The preclinical phase of the pathological process underlying sporadic Alzheimer's disease

Brain

Volumn 138, Issue 10, 2015, Pages 2814-2833

  Braak, Heiko ^a   Del Tredici, Kelly ^a  

^a UNIVERSITY OF ULM   (Germany)

Author keywords

Alzheimer's disease; amyloid protein; evolutionary medicine; tau protein; transentorhinal entorhinal cortex

Indexed keywords

AMYLOID BETA PROTEIN; TAU PROTEIN;

ALZHEIMER DISEASE; ARTICLE; BASAL GANGLION; BRAIN CORTEX; BRAIN CORTEX LESION; CONFORMATIONAL TRANSITION; ENTORHINAL CORTEX; EXECUTIVE FUNCTION; HIPPOCAMPUS; HUMAN; LOCUS CERULEUS; MYELIN SHEATH; NERVE ENDING; PHYLOGENY; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PSYCHOLOGICAL ADJUSTMENT; TRIGEMINAL NUCLEUS; TRIGEMINUS GANGLION; AGE; ANIMAL; BRAIN; DISEASE COURSE; METABOLISM; PATHOLOGY;

AGE FACTORS; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; BRAIN; DISEASE PROGRESSION; HUMANS; TAU PROTEINS;

EID: 84952898119     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awv236     Document Type: Article

References (224)

1. Agnati LF, Bjelke B, Fuxe K. Volume versus wiring transmission in the brain: a new theoretical frame of neuropsychopharmacology. Med Res Rev 1995; 15: 33-45.
2. Ahmed Z, Cooper J, Murray TK, Garn K, McNaughton E, Clark H, et al. A novel in vivo model of tau propagation with rapid and progressive neurofibrillary tangle pathology: the pattern of spread is determined by connectivity, not proximity. Acta Neuropathol 2014; 127: 667-83.
3. Alafuzoff I, Thal DR, Arzberger T, Bogdanovic N, Al-Sarraj S, Bodi I, et al. Assessment of beta-amyloid deposits in human brain: a study of the BrainNet Europe Consortium. Acta Neuropathol 2009; 117: 309-20.
4. Albert MS, Dekosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, et al. The diagnosis of mild cognitive impairment due to Alzheimers disease: recommendations from the National Institute on Aging- Alzheimers association workgroups on diagnostic guidelines for Alzheimers disease. Alzheimers Dement 2011; 7: 270-9.
5. Alonso AC, Li B, Grundke-Iqbal I, Iqbal K. Mechanism of tau-induced neurodegeneration in Alzheimer disease and related tauopathies. Curr Alzheimer Res 2008; 5: 375-84.
6. Amunts K, Zilles K. Advances in cytoarchitectonic mapping of the human cerebral cortex. Neuroimaging Clin N Am 2001; 11: 151-69.
7. Amunts K, Kedo O, Kindler M, Pieperhoff P, Mohlberg H, Shah NJ, et al. Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps. Anat Embryol 2005; 210: 343-52.
8. Anderton BH, Callahan L, Coleman P, Davies P, Flood D, Jicha GA, et al. Dendritic changes in Alzheimers disease and factors that may underlie these changes. Prog Neurobiol 1998; 55: 595-609.
9. Arendt T. Alzheimers disease as a loss of differentiation control in a subset of neurons that retain immature features in the adult brain. Neurobiol Aging 2000; 21: 783-96.
10. Arendt T, Bruckner MK, Gertz HJ, Marcova L. Cortical distribution of neurofibrillary tangles in Alzheimers disease matches the pattern of neurones that retain their capacity of plastic remodelling in the adult brain. Neuroscience 1998; 83: 991-1002.
11. Arendt T, Bruckner MK, Morawski M, Jager C, Gertz HJ. Early neurone loss in Alzheimers disease: cortical or subcortical? Acta Neuropathol Comm 2015a; 3: 10.
12. Arendt T, Stieler J, Holzer M. Brain hypometabolism triggers PHF-like phosphorylation of tau, a major hallmark of Alzheimers disease pathology. J Neural Transm 2015b; 122: 531-9.
13. Arnold SE, Hyman BT, Flory J, Damasio AR, Van HoesenGW. The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimers disease. Cereb Cortex 1991; 1: 103-16.
14. Arnold SE, Lee EB, Moberg PJ, Stutzbach L, Kazi H, Han LY, et al. Olfactory epithelium amyloid-beta and PHF tau pathology in Alzheimers disease. Ann Neurol 2010; 67: 462-9.
15. Aston-Jones C, Cohen JD. An integrative theory of locus coeruleusnorepinephrine function: adaptive gain and optimal performance. Ann Rev Neurosci 2005; 28: 403-50.
16. Attems J, Jellinger K, Thal DR, Van Nostrand W. Review: sporadic cerebral amyloid angiopathy. Neuropathol Appl Neurobiol 2011; 37: 75-93.
17. Attems J, Thal DR, Jellinger K. The relationship between subcortical tau pathology and Alzheimers disease. Biochem Soc Trans 2012; 40: 711-5.
18. Ball MJ. Limbic predilection in Alzheimers dementia: is reactivated herpesvirus involved? Can J Neurol Sci 1982; 9: 303-6.
19. Ball MJ. Unexplained sudden amnesia, postencephalitic Parkinson disease, subacute sclerosing panencephalitis, and Alzheimer disease: does viral synergy produce neurofibrillary tangles? Arch Neurol 2003; 60: 641-2.
20. Ball MJ, Lukiw WJ, Kammerman EM, Hill JM. Intracerebral propagation of Alzheimers disease: strengthening evidence of a herpes simplex virus etiology. Alzheimers Dement 2013; 9: 169-75.
