Age-related changes of neuron numbers in the frontal cortex of a transgenic mouse model of Alzheimer’s disease

Anderson CT, Sheets PL, Kiritani T, Shepherd GMG (2010) Sublayer-specific microcircuits of corticospinal and corticostriatal neurons in motor cortex. Nat Neurosci 13(6):739–744 Arai H, Emson PC, Mountjoy CQ, Carassco LH, Heizmann CW (1987) Loss of parvalbumin-immunoreactive neurones from cortex in Alzheimer-type dementia. Brain Res 418(1):164–169 Bayer TA, Wirths O (2008) Review on the APP/PS1KI mouse model: intraneuronal Abeta accumulation triggers axonopathy, neuron loss and working memory impairment. Genes Brain Behav 7(Suppl 1):6–11. doi:10.1111/j.1601-183X.2007.00372.x Braak H, Braak E, Yilmazer D, de Vos RA, Jansen EN, Bohl J (1996) Pattern of brain destruction in Parkinson’s and Alzheimer’s diseases. J Neural Transm 103(4):455–490 Brady DR, Mufson EJ (1997) Parvalbumin-immunoreactive neurons in the hippocampal formation of Alzheimer’s diseased brain. Neuroscience 80(4):1113–1125 Brun A, Englund E (1981) Regional pattern of degeneration in Alzheimer’s disease: neuronal loss and histopathological grading. Histopathology 5(5):549–564 Bussiere T, Giannakopoulos P, Bouras C, Perl DP, Morrison JH, Hof PR (2003) Progressive degeneration of nonphosphorylated neurofilament protein-enriched pyramidal neurons predicts cognitive impairment in Alzheimer’s disease: stereologic analysis of prefrontal cortex area 9. J Comp Neurol 463(3):281–302 Casas C, Sergeant N, Itier JM, Blanchard V, Wirths O, van der Kolk N, Vingtdeux V, van de Steeg E, Ret G, Canton T, Drobecq H, Clark A, Bonici B, Delacourte A, Benavides J, Schmitz C, Tremp G, Bayer TA, Benoit P, Pradier L (2004) Massive CA1/2 neuronal loss with intraneuronal and N-terminal truncated Abeta42 accumulation in a novel Alzheimer transgenic model. Am J Pathol 165(4):1289–1300 Cauli B, Audinat E, Lambolez B, Angulo MC, Ropert N, Tsuzuki K, Hestrin S, Rossier J (1997) Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 17(10):3894–3906 Christensen DZ, Kraus SL, Flohr A, Cotel MC, Wirths O, Bayer TA (2008) Transient intraneuronal A beta rather than extracellular plaque pathology correlates with neuron loss in the frontal cortex of APP/PS1KI mice. Acta Neuropathol 116(6):647–655. doi:10.1007/s00401-008-0451-6 Conde F, Lund JS, Jacobowitz DM, Baimbridge KG, Lewis DA (1994) Local circuit neurons immunoreactive for calretinin, calbindin D-28k or parvalbumin in monkey prefrontal cortex: distribution and morphology. J Comp Neurol 341(1):95–116. doi:10.1002/cne.903410109 Cummings JL, Cole G (2002) Alzheimer disease. JAMA 287(18):2335–2338 Dickson DW (2001) Neuropathology of Alzheimer’s disease and other dementias. Clin Geriatr Med 17(2):209–228 Duyckaerts C, Delatour B, Potier MC (2009) Classification and basic pathology of Alzheimer disease. Acta Neuropathol 118(1):5–36. doi:10.1007/s00401-009-0532-1 Duyckaerts C, Potier MC, Delatour B (2008) Alzheimer disease models and human neuropathology: similarities and differences. Acta Neuropathol 115(1):5–38. doi:10.1007/s00401-007-0312-8 Ferrer I, Soriano E, Tunon T, Fonseca M, Guionnet N (1991) Parvalbumin immunoreactive neurons in normal human temporal neocortex and in patients with Alzheimer’s disease. J Neurol Sci 106(2):135–141 Francis P (2006) Targeting cell death in dementia. Alzheimer Dis Assoc Disord 20(2 Suppl 1):S3–S7. doi:10.1097/01.wad.0000213803.82058.46 Franklin KBJ, Paxinos G (1997) The mouse brain in stereotaxic coordinates. Academic Press, San Diego Giannakopoulos P, Herrmann FR, Bussiere T, Bouras C, Kovari E, Perl DP, Morrison JH, Gold G, Hof PR (2003) Tangle and neuron numbers, but not amyloid load, predict cognitive status in Alzheimer’s disease. Neurology 60(9):1495–1500 