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Current Alzheimer Research

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ISSN (Print): 1567-2050
ISSN (Online): 1875-5828

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Review Article

Retinal Changes in Transgenic Mouse Models of Alzheimer’s Disease

Author(s): Li Guo*, Nivedita Ravindran, Ehtesham Shamsher, Daniel Hill and M. Francesca Cordeiro

Volume 18, Issue 2, 2021

Published on: 14 April, 2021

Page: [89 - 102] Pages: 14

DOI: 10.2174/1567205018666210414113634

Price: $65

Open Access Journals Promotions 2
Abstract

Alzheimer’s disease (AD) is a neurodegenerative disorder, the most common form of dementia. AD is characterised by amyloid-β (Aβ) plaques and neurofibrillary tangles (NFT) in the brain, in association with neuronal loss and synaptic failure, causing cognitive deficits. Accurate and early diagnosis is currently unavailable in lifespan, hampering early intervention of potential new treatments. Visual deficits have been well documented in AD patients, and the pathological changes identified in the brain are also believed to be found in the retina, an integral part of the central nervous system. Retinal changes can be detected by real-time non-invasive imaging, due to the transparent nature of the ocular media, potentially allowing an earlier diagnosis as well as monitoring disease progression and treatment outcome. Animal models are essential for AD research, and this review has a focus on retinal changes in various transgenic AD mouse models with retinal imaging and immunohistochemical analysis as well as therapeutic effects in those models. We also discuss the limitations of transgenic AD models in clinical translations.

Keywords: Alzheimer's disease, transgenic mouse models, retina, in vivo imaging, histology, treatment.

« Previous Next »
[1]
Baumgart M, Snyder HM, Carrillo MC, Fazio S, Kim H, Johns H. Summary of the evidence on modifiable risk factors for cognitive decline and dementia: A population-based perspective. Alzheimers Dement 2015; 11(6): 718-26.
[http://dx.doi.org/10.1016/j.jalz.2015.05.016 ] [PMID: 26045020]
[2]
Möller HJ, Graeber MB. The case described by Alois Alzheimer in 1911. Historical and conceptual perspectives based on the clinical record and neurohistological sections. Eur Arch Psychiatry Clin Neurosci 1998; 248(3): 111-22.
[http://dx.doi.org/10.1007/s004060050027 ] [PMID: 9728729]
[3]
Henriques AD, Benedet AL, Camargos EF, Rosa-Neto P, Nóbrega OT. Fluid and imaging biomarkers for Alzheimer’s disease: Where we stand and where to head to. Exp Gerontol 2018; 107: 169-77.
[http://dx.doi.org/10.1016/j.exger.2018.01.002 ] [PMID: 29307736]
[4]
Hinton DR, Sadun AA, Blanks JC, Miller CA. Optic-nerve degeneration in Alzheimer’s disease. N Engl J Med 1986; 315(8): 485-7.
[http://dx.doi.org/10.1056/NEJM198608213150804 ] [PMID: 3736630]
[5]
Koronyo-Hamaoui M, Koronyo Y, Ljubimov AV, et al. Identification of amyloid plaques in retinas from Alzheimer’s patients and noninvasive in vivo optical imaging of retinal plaques in a mouse model. Neuroimage 2011; 54(1): S204-17.
[http://dx.doi.org/10.1016/j.neuroimage.2010.06.020 ] [PMID: 20550967]
[6]
Guo L, Duggan J, Cordeiro MF. Alzheimer’s disease and retinal neurodegeneration. Curr Alzheimer Res 2010; 7(1): 3-14.
[http://dx.doi.org/10.2174/156720510790274491 ] [PMID: 20205667]
[7]
Parnell M, Guo L, Abdi M, Cordeiro MF. Ocular manifestations of Alzheimer’s disease in animal models. Int J Alzheimers Dis 2012; 2012786494
[http://dx.doi.org/10.1155/2012/786494 ] [PMID: 22666623]
[8]
Chiquita S, Rodrigues-Neves AC, Baptista FI, et al. The retina as a window or mirror of the brain changes detected in Alzheimer’s disease: Critical aspects to unravel. Mol Neurobiol 2019; 56(8): 5416-35.
[http://dx.doi.org/10.1007/s12035-018-1461-6 ] [PMID: 30612332]
[9]
Javaid FZ, Brenton J, Guo L, Cordeiro MF. Visual and ocular manifestations of Alzheimer’s disease and their use as biomarkers for diagnosis and progression. Front Neurol 2016; 7: 55.
[http://dx.doi.org/10.3389/fneur.2016.00055 ] [PMID: 27148157]
[10]
Moore RY, Lenn NJ. A retinohypothalamic projection in the rat. J Comp Neurol 1972; 146(1): 1-14.