21. Ballatore C, Lee VMY, Trojanowski JQ. Tau-mediated neurodegeneration in Alzheimers disease and related disorders. Nature Rev Neurosci 2007; 8: 663-72.
22. Bancher C, Brunner C, Lassmann H, Budka H, Jellinger K, Wiche G, et al. Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles in Alzheimers disease. Brain Res 1989; 477: 90-9.
23. Bannister AP. Inter- and intra-laminar connections of pyramidal cells in the neocortex. Neurosci Res 2005; 53: 95-103.
24. Barbas H. Specialized elements of orbitofrontal cortex in primates. Ann NY Acad Sci 2007; 1121: 10-32.
25. Barbas H, Rempel-Clower N. Cortical structure predicts the pattern of corticocortical connections. Cereb Cortex 1997; 7: 635-46.
26. Barnett EM, Cassell MD, Perlman D. Two neurotropic viruses, herpes simplex virus type 1 and mouse hepatitis virus, spread along different neural pathways from the main olfactory bulb. Neurosci 1993; 57: 1007-25.
27. Bartzokis G. Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimers disease. Neurobiol Aging 2004; 25: 5-18.
28. Barulli D, Stern Y. Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn Sci 2013; 17: 502-9.
29. Becker Y. HSV-1 brain infection by the olfactory nerve route and virus latency and reactivation may cause learning and behavioral deficiencies and violence in children and adults: a point of view. Virus Genes 1995; 10: 217-26.
30. Beekes M, Thomzig A, Schulz-Schaeffer WJ, Burger R. Is there a risk of prion-like disease transmission by Alzheimer- or Parkinson-associated protein particles? Acta Neuropathol 2014; 128: 463-76.
31. Benarroch EE. The central autonomic network: functional organization, dysfunction, and perspective. Mayo Clin Proc 1993; 68: 988-1001.
32. Benarroch EE. The locus ceruleus norepinephrine system. Functional organization and potential clinical significance. Neurology 2009; 17: 1699-1704.
33. Benarroch EE. Neocortical interneurons. Functional diversity and clinical correlations. Am Acad Neurol 2013; 81: 273-80.
34. Bengtsson SL, Nagy Z, Skare S, Forsman L, Forssberg H, Ullen F. Extensive piano practicing has regionally specific effects on white matter development. Nat Neurosci 2005; 8: 1148-50.
35. Braak E, Braak H, Mandelkow EM. A sequence of cytoskeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol 1994; 87: 554-67.
36. Braak H. Architectonics of the human telencephalic cortex. Berlin: Springer; 1980. p. 1-NNN.
37. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991; 82: 239-59.
38. Braak H, Braak E. The human entorhinal cortex: normal morphology and lamina-specific pathology in various diseases. Neurosci Res 1992; 15: 6-31.
39. Braak H, Braak E. Development of Alzheimer-related neurofibrillary changes in the neocortex inversely recapitulates cortical myelogenesis. Acta Neuropathol 1996; 92: 97-101.
40. Braak H, Braak E. Frequency of stages of Alzheimer-related lesions in different age categories. Neurobiol Aging 1997; 18: 351-7.
41. Braak H, Del Tredici K. Poor and protracted myelination as a contributory factor to neurodegenerative disorders. Neurobiol Aging 2004; 25: 19-23.
42. Braak H, Del Tredici K. The pathological process underlying Alzheimers disease in individuals under thirty. Acta Neuropathol 2011a; 121: 171-81.
43. Braak H, Del Tredici K. Alzheimers pathogenesis: is there neuron-toneuron propagation? Acta Neuropathol 2011b; 121: 589-95.
44. Braak H, Del Tredici K. Where, when, and in what form does sporadic Alzheimers disease begin? Curr Opin Neurol 2012a; 25: 708-14.
45. Braak H, Del Tredici K. Evolutional aspects of Alzheimers disease pathogenesis. J Alzheimer Dis 2012b; 30: 1-7.
46. Braak H, Del Tredici K. Alzheimers disease: pathogenesis and prevention. Alzheimers Dement 2012c; 8: 227-33.
47. Braak H, Del Tredici K. Amyloid-b may be released from non-junctional varicosities of axons generated from abnormal tau-containing brainstem nuclei in sporadic Alzheimers disease: a hypothesis. Acta Neuropathol 2013; 126: 303-6.
48. Braak H, Del Tredici K. Are cases with tau pathology occurring in the absence of Ab deposits part of the AD-related pathological process?. Acta Neuropathol 2014; 128: 767-72.
49. Braak H, Del Tredici K. Neuroanatomy and pathology of sporadic Alzheimers disease. Adv Anat Embryol Cell Biol 2015a; 215: 1-162.
50. Braak H, Del Tredici K. Potential pathways of abnormal tau and-- synuclein dissemination in sporadic Alzheimers and Parkinsons diseases. Cold Spring Harb Perspect Biol 2015b. doi: 10.1101/ CSHPERSPECT.a023630.
51. Braak H, Braak E, Yilmazer D, Bohl J. Functional anatomy of human hippocampal formation and related structures. J Child Neurol 1996; 11: 265-75.
52. Braak H, Thal DR, Ghebremedhin E, Del Tredici K. Stages of the pathologic process in Alzheimer disease: age categories from 1 to 100 years. J Neuropathol Exp Neurol 2011; 70: 960-9.
53. Brookmeyer R, Johnson E, Ziegler-Graham K, Arrighi HM. Forecasting the global burden of Alzheimers disease. Alzheimers Dement 2007; 3: 186-91.
54. Brundin P, Melki R, Kopito R. Prion-like transmission of protein aggregates in neurodegenerative diseases. Nat Rev Mol Cell Biol 2010; 11: 301-7.
