Effects of mild chronic cerebral hypoperfusion and early amyloid pathology on spatial learning and the cellular innate immune response in mice

Neurobiology of Aging

Volumn 34, Issue 3, 2013, Pages 679-693

  Pimentel Coelho, Pedro M ^a   Michaud, Jean Philippe ^a   Rivest, Serge ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

Alzheimer's disease; Cerebral blood flow; Cerebral ischemia; Cerebrovascular disease; Chronic cerebral hypoperfusion; Oligoemia; Vascular dysfunction; Vascular risk factors

Indexed keywords

AMYLOID;

ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD; BONE MARROW; BRAIN BLOOD FLOW; BRAIN PERFUSION; CAROTID ARTERY OBSTRUCTION; CELL COUNT; CELL MOTILITY; CELLULAR IMMUNITY; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; DISEASE SEVERITY; INNATE IMMUNITY; LEARNING; LEARNING DISORDER; MALE; MICROGLIA; MONOCYTE; MOUSE; NERVE CELL NECROSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SPATIAL LEARNING;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN ISCHEMIA; CEREBRAL CORTEX; CEREBROVASCULAR CIRCULATION; DISEASE MODELS, ANIMAL; GENE-ENVIRONMENT INTERACTION; GENETIC PREDISPOSITION TO DISEASE; IMMUNITY, CELLULAR; IMMUNITY, INNATE; MALE; MICE; MICE, TRANSGENIC; MICROGLIA; MONOCYTES; PLAQUE, AMYLOID;

EID: 84870493605     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2012.06.025     Document Type: Article

References (59)

