Structural determinants of tau aggregation inhibitor potency

Journal of Biological Chemistry

Volumn 288, Issue 45, 2013, Pages 32599-32611

  Schafer, Kelsey N ^a   Cisek, Katryna ^a   Huseby, Carol J ^a   Chang, Edward ^a   Kuret, Jeff ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATION INHIBITORS; ALZHEIMER DISEASE; ELECTRON DELOCALIZATION; MISSENSE MUTANTS; MOLECULAR TARGETS; POLARIZABILITIES; STRUCTURAL DETERMINANTS; THERAPEUTIC AGENTS;

POLARIZATION;

LIGANDS;

ARYLMETHINE; CYANIDIN 3,5 DIGLUCOSIDE; DODECYL SULFATE SODIUM; PHENOTHIAZINE; PROTEIN INHIBITOR; RHODAMINE; TAU PROTEIN; UNCLASSIFIED DRUG;

AB INITIO CALCULATION; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CORRELATION ANALYSIS; DRUG STRUCTURE; DRUG TARGETING; GENE DELETION; MICROTUBULE; MISSENSE MUTATION; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN STABILITY; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION;

AGGREGATION; ALZHEIMER DISEASE; CHEMICAL BIOLOGY; PROTEIN STRUCTURE; TAU;

HUMANS; MUTATION, MISSENSE; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RHODANINE; SEQUENCE DELETION; SODIUM DODECYL SULFATE; SOLUBILITY; TAU PROTEINS;

EID: 84887440374     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.503474     Document Type: Article

References (76)

