What we can learn from animal models about cerebral multi-morbidity

Alzheimer's Research and Therapy

Volumn 7, Issue 1, 2015, Pages

  Baker, Siân ^a   Götz, Jürgen ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID BETA PROTEIN; TAU PROTEIN;

AGING; ALZHEIMER DISEASE; COMORBIDITY; DIFFUSE LEWY BODY DISEASE; EXPERIMENTAL MODEL; FRONTOTEMPORAL DEMENTIA; HUMAN; INVERTEBRATE MODEL; LEWY BODY; MOUSE MODEL; NEUROFIBRILLARY TANGLE; NEUROTRANSMISSION; NONHUMAN; PARKINSON DISEASE; PREVALENCE; PRIORITY JOURNAL; PROTEIN AGGREGATION; REVIEW; SENESCENCE ACCELERATED MOUSE; TRANSGENIC ANIMAL; VERTEBRATE;

EID: 84928009375     PISSN: None     EISSN: 17589193     Source Type: Journal    
DOI: 10.1186/s13195-015-0097-2     Document Type: Review

References (84)

1. Attems J, Jellinger K. Neuropathological correlates of cerebral multimorbidity. Curr Alzheimer Res. 2013;10:569-77.
2. Nagy Z, Esiri MM, Jobst KA, Morris JH, King EM, McDonald B, et al. The effects of additional pathology on the cognitive deficit in Alzheimer disease. J Neuropathol Exp Neurol. 1997;56:165-70.
3. Schneider JA, Arvanitakis Z, Bang W, Bennett DA. Mixed brain pathologies account for most dementia cases in community-dwelling older persons. Neurology. 2007;69:2197-204.
4. Nelson PT, Jicha GA, Schmitt FA, Liu H, Davis DG, Mendiondo MS, et al. Clinicopathologic correlations in a large Alzheimer disease center autopsy cohort: neuritic plaques and neurofibrillary tangles "do count" when staging disease severity. J Neuropathol Exp Neurol. 2007;66:1136-46.
5. Jellinger KA, Attems J. Prevalence and pathology of vascular dementia in the oldest-old. J Alzheimers Dis. 2010;21:1283-93.
6. Davidson YS, Raby S, Foulds PG, Robinson A, Thompson JC, Sikkink S, et al. TDP-43 pathological changes in early onset familial and sporadic Alzheimer's disease, late onset Alzheimer's disease and Down's syndrome: association with age, hippocampal sclerosis and clinical phenotype. Acta Neuropathol. 2011;122:703-13.
7. Duyckaerts C, Delatour B, Potier MC. Classification and basic pathology of Alzheimer disease. Acta Neuropathol. 2009;118:5-36.
8. Robinson JL, Geser F, Corrada MM, Berlau DJ, Arnold SE, Lee VM, et al. Neocortical and hippocampal amyloid-beta and tau measures associate with dementia in the oldest-old. Brain. 2011;134:3708-15.
9. Reser JE. Alzheimer's disease and natural cognitive aging may represent adaptive metabolism reduction programs. Behav Brain Funct. 2009;5:13.
10. West MJ, Coleman PD, Flood DG, Troncoso JC. Differences in the pattern of hippocampal neuronal loss in normal aging and Alzheimer's disease. Lancet. 1994;344:769-72.
11. Boyle PA, Wilson RS, Yu L, Barr AM, Honer WG, Schneider JA, et al. Much of late life cognitive decline is not due to common neurodegenerative pathologies. Ann Neurol. 2013;74:478-89.
12. Kimura N, Nakamura S, Goto N, Narushima E, Hara I, Shichiri S, et al. Senile plaques in an aged western lowland gorilla. Exp Anim. 2001;50:77-81.
13. Finch CE, Sapolsky RM. The evolution of Alzheimer disease, the reproductive schedule, and apoE isoforms. Neurobiol Aging. 1999;20:407-28.
14. Glass DJ, Arnold SE. Some evolutionary perspectives on Alzheimer's disease pathogenesis and pathology. Alzheimers Dement. 2012;8:343-51.