1. Adhami F., Liao G., Morozov Y.M., Schloemer A., Schmithorst V.J., Lorenz J.N., Dunn R.S., Vorhees C.V., Wills-Karp M., Degen J.L., Davis R.J., Mizushima N., Rakic P., Dardzinski B.J., Holland S.K., Sharp F.R., Kuan C.Y. Cerebral ischemia-hypoxia induces intravascular coagulation and autophagy. Am. J. Pathol 2006, 169:566-583.
2. Aliev G., Palacios H.H., Walrafen B., Lipsitt A.E., Obrenovich M.E., Morales L. Brain mitochondria as a primary target in the development of treatment strategies for Alzheimer disease. Int. J. Biochem. Cell Biol 2009, 41:1989-2004.
3. Arnold L., Henry A., Poron F., Baba-Amer Y., van Rooijen N., Plonquet A., Gherardi R.K., Chazaud B. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med 2007, 204:1057-1069.
4. Barnes D.E., Yaffe K. The projected effect of risk factor reduction on Alzheimer's disease prevalence. Lancet Neurol 2011, 10:819-828.
5. Beach T.G., Wilson J.R., Sue L.I., Newell A., Poston M., Cisneros R., Pandya Y., Esh C., Connor D.J., Sabbagh M., Walker D.G., Roher A.E. Circle of Willis atherosclerosis: association with Alzheimer's disease, neuritic plaques and neurofibrillary tangles. Acta Neuropathol 2007, 113:13-21.
6. Borroni B., Anchisi D., Paghera B., Vicini B., Kerrouche N., Garibotto V., Terzi A., Vignolo L.A., Di Luca M., Giubbini R., Padovani A., Perani D. Combined 99mTc-ECD SPECT and neuropsychological studies in MCI for the assessment of conversion to AD. Neurobiol. Aging 2006, 27:24-31.
7. Chapman G.A., Moores K., Harrison D., Campbell C.A., Stewart B.R., Strijbos P.J. Fractalkine cleavage from neuronal membranes represents an acute event in the inflammatory response to excitotoxic brain damage. J. Neurosci 2000, 20:RC87.
8. de la Torre J.C. A turning point for Alzheimer's disease?. Biofactors 2012, 38:78-83.
9. Deane R., Du Yan S., Submamaryan R.K., LaRue B., Jovanovic S., Hogg E., Welch D., Manness L., Lin C., Yu J., Zhu H., Ghiso J., Frangione B., Stern A., Schmidt A.M., Armstrong D.L., Arnold B., Liliensiek B., Nawroth P., Hofman F., Kindy M., Stern D., Zlokovic B. RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain. Nat. Med 2003, 9:907-913.
10. Dubois B., Feldman H.H., Jacova C., Cummings J.L., Dekosky S.T., Barberger-Gateau P., Delacourte A., Frisoni G., Fox N.C., Galasko D., Gauthier S., Hampel H., Jicha G.A., Meguro K., O'Brien J., Pasquier F., Robert P., Rossor M., Salloway S., Sarazin M., de Souza L.C., Stern Y., Visser P.J., Scheltens P. Revising the definition of Alzheimer's disease: a new lexicon. Lancet Neurol 2010, 9:1118-1127.
11. El Khoury J., Toft M., Hickman S.E., Means T.K., Terada K., Geula C., Luster A.D. Ccr2 deficiency impairs microglial accumulation and accelerates progression of Alzheimer-like disease. Nat. Med 2007, 13:432-438.
12. Encinas M., De Juan R., Marcos A., Gil P., Barabash A., Fernández C., De Ugarte C., Cabranes J.A. Regional cerebral blood flow assessed with 99mTc-ECD SPET as a marker of progression of mild cognitive impairment to Alzheimer's disease. Eur. J. Nucl. Med. Mol. Imaging 2003, 30:1473-1480.
13. Ferreira S.T., Klein W.L. The Aβ oligomer hypothesis for synapse failure and memory loss in Alzheimer's disease. Neurobiol. Learn. Mem 2011, 96:529-543.
14. Filali M., Lalonde R., Rivest S. Cognitive and non-cognitive behaviors in an APPswe/PS1 bigenic model of Alzheimer's disease. Genes Brain Behav 2009, 8:143-148.
15. Ginsberg M.D. Adventures in the pathophysiology of brain ischemia: penumbra, gene expression, neuroprotection: the 2002 Thomas Willis Lecture. Stroke 2003, 34:214-223.
16. Grammas P. Neurovascular dysfunction, inflammation and endothelial activation: implications for the pathogenesis of Alzheimer's disease. J. Neuroinflammation 2011, 8:26.
17. Guo W., Allan A.M., Zong R., Zhang L., Johnson E.B., Schaller E.G., Murthy A.C., Goggin S.L., Eisch A.J., Oostra B.A., Nelson D.L., Jin P., Zhao X. Ablation of Fmrp in adult neural stem cells disrupts hippocampus-dependent learning. Nat. Med 2011, 17:559-565.
18. Habert M.O., Horn J.F., Sarazin M., Lotterie J.A., Puel M., Onen F., Zanca M., Portet F., Touchon J., Verny M., Mahieux F., Giron A., Fertil B., Dubois B. Brain perfusion SPECT with an automated quantitative tool can identify prodromal Alzheimer's disease among patients with mild cognitive impairment. Neurobiol. Aging 2011, 32:15-23.
19. Harrison J.K., Jiang Y., Chen S., Xia Y., Maciejewski D., McNamara R.K., Streit W.J., Salafranca M.N., Adhikari S., Thompson D.A., Botti P., Bacon K.B., Feng L. Role for neuronally derived fractalkine in mediating interactions between neurons and CX3CR1-expressing microglia. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:10896-10901.