[http://dx.doi.org/10.1002/cne.901460102 ] [PMID: 4116104]
[11]
Phan TX, Malkani RG. Sleep and circadian rhythm disruption and stress intersect in Alzheimer’s disease. Neurobiol Stress 2018; 10100133
[http://dx.doi.org/10.1016/j.ynstr.2018.10.001 ] [PMID: 30937343]
[12]
Games D, Adams D, Alessandrini R, et al. Alzheimer-type neuropathology in transgenic mice overexpressing V717F beta-amyloid precursor protein 1995; 373(6514): 523-7.
[13]
Lesné S, Koh MT, Kotilinek L, et al. A specific amyloid-β protein assembly in the brain impairs memory. Nature 2006; 440(7082): 352-7.
[http://dx.doi.org/10.1038/nature04533 ] [PMID: 16541076]
[14]
Irizarry MC, McNamara M, Fedorchak K, Hsiao K, Hyman BT. APPSw transgenic mice develop age-related A beta deposits and neuropil abnormalities, but no neuronal loss in CA1. J Neuropathol Exp Neurol 1997; 56(9): 965-73.
[http://dx.doi.org/10.1097/00005072-199709000-00002 ] [PMID: 9291938]
[15]
Kitazawa M, Medeiros R, Laferla FM. Transgenic mouse models of Alzheimer disease: Developing a better model as a tool for therapeutic interventions. Curr Pharm Des 2012; 18(8): 1131-47.
[http://dx.doi.org/10.2174/138161212799315786 ] [PMID: 22288400]
[16]
Scheuner D, Eckman C, Jensen M, et al. Secreted amyloid beta-protein similar to that in the senile plaques of Alzheimer’s disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer’s disease. Nat Med 1996; 2(8): 864-70.
[http://dx.doi.org/10.1038/nm0896-864 ] [PMID: 8705854]
[17]
Dyrks T, Dyrks E, Masters CL, Beyreuther K. Amyloidogenicity of rodent and human beta A4 sequences. FEBS Lett 1993; 324(2): 231-6.
[http://dx.doi.org/10.1016/0014-5793(93)81399-K ] [PMID: 8508926]
[18]
Borchelt DR, Ratovitski T, van Lare J, et al. Accelerated amyloid deposition in the brains of transgenic mice coexpressing mutant presenilin 1 and amyloid precursor proteins. Neuron 1997; 19(4): 939-45.
[http://dx.doi.org/10.1016/S0896-6273(00)80974-5 ] [PMID: 9354339]
[19]
Götz J, Chen F, Barmettler R, Nitsch RM. Tau filament formation in transgenic mice expressing P301L tau. J Biol Chem 2001; 276(1): 529-34.
[http://dx.doi.org/10.1074/jbc.M006531200 ] [PMID: 11013246]
[20]
Sahara N, Lewis J, DeTure M, et al. Assembly of tau in transgenic animals expressing P301L tau: Alteration of phosphorylation and solubility. J Neurochem 2002; 83(6): 1498-508.
[http://dx.doi.org/10.1046/j.1471-4159.2002.01241.x ] [PMID: 12472903]
[21]
Tanemura K, Murayama M, Akagi T, et al. Neurodegeneration with tau accumulation in a transgenic mouse expressing V337M human tau. J Neurosci 2002; 22(1): 133-41.
[http://dx.doi.org/10.1523/JNEUROSCI.22-01-00133.2002 ] [PMID: 11756496]
[22]
Tatebayashi Y, Miyasaka T, Chui D-H, et al. Tau filament formation and associative memory deficit in aged mice expressing mutant (R406W) human tau. Proc Natl Acad Sci USA 2002; 99(21): 13896-901.
[http://dx.doi.org/10.1073/pnas.202205599 ] [PMID: 12368474]
[23]
Yoshiyama Y, Higuchi M, Zhang B, et al. Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 2007; 53(3): 337-51.
[http://dx.doi.org/10.1016/j.neuron.2007.01.010 ] [PMID: 17270732]
[24]
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(5534): 1491-5.
[http://dx.doi.org/10.1126/science.1062097 ] [PMID: 11520988]
[25]
Oddo S, Caccamo A, Shepherd JD, et al. Triple-transgenic model of Alzheimer’s disease with plaques and tangles: Intracellular Abeta and synaptic dysfunction. Neuron 2003; 39(3): 409-21.
[http://dx.doi.org/10.1016/S0896-6273(03)00434-3 ] [PMID: 12895417]
[26]
Fuhrmann M, Bittner T, Jung CKE, et al. Microglial Cx3cr1 knockout prevents neuron loss in a mouse model of Alzheimer’s disease. Nat Neurosci 2010; 13(4): 411-3.
[http://dx.doi.org/10.1038/nn.2511 ] [PMID: 20305648]
[27]
Oddo S, Caccamo A, Kitazawa M, Tseng BP, LaFerla FM. Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer’s disease. Neurobiol Aging 2003; 24(8): 1063-70.