15. Götz J, Ittner LM. Animal models of Alzheimer's disease and frontotemporal dementia. Nat Rev Neurosci. 2008;9:532-44.
16. Götz J, Probst A, Spillantini MG, Schafer T, Jakes R, Burki K, et al. Somatodendritic localization and hyperphosphorylation of tau protein in transgenic mice expressing the longest human brain tau isoform. Embo J. 1995;14:1304-13.
17. Spittaels K, Van den Haute C, Van Dorpe J, Bruynseels K, Vandezande K, Laenen I, et al. Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein. Am J Pathol. 1999;155:2153-65.
18. Ishihara T, Hong M, Zhang B, Nakagawa Y, Lee MK, Trojanowski JQ, et al. Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron. 1999;24:751-62.
19. Probst A, Götz J, Wiederhold KH, Tolnay M, Mistl C, Jaton AL, et al. Axonopathy and amyotrophy in mice transgenic for human four-repeat tau protein. Acta Neuropathol (Berl). 2000;99:469-81.
20. Ishihara T, Zhang B, Higuchi M, Yoshiyama Y, Trojanowski JQ, Lee VM. Age-dependent induction of congophilic neurofibrillary tau inclusions in tau transgenic mice. Am J Pathol. 2001;158:555-62.
21. Umeda T, Maekawa S, Kimura T, Takashima A, Tomiyama T, Mori H. Neurofibrillary tangle formation by introducing wild-type human tau into APP transgenic mice. Acta Neuropathol. 2014;127:685-98.
22. Lewis J, McGowan E, Rockwood J, Melrose H, Nacharaju P, Van Slegtenhorst M, et al. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet. 2000;25:402-5.
23. Götz J, Chen F, van Dorpe J, Nitsch RM. Formation of neurofibrillary tangles in P301L tau transgenic mice induced by Abeta 42 fibrils. Science. 2001;293:1491-5.
24. Santacruz K, Lewis J, Spires T, Paulson J, Kotilinek L, Ingelsson M, et al. Tau suppression in a neurodegenerative mouse model improves memory function. Science. 2005;309:476-81.
25. Li J, Le W. Modeling neurodegenerative diseases in Caenorhabditis elegans. Exp Neurol. 2013;250:94-103.
26. Chew YL, Fan X, Götz J, Nicholas HR. Protein with tau-like repeats regulates neuronal integrity and lifespan in C. elegans. J Cell Sci. 2013;126:2079-91.
27. Feany MB, Bender WW. A Drosophila model of Parkinson's disease. Nature. 2000;404:394-8.
28. Wittmann CW, Wszolek MF, Shulman JM, Salvaterra PM, Lewis J, Hutton M, et al. Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science. 2001;293:711-4.
29. Kraemer BC, Zhang B, Leverenz JB, Thomas JH, Trojanowski JQ, Schellenberg GD. From the cover: neurodegeneration and defective neurotransmission in a Caenorhabditis elegans model of tauopathy. Proc Natl Acad Sci U S A. 2003;100:9980-5.
30. Guthrie CR, Schellenberg GD, Kraemer BC. SUT-2 potentiates tau-induced neurotoxicity in Caenorhabditis elegans. Hum Mol Genet. 2009;18:1825-38.
31. Mershin A, Pavlopoulos E, Fitch O, Braden BC, Nanopoulos DV, Skoulakis EM. Learning and memory deficits upon TAU accumulation in Drosophila mushroom body neurons. Learn Mem. 2004;11:277-87.
32. Steinhilb ML, Dias-Santagata D, Fulga TA, Felch DL, Feany MB. Tau phosphorylation sites work in concert to promote neurotoxicity in vivo. Mol Biol Cell. 2007;18:5060-8.
33. Kosmidis S, Grammenoudi S, Papanikolopoulou K, Skoulakis EM. Differential effects of Tau on the integrity and function of neurons essential for learning in Drosophila. J Neurosci. 2010;30:464-77.
