Passive immunization targeting the N-terminal region of phosphorylated tau (residues 68–71) improves spatial memory in okadaic acid induced tauopathy model rats

Biochemical and Biophysical Research Communications

Volumn 483, Issue 1, 2017, Pages 585-589

  Subramanian, Sarada ^a   Savanur, Ganesh ^a   Madhavadas, Sowmya ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH AND NEUROSCIENCES   (India)

Author keywords

Alzheimer disease; Okadaic acid; Phosphopeptide; Spatial memory; Tau; Tauopathy

Indexed keywords

EPITOPE; OKADAIC ACID; PHOSPHOTHREONINE; TAU PROTEIN; MAPT PROTEIN, RAT; PEPTIDE; PHOSPHOPROTEIN PHOSPHATASE 2; PPP2CA PROTEIN, RAT; RECOMBINANT PROTEIN;

ADULT; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INCLUSION; COGNITIVE DEFECT; COLUMN CHROMATOGRAPHY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HOMOGENATE; IN VITRO STUDY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; OLIGOMERIZATION; PASSIVE IMMUNIZATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RAT; SPATIAL MEMORY; T LYMPHOCYTE; TAUOPATHY; ANIMAL; CHEMICALLY INDUCED; CHEMISTRY; DISEASE MODEL; HIPPOCAMPUS; IMMUNIZATION; LEPORIDAE; METABOLISM; PHOSPHORYLATION; PROCEDURES; PROTEIN DOMAIN; SPRAGUE DAWLEY RAT;

ANIMALS; DISEASE MODELS, ANIMAL; EPITOPES; FEMALE; HIPPOCAMPUS; IMMUNIZATION; MALE; OKADAIC ACID; PEPTIDES; PHOSPHORYLATION; PROTEIN DOMAINS; PROTEIN PHOSPHATASE 2; RABBITS; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; SPATIAL MEMORY; TAU PROTEINS; TAUOPATHIES;

EID: 85008168863     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2016.12.101     Document Type: Article

References (28)

