The type of Aβ-related neuronal degeneration differs between amyloid precursor protein (APP23) and amyloid β-peptide (APP48) transgenic mice

Acta Neuropathologica Communications

Volumn 2, Issue 1, 2014, Pages

  Upadhaya1a, Ajeet Rijal ^a   Scheibe, Frederik ^a   Kosterin, Irina ^a   Abramowski, Dorothee ^b   Gerth, Janina ^c   Kumar, Sathish ^c   Liebau, Stefan ^a   Yamaguchi, Haruyasu ^d   Walter, Jochen ^c   Staufenbiel, Matthias ^b   Thal, Dietmar Rudolf ^a  

^a UNIVERSITY OF ULM   (Germany)

^b NOVARTIS PHARMA AG   (Switzerland)

^c UNIVERSITY OF BONN   (Germany)

^d GUNMA UNIVERSITY   (Japan)

Author keywords

Degeneration; Dendrites; Extracellular amyloid protein; Intracellular amyloid protein; Mitochondria; Toxicity

Indexed keywords

EID: 85005865078     PISSN: None     EISSN: 20515960     Source Type: Journal    
DOI: 10.1186/2051-5960-1-77     Document Type: Article

References (61)

1. Alzheimer A: Über eine eigenartige Erkrankung der Hirnrinde. Allg Zschr Psych 1907, 64: 146-148.
2. Masters CL, Simms G, Weinman NA, Multhaup G, McDonald BL, Beyreuther K: Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proc Natl Acad Sci USA 1985, 82: 4245-4249. 10.1073/pnas.82.12.4245
3. DeKosky ST, Scheff SW: Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol 1990, 27: 457-464. 10.1002/ana.410270502
4. Masliah E, Terry RD, DeTeresa RM, Hansen LA: Immunohistochemical quantification of the synapse-related protein synaptophysin in Alzheimer disease. Neurosci Lett 1989, 103: 234-239. 10.1016/0304-3940(89)90582-X
5. Terry RD, Peck A, DeTeresa R, Schechter R, Horoupian DS: Some morphometric aspects of the brain in senile dementia of the Alzheimer type. Ann Neurol 1981, 10: 184-192. 10.1002/ana.410100209
6. Haass C, Koo EH, Mellon A, Hung AY, Selkoe DJ: Targeting of cell-surface beta-amyloid precursor protein to lysosomes: alternative processing into amyloid-bearing fragments. Nature 1992, 357: 500-503. 10.1038/357500a0
7. Kang J, Lemaire HG, Unterbeck A, Salbaum JM, Masters CL, Grzeschik KH, Multhaup G, Beyreuther K, Muller-Hill B: The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 1987, 325: 733-736. 10.1038/325733a0
8. Hardy J, Selkoe DJ: The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297: 353-356. 10.1126/science.1072994
9. D'Andrea MR, Nagele RG, Wang HY, Lee DH: Consistent immunohistochemical detection of intracellular beta-amyloid42 in pyramidal neurons of Alzheimer's disease entorhinal cortex. Neurosci Lett 2002, 333: 163-166. 10.1016/S0304-3940(02)00875-3
10. Gouras GK, Tsai J, Naslund J, Vincent B, Edgar M, Checler F, Greenfield JP, Haroutunian V, Buxbaum JD, Xu H, Greengard P, Relkin NR: Intraneuronal Abeta42 accumulation in human brain. Am J Pathol 2000, 156: 15-20. 10.1016/S0002-9440(10)64700-1
11. Takahashi RH, Milner TA, Li F, Nam EE, Edgar MA, Yamaguchi H, Beal MF, Xu H, Greengard P, Gouras GK: Intraneuronal Alzheimer abeta42 accumulates in multivesicular bodies and is associated with synaptic pathology. Am J Pathol 2002, 161: 1869-1879. 10.1016/S0002-9440(10)64463-X
