Three dimensions of the amyloid hypothesis: time, space and 'wingmen'

The amyloid hypothesis, which has been the predominant framework for research in Alzheimer's disease (AD), has been the source of considerable controversy. The amyloid hypothesis postulates that amyloid-β peptide (Aβ) is the causative agent in AD. It is strongly supported by data from rare autosomal dominant forms of AD. However, the evidence that Aβ causes or contributes to age-associated sporadic AD is more complex and less clear, prompting criticism of the hypothesis. We provide an overview of the major arguments for and against the amyloid hypothesis. We conclude that Aβ likely is the key initiator of a complex pathogenic cascade that causes AD. However, we argue that Aβ acts primarily as a trigger of other downstream processes, particularly tau aggregation, which mediate neurodegeneration. Aβ appears to be necessary, but not sufficient, to cause AD. Its major pathogenic effects may occur very early in the disease process.

[1]  Florence Pasquier,et al.  Phenotype associated with APP duplication in five families. , 2006, Brain : a journal of neurology.

[2]  D. Selkoe,et al.  Soluble amyloid β-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration , 2011, Proceedings of the National Academy of Sciences.

[3]  Maiken Nedergaard,et al.  Impairment of paravascular clearance pathways in the aging brain , 2014, Annals of neurology.

[4]  D. Holtzman,et al.  Haploinsufficiency of Human APOE Reduces Amyloid Deposition in a Mouse Model of Amyloid-β Amyloidosis , 2011, The Journal of Neuroscience.

[5]  H. Braak,et al.  The pathological process underlying Alzheimer’s disease in individuals under thirty , 2011, Acta Neuropathologica.

[6]  D. Borchelt,et al.  Reversible Pathologic and Cognitive Phenotypes in an Inducible Model of Alzheimer-Amyloidosis , 2013, The Journal of Neuroscience.

[7]  Nick C Fox,et al.  Clinical and biomarker changes in dominantly inherited Alzheimer's disease. , 2012, The New England journal of medicine.

[8]  S. Paul,et al.  Lack of apolipoprotein E dramatically reduces amyloid beta-peptide deposition. , 1997, Nature genetics.

[9]  A. Fagan,et al.  Preclinical Alzheimer's disease and its outcome: a longitudinal cohort study , 2013, The Lancet Neurology.

[10]  J. Troncoso,et al.  Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease , 1994, The Lancet.

[11]  T. Prolla,et al.  Increased mtDNA mutations with aging promotes amyloid accumulation and brain atrophy in the APP/Ld transgenic mouse model of Alzheimer’s disease , 2014, Molecular Neurodegeneration.

[12]  Holly Soares,et al.  Cerebrospinal fluid β-amyloid1–42 and tau in control subjects at risk for Alzheimer’s disease: The effect of APOE ε4 allele , 2004, Biological Psychiatry.

[13]  D. Holtzman,et al.  Altered microglial response to Aβ plaques in APPPS1-21 mice heterozygous for TREM2 , 2014, Molecular Neurodegeneration.

[14]  C. Cotman,et al.  Oxidation of Abeta and plaque biogenesis in Alzheimer's disease and Down syndrome. , 2001, Neurobiology of disease.

[15]  G. Waldemar,et al.  Alzheimer disease‐like clinical phenotype in a family with FTDP‐17 caused by a MAPT R406W mutation , 2008, European journal of neurology.

[16]  Menno P. Witter,et al.  Trans-Synaptic Spread of Tau Pathology In Vivo , 2012, PloS one.

[17]  C. Jack,et al.  Tracking pathophysiological processes in Alzheimer's disease: an updated hypothetical model of dynamic biomarkers , 2013, The Lancet Neurology.

[18]  R. Nitsch,et al.  Formation of Neurofibrillary Tangles in P301L Tau Transgenic Mice Induced by Aβ42 Fibrils , 2001, Science.

[19]  D. Campion,et al.  APP locus duplication causes autosomal dominant early-onset Alzheimer disease with cerebral amyloid angiopathy , 2006, Nature Genetics.

[20]  M N Rossor,et al.  Preclinical trials in autosomal dominant AD: implementation of the DIAN-TU trial. , 2013, Revue neurologique.

