Ultrastructural studies in APP/PS1 mice expressing human apoe isoforms: Implications for Alzheimer's disease

International Journal of Clinical and Experimental Pathology

Volumn 5, Issue 6, 2012, Pages 482-495

  Dikranian, Krikor ^a   Kim, Jungsu ^a   Stewart, Floy R ^a   Levy, Marilyn A ^a   Holtzman, David M ^a  

^a WASHINGTON UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; Amyloid precursor protein; APoE; Electron microscopy; Presenilin 1

Indexed keywords

AMYLOID PRECURSOR PROTEIN; APOLIPOPROTEIN E; ISOPROTEIN; PRESENILIN 1;

ALZHEIMER DISEASE; AMYLOID PLAQUE; AMYLOIDOSIS; ANIMAL; ARTICLE; C57BL MOUSE; DISEASE MODEL; FEMALE; HUMAN; MALE; METABOLISM; MOUSE; MUTATION; NERVE CELL; PATHOLOGY; TRANSGENIC MOUSE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOIDOSIS; ANIMALS; APOLIPOPROTEINS E; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION; NEURONS; PLAQUE, AMYLOID; PRESENILIN-1; PROTEIN ISOFORMS;

EID: 84865995244     PISSN: None     EISSN: 19362625     Source Type: Journal    
DOI: None     Document Type: Article

References (79)