1. Congdon, E. E., and Duff, K. E. (2008) Is tau aggregation toxic or protective? J. Alzheimers Dis. 14, 453-457
2. Honson, N. S., and Kuret, J. (2008) Tau aggregation and toxicity in tauopathic neurodegenerative diseases. J. Alzheimers Dis. 14, 417-422
3. Kuret, J. (2007) in Protein Folding Diseases: Enzyme Inhibitors and Other Agents as Prospective Therapies (Smith, H. J., Sewell, R. D. E., and Simons, C., eds) pp. 287-324, CRC Press, Taylor & Francis Books, Boca Raton, FL
4. Smith, M. C., and Gestwicki, J. E. (2012) Features of protein-protein interactions that translate into potent inhibitors. Topology, surface area and affinity. Expert Rev. Mol. Med. 14, e16
5. Wischik, C. M., Edwards, P. C., Harrington, C. R., Roth, M., and Klug, A. (October 11, 2005) Inhibition of tau-tau association. U.S. Patent 6,953,794
6. Wischik, C. M., Edwards, P. C., Lai, R. Y., Roth, M., and Harrington, C. R. (1996) Selective inhibition of Alzheimer disease-like tau aggregation by phenothiazines. Proc. Natl. Acad. Sci. U.S.A. 93, 11213-11218
7. Taniguchi, S., Suzuki, N., Masuda, M., Hisanaga, S., Iwatsubo, T., Goedert, M., and Hasegawa, M. (2005) Inhibition of heparin-induced Tau filament formation by phenothiazines, polyphenols, and porphyrins. J. Biol. Chem. 280, 7614-7623
8. Bulic, B., Pickhardt, M., Khlistunova, I., Biernat, J., Mandelkow, E. M., Mandelkow, E., and Waldmann, H. (2007) Rhodanine-based tau aggregation inhibitors in cell models of tauopathy. Angew. Chem. Int. Ed. Engl. 46, 9215-9219
9. Chirita, C., Necula, M., and Kuret, J. (2004) Ligand-dependent inhibition and reversal of Tau filament formation. Biochemistry 43, 2879-2887
10. Chang, E., Congdon, E. E., Honson, N. S., Duff, K. E., and Kuret, J. (2009) Structure-activity relationship of cyanine tau aggregation inhibitors. J. Med. Chem. 52, 3539-3547
11. Wischik, C. M., Bentham, P., Wischik, D. J., and Seng, K. M. (2008) Tau aggregation inhibitor (TAI) therapy with RemberTM arrests disease progression in mild and moderate Alzheimer's disease over 50 weeks. 11th International Conference on Alzheimer's Disease, Chicago, IL, July 26-31
12. Honson, N. S., Johnson, R. L., Huang, W., Inglese, J., Austin, C. P., and Kuret, J. (2007) Differentiating Alzheimer disease-associated aggregates with small molecules. Neurobiol. Dis. 28, 251-260
13. Schafer, K. N., Murale, D. P., Kim, K., Cisek, K., Kuret, J., and Churchill, D. G. (2011) Structure-activity relationship of cyclic thiacarbocyanine tau aggregation inhibitors. Bioorg. Med. Chem. Lett. 21, 3273-3276
14. Jensen, J. R., Cisek, K., Honson, N. S., and Kuret, J. (2011) Ligand polarizability contributes to tau fibril binding affinity. Bioorg. Med. Chem. 19, 5147-5154
15. Crowe, A., Ballatore, C., Hyde, E., Trojanowski, J. Q., and Lee, V. M. (2007) High throughput screening for small molecule inhibitors of heparin-induced tau fibril formation. Biochem. Biophys. Res. Commun. 358, 1-6
16. Bulic, B., Pickhardt, M., Mandelkow, E. M., and Mandelkow, E. (2010) Tau protein and tau aggregation inhibitors. Neuropharmacology 59, 276-289
17. Congdon, E. E., Kim, S., Bonchak, J., Songrug, T., Matzavinos, A., and Kuret, J. (2008) Nucleation-dependent tau filament formation. The importance of dimerization and an estimation of elementary rate constants. J. Biol. Chem. 283, 13806-13816
18. Kuret, J., Congdon, E. E., Li, G., Yin, H., Yu, X., and Zhong, Q. (2005) Evaluating triggers and enhancers of tau fibrillization. Microsc. Res. Tech. 67, 141-155
19. Li, W., Sperry, J. B., Crowe, A., Trojanowski, J. Q., Smith, A. B., 3rd, and Lee, V. M. (2009) Inhibition of tau fibrillization by oleocanthal via reaction with the amino groups of tau. J. Neurochem. 110, 1339-1351