[http://dx.doi.org/10.1016/j.neurobiolaging.2003.08.012 ] [PMID: 14643377]
[28]
Kitazawa M, Oddo S, Yamasaki TR, Green KN, LaFerla FM. Lipopolysaccharide-induced inflammation exacerbates tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer’s disease. J Neurosci 2005; 25(39): 8843-53.
[http://dx.doi.org/10.1523/JNEUROSCI.2868-05.2005 ] [PMID: 16192374]
[29]
Oakley H, Cole SL, Logan S, et al. Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer’s disease mutations: Potential factors in amyloid plaque formation. J Neurosci 2006; 26(40): 10129-40.
[http://dx.doi.org/10.1523/JNEUROSCI.1202-06.2006 ] [PMID: 17021169]
[30]
Sadleir KR, Popovic J, Vassar R. ER stress is not elevated in the 5XFAD mouse model of Alzheimer’s disease. J Biol Chem 2018; 293(48): 18434-43.
[http://dx.doi.org/10.1074/jbc.RA118.005769 ] [PMID: 30315100]
[31]
Crouzin N, Baranger K, Cavalier M, et al. Area-specific alterations of synaptic plasticity in the 5XFAD mouse model of Alzheimer’s disease: Dissociation between somatosensory cortex and hippocampus. PLoS One 2013; 8(9)e74667
[http://dx.doi.org/10.1371/journal.pone.0074667 ] [PMID: 24069328]
[32]
Duyckaerts C, Potier M-C, Delatour B. Alzheimer disease models and human neuropathology: Similarities and differences. Acta Neuropathol 2008; 115(1): 5-38.
[http://dx.doi.org/10.1007/s00401-007-0312-8 ] [PMID: 18038275]
[33]
Mullane K, Williams M. Preclinical models of Alzheimer’s Disease: relevance and translational validity. Curr Protocols Pharmacol 2019; 84(1)e57
[http://dx.doi.org/10.1002/cpph.57 ] [PMID: 30802363]
[34]
Drummond E, Wisniewski T. Alzheimer’s disease: Experimental models and reality. Acta Neuropathol 2017; 133(2): 155-75.
[http://dx.doi.org/10.1007/s00401-016-1662-x ] [PMID: 28025715]
[35]
Myers A, McGonigle P. Overview of transgenic mouse models for Alzheimer’s disease. Curr Protoc Neurosci 2019; 89(1)e81
[http://dx.doi.org/10.1002/cpns.81 ] [PMID: 31532917]
[36]
Liu B, Rasool S, Yang Z, et al. Amyloid-peptide vaccinations reduce beta-amyloid plaques but exacerbate vascular deposition and inflammation in the retina of Alzheimer’s transgenic mice. Am J Pathol 2009; 175(5): 2099-110.
[http://dx.doi.org/10.2353/ajpath.2009.090159 ] [PMID: 19834067]
[37]
Perez SE, Lumayag S, Kovacs B, Mufson EJ, Xu S. β-amyloid deposition and functional impairment in the retina of the APPswe/PS1DeltaE9 transgenic mouse model of Alzheimer’s disease. Invest Ophthalmol Vis Sci 2009; 50(2): 793-800.
[http://dx.doi.org/10.1167/iovs.08-2384 ] [PMID: 18791173]
[38]
Dutescu RM, Li Q-X, Crowston J, Masters CL, Baird PN, Culvenor JG. Amyloid precursor protein processing and retinal pathology in mouse models of Alzheimer’s disease. Graefes Arch Clin Exp Ophthalmol 2009; 247(9): 1213-21.
[http://dx.doi.org/10.1007/s00417-009-1060-3 ] [PMID: 19271231]
[39]
Chidlow G, Wood JPM, Manavis J, Finnie J, Casson RJ. Investigations into retinal pathology in the early stages of a mouse model of Alzheimer’s disease. J Alzheimers Dis 2017; 56(2): 655-75.
[http://dx.doi.org/10.3233/JAD-160823 ] [PMID: 28035930]
[40]
Schön C, Hoffmann NA, Ochs SM, et al. Long-term in vivo imaging of fibrillar tau in the retina of P301S transgenic mice. PLoS One 2012; 7(12)e53547
[http://dx.doi.org/10.1371/journal.pone.0053547 ] [PMID: 23300938]
[41]
Hsiao K, Chapman P, Nilsen S, et al. Correlative memory deficits, a elevation, and amyloid plaques in transgenic mice. Science 1996; 274(5284): 99-103.
[42]
Buccarello L, Sclip A, Sacchi M, et al. The c-jun N-terminal kinase plays a key role in ocular degenerative changes in a mouse model of Alzheimer disease suggesting a correlation between ocular and brain pathologies. Oncotarget 2017; 8(47): 83038-51.
[http://dx.doi.org/10.18632/oncotarget.19886 ] [PMID: 29137322]
[43]
Kim T-K, Lee J-E, Park S-K, et al. Analysis of differential plaque depositions in the brains of Tg2576 and Tg-APPswe/PS1dE9 transgenic mouse models of Alzheimer disease. Exp Mol Med 2012; 44(8): 492-502.