[21]  I. Lieberburg,et al.  Mutation of the Alzheimer's disease amyloid gene in hereditary cerebral hemorrhage, Dutch type. , 1990, Science.

[22]  M. Arimon,et al.  Presenilin-1 adopts pathogenic conformation in normal aging and in sporadic Alzheimer’s disease , 2013, Acta Neuropathologica.

[23]  C. Holmes,et al.  Reduction of aggregated Tau in neuronal processes but not in the cell bodies after Aβ42 immunisation in Alzheimer’s disease , 2010, Acta Neuropathologica.

[24]  Nick C Fox,et al.  Long-Term Follow-Up of Patients Immunized with AN1792: Reduced Functional Decline in Antibody Responders , 2009, Current Alzheimer research.

[25]  Basavaraj Hooli,et al.  A three-dimensional human neural cell culture model of Alzheimer’s disease , 2014, Nature.

[26]  Hui Zheng,et al.  Biology and pathophysiology of the amyloid precursor protein , 2011, Molecular Neurodegeneration.

[27]  L. Grinberg,et al.  Distinct Tau Prion Strains Propagate in Cells and Mice and Define Different Tauopathies , 2014, Neuron.

[28]  J. Morris,et al.  Profound Loss of Layer II Entorhinal Cortex Neurons Occurs in Very Mild Alzheimer’s Disease , 1996, The Journal of Neuroscience.

[29]  M. Hipp,et al.  Proteostasis impairment in protein-misfolding and -aggregation diseases. , 2014, Trends in cell biology.

[30]  Xin Wu,et al.  Immunization reverses memory deficits without reducing brain Aβ burden in Alzheimer's disease model , 2002, Nature Neuroscience.

[31]  B. de Strooper Proteases and proteolysis in Alzheimer disease: a multifactorial view on the disease process. , 2010, Physiological reviews.

[32]  A. Shah,et al.  ApoE influences amyloid-β (Aβ) clearance despite minimal apoE/Aβ association in physiological conditions , 2013, Proceedings of the National Academy of Sciences.

[33]  B. Strooper Proteases and Proteolysis in Alzheimer Disease: A Multifactorial View on the Disease Process , 2010 .

[34]  A. Fagan,et al.  Amyloid imaging and CSF biomarkers in predicting cognitive impairment up to 7.5 years later , 2013, Alzheimer's & Dementia.

[35]  C. Soto,et al.  Smoking exacerbates amyloid pathology in a mouse model of Alzheimer’s disease , 2013, Nature Communications.

[36]  B. Hyman,et al.  Gene Transfer of Human Apoe Isoforms Results in Differential Modulation of Amyloid Deposition and Neurotoxicity in Mouse Brain , 2013, Science Translational Medicine.

[37]  M. Farrer,et al.  Molecular mapping of alzheimer‐type dementia in Down's syndrome , 1998, Annals of neurology.

[38]  C R Jack,et al.  Hippocampal atrophy rates and CSF biomarkers in elderly APOE2 normal subjects , 2010, Neurology.

[39]  A. Pestronk,et al.  TREM2 variant p.R47H as a risk factor for sporadic amyotrophic lateral sclerosis. , 2014, JAMA neurology.

[40]  J. Growdon,et al.  Beneficial effect of human anti-amyloid-beta active immunization on neurite morphology and tau pathology. , 2010, Brain : a journal of neurology.

[41]  E. Mandelkow,et al.  Aβ Oligomers Cause Localized Ca2+ Elevation, Missorting of Endogenous Tau into Dendrites, Tau Phosphorylation, and Destruction of Microtubules and Spines , 2010, The Journal of Neuroscience.

[42]  D. Selkoe,et al.  Mutation of the beta-amyloid precursor protein in familial Alzheimer's disease increases beta-protein production. , 1992, Nature.

[43]  H. Soininen,et al.  Hyperphosphorylated tau in young and middle-aged subjects , 2011, Acta Neuropathologica.

[44]  A. Fagan,et al.  Visinin‐like protein‐1: Diagnostic and prognostic biomarker in Alzheimer disease , 2011, Annals of neurology.

