Transgenic mice overexpressing APP and transforming growth factor-β1 feature cognitive and vascular hallmarks of Alzheimer's disease

American Journal of Pathology

Volumn 177, Issue 6, 2010, Pages 3071-3080

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

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; NITRIC OXIDE; SUPEROXIDE DISMUTASE; TRANSFORMING GROWTH FACTOR BETA1;

ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BLOOD VESSEL REACTIVITY; BRAIN BLOOD FLOW; BRAIN FUNCTION; CELL ACTIVATION; CHOLINERGIC SYSTEM; COGNITIVE DEFECT; CONTROLLED STUDY; FEMALE; FIBROSIS; GENE OVEREXPRESSION; GLUCOSE TRANSPORT; MALE; MAZE TEST; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SPATIAL MEMORY; TRANSGENIC MOUSE;

EID: 78650206599     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.100339     Document Type: Article

References (62)

1. de la Torre JC: Is Alzheimer's disease a neurodegenerative or a vascular disorder? Data, dogma, and dialectics. Lancet Neurol 2004, 3:184-190
2. Zlokovic BV: Neurovascular mechanisms of Alzheimer's neurodegeneration. Trends Neurosci 2005, 28:202-208
3. Kalaria RN, Maestre GE, Arizaga R, Friedland RP, Galasko D, Hall K, Luchsinger JA, Ogunniyi A, Perry EK, Potocnik F, Prince M, Stewart R, Wimo A, Zhang ZX, Antuono P: Alzheimer's disease and vascular dementia in developing countries: prevalence, management, and risk factors. Lancet Neurol 2008, 7:812-826
4. Mancardi GL, Perdelli F, Rivano C, Leonardi A, Bugiani O: Thickening of the basement membrane of cortical capillaries in Alzheimer's disease. Acta Neuropathol 1980, 49:79-83 (Pubitemid 10139968)
5. Perlmutter LS, Chui HC: Microangiopathy, the vascular basement membrane and Alzheimer's disease: a review. Brain Res Bull 1990, 24:677-686
6. Iadecola C: Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Neurosci Rev 2004, 5:347-360
7. Sun X, He G, Qing H, Zhou W, Dobie F, Cai F, Staufenbiel M, Huang LE, Song W: Hypoxia facilitates Alzheimer's disease pathogenesis by up-regulating BACE1 gene expression. Proc Natl Acad Sci USA 2006, 103:18727-18732
8. Langbaum JB, Chen K, Lee W, Reschke C, Bandy D, Fleisher AS, Alexander GE, Foster NL, Weiner MW, Koeppe RA, Jagust WJ, Reiman EM: Alzheimer's Disease Neuroimaging Initiative. Categorical and correlational analyses of baseline fluorodeoxyglucose positron emission tomography images from the Alzheimer's Disease Neuroimaging Initiative (ADNI) Neuroimage 2009, 45:1107-1116
9. Vinters HV, Wang ZZ, Secor DL: Brain parenchymal and microvascular amyloid in Alzheimer's disease. Brain Pathol 1996, 6:179-195
10. Roher AE, Kuo YM, Esh C, Knebel C, Weiss N, Kalback W, Luehrs DC, Childress JL, Beach TG, Weller RO, Kokjohn TA: Cortical and leptomeningeal cerebrovascular amyloid and white matter pathology in Alzheimer's disease. Mol Med 2003, 9:112-122
11. Wyss-Coray T, Masliah E, Mallory M, McConlogue L, Johnson-Wood K, Lin C, Mucke L: Amyloidogenic role of cytokine TGF-β1 in transgenic mice and in Alzheimer's disease. Nature 1997, 389:603-606 (Pubitemid 27446177)
12. Wyss-Coray T, Lin C, Sanan DA, Mucke L, Masliah E: Chronic overproduction of transforming growth factor-beta1 by astrocytes promotes Alzheimer's disease-like microvascular degeneration in transgenic mice. Am J Pathol 2000, 156:139-150
13. Grammas P, Ovase R: Cerebrovascular transforming growth factor-β contributes to inflammation in the Alzheimer's disease brain. Am J Pathol 2002, 160:1583-1587
14. Tarkowski E, Issa R, Sjögren M, Wallin A, Blennow K, Tarkowski A, Kumar P: Increased intrathecal levels of the angiogenic factors VEGF and TGF-beta in Alzheimer's disease and vascular dementia. Neurobiol Aging 2002, 23:237-243