34. Cowan CM, Bossing T, Page A, Shepherd D, Mudher A. Soluble hyperphosphorylated tau causes microtubule breakdown and functionally compromises normal tau in vivo. Acta Neuropathol. 2010;120:593-604.
35. Frost B, Gotz J, Feany MB. Connecting the dots between tau dysfunction and neurodegeneration. Trends Cell Biol. 2015;25:46-53.
36. Krstic D, Knuesel I. Deciphering the mechanism underlying late-onset Alzheimer disease. Nat Rev Neurol. 2013;9:25-34.
37. Gilley J, Seereeram A, Ando K, Mosely S, Andrews S, Kerschensteiner M, et al. Age-dependent axonal transport and locomotor changes and tau hypophosphorylation in a "P301L" tau knockin mouse. Neurobiol Aging. 2012;33:621 e1-621 e15.
38. Gaj T, Gersbach CA, Barbas 3rd CF. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 2013;31:397-405.
39. Delerue F, Sjollema G, Whittle B, Kruger S, Andrews D, Gotz J. Single nucleotide variants (SNVs) define senescence-accelerated SAMP8 mice, a model of a geriatric condition. J Alzheimers Dis. 2013;36:349-63.
40. Takeda T. Senescence-accelerated mouse (SAM): a biogerontological resource in aging research. Neurobiol Aging. 1999;20:105-10.
41. Shimada A, Hasegawa-Ishii S. Senescence-accelerated mice (SAMs) as a model for brain aging and immunosenescence. Aging Dis. 2011;2:414-35.
42. Flood JF, Morley JE. Learning and memory in the SAMP8 mouse. Neurosci Biobehav Rev. 1998;22:1-20.
43. Schmitt K, Grimm A, Kazmierczak A, Strosznajder JB, Götz J, Eckert A. Insights into mitochondrial dysfunction: aging, amyloid-beta, and tau-A deleterious trio. Antioxid Redox Signal. 2012;16:1456-66.
44. Kurokawa T, Sato E, Inoue A, Ishibashi S. Evidence that glucose metabolism is decreased in the cerebrum of aged female senescence-accelerated mouse; possible involvement of a low hexokinase activity. Neurosci Lett. 1996;214:45-8.
45. Kitamura Y, Zhao XH, Ohnuki T, Nomura Y. Ligand-binding characteristics of [3H]QNB, [3H]prazosin, [3H]rauwolscine, [3H]TCP and [3H]nitrendipine to cerebral cortical and hippocampal membranes of senescence accelerated mouse. Neurosci Lett. 1989;106:334-8.
46. Canudas AM, Gutierrez-Cuesta J, Rodriguez MI, Acuna-Castroviejo D, Sureda FX, Camins A, et al. Hyperphosphorylation of microtubule-associated protein tau in senescence-accelerated mouse (SAM). Mech Ageing Dev. 2005;126:1300-4.
47. Takemura M, Nakamura S, Akiguchi I, Ueno M, Oka N, Ishikawa S, et al. Beta/A4 proteinlike immunoreactive granular structures in the brain of senescence-accelerated mouse. Am J Pathol. 1993;142:1887-97.
48. Fukunari A, Kato A, Sakai Y, Yoshimoto T, Ishiura S, Suzuki K, et al. Colocalization of prolyl endopeptidase and amyloid beta-peptide in brains of senescence-accelerated mouse. Neurosci Lett. 1994;176:201-4.
49. Manich G, Mercader C, del Valle J, Duran-Vilaregut J, Camins A, Pallas M, et al. Characterization of amyloid-beta granules in the hippocampus of SAMP8 mice. J Alzheimers Dis. 2011;25:535-46.
50. Caballero B, Vega-Naredo I, Sierra V, Huidobro-Fernandez C, Soria-Valles C, De Gonzalo-Calvo D, et al. Favorable effects of a prolonged treatment with melatonin on the level of oxidative damage and neurodegeneration in senescence-accelerated mice. J Pineal Res. 2008;45:302-11.