1. Terry RD. The Fine Structure of Neurofibrillary Tangles in Alzheimer's Disease. J Neuropathol Exp Neurol 1963; 22: 629-42.
2. Terry RD, Gonatas NK and Weiss M. Ultrastructural Studies in Alzheimer's Presenile Dementia. Am J Pathol 1964; 44: 269-97.
3. Kidd M. Paired helical filaments in electron microscopy of Alzheimer's disease. Nature 1963; 197: 192-3.
4. Kidd M. Alzheimer's Disease--an Electron Microscopical Study. Brain 1964; 87: 307-20.
5. Ikeda K, Haga C and Kosaka K. Light and electron microscopic examination of amyloid-rich primitive plaques: comparison with diffuse plaques. J Neurol 1990; 237: 88-93.
6. Wisniewski H, Terry R. Re-examination of the pathogenesis of the senile plaque. In: Zimmerman HM (ed). Progress in neuropathology, NY and London: Grune and Stratton 1973; 2: 26.
7. Yamaguchi H, Hirai S, Shoji M, Harigaya Y, Okamoto Y, Nakazato Y. Alzheimer type dementia: diffuse type of senile plaques demonstrated by beta protein immunostaining. Prog Clin Biol Res 1989; 317: 467-74.
8. Terry RD, Masliah E, Salmon DP, Butters N, De-Teresa R, Hill R, Hansen LA, Katzman R. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 1991; 30: 572-80.
9. Martin LJ, Pardo CA, Cork LC, Price DL. Synaptic pathology and glial responses to neuronal injury precede the formation of senile plaques and amyloid deposits in the aging cerebral cortex. Am J Pathol 1994; 145: 1358-81.
10. Scheff SW and Price DA. Synaptic pathology in Alzheimer's disease: a review of ultrastructural studies. Neurobiol Aging 2003; 24: 1029-46.
11. DeKosky ST and Scheff SW. Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol 1990; 27: 457-64.
12. Masliah E and Terry R. The role of synaptic proteins in the pathogenesis of disorders of the central nervous system. Brain Pathol 1993; 3: 77-85.
13. DeKosky ST, Scheff SW and Styren SD. Structural correlates of cognition in dementia: quantification and assessment of synapse change. Neurodegeneration 1996; 5: 417-21.
14. Janus C, Chishti MA and Westaway D. Transgenic mouse models of Alzheimer's disease. Biochim Biophys Acta 2000; 1502: 63-75.
15. Van Leuven F. Single and multiple transgenic mice as models for Alzheimer's disease. Prog Neurobiol 2000; 61: 305-12.
16. Holtzman DM, Bales KR, Tenkova T, Fagan AM, Parsadanian M, Sartorius LJ, Mackey B, Olney J, Mckeel D, Wozniak D, Paul SM. Apolipoprotein E isoform-dependent amyloid deposition and neuritic degeneration in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 2000; 97: 2892-7.
17. Gotz J. Tau and transgenic animal models. Brain Res Brain Res Rev 2001; 35: 266-86.
18. Crews L, Rockenstein E and Masliah E. APP transgenic modeling of Alzheimer's disease: mechanisms of neurodegeneration and aberrant neurogenesis. Brain Struct Funct 2010; 214: 111-26.
19. Hutton M and Hardy J. The presenilins and Alzheimer's disease. Hum Mol Genet 1997; 6: 1639-46.
20. Cruts M and Van Broeckhoven C. Molecular genetics of Alzheimer's disease. Ann Med 1998; 30: 560-5.
21. Rocchi A, Pellegrini S, Siciliano G, Murri L. Causative and susceptibility genes for Alzheimer's disease: a review. Brain Res Bull 2003; 61: 1-24.
22. Pastor P and Goate AM. Molecular genetics of Alzheimer's disease. Curr Psychiatry Rep 2004; 6: 125-33.
23. Masliah E, Sisk A, Mallory M, Mucke L, Schenk D, Games D. Comparison of neurodegenerative pathology in transgenic mice overexpressing V717F beta-amyloid precursor protein and Alzheimer's disease. J Neurosci 1996; 16: 5795-811.
24. Masliah E, Sisk A, Mallory M, Games D. Neurofibrillary pathology in transgenic mice overexpressing V717F beta-amyloid precursor protein. J Neuropathol Exp Neurol 2001; 60: 357-68.