15. Tong XK, Nicolakakis N, Kocharyan A, Hamel E: Vascular remodeling versus amyloid β-induced oxidative stress in the cerebrovascular dysfunctions associated with Alzheimer's disease. J Neurosci 2005, 25:11165-11174
16. Wyss-Coray T, Lin C, Yan F, Yu GQ, Rohde M, McConlogue L, Masliah E, Mucke L: TGF-beta1 promotes microglial amyloid-beta clearance and reduces plaque burden in transgenic mice. Nat Med 2001, 7:612-618
17. Town T, Laouar Y, Pittenger C, Mori T, Szekely CA, Tan J, Duman RS, Flavell RA: Blocking TGF-β-Smad2/3 innate immune signaling mitigates Alzheimer-like pathology. Nat Med 2008, 14:681-687 (Pubitemid 351809551)
18. Iadecola C, Zhang F, Niwa K, Eckman C, Turner SK, Fischer E, Younkin S, Borchelt DR, Hsiao KK, Carlson GA: SOD1 rescues cerebral endothelial dysfunction in mice overexpressing amyloid precursor protein. Nat Neurosci 1999, 2:157-161
19. Gaertner RF, Wyss-Coray T, Von Euw D, Lesné S, Vivien D, Lacombe P: Reduced brain tissue perfusion in TGF-β1 transgenic mice showing Alzheimer's disease-like cerebrovascular abnormalities. Neurobiol Dis 2005, 19:38-46
20. Park L, Anrather J, Zhou P, Frys K, Pitstick R, Younkin S, Carlson GA, Iadecola C: NADPH-oxidase-derived reactive oxygen species mediate the cerebrovascular dysfunction induced by the amyloid beta peptide. J Neurosci 2005, 25:1769-1777
21. Mucke L, Masliah E, Yu GQ, Mallory M, Rockenstein EM, Tatsuno G, Hu K, Kholodenko D, Johnson-Wood K, McConlogue L: High-level neuronal expression of Aβ1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J Neurosci 2000, 20:4050-4058
22. Wyss-Coray T, Feng L, Masliah E, Ruppe MD, Lee HS, Toggas SM, Rockenstein EM, Mucke L: Increased central nervous system production of extracellular matrix components and development of hydrocephalus in transgenic mice overexpressing transforming growth factor-beta 1. Am J Pathol 1995, 147:53-67
23. Nicolakakis N, Aboulkassim T, Ongali B, Lecrux C, Fernandes P, Rosa-Neto P, Tong XK, Hamel E: Complete rescue of cerebrovascular function in aged Alzheimer's disease transgenic mice by antioxidants and pioglitazone, a peroxisome proliferator-activated receptor gamma agonist. J Neurosci 2008, 28:9287-9296
24. Nicolakakis N, Aboulkassim T, Aliaga A, Tong XK, Rosa-Neto P, Hamel E: Intact memory in TGF-β1 transgenic mice featuring chronic cerebrovascular deficit: recovery with pioglitazone. J Cereb Blood Flow Metab doi: 10.1038/jcbfm.2010.78
25. Aucoin JS, Jiang P, Aznavour N, Tong XK, Buttini M, Descarries L, Hamel E: Selective cholinergic denervation, independent from oxidative stress, in a mouse model of Alzheimer's disease. Neurosci 2005, 132:73-86
26. Lau JC, Lerch JP, Sled JG, Henkelman RM, Evans AC, Bedell BJ: Longitudinal neuroanatomical changes determined by deformation-based morphometry in a mouse model of Alzheimer's disease. NeuroImage 2008, 42:19-27
27. Kornblum HI, Araujo DM, Annala AJ, Tatsukawa KJ, Phelps ME, Cherry SR: In vivo imaging of neuronal activation and plasticity in the rat brain by high resolution positron emission tomography (micro-PET). Nature Biotechnol 2000, 18:655-660
28. Tong XK, Nicolakakis N, Fernandes P, Ongali B, Brouillette J, Quirion R, Hamel E: Simvastatin improves cerebrovascular function and counters soluble amyloid-beta, inflammation and oxidative stress in aged APP mice. Neurobiol Dis 2009, 35:406-414
29. Papadopoulos P, Ongali B, Hamel E: Selective in vivo antagonism of endothelin receptors in transforming growth factor-β1 transgenic mice that mimic the vascular pathology of Alzheimer's disease. Can J Physiol Pharmacol 2010, 88:652-660