55. Bulic B, Pickhardt M, Mandelkow EM, Mandelkow E. Tau protein and tau aggregation inhibitors. Neuropharmacol 2010; 59: 276-89.
56. Busch C, Bohl J, Ohm TG. Spatial, temporal and numeric analysis of Alzheimer changes in the nucleus coeruleus. Neurobiol Aging 1997; 18: 401-6.
57. Buxbaum JD, Thinakaran G, Koliatsos V, OCallahan J, Slunt HH, Price DL, et al. Alzheimer amyloid protein precursor in the rat hippocampus: transport and processing through the perforant path. J Neurosci 1998; 18: 9629-37.
58. Calafate S, Buist A, Miskiewicz K, Vijayan V, Daneels G, de Strooper B, et al. Synaptic contacts enhance cell-to-cell tau pathology propagation. Cell Reports 2015; 11: 1-8.
59. Chalermpalanupap T, Kinkead B, Hu WT, Kummer MP, Hammerschidt T, Heneka MT, et al. Targeting norepinephrine in mild cognitive impairment and Alzheimers disease. Alzheimers Res Ther 2013; 5: 21.
60. Chetelat G Alzheimer disease: Ab-independent processes - rethinking preclinical AD. Nat Rev Neurol 2013; 9: 123-4.
61. Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, Probst A, et al. Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 2009; 11: 909-13.
62. Clavaguera F, Akatsu H, Fraser G, Crowther RA, Frank S, Hench J, et al. Brain homogenates from human tauopathies induce tau inclusions in mouse brain. Proc Natl Acad Sci USA 2013a; 110: 9535-40.
63. Clavaguera F, Lavenir I, Falcon B, Frank S, Goedert M, Tolnay M. Prion-like templated misfolding in tauopathies. Brain Pathol 2013b; 23: 342-9.
64. Clavaguera F, Grueninger F, Tolnay M. Intercellular transfer of tau aggregates and spreading of tau pathology: implications for therapeutic strategies. Neuropharmacology 2014; 76: Pt A: 9-15. doi:10.1016.
65. Cohen ML, Kim C, Haldiman T, ElHag M, Mehndiratta P, Pichet T, et al. Rapidly progressive Alzheimers disease features distinct structures of amyloid-b. Brain 2015; 138: 1009-22.
66. Coleman PD, Flood DG. Neuron numbers and dendritic extent in normal aging and Alzheimers disease. Neurobiol Aging 1987; 8: 521-45.
67. Cowan CM, Bossing T, Page A, Shepherd D, Mudher A. Soluble hyper-phosphorylated tau causes microtubule breakdown and functionally compromises normal tau in vivo. Acta Neuropathol 2010; 120: 593-604.
68. Crary J, Trojanowski JQ, Schneider JA, Abisambra JF, Abner EL, Alafuzoff I, et al. Primary age-related tauopathy (PART): a common pathology associated with human aging. Acta Neuropathol 2014; 128: 755-66.
69. Curcio CA, Kemper T. Nucleus raphe dorsalis in dementia of the Alzheimer type: neurofibrillary changes and neuronal packing density. J Neuropathol Exp Neurol 1984; 43: 359-68.
70. de Calignon A, Polydoro M, Sua rez-Calvet M, William C, Adamowicz DH, Kopeikina KJ, et al. Propagation of tau pathology in a model of early Alzheimers disease. Neuron 2012; 73: 685-97.
71. Delbeuck X, van der Linden M, Collette F. Alzheimers disease as a disconnection syndrome? Neuropsychol Rev 2003; 13: 79-92.
72. Deruelle MJ, Favoreel HW. Keep it in the subfamily: the conserved alphaherpesvirus US3 protein kinase. J Gen Virol 2011; 92: 18-30.
73. Dong S, Duan Y, Hu Y, Zhao Z. Advances in the pathogenesis of Alzheimers disease: a re-evaluation of amyloid cascade hypothesis. Transl Neurodegener 2012; 1: 1-18.
74. Draganski B, May A. Training-induced structural changes in the adult human brain. Behav Brain Res 2008; 192: 137-42.
75. Dringenberg HC. Alzheimers disease: more than a cholinergic disorder- evidence that cholinergic-monoaminergic interactions contribute to EEG slowing and dementia. Behav Brain Res 2000; 115: 236-49.
76. Dugger BL, Hidalgo JA, Chiarolanza G, Mariner M, Henry-Watson J, Sue LI, et al. The distribution of phosphorylated tau in the spinal cords of Alzheimers disease and non-demented individuals. J Alzheimers Dis 2013; 34: 529-36.
77. Dujardin S, Lecolle K, Caillierez R, Begard S, Zommer N, Lachaud C, et al. Neuron-to-neuron wild-type Tau protein transfer through a trans-synaptic mechanism: relevance to sporadic tauopathies. Acta Neuropathol Commun 2014; 2: 1-14.
78. Duyckaerts C. Tau pathology in children and young adults: can you still be unconditionally baptist? Acta Neuropathol 2011; 121: 145-7.
79. Duyckaerts C. Neurodegenerative lesions: seeding and spreading. Rev Neurol 2013; 169: 825-33.
80. Duyckaerts C, Delatour B, Potier MC. Classification and basic pathology of Alzheimers disease. Acta Neuropathol 2009; 118: 5-36.
81. Duyckaerts C, Braak H, Brion J-P, Buee L, Del Tredici K, Goedert M, et al. PART is part of Alzheimer disease. Acta Neuropathol 2015; 129: 749-56.
82. Elobeid A, Soininen H, Alafuzoff I. Hyperphosphorylated tau in young and middle-aged subjects. Acta Neuropathol 2011; 123: 97-104.