[http://dx.doi.org/10.3858/emm.2012.44.8.056 ] [PMID: 22644036]
[44]
Ning A, Cui J, To E, Ashe KH, Matsubara J. Amyloid-beta deposits lead to retinal degeneration in a mouse model of Alzheimer disease. Invest Ophthalmol Vis Sci 2008; 49(11): 5136-43.
[http://dx.doi.org/10.1167/iovs.08-1849 ] [PMID: 18566467]
[45]
Gupta VK, Chitranshi N, Gupta VB, et al. Amyloid β accumulation and inner retinal degenerative changes in Alzheimer’s disease transgenic mouse. Neurosci Lett 2016; 623: 52-6.
[http://dx.doi.org/10.1016/j.neulet.2016.04.059 ] [PMID: 27133194]
[46]
Joly S, Lamoureux S, Pernet V. Nonamyloidogenic processing of amyloid beta precursor protein is associated with retinal function improvement in aging male APPswe/PS1ΔE9 mice. Neurobiol Aging 2017; 53: 181-91.
[http://dx.doi.org/10.1016/j.neurobiolaging.2017.02.004 ] [PMID: 28262325]
[47]
Grimaldi A, Brighi C, Peruzzi G, et al. Inflammation, neurodegeneration and protein aggregation in the retina as ocular biomarkers for Alzheimer’s disease in the 3xTg-AD mouse model. Cell Death Dis 2018; 9(6): 685.
[http://dx.doi.org/10.1038/s41419-018-0740-5 ] [PMID: 29880901]
[48]
Edwards MM, Rodríguez JJ, Gutierrez-Lanza R, Yates J, Verkhratsky A, Lutty GA. Retinal macroglia changes in a triple transgenic mouse model of Alzheimer’s disease. Exp Eye Res 2014; 127: 252-60.
[http://dx.doi.org/10.1016/j.exer.2014.08.006 ] [PMID: 25149907]
[49]
Park SW, Kim JH, Mook-Jung I, et al. Intracellular amyloid beta alters the tight junction of retinal pigment epithelium in 5XFAD mice. Neurobiol Aging 2014; 35(9): 2013-20.
[http://dx.doi.org/10.1016/j.neurobiolaging.2014.03.008 ] [PMID: 24709310]
[50]
Park SW, Im S, Jun HO, et al. Dry age-related macular degeneration like pathology in aged 5XFAD mice: Ultrastructure and microarray analysis. Oncotarget 2017; 8(25): 40006-18.
[http://dx.doi.org/10.18632/oncotarget.16967 ] [PMID: 28467791]
[51]
Pogue AI, Dua P, Hill JM, Lukiw WJ. Progressive inflammatory pathology in the retina of aluminum-fed 5xFAD transgenic mice. J Inorg Biochem 2015; 152: 206-9.
[http://dx.doi.org/10.1016/j.jinorgbio.2015.07.009 ] [PMID: 26213226]
[52]
Alexandrov PN, Pogue A, Bhattacharjee S, Lukiw WJ. Retinal amyloid peptides and complement factor H in transgenic models of Alzheimer’s disease. Neuroreport 2011; 22(12): 623-7.
[http://dx.doi.org/10.1097/WNR.0b013e3283497334 ] [PMID: 21734608]
[53]
Hunter S, Brayne C. Do anti-amyloid beta protein antibody cross reactivities confound Alzheimer disease research? J Negat Results Biomed 2017; 16(1): 1.
[http://dx.doi.org/10.1186/s12952-017-0066-3 ] [PMID: 28126004]
[54]
Hewitt SM, Baskin DG, Frevert CW, Stahl WL, Rosa-Molinar E. Controls for immunohistochemistry: The Histochemical Society’s standards of practice for validation of immunohistochemical assays. J Histochem Cytochem 2014; 62(10): 693-7.
[http://dx.doi.org/10.1369/0022155414545224 ] [PMID: 25023613]
[55]
Ordóñez-Gutiérrez L, Antón M, Wandosell F. Peripheral amyloid levels present gender differences associated with aging in AβPP/PS1 mice. J Alzheimers Dis 2015; 44(4): 1063-8.
[http://dx.doi.org/10.3233/JAD-141158 ] [PMID: 25408213]
[56]
Callahan MJ, Lipinski WJ, Bian F, Durham RA, Pack A, Walker LC. Augmented senile plaque load in aged female β-amyloid precursor protein-transgenic mice. Am J Pathol 2001; 158(3): 1173-7.
[http://dx.doi.org/10.1016/S0002-9440(10)64064-3 ] [PMID: 11238065]
[57]
Yassine N, Lazaris A, Dorner-Ciossek C, et al. Detecting spatial memory deficits beyond blindness in tg2576 Alzheimer mice. Neurobiol Aging 2013; 34(3): 716-30.