25. Kurt MA, Davies DC, Kidd M, Duff K, Rolph SC, Jennings KH, Howlett DR. Neurodegenerative changes associated with beta-amyloid deposition in the brains of mice carrying mutant amyloid precursor protein and mutant presenilin-1 transgenes. Exp Neurol 2001; 171: 59-71.
26. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, LaFerla FM. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 2003; 39: 409-21.
27. Mucke L, Yu GQ, McConlogue L, Rockenstein EM, Abraham CR, Masliah E. Astroglial expression of human alpha(1)-antichymotrypsin enhances alzheimer-like pathology in amyloid protein precursor transgenic mice. Am J Pathol 2000; 157: 2003-10.
28. Sturchler-Pierrat C, Abramowski D, Duke M, Wiederhold KH, Mistl C, Rothacher S, Ledermann B, Bürki 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: 13287-92.
29. Moechars D, Dewachter I, Lorent K, Reversé D, Baekelandt V, Naidu A, Tesseur I, Spittaels K, Haute CV, Checler F, Godaux E, Cordell B, Van Leuven F. Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J Biol Chem 1999; 274: 6483-92.
30. Phinney AL, Deller T, Stalder M, Calhoun ME, Frotscher M, Sommer B, Staufenbiel M, Jucker M. Cerebral amyloid induces aberrant axonal sprouting and ectopic terminal formation in amyloid precursor protein transgenic mice. J Neurosci 1999; 19: 8552-9.
31. Bornemann KD and Staufenbiel M. Transgenic mouse models of Alzheimer's disease. Ann N Y Acad Sci 2000; 908: 260-6.
32. Rockenstein E, Mallory M, Mante M, Sisk A, Masliah E. Early formation of mature amyloidbeta protein deposits in a mutant APP transgenic model depends on levels of Abeta(1-42). J Neurosci Res 2001; 66: 573-82.
33. 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.
34. Borchelt DR, Ratovitski T, van Lare J, Lee MK, Gonzales V, Jenkins NA, Copeland NG, Price DL, Sisodia SS. Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 1997; 19: 939-45.
35. Stalder M, Phinney A, Probst A, Sommer B, Staufenbiel M, Jucker M. Association of microglia with amyloid plaques in brains of APP23 transgenic mice. Am J Pathol 1999; 154: 1673-84.
36. Holcomb L, Gordon MN, McGowan E, Yu X, Benkovic S, Jantzen P, Wright K, Saad I, Muel ler R, Morgan D, Sanders S, Zehr C, O'Campo K, Hardy J, Prada CM, Eckman C, Younkin S, Hsiao K, Duff K. Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 1998; 4: 97-100.
37. Wirths O, Weis J, Szczygielski J, Multhaup G, Bayer TA. Axonopathy in an APP/PS1 transgenic mouse model of Alzheimer's disease. Acta Neuropathol 2006; 111: 312-9.
38. Samura E, Shoji M, Kawarabayashi T, Sasaki A, Matsubara E, Murakami T, Wuhua X, Tamura S, Ikeda M, Ishiguro K, Saido TC, Westaway D, St George Hyslop P, Harigaya Y, Abe K. Enhanced accumulation of tau in doubly transgenic mice expressing mutant betaAPP and presenilin-1. Brain Res 2006; 1094: 192-9.
39. Bertram L, McQueen MB, Mullin K, Blacker D, Tanzi RE. Systematic meta-analyses of Alzheimer disease genetic association: the Alz-Gene database. Nat Genet 2007; 39: 7-23.
40. Holtzman DM, Fagan AM, Mackey B, Tenkova T, Sartorius L, Paul SM, Bales K, Ashe KH, Irizarry MC, Hyman BT. Apolipoprotein E facilitates neuritic and cerebrovascular plaque formation in an Alzheimer's disease model. Ann Neurol 2000; 47: 739-47.
41. Kim J, Basak JM and Holtzman DM. The role of apolipoprotein E in Alzheimer's disease. Neuron 2009; 63: 287-303.
42. Knouff C, Hinsdale ME, Mezdour H, Altenburg MK, Watanabe M, Quarfordt SH, Sullivan PM, Maeda N. Apo E structure determines VLDL clearance and atherosclerosis risk in mice. J Clin Invest 1999; 103: 1579-86.
43. Sullivan PM, Mezdour H, Aratani Y, Knouff C, Najib J, Reddick RL, Quarfordt SH, Maeda N. Targeted replacement of the mouse apolipoprotein E gene with the common human APOE3 allele enhances diet-induced hypercholesterolemia and atherosclerosis. J Biol Chem 1997; 272: 17972-80.
