Alzheimer's pathogenesis: Is there neuron-to-neuron propagation?

Acta Neuropathologica

Volumn 121, Issue 5, 2011, Pages 589-595

  Braak, Heiko ^a   Del Tredici, Kelly ^a  

^a UNIVERSITY OF ULM   (Germany)

Author keywords

Alzheimer's disease; Amyloid ; Locus coeruleus; Microtubules; Pretangles; Prion diseases; Protein misfolding; Staging; Tau

Indexed keywords

AMYLOID BETA PROTEIN; TAU PROTEIN;

AGING; ALZHEIMER DISEASE; DISEASE ASSOCIATION; DISEASE CLASSIFICATION; GENE LOSS; HUMAN; IMMUNOREACTIVITY; NEUROPATHOLOGY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVIEW; SYNAPTIC TRANSMISSION;

ALZHEIMER DISEASE; DISEASE PROGRESSION; HUMANS; NEURONS; PRION DISEASES; TAU PROTEINS;

EID: 79958110883     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-011-0825-z     Document Type: Review

References (79)

1. Aguzzi A, Rajendran L (2009) The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 64:783-790
2. Alafuzoff I, Arzberger T, Al-Sarraj S et al (2008) Staging of neurofibrillary pathology in Alzheimer's disease: a study for the Brain Net Europe Consortium. Brain Pathol 18:484-496
3. Alonso AC, Li B, Grundke-Iqbal I, Iqbal K (2008) Mechanism of tau-induced neurodegeneration in Alzheimer disease and related tauopathies. Curr Alzheimer Res 5:375-384
4. Amieva H, Le Goff M, Millet X et al (2008) Prodromal Alzheimer's disease: successive emergence of clinical symptoms. Ann Neurol 64:492-498
5. Angot E, Steiner JA, Hansen C, Brundin P (2010) Are synucleinopathies prion-like disorders? Lancet Neurol 9:1128-1138
6. Arnold SE, Hyman BT, Flory J et al (1991) The topographical and neuroanatomical distribution of neurofibrillary tangles and neuritic plaques in the cerebral cortex of patients with Alzheimer's disease. Cerebr Cortex 1:103-116
7. Ballatore C, Lee VM, Trojanowski JQ (2007) Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nat Rev Neurosci 8:663-672 (Pubitemid 47283144)
8. Benarroch EE (2009) The locus coeruleus norepinephrine system. Neurology 73:1699-1704
9. Bobinski M, Wegiel J, Tarnawski M et al (1998) Duration of neurofibrillary changes in the hippocampal pyramidal neurons. Brain Res 799:156-158 (Pubitemid 28351215)
10. Braak H, Braak E (1991) Neuropathological staging of Alzheimer- related changes. Acta Neuropathol 82:239-259
11. Braak H, Braak E (1997) Frequency of stages of Alzheimerrelated lesions in different age categories. Neurobiol Aging 18:351-357 (Pubitemid 27435070)
12. Braak E, Braak H, Mandelkow EM (1994) A sequence of cyto-skeleton changes related to the formation of neurofibrillary tangles and neuropil threads. Acta Neuropathol 87:554-567 (Pubitemid 24158408)
13. Braak H, Del Tredici K (2004) Alzheimer's disease: intraneuronal alterations precede insoluble amyloid-β formation. Neurobiol Aging 25:713-718 (Pubitemid 38698242)
14. Braak H, Del Tredici K (2011) The pathological process under-lying Alzheimer's disease in individuals under thirty. Acta Neuropathol 121:171-181
15. Brundin P, Melki R, Kopito R (2010) Prion-like transmission of protein aggregates in neurodegenerative diseases. Nat Rev Mol Cell Biol 11:301-307
16. Buée L, Bussiere T, Buée-Scherrer V et al (2003) Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Rev 33:95-130
17. Clavaguera F, Bolmont T, Crowther RA et al (2009) Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 11:909-913
18. Cowan CM, Bossing T, Page A et al (2010) Soluble hyper-phosphorylated tau causes microtubule breakdown and functionally compromises normal tau in vivo. Acta Neuropathol 120:593-604
19. Cramer SC, Chopp M (2000) Recovery recapitulates ontogeny. Trends Neurosci 23:265-271 (Pubitemid 30331113)
20. Davis DM, Sowinski S (2008) Membrane nanotubes: dynamic long-distance connections between animal cells. Nat Rev Mol Cell Biol 9:431-436 (Pubitemid 351733399)
21. DeLacoste MC, White CL (1993) The role of cortical connectivity in Alzheimer's disease pathogenesis: a review and model system. Neurobiol Aging 14:1-16
22. Deramecourt V, Lebert F, Debachy B, Mackowiak-Cordoliani MA, Bombois S, Kerdraon O, Buée L, Maurage CA, Pasquier F (2010) Prediction of pathology in primary progressive language and speech disorders. Neurology 74:42-49
23. Desplats P, Lee H-J, Bae E-J et al (2009) Inclusion formation and neuronal cell death through neuron-to-neuron transmission of α-synuclein. PNAS 106:13010-13015
