Prolonged Running, not Fluoxetine Treatment, Increases Neurogenesis, but does not Alter Neuropathology, in the 3xTg Mouse Model of Alzheimer’s Disease (original) (raw)
Andorfer C, Acker CM, Kress Y, Hof PR, Duff K, Davies P (2005) Cell cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms. J Neurosci 25(22):5446–5454 ArticlePubMedCAS Google Scholar
Bayer TA, Wirths O (2010) Intracellular accumulation of amyloid-Beta—a predictor for synaptic dysfunction and neuron loss in Alzheimer’s disease. Front Aging Neurosci 2:8 PubMedCAS Google Scholar
Billings LM, Oddo S, Green KN, McGaugh JL, LaFerla FM (2005) Intraneuronal Abeta causes the onset of early Alzheimer’s disease-related cognitive deficits in transgenic mice. Neuron 45(5):675–688 Google Scholar
Boekhoorn K, Joels M, Lucassen PJ (2006a) Increased proliferation reflects glial and vascular-associated changes, but not neurogenesis in the presenile Alzheimer hippocampus. Neurobiol Dis 24(1):1–14 Google Scholar
Boekhoorn K, Terwel D, Biemans B, Borghgraef P, Wiegert O et al (2006b) Improved long-term potentiation and memory in young tau-P301L transgenic mice before onset of hyperphosphorylation and tauopathy. J Neurosci 26(13):3514–3523 ArticlePubMedCAS Google Scholar
Boldrini M, Underwood MD, Hen R, Rosoklija GB, Dwork AJ, Mann JJ, Arango V (2009) Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology 34(11):2376–2389 Google Scholar
Brocco M, Dekeyne A, Veiga S, Girardon S, Millan MJ (2002) Induction of hyperlocomotion in mice exposed to a novel environment by inhibition of serotonin reuptake. A pharmacological characterization of diverse classes of antidepressant agents. Pharmacol biochem behav 71(4):667–680 Google Scholar
Brown J, Cooper-Kuhn CM, Kempermann G, van Praag H, Winkler J, Gage FH et al (2003) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 17(10):2042–2046 ArticlePubMed Google Scholar
Cai Y, Zhang X-M, Macklin LN, Cai H, Luo X-G, Oddo S et al (2012) BACE1 elevation is involved in amyloid plaque development in the triple transgenic model of Alzheimer’s disease: differential Aβ antibody labeling of early-onset axon terminal pathology. Neurotox Res 21(2):160–174 ArticlePubMed Google Scholar
Chadwick W, Mitchell N, Caroll J, Zhou Y, Park S-S, Wang L et al (2011) Amitriptyline-mediated cognitive enhancement in aged 3xTg Alzheimer’s disease mice is associated with neurogenesis and neurotrophic activity. PLoS One 6(6):e21660 ArticlePubMedCAS Google Scholar
Christensen DZ, Bayer TA, Wirths O (2009) Formic acid is essential for immunohistochemical detection of aggregated intraneuronal Abeta peptides in mouse models of Alzheimer’s disease. Brain Res 1301:116–125 Google Scholar
Christensen DZ, Schneider-Axmann T, Lucassen PJ, Bayer TA, Wirths O (2010) Accumulation of intraneuronal Abeta correlates with ApoE4 genotype. Acta Neuropathol 119(5):555–566 ArticlePubMedCAS Google Scholar
Clinton LK, Billings LM, Green KN, Caccamo A, Ngo J, Oddo S et al (2007) Age-dependent sexual dimorphism in cognition and stress response in the 3xTg-AD mice. Neurobiol Dis 28(1):76–82 ArticlePubMedCAS Google Scholar
Couillard-Despres S et al (2009). Ageing abolishes the effects of fluoxetine on Neurogenesis. Mol Psychiatry 14:856–864 Google Scholar
Ermini FV, Grathwohl S, Radde R, Yamaguchi M, Staufenbiel M, Palmer TD et al (2008) Neurogenesis and alterations of neural stem cells in mouse models of cerebral amyloidosis. Am J Pathol 172(6):1520–1528 ArticlePubMedCAS Google Scholar
Fuster-Matanzo A, Llorens-Martín M, Jurado-Arjona J, Avila J, Hernández F (2012) Tau protein and adult hippocampal neurogenesis. Front Neurosci 6:104 ArticlePubMedCAS Google Scholar
Gan L, Qiao S, Lan X, Chi L, Luo C, Lien L et al (2008) Neurogenic responses to amyloid-beta plaques in the brain of Alzheimer’s disease like transgenic (pPDGF-APPSw, Ind) mice. Neurobiol Dis 29(1):71–80 ArticlePubMedCAS Google Scholar
