Behavioral and neuropathological consequences of transient global ischemia in APP/PS1 Alzheimer model mice

Behavioural Brain Research

Volumn 275, Issue , 2014, Pages 15-26

  Kemppainen, S ^a   Hamalainen E ^a   Miettinen, P O ^a   Koistinaho, J ^a   Tanila, H ^a,b  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b KUOPIO UNIVERSITY HOSPITAL   (Finland)

Author keywords

Alzheimer's disease; Amyloid; Cerebrovascular disease; Hypotension; Memory; Neuroinflammation; Transgenic mice

Indexed keywords

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTROCYTE; BEHAVIOR DISORDER; BODY EQUILIBRIUM; BRAIN CIRCULATION; CELL ACTIVATION; CELL LOSS; CELL SURVIVAL; CONTROLLED STUDY; DISEASE SEVERITY; GENOTYPE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; ISCHEMIA; LEARNING DISORDER; LONG TERM MEMORY; MALE; MEMORY DISORDER; MICROGLIA; MOTOR COORDINATION; MOUSE; NERVE CELL; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NONHUMAN; PYRAMIDAL NERVE CELL; SPATIAL MEMORY; TRANSIENT GLOBAL ISCHEMIA; WORKING MEMORY; ANIMAL; BRAIN; COMPLICATION; DISEASE MODEL; EXPLORATORY BEHAVIOR; GENETICS; HUMAN; INSTRUMENTAL CONDITIONING; MAZE TEST; MENTAL DISORDERS; METABOLISM; MOTOR ACTIVITY; PATHOLOGY; PHYSIOLOGY; PSYCHOLOGY; REACTION TIME; SHORT TERM MEMORY; SWIMMING; TRANSGENIC MOUSE; TRANSIENT ISCHEMIC ATTACK;

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; PRESENILIN 1; PSEN1 PROTEIN, HUMAN;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; CONDITIONING, OPERANT; DISEASE MODELS, ANIMAL; EXPLORATORY BEHAVIOR; HUMANS; ISCHEMIC ATTACK, TRANSIENT; MALE; MAZE LEARNING; MEMORY, SHORT-TERM; MENTAL DISORDERS; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; NEURONS; PRESENILIN-1; REACTION TIME; SWIMMING;

EID: 84907174390     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2014.08.050     Document Type: Article

References (43)