83. Erickson KI, Weinstein AM, Lopez OL. Physical activity, brain plasticity, and Alzheimer disease. Arch Med Res 2012; 43: 615-21.
84. Falcon B, Cavallini A, Angers R, Glover S, Murray TK, Barnham L, et al. Conformation determines the seeding potencies of native and recombinant tau aggregates. J Biol Chem 2015; 290: 1049-65.
85. Ferrer I. Defining Alzheimer as a common age-related neurodegenerative process not inevitably leading to dementia. Prog Neurobiol 2012; 97: 38-51.
86. Fewster PH, Griffin-Brooks S, MacGregor J, Ojalvo-Rose E, Ball MJ. A topographical pathway by which histopathological lesions disseminate through the brain of patients with Alzheimers disease. Dementia 1991; 2: 121-32.
87. Fiala JC. Mechanisms of amyloid plaque pathogenesis. Acta Neuropathol 2007; 114: 551-71.
88. Fields RD. Imaging learning: the search for a memory trace. Neuroscientist 2011; 17: 185-96.
89. Freedman M, Alladi S, Chertkow H, Bialystok E, Craik FI, Phillips NA, et al. Delaying onset of dementia: are two languages enough? Behav Neurol 2014; 2014: 808137.
90. Frost B, Diamond MI. Prion-like mechanisms in neurodegenerative diseases. Nat Rev Neurosci 2010; 11: 155-9.
91. Frost B, Jacks RL, Diamond MI. Propagation of tau misfolding from the outside to the inside of a cell. J Biol Chem 2009; 284: 12845-52.
92. Gallyas F. Silver staining of Alzheimers neurofibrillary changes by means of physical development. Acta Morph Acad Sci Hung 1971; 19: 1-8.
93. Gartner H, Minnerop M, Pieperhoff P, Schleicher A, Zilles K, Altenmuller E, et al. Brain morphometry shows effects of longterm musical practice in middle-aged keyboard players. Front Psychol 2013; 4: 636.
94. German DC, White CL, Sparkman DR. Alzheimers disease: Neurofibrillary tangles in nuclei that project to the cerebral cortex. Neurosci 1987; 21: 305-12.
95. German DC, Manaye KF, White CL 3rd, Woodward DJ, McIntire DD, Smith WK, et al. Disease-specific patterns of locus coeruleus cell loss. Ann Neurol 1992; 32: 667-76.
96. Goedert M, Spillantini MG. A century of Alzheimers disease. Science 2006; 314: 777-81.
97. Goedert M, Klug A, Crowther RA. Tau protein, the paired helical filament and Alzheimers disease. J Alzheimers Dis 2006; 9(Suppl 3): 195-207.
98. Goedert M, Clavaguera F, Tolnay M. The propagation of prion-like protein inclusions in neurodegenerative diseases. Trends Neurosci 2010; 33: 317-25.
99. Goedert M, Falcon B, Clavaguera F, Tolnay M. Prion-like mechanisms in the pathogenesis of tauopathies and synucleinopathies. Curr Neurol Neurosci Rep 2014; 14: 495.
100. Graham I, Atara D, Borch-Johnsen K, Boysend G, Burelle G, Cifkovaf R, et al., European guidelines on cardiovascular disease prevention in clinical practice: full text. Fourth Joint Task Force of the European Society of Cardiology and other societies on cardiovascular disease prevention in clinical practice (constituted by representatives of nine societies and by invited experts). Eur J Cardiovas Prev Rehabil 2007; 14 (Suppl 2) :S1-113.
101. Grinberg LT, Rub U, Ferretti RE, Nitrini R, Farfel JM, Polichiso L, et al. The dorsal raphe nucleus shows phospho-tau neurofibrillary changes before the transentorhinal region in Alzheimers disease. A precocious onset? Neuropathol Appl Neurobiol 2009; 35: 406-16.
102. Grudzien A, Shaw P, Weintraub S, Bigio E, Mash DC, Mesulam MM. Locus coeruleus neurofibrillary degeneration in aging, mild cognitive impairment and early Alzheimers disease. Neurobiol Aging 2007; 28: 327-35.
103. Guo JL, Lee VM. Seeding of normal tau by pathological tau conformers drives pathogenesis of Alzheimer-like tangles. J Biol Chem 2011; 286: 15317-31.
104. Guo JL, Lee VM. Neurofibrillary tangle-like tau pathology induced by synthetic tau fibrils in primary neurons over-expressing mutant tau. FEBS Lett 2013; 587: 717-23.
105. Haass C, Kaether C, Thinakaran G, Sisodia S. Trafficking and proteolytic processing of APP. Cold Spring Harb Perspect Med 2012; 2: a006270.
106. Hafting T, Fyhn M, Molden S, Moser M-B, Moser IE. Microstructure of a spatial map in the entorhinal cortex. Nature 2005; 436: 801-6.
107. Haglund M, Sjobeck M, Englund E. Locus ceruleus degeneration is ubiquitous in Alzheimers disease: possible implications for diagnosis and treatment. Neuropathology 2006; 26: 528-32.
108. Henkins KM, Sokolow S, Miller CA, Vinters HV, Poon WW, Cornwall LB, et al. Extensive p-tau pathology and SDS-stable ptau oligomers in Alzheimers cortical synapses. Brain Pathol 2012; 22: 826-33.
109. Heimer L, de Olmos J, Alheid GF, Zaborsky L. Perestroika in the basal forebrain: opening the border between neurology and psychiatry. Progr Brain Res 1991; 87: 109-65.
110. Herrup K, Yang Y. Cell cycle regulation in the postmitotic neuron: oxymoron or new biology? Nat Rev Neurosci 2007; 8: 368-78.