Gomez-Isla T, Hollister R, West H, Mui S, Growdon JH, Petersen RC, Parisi JE, Hyman BT (1997) Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer’s disease. Ann Neurol 41(1):17–24 Gotz J, Gotz NN (2009) Animal models for Alzheimer’s disease and frontotemporal dementia: a perspective. ASN Neuro 1(4). doi: 10.1042/AN20090042 Gould E (2007) How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 8(6):481–488. doi:10.1038/nrn2147 Gundersen HJ, Jensen EB (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147(Pt 3):229–263 Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics. Science 297(5580):353–356 Herms J, Anliker B, Heber S, Ring S, Fuhrmann M, Kretzschmar H, Sisodia S, Muller U (2004) Cortical dysplasia resembling human type 2 lissencephaly in mice lacking all three APP family members. EMBO J 23(20):4106–4115. doi:10.1038/sj.emboj.7600390 Hof PR, Cox K, Morrison JH (1990) Quantitative analysis of a vulnerable subset of pyramidal neurons in Alzheimer’s disease: I. superior frontal and inferior temporal cortex. J Comp Neurol 301(1):44–54. doi:10.1002/cne.903010105 Hof PR, Cox K, Young WG, Celio MR, Rogers J, Morrison JH (1991) Parvalbumin-immunoreactive neurons in the neocortex are resistant to degeneration in Alzheimer’s disease. J Neuropathol Exp Neurol 50(4):451–462 Kantor O, Temel Y, Holzmann C, Raber K, Nguyen HP, Cao C, Turkoglu HO, Rutten BP, Visser-Vandewalle V, Steinbusch HW, Blokland A, Korr H, Riess O, von Horsten S, Schmitz C (2006) Selective striatal neuron loss and alterations in behavior correlate with impaired striatal function in Huntington’s disease transgenic rats. Neurobiol Dis 22:538–547 Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7(6):476–486 Kubota Y, Kawaguchi Y (1994) Three classes of GABAergic interneurons in neocortex and neostriatum. Jpn J Physiol 44(Suppl 2):S145–148 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. doi:10.1007/s00406-007-0732-4 Kwak YD, Brannen CL, Qu T, Kim HM, Dong X, Soba P, Majumdar A, Kaplan A, Beyreuther K, Sugaya K (2006) Amyloid precursor protein regulates differentiation of human neural stem cells. Stem Cells Dev 15(3):381–389. doi:10.1089/scd.2006.15.381 Louvi A, Sisodia SS, Grove EA (2004) Presenilin 1 in migration and morphogenesis in the central nervous system. Development 131(13):3093–3105. doi:10.1242/dev.01191 Mann DM, Marcyniuk B, Yates PO, Neary D, Snowden JS (1988) The progression of the pathological changes of Alzheimer’s disease in frontal and temporal neocortex examined both at biopsy and at autopsy. Neuropathol Appl Neurobiol 14(3):177–195 Marlatt MW, Lucassen PJ (2010) Neurogenesis and Alzheimer’s disease: biology and pathophysiology in mice and men. Curr Alzheimer Res 7(2):113–125 Mattson MP, Cheng B, Davis D, Bryant K, Lieberburg I, Rydel RE (1992) Beta-amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J Neurosci 12(2):376–389 Mesulam MM, Geula C (1988) Acetylcholinesterase-rich pyramidal neurons in the human neocortex and hippocampus: absence at birth, development during the life span, and dissolution in Alzheimer’s disease. Ann Neurol 24(6):765–773 Mikkonen M, Alafuzoff I, Tapiola T, Soininen H, Miettinen R (1999) Subfield- and layer-specific changes in parvalbumin, calretinin and calbindin-D28 K immunoreactivity in the entorhinal cortex in Alzheimer’s disease. Neuroscience 92(2):515–532 Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167–202. doi:10.1146/annurev.neuro.24.1.167 Moechars D, Dewachter I, Lorent K, Reverse D, Baekelandt V, Naidu A, Tesseur I, Spittaels K, Haute CV, Checler F, Godaux E, Cordell B, Van Leuven F (1999) Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J Biol Chem 274(10):6483–6492 Morrison JH, Hof PR (2002) Selective vulnerability of