[http://dx.doi.org/10.1016/j.neurobiolaging.2012.06.016 ] [PMID: 22819136]
[58]
Saint-Aubert L, Lemoine L, Chiotis K, Leuzy A, Rodriguez-Vieitez E, Nordberg A. Tau PET imaging: Present and future directions. Mol Neurodegener 2017; 12(1): 19.
[http://dx.doi.org/10.1186/s13024-017-0162-3 ] [PMID: 28219440]
[59]
Oh J, Eser RA, Ehrenberg AJ, et al. Profound degeneration of wake-promoting neurons in Alzheimer’s disease. Alzheimers Dement 2019; 15(10): 1253-63.
[http://dx.doi.org/10.1016/j.jalz.2019.06.3916 ] [PMID: 31416793]
[60]
Congdon EE, Sigurdsson EM. Tau-targeting therapies for Alzheimer disease. Nat Rev Neurol 2018; 14(7): 399-415.
[http://dx.doi.org/10.1038/s41582-018-0013-z ] [PMID: 29895964]
[61]
Otth C, Concha II, Arendt T, et al. AbetaPP induces cdk5-dependent tau hyperphosphorylation in transgenic mice Tg2576. J Alzheimers Dis 2002; 4(5): 417-30.
[http://dx.doi.org/10.3233/JAD-2002-4508 ] [PMID: 12446973]
[62]
Kurt MA, Davies DC, Kidd M, Duff K, Howlett DR. Hyperphosphorylated tau and paired helical filament-like structures in the brains of mice carrying mutant amyloid precursor protein and mutant presenilin-1 transgenes. Neurobiol Dis 2003; 14(1): 89-97.
[http://dx.doi.org/10.1016/S0969-9961(03)00084-6 ] [PMID: 13678670]
[63]
Yang Y, Shiao C, Hemingway JF, et al. Suppressed retinal degeneration in aged wild type and APPswe/PS1ΔE9 mice by bone marrow transplantation. PLoS One 2013; 8(6)e64246
[http://dx.doi.org/10.1371/journal.pone.0064246 ] [PMID: 23750207]
[64]
Zhao H, Chang R, Che H, et al. Hyperphosphorylation of tau protein by calpain regulation in retina of Alzheimer’s disease transgenic mouse. Neurosci Lett 2013; 551: 12-6.
[http://dx.doi.org/10.1016/j.neulet.2013.06.026 ] [PMID: 23810804]
[65]
King A. The search for better animal models of Alzheimer’s disease. Nature 2018; 559(7715): S13-5.
[http://dx.doi.org/10.1038/d41586-018-05722-9 ] [PMID: 30046083]
[66]
Gasparini L, Crowther RA, Martin KR, et al. Tau inclusions in retinal ganglion cells of human P301S tau transgenic mice: Effects on axonal viability. Neurobiol Aging 2011; 32(3): 419-33.
[http://dx.doi.org/10.1016/j.neurobiolaging.2009.03.002 ] [PMID: 19356824]
[67]
Chiasseu M, Alarcon-Martinez L, Belforte N, et al. Tau accumulation in the retina promotes early neuronal dysfunction and precedes brain pathology in a mouse model of Alzheimer’s disease. Mol Neurodegener 2017; 12(1): 58.
[http://dx.doi.org/10.1186/s13024-017-0199-3 ] [PMID: 28774322]
[68]
Rodriguez L, Mdzomba JB, Joly S, Boudreau-Laprise M, Planel E, Pernet V. Human tau expression does not induce mouse retina neurodegeneration, suggesting differential toxicity of tau in brain vs. retinal neurons. Front Mol Neurosci 2018; 11: 293.
[http://dx.doi.org/10.3389/fnmol.2018.00293 ] [PMID: 30197586]
[69]
Kim YS, Jung HM, Yoon B-E. Exploring glia to better understand Alzheimer’s disease. Anim Cells Syst (Seoul) 2018; 22(4): 213-8.
[http://dx.doi.org/10.1080/19768354.2018.1508498 ] [PMID: 30460100]
[70]
Fernández-Albarral JA, Salobrar-García E, Martínez-Páramo R, et al. Retinal glial changes in Alzheimer’s disease - A review. J Optom 2019; 12(3): 198-207.
[http://dx.doi.org/10.1016/j.optom.2018.07.001 ] [PMID: 30377086]
[71]
Navarro V, Sanchez-Mejias E, Jimenez S, et al. Microglia in Alzheimer’s disease: activated, dysfunctional or degenerative. Front Aging Neurosci 2018; 10: 140.
[http://dx.doi.org/10.3389/fnagi.2018.00140 ] [PMID: 29867449]
[72]
Oliveira-Souza FG, DeRamus ML, van Groen T, Lambert AE, Bolding MS, Strang CE. Retinal changes in the Tg-SwDI mouse model of Alzheimer’s disease. Neuroscience 2017; 354: 43-53.
