Pathological Interface between Oligomeric Alpha-Synuclein and Tau in Synucleinopathies

Biological Psychiatry

Volumn 78, Issue 10, 2015, Pages 672-683

  Sengupta, Urmi ^a,b   Guerrero Muñoz, Marcos J ^a,b   Castillo Carranza, Diana L ^a,b   Lasagna Reeves, Cristian A ^a   Gerson, Julia E ^a,b   Paulucci Holthauzen, Adriana A ^a,b   Krishnamurthy, Shashirekha ^a,b   Farhed, Malika ^a,b   Jackson, George R ^a,b   Kayed, Rakez ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

Author keywords

Co aggregation; Hybrid oligomers; Interaction; Synucleinopathy; Tau oligomers; Synuclein oligomers

Indexed keywords

ALPHA SYNUCLEIN; F8H7 ANTIBODY; MONOCLONAL ANTIBODY; OLIGOMER; SYN33 ANTIBODY; TAU PROTEIN; UNCLASSIFIED DRUG; ANTIBODY; MAPT PROTEIN, HUMAN;

AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; BRAIN BIOCHEMISTRY; BRAIN TISSUE; CLINICAL ARTICLE; CONTROLLED STUDY; DIFFUSE LEWY BODY DISEASE; HUMAN; HUMAN TISSUE; HYBRID; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FRONTAL LOBE; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; MALE; METABOLISM; MIDDLE AGED; NERVE CELL; PATHOLOGY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALPHA-SYNUCLEIN; ANTIBODIES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FRONTAL LOBE; HUMANS; IMMUNOHISTOCHEMISTRY; LEWY BODY DISEASE; MALE; MIDDLE AGED; NEURONS; PARKINSON DISEASE; TAU PROTEINS;

EID: 84940894409     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2014.12.019     Document Type: Article

References (72)