24. Dickson DW, Braak H, Duda JE et al (2009) Neuropathological assessment of Parkinson's disease: refining the diagnostic criteria. Lancet Neurol 8:1150-1157
25. Duyckaerts C, Hauw JJ (1997) Prevalence, incidence and duration of Braak's stages in the general population: can we know? Neurobiol Aging 18:362-369
26. Frautschy SA, Cole GM (2010) Why pleiotropic interventions are needed for Alzheimer's disease. Mol Neurobiol 41:392-409
27. Frost B, Diamond MI (2010) The expanding realm of prion phenomena in neurodegenerative disease. Prion 3:74-77
28. Frost B, Jacks RL, Diamond MI (2009) Propagation of tau misfolding from the outside to the inside of a cell. J Biol Chem 284:12845-12852
29. Frost B, Ollesch J, Wille H, Diamond MI (2009) Conformational diversity of wild-type tau fibrils specified by templated conformation change. J Biol Chem 284:3546-3551
30. German DC, Manaye KF, White CL 3rd (1992) Disease-specific patterns of locus coeruleus cell loss. Ann Neurol 32:667-676
31. Goedert M, Jakes R, Vandermeeren E (1995) Monoclonal antibody AT8 recognizes tau protein phosphorylated at serine 202 and threonine 205. Neurosci Lett 189:167-170
32. Goedert M, Clavaguera F, Tolnay M (2010) The propagation of prion-like protein inclusions in neurodegenerative diseases. Trends Neurosci 33:317-325
33. Goedert M, Klug A, Crowther RA (2006) Tau protein, the paired helical filament and Alzheimer's disease. J Alzheimers Dis 9:195-207 (Pubitemid 44253313)
34. Gousset K, Zurzolo C (2008) Tunnelling nanotubes: a highway for prion spreading? Prion 3:94-98
35. Grinberg LT, Rüb U, Ferretti RE et al (2009) The dorsal raphe nucleus shows phospho-tau neurofibrillary changes before the transentorhinal region in Alzheimer's disease. A precocious onset? Neuropathol Appl Neurobiol 35:406-416
36. Grudzien A, Shaw P, Weintraub S et al (2007) Locus coeruleus neurofibrillary degeneration in aging, mild cognitive impairment and early Alzheimer's disease. Neurobiol Aging 28:327-335 (Pubitemid 46178530)
37. Guo JL, Lee VM (2011) Seeding of normal tau by pathological tau conformers drives pathogenesis of Alzheimer-like tangles. J Biol Chem. doi:10.1074/jbc.M110.209296
38. Haglund M, Sjöbeck M, Englund E (2006) Locus ceruleus degeneration is ubiquitous in Alzheimer's disease: possible implications for diagnosis and treatment. Neuropathology 26:528-532 (Pubitemid 44800288)
39. Hansen C, Angot E, Bergström A-L et al (2011) α-Synuclein propagates from mouse brain to grafted dopaminergic neurons and seeds aggregation in cultured human cells. J Clin Invest 121:715-725
40. Hardy J, Allsop D (1991) Amyloid deposition as the central event in the aetiology of Alzheimer's disease. Trends Pharmacol Sci 12:383-388
41. Hardy JA, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297:353-356
42. Hyman BT (1998) New pathological criteria for Alzheimer's disease. Arch Neurol 55:1174-1176
43. Iqbal K, Liu F, Gong CX et al (2009) Mechanisms of tau-induced neurodegeneration. Acta Neuropathol 118:53-69
44. Kertesz A, McMonagle P, Blair M, Davidson W, Munoz DG (2005) The evolution and pathology of frontotemporal dementia. Brain 128:1996-2005 (Pubitemid 41253267)
45. Klein WL, Stine WB Jr, Teplow DB (2004) Small assemblies of unmodified amyloid beta-protein are the proximate neurotoxin in Alzheimer's disease. Neurobiol Aging 25:569-580 (Pubitemid 38686476)
46. Kovacech B, Skrabana R, Novak M (2010) Transition of tau protein from disordered to misordered in Alzheimer's disease. Neurodegen Dis 7:24-27
47. Li B, Chohan MO, Grundke-Iqbal I, Iqbal K (2007) Disruption of microtubule network by Alzheimer abnormally hyperphosphorylated tau. Acta Neuropathol 113:501-511 (Pubitemid 46672596)
48. Li S, Shankar GM, Selkoe DJ (2010) How do soluble oligomers of amyloid beta-protein impair hippocampal synaptic plasticity? Front Cell Neurosci 4:5
49. Lyness SA, Zarow C, Chui HC (2003) Neuron loss in key cholinergic and aminergic nuclei in Alzheimer's disease: a meta-analysis. Neurobiol Aging 24:1-23 (Pubitemid 35454140)
50. Mackenzie IRA, Neumann M, Bigio EH, Dickson DW et al (2010) Nomenclature and nosology for neuropathologic subtypes of frontotemporal lobar degeneration: an update. Acta Neuropathol 119:1-4
