NADPH oxidase-derived reactive oxygen species mediate the cerebrovascular dysfunction induced by the amyloid β peptide

Journal of Neuroscience

Volumn 25, Issue 7, 2005, Pages 1769-1777

  Park, Laibaik ^a   Anrather, Josef ^a   Zhou, Ping ^a   Frys, Kelly ^a   Pitstick, Rose ^c   Younkin, Steven ^b   Carlson, George A ^c   Iadecola, Costantino ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b MAYO CLINIC   (United States)

^c MCLAUGHLIN RESEARCH INSTITUTE   (United States)

Author keywords

Alzheimer's disease; Cerebral blood flow; gp91phox; Hydroethidine; Reactive oxygen species; Tg2576

Indexed keywords

ACETYLCHOLINE; AMYLOID BETA PROTEIN; N ACETYL S NITROSOPENICILLAMINE; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOREGULATION; BRAIN BLOOD FLOW; CEREBROVASCULAR DISEASE; CONTROLLED STUDY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL;

ACETYLCHOLINE; ADENOSINE; ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRADYKININ; CALCIMYCIN; CEREBROVASCULAR CIRCULATION; FEMALE; GLYCOPROTEINS; HUMANS; HYPEREMIA; LASER-DOPPLER FLOWMETRY; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; NADPH OXIDASE; NERVE TISSUE PROTEINS; NITRIC OXIDE DONORS; OXIDATIVE STRESS; PEPTIDE FRAGMENTS; PHENANTHRIDINES; REACTIVE OXYGEN SPECIES; S-NITROSO-N-ACETYLPENICILLAMINE; VIBRISSAE; X CHROMOSOME;

EID: 14044258771     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5207-04.2005     Document Type: Article

References (80)

