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Heterotypic seeding of Tau fibrillization by pre-aggregated Abeta provides potent seeds for prion-like seeding and propagation of Tau-pathology in vivo.

Bibliographic reference Barbosa de Vasconcelos, Bruno ; Stancu, Ilie-Cosmin ; Buist, Arjan ; Bird, Matthew ; Wang, Peng ; et. al. Heterotypic seeding of Tau fibrillization by pre-aggregated Abeta provides potent seeds for prion-like seeding and propagation of Tau-pathology in vivo.. In: Acta Neuropathologica, Vol. 131, no. 4, p. 549-569 (April 2016)
Permanent URL http://hdl.handle.net/2078.1/169893
  1. Ahmed Zeshan, Cooper Jane, Murray Tracey K., Garn Katya, McNaughton Emily, Clarke Hannah, Parhizkar Samira, Ward Mark A., Cavallini Annalisa, Jackson Samuel, Bose Suchira, Clavaguera Florence, Tolnay Markus, Lavenir Isabelle, Goedert Michel, Hutton Michael L., O’Neill Michael J., 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, 10.1007/s00401-014-1254-6
  2. Bolmont Tristan, Clavaguera Florence, Meyer-Luehmann Melanie, Herzig Martin C., Radde Rebecca, Staufenbiel Matthias, Lewis Jada, Hutton Mike, Tolnay Markus, Jucker Mathias, Induction of Tau Pathology by Intracerebral Infusion of Amyloid-β-Containing Brain Extract and by Amyloid-β Deposition in APP × Tau Transgenic Mice, 10.2353/ajpath.2007.070403
  3. Braak H., Braak E., Neuropathological stageing of Alzheimer-related changes, 10.1007/bf00308809
  4. Braak Heiko, Del Tredici Kelly, The pathological process underlying Alzheimer’s disease in individuals under thirty, 10.1007/s00401-010-0789-4
  5. Choi Se Hoon, Kim Young Hye, Hebisch Matthias, Sliwinski Christopher, Lee Seungkyu, D’Avanzo Carla, Chen Hechao, Hooli Basavaraj, Asselin Caroline, Muffat Julien, Klee Justin B., Zhang Can, Wainger Brian J., Peitz Michael, Kovacs Dora M., Woolf Clifford J., Wagner Steven L., Tanzi Rudolph E., Kim Doo Yeon, A three-dimensional human neural cell culture model of Alzheimer’s disease, 10.1038/nature13800
  6. Clavaguera Florence, Bolmont Tristan, Crowther R. Anthony, Abramowski Dorothee, Frank Stephan, Probst Alphonse, Fraser Graham, Stalder Anna K., Beibel Martin, Staufenbiel Matthias, Jucker Mathias, Goedert Michel, Tolnay Markus, Transmission and spreading of tauopathy in transgenic mouse brain, 10.1038/ncb1901
  7. de Calignon Alix, Polydoro Manuela, Suárez-Calvet Marc, William Christopher, Adamowicz David H., Kopeikina Kathy J., Pitstick Rose, Sahara Naruhiko, Ashe Karen H., Carlson George A., Spires-Jones Tara L., Hyman Bradley T., Propagation of Tau Pathology in a Model of Early Alzheimer's Disease, 10.1016/j.neuron.2011.11.033
  8. Eisenberg David, Jucker Mathias, The Amyloid State of Proteins in Human Diseases, 10.1016/j.cell.2012.02.022
  9. Fernández Marta S., Human IAPP amyloidogenic properties and pancreatic β-cell death, 10.1016/j.ceca.2014.08.011
  10. Friedhoff Peter, Schneider Anja, Mandelkow Eva-Maria, Mandelkow Eckhard, Rapid Assembly of Alzheimer-like Paired Helical Filaments from Microtubule-Associated Protein Tau Monitored by Fluorescence in Solution†, 10.1021/bi980537d
  11. Giasson B. I., Initiation and Synergistic Fibrillization of Tau and Alpha-Synuclein, 10.1126/science.1082324
  12. Goedert M., Alzheimer's and Parkinson's diseases: The prion concept in relation to assembled A , tau, and  -synuclein, 10.1126/science.1255555
