Neuron-to-neuron wild-type Tau protein transfer through a trans-synaptic mechanism: Relevance to sporadic tauopathies

Acta Neuropathologica Communications

Volumn 2, Issue 1, 2014, Pages

  Dujardin, Simon ^a,b   Lécolle, Katia ^a,b   Caillierez, Raphaëlle ^a,b   Bégard, Séverine ^a,b   Zommer, Nadège ^a,b,c   Lachaud, Cédrick ^a,b   Carrier, Sébastien ^a,b   Dufour, Noëlle ^d,e   Aurégan, Gwennaëlle ^d,e   Winderickx, Joris ^f   Hantraye, Philippe ^d,e   Déglon, Nicole ^d,e,g   Colin, Morvane ^a,b,c   Buée, Luc ^a,b,c  

^a INSERM   (France)

^b JEAN PIERRE AUBERT RESEARCH CENTER   (France)

^c CHR   (France)

^d INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^e Molecular Imaging Research Center   (France)

^f UNIVERSITY OF LEUVEN   (Belgium)

^g LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Alzheimer; Prion; Propagation; Secretion; Spreading

Indexed keywords

MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN; TAU PROTEIN;

ANIMAL; ANIMAL EMBRYO; BRAIN; CELL CULTURE; CELL DIFFERENTIATION; CONFOCAL MICROSCOPY; DISEASE COURSE; DISEASE MODEL; GENE TRANSFER; GENETICS; HUMAN; METABOLISM; MICROFLUIDIC ANALYSIS; MUTATION; NERVE CELL; PATHOLOGY; PHYSIOLOGY; PROTEIN TRANSPORT; RAT; TAUOPATHY; WISTAR RAT;

ANIMALS; BRAIN; CELL DIFFERENTIATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; EMBRYO, MAMMALIAN; GENE TRANSFER TECHNIQUES; HUMANS; MICROFLUIDIC ANALYTICAL TECHNIQUES; MICROSCOPY, CONFOCAL; MICROTUBULE-ASSOCIATED PROTEINS; MUTATION; NEURONS; PROTEIN TRANSPORT; RATS; RATS, WISTAR; RNA, MESSENGER; TAU PROTEINS; TAUOPATHIES;

EID: 84903541550     PISSN: None     EISSN: 20515960     Source Type: Journal    
DOI: 10.1186/2051-5960-2-14     Document Type: Article

References (52)

