Antibody-Mediated Targeting of Tau In Vivo Does Not Require Effector Function and Microglial Engagement

Cell Reports

Volumn 16, Issue 6, 2016, Pages 1690-1700

  Lee, Seung Hye ^a   Le Pichon, Claire E ^a   Adolfsson, Oskar ^b   Gafner, Valérie ^b   Pihlgren, Maria ^b   Lin, Han ^a   Solanoy, Hilda ^a   Brendza, Robert ^a   Ngu, Hai ^a   Foreman, Oded ^a   Chan, Ruby ^a   Ernst, James A ^a   DiCara, Danielle ^a   Hotzel, Isidro ^a   Srinivasan, Karpagam ^a   Hansen, David V ^a   Atwal, Jasvinder ^a   Lu, Yanmei ^a   Bumbaca, Daniela ^a   Pfeifer, Andrea ^b   Watts, Ryan J ^a   Muhs, Andreas ^b   Scearce Levie, Kimberly ^a   Ayalon, Gai ^a   more..

^a GENENTECH INC   (United States)

^b AC IMMUNE SA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

FC RECEPTOR; IMMUNOGLOBULIN G2A ANTIBODY; INTERLEUKIN 1BETA; INTERLEUKIN 6; MICROTUBULE ASSOCIATED PROTEIN 2; TAU PROTEIN; TUMOR NECROSIS FACTOR; ANTIBODY; CYTOKINE;

AGE; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COCULTURE; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG EFFICACY; DRUG TARGETING; HIPPOCAMPAL NEURONAL CULTURE; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOTHERAPY; IN VITRO STUDY; IN VIVO STUDY; MICROGLIA; MOUSE; NERVE CELL; NERVOUS SYSTEM INFLAMMATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TRANSGENIC MOUSE; ANIMAL; BRAIN; CELL CULTURE; IMMUNOLOGY; METABOLISM; PATHOLOGY; PROCEDURES;

ALZHEIMER DISEASE; ANIMALS; ANTIBODIES; BRAIN; CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOKINES; MICE, TRANSGENIC; MICROGLIA; NEURONS; TAU PROTEINS;

EID: 84979752510     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.06.099     Document Type: Article

References (37)