20. Akoury, E., Pickhardt, M., Gajda, M., Biernat, J., Mandelkow, E., and Zweckstetter, M. (2013) Mechanistic basis of phenothiazine-driven inhibition of Tau aggregation. Angew. Chem. Int. Ed. Engl. 52, 3511-3515
21. Crowe, A., James, M. J., Lee, V. M., Smith, A. B., 3rd, Trojanowski, J. Q., Ballatore, C., and Brunden, K. R. (2013) Aminothienopyridazines and methylene blue affect Tau fibrillization via cysteine oxidation. J. Biol. Chem. 288, 11024-11037
22. Ahmad, B., Chen, Y., and Lapidus, L. J. (2012) Aggregation of α-synuclein is kinetically controlled by intramolecular diffusion. Proc. Natl. Acad. Sci. U.S.A. 109, 2336-2341
23. Ahmad, B., and Lapidus, L. J. (2012) Curcumin prevents aggregation in α-synuclein by increasing reconfiguration rate. J. Biol. Chem. 287, 9193-9199
24. Akoury, E., Gajda, M., Pickhardt, M., Biernat, J., Soraya, P., Griesinger, C., Mandelkow, E., and Zweckstetter, M. (2013) Inhibition of tau filament formation by conformational modulation. J. Am. Chem. Soc. 135, 2853-2862
25. Masuda, M., Suzuki, N., Taniguchi, S., Oikawa, T., Nonaka, T., Iwatsubo, T., Hisanaga, S., Goedert, M., and Hasegawa, M. (2006) Small molecule inhibitors of α-synuclein filament assembly. Biochemistry 45, 6085-6094
26. Carmel, G., Mager, E. M., Binder, L. I., and Kuret, J. (1996) The structural basis of monoclonal antibody Alz50's selectivity for Alzheimer's disease pathology. J. Biol. Chem. 271, 32789-32795
27. Chang, E., Kim, S., Yin, H., Nagaraja, H. N., and Kuret, J. (2008) Pathogenic missense MAPT mutations differentially modulate tau aggregation propensity at nucleation and extension steps. J. Neurochem. 107, 1113-1123
28. Gamblin, T. C., King, M. E., Kuret, J., Berry, R. W., and Binder, L. I. (2000) Oxidative regulation of fatty acid-induced tau polymerization. Biochemistry 39, 14203-14210
29. King, M. E., Gamblin, T. C., Kuret, J., and Binder, L. I. (2000) Differential assembly of human tau isoforms in the presence of arachidonic acid. J. Neurochem. 74, 1749-1757
30. Necula, M., and Kuret, J. (2004) A static laser light scattering assay for surfactant-induced tau fibrillization. Anal. Biochem. 333, 205-215
31. LoPresti, P., Szuchet, S., Papasozomenos, S. C., Zinkowski, R. P., and Binder, L. I. (1995) Functional implications for the microtubule-associated protein tau. Localization in oligodendrocytes. Proc. Natl. Acad. Sci. U.S.A. 92, 10369-10373
32. Kuret, J., Chirita, C. N., Congdon, E. E., Kannanayakal, T., Li, G., Necula, M., Yin, H., and Zhong, Q. (2005) Pathways of tau fibrillization. Biochim. Biophys. Acta 1739, 167-178
33. Li, G., Yin, H., and Kuret, J. (2004) Casein kinase 1δ phosphorylates Tau and disrupts its binding to microtubules. J. Biol. Chem. 279, 15938-15945
34. Cohen, T. J., Guo, J. L., Hurtado, D. E., Kwong, L. K., Mills, I. P., Trojanowski, J. Q., and Lee, V. M. (2011) The acetylation of tau inhibits its function and promotes pathological tau aggregation. Nat. Commun. 2, 252
35. Maeda, S., Sahara, N., Saito, Y., Murayama, M., Yoshiike, Y., Kim, H., Miyasaka, T., Murayama, S., Ikai, A., and Takashima, A. (2007) Granular tau oligomers as intermediates of tau filaments. Biochemistry 46, 3856-3861
36. Maeda, S., Sahara, N., Saito, Y., Murayama, S., Ikai, A., and Takashima, A. (2006) Increased levels of granular tau oligomers: an early sign of brain aging and Alzheimer's disease. Neurosci. Res. 54, 197-201
37. Cisek, K., Jensen, J. R., Honson, N. S., Schafer, K. N., Cooper, G. L., and Kuret, J. (2012) Ligand electronic properties modulate tau filament binding site density. Biophys. Chem. 170, 25-33
38. Necula, M., Chirita, C. N., and Kuret, J. (2005) Cyanine dye n744 inhibits tau fibrillization by blocking filament extension. Implications for the treatment of tauopathic neurodegenerative diseases. Biochemistry 44, 10227-10237
