Microglial internalization and degradation of pathological tau is enhanced by an anti-tau monoclonal antibody

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Luo, Wenjie ^a   Liu, Wencheng ^a   Hu, Xiaoyan ^a   Hanna, Mary ^a   Caravaca, April ^a   Paul, Steven M ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MONOCLONAL ANTIBODY; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL; IMMUNOLOGY; METABOLISM; MICROGLIA; MOUSE; PATHOLOGY; PROTEIN DEGRADATION;

ALZHEIMER DISEASE; ANIMALS; ANTIBODIES, MONOCLONAL; MICE; MICROGLIA; PROTEOLYSIS; TAU PROTEINS;

EID: 84930966153     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep11161     Document Type: Article

References (47)

1. Tosto, G. & Reitz, C. Genome-wide association studies in Alzheimer's disease: a review. Curr Neurol Neurosci Rep. 13, 381 (2013).
2. Gandy, S. & Heppner, F. L. Microglia as dynamic and essential components of the amyloid hypothesis. Neuron 78, 575-577 (2013).
3. Griciuc, A. et al. Alzheimer's disease risk gene CD33 inhibits microglial uptake of amyloid beta. Neuron 78, 631-643 (2013).
4. Zhao, L. et al. Macrophage-mediated degradation of beta-amyloid via an apolipoprotein E isoform-dependent mechanism. J Neurosci 29, 3603-3612 (2009).
5. Hickman, S. E., Allison, E. K. & El Khoury, J. Microglial dysfunction and defective beta-amyloid clearance pathways in aging Alzheimer's disease mice. J Neurosci. 28, 8354-8360 (2008).
6. Lee, C. Y. & Landreth, G. E. The role of microglia in amyloid clearance from the AD brain. J Neural Transm. 117, 949-960 (2010).
7. Wilkinson, K. & El Khoury, J. Microglial scavenger receptors and their roles in the pathogenesis of Alzheimer's disease. International journal of Alzheimer's disease 2012, 489456 (2012).
8. Tato, R. E., Frank, A. & Hernanz, A. Tau protein concentrations in cerebrospinal fluid of patients with dementia of the Alzheimer type. J Neurol Neurosurg Psychiatry. 59, 280-283 (1995).
9. Yamada, K. et al. Neuronal activity regulates extracellular tau in vivo. J Exp Med. 211, 387-393 (2014).
10. Sheng, J. G., Mrak, R. E. & Griffin, W. S. Glial-neuronal interactions in Alzheimer disease: progressive association of IL-1alpha + microglia and S100beta + astrocytes with neurofibrillary tangle stages. J Neuropathol Exp Neurol. 56, 285-290 (1997).
11. DiPatre, P. L. & Gelman, B. B. Microglial cell activation in aging and Alzheimer disease: partial linkage with neurofibrillary tangle burden in the hippocampus. J Neuropathol Exp Neurol. 56, 143-149 (1997).
12. Serrano-Pozo, A. et al. Reactive glia not only associates with plaques but also parallels tangles in Alzheimer's disease. Am J Pathol. 179, 1373-1384 (2011).
13. Serrano-Pozo, A. et al. Differential Relationships of Reactive Astrocytes and Microglia to Fibrillar Amyloid Deposits in Alzheimer Disease. J Neuropathol Exp Neurol. 72, 462-471 (2013).
14. 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).
15. Clavaguera, F. et al. Transmission and spreading of tauopathy in transgenic mouse brain. Nat Cell Biol 11, 909-913 (2009).
16. Liu, L. et al. Trans-synaptic spread of tau pathology in vivo. PLoS One 7, e31302 (2012).
17. Lasagna-Reeves, C. A. et al. Alzheimer brain-derived tau oligomers propagate pathology from endogenous tau. Sci Rep. 2, 700 (2012).
18. de Calignon, A. et al. Propagation of tau pathology in a model of early Alzheimer's disease. Neuron 73, 685-697 (2012).
19. Iba, M. et al. Synthetic tau fibrils mediate transmission of neurofibrillary tangles in a transgenic mouse model of Alzheimer's-like tauopathy. J Neurosci 33, 1024-1037 (2013).
20. Clavaguera, F. et al. Brain homogenates from human tauopathies induce tau inclusions in mouse brain. Proc Natl Acad Sci USA 110, 9535-9540 (2013).
21. Sanders, D. W. et al. Distinct tau prion strains propagate in cells and mice and define different tauopathies. Neuron 82, 1271-1288 (2014).
22. Yanamandra, K. et al. Anti-tau antibodies that block tau aggregate seeding in vitro markedly decrease pathology and improve cognition in vivo. Neuron 80, 402-414 (2013).