1. Buee L, Bussiere T, Buee-Scherrer V, Delacourte A, Hof PR: Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Res Brain Res Rev 2000, 33: 95-130.
2. Duyckaerts C, Potier MC, Delatour B: Alzheimer disease models and human neuropathology: similarities and differences. Acta Neuropathol 2008, 115: 5-38.
3. Gotz J, Ittner LM: Animal models of Alzheimer's disease and frontotemporal dementia. Nat Rev Neurosci 2008, 9: 532-544.
4. Chang E, Kim S, Yin H, Nagaraja HN, Kuret J: Pathogenic missense MAPT mutations differentially modulate tau aggregation propensity at nucleation and extension steps. J Neurochem 2008, 107: 1113-1123.
5. Chaunu MP, Deramecourt V, Buée-Scherrer V, Le Ber I, Brice A, Ehrle N, Hachimi KE, Pluot M, Maurage CA, Bakchine S, Buée L: Juvenile frontotemporal dementia with parkinsonism associated with Tau mutation G389R. J Alzheimer dis 2013, 37: 769-776.
6. Braak H, Braak E: Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991, 82: 239-259.
7. Delacourte A, David JP, Sergeant N, Buee L, Wattez A, Vermersch P, Ghozali F, Fallet-Bianco C, Pasquier F, Lebert F, et al.: The biochemical pathway of neurofibrillary degeneration in aging and Alzheimer's disease. Neurology 1999, 52: 1158-1165.
8. Duyckaerts C, Bennecib M, Grignon Y, Uchihara T, He Y, Piette F, Hauw JJ: Modeling the relation between neurofibrillary tangles and intellectual status. Neurobiol Aging 1997, 18: 267-273.
9. Verny M, Duyckaerts C, Agid Y, Hauw JJ: The significance of cortical pathology in progressive supranuclear palsy. Clinico-pathological data in 10 cases. Brain 1996, 119(Pt 4):1123-1136.
10. Saito Y, Ruberu NN, Sawabe M, Arai T, Tanaka N, Kakuta Y, Yamanouchi H, Murayama S: Staging of argyrophilic grains: an age-associated tauopathy. J Neuropathol Exp Neurol 2004, 63: 911-918.
11. Clavaguera F, Akatsu H, Fraser G, Crowther RA, Frank S, Hench J, Probst A, Winkler DT, Reichwald J, Staufenbiel M, et al.: Brain homogenates from human tauopathies induce tau inclusions in mouse brain. Proc Natl Acad Sci U S A 2013, 110: 9535-9540.
12. Clavaguera F, Bolmont T, Crowther RA, Abramowski D, Frank S, Probst A, Fraser G, Stalder AK, Beibel M, Staufenbiel M, et al.: Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 2009, 11: 909-913.
13. Iba M, Guo JL, McBride JD, Zhang B, Trojanowski JQ, Lee VM: Synthetic tau fibrils mediate transmission of neurofibrillary tangles in a transgenic mouse model of Alzheimer's-like tauopathy. J Neurosci 2013, 33: 1024-1037.
14. Lasagna-Reeves CA, Castillo-Carranza DL, Sengupta U, Sarmiento J, Troncoso J, Jackson GR, Kayed R: Identification of oligomers at early stages of tau aggregation in Alzheimer's disease. FASEB J 2012, 26: 1946-1959.
15. Frost B, Jacks RL, Diamond MI: Propagation of tau misfolding from the outside to the inside of a cell. J Biol Chem 2009, 284: 12845-12852.
16. Guo JL, Lee VM: Seeding of normal Tau by pathological Tau conformers drives pathogenesis of Alzheimer-like tangles. J Biol Chem 2011, 286: 15317-15331.
17. Santa-Maria I, Varghese M, Ksiezak-Reding H, Dzhun A, Wang J, Pasinetti GM: Paired helical filaments from Alzheimer disease brain induce intracellular accumulation of tau protein in aggresomes. J Biol Chem 2012, 287: 20522-20533.
18. Kfoury N, Holmes BB, Jiang H, Holtzman DM, Diamond MI: Trans-cellular Propagation of Tau Aggregation by Fibrillar Species. J Biol Chem 2012, 287: 19440-19451.
19. 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: 717-723.
20. de Calignon A, Polydoro M, Suarez-Calvet M, William C, Adamowicz DH, Kopeikina KJ, Pitstick R, Sahara N, Ashe KH, Carlson GA, et al.: Propagation of tau pathology in a model of early Alzheimer's disease. Neuron 2012, 73: 685-697.
21. Liu L, Drouet V, Wu JW, Witter MP, Small SA, Clelland C, Duff K: Trans-synaptic spread of tau pathology in vivo. PLoS One 2012, 7: e31302.
22. Caillierez R, Begard S, Lecolle K, Deramecourt V, Zommer N, Dujardin S, Loyens A, Dufour N, Auregan G, Winderickx J, et al.: Lentiviral Delivery of the Human Wild-type Tau Protein Mediates a Slow and Progressive Neurodegenerative Tau Pathology in the Rat Brain. Mol Ther 2013, 21: 1358-1368.
23. Sergeant N, Sablonniere B, Schraen-Maschke S, Ghestem A, Maurage CA, Wattez A, Vermersch P, Delacourte A: Dysregulation of human brain microtubule-associated tau mRNA maturation in myotonic dystrophy type 1. Hum Mol Genet 2001, 10: 2143-2155.
24. Hottinger AF, Azzouz M, Deglon N, Aebischer P, Zurn AD: Complete and long-term rescue of lesioned adult motoneurons by lentiviral-mediated expression of glial cell line-derived neurotrophic factor in the facial nucleus. J Neurosci 2000, 20: 5587-5593.
25. Lobbestael E, Reumers V, Ibrahimi A, Paesen K, Thiry I, Gijsbers R, Van den Haute C, Debyser Z, Baekelandt V, Taymans JM: Immunohistochemical detection of transgene expression in the brain using small epitope tags. BMC Biotechnol 2010, 10: 16.
26. Galas MC, Dourlen P, Begard S, Ando K, Blum D, Hamdane M, Buee L: The peptidylprolyl cis/trans-isomerase Pin1 modulates stress-induced dephosphorylation of Tau in neurons. Implication in a pathological mechanism related to Alzheimer disease. J Biol Chem 2006, 281: 19296-19304.
