Miller MS (1993) Polyethylene glycol-conjugated superoxide dismutase in focal cerebral ischemia-reperfusion. Am J Physiol 265, H252-256.
74. Davis AS, Zhao H, Sun GH, Sapolsky RM, Steinberg GK (2007) Gene therapy using SOD1 protects striatal neurons from experimental stroke. Neurosci Lett 411, 32-36. (Pubitemid 44751934)
75. Murakami K, Kondo T, Kawase M, Li Y, Sato S, Chen SF, Chan PH (1998) Mitochondrial susceptibility to oxidative stress exacerbates cerebral infarction that follows permanent focal cerebral ischemia in mutant mice with manganese superoxide dismutase deficiency. J Neurosci 18, 205-213. (Pubitemid 28046782)
76. Fujimura M, Morita-Fujimura Y, Kawase M, Copin JC, Calagui B, Epstein CJ, Chan PH (1999) Manganese superoxide dismutase mediates the early release of mitochondrial cytochrome C and subsequent DNA fragmentation after permanent focal cerebral ischemia in mice. J Neurosci 19, 3414-3422. (Pubitemid 29203121)
77. Keller JN, Kindy MS, Holtsberg FW, St Clair DK, Yen HC, Germeyer A, Steiner SM, Bruce-Keller AJ, Hutchins JB, Mattson MP (1998) Mitochondrial manganese superoxide dismutase prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation, and mitochondrial dysfunction. J Neurosci 18, 687-697. (Pubitemid 28041905)
78. Maier CM, Hsieh L, Crandall T, Narasimhan P, Chan PH (2006) A new approach for the investigation of reperfusion-related brain injury. Biochem Soc Trans 34, 1366-1369. (Pubitemid 46769056)
79. Kitayama J, Yi C, Faraci FM, Heistad DD (2006) Modulation of dilator responses of cerebral arterioles by extracellular superoxide dismutase. Stroke 37, 2802-2806. (Pubitemid 44922543)
80. Sheng H, Brady TC, Pearlstein RD, Crapo JD, Warner DS (1999) Extracellular superoxide dismutase deficiency worsens outcome from focal cerebral ischemia in the mouse. Neurosci Lett 267, 13-16. (Pubitemid 29251611)
81. Sheng H, Bart RD, Oury TD, Pearlstein RD, Crapo JD, Warner DS (1999) Mice overexpressing extracellular superoxide dismutase have increased resistance to focal cerebral ischemia. Neuroscience 88, 185-191. (Pubitemid 28440401)
82. Weisbrot-Lefkowitz M, Reuhl K, Perry B, Chan PH, Inouye M, Mirochnitchenko O (1998) Overexpression of human glutathione peroxidase protects transgenic mice against focal cerebral ischemia/reperfusion damage. Brain Res Mol Brain Res 53, 333-338. (Pubitemid 28085473)
83. Crack PJ, Taylor JM, Flentjar NJ, de Haan J, Hertzog P, Iannello RC, Kola I (2001) Increased infarct size and exacerbated apoptosis in the glutathione peroxidase-1 (Gpx-1) knockout mouse brain in response to ischemia/reperfusion injury. J Neurochem 78, 1389-1399. (Pubitemid 32899770)
84. Thomas T, Thomas G, McLendon C, Sutton T, Mullan M (1996) [beta]-Amyloid-mediated vasoactivity and vascular endothelial damage. Nature 380, 168-171. (Pubitemid 26085884)
85. Iadecola C, Zhang F, Niwa K, Eckman C, Turner SK, Fischer E, Younkin S, Borchelt DR, Hsiao KK, Carlson GA (1999) SOD1 rescues cerebral endothelial dysfunction in mice overexpressing amyloid precursor protein. Nat Neurosci 2, 157-161. (Pubitemid 30491316)
86. Park L, Anrather J, Zhou P, Frys K, Pitstick R, Younkin S, Carlson GA, Iadecola C (2005) NADPH-oxidase-derived reactive oxygen species mediate the cerebrovascular dysfunction induced by the amyloid beta peptide. J Neurosci 25, 1769-1777. (Pubitemid 40279282)
87. Nunomura A, Perry G, Aliev G, Hirai K, Takeda A, Balraj EK, Jones PK, Ghanbari H, Wataya T, Shimohama S, Chiba S, Atwood CS, Petersen RB, Smith MA (2001) Oxidative damage is the earliest event in Alzheimer disease. J Neuropathol Exp Neurol 60, 759-767. (Pubitemid 32678256)
88. Shan X, Chang Y, Lin C-lG (2007) Messenger RNA oxidation is an early event preceding cell death and causes reduced protein expression. FASEB J 21, 2753-2764. (Pubitemid 47372743)
89. 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. (Pubitemid 27176147)
90. Pratico D, Uryu K, Leight S, Trojanoswki JQ, Lee VM (2001) Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis. J Neurosci 21, 4183-4187. (Pubitemid 32538543)
91. Cente M, Filipcik P, Pevalova M, Novak M (2006) Expression of a truncated tau protein induces oxidative stress in a rodent model of tauopathy. Eur J Neurosci 24, 1085-1090. (Pubitemid 44268139)
92. Melov S, Adlard PA, Morten K, Johnson F, Golden TR, Hinerfeld D, Schilling B, Mavros C, Masters CL, Volitakis I, Li QX, Laughton K, Hubbard A, Cherny RA, Gibson B, Bush AI (2007) Mitochondrial oxidative stress causes hyperphosphorylation of tau. PLoS ONE 2, e536. (Pubitemid 351194010)
93. Fukui H, Moraes CT (2008) The mitochondrial impairment, oxidative stress and neurodegeneration connection: reality or just an attractive hypothesis? Trends Neurosci 31, 251-256.