[45]  Rie Teraoka,et al.  A Mouse Model of Amyloid β Oligomers: Their Contribution to Synaptic Alteration, Abnormal Tau Phosphorylation, Glial Activation, and Neuronal Loss In Vivo , 2010, The Journal of Neuroscience.

[46]  D. Walsh,et al.  Exogenous Induction of Cerebral ß-Amyloidogenesis Is Governed by Agent and Host , 2006, Science.

[47]  Amyloid imaging and CSF biomarkers in predicting cognitive impairment up to 7.5 years later , 2013, Neurology.

[48]  L. Mucke,et al.  Neurotoxicity of amyloid β-protein: synaptic and network dysfunction. , 2012, Cold Spring Harbor perspectives in medicine.

[49]  J. Price,et al.  The distribution of tangles, plaques and related immunohistochemical markers in healthy aging and Alzheimer's disease , 1991, Neurobiology of Aging.

[50]  L. Mucke,et al.  Reducing Endogenous Tau Ameliorates Amyloid ß-Induced Deficits in an Alzheimer's Disease Mouse Model , 2007, Science.

[51]  D. Selkoe,et al.  Mutation of the β-amyloid precursor protein in familial Alzheimer's disease increases β-protein production , 1992, Nature.

[52]  M. Vitek,et al.  Tau is essential to β-amyloid-induced neurotoxicity , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[53]  K. Kosik,et al.  Selective Phosphorylation of Adult Tau Isoforms in Mature Hippocampal Neurons Exposed to Fibrillar Aβ , 1997, Molecular and Cellular Neuroscience.

[54]  Bradley T. Hyman,et al.  Distribution of Alzheimer‐type pathologic changes in nondemented elderly individuals matches the pattern in Alzheimer's disease , 1992, Neurology.

[55]  A. Fagan,et al.  Human and Murine ApoE Markedly Alters Aβ Metabolism before and after Plaque Formation in a Mouse Model of Alzheimer's Disease , 2002, Neurobiology of Disease.

[56]  B. Hyman,et al.  Neuropathological alterations in Alzheimer disease. , 2011, Cold Spring Harbor perspectives in medicine.

[57]  Makoto Hashimoto,et al.  β-Amyloid peptides enhance α-synuclein accumulation and neuronal deficits in a transgenic mouse model linking Alzheimer's disease and Parkinson's disease , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[58]  D. Holtzman,et al.  Amyloid‐beta oligomerization in Alzheimer dementia versus high‐pathology controls , 2013, Annals of neurology.

[59]  W. Benzing,et al.  Evidence for glial-mediated inflammation in aged APPSW transgenic mice , 1999, Neurobiology of Aging.

[60]  M. L. Schmidt,et al.  Autosomal dominant dementia with widespread neurofibrillary tangles , 1997, Annals of neurology.

[61]  J. Haines,et al.  Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. , 1993, Science.

[62]  A. Gillespie,et al.  Reducing Human Apolipoprotein E Levels Attenuates Age-Dependent Aβ Accumulation in Mutant Human Amyloid Precursor Protein Transgenic Mice , 2012, The Journal of Neuroscience.

[63]  Seth Love,et al.  Long-term effects of Aβ42 immunisation in Alzheimer's disease: follow-up of a randomised, placebo-controlled phase I trial , 2008, The Lancet.

[64]  L. Mucke,et al.  Amyloid-β/Fyn–Induced Synaptic, Network, and Cognitive Impairments Depend on Tau Levels in Multiple Mouse Models of Alzheimer's Disease , 2011, The Journal of Neuroscience.

[65]  Michela Gallagher,et al.  A specific amyloid-beta protein assembly in the brain impairs memory. , 2006, Nature.

[66]  E. Mandelkow,et al.  Fyn-Tau-Amyloid: A Toxic Triad , 2010, Cell.

[67]  L. Wilkins Short-term clinical outcomes for stages of NIA-AA preclinical Alzheimer disease , 2017, Neurology.

[68]  J. Hardy,et al.  Alzheimer's disease: the amyloid cascade hypothesis. , 1992, Science.

[69]  M. Pericak-Vance,et al.  Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease , 1991, Nature.

