Complete rescue of cerebrovascular function in aged Alzheimer's disease transgenic mice by antioxidants and pioglitazone, a peroxisome proliferator-activated receptor γ agonist

Journal of Neuroscience

Volumn 28, Issue 37, 2008, Pages 9287-9296

  Nicolakakis, Nektaria ^a   Aboulkassim, Tahar ^a   Ongali, Brice ^a   Lecrux, Clotilde ^a   Fernandes, Priscilla ^a   Rosa Neto, Pedro ^a,b   Tong, Xin Kang ^a   Hamel, Edith ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Amyloid ; Cerebral blood vessels; Cholinergic; Memory; Oxidative stress; PPAR

Indexed keywords

ANTIOXIDANT; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA AGONIST; PIOGLITAZONE; 2,4 THIAZOLIDINEDIONE DERIVATIVE; ACETYLCHOLINE; ACETYLCYSTEINE; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN (1 42); AMYLOID BETA-PROTEIN (1-42); AMYLOID PRECURSOR PROTEIN; ANTIDIABETIC AGENT; MANGANESE SUPEROXIDE DISMUTASE; NERVE PROTEIN; NITRIC OXIDE SYNTHASE; PEPTIDE FRAGMENT; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SUPEROXIDE DISMUTASE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN BLOOD FLOW; BRAIN FUNCTION; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; GLUCOSE TRANSPORT; MACROGLIA; MEMORY DISORDER; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SPATIAL MEMORY; AGING; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; CEREBROVASCULAR DISEASE; DISEASE MODEL; DRUG POTENTIATION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MEMORY; METABOLISM; MUTATION; TRANSGENIC MOUSE;

ACETYLCHOLINE; ACETYLCYSTEINE; AGING; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANTIOXIDANTS; BEHAVIOR, ANIMAL; CEREBROVASCULAR DISORDERS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HUMANS; HYPOGLYCEMIC AGENTS; MEMORY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; NERVE TISSUE PROTEINS; NITRIC OXIDE SYNTHASE; PEPTIDE FRAGMENTS; PPAR GAMMA; SUPEROXIDE DISMUTASE; THIAZOLIDINEDIONES;

EID: 55249125525     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3348-08.2008     Document Type: Article

References (65)