44. Radde R, Bolmont T, Kaeser SA, Coomaraswamy J, Lindau D, Stoltze L, Calhoun ME, Jäggi F, Wolburg H, Gengler S, Haass C, Ghetti B, Czech C, Hölscher C, Mathews PM, Jucker M. Abeta42-driven cerebral amyloidosis in transgenic mice reveals early and robust pathology. EMBO Rep 2006; 7: 940-6.
45. Kim J, Jiang H, Park S, Eltorai AE, Stewart FR, Yoon H, Basak JM, Finn MB, Holtzman DM. Haploinsufficiency of human APOE reduces amyloid deposition in a mouse model of amyloid-beta amyloidosis. J Neurosci 2011; 31: 18007-12.
46. Piedrahita JA, Zhang SH, Hagaman JR, Oliver PM, Maeda N. Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. Proc Natl Acad Sci USA 1992; 89: 4471-5.
47. Mattiace LA, Davies P and Dickson DW. Detection of HLA-DR on microglia in the human brain is a function of both clinical and technical factors. Am J Pathol 1990; 136: 1101-14.
48. Stalder M, Deller T, Staufenbiel M, Jucker M. 3D-Reconstruction of microglia and amyloid in APP23 transgenic mice: no evidence of intracellular amyloid. Neurobiol Aging 2001; 22: 427-34.
49. Wegiel J, Wang KC, Imaki H, Rubenstein R, Wronska A, Osuchowski M, Lipinski WJ, Walker LC, LeVine H. The role of microglial cells and astrocytes in fibrillar plaque evolution in transgenic APP(SW) mice. Neurobiol Aging 2001; 22: 49-61.
50. Nagele RG, Wegiel J, Venkataraman V, Imaki H, Wang KC. Contribution of glial cells to the development of amyloid plaques in Alzheimer's disease. Neurobiol Aging 2004; 25: 663-74.
51. Koenigsknecht-Talboo J, Meyer-Luehmann M, Parsadanian M, Garcia-Alloza M, Finn MB, Hyman BT, Bacskai BJ, Holtzman DM. Rapid microglial response around amyloid pathology after systemic anti-Abeta antibody administration in PDAPP mice. J Neurosci 2008; 28: 14156-64.
52. Meyer-Luehmann M, Spires-Jones TL, Prada C, Garcia-Alloza M, de Calignon A, Rozkalne A, Koenigsknecht-Talboo J, Holtzman DM, Bacskai BJ, Hyman BT. Rapid appearance and local toxicity of amyloid-beta plaques in a mouse model of Alzheimer's disease. Nature 2008; 451: 720-4.
53. Wisniewski HM, Wegiel J, Wang KC, Kujawa M, Lach B. Ultrastructural studies of the cells forming amyloid fibers in classical plaques. Can J Neurol Sci 1989; 16: 535-42.
54. Perlmutter LS, Barron E and Chui HC. Morphologic association between microglia and senile plaque amyloid in Alzheimer's disease. Neurosci Lett 1990; 119: 32-6.
55. Wegiel J, Imaki H, Wang KC, Wegiel J, Rubenstein R. Cells of monocyte/microglial lineage are involved in both microvessel amyloidosis and fibrillar plaque formation in APPsw tg mice. Brain Res 2004; 1022: 19-29.
56. Wisniewski HM, Wegiel J, Wang KC, Lach B. Ultrastructural studies of the cells forming amyloid in the cortical vessel wall in Alzheimer's disease. Acta Neuropathol 1992; 84: 117-27.
57. Wegiel J, Wang KC, Tarnawski M, Lach B. Microglia cells are the driving force in fibrillar plaque formation, whereas astrocytes are a leading factor in plague degradation. Acta Neuropathol 2000; 100: 356-64.
58. Lee CY and Landreth GE. The role of microglia in amyloid clearance from the AD brain. J Neural Transm 2010; 117: 949-60.
59. Grathwohl SA, Kälin RE, Bolmont T, Prokop S, Winkelmann G, Kaeser SA, Odenthal J, Radde R, Eldh T, Gandy S, Aguzzi A, Staufenbiel M, Mathews PM, Wolburg H, Heppner FL, Jucker M. Formation and maintenance of Alzheimer's disease beta-amyloid plaques in the absence of microglia. Nat Neurosci 2009; 12: 1361-3.
60. Kurt MA, Davies DC and Kidd M. beta-Amyloid immunoreactivity in astrocytes in Alzheimer's disease brain biopsies: an electron microscope study. Exp Neurol 1999; 158: 221-8.