94. Behl C, Davis J, Lesley R, Schubert D (1994) Hydrogen peroxide mediates amyloid β protein toxicity. Cell 77, 817-827. (Pubitemid 24187680)
95. Yan SD, Chen X, Fu J, Chen M, Zhu H, Roher A, Slattery T, Zhao L, Nagashima M, Morser J, Migheli A, Nawroth P, Stern D, Schmidt AM (1996) RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 382, 685-691. (Pubitemid 26282167)
96. Smith MA, Wehr K, Harris PL, Siedlak SL, Connor JR, Perry G (1998) Abnormal localization of iron regulatory protein in Alzheimer's disease. Brain Res 788, 232-236. (Pubitemid 28202166)
97. Weggen S, Rogers M, Eriksen J (2007) NSAIDs: small molecules for prevention of Alzheimer's disease or precursors for future drug development? Trends Pharmacol Sci 28, 536-543. (Pubitemid 47488508)
98. Martins RN, Harper CG, Stokes GB, Masters CL (1986) Increased cerebral glucose-6-phosphate dehydrogenase activity in Alzheimer's disease may reflect oxidative stress. J Neurochem 46, 1042-1045.
99. Premkumar DR, Smith MA, Richey PL, Petersen RB, Castellani R, Kutty RK, Wiggert B, Perry G, Kalaria RN (1995) Induction of heme oxygenase-1 mRNA and protein in neocortex and cerebral vessels in Alzheimer's disease. J Neurochem 65, 1399-1402.
100. Aksenov MY, Tucker HM, Nair P, Aksenova MV, Butterfield DA, Estus S, Markesbery WR (1998) The expression of key oxidative stress-handling genes in different brain regions in Alzheimer's disease. J Mol Neurosci 11, 151-164. (Pubitemid 29140165)
101. Esposito L, Raber J, Kekonius L, Yan F, Yu GQ, Bien-Ly N, Puolivali J, Scearce-Levie K, Masliah E, Mucke L (2006) Reduction in mitochondrial superoxide dismutase modulates Alzheimer's disease-like pathology and accelerates the onset of behavioral changes in human amyloid precursor protein transgenic mice. J Neurosci 26, 5167-5179. (Pubitemid 44315298)
102. Kaltschmidt B, Uherek M, Volk B, Baeuerle PA, Kaltschmidt C (1997) Transcription factor NF-kB is activated in primary neurons by amyloid β peptides and in neurons surrounding early plaques from patients with Alzheimer disease. Proc Natl Acad Sci U S A 94, 2642-2647. (Pubitemid 27136929)
103. Sano M, Ernesto C, Thomas RG, Klauber MR, Schafer K, Grundman M, Woodbury P, Growdon J, Cotman CW, Pfeiffer E, Schneider LS, Thal LJ (1997) A controlled trial of selegiline, alpha-tocopherol, or both as treatment for Alzheimer's disease. The Alzheimer's Disease Cooperative Study. N Engl J Med 336, 1216-1222.
104. Adair JC, Knoefel JE, Morgan N (2001) Controlled trial of N-acetylcysteine for patients with probable Alzheimer's disease. Neurology 57, 1515-1517. (Pubitemid 32995744)
105. Thal LJ, Grundman M, Berg J, Ernstrom K, Margolin R, Pfeiffer E, Weiner MF, Zamrini E, Thomas RG (2003) Idebenone treatment fails to slow cognitive decline in Alzheimer's disease. Neurology 61, 1498-1502. (Pubitemid 37505568)
106. Masaki KH, Losonczy KG, Izmirlian G, Foley DJ, Ross GW, Petrovitch H, Havlik R, White LR (2000) Association of vitamin E and C supplement use with cognitive function and dementia in elderly men. Neurology 54, 1265-1272. (Pubitemid 30174045)
107. Shuaib A, Lees KR, Lyden P, Grotta J, Davalos A, Davis SM, Diener HC, Ashwood T, Wasiewski WW, Emeribe U (2007) NXY-059 for the treatment of acute ischemic stroke. N Engl J Med 357, 562-571. (Pubitemid 47236281)
108. Macleod MR, van der Worp HB, Sena ES, Howells DW, Dirnagl U, Donnan GA (2008) Evidence for the efficacy of NXY-059 in experimental focal cerebral ischaemia is confounded by study quality. Stroke 39, 2824-2829.