1. M.G. Spillantini, R.A. Crowther, R. Jakes, M. Hasegawa, and M. Goedert alpha-Synuclein in filamentous inclusions of Lewy bodies from Parkinsons disease and dementia with lewy bodies Proc Natl Acad Sci U S A 95 1998 6469 6473
2. L.S. Forno Neuropathology of Parkinsons disease J Neuropathol Exp Neurol 55 1996 259 272
3. S. Engelender Ubiquitination of alpha-synuclein and autophagy in Parkinsons disease Autophagy 4 2008 372 374
4. V.N. Uversky Neuropathology, biochemistry, and biophysics of alpha-synuclein aggregation J Neurochem 103 2007 17 37
5. M.G. Spillantini, M.L. Schmidt, V.M. Lee, J.Q. Trojanowski, R. Jakes, and M. Goedert Alpha-synuclein in Lewy bodies Nature 388 1997 839 840
6. F. Cheng, G. Vivacqua, and S. Yu The role of alpha-synuclein in neurotransmission and synaptic plasticity J Chem Neuroanat 42 2011 242 248
7. T. Rahkonen, U. Eloniemi-Sulkava, S. Rissanen, A. Vatanen, P. Viramo, and R. Sulkava Dementia with Lewy bodies according to the consensus criteria in a general population aged 75 years or older J Neurol Neurosurg Psychiatry 74 2003 720 724
8. R.E. Mrak, and W.S. Griffin Dementia with Lewy bodies: Definition, diagnosis, and pathogenic relationship to Alzheimers disease Neuropsychiatr Dis Treat 3 2007 619 625
9. T. Ziemssen, and H. Reichmann Non-motor dysfunction in Parkinsons disease Parkinsonism Relat Disord 13 2007 323 332
10. A.E. Lang, and A.M. Lozano Parkinsons disease. First of two parts N Engl J Med 339 1998 1044 1053
11. J.G. Goldman, C. Williams-Gray, R.A. Barker, J.E. Duda, and J.E. Galvin The spectrum of cognitive impairment in Lewy body diseases Mov Disord 29 2014 608 621
12. M. Periquet, T. Fulga, L. Myllykangas, M.G. Schlossmacher, and M.B. Feany Aggregated alpha-synuclein mediates dopaminergic neurotoxicity in vivo J Neurosci 27 2007 3338 3346
13. S. Chandra, G. Gallardo, R. Fernandez-Chacon, O.M. Schluter, and T.C. Sudhof Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration Cell 123 2005 383 396
14. H. Fujiwara, M. Hasegawa, N. Dohmae, A. Kawashima, E. Masliah, M.S. Goldberg, and et al. alpha-Synuclein is phosphorylated in synucleinopathy lesions Nat Cell Biol 4 2002 160 164
15. L. Chen, and M.B. Feany Alpha-synuclein phosphorylation controls neurotoxicity and inclusion formation in a Drosophila model of Parkinson disease Nat Neurosci 8 2005 657 663
16. W. Li, N. West, E. Colla, O. Pletnikova, J.C. Troncoso, L. Marsh, and et al. Aggregation promoting C-terminal truncation of alpha-synuclein is a normal cellular process and is enhanced by the familial Parkinsons disease-linked mutations Proc Natl Acad Sci U S A 102 2005 2162 2167
17. B.I. Giasson, J.E. Duda, I.V. Murray, Q. Chen, J.M. Souza, H.I. Hurtig, and et al. Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions Science 290 2000 985 989
18. J.E. Duda, V.M. Lee, and J.Q. Trojanowski Neuropathology of synuclein aggregates J Neurosci Res 61 2000 121 127
19. K.M. Danzer, D. Haasen, A.R. Karow, S. Moussaud, M. Habeck, A. Giese, and et al. Different species of alpha-synuclein oligomers induce calcium influx and seeding J Neurosci 27 2007 9220 9232
20. P.O. Fernagut, and M.F. Chesselet Alpha-synuclein and transgenic mouse models Neurobiol Dis 17 2004 123 130
21. C. Ballatore, V.M. Lee, and J.Q. Trojanowski Tau-mediated neurodegeneration in Alzheimers disease and related disorders Nat Rev Neurosci 8 2007 663 672
22. B. Zhang, M. Higuchi, Y. Yoshiyama, T. Ishihara, M.S. Forman, D. Martinez, and et al. Retarded axonal transport of R406W mutant tau in transgenic mice with a neurodegenerative tauopathy J Neurosci 24 2004 4657 4667
23. K.R. Brunden, J.Q. Trojanowski, and V.M. Lee Evidence that non-fibrillar tau causes pathology linked to neurodegeneration and behavioral impairments J Alzheimers Dis 14 2008 393 399
24. A. Bretteville, and E. Planel Tau aggregates: Toxic, inert, or protective species? J Alzheimers Dis 14 2008 431 436
25. K.H. Ashe A tale about tau N Engl J Med 357 2007 933 935
26. K. Santacruz, J. Lewis, T. Spires, J. Paulson, L. Kotilinek, M. Ingelsson, and et al. Tau suppression in a neurodegenerative mouse model improves memory function Science 309 2005 476 481
27. Z. Berger, H. Roder, A. Hanna, A. Carlson, V. Rangachari, M. Yue, and et al. Accumulation of pathological tau species and memory loss in a conditional model of tauopathy J Neurosci 27 2007 3650 3662
28. D.L. Castillo-Carranza, C.A. Lasagna-Reeves, and R. Kayed Tau aggregates as immunotherapeutic targets Front Biosci (Schol Ed) 5 2013 426 438