1. Adolfsson, O., Pihlgren, M., Toni, N., Varisco, Y., Buccarello, A.L., Antoniello, K., Lohmann, S., Piorkowska, K., Gafner, V., Atwal, J.K., et al. An effector-reduced anti-β-amyloid (Aβ) antibody with unique aβ binding properties promotes neuroprotection and glial engulfment of Aβ. J. Neurosci. 32 (2012), 9677–9689.
2. 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 (2011), 658–667.
3. Braak, H., Braak, E., Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 82 (1991), 239–259.
4. Braak, H., Braak, E., Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiol. Aging 16 (1995), 271–278, discussion 278–284.
5. Chai, X., Wu, S., Murray, T.K., Kinley, R., Cella, C.V., Sims, H., Buckner, N., Hanmer, J., Davies, P., O'Neill, M.J., 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 (2011), 34457–34467.
6. Chai, X., Dage, J.L., Citron, M., Constitutive secretion of tau protein by an unconventional mechanism. Neurobiol. Dis. 48 (2012), 356–366.
7. Congdon, E.E., Gu, J., Sait, H.B., Sigurdsson, E.M., Antibody uptake into neurons occurs primarily via clathrin-dependent Fcγ receptor endocytosis and is a prerequisite for acute tau protein clearance. J. Biol. Chem. 288 (2013), 35452–35465.
8. Couch, J.A., Yu, Y.J., Zhang, Y., Tarrant, J.M., Fuji, R.N., Meilandt, W.J., Solanoy, H., Tong, R.K., Hoyte, K., Luk, W., et al. Addressing safety liabilities of TfR bispecific antibodies that cross the blood-brain barrier. Sci. Transl. Med., 5, 2013 183ra57, 1–12.
9. 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, 2013, e62402.
10. de Calignon, A., Polydoro, M., Suárez-Calvet, M., William, C., Adamowicz, D.H., Kopeikina, K.J., Pitstick, R., Sahara, N., Ashe, K.H., Carlson, G.A., et al. Propagation of tau pathology in a model of early Alzheimer's disease. Neuron 73 (2012), 685–697.
11. Funk, K.E., Mirbaha, H., Jiang, H., Holtzman, D.M., Diamond, M.I., Distinct therapeutic mechanisms of Tau antibodies: promoting microglial clearance versus blocking neuronal uptake. J. Biol. Chem. 290 (2015), 21652–21662.
12. Glass, C.K., Saijo, K., Winner, B., Marchetto, M.C., Gage, F.H., Mechanisms underlying inflammation in neurodegeneration. Cell 140 (2010), 918–934.
13. Goedert, M., Ghetti, B., Spillantini, M.G., Frontotemporal dementia: implications for understanding Alzheimer disease. Cold Spring Harb. Perspect. Med., 2, 2012, a006254.
14. Golde, T.E., Open questions for Alzheimer's disease immunotherapy. Alzheimers Res. Ther., 6, 2014, 3.
15. Götz, J., Chen, F., Barmettler, R., Nitsch, R.M., Tau filament formation in transgenic mice expressing P301L tau. J. Biol. Chem. 276 (2001), 529–534.
16. Gu, J., Congdon, E.E., Sigurdsson, E.M., Two novel Tau antibodies targeting the 396/404 region are primarily taken up by neurons and reduce Tau protein pathology. J. Biol. Chem. 288 (2013), 33081–33095.
17. Hanisch, U.K., Kettenmann, H., Microglia: active sensor and versatile effector cells in the normal and pathologic brain. Nat. Neurosci. 10 (2007), 1387–1394.
18. Iba, M., Guo, J.L., McBride, J.D., Zhang, B., Trojanowski, J.Q., Lee, V.M., Synthetic tau fibrils mediate transmission of neurofibrillary tangles in a transgenic mouse model of Alzheimer's-like tauopathy. J. Neurosci. 33 (2013), 1024–1037.
19. Jicha, G.A., O'Donnell, A., Weaver, C., Angeletti, R., Davies, P., Hierarchical phosphorylation of recombinant tau by the paired-helical filament-associated protein kinase is dependent on cyclic AMP-dependent protein kinase. J. Neurochem. 72 (1999), 214–224.
20. Kfoury, N., Holmes, B.B., Jiang, H., Holtzman, D.M., Diamond, M.I., Trans-cellular propagation of Tau aggregation by fibrillar species. J. Biol. Chem. 287 (2012), 19440–19451.
21. Kimura, T., Ono, T., Takamatsu, J., Yamamoto, H., Ikegami, K., Kondo, A., Hasegawa, M., Ihara, Y., Miyamoto, E., Miyakawa, T., Sequential changes of tau-site-specific phosphorylation during development of paired helical filaments. Dementia 7 (1996), 177–181.