1. Adair JC, Knoefel JE, Morgan N (2001) Controlled trial of N-acetylcysteine for patients with probable Alzheimer's disease. Neurology 57:1515-1517.
2. Andresen J, Shafi NI, Bryan RM Jr (2006) Endothelial influences on cerebrovascular tone. J Appl Physiol 100:318-327.
3. Aucoin JS, Jiang P, Aznavour N, Tong XK, Buttini M, Descarries L, Hamel E (2005) Selective cholinergic denervation, independent of oxidative stress, in a mouse model of Alzheimer's disease. Neuroscience 132:73-86.
4. Auld DS, Kornecook TJ, Bastianetto S, Quirion R (2002) Alzheimer's disease and the basal forebrain cholinergic system: relations to beta-amyloid peptides, cognition, and treatment strategies. Prog Neurobiol 68:209-245.
5. Bagi Z, Koller A, Kaley G (2004) PPARγ activation, by reducing oxidative stress, increases NO bioavailability in coronary arterioles of mice with Type 2 diabetes. Am J Physiol Heart Circ Physiol 286:H742-H748.
6. Beckmann N, Schuler A, Mueggler T, Meyer EP, Wiederhold KH, Staufenbiel M, Krucker T (2003) Age-dependent cerebrovascular abnormalities and blood flow disturbances in APP23 mice modeling Alzheimer's disease. J Neurosci 23:8453-8459.
7. Brouillette J, Quirion R (2008) The common environmental pollutant dioxin-induced memory deficits by altering estrogen pathways and a major route of retinol transport involving transthyretin. Neurotoxicology 29:318-327.
8. Cabassi A, Dumont EC, Girouard H, Bouchard JF, Le Jossec M, Lamontagne D, Besner JG, de Champlain J (2001) Effects of chronic N-acetylcysteine treatment on the actions of peroxynitrite on aortic vascular reactivity in hypertensive rats. J Hypertens 19:1233-1244.
9. Cardoso A, Paula-Barbosa MM, Lukoyanov NV (2006) Reduced density of neuropeptide Y neurons in the somatosensory cortex of old male and female rats: relation to cholinergic depletion and recovery after nerve growth factor treatment. Neuroscience 137:937-948.
10. Chen XJ, Kovacevic N, Lobaugh NJ, Sled JG, Henkelman RM, Henderson JT (2006) Neuroanatomical differences between mouse strains as shown by high-resolution 3D MRI. Neuroimage 29:99-105.
11. Cummings JL (2004) Alzheimer's disease. N Engl J Med 351:59-67.
12. de la Monte SM, Tong M, Lester-Coll N, Plater M Jr, Wands JR (2006) Therapeutic rescue of neurodegeneration in experimental type 3 diabetes: relevance to Alzheimer's disease. J Alzheimer's Dis 10:89-109.
13. de la Torre JC (2004) Is Alzheimer's disease a neurodegenerative or a vascular disorder? Data, dogma, and dialectics. Lancet Neurol 3:184-190.
14. de la Torre JC, Fortin T, Park GA, Butler KS, Kozlowski P, Pappas BA, de Socarraz H, Saunders JK, Richard MT (1992) Chronic cerebrovascular insufficiency induces dementia-like deficits in aged rats. Brain Res 582:186-195.
15. DeWitt DS, Mathew BP, Chaisson JM, Prough DS (2001) Peroxynitrite reduces vasodilatory responses to reduced intravascular pressure, calcitonin gene-related peptide, and cromakalim in isolated middle cerebral arteries. J Cereb Blood Flow Metab 21:253-261.
16. Diep QN, El Mabrouk M, Cohn JS, Endemann D, Amiri F, Virdis A, Neves MF, Schiffrin EL (2002) Structure, endothelial function, cell growth, and inflammation in blood vessels of angiotensin II-infused rats: role of peroxisome proliferator-activated receptor-γ. Circulation 105:2296-2302.
17. Dröge W, Schipper HM (2007) Oxidative stress and aberrant signaling in aging and cognitive decline. Aging Cell 6:361-370.
18. Elder GA, Cho JY, English DF, Franciosi S, Schmeidler J, Sosa MA, Gasperi RD, Fisher EA, Mathews PM, Haroutunian V, Buxbaum JD (2007) Elevated plasma cholesterol does not affect brain Aβ in mice lacking the low-density lipoprotein receptor. J Neurochem 102:1220-1231.
19. Farr SA, Poon F, Dogrukol-AK D, Drake J, Banks WA, Eyerman E, Butterfield DA, Morley JE (2003) The antioxidants α-lipoic acid and N-acetylcysteine reverse memory impairment and brain oxidative stress in aged SAMP8 mice. J Neurochem 84:1173-1183.
20. Girouard H, Iadecola C (2006) Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol 100:328-335.
21. Hamel E (2004) Cholinergic modulation of the cortical microvascular bed. Prog Brain Res 145:171-178.