1. Abramov AY, Canevari L, Duchen MR (2004) β-Amyloid peptides induce mitochondrial dysfunction and oxidative stress in astrocytes and death of neurons through activation of NADPH oxidase. J Neurosci 24:565-575.
2. Adachi T, Weisbrod RM, Pimentel DR, Ying J, Sharov VS, Schoneich C, Cohen RA (2004) S-Glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide. Nat Med 10:1200-1207.
3. Ayata C, Ma J, Meng W, Huang P, Moskowitz MA (1996) L-NA-sensitive rCBF augmentation during vibrissal stimulation in type III nitric oxide synthase mutant mice. J Cereb Blood Flow Metab 16:539-541.
4. Babior BM (2004) NADPH oxidase. Curr Opin Immunol 16:42-47.
5. Bamberger ME, Harris ME, McDonald DR, Husemann J, Landreth GE (2003) A cell surface receptor complex for fibrillar β-amyloid mediates microglial activation. J Neurosci 23:2665-2674.
6. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA (1990) Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87:1620-1624.
7. 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. A possible inflammatory mechanism of neuronal damage in Alzheimer's disease. J Biol Chem 274:15493-15499.
8. Breteler MM (2000) Vascular risk factors for Alzheimer's disease: an epidemiologic perspective. Neurobiol Aging 21:153-160.
9. Brun A, Englund E (1986) A white matter disorder in dementia of the Alzheimer type: a pathoanatomical study. Ann Neurol 19:253-262.
10. Busse R, Fleming I (2003) Regulation of endothelium-derived vasoactive autacoid production by hemodynamic forces. Trends Pharmacol Sci 24:24-29.
11. Casserly I, Topol E (2004) Convergence of atherosclerosis and Alzheimer's disease: inflammation, cholesterol, and misfolded proteins. Lancet 363:1139-1146.
12. Chillon JM, Baumbach GL (2002) Autoregulation: arterial and intracranial pressure. In: Cerebral blood flow and metabolism (Edvinsson L, Krause DN, eds), pp 395-412. Philadelphia: Lippincott Williams and Wilkins.
13. Coraci IS, Husemann J, Berman JW, Hulette C, Dufour JH, Campanella GK, Luster AD, Silverstein SC, El-Khoury JB (2002) CD36, a class B scavenger receptor, is expressed on microglia in Alzheimer's disease brains and can mediate production of reactive oxygen species in response to beta-amyloid fibrils. Am J Pathol 160:101-112.
14. Crawford F, Suo Z, Fang C, Mullan M (1998) Characteristics of the in vitro vasoactivity of beta-amyloid peptides. Exp Neurol 150:159-168.
15. Deane R, Du Yan S, Submamaryan RK, LaRue B, Jovanovic S, Hogg E, Weich D, Manness L, Lin C, Yu J, Zhu H, Ghiso J, Frangione B, Stern A, Schmidt AM, Armstrong DL, Arnold B, Liliensiek B, Nawroth P, Hofman F, et al. (2003) RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain. Nat Med 9:907-913.
16. de la Torre JC (2004) Is Alzheimer's disease a neurodegenerative or a vascular disorder? Data, dogma, and dialectics. Lancet Neurol 3:184-190.
17. Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47-95.
18. Duerrschmidt N, Wippich N, Goettsch W, Broemme HJ, Morawietz H (2000) Endothelin-1 induces NAD(P)H oxidase in human endothelial cells. Biochem Biophys Res Commun 269:713-717.
19. El Khoury J, Hickman SE, Thomas CA, Cao L, Silverstein SC, Loike JD (1996) Scavenger receptor-mediated adhesion of microglia to beta-amyloid fibrils. Nature 382:716-719.
20. El Khoury JB, Moore KJ, Means TK, Leung J, Terada K, Toft M, Freeman MW, Luster AD (2003) CD36 mediates the innate host response to beta-amyloid. J Exp Med 197:1657-1666.
21. Faraci FM (2003) Hyperhomocysteinemia: a million ways to lose control. Arterioscler Thromb Vasc Biol 23:371-373.
22. Farkas E, de Wilde MC, Kiliaan AJ, Luiten PG (2002) Chronic cerebral hypoperfusion-related neuropathologic changes and compromised cognitive status: window of treatment. Drugs Today (Barc) 38:365-376.
23. Fuhrman B, Shiner M, Volkova N, Aviram M (2004) Cell-induced copper ion-mediated low density lipoprotein oxidation increases during in vivo monocyte-to-macrophage differentiation. Free Radic Biol Med 37:259-271.
24. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW (1994) Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res 74:1141-1148.
25. Guo W, Adachi T, Matsui R, Xu S, Jiang B, Zou MH, Kirber M, Lieberthal W, Cohen RA (2003) Quantitative assessment of tyrosine nitration of manganese superoxide dismutase in angiotensin II-infused rat kidney. Am J Physiol Heart Circ Physiol 285:H1396-H1403.
26. Hock C, Villringer K, Muller-Spahn F, Wenzel R, Heekeren H, Schuh-Hofer S, Hofmann M, Minoshima S, Schwaiger M, Dirnagl U, Villringer A (1997) Decrease in parietal cerebral hemoglobin oxygenation during performance of a verbal fluency task in patients with Alzheimer's disease monitored by means of near-infrared spectroscopy (NIRS)-correlation with simultaneous rCBF-PET measurements. Brain Res 755:293-303.
