Monoclonal antibody MN423 as a stable mold facilitates structure determination of disordered tau protein

Journal of Structural Biology

Volumn 171, Issue 1, 2010, Pages 74-81

  Skrabana, Rostislav ^a,b   Dvorsky, Radovan ^c   Sevcik, Jozef ^a,d   Novak, Michal ^a,b  

^a INSTITUTE OF NEUROIMMUNOLOGY   (Slovakia)

^b Axon Neuroscience Forschungs und Entwicklungs GmbH   (Austria)

^c MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^d INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

Conformation specific monoclonal antibody; Core PHF; In silico docking; Intrinsically disordered protein; Tau protein; X ray structure

Indexed keywords

MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY MN423; RECOMBINANT PROTEIN; TAU PROTEIN; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ANTIBODY COMBINING SITE; ANTIBODY STRUCTURE; ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; COMPUTER MODEL; CONTROLLED STUDY; MOLECULAR DOCKING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

ANTIBODIES, MONOCLONAL; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; TAU PROTEINS;

EID: 77953616095     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2010.02.016     Document Type: Article

References (51)

1. Alonso A., Zaidi T., Novak M., Grundke-Iqbal I., Iqbal K. Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments. Proc. Natl. Acad. Sci. USA 2001, 98:6923-6928.
2. Andronesi O.C., von Bergen M., Biernat J., Seidel K., Griesinger C., Mandelkow E., Baldus M. Characterization of Alzheimer's-like paired helical filaments from the core domain of tau protein using solid-state NMR spectroscopy. J. Am. Chem. Soc. 2008, 130:5922-5928.
3. Barghorn S., Davies P., Mandelkow E. Tau paired helical filaments from Alzheimer's disease brain and assembled in vitro are based on beta-structure in the core domain. Biochemistry 2004, 43:1694-1703.
4. Berriman J., Serpell L.C., Oberg K.A., Fink A.L., Goedert M., Crowther R.A. Tau filaments from human brain and from in vitro assembly of recombinant protein show cross-beta structure. Proc. Natl. Acad. Sci. USA 2003, 100:9034-9038.
5. Bonvin A.M. Flexible protein-protein docking. Curr. Opin. Struct. Biol. 2006, 16:194-200.
6. Chakrabarti P., Bhattacharyya R. Geometry of nonbonded interactions involving planar groups in proteins. Prog. Biophys. Mol. Biol. 2007, 95:83-137.
7. Collaborative Computational Project, N, 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D D50, 760-763.
8. Csokova N., Skrabana R., Urbanikova L., Kovacech B., Popov A., Sevcik J., Novak M. Preparation, crystallization and preliminary X-ray analysis of the Fab fragment of monoclonal antibody MN423, revealing the structural aspects of Alzheimer's paired helical filaments. Protein Pept. Lett. 2006, 13:941-944.
9. Davis I.W., Leaver-Fay A., Chen V.B., Block J.N., Kapral G.J., Wang X., Murray L.W., Arendall W.B., Snoeyink J., Richardson J.S., Richardson D.C. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 2007, 35:W375-W383.
10. DeLano, W.L., 2002. The PyMOL Molecular Graphics System. DeLano Scientific LLC, San Carlos, CA, USA. Available from: http://www.pymol.org.
11. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 2004, 60:2126-2132.
12. Garcia M.L., Cleveland D.W. Going new places using an old MAP: tau, microtubules and human neurodegenerative disease. Curr. Opin. Cell Biol. 2001, 13:41-48.
13. Ghoshal N., Garcia-Sierra F., Fu Y., Beckett L.A., Mufson E.J., Kuret J., Berry R.W., Binder L.I. Tau-66: evidence for a novel tau conformation in Alzheimer's disease. J. Neurochem. 2001, 77:1372-1385.
14. Hagestedt T., Lichtenberg B., Wille H., Mandelkow E.M., Mandelkow E. Tau protein becomes long and stiff upon phosphorylation: correlation between paracrystalline structure and degree of phosphorylation. J. Cell Biol. 1989, 109:1643-1651.
15. James L.C., Roversi P., Tawfik D.S. Antibody multispecificity mediated by conformational diversity. Science 2003, 299:1362-1367.
16. 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. 1997, 48:128-132.
17. Jicha G.A., Lane E., Vincent I., Otvos L., Hoffmann R., Davies P. A conformation- and phosphorylation-dependent antibody recognizing the paired helical filaments of Alzheimer's disease. J. Neurochem. 1997, 69:2087-2095.
18. Khuebachova M., Verzillo V., Skrabana R., Ovecka M., Vaccaro P., Panni S., Bradbury A., Novak M. Mapping the C terminal epitope of the Alzheimer's disease specific antibody MN423. J. Immunol. Methods 2002, 262:205-215.
19. Kowalsman N., Eisenstein M. Combining interface core and whole interface descriptors in postscan processing of protein-protein docking models. Proteins 2009, 77:297-318.
20. Lamzin V., Wilson K.S. Automated refinement for protein crystallography. Methods Enzymol. 1997, 277:269-305.
21. Laskowski R.A., Macarthur M.W., Moss D.S., Thornton J.M. Procheck - a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 1993, 26:283-291.
22. Lichtenberg B., Mandelkow E.M., Hagestedt T., Mandelkow E. Structure and elasticity of microtubule-associated protein tau. Nature 1988, 334:359-362.
23. Lovell S.C., Davis I.W., Arendall W.B., de Bakker P.I., Word J.M., Prisant M.G., Richardson J.S., Richardson D.C. Structure validation by Calpha geometry: phi, psi and Cbeta deviation. Proteins 2003, 50:437-450.