22. Hamel E (2006) Perivascular nerves and the regulation of cerebrovascular tone. J Appl Physiol 100:1059-1064.
23. Hamel E, Nicolakakis N, Aboulkassim T, Ongali B, Tong XK (2008) Oxidative stress and cerebrovascular dysfunction in mouse models of Alzheimer's disease. Exp Physiol 93:116-120.
24. Haydon PG, Carmignoto G (2006) Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 86:1009-1031.
25. Heneka MT, Sastre M, Dumitrescu-Ozimek L, Hanke A, Dewachter I, Kuiperi C, O'Banion K, Klockgether T, Van Leuven F, Landreth GE (2005) Acute treatment with the PPARγ agonist pioglitazone and ibuprofen reduces glial inflammation and Aβ1-42 levels in APPV717I transgenic mice. Brain 128:1442-1453.
26. Heneka MT, Landreth GE, Hüll M (2007) Drug insight: effects mediated by peroxisome proliferator-activated receptor-γ in CNS disorders. Nat Clin Pract Neurol 3:496-504.
27. Hermann DM, Kilic E, Hata R, Hossmann KA, Mies G (2001) Relationship between metabolic dysfunctions, gene responses and delayed cell death after mild focal cerebral ischemia in mice. Neuroscience 104:947-955.
28. Hwang J, Kleinhenz DJ, Rupnow HL, Campbell AG, Thulé PM, Sutliff RL, Hart CM (2007) The PPARγ ligand, rosiglitazone, reduces vascular oxidative stress and NADPH oxidase expression in diabetic mice. Vasc Pharmacol 46:456-462.
29. 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.
30. phox message expression in primary endothelial cells. Metabolism 50:3-11.
31. Kalaria RN (2000) The role of cerebral ischemia in Alzheimer's disease. Neurobiol Aging 21:321-330.
32. + channels in CGRP-induced dilatation of basilar artery in vivo. Am J Physiol 265:H581-H585.
33. Kornblum HI, Araujo DM, Annala AJ, Tatsukawa KJ, Phelps ME, Cherry SR (2000) In vivo imaging of neuronal activation and plasticity in the rat brain by high resolution positron emission tomography (microPET). Nat Biotechnol 18:655-660.
34. Lesné S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, Gallagher M, Ashe KH (2006) A specific amyloid-β protein assembly in the brain impairs memory. Nature 440:352-357.
35. Liu R, Liu IY, Bi X, Thompson RF, Doctrow SR, Malfroy B, Baudry M (2003) Reversal of age-related learning deficits and brain oxidative stress in mice with superoxide dismutase/catalase mimetics. Proc Natl Acad Sci U S A 100:8526-8531.
36. Martens FM, Visseren FL, de Koning EJ, Rabelink TJ (2005) Short-term pioglitazone treatment improves vascular function irrespective of metabolic changes in patients with type 2 diabetes. J Cardiovasc Pharmacol 46:773-778.
37. Mayhan WG, Arrick DM, Sharpe GM, Patel KP, Sun H (2006) Inhibition of NAD(P)H oxidase alleviates impaired NOS-dependent responses of pial arterioles in type 1 diabetes mellitus. Microcirculation 13:567-575.
38. Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47-60.
39. Moosavi M, Naghdi N, Maghsoudi N, Zahedi Asl S (2007) Insulin protects against stress-induced impairments in water maze performance. Behav Brain Res 176:230-236.
40. Mosconi L, Perani D, Sorbi S, Herholz K, Nacmias B, Holthoff V, Salmon E, Baron J-C, De Cristofaro MT, Padovani A, Borroni B, Franceschi M, Bracco L, Pupi A (2004) MCI conversion to dementia and the APOE genotype: a prediction study with FDG-PET. Neurology 63:2332-2340.
41. 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J Neurosci 20:4050-4058.
42. Niwa K, Younkin L, Ebeling C, Turner SK, Westaway D, Younkin S, Ashe KH, Carlson GA, Iadecola C (2000) Abeta 1-40-related reduction in functional hyperemia in mouse neocortex during somatosensory activation. Proc Natl Acad Sci U S A 97:9735-9740.
43. Niwa K, Kazama K, Younkin L, Younkin SG, Carlson GA, Iadecola C (2002) Cerebrovascular autoregulation is profoundly impaired in mice overexpressing amyloid precursor protein. Am J Physiol Heart Circ Physiol 283:H315-H323.
44. Palop JJ, Jones B, Kekonius L, Chin J, Yu GQ, Raber J, Masliah E, Mucke L (2003) Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer's disease-related cognitive deficits. Proc Natl Acad Sci U S A 100:9572-9577.
45. 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-β peptide. J Neurosci 25:1769-1777.
46. 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.