[70]  A. Korczyn The amyloid cascade hypothesis , 2008, Alzheimer's & Dementia.

[71]  C. Cotman,et al.  Oxidation of Aβ and Plaque Biogenesis in Alzheimer's Disease and Down Syndrome , 2001, Neurobiology of Disease.

[72]  H. Braak,et al.  Neuropathological stageing of Alzheimer-related changes , 2004, Acta Neuropathologica.

[73]  Nick C Fox,et al.  Symptom onset in autosomal dominant Alzheimer disease , 2014, Neurology.

[74]  L A Hansen,et al.  The importance of neuritic plaques and tangles to the development and evolution of AD , 2004, Neurology.

[75]  Holly Soares,et al.  Cerebrospinal fluid beta-amyloid1-42 and tau in control subjects at risk for Alzheimer's disease: the effect of APOE epsilon4 allele. , 2004, Biological psychiatry.

[76]  Y. Xiong,et al.  Pittsburgh compound B retention and progression of cognitive status – a meta‐analysis , 2014, European journal of neurology.

[77]  Jee Hoon Roh,et al.  Neuronal activity regulates the regional vulnerability to amyloid-β deposition , 2011, Nature Neuroscience.

[78]  B. de Strooper,et al.  Modification of γ-secretase by nitrosative stress links neuronal ageing to sporadic Alzheimer's disease , 2012, EMBO molecular medicine.

[79]  Mutation of the Alzheimer's disease amyloid gene in hereditary cerebral hemorrhage, Dutch type. , 1990, Science.

[80]  William T. Hu,et al.  Cleavage of tau by asparagine endopeptidase mediates the neurofibrillary pathology in Alzheimer’s disease , 2014, Nature Medicine.

[81]  David A. Bennett,et al.  REST and Stress Resistance in Aging and Alzheimer’s Disease , 2014, Nature.

[82]  P. Reddy,et al.  Impaired mitochondrial biogenesis, defective axonal transport of mitochondria, abnormal mitochondrial dynamics and synaptic degeneration in a mouse model of Alzheimer's disease. , 2011, Human molecular genetics.

[83]  D. Bennett,et al.  Soluble α-Synuclein Is a Novel Modulator of Alzheimer's Disease Pathophysiology , 2012, The Journal of Neuroscience.

[84]  Cornelia M. Wilson,et al.  Tau protein kinases: Involvement in Alzheimer's disease , 2013, Ageing Research Reviews.

[85]  T. Saido,et al.  Dutch, Flemish, Italian, and Arctic mutations of APP and resistance of Aβ to physiologically relevant proteolytic degradation , 2003, The Lancet.

[86]  G. Rebeck,et al.  Aging reduces glial uptake and promotes extracellular accumulation of Aβ from a lentiviral vector , 2014, Front. Aging Neurosci..

[87]  Seiji Nishino,et al.  Amyloid-β Dynamics Are Regulated by Orexin and the Sleep-Wake Cycle , 2009, Science.

[88]  D. Holtzman,et al.  Anti-apoE immunotherapy inhibits amyloid accumulation in a transgenic mouse model of Aβ amyloidosis , 2012, The Journal of experimental medicine.

[89]  V. Preedy,et al.  Prospective Cohort Study , 2010 .

[90]  C. Masters,et al.  Soluble pool of Aβ amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease , 1999, Annals of neurology.

[91]  C. Jack,et al.  TDP-43 is a key player in the clinical features associated with Alzheimer’s disease , 2014, Acta Neuropathologica.

[92]  Bin Zhang,et al.  Distinct α-Synuclein Strains Differentially Promote Tau Inclusions in Neurons , 2013, Cell.

[93]  A. Pestronk,et al.  TREM 2 Variant p . R 47 H as a Risk Factor for Sporadic Amyotrophic Lateral Sclerosis , 2014 .

[94]  Kewei Chen,et al.  Alzheimer's Prevention Initiative: a plan to accelerate the evaluation of presymptomatic treatments. , 2011, Journal of Alzheimer's disease : JAD.

[95]  R. Petersen,et al.  neurodegeneration : evidence for association of the p . R 47 H variant with frontotemporal dementia and Parkinson ¿ s disease Permalink , 2013 .