111. Holmes BB, Furman, JL, Mahan, TE, Yamasaki TR, Mirbaha H, Eades WC, et al. Proteopathic tau seeding predicts tauopathy in vivo. Proc Natl Acad Sci USA 2014; 111: E4376-85.
112. Hyman BT, Go mez-Isla T. Alzheimers is a laminar, regional, and neural system specific disease, not a global brain disease. Neurobiol Aging 1994; 15: 353-4.
113. Iba M, McBride JD, Guo JL, Zhang B, Trojanowski JQ, Lee VMY. Tau pathology spread in PS19 tau transgenic mice following locus coeruleus (LC) injections of synthetic tau fibrils is determined by the LCs afferent and efferent connections. Acta Neuropathol 2015; doi: 10.1007/s00401-015-1458-4.
114. Ichimiya Y, Arai H, Kosaka K, Iizuka R. Morphological and biochemical changes in the cholinergic and monoaminergic systems in Alzheimer-type dementia. Acta Neuropathol 1986; 70: 112-6.
115. Iqbal K, Grundke-Iqbal I. Alzheimer neurofibrillary degeneration: significance, etiopathogenesis, therapeutics and prevention. J Cell Mol Med 2008; 12: 38-55.
116. Iqbal K, Grundke-Iqbal I. Opportunities and challenges in developing Alzheimer disease therapeutics. Acta Neuropathol 2011; 122: 543-9.
117. Iqbal K, Liu F, Gong CX, Alonso C, Grundke-Iqbal I. Mechanisms of tau-induced neurodegeneration. Acta Neuropathol 2009; 118: 53-69.
118. Ittner A, Ke JD, van Eersel J, Gladbach A, Gotz J, Ittner LM. Brief update on different roles of tau in neurodegeneration. IUBMB Life 2011; 63: 495-502.
119. Itzhaki RF. Herpes simplex virus type 1 and Alzheimers disease: increasing evidence for a major role of the virus. Front Aging Neurosci 2014; 6: 202.
120. Itzhaki RF, Liu WR, Shang D, Wilcock GK, Faragher B, Jamieson GA. Herpes simplex virus type 1 in brain and risk of Alzheimers disease. Lancet 1997; 349: 241-4.
121. Itzhaki RF, Liu WR, Wilcock GK, Faragher B. HSV-1 and risk of Alzheimers disease. Lancet 1998; 352: 238.
122. Itzhaki RF, Wozniak MA. Alzheimers disease and infection: Do infectious agents contribute to progression of Alzheimers disease? Alzheimers Dement 2010; 6: 83-4.
123. Jamieson GA, Maitland NJ, Wilcock GK, Craske J, Itzhaki RF. Latent herpes simplex virus type 1 in normal and Alzheimers disease brains. J Med Virol 1991; 33: 224-7.
124. Jucker M, Walker LC. Pathogenic protein seeding in Alzheimers disease and other neurodegenerative disorders. Ann Neurol 2011; 70: 532-40.
125. Kemper TL. Neuroanatomical and neuropathological changes in normal aging and in dementia. In: Albert, ML editor. Clinical neurology of aging. New York: Oxford University Press; 1984. p. 9-52.
126. Kopke E, Tung YC, Shaikh S, Alonso AC, Iqbal K, Grundke-Iqbal I. Microtubule-associated protein tau. Abnormal phosphorylation of a non-paired helical filament pool in Alzheimers disease. J Biol Chem 1993; 268: 24374-84.
127. Koo EH, Sisodia SS, Archer DR, Martin LJ, Weidemann A, Beyreuther K, et al. Precursor of amyloid protein in Alzheimer disease undergoes fast axonal transport. Proc Natl Acad Sci USA 1990; 87: 1561-65.
128. Kopelkina KJ, Hyman BT, Spires-Jones TL. Soluble forms of tau are toxic in Alzheimers disease. Transl Neurosci 2012; 3: 223-33.
129. Kovacech B, Skrabana R, Novak M. Transition of tau protein from disordered to misordered in Alzheimers disease. Neurodegener Dis 2010; 7: 24-7.
130. Lee SJ, Lim HS, Masliah E, Lee HJ. Protein aggregate spreading in neurodegenerative disease: problems and perspectives. Neurosci Res 2011; 70: 339-48.
131. Li B, Chohan MO, Grundke-Iqbal I, Iqbal K. Disruption of microtubule network by Alzheimer abnormally hyperphosphorylated tau. Acta Neuropathol 2007; 113: 501-11.
132. Liu L, Drouet V, Wu JW, Witter MP, Smith SA Clelland C, et al. Trans-synaptic spread of tau pathology in vivo. PLoS One 2012; 7: e31302.
133. Lyness SA, Zarow C, Chui HC. Neuron loss in key cholinergic and aminergic nuclei in Alzheimer disease: a meta-analysis. Neurobiol Aging 2003; 24: 1-23.
134. Maarouf CL, Daugs ID, Kokjohn TA, Kalback WM, Patton RL, Luehrs DC, et al. The biochemical aftermath of anti-amyloid immunotherapy. Mol Neurodegen 2010; 5: 39.
135. Maeda S, Sahara N, Saito Y, Murayama M, Yoshiiike Y, Kim H, et al. Granular tau oligomers as intermediates of tau filaments. Biochemistry 2007; 46: 3856-61.
136. Mandelkow EM, Mandelkow E. Biochemistry and cell biology of tau protein in neurofibrillary degeneration. Cold Spring Harb Perspect Med 2012; 2: a006247.
137. Mandelkow EM, Thies E, Biernat J, Mandelkow E. Influence of tau on neuronal traffic mechanisms. In: Jucker M, Beyreuther K, Haass C, Nitsch R, Christen Y, editors. Alzheimer: 100 years and beyond. Berlin, Heidelberg: Springer; 2006. p. 345-54.