51. Tsigelny IF, Crews L, Desplats P, Shaked GM, Sharikov Y, Mizuno H, et al. Mechanisms of hybrid oligomer formation in the pathogenesis of combined Alzheimer's and Parkinson's diseases. PLoS One. 2008;3:e3135.
52. Crews L, Tsigelny I, Hashimoto M, Masliah E. Role of synucleins in Alzheimer's disease. Neurotox Res. 2009;16:306-17.
53. Overk CR, Cartier A, Shaked G, Rockenstein E, Ubhi K, Spencer B, et al. Hippocampal neuronal cells that accumulate alpha-synuclein fragments are more vulnerable to Abeta oligomer toxicity via mGluR5 - implications for dementia with Lewy bodies. Mol Neurodegener. 2014;9:18.
54. Ueda K, Fukushima H, Masliah E, Xia Y, Iwai A, Yoshimoto M, et al. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc Natl Acad Sci U S A. 1993;90:11282-6.
55. Yang F, Ueda K, Chen P, Ashe KH, Cole GM. Plaque-associated alpha-synuclein (NACP) pathology in aged transgenic mice expressing amyloid precursor protein. Brain Res. 2000;853:381-3.
56. Masliah E, Rockenstein E, Veinbergs I, Sagara Y, Mallory M, Hashimoto M, et al. beta-Amyloid peptides enhance alpha-synuclein accumulation and neuronal deficits in a transgenic mouse model linking Alzheimer's disease and Parkinson's disease. Proc Natl Acad Sci U S A. 2001;98:12245-50.
57. Kallhoff V, Peethumnongsin E, Zheng H. Lack of alpha-synuclein increases amyloid plaque accumulation in a transgenic mouse model of Alzheimer's disease. Mol Neurodegener. 2007;2:6.
58. Giasson BI, Forman MS, Higuchi M, Golbe LI, Graves CL, Kotzbauer PT, et al. Initiation and synergistic fibrillization of tau and alpha-synuclein. Science. 2003;300:636-40.
59. Frasier M, Walzer M, McCarthy L, Magnuson D, Lee JM, Haas C, et al. Tau phosphorylation increases in symptomatic mice overexpressing A30P alpha-synuclein. Exp Neurol. 2005;192:274-87.
60. Haggerty T, Credle J, Rodriguez O, Wills J, Oaks AW, Masliah E, et al. Hyperphosphorylated Tau in an alpha-synuclein-overexpressing transgenic model of Parkinson's disease. Eur J Neurosci. 2011;33:1598-610.
61. Emmer KL, Waxman EA, Covy JP, Giasson BI. E46K human alpha-synuclein transgenic mice develop Lewy-like and tau pathology associated with age-dependent, detrimental motor impairment. J Biol Chem. 2011;286:35104-18.
62. Duka T, Duka V, Joyce JN, Sidhu A. Alpha-Synuclein contributes to GSK-3beta-catalyzed Tau phosphorylation in Parkinson's disease models. FASEB J. 2009;23:2820-30.
63. Roy B, Jackson GR. Interactions between Tau and alpha-synuclein augment neurotoxicity in a Drosophila model of Parkinson's disease. Hum Mol Genet. 2014;23:3008-23.
64. Wu TH, Lu YN, Chuang CL, Wu CL, Chiang AS, Krantz DE, et al. Loss of vesicular dopamine release precedes tauopathy in degenerative dopaminergic neurons in a Drosophila model expressing human tau. Acta Neuropathol. 2013;125:711-25.
65. Gunawardena S, Goldstein LS. Disruption of axonal transport and neuronal viability by amyloid precursor protein mutations in Drosophila. Neuron. 2001;32:389-401.
66. Greeve I, Kretzschmar D, Tschape JA, Beyn A, Brellinger C, Schweizer M, et al. Age-dependent neurodegeneration and Alzheimer-amyloid plaque formation in transgenic Drosophila. J Neurosci. 2004;24:3899-906.