[http://dx.doi.org/10.1016/j.neuroscience.2017.04.021 ] [PMID: 28450267]
[73]
Wirths O, Bayer TA. Neuron loss in transgenic mouse models of Alzheimer’s disease. Int J Alzheimers Dis 2010; 2010: 1-6.
[http://dx.doi.org/10.4061/2010/723782 ] [PMID: 20871861]
[74]
Chiu K, Chan T-F, Wu A, Leung IY-P, So K-F, Chang RC-C. Neurodegeneration of the retina in mouse models of Alzheimer’s disease: What can we learn from the retina? Age (Dordr) 2012; 34(3): 633-49.
[http://dx.doi.org/10.1007/s11357-011-9260-2 ] [PMID: 21559868]
[75]
Götz J, Deters N, Doldissen A, et al. A decade of tau transgenic animal models and beyond. Brain Pathol 2007; 17(1): 91-103.
[http://dx.doi.org/10.1111/j.1750-3639.2007.00051.x ] [PMID: 17493043]
[76]
Masuzzo A, Dinet V, Cavanagh C, Mascarelli F, Krantic S. Amyloidosis in retinal neurodegenerative diseases. Front Neurol 2016; 7: 127.
[http://dx.doi.org/10.3389/fneur.2016.00127 ] [PMID: 27551275]
[77]
Sadun AA, Bassi CJ. Optic nerve damage in Alzheimer’s disease. Ophthalmology 1990; 97(1): 9-17.
[http://dx.doi.org/10.1016/S0161-6420(90)32621-0 ] [PMID: 2314849]
[78]
Blanks JC, Hinton DR, Sadun AA, Miller CA. Retinal ganglion cell degeneration in Alzheimer’s disease. Brain Res 1989; 501(2): 364-72.
[http://dx.doi.org/10.1016/0006-8993(89)90653-7 ] [PMID: 2819446]
[79]
Blanks JC, Torigoe Y, Hinton DR, Blanks RH. Retinal pathology in Alzheimer’s disease. I. Ganglion cell loss in foveal/parafoveal retina. Neurobiol Aging 1996; 17(3): 377-84.
[http://dx.doi.org/10.1016/0197-4580(96)00010-3 ] [PMID: 8725899]
[80]
Koronyo Y, Biggs D, Barron E, et al. Retinal amyloid pathology and proof-of-concept imaging trial in Alzheimer’s disease. JCI Insight 2017; 2(16): 93621.
[http://dx.doi.org/10.1172/jci.insight.93621 ] [PMID: 28814675]
[81]
Blanks JC, Schmidt SY, Torigoe Y, Porrello KV, Hinton DR, Blanks RH. Retinal pathology in Alzheimer’s disease. II. Regional neuron loss and glial changes in GCL 1996; 17(3): 385-95.
[82]
Koronyo-Hamaoui M, Ko MK, Koronyo Y, et al. Attenuation of AD-like neuropathology by harnessing peripheral immune cells: Local elevation of IL-10 and MMP-9. J Neurochem 2009; 111(6): 1409-24.
[http://dx.doi.org/10.1111/j.1471-4159.2009.06402.x ] [PMID: 19780903]
[83]
Yang J, Yang J, Li Y, Xu Y, Ran C. Near-infrared fluorescence ocular imaging (NIRFOI) of Alzheimer’s disease. Mol Imaging Biol 2019; 21(1): 35-43.
[http://dx.doi.org/10.1007/s11307-018-1213-z ] [PMID: 29802553]
[84]
More SS, Beach JM, Vince R. Early Detection of amyloidopathy in Alzheimer’s mice by hyperspectral endoscopy. Invest Ophthalmol Vis Sci 2016; 57(7): 3231-8.
[http://dx.doi.org/10.1167/iovs.15-17406 ] [PMID: 27333181]
[85]
de Calignon A, Fox LM, Pitstick R, et al. Caspase activation precedes and leads to tangles. Nature 2010; 464(7292): 1201-4.
[http://dx.doi.org/10.1038/nature08890 ] [PMID: 20357768]
[86]
Cordeiro MF, Guo L, Coxon KM, et al. Imaging multiple phases of neurodegeneration: A novel approach to assessing cell death in vivo. Cell Death Dis 2010; 1(1): e3-3.
[http://dx.doi.org/10.1038/cddis.2009.3 ] [PMID: 21364622]
[87]
Cunha JP, Proença R, Dias-Santos A, et al. OCT in Alzheimer’s disease: Thinning of the RNFL and superior hemiretina. Graefes Arch Clin Exp Ophthalmol 2017; 255(9): 1827-35.
[http://dx.doi.org/10.1007/s00417-017-3715-9 ] [PMID: 28643042]
[88]
Ferrari L, Huang S-C, Magnani G, Ambrosi A, Comi G, Leocani L. Optical coherence tomography reveals retinal neuroaxonal thinning in frontotemporal dementia as in Alzheimer’s disease. J Alzheimers Dis 2017; 56(3): 1101-7.