corticocortical and hippocampal circuits in aging and Alzheimer’s disease. Prog Brain Res 136:467–486 Morrison JH, Hof PR (2007) Life and death of neurons in the aging cerebral cortex. Int Rev Neurobiol 81:41–57. doi:10.1016/S0074-7742(06)81004-4 Phinney AL, Horne P, Yang J, Janus C, Bergeron C, Westaway D (2003) Mouse models of Alzheimer’s disease: the long and filamentous road. Neurol Res 25(6):590–600 Pratico D, Uryu K, Leight S, Trojanoswki JQ, Lee VM (2001) Increased lipid peroxidation precedes amyloid plaque formation in an animal model of Alzheimer amyloidosis. J Neurosci 21(12):4183–4187 Price DL, Sisodia SS (1998) Mutant genes in familial Alzheimer’s disease and transgenic models. Annu Rev Neurosci 21:479–505 Probst A, Langui D, Ulrich J (1991) Alzheimer’s disease: a description of the structural lesions. Brain Pathol 1(4):229–239 Rakic P (2002) Neurogenesis in adult primate neocortex: an evaluation of the evidence. Nat Rev Neurosci 3(1):65–71. doi:10.1038/nrn700 Sampson VL, Morrison JH, Vickers JC (1997) The cellular basis for the relative resistance of parvalbumin and calretinin immunoreactive neocortical neurons to the pathology of Alzheimer’s disease. Exp Neurol 145(1):295–302. doi:10.1006/exnr.1997.6433 Satoh J, Tabira T, Sano M, Nakayama H, Tateishi J (1991) Parvalbumin-immunoreactive neurons in the human central nervous system are decreased in Alzheimer’s disease. Acta Neuropathol 81(4):388–395 Schmitz C (1998) Variation of fractionator estimates and its prediction. Anat Embryol (Berl) 198(5):371–397 Schmitz C, Hof PR (2005) Design-based stereology in neuroscience. Neuroscience 130(4):813–831 Schmitz C, Rutten BP, Pielen A, Schafer S, Wirths O, Tremp G, Czech C, Blanchard V, Multhaup G, Rezaie P, Korr H, Steinbusch HW, Pradier L, Bayer TA (2004) Hippocampal neuron loss exceeds amyloid plaque load in a transgenic mouse model of Alzheimer’s disease. Am J Pathol 164(4):1495–1502 Selkoe DJ (2001) Alzheimer’s disease: genes, proteins, and therapy. Physiol Rev 81(2):741–766 Solodkin A, Veldhuizen SD, Van Hoesen GW (1996) Contingent vulnerability of entorhinal parvalbumin-containing neurons in Alzheimer’s disease. J Neurosci 16(10):3311–3321 Takahashi H, Brasnjevic I, Rutten BP, Van Der Kolk N, Perl DP, Bouras C, Steinbusch HW, Schmitz C, Hof PR, Dickstein DL (2010) Hippocampal interneuron loss in an APP/PS1 double mutant mouse and in Alzheimer’s disease. Brain Struct Funct 214(2–3):145–160. doi:10.1007/s00429-010-0242-4 Tanzi RE, Bertram L (2005) Twenty years of the Alzheimer’s disease amyloid hypothesis: a genetic perspective. Cell 120(4):545–555 Thompson A, Boekhoorn K, Van Dam AM, Lucassen PJ (2008) Changes in adult neurogenesis in neurodegenerative diseases: cause or consequence? Genes Brain Behav 7(Suppl 1):28–42. doi:10.1111/j.1601-183X.2007.00379.x Trotti D, Danbolt NC, Volterra A (1998) Glutamate transporters are oxidant-vulnerable: a molecular link between oxidative and excitotoxic neurodegeneration? Trends Pharmacol Sci 19(8):328–334 Wirths O, Bethge T, Marcello A, Harmeier A, Jawhar S, Lucassen PJ, Multhaup G, Brody DL, Esparza T, Ingelsson M, Kalimo H, Lannfelt L, Bayer TA (2010) Pyroglutamate Abeta pathology in APP/PS1KI mice, sporadic and familial Alzheimer’s disease cases. J Neural Transm 117(1):85–96. doi:10.1007/s00702-009-0314-x Wirths O, Multhaup G, Czech C, Blanchard V, Moussaoui S, Tremp G, Pradier L, Beyreuther K, Bayer TA (2001) Intraneuronal Abeta accumulation precedes plaque formation in beta-amyloid precursor protein and presenilin-1 double-transgenic mice. Neurosci Lett 306(1–2):116–120 Yankner BA, Duffy LK, Kirschner DA (1990) Neurotrophic and neurotoxic effects of amyloid beta protein: reversal by tachykinin neuropeptides. Science 250(4978):279–282