Starvation and inhibition of lysosomal function increased tau secretion by primary cortical neurons

Scientific Reports

Volumn 4, Issue , 2014, Pages

  Mohamed, Nguyen Vi ^a   Plouffe, Vanessa ^a   Rémillard Labrosse, Gaudeline ^a   Planel, Emmanuel ^b   Leclerc, Nicole ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b LAVAL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CULTURE MEDIUM; LEUPEPTIN; MAPT PROTEIN, MOUSE; TAU PROTEIN;

ANIMAL; BRAIN CORTEX; C57BL MOUSE; CELL CULTURE; CULTURE MEDIUM; CYTOLOGY; LYSOSOME; NERVE CELL; PHOSPHORYLATION; PHYSIOLOGY; PRIMARY CELL CULTURE; PROTEIN PROCESSING; SECRETION (PROCESS);

ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; CULTURE MEDIA; LEUPEPTINS; LYSOSOMES; MICE, INBRED C57BL; NEURONS; PHOSPHORYLATION; PRIMARY CELL CULTURE; PROTEIN PROCESSING, POST-TRANSLATIONAL; TAU PROTEINS;

EID: 84904607788     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep05715     Document Type: Article

References (66)

1. Grundke-Iqbal, I. et al. Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J biol chem 261, 6084-6089 (1986). (Pubitemid 17207447)
2. Grundke-Iqbal, I. et al. Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci USA 83, 4913-4917 (1986).
3. Braak, H. & Braak, E. Neuropathological staging of Alzheimer-related changes. Acta Neuropathol. 82, 239-259 (1991).
4. Morris, M., Maeda, S., Vossel, K. & Mucke, L. The many faces of tau. Neuron 70, 410-426 (2011).
5. Brundin, P., Melki, R. & Kopito, R. Prion-like transmission of protein aggregates in neurodegenerative diseases. Nat Rev Mol Cell Biol 11, 301-307 (2010).
6. Frost, B. & Diamond, M. I. Prion-like mechanisms in neurodegenerative diseases. Nat Rev Neurosci 11, 155-159 (2010).
7. Walker, L. C., Diamond, M. I., Duff, K. E. & Hyman, B. T. Mechanisms of Protein Seeding in Neurodegenerative Diseases. Arch Neurol 1-7 (2012).
8. Mohamed, N. V., Herrou, T., Plouffe, V., Piperno, N. & Leclerc, N. Spreading of tau pathology in Alzheimer's disease by cell-to-cell transmission. Eur J Neurosci 37, 1939-1948 (2013).
9. Kim, W., Lee, S. & Hall, G. F. Secretion of human tau fragments resembling CSFtau in Alzheimer's disease is modulated by the presence of the exon 2 insert. FEBS Lett 584, 3085-3088 (2010).
10. Kim, W. et al. Interneuronal transfer of human tau between Lamprey central neurons in situ. J Alzheimers Dis 19, 647-664 (2010).
11. Avila, J. et al. Looking for novel functions of tau. Biochem Soc trans 40, 653-655 (2012).
12. Plouffe, V. et al. Hyperphosphorylation and cleavage at D421 enhance tau secretion. PLoS One 7, e36873 (2012).
13. Yamada, K. et al. In vivo microdialysis reveals age-dependent decrease of brain interstitial fluid tau levels in P301S human tau transgenic mice. J Neurosci 31, 13110-13117 (2011).
14. Chai, X., Dage, J. L. & Citron, M. Constitutive secretion of tau protein by an unconventional mechanism. Neurobiol Dis 48, 356-366 (2012).
15. Wu, J.W. et al. Small misfolded tau species are internalized via bulk endocytosis and anterogradely and retrogradely transported in neurons. J biol chem 288, 1856-1870 (2012).
16. Karch, C. M., Jeng, A. T. & Goate, A. M. Extracellular tau levels are influenced by variability in tau that is associated with tauopathies. J biol chem 287, 42751-42762 (2012).
17. Kfoury, N., Holmes, B. B., Jiang, H., Holtzman, D. M. & Diamond, M. I. Transcellular propagation of Tau aggregation by fibrillar species. J biol chem 287, 19440-19451 (2012).
18. Saman, S. et al. Exosome-associated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early Alzheimer disease. J biol chem 287, 3842-3849 (2012).
19. Clavaguera, F. et al. Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 11, 909-913 (2009).
20. Frost, B., Jacks, R. L. & Diamond, M. I. Propagation of tau misfolding from the outside to the inside of a cell. J biol chem 284, 12845-12852 (2009).