  13. Gotz J., Formation of Neurofibrillary Tangles in P301L Tau Transgenic Mice Induced by Abeta 42 Fibrils, 10.1126/science.1062097
  14. Guerrero-Muñoz Marcos J., Castillo-Carranza Diana L., Krishnamurthy Shashirekha, Paulucci-Holthauzen Adriana A., Sengupta Urmi, Lasagna-Reeves Cristian A., Ahmad Yembur, Jackson George R., Kayed Rakez, Amyloid-β oligomers as a template for secondary amyloidosis in Alzheimer's disease, 10.1016/j.nbd.2014.08.008
  15. Guo Jing L., Covell Dustin J., Daniels Joshua P., Iba Michiyo, Stieber Anna, Zhang Bin, Riddle Dawn M., Kwong Linda K., Xu Yan, Trojanowski John Q., Lee Virginia M.Y., Distinct α-Synuclein Strains Differentially Promote Tau Inclusions in Neurons, 10.1016/j.cell.2013.05.057
  16. Guo Jing L., Lee Virginia M.-Y., Seeding of Normal Tau by Pathological Tau Conformers Drives Pathogenesis of Alzheimer-like Tangles, 10.1074/jbc.m110.209296
  17. Guo Jing L, Lee Virginia M Y, Cell-to-cell transmission of pathogenic proteins in neurodegenerative diseases, 10.1038/nm.3457
  18. Guo J.-P., Arai T., Miklossy J., McGeer P. L., Abeta and tau form soluble complexes that may promote self aggregation of both into the insoluble forms observed in Alzheimer's disease, 10.1073/pnas.0509386103
  19. Hardy J., The Amyloid Hypothesis of Alzheimer's Disease: Progress and Problems on the Road to Therapeutics, 10.1126/science.1072994
  20. Héraud Céline, Goufak Doris, Ando Kunie, Leroy Karelle, Suain Valérie, Yilmaz Zehra, De Decker Robert, Authelet Michèle, Laporte Vincent, Octave Jean-Noël, Brion Jean-Pierre, Increased misfolding and truncation of tau in APP/PS1/tau transgenic mice compared to mutant tau mice, 10.1016/j.nbd.2013.09.010
  21. Hurtado David E., Molina-Porcel Laura, Iba Michiyo, Aboagye Awo K., Paul Steven M., Trojanowski John Q., Lee Virginia M.-Y., Aβ Accelerates the Spatiotemporal Progression of Tau Pathology and Augments Tau Amyloidosis in an Alzheimer Mouse Model, 10.2353/ajpath.2010.100346
  22. Iba M., Guo J. L., McBride J. D., Zhang B., Trojanowski J. Q., Lee V. M.- Y., Synthetic Tau Fibrils Mediate Transmission of Neurofibrillary Tangles in a Transgenic Mouse Model of Alzheimer's-Like Tauopathy, 10.1523/jneurosci.2642-12.2013
  23. Ittner Lars M., Götz Jürgen, Amyloid-β and tau — a toxic pas de deux in Alzheimer's disease, 10.1038/nrn2967
  24. Ittner Lars M., Ke Yazi D., Delerue Fabien, Bi Mian, Gladbach Amadeus, van Eersel Janet, Wölfing Heidrun, Chieng Billy C., Christie MacDonald J., Napier Ian A., Eckert Anne, Staufenbiel Matthias, Hardeman Edna, Götz Jürgen, Dendritic Function of Tau Mediates Amyloid-β Toxicity in Alzheimer's Disease Mouse Models, 10.1016/j.cell.2010.06.036
  25. Jack Clifford R, Knopman David S, Jagust William J, Petersen Ronald C, Weiner Michael W, Aisen Paul S, Shaw Leslie M, Vemuri Prashanthi, Wiste Heather J, Weigand Stephen D, Lesnick Timothy G, Pankratz Vernon S, Donohue Michael C, Trojanowski John Q, Tracking pathophysiological processes in Alzheimer's disease: an updated hypothetical model of dynamic biomarkers, 10.1016/s1474-4422(12)70291-0
  26. Jack Clifford R, Knopman David S, Jagust William J, Shaw Leslie M, Aisen Paul S, Weiner Michael W, Petersen Ronald C, Trojanowski John Q, Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade, 10.1016/s1474-4422(09)70299-6
  27. Jucker Mathias, Walker Lary C., Self-propagation of pathogenic protein aggregates in neurodegenerative diseases, 10.1038/nature12481