1. [1] Glenner, G.G., Wong, C.W., Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 120 (1984), 885–890.
2. [2] Grundke-Iqbal, I., Iqbal, K., Tung, Y.C., Quinlan, M., Wisniewski, H.M., Binder, L.I., Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acd. Sci. U. S. A. 83 (1986), 4913–4917.
3. [3] Golde, T.E., Open questions for Alzheimer's disease immunotherapy. Alzheimers Res. Ther., 6, 2014, 3.
4. [4] Crary, J.F., Trojanowski, J.Q., Schneider, J.A., Abisambra, J.F., Abner, E.L., Alafuzoff, I., Arnold, S.E., Attems, J., Beach, T.G., Bigio, E.H., Cairns, N.J., Dickson, D.W., Gearing, M., Grinberg, L.T., Hof, P.R., Hyman, B.T., Jellinger, K., Jicha, G.A., Kovacs, G.G., Knopman, D.S., Kofler, J., Kukull, W.A., Mackenzie, I.R., Masliah, E., McKee, A., Montine, T.J., Murray, M.E., Neltner, J.H., Santa-Maria, I., Seeley, W.W., Serrano-Pozo, A., Shelanski, M.L., Stein, T., Takao, M., Thal, D.R., Toledo, J.B., Troncoso, J.C., Vonsattel, J.P., White, C.L., Wisniewski, T., Woltjer, R.L., Yamada, M., Nelson, P.T., Primary age-related tauopathy (PART): a common pathology associated with human aging. Acta Neuropathol. 128 (2014), 755–766.
5. [5] Nelson, P.T., Alafuzoff, I., Bigio, E.H., Bouras, C., Braak, H., Cairns, N.J., Castellani, R.J., Crain, B.J., Davies, P., Del Tredici, K., Duyckaerts, C., Frosch, M.P., Haroutunian, V., Hof, P.R., Hulette, C.M., Hyman, B.T., Iwatsubo, T., Jellinger, K.A., Jicha, G.A., Kovari, E., Kukull, W.A., Leverenz, J.B., Love, S., Mackenzie, I.R., Mann, D.M., Masliah, E., Mckee, A.C., Montine, T.J., Morris, J.C., Schneider, J.A., Sonnen, J.A., Thal, D.R., Trojanowski, J.Q., Troncoso, J.C., Wisniewski, T., Woltzer, R.L., Beach, T.G., Correlation of Alzheimer disease neuropathologic changes with cognitive status: a reviewof the literature. J. Neuropathol. Exp. Neurol. 71 (2012), 362–381.
6. [6] 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 (2007), 9115–9129.
7. [7] Boutajangout, A., Ingadottir, J., Davies, P., Sigurdsson, E.M., Passive immunization targeting pathological phosphor-tau protein in a mouse model reduces functional decline and clears tau aggregates from the brain. J. Neurochem. 118 (2011), 658–667.
8. [8] Congdon, E.E., Krishnaswamy, S., Sigurdsson, E.M., Harnessing the immune system for treatment and detection of tau pathology. J. Alzheimers Dis. 40:Suppl. 1 (2014), S113–S121.
9. [9] Trinczek, B., Biernat, J., Baumann, K., Mandelkow, E.M., Mandelkow, E., Domains of tau protein, differential phosphorylation, and dynamic instability of microtubules. Mol. Cell. Biol. 6 (1995), 1887–1902.
10. [10] Feinstein, H.E., Benbow, S.J., LaPointe, N.E., Patel, N., Ramachandran, S., Do, T.D., Gaylord, M.R., Huskey, N.E., Dressler, N., Korff, M., Quon, B., Cantrell, K.L., Bowers, M.T., Lal, R., Feinstein, S.C., Oligomerization of the microtubule-associated protein tau is mediated by its N-terminal sequences: implications for normal and pathological tau action. J. Neurochem. 137 (2016), 939–954.
11. [11] Dai, C., Chen, X., Kazim, S.F., Liu, F., Gong, C.-X., Grundke-Iqbal, I., Iqbal, K., Passive immunization targeting the N-terminal projection domain of tau decreases tau pathology and improves cognition in a transgenic mouse model of Alzheimer disease and tauopathies. J. Neural Transm. 122 (2015), 607–617.
12. [12] 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.
13. [13] Pedersen, J.T., Sigurdsson, E.M., Tau immunotherapy for Alzheimer's disease. Trends Mol. Med. 21 (2015), 394–402.
14. [14] Subramanian, S., Divya Shree, A.N., Expression, purification and characterization of a synthetic gene encoding human amyloid ß (Aß1-42) in Escherichia coli. Indian J. Biochem. Biophys. 44 (2007), 71–75.
15. [15] Subramanian, S., Divya Shree, A.N., Enhanced Th2 immunity after DNA prime-protein boost immunization with amyloid ß (1-42) plus CpG oligodeoxynucleotides in aged rats. Neurosci. Lett. 436 (2008), 219–222.
16. [16] Subramanian, N., Subramanian, S., Karande, A.A., Adiga, P.R., A monoclonal antibody to avidin dissociates quaternary structure and curtails biotin binding to avidin and streptavidin. Arch. Biochem. Biophys. 344 (1997), 281–288.
17. [17] Madhavadas, S., Kutty, B.M., Subramanian, S., Amyloid ß lowering and cognition enhancing effects of ghrelin receptor analog [D-Lys (3)] GHRP-6 in rat model of obesity. Indian J. Biochem. Biophys. 51 (2014), 257–262.
18. [18] Himmler, A., Drechsel, D., Kirschner, M.W., Martin, D.W., Tau consists of a set of proteins with repeated C-terminal microtubule-binding domains and variable N-terminal domains. Mol. Cell. Biol. 9 (1989), 1381–1388.
19. [19] Hasegawa, M., Morishima-Kawashima, M., Takio, K., Suzuki, M., Titani, K., Ihara, Y., Protein sequence and mass spectrometric analyses of tau in the Alzheimer's disease brain. J. Biol. Chem. 267 (1992), 17047–17054.
20. [20] Mi, K., Johnson, G.V., The role of phosphorylation in the pathogenesis of Alzheimer's disease. Curr. Alzheimer Res. 3 (2006), 449–463.
21. [21] Theunis, C., Crespo-Biel, N., Gafner, V., Pihlgren, M., Lopez-Deber, M.P., Reis, P., Hickman, D.T., Adolfsson, O., Chuard, N., Ndao, D.M., Borghgraef, P., Devijver, H., Van Leuven, F., Pfeifer, A., Muhs, A., Efficacy and safety of a liposome-based vaccine against protein Tau, assessed in tau P301L mice that model tauopathy. PLoS One, 8, 2013, e72301.
22. [22] Troquier, L., Caillierez, R., Burnouf, S., Fernandez-Gomez, F.J., Grosjean, M.E., Zommer, N., Sergeant, N., Schraen-Maschke, S., Blum, D., Buee, L., Targeting phosphor Ser422 by active tau immunotherapy in the THYTau22 mouse model: a suitable therapeutic approach. Curr. Alzheimer Res. 9 (2012), 397–405.
23. [23] Collin, L., Bohrmann, B., Gopfert, U., Oroszlan-Szovik, K., Ozmen, L., Gruninger, F., Neuronal uptake of tau/pS422 antibody and reduced progression of tau pathology in a mouse model of Alzheimer's disease. Brain 137 (2014), 2834–2846.
24. [24] Vita, R., Overton, J.A., Greenbaum, J.A., Ponomarenko, J., Clark, J.D., Cantrell, J.R., Wheeler, D.K., Gabbard, J.L., Hix, D., Sette, A., Peters, B., The immune epitope database (IEDB) 3.0. Nucleic Acids Res. 43 (2015), D405–D412.
25. [25] Gong, C.X., Liu, F., Grundke-Iqbal, I., Iqbal, K., Dysregulation of protein phosphorylation/dephosphorylation in Alzheimer's disease: a therapeutic target. J. Biomed. Biotechnol., 2006, 2006, 31825.
26. [26] Zhang, Z., Simpkins, J.W., An okadaic acid-induced model of tauopathy and cognitive deficiency. Brain Res. 1359 (2010), 233–246.
27. [27] M.E. Bach, R.D. Hawkins, M. Osman, E.R. Kandel, Impairment of spatial but not contextual memory in CaMKII mutant mice with a selective loss of hippocampal LTP in the range of the theta frequency, Cell 81 (19950 905–915.
28. [28] 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.