27. Hossmann KA (1994) Viability thresholds and the penumbra of focal ischemia. Ann Neurol 36:557-565.
28. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G (1996) Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 274:99-102.
29. 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.
30. Iadecola C (1992) Nitric oxide participates in the cerebrovasodilation elicited from cerebellar fastigial nucleus. Am J Physiol 263:R1156-R1161.
31. Iadecola C (2004) Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Rev Neurosci 5:347-360.
32. Iadecola C, Niwa K (2002) Nitric oxide. In: Cerebral blood flow and metabolism (Edvinsson L, Krause DN, eds), pp 295-310. Philadelphia: Lippincott, Williams and Wilkins.
33. 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.
34. Ischiropoulos H, Beckman JS (2003) Oxidative stress and nitration in neurodegeneration: cause, effect, or association? J Clin Invest 111:163-169.
35. Jagust WJ (2000) Neuroimaging in dementia. Neurol Clin 18:885-902.
36. Jones SC, Radinsky CR, Furlan AJ, Chyatte D, Perez-Trepichio AD (1999) Cortical NOS inhibition raises the lower limit of cerebral blood flow-arterial pressure autoregulation. Am J Physiol 276:H1253-H1262.
37. Katusic ZS (2001) Vascular endothelial dysfunction: does tetrahydrobiopterin play a role? Am J Physiol Heart Circ Physiol 281:H981-H986.
38. Kawarabayashi T, Younkin LH, Saido TC, Shoji M, Ashe KH, Younkin SG (2001) Age-dependent changes in brain, CSF, and plasma amyloid β protein in the Tg2576 transgenic mouse model of Alzheimer's disease. J Neurosci 21:372-381.
39. Lambeth JD (2004) NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4:181-189.
40. Li JM, Shah AM (2004) Endothelial cell superoxide generation: regulation and relevance for cardiovascular pathophysiology. Am J Physiol Regul Integr Comp Physiol 287:R1014-R1030.
41. Martin KC, Barad M, Kandel ER (2000) Local protein synthesis and its role in synapse-specific plasticity. Curr Opin Neurobiol 10:587-592.
42. Matsushita K, Kuriyama Y, Nagatsuka K, Nakamura M, Sawada T, Omae T (1994) Periventricular white matter lucency and cerebral blood flow autoregulation in hypertensive patients. Hypertension 23:565-568.
43. Mentis MJ, Alexander GE, Krasuski J, Pietrini P, Furey ML, Schapiro MB, Rapoport SI (1998) Increasing required neural response to expose abnormal brain function in mild versus moderate or severe Alzheimer's disease: PET study using parametric visual stimulation. Am J Psychiatry 155:785-794.
44. Mies G, Ishimaru S, Xie Y, Seo K, Hossmann KA (1991) Ischemic thresholds of cerebral protein synthesis and energy state following middle cerebral artery occlusion in rat. J Cereb Blood Flow Metab 11:753-761.
45. Milekic MH, Alberini CM (2002) Temporally graded requirement for protein synthesis following memory reactivation. Neuron 36:521-525.
46. Mohazzab KM, Kaminski PM, Wolin MS (1994) NADH oxidoreductase is a major source of superoxide anion in bovine coronary artery endothelium. Am J Physiol 266:H2568-H2572.
47. Niwa K, Younkin L, Ebeling C, Turner SK, Westaway D, Younkin S, Ashe KH, Carlson GA, Iadecola C (2000a) Abeta 1-40-related reduction in functional hyperemia in mouse neocortex during somatosensory activation. Proc Natl Acad Sci USA 97:9735-9740.
48. Niwa K, Carlson GA, Iadecola C (2000b) Exogenous A beta 1-40 reproduces cerebrovascular alterations resulting from amyloid precursor protein overexpression in mice. J Cereb Blood Flow Metab 20:1659-1668.
49. Niwa K, Haensel C, Ross ME, Iadecola C (2001a) Cyclooxygenase-1 participates in selected vasodilator responses of the cerebral circulation. Circ Res 88:600-608.
50. Niwa K, Porter VA, Kazama K, Cornfield D, Carlson GA, Iadecola C (2001b) Abeta-peptides enhance vasoconstriction in cerebral circulation. Am J Physiol Heart Circ Physiol 281:H2417-H2424.
51. Niwa K, Kazama K, Younkin SG, Carlson GA, Iadecola C (2002a) Alterations in cerebral blood flow and glucose utilization in mice overexpressing the amyloid precursor protein. Neurobiol Dis 9:61-68.
52. Niwa K, Kazama K, Younkin L, Younkin SG, Carlson GA, Iadecola C (2002b) Cerebrovascular autoregulation is profoundly impaired in mice overexpressing amyloid precursor protein. Am J Physiol Heart Circ Physiol 283:H315-H323.
53. Paris D, Humphrey J, Quadros A, Patel N, Crescentini R, Crawford F, Mullan M (2003) Vasoactive effects of A beta in isolated human cerebrovessels and in a transgenic mouse model of Alzheimer's disease: role of inflammation. Neurol Res 25:642-651.
54. Park L, Anrather J, Forster C, Kazama K, Carlson GA, Iadecola C (2004a) Abeta-induced vascular oxidative stress and attenuation of functional hyperemia in mouse somatosensory cortex. J Cereb Blood Flow Metab 24:334-342.