138. Mandelkow E, von Bergen M, Biernat J, Mandelkow E. Structural principles of tau and the paired helical filaments of Alzheimers disease. Brain Pathol 2007; 17: 83-90.
139. Mann DM, Lincoln J, Yates PO, Stamp JE, Toper S. Changes in the monoamine containing neurones of the human CNS in senile dementia. Br J Psychiatry 1980; 136: 533-41.
140. Marcyniuk B, Mann DM, Yates PO. The topography of cell loss from locus coeruleus in Alzheimers disease. J Neurol Sci 1986a: 76: 335-45.
141. Marcyniuk B, Mann DM, Yates PO. Loss of nerve cells from locus coeruleus in Alzheimers disease is topographically arranged. Neurosci Lett 1986b; 64: 247-52.
142. Marien MR, Colpaert FC, Rosenquist AC. Noradrenergic mechanisms in neurodegenerative diseases: a theory. Brain Res Brains Res Rev 2004; 45: 38-78.
143. Masters CL, Selkoe DJ. Biochemistry of amyloid b-protein and amyloid deposits in Alzheimers disease. Cold Spring Harb Perspect Med 2012; 2: a006262.
144. Matsuo ES, Shin RW, Billingsley ML, Van deVoorde A, OConnor M, Trojanowski JQ, et al. Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimers disease paired helical filament tau. Neuron 1994; 13: 989-1002.
145. Matsuzawa Y, Lerman A. Endothelial dysfunction and coronary artery disease: assessment, prognosis, and treatment. Coron Artery Dis 2014; 25: 713-24.
146. Mayeux R, Stern Y. Epidemiology of Alzheimers disease. Cold Spring Harb Persp Med 2012; 2: pii:a006239.
147. McLean JH, Shipley MT, Bernstein DI, Corbett D. Selective lesions of neural pathways following viral inoculation of the olfactory bulb. Exp Neurol 1993; 122: 209-22.
148. McMillan PJ, White SS, Franklin A, Greenup JL, Leverenz JB, Raskind MA, et al. Differential response of the central noradrenergic nervous system to the loss of locus coeruleus neurons in Parkinsons disease and Alzheimers disease. Brain Pathol 2011; 1373: 240-52.
149. Meng X, DArcy C. Education and dementia in the context of the cognitive reserve hypothesis: a systematic review with meta-analyses and quantitative analyses. PLoS One 2012; 7: e38268.
150. Mercken M, Vandermeeren M, Lubke U, et al. Monoclonal antibodies with selective specifity for Alzheimer Tau are directed against phosphatase- sensitive epitopes. Acta Neuropathol 1992; 84: 265-72.
151. Mesulam MM. The cholinergic innervation of the human cerebral cortex. Progr Brain Res 2004; 145: 67-78.
152. Mesulam MM, Shaw P, Mash D, Weintraub S. Cholinergic nucleus basalis tauopathy emerges early in the aging-MCI-AD continuum. Ann Neurol 2004; 55: 815-28.
153. Mirbaha H, Holmes BB, Sanders DW, Bieschke J, Diamond MI. Tau trimers are the minimal propagation unit spontaneously internalized to seed intracellar aggregation. J Biol Chem 2015; 290: 14893-903.
154. Molnar FJ, Man-Son-Hing M, Fergusson D. Systematic review of measures of clinical significance employed in randomized controlled trials of drugs for dementia. J Am Geriatr Soc 2009; 57: 536-46.
155. Montine TJ, Phelps CH, Beach TG, Bigio EH, Cairns NJ, Carrillo MC, et al. National Institute on Aging-Alzheimers Association guidelines for the neuropathologic assessment of Alzheimers disease: a practical approach. Acta Neuropathol 2012; 123: 1-11.
156. Moreno-Trevino MG, Castillo-Lo pez J, Meester I. Moving away from amyloid beta to move on in Alzheimer research. Front Aging Neurosci 2015; 7: 1-4.
157. Morsch R, Simon W, Coleman PD. Neurons may live for decades with neurofibrillary tangles. J Neuropathol Exp Neurol 1999; 58: 188-97.
158. Moser EI, Moser M-B. Grid cells and neural coding in high-end cortices. Neuron 2013; 80: 765-774.
159. Moser EI, Roudi Y, Witter MP, Kentros C, Bonhoeffer T, Moser M-B. Grid cells and cortical representation. Nat Rev Neurosci 2014; 15: 466-81.
160. Muresan Z, Muresan V. Seeding neuritic plaques from the distance: a possible role for brainstem neurons in the development of Alzheimers disease pathology. Neurodeg Dis 2008; 5: 250-53.
161. Nelson PT, Alafuzoff I, Bigio EH, Bouras C, Braak H, Cairns NJ, et al. Correlation of Alzheimers disease neuropathologic changes with cognitive status: a review of the literature. J Neuropathol Exp Neurol 2012; 71: 362-81.
162. Nieuwenhuys R. Comparative aspects of volume transmission, with sidelight on other forms of intercellular communication. Prog. Brain Res 2000; 125: 49-126.
163. ODonnell J, Zeppenfeld D, McConnell E, Pena S, Nedergaard M. Norepinephrine: a neuromodulator that boosts the function of multiple cell types to optimize CNS performance. Neurochem Res 2012; 37: 2496-512.
164. Parvizi J, Van Hoesen GW, Damasio A. The selective vulnerability of brainstem nuclei to Alzheimers disease. Ann Neurol 2001; 49: 53-66.
165. Paus T, Collins DL, Evans AC, Leonard G, Pike B, Zijdenbos A. Maturation of white matter in the human brain: a review of magnetic resonance studies. Brain Res Bull 2001; 54: 255-66.