51. Mandelkow E, von Bergen M, Biernat J, Mandelkow EM (2007) Structural principles of tau and the paired helical filaments of Alzheimer's disease. Brain Pathol 17:83-90
52. Mattson MP (2006) Molecular and cellular pathways towards and away from Alzheimer's disease. In: Jucker M, Beyreuther K, Haass C, Nitsch R, Christen Y (eds) Alzheimer: 100 years and beyond. Springer, Berlin, pp 371-378
53. Mattsson N, Sävman K, Osterlundh G et al (2010) Converging molecular pathways in human and neural development and degeneration. Neurosci Res 66:330-332
54. Mesulam MM (1998) From sensation to cognition. Brain 121:1013-1052
55. Moceri VM, Kukull WA, Emanuel I et al (2000) Early-life risk factors and the development of Alzheimer's disease. Neurology 54:415-420 (Pubitemid 30078075)
56. Morsch R, Simon W, Coleman PD (1999) Neurons may live for decades with neurofibrillary tangles. J Neuropathol Exp Neurol 58:188-197 (Pubitemid 29088942)
57. Neumann M (2009) Molecular neuropathology of TDP-43 proteinopathies. Int J Mol Sci 10:232-246
58. Olanow CW, Prusiner SB (2009) Is Parkinson's disease a prion disorder? Proc Natl Acad Sci USA 106:12571-12572
59. Pan-Montojo F, Anichtchik O, Dening Y et al (2010) Progression of Parkinson's disease pathology is reproduced by intragastric administration of rotenone in mice. PLoS One 5:38762
60. Parvizi J, Van Hoesen GW, Damasio A (2001) The selective vulnerability of brainstem nuclei to Alzheimer's disease. Ann Neurol 49:53-66 (Pubitemid 32163006)
61. Pearson RCA (1996) Cortical connections and the pathology of Alzheimer's disease. Neurodegeneration 5:429-434
62. Pimplikar SW (2009) Reassessing the amyloid cascade hypothesis of Alzheimer's disease. Int J Biochem Cell Biol 41:1261-1268
63. Rockland KS, Pandya DN (1979) Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res 179:3-20 (Pubitemid 10196213)
64. Saper CB, Wainer BH, German DC (1987) Axonal and transneuronal transport in the transmission of neurological disease: potential role in system degenerations, including Alzheimer's disease. Neuroscience 23:389-398 (Pubitemid 18004218)
65. Sara SJ (2009) The locus coeruleus and noradrenergic modulation of cognition. Nat Rev Neurosci 10:211-223
66. Schönheit B, Zarski R, Ohm TG (2004) Spatial and temporal relationships between plaques and tangles in Alzheimer-pathology. Neurobiol Aging 25:697-711 (Pubitemid 38698241)
67. Selkoe DJ (1994) Alzheimer's disease: a central role for amyloid. J Neuropathol Exp Neurol 53:438-447
68. Simic G, Stanic G, Mladinov M et al (2009) Does Alzheimer's disease begin in the brainstem? Neuropathol Appl Neurobiol 35:532-554
69. Simons M, Raposo G (2009) Exosomes: vesicular carriers for intercellular communication. Curr Opin Cell Biol 21:575-581
70. Spires-Johnes TL, Stoothoff WH, de Calignon A et al (2009) Tau pathophysiology in neurodegeneration: a tangled issue. Trends Neurosci 32:150-159
71. Stamer K, Vogel R, Thies E et al (2002) Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J Cell Biol 156:1051-1063 (Pubitemid 34839854)
72. Teter B, Ashford JW (2002) Neuroplasticity in Alzheimer's disease. J Neurosci Res 70:402-437 (Pubitemid 35222379)
73. Thal DR, Rüb U, Orantes M, Braak H (2002) Phases of Aβ-deposition in the human brain and its relevance for the development of AD. Neurology 58:1791-1800 (Pubitemid 34663580)
74. Tsermentseli S, Leigh PN, Goldstein LH (2011) The anatomy of cognitive impairment in amyotrophic lateral sclerosis: More than frontal lobe dysfunction. Cortex (Epub ahead of print)
75. Von Bartheld CS, Altick AL (2011) Multivesicular bodies in neurons: distribution, protein content, and trafficking functions. Prog Neurobiol 93:313-340
76. Wegorzewska I, Bell S, Cairns NJ, Miller TM, Baloh RH (2009) TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration. Proc Natl Acad Sci USA 106:18809-18814
77. Wilson AC, Dugger BN, Dickson DW, Wang DS (2011) TDP-43 in aging and Alzheimer's disease-a review. Int J Clin Exp Pathol 4:147-155
78. Wirths O, Multhaup G, Bayer TA (2004) A modified β-amyloid hypothesis: intraneuronal accumulation of the β-amyloid peptide-the first step of a fatal cascade. J Neurochem 91:513-520
79. Zarow C, Lyness SA, Mortimer JA, Chui HC (2003) Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases. Arch Neurol 60:337-341 (Pubitemid 36314358)