61. Boutajangout A, Authelet M, Blanchard V, Touchet N, Tremp G, Pradier L, Brion JP. Characterisation of cytoskeletal abnormalities in mice transgenic for wild-type human tau and familial Alzheimer's disease mutants of APP and presenilin-1. Neurobiol Dis 2004; 15: 47-60.
62. Masliah E, Hansen L, Albright T, Mallory M, Terry RD. Immunoelectron microscopic study of synaptic pathology in Alzheimer's disease. Acta Neuropathol 1991; 81: 428-33.
63. Probst A, Gotz J, Wiederhold KH, Tolnay M, Mistl C, Jaton AL, Hong M, Ishihara T, Lee VM, Trojanowski JQ, Jakes R, Crowther RA, Spillantini MG, Burki K, Goedert M. Axonopathy and amyotrophy in mice transgenic for human fourrepeat tau protein. Acta Neuropathol 2000; 99: 469-81.
64. Lin WL, Lewis J, Yen SH, Hutton M, Dickson DW. Ultrastructural neuronal pathology in transgenic mice expressing mutant (P301L) human tau. J Neurocytol 2003; 32: 1091-105.
65. Lin WL, Zehr C, Lewis J, Hutton M, Yen SH, Dickson DW. Progressive white matter pathology in the spinal cord of transgenic mice expressing mutant (P301L) human tau. J Neurocytol 2005; 34: 397-410.
66. Tsukita S and Ishikawa H. The movement of membranous organelles in axons. Electron microscopic identification of anterogradely and retrogradely transported organelles. J Cell Biol 1980; 84: 513-30.
67. Mac Donald CL, Dikranian K, Bayly P, Holtzman D, Brody D. Diffusion tensor imaging reliably detects experimental traumatic axonal injury and indicates approximate time of injury. J Neurosci 2007; 27: 11869-76.
68. Rodriguez-Paez AC, Brunschwig JP and Bramlett HM. Light and electron microscopic assessment of progressive atrophy following moderate traumatic brain injury in the rat. Acta Neuropathol 2005; 109: 603-16.
69. Kelley BJ, Farkas O, Lifshitz J, Povlishock JT. Traumatic axonal injury in the perisomatic domain triggers ultrarapid secondary axotomy and Wallerian degeneration. Exp Neurol 2006; 198: 350-60.
70. Buki A and Povlishock JT. All roads lead to disconnection? Traumatic axonal injury revisited. Acta Neurochir (Wien) 2006; 148: 181-93; discussion 193-4.
71. Perl DP. Neuropathology of Alzheimer's disease. Mt Sinai J Med 2010; 77: 32-42.
72. Galloway PG, Perry G, Kosik KS, Gambetti P. Hirano bodies contain tau protein. Brain Res 1987; 403: 337-40.
73. Goldman JE. The association of actin with Hirano bodies. J Neuropathol Exp Neurol 1983; 42: 146-52.
74. Cataldo AM, Peterhoff CM, Schmidt SD, Terio NB, Duff K, Beard M, Mathews PM, Nixon RA. Presenilin mutations in familial Alzheimer disease and transgenic mouse models accelerate neuronal lysosomal pathology. J Neuropathol Exp Neurol 2004; 63: 821-30.
75. Blanchard V, Moussaoui S, Czech C, Touchet N, Bonici B, Planche M, Canton T, Jedidi I, Gohin M, Wirths O, Bayer TA, Langui D, Duyckaerts C, Tremp G, Pradier L. Time sequence of maturation of dystrophic neurites associated with Abeta deposits in APP/PS1 transgenic mice. Exp Neurol 2003; 184: 247-63.
76. Yang DS, Kumar A, Stavrides P, Peterson J, Peterhoff CM, Pawlik M, Levy E, Cataldo AM, Nixon RA. Neuronal apoptosis and autophagy cross talk in aging PS/APP mice, a model of Alzheimer's disease. Am J Pathol 2008; 173: 665-81.
77. Selznick LA, Holtzman DM, Han BH, Gokden M, Srinivasan AN, Johnson EM, Roth KA Jr. In situ immunodetection of neuronal caspase-3 activation in Alzheimer disease. J Neuropathol Exp Neurol 1999; 58: 1020-6.
78. Roth KA. Caspases, apoptosis, and Alzheimer disease: causation, correlation, and confusion. J Neuropathol Exp Neurol 2001; 60: 829-38.
79. Stadelmann C, Deckwerth TL, Srinivasan A, Bancher C, Brück W, Jellinger K, Lassmann H. Activation of caspase-3 in single neurons and autophagic granules of granulovacuolar degeneration in Alzheimer's disease. Evidence for apoptotic cell death. Am J Pathol 1999; 155: 1459-66.