20. Hirao K., Ohnishi T., Hirata Y., Yamashita F., Mori T., Moriguchi Y., Matsuda H., Nemoto K., Imabayashi E., Yamada M., Iwamoto T., Arima K., Asada T. The prediction of rapid conversion to Alzheimer's disease in mild cognitive impairment using regional cerebral blood flow SPECT. NeuroImage 2005, 28:1014-1021.
21. Hofman A., Ott A., Breteler M.M., Bots M.L., Slooter A.J., van Harskamp F., van Duijn C.N., Van Broeckhoven C., Grobbee D.E. Atherosclerosis, apolipoprotein E, and prevalence of dementia and Alzheimer's disease in the Rotterdam Study. Lancet 1997, 349:151-154.
22. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., Yang F., Cole G. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996, 274:99-102.
23. Iadecola C. The overlap between neurodegenerative and vascular factors in the pathogenesis of dementia. Acta Neuropathol 2010, 120:287-296.
24. Johnson K.A., Lopera F., Jones K., Becker A., Sperling R., Hilson J., Londono J., Siegert I., Arcos M., Moreno S., Madrigal L., Ossa J., Pineda N., Ardila A., Roselli M., Albert M.S., Kosik K.S., Rios A. Presenilin-1-associated abnormalities in regional cerebral perfusion. Neurology 2001, 56:1545-1551.
25. Kalaria R.N. Vascular basis for brain degeneration: faltering controls and risk factors for dementia. Nutr. Rev 2010, 68(suppl 2):S74-S87.
26. Kapogiannis D., Mattson M.P. Disrupted energy metabolism and neuronal circuit dysfunction in cognitive impairment and Alzheimer's disease. Lancet Neurol 2011, 10:187-198.
27. Kitagawa K., Yagita Y., Sasaki T., Sugiura S., Omura-Matsuoka E., Mabuchi T., Matsushita K., Hori M. Chronic mild reduction of cerebral perfusion pressure induces ischemic tolerance in focal cerebral ischemia. Stroke 2005, 36:2270-2274.
28. Kitamura A., Fujita Y., Oishi N., Kalaria R.N., Washida K., Maki T., Okamoto Y., Hase Y., Yamada M., Takahashi J., Ito H., Tomimoto H., Fukuyama H., Takahashi R., Ihara M. Selective white matter abnormalities in a novel rat model of vascular dementia. Neurobiol. Aging 2012, 33:e25-e35.
29. Koistinaho M., Kettunen M.I., Goldsteins G., Keinänen R., Salminen A., Ort M., Bures J., Liu D., Kauppinen R.A., Higgins L.S., Koistinaho J. Beta-amyloid precursor protein transgenic mice that harbor diffuse A beta deposits but do not form plaques show increased ischemic vulnerability: role of inflammation. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:1610-1615.
30. Laflamme N., Rivest S. Toll-like receptor 4: the missing link of the cerebral innate immune response triggered by circulating gram-negative bacterial cell wall components. FASEB J 2001, 15:155-163.
31. Lebson L., Nash K., Kamath S., Herber D., Carty N., Lee D.C., Li Q., Szekeres K., Jinwal U., Koren J., Dickey C.A., Gottschall P.E., Morgan D., Gordon M.N. Trafficking CD11b-positive blood cells deliver therapeutic genes to the brain of amyloid-depositing transgenic mice. J. Neurosci 2010, 30:9651-9658.
32. Lee J.S., Im D.S., An Y.S., Hong J.M., Gwag B.J., Joo I.S. Chronic cerebral hypoperfusion in a mouse model of Alzheimer's disease: an additional contributing factor of cognitive impairment. Neurosci. Lett 2011, 489:84-88.
33. Luckhaus C., Flüb M.O., Wittsack H.J., Grass-Kapanke B., Jänner M., Khalili-Amiri R., Friedrich W., Supprian T., Gaebel W., Mödder U., Cohnen M. Detection of changed regional cerebral blood flow in mild cognitive impairment and early Alzheimer's dementia by perfusion-weighted magnetic resonance imaging. NeuroImage 2008, 40:495-503.
34. Michaud J.P., Richard K.L., Rivest S. MyD88-adaptor protein acts as a preventive mechanism for memory deficits in a mouse model of Alzheimer's disease. Mol. Neurodegener 2011, 6:5.
35. Mildner A., Schlevogt B., Kierdorf K., Böttcher C., Erny D., Kummer M.P., Quinn M., Brück W., Bechmann I., Heneka M.T., Priller J., Prinz M. Distinct and non-redundant roles of microglia and myeloid subsets in mouse models of Alzheimer's disease. J. Neurosci 2011, 31:11159-11171.
36. Naert G., Rivest S. CC chemokine receptor 2 deficiency aggravates cognitive impairments and amyloid pathology in a transgenic mouse model of Alzheimer's disease. J. Neurosci 2011, 31:6208-6220.
37. Naert G., Rivest S. Hematopoietic CC-chemokine receptor 2-(CCR2) competent cells are protective for the cognitive impairments and amyloid pathology in a transgenic mouse model of Alzheimer's disease. Mol. Med 2012, 18:297-313.
38. Plaschke K., Staub J., Ernst E., Marti H.H. VEGF overexpression improves mice cognitive abilities after unilateral common carotid artery occlusion. Exp. Neurol 2008, 214:285-292.