21. Guo, J. L. & Lee, V. M. Seeding of normal Tau by pathological Tau conformers drives pathogenesis of Alzheimer-like tangles. J biol chem 286, 15317-15331 (2011).
22. de Calignon, A. et al. Propagation of Tau Pathology in a Model of Early Alzheimer's Disease. Neuron 73, 685-697 (2012).
23. Liu, L. et al. Trans-synaptic spread of tau pathology in vivo. PLoS One 7, e31302 (2012).
24. Barten, D. M. et al. Tau transgenic mice as models for cerebrospinal fluid tau biomarkers. J Alzheimers Dis 24 Suppl 2, 127-141 (2011).
25. Pooler, A. M., Phillips, E. C., Lau, D. H., Noble, W. & Hanger, D. P. Physiological release of endogenous tau is stimulated by neuronal activity. EMBO reports 14, 389-394 (2013).
26. Simon, D. et al. Tau overexpression results in its secretion via membrane vesicles. Neurodegener Dis 10, 73-75 (2012).
27. Simon, D., Garcia-Garcia, E., Royo, F., Falcon-Perez, J. M. & Avila, J. Proteostasis of tau. Tau overexpression results in its secretion via membrane vesicles. FEBS Lett 586, 47-54 (2012).
28. Saraste, J., Palade, G. E. & Farquhar, M. G. Temperature-sensitive steps in the transport of secretory proteins through the Golgi complex in exocrine pancreatic cells. Proc Natl Acad Sci USA 83, 6425-6429 (1986). (Pubitemid 17174747)
29. Hampel, H. et al. Total and phosphorylated tau protein as biological markers of Alzheimer's disease. Exp Gerontol 45, 30-40 (2010).
30. Kimura, S., Noda, T. & Yoshimori, T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3, 452-460 (2007). (Pubitemid 47293726)
31. Madeira, A., Pommet, J. M., Prochiantz, A. & Allinquant, B. SET protein (TAF1beta, I2PP2A) is involved in neuronal apoptosis induced by an amyloid precursor protein cytoplasmic subdomain. FASEB J 19, 1905-1907 (2005). (Pubitemid 41598790)
32. Klionsky, D. J. et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8, 445-544 (2012).
33. Luft, J. H. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol 9, 409-414 (1961).
34. Allen, S. J., Watson, J. J. & Dawbarn, D. The neurotrophins and their role in Alzheimer's disease. Curr Neuropharmacol 9, 559-573 (2011).
35. Boland, B. et al. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J Neurosci 28, 6926-6937 (2008).
36. Mizushima, N., Yamamoto, A., Matsui, M., Yoshimori, T. & Ohsumi, Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 15, 1101-1111 (2004). (Pubitemid 38316219)
37. Nixon, R. A. et al. Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J neuropathol exp neurol 64, 113-122 (2005). (Pubitemid 40349309)
38. Flach, K. et al. Tau oligomers impair artificial membrane integrity and cellular viability. J biol chem 287, 43223-43233 (2012).
39. Duran, J.M., Anjard, C., Stefan, C., Loomis, W. F. &Malhotra, V.Unconventional secretion of Acb1 is mediated by autophagosomes. J cell biol 188, 527-536 (2010).
40. Andrei, C. et al. The secretory route of the leaderless protein interleukin 1beta involves exocytosis of endolysosome-related vesicles. Mol Biol Cell 10, 1463-1475 (1999). (Pubitemid 29230902)
41. Wang, Y. et al. Tau fragmentation, aggregation and clearance: the dual role of lysosomal processing. Hum Mol Genet 18, 4153-4170 (2009).
42. Kruger, U.,Wang, Y., Kumar, S. &Mandelkow, E. M. Autophagic degradation of tau in primary neurons and its enhancement by trehalose. Neurobiol Aging 33, 2291-2305 (2012).
43. Laulagnier, K. et al. Role of AP1 and Gadkin in the traffic of secretory endolysosomes. Mol Biol Cell 22, 2068-2082 (2011).
44. Farah, C. et al. Tau interacts with Golgi membranes and mediates their association with microtubules. Cell Motil Cytoskeleton 63, 710-724 (2006). (Pubitemid 44673949)
45. Perreault, S., Bousquet, O., Lauzon, M., Paiement, J. & Leclerc, N. Increased association between rough endoplasmic reticulum membranes and mitochondria in transgenic mice that express P301L tau. J neuropathol exp neurol 68, 503-514 (2009).