1. Kalaria R.N. The role of cerebral ischemia in Alzheimer's disease. Neurobiol Aging 2000, 21:321-330.
2. de la Torre J.C. Cerebral hemodynamics and vascular risk factors: setting the stage for Alzheimer's disease. J Alzheimer's Dis 2012, 32:553-567.
3. Nagy Z., Esiri M.M., Jobst K.A., Morris J.H., King E.M., McDonald B., et al. The effects of additional pathology on the cognitive deficit in Alzheimer disease. J Neuropathol Exp Neurol 1997, 56:165-170.
4. Snowdon D.A., Greiner L.H., Mortimer J.A., Riley K.P., Greiner P.A., Markesbery W.R. Brain infarction and the clinical expression of Alzheimer disease. The Nun study. Jr Am Med Assoc 1997, 277:813-817.
5. Kalaria R.N., Akinyemi R., Ihara M. Does vascular pathology contribute to Alzheimer changes. J Neurol Sci 2012, 322:141-147.
6. van der Flier W.M., van Straaten E.C., Barkhof F., Ferro J.M., Pantoni L., Basile A.M., et al. Medial temporal lobe atrophy and white matter hyperintensities are associated with mild cognitive deficits in non-disabled elderly people: the LADIS study. J Neurol Neurosurg Psychiatry 2005, 76:1497-1500.
7. Stephan B.C., Matthews F.E., Ma B., Muniz G., Hunter S., Davis D., et al. Alzheimer and vascular neuropathological changes associated with different cognitive states in a non-demented sample. J Alzheimer's Dis 2012, 29:309-318.
8. Nagy Z., Esiri M.M., Jobst K.A., Morris J.H., King E.M., McDonald B., et al. Relative roles of plaques and tangles in the dementia of Alzheimer's disease: correlations using three sets of neuropathological criteria. Dementia 1995, 6:21-31.
9. Nelson P.T., Alafuzoff I., Bigio E.H., Bouras C., Braak H., Cairns N.J., et al. Correlation of Alzheimer disease neuropathologic changes with cognitive status: a review of the literature. J Neuropathol Exp Neurol 2012, 71:362-381.
10. Johnson K.A., Jones K., Holman B.L., Becker J.A., Spiers P.A., Satlin A., et al. Preclinical prediction of Alzheimer's disease using SPECT. Neurology 1998, 50:1563-1571.
11. 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.
12. Koistinaho M., Kettunen M.I., Goldsteins G., Keinanen R., Salminen A., Ort M., et al. 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.
13. Heikkinen R., Malm T., Heikkila¨ J., Muona A., Tanila H., Koistinaho M., et al. Susceptibility to focal and global brain ischemia of Alzheimer mice displaying abeta deposits: effect of immunoglobulin. Aging Dis 2014, 5:76-87.
14. Yamada M., Ihara M., Okamoto Y., Maki T., Washida K., Kitamura A., et al. The influence of chronic cerebral hypoperfusion on cognitive function and amyloid beta metabolism in APP overexpressing mice. PLoS ONE 2011, 6:e16567. 10.1371/journal.pone.0016567.
15. Pimentel-Coelho P.M., Michaud J.P., Rivest S. Effects of mild chronic cerebral hypoperfusion and early amyloid pathology on spatial learning and the cellular innate immune response in mice. Neurobiol Aging 2013, 34:679-693.
16. Li L., Zhang X., Yang D., Luo G., Chen S., Le W. Hypoxia increases Abeta generation by altering beta- and gamma-cleavage of APP. Neurobiol Aging 2009, 30:1091-1098.
17. Koike M.A., Green K.N., Blurton-Jones M., Laferla F.M. Oligemic hypoperfusion differentially affects tau and amyloid-{beta}. Am J Pathol 2010, 177:300-310.
18. Velliquette R.A., O'Connor T., Vassar R. Energy inhibition elevates beta-secretase levels and activity and is potentially amyloidogenic in APP transgenic mice: possible early events in Alzheimer's disease pathogenesis. J Neurosci 2005, 25:10874-10883.
19. Garcia-Alloza M., Gregory J., Kuchibhotla K.V., Fine S., Wei Y., Ayata C., et al. Cerebrovascular lesions induce transient beta-amyloid deposition. Brain 2011, 134:3697-3707.
20. Van Nostrand W.E., Davis J., Previti M.L., Xu F. Clearance of amyloid-beta protein deposits in transgenic mice following focal cerebral ischemia. Neurodegener Dis 2012, 10:108-111.
21. Niwa K., Carlson G.A., Iadecola C. Exogenous A beta1-40 reproduces cerebrovascular alterations resulting from amyloid precursor protein overexpression in mice. J Cereb Blood Flow Metab 2000, 20:1659-1668.
22. Zerbi V., Jansen D., Dederen P.J., Veltien A., Hamans B., Liu Y., et al. Microvascular cerebral blood volume changes in aging APP(swe)/PS1(dE9) AD mouse model: a voxel-wise approach. Brain Struct Funct 2013, 218:1085-1098.
23. Smith M.L., Bendek G., Dahlgren N., Rosen I., Wieloch T., Siesjo B.K. Models for studying long-term recovery following forebrain ischemia in the rat. A 2-vessel occlusion model. Acta Neurol Scand 1984, 69:385-401.