12. Tomiyama T, Matsuyama S, Iso H, Umeda T, Takuma H, Ohnishi K, Ishibashi K, Teraoka R, Sakama N, Yamashita T, Nishitsuji K, Ito K, Shimada H, Lambert MP, Klein WL, Mori H: A mouse model of amyloid beta oligomers: their contribution to synaptic alteration, abnormal tau phosphorylation, glial activation, and neuronal loss in vivo. J Neurosci 2010, 30: 4845-4856. 10.1523/JNEUROSCI.5825-09.2010
13. Wirths O, Multhaup G, Czech C, Blanchard V, Moussaoui S, Tremp G, Pradier L, Beyreuther K, Bayer TA: Intraneuronal Abeta accumulation precedes plaque formation in beta-amyloid precursor protein and presenilin-1 double-transgenic mice. Neurosci Lett 2001, 306: 116-120. 10.1016/S0304-3940(01)01876-6
14. Umeda T, Tomiyama T, Sakama N, Tanaka S, Lambert MP, Klein WL, Mori H: Intraneuronal amyloid beta oligomers cause cell death via endoplasmic reticulum stress, endosomal/lysosomal leakage, and mitochondrial dysfunction in vivo. J Neurosci Res 2011, 89: 1031-1042. 10.1002/jnr.22640
15. Tampellini D, Capetillo-Zarate E, Dumont M, Huang Z, Yu F, Lin MT, Gouras GK: Effects of synaptic modulation on beta-amyloid, synaptophysin, and memory performance in Alzheimer's disease transgenic mice. J Neurosci 2010, 30: 14299-14304. 10.1523/JNEUROSCI.3383-10.2010
16. Abramowski D, Rabe S, Rijal Upadhaya A, Reichwald J, Danner S, Staab D, Capetillo-Zarate E, Yamaguchi H, Saido TC, Wiederhold KH, Thal DR, Staufenbiel M: Transgenic expression of intraneuronal Abeta42 but not Abeta40 leads to cellular Abeta lesions, degeneration and functional impairment without typical Alzheimer's disease pathology. J Neurosci 2012, 32: 1273-1283. 10.1523/JNEUROSCI.4586-11.2012
17. Calhoun ME, Wiederhold KH, Abramowski D, Phinney AL, Probst A, Sturchler-Pierrat C, Staufenbiel M, Sommer B, Jucker M: Neuron loss in APP transgenic mice. Nature 1998, 395: 755-756. 10.1038/27351
18. Capetillo-Zarate E, Staufenbiel M, Abramowski D, Haass C, Escher A, Stadelmann C, Yamaguchi H, Wiestler OD, Thal DR: Selective vulnerability of different types of commissural neurons for amyloid beta-protein induced neurodegeneration in APP23 mice correlates with dendritic tree morphology. Brain 2006, 129: 2992-3005. 10.1093/brain/awl176
19. Rijal Upadhaya A, Capetillo-Zarate E, Kosterin I, Abramowski D, Kumar S, Yamaguchi H, Walter J, Fändrich M, Staufenbiel M, Thal DR: Dispersible amyloid β-protein oligomers, protofibrils, and fibrils represent diffusible but not soluble aggregates: Their role in neurodegeneration in amyloid precursor protein (APP) transgenic mice. Neurobiol Aging 2012, 33: 2641-2660. 10.1016/j.neurobiolaging.2011.12.032
20. Sturchler-Pierrat C, Abramowski D, Duke M, Wiederhold KH, Mistl C, Rothacher S, Ledermann B, Burki K, Frey P, Paganetti PA, Waridel C, Calhoun ME, Jucker M, Probst A, Staufenbiel M, Sommer B: Two amyloid precursor protein transgenic mouse models with Alzheimer disease-like pathology. Proc Natl Acad Sci USA 1997, 94: 13287-13292. 10.1073/pnas.94.24.13287
21. Haass C, Lemere CA, Capell A, Citron M, Seubert P, Schenk D, Lannfelt L, Selkoe DJ: The Swedish mutation causes early-onset Alzheimer's disease by beta-secretase cleavage within the secretory pathway. Nat Med 1995, 1: 1291-1296. 10.1038/nm1295-1291