García-Mesa Y, López-Ramos JC, Giménez-Llort L, Revilla S, Guerra R, Gruart A et al (2011) Physical exercise protects against Alzheimer’s disease in 3xTg-AD mice. J Alzheimers Dis 24(3):421–454 PubMed Google Scholar
Goedert M, Spillantini MG, Cairns NJ, Crowther RA (1992) Tau proteins of Alzheimer paired helical filaments: abnormal phosphorylation of all six brain isoforms. Neuron 8(1):159–168 ArticlePubMedCAS Google Scholar
Goedert M, Jakes R, Vanmechelen E (1995) Monoclonal antibody AT8 recognises tau protein phosphorylated at both serine 202 and threonine 205. Neurosci lett 189(3):167–169 Google Scholar
Götz J, Ittner LM (2008) Animal models of Alzheimer’s disease and frontotemporal dementia. Nat Rev Neurosci 9(7):532–544 ArticlePubMed Google Scholar
Gouras GK, Tsai J, Naslund J, Vincent B, Edgar M, Checler F et al (2000) Intraneuronal Abeta42 accumulation in human brain. Am J Pathol 156(1):15–20 ArticlePubMedCAS Google Scholar
Gouras GK, Tampellini D, Takahashi RH, Capetillo-Zarate E (2010) Intraneuronal beta-amyloid accumulation and synapse pathology in Alzheimer’s disease. Acta Neuropathol 119(5):523–541 ArticlePubMedCAS Google Scholar
Kayed R, Head E, Sarsoza F, Saing T, Cotman CW, Necula M et al (2007) Fibril specific, conformation dependent antibodies recognize a generic epitope common to amyloid fibrils and fibrillar oligomers that is absent in prefibrillar oligomers. Mol Neurodegener 2:18 ArticlePubMed Google Scholar
Kempermann G (2008) The neurogenic reserve hypothesis: what is adult hippocampal neurogenesis good for? Trends Neurosci 31(4):163–169 ArticlePubMedCAS Google Scholar
Kempermann G, Fabel K, Ehninger D, Babu H, Leal-Galicia P, Garthe A et al (2010) Why and how physical activity promotes experience-induced brain plasticity. Front Neurosci. 4:189 ArticlePubMed Google Scholar
Kuhn HG, Cooper-Kuhn CM, Boekhoorn K, Lucassen PJ (2007) Changes in neurogenesis in dementia and Alzheimer mouse models: are they functionally relevant? Eur Arch Psychiatry Clin Neurosci 257(5):281–289 ArticlePubMed Google Scholar
Lee VM, Goedert M, Trojanowski JQ (2001) Neurodegenerative tauopathies. Annu Rev Neurosci 24:1121–1159 ArticlePubMedCAS Google Scholar
Li B, Yamamori H, Tatebayashi Y, Shafit-Zagardo B, Tanimukai H, Chen S, Iqbal K, Grundke-Iqbal I (2008) Failure of neuronal maturation in Alzheimer disease dentate gyrus. J Neuropathol Exp Neurol 67(1):78–84 ArticlePubMedCAS Google Scholar
Llorens-Martin M, Teixeira CM, Fuster-Matanzo A, Jurado-Arjona J, Borrell V, Soriano E, Avila J, Hernández F (2012) Tau isoform with three microtubule binding domains is a marker of new axons generated from the subgranular zone in the hippocampal dentate gyrus: implications for Alzheimer’s disease. J Alzheimers Dis 29(4):921–930 PubMedCAS Google Scholar
Lucassen PJ, Meerlo P, Naylor AS, van Dam AM, Dayer AG, Fuchs E, Oomen CA, Czéh B (2010) Regulation of adult neurogenesis by stress, sleep disruption, exercise and inflammation: implications for depression and antidepressant action. Eur Neuropsychopharmacol 20(1):1–17 ArticlePubMedCAS Google Scholar
Lucassen PJ, Stumpel M, Wang Q, Aronica E (2010a) Decreased numbers of progenitor cells but no response to antidepressant drugs in the hippocampus of elderly depressed patients. Neuropharmacology 58:940–949 Google Scholar
Marlatt MW, Lucassen PJ (2010) Neurogenesis and dementia: biology and pathophysiology of mice and men. Curr Alzheimer’s Res 7(2):113–125 ArticleCAS Google Scholar
Marlatt MW, Lucassen PJ, Van Praag H (2010) Side by side comparison of effects of running and antidepressants on neurogenesis in mice. Brain Res 1341:93–99 ArticlePubMedCAS Google Scholar
Marlatt MW, Potter MC, Lucassen PJ, van Praag H (2012) Running throughout middle-age improves memory function, hippocampal neurogenesis and BDNF levels in female C57Bl/6 J mice. Dev Neurobiol. doi:10.1002/dneu.22009 PubMed Google Scholar
Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11(1):47–60 ArticlePubMedCAS Google Scholar
Mu Y, Gage FH (2011) Adult hippocampal neurogenesis and its role in Alzheimer’s disease. Mol Neurodegener 22(6):85 Article Google Scholar
Navailles S et al (2008) Antidepressant drug-induced stimulation of mouse hippocampal neurogenesis is age-dependent and altered by early life stress. J Comp Neurol 509:372–381 Google Scholar
Neeper SA, Gomez-Pinilla F, Choi J, Cotman C (1995) Exercise and brain neurotrophins. Nature 373(6510):109 Google Scholar
Nelson RL, Guo Z, Halagappa VM, Pearson M, Gray AJ, Matsuoka Y et al (2007) Prophylactic treatment with paroxetine ameliorates behavioral deficits and retards the development of amyloid and tau pathologies in 3xTgAD mice. Exp Neurol 205(1):166–176 ArticlePubMedCAS Google Scholar
Nelson PT, Alafuzoff I, Bigio EH, Bouras C, Braak H, Cairns NJ, Castellani RJ, Crain BJ, Davies P, Del Tredici K, Duyckaerts C, Frosch MP, Haroutunian V, Hof PR, Hulette CM, Hyman BT, Iwatsubo T, Jellinger KA, Jicha GA, Kövari E, Kukull WA, Leverenz JB, Love S, Mackenzie IR, Mann DM, Masliah E, McKee AC, Montine TJ, Morris JC, Schneider JA, Sonnen JA, Thal DR, Trojanowski JQ, Troncoso JC, Wisniewski T, Woltjer RL, Beach TG (2012) Correlation of Alzheimer disease neuropathologic changes with cognitive status: a review of the literature. J Neuropathol Exp Neurol 71(5):362–381 ArticlePubMed Google Scholar
Oddo S, Caccamo A, Kitazawa M, Tseng BP, LaFerla FM (2003a) Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer’s disease. Neurobiol Aging 24(8):1063–1070 ArticleCAS Google Scholar
Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R et al (2003b) Triple-transgenic model of Alzheimer’s disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39(3):409–421 Google Scholar
Oitzl MS, Fluttert M, Sutanto W, de Kloet ER (1998) Continuous blockade of brain glucocorticoid receptors facilitates spatial learning and memory in rats. Eur J neurosci 10(12):3759–3766 Google Scholar
Pietropaolo S, Sun Y, Li R, Brana C, Feldon J, Yee BK (2008) The impact of voluntary exercise on mental health in rodents: a neuroplasticity perspective. Behav Brain Res 192(1):42–60 Google Scholar
Prinssen EP, Ballard TM, Kolb Y, Nicolas LB (2006) The effects of serotonin reuptake inhibitors on locomotor activity in gerbils. Pharmacol Biochem Behav 85(1):44–49 ArticlePubMedCAS Google Scholar
Rodriguez JJ, Jones VC, Tabuchi M, Allan SM, Knight EM, LaFerla FM et al (2008) Impaired adult neurogenesis in the dentate gyrus of a triple transgenic mouse model of Alzheimer’s disease. PLoS One 3(8):e2935 ArticlePubMed Google Scholar
Rodriguez JJ, Noristani HN, Olabarria M, Fletcher J, Somerville TDD, Yeh CY et al (2011) Voluntary running and environmental enrichment restores impaired hippocampal neurogenesis in a triple transgenic mouse model of Alzheimer’s disease. Curr Alzheimer Res 8(7):707–717 ArticlePubMedCAS Google Scholar
Rothman SM, Herdener N, Camandola S, Texel SJ, Mughal MR, Cong WN et al (2012) 3xTgAD mice exhibit altered behavior and elevated Aβ after chronic mild social stress. Neurobiol Aging 33(4):830, e1−12 Google Scholar
Russo-Neustadt AA, Beard RC, Huang YM, Cotman CW (2000) Physical activity and antidepressant treatment potentiate the expression of specific brain-derived neurotrophic factor transcripts in the rat hippocampus. Neuroscience 101(2):305–312 ArticlePubMedCAS Google Scholar
Schaaf MJ, Sibug RM, Duurland R, Fluttert MF, Oitzl MS, de Kloet ER et al (1999) Corticosterone effects on BDNF mRNA expression in the rat hippocampus during Morris water maze training. Stress 3(2):173–183 ArticlePubMedCAS Google Scholar
Schindowski K, Belarbi K, Bretteville A, Ando K, Buee L (2008) Neurogenesi and cell cycle-reactivated neuronal death during pathogenic tau aggregation. Genes Brain Behav 7(Suppl 1):92–100 PubMedCAS Google Scholar