24. MacCallum R.M., Martin A.C., Thornton J.M. Antibody-antigen interactions: contact analysis and binding site topography. J. Mol. Biol. 1996, 262:732-745.
25. Mittag T., Forman-Kay J.D. Atomic-level characterization of disordered protein ensembles. Curr. Opin. Struct. Biol. 2007, 17:3-14.
26. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D 1997, 53:240-255.
27. Nair D.T., Singh K., Siddiqui Z., Nayak B.P., Rao K.V., Salunke D.M. Epitope recognition by diverse antibodies suggests conformational convergence in an antibody response. J. Immunol. 2002, 168:2371-2382.
28. Notkins A.L. Polyreactivity of antibody molecules. Trends Immunol. 2004, 25:174-179.
29. Novak M. Truncated tau protein as a new marker for Alzheimer's disease. Acta Virol. 1994, 38:173-189.
30. Novak M., Kabat J., Wischik C.M. Molecular characterization of the minimal protease resistant tau unit of the Alzheimer's disease paired helical filament. EMBO J. 1993, 12:365-370.
31. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Macromol. Crystallogr. A 1997, 276:307-326.
32. Painter J., Merritt E.A. Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr. D Biol. Crystallogr. 2006, 62:439-450.
33. Rosenberg K.J., Ross J.L., Feinstein H.E., Feinstein S.C., Israelachvili J. Complementary dimerization of microtubule-associated tau protein: implications for microtubule bundling and tau-mediated pathogenesis. Proc. Natl. Acad. Sci. USA 2008, 105:7445-7450.
34. Sawaya M.R., Sambashivan S., Nelson R., Ivanova M.I., Sievers S.A., Apostol M.I., Thompson M.J., Balbirnie M., Wiltzius J.J., McFarlane H.T., Madsen A.O., Riekel C., Eisenberg D. Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 2007, 447:453-457.
35. Sevcik J., Skrabana R., Kontsekova E., Novak M. Structure solution of misfolded conformations adopted by intrinsically disordered Alzheimer's tau protein. Protein Pept. Lett. 2009, 16:61-64.
36. Sevcik J., Skrabana R., Dvorsky R., Csokova N., Iqbal K., Novak M. X-ray structure of the PHF core C-terminus: insight into the folding of the intrinsically disordered protein tau in Alzheimer's disease. FEBS Lett. 2007, 581:5872-5878.
37. Sheriff S., Jeffrey P.D., Bajorath J. Comparison of CH1 domains in different classes of murine antibodies. J. Mol. Biol. 1996, 263:385-389.
38. Sillen A., Leroy A., Wieruszeski J.M., Loyens A., Beauvillain J.C., Buee L., Landrieu I., Lippens G. Regions of tau implicated in the paired helical fragment core as defined by NMR. Chembiochem 2005, 6:1849-1856.
39. Skrabana R., Sevcik J., Novak M. Intrinsically disordered proteins in the neurodegenerative processes: formation of tau protein paired helical filaments and their analysis. Cell. Mol. Neurobiol. 2006, 26:1085-1097.
40. Skrabana R., Skrabanova-Khuebachova M., Kontsek P., Novak M. Alzheimer's-disease-associated conformation of intrinsically disordered tau protein studied by intrinsically disordered protein liquid-phase competitive enzyme-linked immunosorbent assay. Anal. Biochem. 2006, 359:230-237.
41. Skrabana R., Kontsek P., Mederlyova A., Iqbal K., Novak M. Folding of Alzheimer's core PHF subunit revealed by monoclonal antibody 423. FEBS Lett. 2004, 568:178-182.
42. Skrabana R., Skrabanova M., Csokova N., Sevcik J., Novak M. Intrinsically disordered tau protein in Alzheimer's tangles: a coincidence or a rule?. Bratisl. Lek. Listy 2006, 107:354-358.
43. Tompa P. The interplay between structure and function in intrinsically unstructured proteins. FEBS Lett. 2005, 579:3346-3354.
44. Uversky V.N. Natively unfolded proteins: a point where biology waits for physics. Protein Sci. 2002, 11:739-756.
45. Vagin A., Teplyakov A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallogr. 1997, 30:1022-1025.
46. Vechterova L., Kontsekova E., Zilka N., Ferencik M., Ravid R., Novak M. DC11: a novel monoclonal antibody revealing Alzheimer's disease-specific tau epitope. Neuroreport 2003, 14:87-91.
47. von Bergen M., Friedhoff P., Biernat J., Heberle J., Mandelkow E.M., Mandelkow E. Assembly of tau protein into Alzheimer paired helical filaments depends on a local sequence motif ((306)VQIVYK(311)) forming beta structure. Proc. Natl. Acad. Sci. USA 2000, 97:5129-5134.
48. Wedemayer G.J., Patten P.A., Wang L.H., Schultz P.G., Stevens R.C. Structural insights into the evolution of an antibody combining site. Science 1997, 276:1665-1669.
49. Wischik C.M., Novak M., Thogersen H.C., Edwards P.C., Runswick M.J., Jakes R., Walker J.E., Milstein C., Roth M., Klug A. Isolation of a fragment of tau derived from the core of the paired helical filament of Alzheimer disease. Proc. Natl. Acad. Sci. USA 1988, 85:4506-4510.
50. Zilka N., Filipcik P., Koson P., Fialova L., Skrabana R., Zilkova M., Rolkova G., Kontsekova E., Novak M. Truncated tau from sporadic Alzheimer's disease suffices to drive neurofibrillary degeneration in vivo. FEBS Lett. 2006, 580:3582-3588.
51. Zimmermann J., Oakman E.L., Thorpe I.F., Shi X., Abbyad P., Brooks C.L., Boxer S.G., Romesberg F.E. Antibody evolution constrains conformational heterogeneity by tailoring protein dynamics. Proc. Natl. Acad. Sci. USA 2006, 103:13722-13727.