22. Le Pichon, C.E., Dominguez, S.L., Solanoy, H., Ngu, H., Lewin-Koh, N., Chen, M., Eastham-Anderson, J., Watts, R., Scearce-Levie, K., EGFR inhibitor erlotinib delays disease progression but does not extend survival in the SOD1 mouse model of ALS. PLoS ONE, 8, 2013, e62342.
23. Leabman, M.K., Meng, Y.G., Kelley, R.F., DeForge, L.E., Cowan, K.J., Iyer, S., Effects of altered FcγR binding on antibody pharmacokinetics in cynomolgus monkeys. MAbs 5 (2013), 896–903.
24. Liu, L., Drouet, V., Wu, J.W., Witter, M.P., Small, S.A., Clelland, C., Duff, K., Trans-synaptic spread of tau pathology in vivo. PLoS ONE, 7, 2012, e31302.
25. Luo, W., Liu, W., Hu, X., Hanna, M., Caravaca, A., Paul, S.M., Microglial internalization and degradation of pathological tau is enhanced by an anti-tau monoclonal antibody. Sci. Rep., 5, 2015, 11161.
26. Mandelkow, E.M., Mandelkow, E., Biochemistry and cell biology of tau protein in neurofibrillary degeneration. Cold Spring Harb. Perspect. Med., 2, 2012, a006247.
27. Muhs, A., Hickman, D.T., Pihlgren, M., Chuard, N., Giriens, V., Meerschman, C., van der Auwera, I., van Leuven, F., Sugawara, M., Weingertner, M.C., et al. Liposomal vaccines with conformation-specific amyloid peptide antigens define immune response and efficacy in APP transgenic mice. Proc. Natl. Acad. Sci. USA 104 (2007), 9810–9815.
28. Ostrowitzki, S., Deptula, D., Thurfjell, L., Barkhof, F., Bohrmann, B., Brooks, D.J., Klunk, W.E., Ashford, E., Yoo, K., Xu, Z.X., et al. Mechanism of amyloid removal in patients with Alzheimer disease treated with gantenerumab. Arch. Neurol. 69 (2012), 198–207.
29. Prinz, M., Priller, J., Microglia and brain macrophages in the molecular age: from origin to neuropsychiatric disease. Nat. Rev. Neurosci. 15 (2014), 300–312.
30. Shaw, L.M., Vanderstichele, H., Knapik-Czajka, M., Clark, C.M., Aisen, P.S., Petersen, R.C., Blennow, K., Soares, H., Simon, A., Lewczuk, P., et al., Alzheimer's Disease Neuroimaging Initiative. Cerebrospinal fluid biomarker signature in Alzheimer's disease neuroimaging initiative subjects. Ann. Neurol. 65 (2009), 403–413.
31. Skovronsky, D.M., Lee, V.M., Trojanowski, J.Q., Neurodegenerative diseases: new concepts of pathogenesis and their therapeutic implications. Annu. Rev. Pathol. 1 (2006), 151–170.
32. Sperling, R., Salloway, S., Brooks, D.J., Tampieri, D., Barakos, J., Fox, N.C., Raskind, M., Sabbagh, M., Honig, L.S., Porsteinsson, A.P., et al. Amyloid-related imaging abnormalities in patients with Alzheimer's disease treated with bapineuzumab: a retrospective analysis. Lancet Neurol. 11 (2012), 241–249.
33. Wyss-Coray, T., Rogers, J., Inflammation in Alzheimer disease-a brief review of the basic science and clinical literature. Cold Spring Harb. Perspect. Med., 2, 2012, a006346.
34. Yamada, K., Cirrito, J.R., Stewart, F.R., Jiang, H., Finn, M.B., Holmes, B.B., Binder, L.I., Mandelkow, E.M., Diamond, M.I., Lee, V.M., Holtzman, D.M., In vivo microdialysis reveals age-dependent decrease of brain interstitial fluid tau levels in P301S human tau transgenic mice. J. Neurosci. 31 (2011), 13110–13117.
35. Yanamandra, K., Kfoury, N., Jiang, H., Mahan, T.E., Ma, S., Maloney, S.E., Wozniak, D.F., Diamond, M.I., Holtzman, D.M., Anti-tau antibodies that block tau aggregate seeding in vitro markedly decrease pathology and improve cognition in vivo. Neuron 80 (2013), 402–414.
36. Yu, Y.J., Watts, R.J., Developing therapeutic antibodies for neurodegenerative disease. Neurotherapeutics 10 (2013), 459–472.
37. Zhang, Y., Chen, K., Sloan, S.A., Bennett, M.L., Scholze, A.R., O'Keeffe, S., Phatnani, H.P., Guarnieri, P., Caneda, C., Ruderisch, N., et al. An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. J. Neurosci. 34 (2014), 11929–11947.