22. Rajendran L, Honsho M, Zahn TR, Keller P, Geiger KD, Verkade P, Simons K: Alzheimer's disease beta-amyloid peptides are released in association with exosomes. Proc Natl Acad Sci USA 2006, 103: 11172-11177. 10.1073/pnas.0603838103
23. Galuske RA, Schlote W, Bratzke H, Singer W: Interhemispheric asymmetries of the modular structure in human temporal cortex. Science 2000, 289: 1946-1949. 10.1126/science.289.5486.1946
24. Thal DR, Larionov S, Abramowski D, Wiederhold KH, van Dooren T, Yamaguchi H, Haass C, van Leuven F, Staufenbiel M, Capetillo-Zarate E: Occurrence and co-localization of amyloid beta-protein and apolipoprotein E in perivascular drainage channels of wild-type and APP-transgenic mice. Neurobiol Aging 2007, 28: 1221-1230. 10.1016/j.neurobiolaging.2006.05.029
25. Yamaguchi H, Sugihara S, Ogawa A, Saido TC, Ihara Y: Diffuse plaques associated with astroglial amyloid beta protein, possibly showing a disappearing stage of senile plaques. Acta Neuropathol 1998, 95: 217-222. 10.1007/s004010050790
26. Saido TC, Iwatsubo T, Mann DM, Shimada H, Ihara Y, Kawashima S: Dominant and differential deposition of distinct beta-amyloid peptide species, A beta N3(pE), in senile plaques. Neuron 1995, 14: 457-466. 10.1016/0896-6273(95)90301-1
27. Kumar S, Rezaei-Ghaleh N, Terwel D, Thal DR, Richard M, Hoch M, Mc Donald JM, Wullner U, Glebov K, Heneka MT, Walsh DM, Zweckstetter M, Walter J: Extracellular phosphorylation of the amyloid beta-peptide promotes formation of toxic aggregates during the pathogenesis of Alzheimer's disease. EMBO J 2011, 30: 2255-2265. 10.1038/emboj.2011.138
28. Kumar S, Wirths O, Theil S, Gerth J, Bayer TA, Walter J: Early intraneuronal accumulation and increased aggregation of phosphorylated Abeta in a mouse model of Alzheimer's disease. Acta Neuropathol 2013, 125: 699-709. 10.1007/s00401-013-1107-8
29. Hsu SM, Raine L, Fanger H: Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 1981, 29: 577-580. 10.1177/29.4.6166661
30. Mc Donald JM, Savva GM, Brayne C, Welzel AT, Forster G, Shankar GM, Selkoe DJ, Ince PG, Walsh DM: The presence of sodium dodecyl sulphate-stable Abeta dimers is strongly associated with Alzheimer-type dementia. Brain 2010, 133: 1328-1341. 10.1093/brain/awq065
31. Schmitz C, Hof PR: Recommendations for straightforward and rigorous methods of counting neurons based on a computer simulation approach. J Chem Neuroanat 2000, 20: 93-114. 10.1016/S0891-0618(00)00066-1
32. DeFelipe J, Marco P, Busturia I, Merchan-Perez A: Estimation of the number of synapses in the cerebral cortex: methodological considerations. Cereb Cortex 1999, 9: 722-732. 10.1093/cercor/9.7.722
33. Colonnier M: Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res 1968, 9: 268-287. 10.1016/0006-8993(68)90234-5
34. Miranda R, Sebrie C, Degrouard J, Gillet B, Jaillard D, Laroche S, Vaillend C: Reorganization of inhibitory synapses and increased PSD length of perforated excitatory synapses in hippocampal area CA1 of dystrophin-deficient mdx mice. Cereb Cortex 2009, 19: 876-888. 10.1093/cercor/bhn135
35. Siskova Z, Mahad DJ, Pudney C, Campbell G, Cadogan M, Asuni A, O'Connor V, Perry VH: Morphological and functional abnormalities in mitochondria associated with synaptic degeneration in prion disease. Am J Pathol 2010, 177: 1411-1421. 10.2353/ajpath.2010.091037