[96]  Keith A. Johnson,et al.  Neuropathology of Cognitively Normal Elderly , 2003, Journal of neuropathology and experimental neurology.

[97]  K. Zahs,et al.  Correlation of specific amyloid-β oligomers with tau in cerebrospinal fluid from cognitively normal older adults. , 2013, JAMA neurology.

[98]  D. Borchelt,et al.  Normal cognition in transgenic BRI2-Aβ mice , 2013, Molecular Neurodegeneration.

[99]  J. Hardy,et al.  Enhanced Neurofibrillary Degeneration in Transgenic Mice Expressing Mutant Tau and APP , 2001, Science.

[100]  C. Geula,et al.  A Lifespan Observation of a Novel Mouse Model: In Vivo Evidence Supports Aβ Oligomer Hypothesis , 2014, PloS one.

[101]  R. Sperling,et al.  The preclinical Alzheimer cognitive composite: measuring amyloid-related decline. , 2014, JAMA neurology.

[102]  Daniel J. R. Christensen,et al.  Sleep Drives Metabolite Clearance from the Adult Brain , 2013, Science.

[103]  J. Morris,et al.  Tangles and plaques in nondemented aging and “preclinical” Alzheimer's disease , 1999, Annals of neurology.

[104]  G. Halliday,et al.  Variations in the neuropathology of familial Alzheimer’s disease , 2009, Acta Neuropathologica.

[105]  J. Kelly,et al.  The oxidative stress metabolite 4-hydroxynonenal promotes Alzheimer protofibril formation. , 2007, Biochemistry.

[106]  E. Masliah,et al.  Alpha‐synuclein in Lewy Body Disease and Alzheimer's Disease , 1999, Brain pathology.

[107]  Ralph A. Nixon,et al.  Autophagy failure in Alzheimer's disease—locating the primary defect , 2011, Neurobiology of Disease.

[108]  Richard Hollister,et al.  Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease , 1997, Annals of neurology.

[109]  J. Keller,et al.  Oxidative stress, neurodegeneration, and the balance of protein degradation and protein synthesis. , 2013, Free radical biology & medicine.

[110]  Naruhiko Sahara,et al.  Propagation of Tau Pathology in a Model of Early Alzheimer's Disease , 2012, Neuron.

[111]  John Q Trojanowski,et al.  A{beta} accelerates the spatiotemporal progression of tau pathology and augments tau amyloidosis in an Alzheimer mouse model. , 2010, The American journal of pathology.

[112]  L. Mucke,et al.  Amyloid-beta / Fyn – Induced Synaptic , Network , and Cognitive Impairments Depend on Tau Levels in Multiple Mouse Models of Alzheimer ’ s Disease , 2015 .

[113]  Bradley T. Hyman,et al.  Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease , 1992, Neurology.

[114]  W. K. Cullen,et al.  Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo , 2002, Nature.

[115]  M. Vitek,et al.  Tau is essential to beta -amyloid-induced neurotoxicity. , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[116]  C. Rowe,et al.  Amyloid β deposition, neurodegeneration, and cognitive decline in sporadic Alzheimer's disease: a prospective cohort study , 2013, The Lancet Neurology.

[117]  Jürgen Götz,et al.  Dendritic Function of Tau Mediates Amyloid-β Toxicity in Alzheimer's Disease Mouse Models , 2010, Cell.

[118]  K. Sleegers,et al.  APP duplication is sufficient to cause early onset Alzheimer's dementia with cerebral amyloid angiopathy. , 2006, Brain : a journal of neurology.

[119]  B. de Strooper,et al.  The mechanism of γ-Secretase dysfunction in familial Alzheimer disease , 2012, The EMBO journal.

[120]  E. Tangalos,et al.  Neuropathologic features of amnestic mild cognitive impairment. , 2006, Archives of neurology.

[121]  Yasuyoshi Watanabe,et al.  A new amyloid β variant favoring oligomerization in Alzheimer's‐type dementia , 2008, Annals of neurology.

[122]  A. Dillin,et al.  Aging as an event of proteostasis collapse. , 2011, Cold Spring Harbor perspectives in biology.