29. E.E. Congdon, and K.E. Duff Is tau aggregation toxic or protective? J Alzheimers Dis 14 2008 453 457
30. C.A. Lasagna-Reeves, D.L. Castillo-Carranza, U. Sengupta, A.L. Clos, G.R. Jackson, and R. Kayed Tau oligomers impair memory and induce synaptic and mitochondrial dysfunction in wild-type mice Mol Neurodegener 6 2011 39
31. C. Ullrich, N. Daschil, and C. Humpel Organotypic vibrosections: Novel whole sagittal brain cultures J Neurosci Methods 201 2011 131 141
32. S. Gispert, D. Del Turco, L. Garrett, A. Chen, D.J. Bernard, J. Hamm-Clement, and et al. Transgenic mice expressing mutant A53T human alpha-synuclein show neuronal dysfunction in the absence of aggregate formation Mol Cell Neurosci 24 2003 419 429
33. E. Tsika, M. Moysidou, J. Guo, M. Cushman, P. Gannon, R. Sandaltzopoulos, and et al. Distinct region-specific alpha-synuclein oligomers in A53T transgenic mice: Implications for neurodegeneration J Neurosci 30 2010 3409 3418
34. K.M. Danzer, S.K. Krebs, M. Wolff, G. Birk, and B. Hengerer Seeding induced by alpha-synuclein oligomers provides evidence for spreading of alpha-synuclein pathology J Neurochem 111 2009 192 203
35. R. Kayed, E. Head, J.L. Thompson, T.M. McIntire, S.C. Milton, C.W. Cotman, and C.G. Glabe Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis Science 300 2003 486 489
36. D.M. Walsh, I. Klyubin, J.V. Fadeeva, W.K. Cullen, R. Anwyl, M.S. Wolfe, and et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo Nature 416 2002 535 539
37. K.A. Lewis, A. Yaeger, G.N. DeMartino, and P.J. Thomas Accelerated formation of alpha-synuclein oligomers by concerted action of the 20S proteasome and familial Parkinson mutations J Bioenerg Biomembr 42 2010 85 95
38. C.A. Lasagna-Reeves, U. Sengupta, D. Castillo-Carranza, J.E. Gerson, M. Guerrero-Munoz, J.C. Troncoso, and et al. The formation of tau pore-like structures is prevalent and cell specific: Possible implications for the disease phenotypes Acta Neuropathol Commun 2 2014 56
39. L.K. Clinton, M. Blurton-Jones, K. Myczek, J.Q. Trojanowski, and F.M. LaFerla Synergistic interactions between abeta, tau, and alpha-synuclein: Acceleration of neuropathology and cognitive decline J Neurosci 30 2002 7281 7289
40. C.A. Lasagna-Reeves, D.L. Castillo-Carranza, M.J. Guerrero-Muoz, G.R. Jackson, and R. Kayed Preparation and characterization of neurotoxic tau oligomers Biochemistry 49 2010 10039 10041
41. J. Simon-Sanchez, C. Schulte, J.M. Bras, M. Sharma, J.R. Gibbs, D. Berg, and et al. Genome-wide association study reveals genetic risk underlying Parkinsons disease Nat Genet 41 2009 1308 1312
42. E.A. Waxman, and B.I. Giasson Induction of intracellular tau aggregation is promoted by alpha-synuclein seeds and provides novel insights into the hyperphosphorylation of tau J Neurosci 31 2011 7604 7618
43. P.H. Jensen, H. Hager, M.S. Nielsen, P. Hojrup, J. Gliemann, and R. Jakes Alpha-synuclein binds to tau and stimulates the protein kinase A-catalyzed tau phosphorylation of serine residues 262 and 356 J Biol Chem 274 1999 25481 25489
44. E. Iseki, N. Takayama, W. Marui, K. Ueda, and K. Kosaka Relationship in the formation process between neurofibrillary tangles and Lewy bodies in the hippocampus of dementia with Lewy bodies brains J Neurol Sci 195 2002 85 91
45. M. Colom-Cadena, E. Gelpi, S. Charif, O. Belbin, R. Blesa, M.J. Marti, and et al. Confluence of alpha-synuclein, tau, and beta-amyloid pathologies in dementia with Lewy bodies J Neuropathol Exp Neurol 72 2013 1203 1212
46. J.L. Guo, D.J. Covell, J.P. Daniels, M. Iba, A. Stieber, B. Zhang, and et al. Distinct alpha-synuclein strains differentially promote tau inclusions in neurons Cell 154 2013 103 117
47. B.I. Giasson, M.S. Forman, M. Higuchi, L.I. Golbe, C.L. Graves, P.T. Kotzbauer, and et al. Initiation and synergistic fibrillization of tau and alpha-synuclein Science 300 2003 636 640
48. C.A. Lasagna-Reeves, D.L. Castillo-Carranza, U. Sengupta, J. Sarmiento, J. Troncoso, G.R. Jackson, and R. Kayed Identification of oligomers at early stages of tau aggregation in Alzheimers disease FASEB J 26 2012 1946 1959
49. A. Der-Sarkissian, C.C. Jao, J. Chen, and R. Langen Structural organization of alpha-synuclein fibrils studied by site-directed spin labeling J Biol Chem 278 2003 37530 37535
50. M. Margittai, and R. Langen Template-assisted filament growth by parallel stacking of tau Proc Natl Acad Sci U S A 101 2004 10278 10283