46. Pooler, A. M. et al. Dynamic association of tau with neuronal membranes is regulated by phosphorylation. Neurobiol Aging 33, 431 e427-438 (2012).
47. Brandt, R., Leger, J. & Lee, G. Interaction of tau with the neural plasmamembrane mediated by tau's amino-terminal projection domain. J cell biol 131, 1327-1340 (1995).
48. Davis, D. R., Anderton, B. H., Brion, J. P., Reynolds, C. H. & Hanger, D. P. Oxidative stress induces dephosphorylation of tau in rat brain primary neuronal cultures. J neurochem 68, 1590-1597 (1997). (Pubitemid 27133067)
49. Kuszczyk, M., Gordon-Krajcer, W. & Lazarewicz, J. W. Homocysteine-induced acute excitotoxicity in cerebellar granule cells in vitro is accompanied by PP2Amediated dephosphorylation of tau. Neurochem Int 55, 174-180 (2009).
50. Burkhart, K. K., Beard, D. C., Lehman, R. A. & Billingsley, M. L. Alterations in tau phosphorylation in rat and human neocortical brain slices following hypoxia and glucose deprivation. Exp Neurol 154, 464-472 (1998). (Pubitemid 29044216)
51. Mailliot, C. et al. Rapid tau protein dephosphorylation and differential rephosphorylation during cardiac arrest-induced cerebral ischemia and reperfusion. J Cereb Blood Flow Metab 20, 543-549 (2000). (Pubitemid 30164899)
52. Shackelford, D. A. & Nelson, K. E. Changes in phosphorylation of tau during ischemia and reperfusion in the rabbit spinal cord. J neurochem 66, 286-295 (1996). (Pubitemid 26010792)
53. Shackelford, D. A. & Yeh, R. Y. Dephosphorylation of tau during transient forebrain ischemia in the rat. Mol Chem Neuropathol 34, 103-120 (1998). (Pubitemid 29168572)
54. Kopke, E. et al.Microtubule-associated protein tau. Abnormal phosphorylation of a non-paired helical filament pool in Alzheimer disease. J biol chem 268, 24374-24384 (1993). (Pubitemid 23335430)
55. Gotz, J. Tau and transgenic animal models. Brain Res Brain Res Rev 35, 266-286 (2001). (Pubitemid 32566200)
56. Zheng, W. H., Bastianetto, S., Mennicken, F., Ma, W. & Kar, S. Amyloid beta peptide induces tau phosphorylation and loss of cholinergic neurons in rat primary septal cultures. Neuroscience 115, 201-211 (2002). (Pubitemid 35232701)
57. Zempel, H., Thies, E., Mandelkow, E. & Mandelkow, E.M. Abeta oligomers cause localized Ca(21) elevation, missorting of endogenous Tau into dendrites, Tau phosphorylation, and destruction of microtubules and spines. J Neurosci 30, 11938-11950 (2010).
58. Jin, M. et al. Soluble amyloid beta-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration. Proc Natl Acad Sci USA 108, 5819-5824 (2011).
59. Diaz-Hernandez, M. et al. Tissue non-specific alkaline phosphatase promotes the neurotoxicity effect of extracellular tau. J biol chem 285, 32539-32548 (2010).
60. Liu, X. A. et al. Tau dephosphorylation potentiates apoptosis by mechanisms involving a failed dephosphorylation/activation of Bcl-2. J Alzheimers Dis 19, 953-962 (2010).
61. Talmat-Amar, Y. et al. Important neuronal toxicity of microtubule-bound Tau in vivo in Drosophila. Hum Mol Genet 20, 3738-3745 (2011).
62. Gomez-Ramos, A., Diaz-Hernandez, M., Rubio, A., Miras-Portugal, M. T. & Avila, J. Extracellular tau promotes intracellular calcium increase through M1and M3 muscarinic receptors in neuronal cells. Mol Cell Neurosci 37, 673-681 (2008).
63. Urushitani, M. et al. Chromogranin-mediated secretion of mutant superoxide dismutase proteins linked to amyotrophic lateral sclerosis. Nat Neurosci 9, 108-118 (2006). (Pubitemid 43011916)
64. Gomes, C., Keller, S., Altevogt, P. & Costa, J. Evidence for secretion of Cu,Zn superoxide dismutase via exosomes from a cell model of amyotrophic lateral sclerosis. Neurosci lett 428, 43-46 (2007). (Pubitemid 47633803)
65. Gousset, K. et al. Prions hijack tunnelling nanotubes for intercellular spread. Nat Cell Biol 11, 328-336 (2009).
66. Fevrier, B. et al. Cells release prions in association with exosomes. Proc Natl Acad Sci USA 101, 9683-9688 (2004). (Pubitemid 38869296)