[123]  D. Holtzman,et al.  Apolipoprotein E in Alzheimer's disease and other neurological disorders , 2011, The Lancet Neurology.

[124]  A. Fagan,et al.  Variation in MAPT is associated with cerebrospinal fluid tau levels in the presence of amyloid-beta deposition , 2008, Proceedings of the National Academy of Sciences.

[125]  J Q Trojanowski,et al.  Lewy bodies contain altered alpha-synuclein in brains of many familial Alzheimer's disease patients with mutations in presenilin and amyloid precursor protein genes. , 1998, The American journal of pathology.

[126]  L. Mucke,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. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[127]  David A Bennett,et al.  Brain amyloid-β oligomers in ageing and Alzheimer's disease. , 2013, Brain : a journal of neurology.

[128]  H. Vinters,et al.  β-Amyloid Oligomers Induce Phosphorylation of Tau and Inactivation of Insulin Receptor Substrate via c-Jun N-Terminal Kinase Signaling: Suppression by Omega-3 Fatty Acids and Curcumin , 2009, The Journal of Neuroscience.

[129]  Christine Van Broeckhoven,et al.  Genetic insights in Alzheimer's disease , 2013, The Lancet Neurology.

[130]  Virginia M. Y. Lee,et al.  Increased Lipid Peroxidation Precedes Amyloid Plaque Formation in an Animal Model of Alzheimer Amyloidosis , 2001, The Journal of Neuroscience.

[131]  R. Neve,et al.  Impairments in learning and memory accompanied by neurodegeneration in mice transgenic for the carboxyl-terminus of the amyloid precursor protein. , 1999, Brain research. Molecular brain research.

[132]  C. Rowe,et al.  Longitudinal assessment of Aβ and cognition in aging and Alzheimer disease , 2011, Annals of neurology.

[133]  Ole A. Andreassen,et al.  A mutation in APP protects against Alzheimer’s disease and age-related cognitive decline , 2012, Nature.

[134]  C. Glabe,et al.  Soluble fibrillar oligomer levels are elevated in Alzheimer's disease brain and correlate with cognitive dysfunction , 2009, Neurobiology of Disease.

[135]  A. Fagan,et al.  APOE predicts amyloid‐beta but not tau Alzheimer pathology in cognitively normal aging , 2010, Annals of neurology.

[136]  C. Jack,et al.  Evidence for ordering of Alzheimer disease biomarkers. , 2011, Archives of neurology.

[137]  M. Weiner,et al.  Smoking and increased Alzheimer's disease risk: A review of potential mechanisms , 2014, Alzheimer's & Dementia.

[138]  J. Hardy,et al.  A new pathogenic mutation in the APP gene (I716V) increases the relative proportion of A beta 42(43). , 1997, Human molecular genetics.

[139]  J. Gunter,et al.  Short-term clinical outcomes for stages of NIA-AA preclinical Alzheimer disease , 2012, Neurology.

[140]  S. Pimplikar,et al.  The γ-secretase-cleaved C-terminal fragment of amyloid precursor protein mediates signaling to the nucleus , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[141]  C. Rowe,et al.  Accelerated cortical atrophy in cognitively normal elderly with high β-amyloid deposition , 2012, Neurology.

[142]  M. Pasparakis,et al.  IKKβ Deficiency in Myeloid Cells Ameliorates Alzheimer's Disease-Related Symptoms and Pathology , 2014, The Journal of Neuroscience.

[143]  J. Trojanowski,et al.  Initiation and Synergistic Fibrillization of Tau and Alpha-Synuclein , 2003, Science.

[144]  David M Holtzman,et al.  Human Apoe Isoforms Differentially Regulate Brain Amyloid-β Peptide Clearance Nih Public Access , 2022 .

[145]  M. Gallagher,et al.  A specific amyloid-β protein assembly in the brain impairs memory , 2006, Nature.

[146]  J. Morris,et al.  Decreased Clearance of CNS β-Amyloid in Alzheimer’s Disease , 2010, Science.

[147]  Michael Weiner,et al.  Effect of apolipoprotein E on biomarkers of amyloid load and neuronal pathology in Alzheimer disease , 2009, Annals of neurology.