  28. Kfoury Najla, Holmes Brandon B., Jiang Hong, Holtzman David M., Diamond Marc I., Trans-cellular Propagation of Tau Aggregation by Fibrillar Species, 10.1074/jbc.m112.346072
  29. Lewis J., Enhanced Neurofibrillary Degeneration in Transgenic Mice Expressing Mutant Tau and APP, 10.1126/science.1058189
  30. Luk K. C., Kehm V., Carroll J., Zhang B., O'Brien P., Trojanowski J. Q., Lee V. M.- Y., Pathological  -Synuclein Transmission Initiates Parkinson-like Neurodegeneration in Nontransgenic Mice, 10.1126/science.1227157
  31. Mann David M. A., Hardy John, Amyloid or tau: the chicken or the egg?, 10.1007/s00401-013-1162-1
  32. Mares Rosa E., Meléndez-López Samuel G., Ramos Marco A., Acid-Denatured Green Fluorescent Protein (GFP) as Model Substrate to Study the Chaperone Activity of Protein Disulfide Isomerase, 10.3390/ijms12074625
  33. Meyer-Luehmann M., Exogenous Induction of Cerebral  -Amyloidogenesis Is Governed by Agent and Host, 10.1126/science.1131864
  34. Miller Yifat, Ma Buyong, Nussinov Ruth, Synergistic Interactions between Repeats in Tau Protein and Aβ Amyloids May Be Responsible for Accelerated Aggregation via Polymorphic States, 10.1021/bi200400u
  35. Morales Rodrigo, Moreno-Gonzalez Ines, Soto Claudio, Cross-Seeding of Misfolded Proteins: Implications for Etiology and Pathogenesis of Protein Misfolding Diseases, 10.1371/journal.ppat.1003537
  36. Oddo Salvatore, Billings Lauren, Kesslak J.Patrick, Cribbs David H., LaFerla Frank M., Aβ Immunotherapy Leads to Clearance of Early, but Not Late, Hyperphosphorylated Tau Aggregates via the Proteasome, 10.1016/j.neuron.2004.07.003
  37. Paxinos G, Franklin K (2001) The mouse brain in stereotaxic coordinates. Academic, San Diego
  38. Peelaerts W., Bousset L., Van der Perren A., Moskalyuk A., Pulizzi R., Giugliano M., Van den Haute C., Melki R., Baekelandt V., α-Synuclein strains cause distinct synucleinopathies after local and systemic administration, 10.1038/nature14547
  39. Peeraer Eve, Bottelbergs Astrid, Van Kolen Kristof, Stancu Ilie-Cosmin, Vasconcelos Bruno, Mahieu Michel, Duytschaever Hilde, Ver Donck Luc, Torremans An, Sluydts Ellen, Van Acker Nathalie, Kemp John A., Mercken Marc, Brunden Kurt R., Trojanowski John Q., Dewachter Ilse, Lee Virginia M.Y., Moechars Diederik, Intracerebral injection of preformed synthetic tau fibrils initiates widespread tauopathy and neuronal loss in the brains of tau transgenic mice, 10.1016/j.nbd.2014.08.032
  40. Pooler Amy M, Polydoro Manuela, Maury Eduardo A, Nicholls Samantha B, Reddy Snigdha M, Wegmann Susanne, William Christopher, Saqran Lubna, Cagsal-Getkin Ozge, Pitstick Rose, Beier David R, Carlson George A, Spires-Jones Tara L, Hyman Bradley T, Amyloid accelerates tau propagation and toxicity in a model of early Alzheimer’s disease, 10.1186/s40478-015-0199-x
  41. Postina Rolf, Schroeder Anja, Dewachter Ilse, Bohl Juergen, Schmitt Ulrich, Kojro Elzbieta, Prinzen Claudia, Endres Kristina, Hiemke Christoph, Blessing Manfred, Flamez Pascaline, Dequenne Antoine, Godaux Emile, van Leuven Fred, Fahrenholz Falk, A disintegrin-metalloproteinase prevents amyloid plaque formation and hippocampal defects in an Alzheimer disease mouse model, 10.1172/jci20864
  42. Rhoades Elizabeth, Agarwal Jayant, Gafni Ari, Aggregation of an amyloidogenic fragment of human islet amyloid polypeptide, 10.1016/s0167-4838(99)00248-4