23. Frost, B. & Diamond, M. I. Prion-like mechanisms in neurodegenerative diseases. Nat Rev Neurosci. 11, 155-159 (2010).
24. Bi, M., Ittner, A., Ke, Y. D., Gotz, J. & Ittner, L. M. Tau-targeted immunization impedes progression of neurofibrillary histopathology in aged P301L tau transgenic mice. PLoS One 6, e26860 (2011).
25. Boimel, M. et al. Efficacy and safety of immunization with phosphorylated tau against neurofibrillary tangles in mice. Exp Neurol. 224, 472-485 (2010).
26. Asuni, A. A., Boutajangout, A., Quartermain, D. & Sigurdsson, E. M. Immunotherapy targeting pathological tau conformers in a tangle mouse model reduces brain pathology with associated functional improvements. J Neurosci 27, 9115-9129 (2007).
27. Boutajangout, A., Ingadottir, J., Davies, P. & Sigurdsson, E. M. Passive immunization targeting pathological phospho-tau protein in a mouse model reduces functional decline and clears tau aggregates from the brain. J Neurochem 118, 658-667 (2011).
28. Troquier, L. et al. Targeting phospho-Ser422 by active Tau Immunotherapy in the THYTau22 mouse model: a suitable therapeutic approach. Curr Alzheimer Res. 9, 397-405 (2012).
29. Chai, X. et al. Passive immunization with anti-Tau antibodies in two transgenic models: reduction of Tau pathology and delay of disease progression. J Biol Chem 286, 34457-34467 (2011).
30. d'Abramo, C., Acker, C. M., Jimenez, H. T. & Davies, P. Tau passive immunotherapy in mutant P301L mice: antibody affinity versus specificity. PLoS One 8, e62402 (2013).
31. Greenberg, S. G. & Davies, P. A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Proc Natl Acad Sci U S A 87, 5827-5831 (1990).
32. Allen, B. et al. Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein. J Neurosci 22, 9340-9351 (2002).
33. Jicha, G. A., Bowser, R., Kazam, I. G. & 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. 48, 128-132 (1997).
34. Perry, V. H., Nicoll, J. A. & Holmes, C. Microglia in neurodegenerative disease. Nat. Rev. Neurol. 6, 193-201 (2010).
35. Guerreiro, R. J. et al. Using exome sequencing to reveal mutations in TREM2 presenting as a frontotemporal dementia-like syndrome without bone involvement. JAMA neurology 70, 78-84 (2013).
36. Guerreiro, R. et al. TREM2 variants in Alzheimer's disease. N Engl J Med. 368, 117-127 (2013).
37. Borroni, B. et al. Heterozygous TREM2 mutations in frontotemporal dementia. Neurobiol Aging. 35, 934 e7-10 (2014).
38. Kleinberger, G. et al. TREM2 mutations implicated in neurodegeneration impair cell surface transport and phagocytosis. Sci. Transl. Med. 6, 243ra86 (2014).
39. Sheffield, L. G., Marquis, J. G. & Berman, N. E. Regional distribution of cortical microglia parallels that of neurofibrillary tangles in Alzheimer's disease. Neurosci Lett. 285, 165-168 (2000).
40. Cras, P., Kawai, M., Siedlak, S. & Perry, G. Microglia are associated with the extracellular neurofibrillary tangles of Alzheimer disease. Brain Res. 558, 312-314 (1991).
41. Lee, D. C. et al. Review: experimental manipulations of microglia in mouse models of Alzheimer's pathology: activation reduces amyloid but hastens tau pathology. Neuropathol Appl Neurobiol. 39, 69-85 (2013).
42. Streit, W. J., Braak, H., Xue, Q. S. & Bechmann, I. Dystrophic (senescent) rather than activated microglial cells are associated with tau pathology and likely precede neurodegeneration in Alzheimer's disease. Acta neuropathol. 118, 475-485 (2009).
43. Mosher, K. I. & Wyss-Coray, T. Microglial dysfunction in brain aging and Alzheimer's disease. Biochemical pharmacology 88, 594-604 (2014).
44. Miners, J. S., Barua, N., Kehoe, P. G., Gill, S. & Love, S. Abeta-degrading enzymes: potential for treatment of Alzheimer disease. J Neuropathol Exp Neurol. 70, 944-959 (2011).
45. Wilcock, D. M. et al. Passive amyloid immunotherapy clears amyloid and transiently activates microglia in a transgenic mouse model of amyloid deposition. J Neurosci 24, 6144-6151 (2004).
46. Morgan, D. Immunotherapy for Alzheimer's disease. J Intern Med. 269, 54-63 (2011).
47. Giulian, D. & Baker, T. J. Characterization of ameboid microglia isolated from developing mammalian brain. J Neurosci 6, 2163-2178 (1986).