39. Reimer M.M., McQueen J., Searcy L., Scullion G., Zonta B., Desmazieres A., Holland P.R., Smith J., Gliddon C., Wood E.R., Herzyk P., Brophy P.J., McCulloch J., Horsburgh K. Rapid disruption of axon-glial integrity in response to mild cerebral hypoperfusion. J. Neurosci 2011, 31:18185-18194.
40. Roher A.E., Esh C., Kokjohn T.A., Kalback W., Luehrs D.C., Seward J.D., Sue L.I., Beach T.G. Circle of willis atherosclerosis is a risk factor for sporadic Alzheimer's disease. Arterioscler. Thromb. Vasc. Biol 2003, 23:2055-2062.
41. Roher A.E., Tyas S.L., Maarouf C.L., Daugs I.D., Kokjohn T.A., Emmerling M.R., Garami Z., Belohlavek M., Sabbagh M.N., Sue L.I., Beach T.G. Intracranial atherosclerosis as a contributing factor to Alzheimer's disease dementia. Alzheimers Dement 2011, 7:436-444.
42. Ruitenberg A., den Heijer T., Bakker S.L., van Swieten J.C., Koudstaal P.J., Hofman A., Breteler M.M. Cerebral hypoperfusion and clinical onset of dementia: the Rotterdam Study. Ann. Neurol 2005, 57:789-794.
43. Seshadri S., Wolf P.A. Lifetime risk of stroke and dementia: current concepts, and estimates from the Framingham Study. Lancet Neurol 2007, 6:1106-1114.
44. Silvestrini M., Gobbi B., Pasqualetti P., Bartolini M., Baruffaldi R., Lanciotti C., Cerqua R., Altamura C., Provinciali L., Vernieri F. Carotid atherosclerosis and cognitive decline in patients with Alzheimer's disease. Neurobiol. Aging 2009, 30:1177-1183.
45. Silvestrini M., Paolino I., Vernieri F., Pedone C., Baruffaldi R., Gobbi B., Cagnetti C., Provinciali L., Bartolini M. Cerebral hemodynamics and cognitive performance in patients with asymptomatic carotid stenosis. Neurology 2009, 72:1062-1068.
46. Silvestrini M., Viticchi G., Falsetti L., Balucani C., Vernieri F., Cerqua R., Luzzi S., Bartolini M., Provinciali L. The role of carotid atherosclerosis in Alzheimer's disease progression. J. Alzheimers Dis 2011, 25:719-726.
47. Simard A.R., Rivest S. Bone marrow stem cells have the ability to populate the entire central nervous system into fully differentiated parenchymal microglia. FASEB J 2004, 18:998-1000.
48. Simard A.R., Soulet D., Gowing G., Julien J.P., Rivest S. Bone marrow-derived microglia play a critical role in restricting senile plaque formation in Alzheimer's disease. Neuron 2006, 49:489-502.
49. Sojkova J., Beason-Held L., Zhou Y., An Y., Kraut M.A., Ye W., Ferrucci L., Mathis C.A., Klunk W.E., Wong D.F., Resnick S.M. Longitudinal cerebral blood flow and amyloid deposition: an emerging pattern?. J. Nucl. Med 2008, 49:1465-1471.
50. Soulet D., Rivest S. Bone-marrow-derived microglia: myth or reality?. Curr. Opin. Pharmacol 2008, 8:508-518.
51. Stalder A.K., Ermini F., Bondolfi L., Krenger W., Burbach G.J., Deller T., Coomaraswamy J., Staufenbiel M., Landmann R., Jucker M. Invasion of hematopoietic cells into the brain of amyloid precursor protein transgenic mice. J. Neurosci 2005, 25:11125-11132.
52. Thambisetty M., Beason-Held L., An Y., Kraut M.A., Resnick S.M. APOE epsilon4 genotype and longitudinal changes in cerebral blood flow in normal aging. Arch. Neurol 2010, 67:93-98.
53. Town T., Laouar Y., Pittenger C., Mori T., Szekely C.A., Tan J., Duman R.S., Flavell R.A. Blocking TGF-beta-Smad2/3 innate immune signaling mitigates Alzheimer-like pathology. Nat. Med 2008, 14:681-687.
54. Turrin N.P., Rivest S. Tumor necrosis factor alpha but not interleukin 1 beta mediates neuroprotection in response to acute nitric oxide excitotoxicity. J. Neurosci 2006, 26:143-151.
55. Urra X., Cervera A., Obach V., Climent N., Planas A.M., Chamorro A. Monocytes are major players in the prognosis and risk of infection after acute stroke. Stroke 2009, 40:1262-1268.
56. Woollard K.J., Geissmann F. Monocytes in atherosclerosis: subsets and functions. Nat. Rev. Cardiol 2010, 7:77-86.
57. Yamada M., Ihara M., Okamoto Y., Maki T., Washida K., Kitamura A., Hase Y., Ito H., Takao K., Miyakawa T., Kalaria R.N., Tomimoto H., Takahashi R. The influence of chronic cerebral hypoperfusion on cognitive function and amyloid β metabolism in APP overexpressing mice. PLoS One 2011, 6:e16567.
58. Yoshizaki K., Adachi K., Kataoka S., Watanabe A., Tabira T., Takahashi K., Wakita H. Chronic cerebral hypoperfusion induced by right unilateral common carotid artery occlusion causes delayed white matter lesions and cognitive impairment in adult mice. Exp. Neurol 2008, 210:585-591.
59. Zhang F., Eckman C., Younkin S., Hsiao K.K., Iadecola C. Increased susceptibility to ischemic brain damage in transgenic mice overexpressing the amyloid precursor protein. J. Neurosci 1997, 17:7655-7661.