27. Liu WW, Goodhouse J, Jeon NL, Enquist LW: A microfluidic chamber for analysis of neuron-to-cell spread and axonal transport of an alpha-herpesvirus. PLoS One 2008, 3: e2382.
28. Taylor AM, Blurton-Jones M, Rhee SW, Cribbs DH, Cotman CW, Jeon NL: A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat Methods 2005, 2: 599-605.
29. Freundt EC, Maynard N, Clancy EK, Roy S, Bousset L, Sourigues Y, Covert M, Melki R, Kirkegaard K, Brahic M: Neuron-to-neuron transmission of alpha-synuclein fibrils through axonal transport. Ann Neurol 2012, 72: 517-524.
30. Wu JW, Herman M, Liu L, Simoes S, Acker CM, Figueroa H, Steinberg JI, Margittai M, Kayed R, Zurzolo C, et al.: Small misfolded Tau species are internalized via bulk endocytosis and anterogradely and retrogradely transported in neurons. J Biol Chem 2013, 288: 1856-1870.
31. Arhel N, Genovesio A, Kim KA, Miko S, Perret E, Olivo-Marin JC, Shorte S, Charneau P: Quantitative four-dimensional tracking of cytoplasmic and nuclear HIV-1 complexes. Nat Methods 2006, 3: 817-824.
32. Arhel NJ, Souquere-Besse S, Munier S, Souque P, Guadagnini S, Rutherford S, Prevost MC, Allen TD, Charneau P: HIV-1 DNA Flap formation promotes uncoating of the pre-integration complex at the nuclear pore. EMBO J 2007, 26: 3025-3037.
33. Cenquizca LA, Swanson LW: Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex. Brain Res Rev 2007, 56: 1-26.
34. Reiner A, Veenman CL, Medina L, Jiao Y, Del Mar N, Honig MG: Pathway tracing using biotinylated dextran amines. J Neurosci Methods 2000, 103: 23-37.
35. Mercken M, Vandermeeren M, Lubke U, Six J, Boons J, Van de Voorde A, Martin JJ, Gheuens J: Monoclonal antibodies with selective specificity for Alzheimer Tau are directed against phosphatase-sensitive epitopes. Acta Neuropathol 1992, 84: 265-272.
36. Jeganathan S, Hascher A, Chinnathambi S, Biernat J, Mandelkow EM, Mandelkow E: Proline-directed pseudo-phosphorylation at AT8 and PHF1 epitopes induces a compaction of the paperclip folding of Tau and generates a pathological (MC-1) conformation. J Biol Chem 2008, 283: 32066-32076.
37. Jicha GA, Bowser R, Kazam IG, Davies P: Alz-50 and MC-1, a new monoclonal antibody raised to paired helical filaments, recognize conformational epitopes on recombinant tau. J Neurosci Res 1997, 48: 128-132.
38. Allen B, Ingram E, Takao M, Smith MJ, Jakes R, Virdee K, Yoshida H, Holzer M, Craxton M, Emson PC, et al.: Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein. J Neurosci 2002, 22: 9340-9351.
39. Mohamed NV, Herrou T, Plouffe V, Piperno N, Leclerc N: Spreading of tau pathology in Alzheimer's disease by cell-to-cell transmission. Eur J Neurosci 2013, 37: 1939-1948.
40. Gomez-Ramos A, Diaz-Hernandez M, Rubio A, Miras-Portugal MT, Avila J: Extracellular tau promotes intracellular calcium increase through M1 and M3 muscarinic receptors in neuronal cells. Mol Cell Neurosci 2008, 37: 673-681.
41. Karch CM, Jeng AT, Goate AM: Extracellular tau levels are influenced by variability in tau that is associated with tauopathies. J Biol Chem 2012, 287: 42751-42762.
42. Chai X, Dage JL, Citron M: Constitutive secretion of tau protein by an unconventional mechanism. Neurobiol Dis 2012, 48: 356-366.
43. Plouffe V, Mohamed NV, Rivest-McGraw J, Bertrand J, Lauzon M, Leclerc N: Hyperphosphorylation and cleavage at D421 enhance tau secretion. PLoS One 2012, 7: e36873.
44. Pooler AM, Phillips EC, Lau DH, Noble W, Hanger DP: Physiological release of endogenous tau is stimulated by neuronal activity. EMBO Rep 2013, 14: 389-394.
45. Holmes BB, Devos SL, Kfoury N, Li M, Jacks R, Yanamandra K, Ouidja MO, Brodsky FM, Marasa J, Bagchi DP, et al.: Heparan sulfate proteoglycans mediate internalization and propagation of specific proteopathic seeds. Proc Natl Acad Sci U S A 2013, 110: E3138-3147.
46. Simon D, Garcia-Garcia E, Royo F, Falcon-Perez JM, Avila J: Proteostasis of tau. Tau overexpression results in its secretion via membrane vesicles. FEBS Lett 2012, 586: 47-54.
47. Yasuda M, Mayford MR: CaMKII activation in the entorhinal cortex disrupts previously encoded spatial memory. Neuron 2006, 50: 309-318.
48. Clavaguera F, Lavenir I, Falcon B, Frank S, Goedert M, Tolnay M: "Prion-like" templated misfolding in tauopathies. Brain Pathol 2013, 23: 342-349.
49. Diaz-Hernandez M, Gomez-Ramos A, Rubio A, Gomez-Villafuertes R, Naranjo JR, Miras-Portugal MT, Avila J: Tissue-nonspecific alkaline phosphatase promotes the neurotoxicity effect of extracellular tau. J Biol Chem 2010, 285: 32539-32548.
50. Gerson JE, Kayed R: Formation and propagation of tau oligomeric seeds. Front Neurol 2013, 4: 93.
51. Troquier L, Caillierez R, Burnouf S, Fernandez-Gomez FJ, Grosjean ME, Zommer N, Sergeant N, Schraen-Maschke S, Blum D, Buee L: Targeting phospho-Ser422 by active Tau Immunotherapy in the THYTau22 mouse model: a suitable therapeutic approach. Curr Alzheimer Res 2012, 9: 397-405.
52. Yanamandra K, Kfoury N, Jiang H, Mahan TE, Ma S, Maloney SE, Wozniak DF, Diamond MI, Holtzman DM: Anti-Tau antibodies that Block Tau aggregate seeding in vitro markedly decrease pathology and improve cognition in vivo. Neuron 2013, 80: 402-414.