[http://dx.doi.org/10.3233/JAD-160886 ] [PMID: 28106555]
[89]
Sánchez D, Castilla-Marti M, Rodríguez-Gómez O, et al. Usefulness of peripapillary nerve fiber layer thickness assessed by optical coherence tomography as a biomarker for Alzheimer’s disease. Sci Rep 2018; 8(1): 16345.
[http://dx.doi.org/10.1038/s41598-018-34577-3 ] [PMID: 30397251]
[90]
Gao L, Chen X, Tang Y, et al. Neuroprotective effect of memantine on the retinal ganglion cells of APPswe/PS1ΔE9 mice and its immunomodulatory mechanisms. Exp Eye Res 2015; 135: 47-58.
[http://dx.doi.org/10.1016/j.exer.2015.04.013 ] [PMID: 25912193]
[91]
Criscuolo C, Cerri E, Fabiani C, Capsoni S, Cattaneo A, Domenici L. The retina as a window to early dysfunctions of Alzheimer’s disease following studies with a 5xFAD mouse model. Neurobiol Aging 2018; 67: 181-8.
[http://dx.doi.org/10.1016/j.neurobiolaging.2018.03.017 ] [PMID: 29735432]
[92]
Mazzaro N, Barini E, Spillantini MG, Goedert M, Medini P, Gasparini L. Tau-driven neuronal and neurotrophic dysfunction in a mouse model of early tauopathy. J Neurosci 2016; 36(7): 2086-100.
[http://dx.doi.org/10.1523/JNEUROSCI.0774-15.2016 ] [PMID: 26888921]
[93]
Leinonen H, Lipponen A, Gurevicius K, Tanila H. Normal amplitude of electroretinography and visual evoked potential responses in AβPP/PS1 mice. J Alzheimers Dis 2016; 51(1): 21-6.
[http://dx.doi.org/10.3233/JAD-150798 ] [PMID: 26836173]
[94]
Shimazawa M, Inokuchi Y, Okuno T, et al. Reduced retinal function in amyloid precursor protein-over-expressing transgenic mice via attenuating glutamate-N-methyl-d-aspartate receptor signaling. J Neurochem 2008; 107(1): 279-90.
[http://dx.doi.org/10.1111/j.1471-4159.2008.05606.x ] [PMID: 18691390]
[95]
Prince M, Comas-Herrera A, Knapp M, Guerchet M, Karagiannidou M. World Alzheimer Report 2016 Improving healthcare for people living with dementia Coverage, Quality and costs now and in the future. Alzheimer’s Dis Int 2016; pp. 1-140.
[96]
Casey DA, Antimisiaris D, O’Brien J. Drugs for Alzheimer’s disease: Are they effective? P&T 2010; 35(4): 208-11.
[PMID: 20498822]
[97]
Cummings JL, Morstorf T, Zhong K. Alzheimer’s disease drug-development pipeline: Few candidates, frequent failures. Alzheimers Res Ther 2014; 6(4): 37.
[http://dx.doi.org/10.1186/alzrt269 ] [PMID: 25024750]
[98]
Chu LW. Alzheimer’s disease: Early diagnosis and treatment. Hong Kong Med J Xianggang yi xue za zhi 2012; 18(3): 228-37.
[99]
Mendes D, Oliveira MM, Moreira PI, et al. Beneficial effects of white wine polyphenols-enriched diet on Alzheimer’s disease-like pathology. J Nutr Biochem 2018; 55: 165-77.
[http://dx.doi.org/10.1016/j.jnutbio.2018.02.001 ] [PMID: 29525608]
[100]
Fukumoto H, Takahashi H, Tarui N, et al. A noncompetitive BACE1 inhibitor TAK-070 ameliorates Abeta pathology and behavioral deficits in a mouse model of Alzheimer’s disease. J Neurosci 2010; 30(33): 11157-66.
[http://dx.doi.org/10.1523/JNEUROSCI.2884-10.2010 ] [PMID: 20720123]
[101]
Yan Q, Zhang J, Liu H, et al. Anti-inflammatory drug therapy alters beta-amyloid processing and deposition in an animal model of Alzheimer’s disease. J Neurosci 2003; 23(20): 7504-9.
[http://dx.doi.org/10.1523/JNEUROSCI.23-20-07504.2003 ] [PMID: 12930788]
[102]
Noble W, Garwood C, Stephenson J, Kinsey AM, Hanger DP, Anderton BH. Minocycline reduces the development of abnormal tau species in models of Alzheimer’s disease. FASEB J 2009; 23(3): 739-50.
[http://dx.doi.org/10.1096/fj.08-113795 ] [PMID: 19001528]
[103]
Parachikova A, Vasilevko V, Cribbs DH, LaFerla FM, Green KN. Reductions in amyloid-β-derived neuroinflammation, with minocycline, restore cognition but do not significantly affect tau hyperphosphorylation. J Alzheimers Dis 2010; 21(2): 527-42.