67. Folwell J, Cowan CM, Ubhi KK, Shiabh H, Newman TA, Shepherd D, et al. Abeta exacerbates the neuronal dysfunction caused by human tau expression in a Drosophila model of Alzheimer's disease. Exp Neurol. 2010;223:401-9.
68. Roberson ED, Scearce-Levie K, Palop JJ, Yan F, Cheng IH, Wu T, et al. Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model. Science. 2007;316:750-4.
69. Ittner LM, Ke YD, Delerue F, Bi M, Gladbach A, van Eersel J, et al. Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell. 2010;142:387-97.
70. Morris M, Koyama A, Masliah E, Mucke L. Tau reduction does not prevent motor deficits in two mouse models of Parkinson's disease. PLoS One. 2011;6:e29257.
71. Clinton LK, Blurton-Jones M, Myczek K, Trojanowski JQ, LaFerla FM. Synergistic interactions between Abeta, tau, and alpha-synuclein: acceleration of neuropathology and cognitive decline. J Neurosci. 2010;30:7281-9.
72. Emmer KL, Covy JP, Giasson BI. Studies of protein aggregation in A53T alpha-synuclein transgenic, Tg2576 transgenic, and P246L presenilin-1 knock-in cross bred mice. Neurosci Lett. 2012;507:137-42.
73. Larson ME, Sherman MA, Greimel S, Kuskowski M, Schneider JA, Bennett DA, et al. Soluble alpha-synuclein is a novel modulator of Alzheimer's disease pathophysiology. J Neurosci. 2012;32:10253-66.
74. Guo JL, Covell DJ, Daniels JP, Iba M, Stieber A, Zhang B, et al. Distinct alpha-synuclein strains differentially promote tau inclusions in neurons. Cell. 2013;154:103-17.
75. Wang JW, Brent JR, Tomlinson A, Shneider NA, McCabe BD. The ALSassociated proteins FUS and TDP-43 function together to affect Drosophila locomotion and life span. J Clin Invest. 2011;121:4118-26.
76. Lanson Jr NA, Maltare A, King H, Smith R, Kim JH, Taylor JP, et al. A Drosophila model of FUS-related neurodegeneration reveals genetic interaction between FUS and TDP-43. Hum Mol Genet. 2011;20:2510-23.
77. Masliah E, Rockenstein E, Inglis C, Adame A, Bett C, Lucero M, et al. Prion infection promotes extensive accumulation of alpha-synuclein in aged human alpha-synuclein transgenic mice. Prion. 2012;6:184-90.
78. Clippinger AK, D'Alton S, Lin WL, Gendron TF, Howard J, Borchelt DR, et al. Robust cytoplasmic accumulation of phosphorylated TDP-43 in transgenic models of tauopathy. Acta Neuropathol. 2013;126:39-50.
79. Kikis EA, Gidalevitz T, Morimoto RI. Protein homeostasis in models of aging and age-related conformational disease. Adv Exp Med Biol. 2010;694:138-59.
80. Giasson BI, Lee VM, Trojanowski JQ. Interactions of amyloidogenic proteins. Neuromolecular Med. 2003;4:49-58.
81. Xu G, Stevens Jr SM, Moore BD, McClung S, Borchelt DR. Cytosolic proteins lose solubility as amyloid deposits in a transgenic mouse model of Alzheimer-type amyloidosis. Hum Mol Genet. 2013;22:2765-74.
82. David DC, Ollikainen N, Trinidad JC, Cary MP, Burlingame AL, Kenyon C. Widespread protein aggregation as an inherent part of aging in C. elegans. PLoS Biol. 2010;8:e1000450.
83. Scherzer CR, Jensen RV, Gullans SR, Feany MB. Gene expression changes presage neurodegeneration in a Drosophila model of Parkinson's disease. Hum Mol Genet. 2003;12:2457-66.
84. Lim Y-A, Rhein V, Baysang G, Meier F, Poljak A, Raftery M, et al. Abeta and human amylin share a common toxicity pathway via mitochondrial dysfunction. Proteomics. 2010;10:1621-33.