24. Gionet T.X., Thomas J.D., Warner D.S., Goodlett C.R., Wasserman E.A., West J.R. Forebrain ischemia induces selective behavioral impairments associated with hippocampal injury in rats. Stroke 1991, 22:1040-1047.
25. Garcia-Alloza M., Robbins E.M., Zhang-Nunes S.X., Purcell S.M., Betensky R.A., Raju S., et al. Characterization of amyloid deposition in the APPswe/PS1dE9 mouse model of Alzheimer disease. Neurobiol Dis 2006, 24:516-524.
26. Minkeviciene R., Ihalainen J., Malm T., Matilainen O., Keksa-Goldsteine V., Goldsteins G., et al. Age-related decrease in stimulated glutamate release and vesicular glutamate transporters in APP/PS1 transgenic and wild-type mice. J Neurochem 2008, 105:584-594.
27. Minkeviciene R., Rheims S., Dobszay M.B., Zilberter M., Hartikainen J., Fulop L., et al. Amyloid beta-induced neuronal hyperexcitability triggers progressive epilepsy. J Neurosci 2009, 29:3453-3462.
28. Gurevicius K., Lipponen A., Tanila H. Increased cortical and thalamic excitability in freely moving APPswe/PS1dE9 mice modeling epileptic activity associated with Alzheimer's disease. Cereb Cortex 2013, 23:1148-1158.
29. Ghosh D., LeVault K.R., Barnett A.J., Brewer G.J. A reversible early oxidized redox state that precedes macromolecular ROS damage in aging nontransgenic and 3xTg-AD mouse neurons. J Neurosci 2012, 32:5821-5832.
30. Jankowsky J.L., Fadale D.J., Anderson J., Xu G.M., Gonzales V., Jenkins N.A., et al. Mutant presenilins specifically elevate the levels of the 42 residue beta-amyloid peptide in vivo: evidence for augmentation of a 42-specific gamma secretase. Hum Mol Genet 2004, 13:159-170.
31. Yang G., Kitagawa K., Matsushita K., Mabuchi T., Yagita Y., Yanagihara T., et al. C57BL/6 strain is most susceptible to cerebral ischemia following bilateral common carotid occlusion among seven mouse strains: selective neuronal death in the murine transient forebrain ischemia. Brain Res 1997, 752:209-218.
32. Sheng H., Laskowitz D.T., Pearlstein R.D., Warner D.S. Characterization of a recovery global cerebral ischemia model in the mouse. J Neurosci Methods 1999, 88:103-109.
33. Tsien J.Z., Huerta P.T., Tonegawa S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 1996, 87:1327-1338.
34. Nakazawa K., Quirk M.C., Chitwood R.A., Watanabe M., Yeckel M.F., Sun L.D., et al. Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 2002, 297:211-218.
35. Dias R., Aggleton J.P. Effects of selective excitotoxic prefrontal lesions on acquisition of nonmatching- and matching-to-place in the T-maze in the rat: differential involvement of the prelimbic-infralimbic and anterior cingulate cortices in providing behavioural flexibility. Eur J Neurosci 2000, 12:4457-4466.
36. Coutureau E., Galani R., Jarrard L.E., Cassel J.C. Selective lesions of the entorhinal cortex, the hippocampus, or the fimbria-fornix in rats: a comparison of effects on spontaneous and amphetamine-induced locomotion. Exp Brain Res 2000, 131:381-392.
37. Bannerman D.M., Gilmour G., Norman G., Lemaire M., Iversen S.D., Rawlins J.N. The time course of the hyperactivity that follows lesions or temporary inactivation of the fimbria-fornix. Behav Brain Res 2001, 120:1-11.
38. Candelario-Jalil E., Mhadu N.H., Al-Dalain S.M., Martinez G., Leon O.S. Time course of oxidative damage in different brain regions following transient cerebral ischemia in gerbils. Neurosci Res 2001, 41:233-241.
39. Pagani L., Eckert A. Amyloid-beta interaction with mitochondria. Int J Alzheimer's Dis 2011, 925050. 10.4061/2011/925050.
40. Yao J., Irwin R.W., Zhao L., Nilsen J., Hamilton R.T., Brinton R.D. Mitochondrial bioenergetic deficit precedes Alzheimer's pathology in female mouse model of Alzheimer's disease. Proc Natl Acad Sci U S A 2009, 106:14670-14675.
41. Puli L., Pomeshchik Y., Olas K., Malm T., Koistinaho J., Tanila H. Effects of human intravenous immunoglobulin on amyloid pathology and neuroinflammation in a mouse model of Alzheimer's disease. J Neuroinflam 2012, 9. 105-2094-9-105 http://dx.doi.org/10.1186/1742-2094-9-105.
42. Hsiao K., Chapman P., Nilsen S., Eckman C., Harigaya Y., Younkin S., et al. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 1996, 274:99-102.
43. Love S., Miners S., Palmer J., Chalmers K., Kehoe P. Insights into the pathogenesis and pathogenicity of cerebral amyloid angiopathy. Front Biosci 2009, 14:4778-4792.