39. Mauri, A., Consonni, V., Pavan, M., and Todeschini, R. (2006) Dragon software. An easy approach to molecular descriptor calculations. Commun. Math. Comp. Chem. 56, 237-248
40. Consonni, V., and Todeschini, R. (2000) Handbook of Molecular Descriptors, Wiley-VCH, New York
41. Kurunczi, L., Funar-Timofei, S., Bora, A., and Seclanian, E. (2007) Application of the MTD-PLS method to heterocyclic dye-cellulose interactions. Int. J. Quantum Chem. 107, 2057-2065
42. Metivier-Pignon, H., Faur, C., and Le Cloirec, P. (2007) Adsorption of dyes onto activated carbon cloth. Using QSPRs as tools to approach adsorption mechanisms. Chemosphere 66, 887-893
43. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Scalmani, G., Barone, V., Mennucci, B., Petersson, G. A., and Nakatsuji, H. (2009) Gaussian 09, Revision A.1, Gaussian, Inc., Wallingford, CT
44. Jacquemin, D., Perpète, E. A., Ciofini, I., and Adamo, C. (2009) Accurate simulation of optical properties in dyes. Acc. Chem. Res. 42, 326-334
45. Cisek, K., and Kuret, J. (2012) QSAR studies for prediction of cross- sheet aggregate binding affinity and selectivity. Bioorg. Med. Chem. 20, 1434-1441
46. Golbraikh, A., and Tropsha, A. (2002) Beware of q2! J. Mol. Graph. Model. 20, 269-276
47. Chirita, C. N., Necula, M., and Kuret, J. (2003) Anionic micelles and vesicles induce Tau fibrillization in vitro. J. Biol. Chem. 278, 25644-25650
48. Ryan, A. J., Gray, N. M., Lowe, P. N., and Chung, C. W. (2003) Effect of detergent on "promiscuous" inhibitors. J. Med. Chem. 46, 3448-3451
49. Hansch, C., Leo, A., and Taft, R. W. (1991) A survey of Hammett substituent constants and resonance and field parameters. Chem. Rev. 91, 165-195
50. Konovalov, D. A., Llewellyn, L. E., Vander Heyden, Y., and Coomans, D. (2008) Robust cross-validation of linear regressionQSARmodels. J. Chem. Inf. Model. 48, 2081-2094
51. Tetko, I. V., Tanchuk, V. Y., and Villa, A. E. (2001) Prediction of n-octanol/ water partition coefficients from PHYSPROP database using artificial neural networks and E-state indices. J. Chem. Inf. Comput. Sci. 41, 1407-1421
52. Ertl, P., Rohde, B., and Selzer, P. (2000) Fast calculation of molecular polar surface area as a sum of fragment-based contributions and its application to the prediction of drug transport properties. J. Med. Chem. 43, 3714-3717
53. Verhaar, H. J., Solbé, J., Speksnijder, J., van Leeuwen, C. J., and Hermens, J. L. (2000) Classifying environmental pollutants. Part 3. External validation of the classification system. Chemosphere 40, 875-883
54. Tetko, I. V., Tanchuk, V. Y., Kasheva, T. N., and Villa, A. E. (2001) Estimation of aqueous solubility of chemical compounds using E-state indices. J. Chem. Inf. Comput. Sci. 41, 1488-1493
55. Abraha, A., Ghoshal, N., Gamblin, T. C., Cryns, V., Berry, R. W., Kuret, J., and Binder, L. I. (2000) C-terminal inhibition of tau assembly in vitro and in Alzheimer's disease. J. Cell Sci. 113, 3737-3745
56. von Bergen, M., Barghorn, S., Li, L., Marx, A., Biernat, J., Mandelkow, E. M., and Mandelkow, E. (2001) Mutations of tau protein in frontotemporal dementia promote aggregation of paired helical filaments by enhancing local -structure. J. Biol. Chem. 276, 48165-48174
57. von Bergen, M., Friedhoff, P., Biernat, J., Heberle, J., Mandelkow, E. M., and Mandelkow, E. (2000) Assembly of tau protein into Alzheimer paired helical filaments depends on a local sequence motif (306VQIVYK311) forming structure. Proc. Natl. Acad. Sci. U.S.A. 97, 5129-5134
58. Barghorn, S., and Mandelkow, E. (2002) Toward a unified scheme for the aggregation of tau into Alzheimer paired helical filaments. Biochemistry 41, 14885-14896
59. Rademakers, R., Cruts, M., and van Broeckhoven, C. (2004) The role of tau (MAPT) in frontotemporal dementia and related tauopathies. Hum. Mutat. 24, 277-295