51. R. Kayed, Y. Sokolov, B. Edmonds, T.M. McIntire, S.C. Milton, J.E. Hall, and C.G. Glabe Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases J Biol Chem 279 2004 46363 46366
52. N. Sergeant, A. Wattez, and A. Delacourte Neurofibrillary degeneration in progressive supranuclear palsy and corticobasal degeneration: Tau pathologies with exclusively "exon 10" isoforms J Neurochem 72 1999 1243 1249
53. N. Sergeant, J.P. David, D. Lefranc, P. Vermersch, A. Wattez, and A. Delacourte Different distribution of phosphorylated tau protein isoforms in Alzheimers and Picks diseases FEBS Lett 412 1997 578 582
54. M.J. Park, S.M. Cheon, H.R. Bae, S.H. Kim, and J.W. Kim Elevated levels of alpha-synuclein oligomer in the cerebrospinal fluid of drug-naive patients with Parkinsons disease J Clin Neurol 7 2011 215 222
55. O.M. El-Agnaf, S.A. Salem, K.E. Paleologou, M.D. Curran, M.J. Gibson, J.A. Court, and et al. Detection of oligomeric forms of alpha-synuclein protein in human plasma as a potential biomarker for Parkinsons disease FASEB J 20 2006 419 425
56. V. Duka, J.H. Lee, J. Credle, J. Wills, A. Oaks, C. Smolinsky, and et al. Identification of the sites of tau hyperphosphorylation and activation of tau kinases in synucleinopathies and Alzheimers diseases PLoS One 8 2013 e75025
57. J. Biernat, and E.M. Mandelkow The development of cell processes induced by tau protein requires phosphorylation of serine 262 and 356 in the repeat domain and is inhibited by phosphorylation in the proline-rich domains Mol Biol Cell 10 1999 727 740
58. M. Goedert, R. Jakes, and E. Vanmechelen Monoclonal antibody AT8 recognises tau protein phosphorylated at both serine 202 and threonine 205 Neurosci Lett 189 1995 167 169
59. H. Braak, D.R. Thal, E. Ghebremedhin, and K. Del Tredici Stages of the pathologic process in Alzheimer disease: Age categories from 1 to 100 years J Neuropathol Exp Neurol 70 2011 960 969
60. K.R. Patterson, C. Remmers, Y. Fu, S. Brooker, N.M. Kanaan, L. Vana, and et al. Characterization of prefibrillar Tau oligomers in vitro and in Alzheimer disease J Biol Chem 286 2011 23063 23076
61. C.A. Lasagna-Reeves, D.L. Castillo-Carranza, U. Sengupta, M.J. Guerrero-Munoz, T. Kiritoshi, V. Neugebauer, and et al. Alzheimer brain-derived tau oligomers propagate pathology from endogenous tau Sci Rep 2 2012 700
62. R.L. Hamilton Lewy bodies in Alzheimers disease: A neuropathological review of 145 cases using alpha-synuclein immunohistochemistry Brain Pathol 10 2000 378 384
63. C.F. Lippa, H. Fujiwara, D.M. Mann, B. Giasson, M. Baba, M.L. Schmidt, and et al. Lewy bodies contain altered alpha-synuclein in brains of many familial Alzheimers disease patients with mutations in presenilin and amyloid precursor protein genes Am J Pathol 153 1998 1365 1370
64. C.F. Lippa, M.L. Schmidt, V.M. Lee, and J.Q. Trojanowski Antibodies to alpha-synuclein detect Lewy bodies in many Downs syndrome brains with Alzheimers disease Ann Neurol 45 1999 353 357
65. P.G. Galloway, I. Grundke-Iqbal, K. Iqbal, and G. Perry Lewy bodies contain epitopes both shared and distinct from Alzheimer neurofibrillary tangles J Neuropathol Exp Neurol 47 1988 654 663
66. T. Ishizawa, P. Mattila, P. Davies, D. Wang, and D.W. Dickson Colocalization of tau and alpha-synuclein epitopes in Lewy bodies J Neuropathol Exp Neurol 62 2003 389 397
67. A. Takeda, M. Mallory, M. Sundsmo, W. Honer, L. Hansen, and E. Masliah Abnormal accumulation of NACP/alpha-synuclein in neurodegenerative disorders Am J Pathol 152 1998 367 372
68. T. Kaul, J. Credle, T. Haggerty, A.W. Oaks, E. Masliah, and A. Sidhu Region-specific tauopathy and synucleinopathy in brain of the alpha-synuclein overexpressing mouse model of Parkinsons disease BMC Neurosci 12 2011 79
69. G. Farias, P. Perez, A. Slachevsky, and R.B. Maccioni Platelet tau pattern correlates with cognitive status in Alzheimers disease J Alzheimers Dis 31 2012 65 69
70. N. Badiola, R.M. de Oliveira, F. Herrera, C. Guardia-Laguarta, S.A. Goncalves, M. Pera, and et al. Tau enhances alpha-synuclein aggregation and toxicity in cellular models of synucleinopathy PLoS One 6 2011 e26609
71. P. Zabrocki, K. Pellens, T. Vanhelmont, T. Vandebroek, G. Griffioen, S. Wera, and et al. Characterization of alpha-synuclein aggregation and synergistic toxicity with protein tau in yeast FEBS J 272 2005 1386 1400
72. L. Parnetti, D. Chiasserini, G. Bellomo, D. Giannandrea, C. De Carlo, M.M. Qureshi, and et al. Cerebrospinal fluid Tau/alpha-synuclein ratio in Parkinsons disease and degenerative dementias Mov Disord 26 2011 1428 1435