36. Weibel ER: Stereological principles for morphometry in electron microscopic cytology. Int Rev Cytol 1969, 26: 235-302.
37. Sturchler-Pierrat C, Staufenbiel M: Pathogenic mechanisms of Alzheimer's disease analyzed in the APP23 transgenic mouse model. Ann N Y Acad Sci 2000, 920: 134-139.
38. Huang SM, Mouri A, Kokubo H, Nakajima R, Suemoto T, Higuchi M, Staufenbiel M, Noda Y, Yamaguchi H, Nabeshima T, Saido TC, Iwata N: Neprilysin-sensitive synapse-associated amyloid-beta peptide oligomers impair neuronal plasticity and cognitive function. J Biol Chem 2006, 281: 17941-17951. 10.1074/jbc.M601372200
39. Rajendran L, Annaert W: Membrane trafficking pathways in Alzheimer's disease. Traffic 2012, 13: 759-770. 10.1111/j.1600-0854.2012.01332.x
40. Lacor PN, Buniel MC, Chang L, Fernandez SJ, Gong Y, Viola KL, Lambert MP, Velasco PT, Bigio EH, Finch CE, Krafft GA, Klein WL: Synaptic targeting by Alzheimer's-related amyloid beta oligomers. J Neurosci 2004, 24: 10191-10200. 10.1523/JNEUROSCI.3432-04.2004
41. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe DJ: Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 2008, 14: 837-842. 10.1038/nm1782
42. Wang HW, Pasternak JF, Kuo H, Ristic H, Lambert MP, Chromy B, Viola KL, Klein WL, Stine WB, Krafft GA, Trommer BL: Soluble oligomers of beta amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus. Brain Res 2002, 924: 133-140. 10.1016/S0006-8993(01)03058-X
43. Spires TL, Meyer-Luehmann M, Stern EA, McLean PJ, Skoch J, Nguyen PT, Bacskai BJ, Hyman BT: Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J Neurosci 2005, 25: 7278-7287. 10.1523/JNEUROSCI.1879-05.2005
44. Tsai J, Grutzendler J, Duff K, Gan WB: Fibrillar amyloid deposition leads to local synaptic abnormalities and breakage of neuronal branches. Nat Neurosci 2004, 7: 1181-1183. 10.1038/nn1335
45. McGowan E, Pickford F, Kim J, Onstead L, Eriksen J, Yu C, Skipper L, Murphy MP, Beard J, Das P, Jansen K, DeLucia M, Lin W-L, Dolios G, Wang R, Eckman CB, Dickson DW, Hutton M, Hardy J, Golde T: Aβ42 is essential for parenchymal and vascular amyloid deposition in mice. Neuron 2005, 47: 191-199. 10.1016/j.neuron.2005.06.030
46. Takuma H, Teraoka R, Mori H, Tomiyama T: Amyloid-beta E22Delta variant induces synaptic alteration in mouse hippocampal slices. Neuroreport 2008, 19: 615-619. 10.1097/WNR.0b013e3282fb78c4
47. Tomiyama T, Nagata T, Shimada H, Teraoka R, Fukushima A, Kanemitsu H, Takuma H, Kuwano R, Imagawa M, Ataka S, Wada Y, Yoshioka E, Nishizaki T, Watanabe Y, Mori H: A new amyloid beta variant favoring oligomerization in Alzheimer's-type dementia. Ann Neurol 2008, 63: 377-387. 10.1002/ana.21321
48. Bignante EA, Heredia F, Morfini G, Lorenzo A: Amyloid beta precursor protein as a molecular target for amyloid beta-induced neuronal degeneration in Alzheimer's disease. Neurobiol Aging 2013, 34: 2525-2537. 10.1016/j.neurobiolaging.2013.04.021
49. Costa RO, Ferreiro E, Cardoso SM, Oliveira CR, Pereira CM: ER stress-mediated apoptotic pathway induced by Abeta peptide requires the presence of functional mitochondria. J Alzheimers Dis 2010, 20: 625-636.