60. Dähne, S. (1978) Color and constitution. One hundred years of research. Science 199, 1163-1167
61. Liu, X., Tu, M., Kelly, R. S., Chen, C., and Smith, B. J. (2004) Development of a computational approach to predict blood-brain barrier permeability. Drug Metab. Dispos. 32, 132-139
62. Ehrnhoefer, D. E., Bieschke, J., Boeddrich, A., Herbst, M., Masino, L., Lurz, R., Engemann, S., Pastore, A., and Wanker, E. E. (2008) EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers. Nat. Struct. Mol. Biol. 15, 558-566
63. Hong, D. P., Fink, A. L., and Uversky, V. N. (2008) Structural characteristics of α-synuclein oligomers stabilized by the flavonoid baicalein. J. Mol. Biol. 383, 214-223
64. Masuda, M., Hasegawa, M., Nonaka, T., Oikawa, T., Yonetani, M., Yamaguchi, Y., Kato, K., Hisanaga, S., and Goedert, M. (2009) Inhibition of α-synuclein fibril assembly by small molecules: analysis using epitopespecific antibodies. FEBS Lett. 583, 787-791
65. Necula, M., and Kuret, J. (2005) Site-specific pseudophosphorylation modulates the rate of tau filament dissociation. FEBS Lett. 579, 1453-1457
66. Jensen, J. R., Cisek, K., Funk, K. E., Naphade, S., Schafer, K. N., and Kuret, J. (2011) Research towards tau imaging. J. Alzheimers Dis. 26, 147-157
67. Ono, K., Li, L., Takamura, Y., Yoshiike, Y., Zhu, L., Han, F., Mao, X., Ikeda, T., Takasaki, J., Nishijo, H., Takashima, A., Teplow, D. B., Zagorski, M. G., and Yamada, M. (2012) Phenolic compounds prevent amyloid -protein oligomerization and synaptic dysfunction by site-specific binding. J. Biol. Chem. 287, 14631-14643
68. Rao, J. N., Dua, V., and Ulmer, T. S. (2008) Characterization of α-synuclein interactions with selected aggregation-inhibiting small molecules. Biochemistry 47, 4651-4656
69. Lamberto, G. R., Binolfi, A., Orcellet, M. L., Bertoncini, C. W., Zweckstetter, M., Griesinger, C., and Fernández, C. O. (2009) Structural and mechanistic basis behind the inhibitory interaction of PcTS on α-synuclein amyloid fibril formation. Proc. Natl. Acad. Sci. U.S.A. 106, 21057-21062
70. Richter, L., Munter, L. M., Ness, J., Hildebrand, P. W., Dasari, M., Unterreitmeier, S., Bulic, B., Beyermann, M., Gust, R., Reif, B., Weggen, S., Langosch, D., and Multhaup, G. (2010) Amyloid42 peptide (A42)-lowering compounds directly bind to A and interfere with amyloid precursor protein (APP) transmembrane dimerization. Proc. Natl. Acad. Sci. U.S.A. 107, 14597-14602
71. Tomoo, K., Yao, T. M., Minoura, K., Hiraoka, S., Sumida, M., Taniguchi, T., and Ishida, T. (2005) Possible role of each repeat structure of the microtubule- binding domain of the tau protein in in vitro aggregation. J. Biochem. 138, 413-423
72. Congdon, E. E., Figueroa, Y. H., Wang, L., Toneva, G., Chang, E., Kuret, J., Conrad, C., and Duff, K. E. (2009) Inhibition of tau polymerization with a cyanine dye in two distinct model systems. J. Biol. Chem. 284, 20830-20839
73. Lasagna-Reeves, C. A., Castillo-Carranza, D. L., Guerrero-Muoz, M. J., Jackson, G. R., and Kayed, R. (2010) Preparation and characterization of neurotoxic tau oligomers. Biochemistry 49, 10039-10041
74. Uversky, V. N. (2010) The mysterious unfoldome. Structureless, underappreciated, yet vital part of any given proteome. J. Biomed. Biotechnol. 2010, 568068
75. Selkoe, D. J., Ihara, Y., and Salazar, F. J. (1982) Alzheimer's disease. Insolubility of partially purified paired helical filaments in sodium dodecyl sulfate and urea. Science 215, 1243-1245
76. Goedert, M., Spillantini, M. G., Potier, M. C., Ulrich, J., and Crowther, R. A. (1989) Cloning and sequencing of the cDNA encoding an isoform of microtubule-associated protein tau containing four tandem repeats. Differential expression of tau protein mRNAs in human brain. EMBO J. 8, 393-399