166. Pearson RCA. Cortical connections and the pathology of Alzheimers disease. Neurodegeneration 1996; 5: 429-34.
167. Petro C, Gonzales PA, Cheshenko N, Jandl T, Khajoueinejad N, Benard A, et al. Herpes simplex type 2 virus deleted in glycoprotein D protects against vaginal, skin and neural disease. eLife 2015; 4: e06054.
168. Pimplikar SW. Reassessing the amyloid cascade hypothesis of Alzheimers disease. Int J Biochem Cell Biol 2009; 41: 1261-68.
169. Pooler AM, Polydoro M, Wegmann S, Nicholls SB, Spires-Jones TL, Hyman BT. Propagation of tau pathology in Alzheimers disease: identification of novel therapeutic targets. Alzheimers Res Thera 2013; 5: 49.
170. Prusiner SB. Cell Biology. A unifying role for prions in neurodegenerative disease. Science 2012; 336: 1511-13.
171. Rapoport SI. Brain evolution and Alzheimers disease. Rev Neurol 1988; 144: 79-90.
172. Rapoport SI. Integrated phylogeny of the primate brain, with special reference to humans and their diseases. Brain Res Rev 1990; 15: 267-94.
173. Rapoport SI. How did the human brain evolve? A proposal based on new evidence from in vivo imaging during attention and ideation. Brain Res Bull 1999; 50: 149-65.
174. Rapoport SI, Nelson PT. Biomarkers and evolution in Alzheimers disease. Prog Neurobiol 2011; 95: 510-13.
175. Reid AT, Evans AC. Structural networks in Alzheimers disease. Eur Neuropsychopharmacol 2013; 23: 63-77.
176. Reisberg B, Franssen EH, Hasan SM, Monteiro I, Boksay I, Souren LE, et al. Retrogenesis: clinical, physiologic, and pathologic mechanisms in brain aging, Alzheimers and other dementing processes. Eur Arch Psychiatry Clin Neurosci 1999; 249 (Suppl 3): 28-36.
177. Reisberg B, Franssen EH, Souren LE, Auer SR, Akram I, Kenowsky S. Evidence and mechanisms of retrogenesis in Alzheimers and other dementias: management and treatment import. Am J Alzheimers Dis Other Demen 2002; 17: 202-12.
178. Rockland KS, Pandya DN. Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res 1979; 179: 3-20.
179. Run X, Liang Z, Zhang L, Iqbal K, Grundke-Iqbal I, Gong CX. Anesthesia induces phosphorylation of tau. J Alzheimer Dis 2009; 16: 619-29.
180. Sabbagh MN, Cooper K, DeLange J, Stoehr JD, Thind K, Lahti T, et al. Functional, global and cognitive decline correlates to accumulation of Alzheimers pathology in MCI and AD. Curr Alzheimer Res 2010; 7: 280-86.
181. Sanders DW, Kaufman SK, DeVos SL, Shama AM, Mirbaha H, Li A, et al. Distinct tau prion strains propagate in cells and mice and define different tauopathies. Neuron 2014; 82: 1271-88.
182. Saper CB, Wainer BH, German DC. Axonal and transneuronal transport in the transmission of neurological disease: potential role in system degenerations, including Alzheimers disease. Neuroscience 1987; 23: 389-98.
183. Sara SJ. The locus coeruleus and noradrenergic modulation of cognition. Nat Rev Neurosci 2009; 10: 211-23.
184. Sassin I, Schultz C, Thal DR, Rub U, Arai K, Braak E, et al. Evolution of Alzheimers disease-related cytoskeletal changes in the basal nucleus of Meynert. Acta Neuropathol 2000; 100: 259-69.
185. Schlaug G, Norton A, Overy K, Winner E. Effects of music training on the childs brain and cognitive development. Ann N Y Acad Sci 2005; 1060: 219-30.
186. Schliebs R, Arendt T. The cholinergic system in aging and neuronal degeneration. Behav Brain Res 2011; 221: 555-63.
187. Schonheit B, Zarski R, Ohm TG. Spatial and temporal relationships between plaques and tangles in Alzheimer-pathology. Neurobiol Aging 2004; 25: 697-711.
188. Selkoe D, Mandelkow E, Holtzman D. Deciphering Alzheimer disease. Cold Spring Harb Perspect Med 2012; 2: 1-8.
189. Simic G, Stanic G, Mladinov M, Jovanov-Milosevic N, Kostovic I, Hof PR. Does Alzheimers disease begin in the brainstem? Neuropathol Appl Neurobiol 2009; 35: 532-54.
190. Smith CY, Bailey KR, Emerson JA, Nemetz PN, Roger VL, Palumbo PJ, et al. Contributions of increasing obesity and diabetes show decline in subclinical coronary artery disease. J Am Heart Assoc 2015; 4: e001524. doi. 10.1161/JAHA.114.001524.
191. Spillantini MG, Goedert M. Tau pathology and neurodegeneration. Lancet Neurol 2013; 12: 609-622.
192. Stern Y. Cognitive reserve. Neuropsychologia 2009; 47: 2015-28.
193. Stokin GB, Goldstein LSB. Axonal transport and Alzheimers disease. Ann Rev Biochem 2006; 75: 607-27.
194. Struble RG, Cork LC, Whitehouse PJ, Price DL. Cholinergic innervation in neuritic plaques. Science 1982; 216: 413-15.
195. Struble RG, Price DL, Cork LC, Price DL. Senile plaques in cortex of aged normal monkeys. Brain Res 1985; 361: 267-75.
196. Sydow A, Mandelkow EM. Prion-like propagation of mouse and human tau aggregates in an inducible mouse model of tauopathy. Neurodegener Dis 2010; 7: 28-31.