30. Park L, Zhou P, Pitstick R, Capone C, Anrather J, Norris EH, Younkin L, Younkin S, Carlson G, McEwen BS, Iadecola C: Nox2-derived radicals contribute to neurovascular and behavioral dysfunction in mice overexpressing the amyloid precursor protein. Proc Natl Acad Sci USA 2008, 105:1347-1352
31. Pellerin L, Bouzier-Sore AK, Aubert A, Serres S, Merle M, Costalat R, Magistretti PJ: Activity-dependent regulation of energy metabolism by astrocytes: an update. Glia 2007, 55:1251-1262
32. Roher AE, Lowenson JD, Clarke S, Woods AS, Cotter RJ, Gowing E, Ball MJ: β-Amyloid-(1-42) is a major component of cerebrovascular amyloid deposits: implications for the pathology of Alzheimer disease. Proc Natl Acad Sci USA 1993, 90:10836-10840
33. Kalaria RN, Pax AB: Increased collagen content of cerebral microvessels in Alzheimer's disease. Brain Res 1995, 705:349-352
34. Castillo GM, Ngo C, Cummings J, Wight TN, Snow AD: Perlecan binds to the β-amyloid proteins (Aβ) of Alzheimer's disease, accelerates Aβ fibril formation, and maintains Aβ fibril stability. J Neurochem 1997, 69:2452-2465 (Pubitemid 27495432)
35. Weller RO, Subash M, Preston SD, Mazanti I, Carare RO: Perivascular drainage of amyloid-β peptides from the brain and its failure in cerebral amyloid angiopathy and Alzheimer's disease. Brain Pathol 2008, 18:253-266
36. Wilcock DM, Gharkholonarehe N, Van Nostrand WE, Davis J, Vitek MP, Colton CA: Amyloid reduction by amyloid-β vaccination also reduces mouse tau pathology and protects from neuron loss in two mouse models of Alzheimer's disease. J Neurosci 2009, 29: 7957-7965 Erratum in. J Neurosci 2010, 30:1197-1198
37. Boche D, Zotova E, Weller RO, Love S, Neal JW, Pickering RM, Wilkinson D, Holmes C, Nicoll JA: Consequence of Aβ immunization on the vasculature of human Alzheimer's disease brain. Brain 2008, 131:3299-3310
38. Haydon PG, Carmignoto G: Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 2006, 86:1009-1031
39. Wilcock DM, Vitek MP, Colton CA: Vascular amyloid alters astrocytic water and potassium channels in mouse models and humans with Alzheimer's disease. Neuroscience 2009, 159:1055-1069
40. Han BH, Zhou ML, Abousaleh F, Brendza RP, Dietrich HH, Koenigsknecht-Talboo J, Cirrito JR, Milner E, Holtzman DM, Zipfel GJ: Cerebrovascular dysfunction in amyloid precursor protein transgenic mice: contribution of soluble and insoluble amyloid-β peptide, partial restoration via γ-secretase inhibition. J Neurosci 2008, 28:13542-13550
41. Hamel E, Nicolakakis N, Aboulkassim T, Ongali B, Tong XK: Oxidative stress and cerebrovascular dysfunction in mouse models of Alzheimer's disease. Exp Physiol 2008, 93:116-120
42. Luterman JD, Haroutunian V, Yemul S, Ho L, Purohit D, Aisen PS, Mohs R, Pasinetti GM: Cytokine gene expression as a function of the clinical progression of Alzheimer disease dementia. Arch Neurol 2000, 57:1153-1160
43. Krupinski J, Kumar P, Kumar S, Kaluza J: Increased expression of TGF-β1 in brain tissue after ischemic stroke in humans. Stroke 1996, 27:852-857
44. Peterson MC: Circulating transforming growth factor β-1: a partial molecular explanation for associations between hypertension, diabetes, obesity, smoking and human disease involving fibrosis. Med Sci Monit 2005, 11:RA229-RA232
45. Kalaria RN: The role of cerebral ischemia in Alzheimer's disease. Neurobiol Aging 2000, 21:321-330
46. Luchsinger JA, Reitz C, Honig LS, Tang M-X, Shea S, Mayeux R: Aggregation of vascular risk factors and risk of incident Alzheimer disease. Neurology 2005, 65:545-551 (Pubitemid 41170713)