Sennvik K, Boekhoorn K, Lasrado R, Terwel D, Verhaeghe S, Korr H et al (2007) Tau-4R suppresses proliferation and promotes neuronal differentiation in the hippocampus of tau knockin/knockout mice. FASEB J 21(9):2149–2161 ArticlePubMedCAS Google Scholar
Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R et al (1991) Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 30(4):572–580 ArticlePubMedCAS Google Scholar
Thompson A, Boekhoorn K, van Dam AM, Lucassen PJ (2008) Changes in adult neurogenesis in neurodegenerative diseases; cause or consequence? Genes Brain Behav 7:28–42 Google Scholar
Tucker S, Ahl M, Bush A, Westaway D, Huang X, Rogers JT (2005) Pilot study of the reducing effect on amyloidosis in vivo by three FDA pre-approved drugs via the Alzheimer’s “APP 5” untranslated region. Curr Alzheimer Res 2(2):249–254 ArticlePubMedCAS Google Scholar
van der Borght K, Kobor-Nyakas DE, Klauke K, Eggen BJ, Nyakas C, van der Zee EA et al (2009) Physical exercise leads to rapid adaptations in hippocampal vasculature: temporal dynamics and relationship to cell proliferation and neurogenesis. Hippocampus 19(10):928–936 ArticlePubMed Google Scholar
van Dooren T, Dewachter I, Borghgraef P, van Leuven F (2005) Transgenic mouse models for APP processing and Alzheimer’s disease: early and late defects. Subcell Biochem 38:45–63 ArticlePubMed Google Scholar
van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999a) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Nat Acad Sci U S A 96(23):13427–13431 Google Scholar
van Praag H, Kempermann G, Gage FH (1999b) Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2(3):266–270 Article Google Scholar
van Praag H, Shubert T, Zhao C, Gage FH (2005) Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 25(38):8680–8685 Google Scholar
Verwer RW, Sluiter AA, Balesar RA, Baayen JC, Noske DP, Dirven CMF, Wouda J, van Dam AM et al (2007) Mature astrocytes in the adult human neocortex express the early neuronal marker doublecortin. Brain 130:3321–3335 Google Scholar
Wang R, Dineley KT, Sweatt JD, Zheng H (2004) Presenilin 1 familial Alzheimer’s disease mutation leads to defective associative learning and impaired adult neurogenesis. Neuroscience 126(2):305–312 ArticlePubMedCAS Google Scholar
Weber M, Talmon S, Schulze I, Boeddinghaus C, Gross G, Schoemaker H et al (2009) Running wheel activity is sensitive to acute treatment with selective inhibitors for either serotonin or norepinephrine reuptake. Psychopharmacology 203(4):753–762 ArticlePubMedCAS Google Scholar
Wen PH, Shao X, Shao Z, Hof PR, Wisniewski T, Kelley K et al (2002) Overexpression of wild type but not an FAD mutant presenilin-1 promotes neurogenesis in the hippocampus of adult mice. Neurobiol Dis 10(1):8–19 Google Scholar
Wen PH, Hof PR, Chen X, Gluck K, Austin G, Younkin SG et al (2004) The presenilin-1 familial Alzheimer disease mutant P117L impairs neurogenesis in the hippocampus of adult mice. Exp Neurol 188(2):224–237 ArticlePubMedCAS Google Scholar
Wirths O, Multhaup G, Bayer TA (2004) A modified beta-amyloid hypothesis: intraneuronal accumulation of the beta-amyloid peptide–the first step of a fatal cascade. J Neurochem 91(3):513–520 ArticlePubMedCAS Google Scholar
Wirths O, Dins A, Bayer TA (2012) AβPP Accumulation and/or Intraneuronal Amyloid-β Accumulation? The 3xTg-AD Mouse Model Revisited. J Alzheimers Dis 28(4):897−904 PubMedCAS Google Scholar
Wolf SA, Kronenberg G, Lehmann K, Blankenship A, Overall R, Staufenbiel M et al (2006) Cognitive and physical activity differently modulate disease progression in the amyloid precursor protein (APP)-23 model of Alzheimer’s disease. Biol Psychiatry 60(12):1314–1323 ArticlePubMedCAS Google Scholar
Zhang C, McNeil E, Dressler L, Siman R (2007) Long-lasting impairment in hippocampal neurogenesis associated with amyloid deposition in a knock-in mouse model of familial Alzheimer’s disease. Exp Neurol 204(1):77–87 ArticlePubMedCAS Google Scholar