197. Thal DR, Rub U, Schultz C, Sassin I, Ghebremedhin E, Del Tredici K, et al. Sequence of Ab-protein deposition in the human medial temporal lobe. J Neuropathol Exp Neurol 2000; 59: 733-48.
198. Thal DR, Rub U, Orantes M, Braak H. Phases of Ab-deposition in the human brain and its relevance for the development of AD. Neurology 2002; 58: 1791-1800.
199. Thies E, Mandelkow EM. Missorting of tau in neurons causes degeneration of synapses that can be rescued by the kinase MARK2/Par-1. J Neurosci 2007; 27: 2896-907.
200. Tomlinson BE, Irving D, Blessed G. Cell loss in the locus coeruleus in senile dementia of Alzheimer type. J Neurol Sci 1981; 49: 419-28.
201. Trillo L, Das D, Hsieh W, Medina B. Moghadam S, Lin B, et al. Ascending monominergic system alterations in Alzheimers disease, translating basic science into clinical care. Neurosci Biobehav Rev 2013; 8: 1363-79.
202. Uchihara T. Silver diagnosis in neuropathology: principles, practice and revised interpretation. Acta Neuropathol 2007; 113: 483-99.
203. Uchihara T. Expanding morphological dimensions in neuropathology, from sequence biology to pathological sequences and clinical consequences. Neuropathology 2011; 31: 201-7.
204. Uchihara T, Nakamura A, Yamazaki M, Mori O. Evolution from pretangle neurons to neurofibrillary tangles monitored by thiazin red combined with Gallyas method and double immunofluorescence. Acta Neuropathol 2001a; 101: 535-9.
205. Uchihara T, Nakamura A, Yamazaki M, Mori O, Ikeda K, Tsuchiya K. Different conformation of neuronal tau deposits distinguished by double immunofluorescence with AT8 and thiazin red combined with Gallyas method. Acta Neuropathol 2001b; 102: 462-6.
206. Ullen F. Is activity regulation of late myelination a plastic mechanism in the human nervous system? Neuron Glia Biol 2009; 5: 29-34.
207. van der Knaap MS, Valk J, Bakker CJ, Schooneveld M, Faber JA, Willemse J, et al. Myelination as an expression of the functional maturity of the brain. Dev Med Child Neurol 1991; 33: 849-57.
208. Velasco ME, Smith MA, Siedlak SI, Nunomura A, Perry G. Striation is the characteristic neuritic abnormality in Alzheimer disease. Brain Res 1998; 813: 329-33.
209. von Bergen M, Barghorn S, Biernat J, Mandelkow EM, Mandelkow E. Tau aggregation is driven by a transition from random coil to beta sheet structure. Biochim Biophys Acta 2005; 1739: 158-66.
210. Vinters HV. Cerebral amyloid angiopathy and Alzheimers disease: two entities or one? J Neurol Sci 1992; 112: 1-3.
211. Walker LC, Diamond MI, Duff KE, Hyman BT. Mechanisms of protein seeding in neurodegenerative diseases. JAMA Neurol 2013; 70: 304-10.
212. Weaver CL, Espinoza M, Kress Y, Davies P. Conformational change as one of the earliest alterations of tau in Alzheimers disease. Neurobiol Aging 2000; 21: 719-27.
213. Weinshenker D. Functional consequences of locus coeruleus degeneration in Alzheimers disease. Curr Alzheimer Res 2008; 5: 342-45.
214. Wisner TW, Sugimoto K, Howard PW, Kawaguchi Y, Johnson DC. Anterograde transport of herpes simplex virus capsids in neurons by both separate and married mechanisms. J Virol 2011; 85: 5919-28.
215. Wollen KA. Alzheimers disease: the pros and cons of pharmaceutical, nutritional, botanical, and stimulatory therapies, with a discussion of treatment strategies from the perspective of patients and practitioners. Altern Med Rev 2010; 15: 223-4.
216. Wozniak MA, Frost AL, Itzhaki RF. Alzheimers disease-specific tau phosphorylation is induced by herpes simplex virus type 1. J Alzheimers Dis 2009a; 16: 341-50.
217. Wozniak MA, Mee AP, Itzhaki RF. Herpes simplex virus type 1 DNA is located within Alzheimers disease amyloid plaques. J Pathol 2009b; 217: 131-8.
218. Wozniak MA, Itzhaki RF. Antiviral agents in Alzheimers disease: hope for the future?. Ther Adv Neurol Disord 2010; 3: 141-52.
219. Wu JW, Herman M, Liu I, Simoes S, Acker CM, Figueroa H, et al. Small misfolded tau species are internalized via bulk endocytosis and anterogradely and retrogradely transported in neurons. J Biol Chem 2013; 288: 1856-70.
220. Xu W, Yu JT, Tan MS, Tan L. Cognitive reserve and Alzheimers disease. Mol Neurobiol 2015; 1: 187-208.
221. Yaffe K, Tocco M, Petersen RC, Sigler C, Burns LC, Cornelius C, et al. The epidemiology of Alzheimers disease: laying the foundation for drug design, conduct, and analysis of clinical trials. Alzheimers Dement 2012; 8: 237-42.
222. Yu Y, Run X, Liang Z, Li Y, Liu Y, Iqbal K, et al. Developmental regulation of tau phosphorylation, tau kinases, and tau phosphatases. J Neurochem 2009; 108: 1480-94.
223. Zilles K, Amunts K. Centenary of Brodmanns map - conception and fate. Nat Rev Neurosci 2010; 11: 139-45.
224. Zweig RM, Ross CA, Hedreen JC, Steele C, Cardillo JF, Whitehouse PJ, et al. Neuropathology of aminergic nuclei in Alzheimers disease. Prog Clin Biol Res 1989; 317: 353-65.