[http://dx.doi.org/10.3233/JAD-2010-100204 ] [PMID: 20555131]
[104]
Schenk D, Barbour R, Dunn W, et al. Immunization with amyloid-β attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 1999; 400(6740): 173-7.
[http://dx.doi.org/10.1038/22124 ] [PMID: 10408445]
[105]
DeMattos RB, Bales KR, Cummins DJ, Dodart JC, Paul SM, Holtzman DM. Peripheral anti-A beta antibody alters CNS and plasma A beta clearance and decreases brain A beta burden in a mouse model of Alzheimer’s disease 2001; 98(15): 8850-5.
[106]
Liu B, Rasool S, Yang Z, et al. Amyloid-peptide vaccinations reduce β-amyloid plaques but exacerbate vascular deposition and inflammation in the retina of Alzheimer’s transgenic mice. Am J Pathol 2009; 175(5): 2099-110.
[http://dx.doi.org/10.2353/ajpath.2009.090159 ] [PMID: 19834067]
[107]
Parthasarathy R, Chow KM, Derafshi Z, et al. Reduction of amyloid-beta levels in mouse eye tissues by intra-vitreally delivered neprilysin. Exp Eye Res 2015; 138: 134-44.
[http://dx.doi.org/10.1016/j.exer.2015.06.027 ] [PMID: 26142956]
[108]
Ding J-D, Lin J, Mace BE, Herrmann R, Sullivan P, Bowes Rickman C. Targeting age-related macular degeneration with Alzheimer’s disease based immunotherapies: Anti-amyloid-β antibody attenuates pathologies in an age-related macular degeneration mouse model. Vision Res 2008; 48(3): 339-45.
[http://dx.doi.org/10.1016/j.visres.2007.07.025 ] [PMID: 17888483]
[109]
Guo L, Salt TE, Luong V, et al. Targeting amyloid-beta in glaucoma treatment 2007; 104(33): 13444-9.
[110]
Koronyo Y, Salumbides BC, Black KL, Koronyo-Hamaoui M. Alzheimer’s disease in the retina: Imaging retinal aβ plaques for early diagnosis and therapy assessment. Neurodegener Dis 2012; 10(1-4): 285-93.
[http://dx.doi.org/10.1159/000335154 ] [PMID: 22343730]
[111]
Tam JHK, Pasternak SH. Alzheimer’s Disease. Cereb Cortex Neurodegener Neuropsychiatr Disord 2017; pp. 83-118.
[http://dx.doi.org/10.1016/B978-0-12-801942-9.00004-5]
[112]
Gilman S, Koller M, Black RS, et al. AN1792(QS-21)-201 Study Team. Clinical effects of Abeta immunization (AN1792) in patients with AD in an interrupted trial. Neurology 2005; 64(9): 1553-62.
[http://dx.doi.org/10.1212/01.WNL.0000159740.16984.3C ] [PMID: 15883316]
[113]
Banik A, Brown RE, Bamburg J, et al. Translation of pre-clinical studies into successful clinical trials for Alzheimer’s disease: What are the roadblocks and how can they be overcome? J Alzheimers Dis 2015; 47(4): 815-43.
[http://dx.doi.org/10.3233/JAD-150136 ] [PMID: 26401762]
[114]
Kodamullil AT, Zekri F, Sood M, et al. Trial watch: Tracing investment in drug development for Alzheimer disease. Nat Rev Drug Discov 2017; 16(12): 819-9.
[http://dx.doi.org/10.1038/nrd.2017.169 ] [PMID: 29056749]
[115]
Michaelis ML, Georg G, Telikepalli H, McIntosh M, Rajewski RA. Ongoing in vivo studies with cytoskeletal drugs in tau transgenic mice. Curr Alzheimer Res 2006; 3(3): 215-9.
[http://dx.doi.org/10.2174/156720506777632880 ] [PMID: 16842098]
[116]
Li C, Ebrahimi A, Schluesener H. Drug pipeline in neurodegeneration based on transgenic mice models of Alzheimer’s disease. Ageing Res Rev 2013; 12(1): 116-40.
[http://dx.doi.org/10.1016/j.arr.2012.09.002 ] [PMID: 22982398]
[117]
Ashe KH, Zahs KR. Probing the biology of Alzheimer’s disease in mice. Neuron 2010; 66(5): 631-45.
[http://dx.doi.org/10.1016/j.neuron.2010.04.031 ] [PMID: 20547123]
[118]
Fang J, Pieper AA, Nussinov R, et al. Harnessing endophenotypes and network medicine for Alzheimer’s drug repurposing. Med Res Rev 2020; 40(6): 2386-426.
[http://dx.doi.org/10.1002/med.21709 ] [PMID: 32656864]

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