47. Pathan AR, Viswanad B, Sonkusare SK, Ramarao P (2006) Chronic administration of pioglitazone attenuates intracerebroventricular streptozotocin induced-memory impairment in rats. Life Sci 79:2209-2216.
48. Pedersen WA, McMillan PJ, Kulstad JJ, Leverenz JB, Craft S, Haynatzki GR (2006) Rosiglitazone attenuates learning and memory deficits in Tg2576 Alzheimer mice. Exp Neurol 199:265-273.
49. Petersen RC, Thomas RG, Grundman M, Bennett D, Doody R, Ferris S, Galasko D, Jin S, Kaye J, Levey A, Pfeiffer E, Sano M, van Dyck CH, Thal LJ (2005) Vitamin E and donepezil for the treatment of mild cognitive impairment. N Engl J Med 352:2379-2388.
50. Risner ME, Saunders AM, Altman JF, Ormandy GC, Craft S, Foley IM, Zvartau-Hind ME, Hosford DA, Roses AD (2006) Efficacy of rosiglitazone in a genetically defined population with mild-to-moderate Alzheimer's disease. Pharmacogenomics J 6:246-254.
51. Ruetzler CA, Furuya K, Takeda H, Hallenbeck JM (2001) Brain vessels normally undergo cyclic activation and inactivation: evidence from tumor necrosis factor-α, heme oxygenase-1, and manganese superoxide dismutase immunostaining of vessels and perivascular brain cells. J Cereb Blood Flow Metab 21:244-252.
52. Ruitenberg A, den Heijer T, Bakker SL, van Swieten JC, Koudstaal PJ, Hofman A, Breteler MM (2005) Cerebral hypoperfusion and clinical onset of dementia: the Rotterdam study. Ann Neurol 57:789-794.
53. 2α. Hypertension 33:424-428.
54. Schnackenberg CG, Wilcox CS (2001) The SOD mimetic tempol restores vasodilation in afferent arterioles of experimental diabetes. Kidney Int 59:1859-1864.
55. Silverman DH, Small GW, Chang CY, Lu CS, Kung De Aburto MA, Chen W, Czernin J, Rapoport SI, Pietrini P, Alexander GE, Schapiro MB, Jagust WJ, Hoffman JM, Welsh-Bohmer KA, Alavi A, Clark CM, Salmon E, de Leon MJ, Mielke R, Cummings JL, et al. (2001) Positron emission tomography in evaluation of dementia: regional brain metabolism and long-term outcome. JAMA 286:2120-2127.
56. Sun X, He G, Qing H, Zhou W, Dobie F, Cai F, Staufenbiel M, Huang LE, Song W (2006) Hypoxia facilitates Alzheimer's disease pathogenesis by up-regulating BACE1 gene expression. Proc Natl Acad Sci U S A 103:18727-18732.
57. Tong XK, Hamel E (1999) Regional cholinergic denervation of cortical microvessels and nitric oxide synthase-containing neurons in Alzheimer's disease. Neuroscience 92:163-175.
58. Tong XK, Nicolakakis N, Kocharyan A, Hamel E (2005) Vascular remodeling versus amyloid beta-induced oxidative stress in the cerebrovascular dysfunctions associated with Alzheimer's disease. J Neurosci 25:11165-11174.
59. Watson GS, Cholerton BA, Reger MA, Baker LD, Plymate SR, Asthana S, Fishel MA, Kulstad JJ, Green PS, Cook DG, Kahn SE, Keeling ML, Craft S (2005) Preserved cognition in patients with early Alzheimer disease and amnestic mild cognitive impairment during treatment with rosiglitazone: a preliminary study. Am J Geriatr Psychiatry 13:950-958.
60. Wilcock DM, Alamed J, Gottschall PE, Grimm J, Rosenthal A, Pons J, Ronan V, Symmonds K, Gordon MN, Morgan D (2006) Deglycosylated anti-amyloid-β antibodies eliminate cognitive deficits and reduce parenchymal amyloid with minimal vascular consequences in aged amyloid precursor protein transgenic mice. J Neurosci 26:5340-5346.
61. Wong GH, Goeddel DV (1988) Induction of manganous superoxide dismutase by tumor necrosis factor: Possible protective mechanism. Science 242:941-944.
62. Wyss-Coray T, Loike JD, Brionne TC, Lu E, Anankov R, Yan F, Silverstein SC, Husemann J (2003) Adult mouse astrocytes degrade amyloid-β in vitro and in situ. Nat Med 9:453-457.
63. Yan Q, Zhang J, Liu H, Babu-Khan S, Vassar R, Biere AL, Citron M, Landreth G (2003) Anti- inflammatory drug therapy alters β-amyloid processing and deposition in an animal model of Alzheimer's disease. J Neurosci 23:7504-7509.
64. Zlokovic BV (2005) Neurovascular mechanisms of Alzheimer's neurodegeneration. Trends Neurosci 28:202-208.
65. Zonta M, Angulo MC, Gobbo S, Rosengarten B, Hossmann KA, Pozzan T, Carmignoto G (2003) Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation. Nat Neurosci 6:43-50.