55. Park L, Anrather J, Zhou P, Frys K, Wang G, Iadecola C (2004b) Exogenous NADPH increases cerebral blood flow through NADPH oxidase-dependent and -independent mechanisms. Arterioscler Thromb Vasc Biol 24:1860-1865.
56. Parvathenani LK, Tertyshnikova S, Greco CR, Roberts SB, Robertson B, Posmantur R (2003) P2X7 mediates superoxide production in primary microglia and is up-regulated in a transgenic mouse model of Alzheimer's disease. J Biol Chem 278:13309-13317.
57. Pollock ID, Williams DA, Gifford MA, Li LL, Du X, Fisherman J, Orkin SH, Doerschuk CM, Dinauer MC (1995) Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat Genet 9:202-209.
58. Prohovnik I, Mayeux R, Sackeim HA, Smith G, Stern Y, Alderson PO (1988) Cerebral perfusion as a diagnostic marker of early Alzheimer's disease. Neurology 38:931-937.
59. Rey FE, Cifuentes ME, Kiarash A, Quinn MT, Pagano PJ (2001) Novel competitive inhibitor of NAD(P)H oxidase assembly attenuates vascular O(2)(-) and systolic blood pressure in mice. Circ Res 89:408-414.
60. Roher AE, Esh C, Kokjohn TA, Kalback W, Luehrs DC, Seward ID, Sue LI, Beach TG (2003) Circle of willis atherosclerosis is a risk factor for sporadic Alzheimer's disease. Arterioscler Thromb Vasc Biol 23:2055-2062.
61. Roher AE, Esh C, Rahman A, Kokjohn TA, Beach TG (2004) Atherosclerosis of cerebral arteries in Alzheimer disease. Stroke 35:2623-2627.
62. Rosenblum WI (1987) Hydroxyl radical mediates the endothelium-dependent relaxation produced by bradykinin in mouse cerebral arterioles. Circ Res 61:601-603.
63. Rosenblum WI, McDonald M, Wormley B (1989) Calcium ionophore and acetylcholine dilate arterioles on the mouse brain by different mechanisms. Stroke 20:1391-1395.
64. Scheuner D, Eckman C, Jensen M, Song X, Citron M, Suzuki N, Bird TD, Hardy J, Hutton M, Kukull W, Larson E, Levy LE, Viitanen M, Peskind E, Poorkaj P, Schellenberg G, Tanzi R, Wasco W, Lannfelt L, Selkoe D, et al. (1996) Secreted amyloid beta-protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease. Nat Med 2:864-870.
65. Selkoe DJ, Schenk D (2003) Alzheimer's disease: molecular understanding predicts amyloid-based therapeutics. Annu Rev Pharmacol Toxicol 43:545-584.
66. Shimohama S, Tanino H, Kawakami N, Okamura N, Kodama H, Yamaguchi T, Hayakawa T, Nunomura A, Chiba S, Perry G, Smith MA, Fujimoto S (2000) Activation of NADPH oxidase in Alzheimer's disease brains. Biochem Biophys Res Commun 273:5-9.
67. Sobey CG, Faraci FM (1997) Effects of a novel inhibitor of guanylyl cyclase on dilator responses of mouse cerebral arterioles. Stroke 28:837-843.
68. Soriano FG, Virag L, Szabo C (2001) Diabetic endothelial dysfunction: role of reactive oxygen and nitrogen species production and poly(ADP-ribose) polymerase activation. J Mol Med 79:437-448.
69. Stamler JS (1996) A radical vascular connection. Nature 380:108-111.
70. Stewart R, Cai H, Harrison DG, Rothe G, Valet G (1998) Cardiovascular factors in Alzheimer's disease. J Neurol Neurosurg Psychiatry 65:143-147.
71. Thomas T, Thomas G, McLendon C, Sutton T, Mullan M (1996) β-Amyloid-mediated vasoactivity and vascular endothelial damage. Nature 380:168-171.
72. Van Dijk EJ, Prins ND, Vermeer SE, Hofman A, Van Duijn CM, Koudstaal PJ, Breteler MM (2004) Plasma amyloid beta, apolipoprotein E, lacunar infarcts, and white matter lesions. Ann Neurol 55:570-575.
73. Wautier MP, Chappey O, Corda S, Stern DM, Schmidt AM, Wautier IL (2001) Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am J Physiol Endocrinol Metab 280:E685-E694.
74. Yan SD, Chen X, Fu I, 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.
75. Yang G, Iadecola C (1997) Obligatory role of NO in glutamate-dependent hyperemia evoked from cerebellar parallel fibers. Am J Physiol 272:R1155-RI161.
76. Yang G, Chen G, Ebner TJ, Iadecola C (1999) Nitric oxide is the predominant mediator of cerebellar hyperemia during somatosensory activation in rats. Am J Physiol 277:R1760-R1770.
77. Yang G, Zhang Y, Ross ME, Iadecola C (2003) Attenuation of activity-induced increases in cerebellar blood flow in mice lacking neuronal nitric oxide synthase. Am J Physiol Heart Circ Physiol 285:H298-H304.
78. Zhang F, Eckman C, Younkin S, Hsiao KK, Iadecola C (1997) Increased susceptibility to ischemic brain damage in transgenic mice overexpressing the amyloid precursor protein. J Neurosci 17:7655-7661.
79. Zheng JS, Yang XQ, Lookingland KJ, Fink GD, Hesslinger C, Kapatos G, Kovesdi I, Chen AF (2003) Gene transfer of human guanosine 5′-triphosphate cyclohydrolase I restores vascular tetrahydrobiopterin level and endothelial function in low renin hypertension. Circulation 108:1238-1245.
80. Zou MH, Leist M, Ullrich V (1999) Selective nitration of prostacyclin synthase and defective vasorelaxation in atherosclerotic bovine coronary arteries. Am J Pathol 154:1359-1365.