  43. Rhoades Elizabeth, Gafni Ari, Micelle Formation by a Fragment of Human Islet Amyloid Polypeptide, 10.1016/s0006-3495(03)70068-x
  44. Sanders David W., Kaufman Sarah K., DeVos Sarah L., Sharma Apurwa M., Mirbaha Hilda, Li Aimin, Barker Scarlett J., Foley Alex C., Thorpe Julian R., Serpell Louise C., Miller Timothy M., Grinberg Lea T., Seeley William W., Diamond Marc I., Distinct Tau Prion Strains Propagate in Cells and Mice and Define Different Tauopathies, 10.1016/j.neuron.2014.04.047
  45. Saul Anika, Sprenger Frederik, Bayer Thomas A., Wirths Oliver, Accelerated tau pathology with synaptic and neuronal loss in a novel triple transgenic mouse model of Alzheimer's disease, 10.1016/j.neurobiolaging.2013.05.003
  46. Selkoe D. J., Alzheimer's Disease, 10.1101/cshperspect.a004457
  47. Serrano-Pozo A., Frosch M. P., Masliah E., Hyman B. T., Neuropathological Alterations in Alzheimer Disease, 10.1101/cshperspect.a006189
  48. Spires-Jones Tara L., Hyman Bradley T., The Intersection of Amyloid Beta and Tau at Synapses in Alzheimer’s Disease, 10.1016/j.neuron.2014.05.004
  49. Stancu Ilie-Cosmin, Vasconcelos Bruno, Terwel Dick, Dewachter Ilse, Models of β-amyloid induced Tau-pathology: the long and “folded” road to understand the mechanism, 10.1186/1750-1326-9-51
  50. Stancu IC, Ris L, Vasconcelos B, Marinangeli C, Goeminne L, Laporte V, Haylani LE, Couturier J, Schakman O, Gailly P, Pierrot N, Kienlen-Campard P, Octave JN, Dewachter I (2014) Tauopathy contributes to synaptic and cognitive deficits in a murine model for Alzheimer’s disease. FASEB J Off Publ Fed Am Soc Exp Biol 28:2620–2631
  51. Stancu Ilie-Cosmin, Vasconcelos Bruno, Ris Laurence, Wang Peng, Villers Agnès, Peeraer Eve, Buist Arjan, Terwel Dick, Baatsen Peter, Oyelami Tutu, Pierrot Nathalie, Casteels Cindy, Bormans Guy, Kienlen-Campard Pascal, Octave Jean-Nöel, Moechars Diederik, Dewachter Ilse, Templated misfolding of Tau by prion-like seeding along neuronal connections impairs neuronal network function and associated behavioral outcomes in Tau transgenic mice, 10.1007/s00401-015-1413-4
  52. Stine W. Blaine, Dahlgren Karie N., Krafft Grant A., LaDu Mary Jo, In VitroCharacterization of Conditions for Amyloid-β Peptide Oligomerization and Fibrillogenesis, 10.1074/jbc.m210207200
  53. Tanzi R. E., The Genetics of Alzheimer Disease, 10.1101/cshperspect.a006296
  54. Thal D. R., Rub U., Orantes M., Braak H., Phases of A -deposition in the human brain and its relevance for the development of AD, 10.1212/wnl.58.12.1791
  55. von Bergen M., Friedhoff P., Biernat J., Heberle J., Mandelkow E.-M., Mandelkow E., Assembly of tau protein into Alzheimer paired helical filaments depends on a local sequence motif (306VQIVYK311) forming beta structure, 10.1073/pnas.97.10.5129
  56. Walker Lary C., Jucker Mathias, Neurodegenerative Diseases: Expanding the Prion Concept, 10.1146/annurev-neuro-071714-033828
  57. Waxman E. A., Giasson B. I., Induction of Intracellular Tau Aggregation Is Promoted by  -Synuclein Seeds and Provides Novel Insights into the Hyperphosphorylation of Tau, 10.1523/jneurosci.0297-11.2011
  58. Yoshiyama Yasumasa, Higuchi Makoto, Zhang Bin, Huang Shu-Ming, Iwata Nobuhisa, Saido Takaomi C., Maeda Jun, Suhara Tetsuya, Trojanowski John Q., Lee Virginia M.-Y., Synapse Loss and Microglial Activation Precede Tangles in a P301S Tauopathy Mouse Model, 10.1016/j.neuron.2007.01.010