47. Lesné S, Docagne F, Gabriel C, Liot G, Lahiri DK, Buée L, Plawinski L, Delacourte A, MacKenzie ET, Buisson A, Vivien D: Transforming growth factor-β1 potentiates amyloid-β generation in astrocytes and in transgenic mice. J Biol Chem 2003, 278:18408-18418
48. Cheng JS, Dubal DB, Kim DH, Legleiter J, Cheng IH, Yu GQ, Tesseur I, Wyss-Coray T, Bonaldo P, Mucke L: Collagen VI protects neurons against Aβ toxicity. Nat Neurosci 2009, 12:119-121
49. Bennett SAL, Pappas BA, Stevens WD, Davidson CM, Fortin T, Chen J: Cleavage of amyloid precursor protein elicited by chronic cerebral hypoperfusion. Neurobiol Aging 2000, 21:207-214
50. Dhandapani KM, Brann DW: Transforming growth factor-β: a neuroprotective factor in cerebral ischemia. Cell Biochem Biophys 2003, 39:13-22
51. Geula C, Mesulam MM: Cortical cholinergic fibers in aging and Alzheimer's disease: a morphometric study. Neuroscience 1989, 33:469-481
52. Wong TP, Debeir T, Duff K, Cuello AC: Reorganization of cholinergic terminals in the cerebral cortex and hippocampus in transgenic mice carrying mutated presenilin-1 and amyloid precursor protein transgenes. J Neurosci 1999, 19:2706-2716
53. Jaffar S, Counts SE, Ma SY, Dadko E, Gordon MN, Morgan D, Mufson EJ: Neuropathology of mice carrying mutant APP(swe) and/or PS1 (M146L) transgenes: alterations in the p75(NTR) cholinergic basal forebrain septohippocampal pathway. Exp Neurol 2001, 170:227-243
54. Klingner M, Apelt J, Kumar A, Sorger D, Sabri O, Steinbach J, Scheunemann M, Schliebs R: Alterations in cholinergic and noncholinergic neurotransmitter receptor densities in transgenic Tg2576 mouse brain with beta-amyloid plaque pathology. Int J Dev Neurosci 2003, 21:357-369
55. Auld DS, Kornecook TJ, Bastianetto S, Quirion R: Alzheimer's disease and the basal forebrain cholinergic system: relations to beta-amyloid peptides, cognition, and treatment strategies. Prog Neurobiol 2002, 68:209-245
56. Hsia AY, Masliah E, McConlogue L, Yu GQ, Tatsuno G, Hu K, Kholodenko D, Malenka RC, Nicoll RA, Mucke L: Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci USA 1999, 96:3228-3233
57. Palop JJ, Jones B, Kekonius L, Chin J, Yu GQ, Raber J, Masliah E, Mucke L: Neuronal depletion of calcium-dependent proteins in the dentate gyrus is tightly linked to Alzheimer's disease-related cognitive deficits. Proc Natl Acad Sci USA 2003, 100:9572-9577
58. Caraci F, Battaglia G, Busceti C, Biagioni F, Mastroiacovo F, Bosco P, Drago F, Nicoletti F, Sortino MA, Copani A: TGF-β1 protects against Aβ-neurotoxicity via the phosphatidylinositol-3-kinase pathway. Neurobiol Dis 2008, 30:234-242
59. Tesseur I, Zou K, Esposito L, Bard F, Berber E, Can JV, Lin AH, Crews L, Tremblay P, Mathews P, Mucke L, Masliah E, Wyss-Coray T: Deficiency in neuronal TGF-beta signaling promotes neurodegeneration and Alzheimer's pathology. J Clin Invest 2006, 116:3060-3069
60. Salins P, He Y, Olson K, Glazner G, Kashour T, Amara F: TGF-beta1 is increased in a transgenic mouse model of familial Alzheimer's disease and causes neuronal apoptosis. Neurosci Lett 2008, 430:81-86
61. Tong XK, Hamel E: Transforming growth factor-beta 1 impairs endothelin-1-mediated contraction of brain vessels by inducing mitogenactivated protein (MAP) kinase phosphatase-1 and inhibiting p38 MAP kinase. Mol Pharmacol 2007, 72:1476-1483
62. Simpson IA, Chundu KR, Davies-Hill T, Honer WG, Davies P: Decreased concentrations of GLUT1 and GLUT3 glucose transporters in the brains of patients with Alzheimer's disease. Ann Neurol 1994, 35:546-551 (Pubitemid 24153837)