50. Wang ZF, Yin J, Zhang Y, Zhu LQ, Tian Q, Wang XC, Li HL, Wang JZ: Overexpression of tau proteins antagonizes amyloid-beta-potentiated apoptosis through mitochondria-caspase-3 pathway in N2a cells. J Alzheimers Dis 2010, 20: 145-157.
51. Caspersen C, Wang N, Yao J, Sosunov A, Chen X, Lustbader JW, Xu HW, Stern D, McKhann G, Yan SD: Mitochondrial Abeta: a potential focal point for neuronal metabolic dysfunction in Alzheimer's disease. FASEB J 2005, 19: 2040-2041.
52. Dragicevic N, Mamcarz M, Zhu Y, Buzzeo R, Tan J, Arendash GW, Bradshaw PC: Mitochondrial amyloid-beta levels are associated with the extent of mitochondrial dysfunction in different brain regions and the degree of cognitive impairment in Alzheimer's transgenic mice. J Alzheimers Dis 2010,20(Suppl 2):S535-S550.
53. Du H, Guo L, Fang F, Chen D, Sosunov AA, McKhann GM, Yan Y, Wang C, Zhang H, Molkentin JD, Gunn-Moore FJ, Vonsattel JP, Arancio O, Chen JX, Yan SD: Cyclophilin D deficiency attenuates mitochondrial and neuronal perturbation and ameliorates learning and memory in Alzheimer's disease. Nat Med 2008, 14: 1097-1105. 10.1038/nm.1868
54. Lustbader JW, Cirilli M, Lin C, Xu HW, Takuma K, Wang N, Caspersen C, Chen X, Pollak S, Chaney M, Trinchese F, Liu S, Gunn-Moore F, Lue LF, Walker DG, Kuppusamy P, Zewier ZL, Arancio O, Stern D, Yan SS, Wu H: ABAD directly links Abeta to mitochondrial toxicity in Alzheimer's disease. Science 2004, 304: 448-452. 10.1126/science.1091230
55. Manczak M, Anekonda TS, Henson E, Park BS, Quinn J, Reddy PH: Mitochondria are a direct site of A beta accumulation in Alzheimer's disease neurons: implications for free radical generation and oxidative damage in disease progression. Hum Mol Genet 2006, 15: 1437-1449. 10.1093/hmg/ddl066
56. Mattson MP: Cellular actions of beta-amyloid precursor protein and its soluble and fibrillogenic derivatives. Physiol Rev 1997, 77: 1081-1132.
57. Ovsepian SV, Antyborzec I, O'Leary VB, Zaborszky L, Herms J, Oliver Dolly J: Neurotrophin receptor p75 mediates the uptake of the amyloid beta (Abeta) peptide, guiding it to lysosomes for degradation in basal forebrain cholinergic neurons. Brain Struct Funct 2013. ehead of print: doi:10.1007/s00429-013-0583-x.
58. Ovsepian SV, Herms J: Drain of the brain: low-affinity p75 neurotrophin receptor affords a molecular sink for clearance of cortical amyloid beta by the cholinergic modulator system. Neurobiol Aging 2013, 34: 2517-2524. 10.1016/j.neurobiolaging.2013.05.005
59. Tampellini D, Magrane J, Takahashi RH, Li F, Lin MT, Almeida CG, Gouras GK: Internalized antibodies to the Abeta domain of APP reduce neuronal Abeta and protect against synaptic alterations. J Biol Chem 2007, 282: 18895-18906. 10.1074/jbc.M700373200
60. Dickson DW: The pathogenesis of senile plaques. J Neuropathol Exp Neurol 1997, 56: 321-339. 10.1097/00005072-199704000-00001
61. Wang D, Munoz DG: Qualitative and quantitative differences in senile plaque dystrophic neurites of Alzheimer's disease and normal aged brain. J Neuropathol Exp Neurol 1995, 54: 548-556. 10.1097/00005072-199507000-00009