Antibody recognition and conformational flexibility of a plaque-specific β-amyloid epitope modulated by non-native peptide flanking regions

Journal of Medicinal Chemistry

Volumn 51, Issue 5, 2008, Pages 1150-1161

  Manea, Marilena ^a   Kalászi, Adrían ^b   Mezo, Gábor ^c   Horváti, Kata ^c   Bodor, Andrea ^b   Horváth, Anikó ^c   Farkas, Ödön ^b   Perczel, András ^b   Przybylski, Michael ^a   Hudecz, Ferenc ^b,c,d  

^a UNIVERSITY OF KONSTANZ   (Germany)

^b EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^c EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^d INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN;

ANTIGEN BINDING; ARTICLE; CIRCULAR DICHROISM; CONFORMATION; CYCLIZATION; DNA FLANKING REGION; ENZYME LINKED IMMUNOSORBENT ASSAY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN SYNTHESIS; QUANTITATIVE STRUCTURE ACTIVITY RELATION;

ALANINE; AMYLOID BETA-PROTEIN; ANTIBODIES, MONOCLONAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITOPES; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; PEPTIDES, CYCLIC; PROTEIN BINDING; PROTEIN CONFORMATION; QUANTITATIVE STRUCTURE-ACTIVITY RELATIONSHIP; SENILE PLAQUES; SOLUTIONS;

EID: 41749119674     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm070196e     Document Type: Article

References (58)

1. Weiner, H. L.; Lemere, C. A.; Maron, R.; Spooner, E. T.; Grenfell, T. J.; Mori, C.; Issazdeh, S.; Hancock, W. W.; Selkoe, D. J. Nasal administration of amyloid-beta peptide decreases cerebral amyloid burden in a mouse model of Alzheimer's disease. Ann. Neurol. 2000, 48, 567-579.
2. Schenk, D.; Barbour, R.; Dunn, W.; Gordon, G.; Grajeda, H.; Guido, T.; Hu, K.; Huang, J. P.; Johnson-Wood, K.; Khan, K.; Kholodenko, D.; Lee, M.; Liao, Z. M.; Lieberburg, I.; Motter, R.; Mutter, L.; Soriano, F.; Shopp, G.; Vasquez, N.; Vandevert, C.; Walker, S.; Wogulis, M.; Yednock, T.; Games, D.; Seubert, P. Immunization with amyloid-beta attenuates Alzheimer disease-like pathology in the PDAPP mouse. Nature 1999, 400, 173-177.
3. Janus, C.; Pearson, J.; McLaurin, J.; Mathews, P. M.; Jiang, Y.; Schmidt, S. D.; Chishti, M. A.; Horne, P.; Heslin, D.; French, J.; Mount, H. T. J.; Nixon, R. A.; Mercken, M.; Bergeron, C.; Fraser, P. E.; St. George-Hyslop, P.; Westaway, D. A beta peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature 2000, 408, 979-982.
4. Bard, F.; Cannon, C.; Barbour, R.; Burke, R. L.; Games, D.; Grajeda, H.; Guido, T.; Hu, K.; Huang, J. P.; Johnson-Wood, K.; Khan, K.; Kholodenko, D.; Lee, M.; Lieberburg, I.; Motter, R.; Nguyen, M.; Soriano, F.; Vasquez, N.; Weiss, K.; Welch, B.; Seubert, P.; Schenk, D.; Yednock, T. Peripherally administered antibodies against amyloid beta-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nature Med. 2000, 6, 916-919.
5. DeMattos, R. B.; Bales, K. R.; Cummins, D. J.; Dodart, J. C.; Paul, S. M.; Holtzman, D. M. Peripheral anti-A beta antibody alters CNS and plasma A beta clearance and decreases brain A beta burden in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 8850-8855.
6. Morgan, D.; Diamond, D. M.; Gottschall, P. E.; Ugen, K. E.; Dickey, C.; Hardy, J.; Duff, K.; Jantzen, P.; DiCarlo, G.; Wilcock, D.; Connor, K.; Hatcher, J.; Hope, C.; Gordon, M.; Arendash, G. W. A beta peptide vaccination prevents memory loss in an animal model of Alzheimer's disease. Nature 2000, 408, 982-985.
7. McLaurin, J.; Cecal, R.; Kierstead, M. E.; Tian, X.; Phinney, A. L.; Manea, M.; French, J. E.; Lambermon, M. H. L.; Darabie, A. A.; Brown, M. E.; Janus, C.; Chishti, M. A.; Horne, P.; Westaway, D.; Fraser, P. E.; Mount, H. T. J.; Przybylski, M.; St George-Hyslop, P. Therapeutically effective antibodies against amyloid-beta peptide target amyloid-beta residues 4-10 and inhibit cytotoxicity and fibrillogenesis. Nature Med. 2002, 8, 1263-1269.
8. Drakopoulou, E.; Uray, K.; Mezö, G.; Price, M. R.; Vita, C.; Hudecz, F. Synthesis and antibody recognition of mucin 1 (MUC1)-alpha-conotoxin chimera. J. Peptide Sci. 2000, 6, 175-185.
9. Hudecz, F. Manipulation of epitope function by modification of peptide structure: A minireview. Biologicals 2001, 29, 197-207.
10. Mezö, G.; Drakopoulou, E.; Paál, V.; Rajnavölgyi, E.; Vita, C.; Hudecz, F. Synthesis and immunological studies of alpha-conotoxin chimera containing an immunodominant epitope from the 268-284 region of HSV gD protein. J. Peptide Res. 2000, 55, 7-17.
11. Tugyi, R.; Mezö, G.; Fellinger, E.; Andreu, D.; Hudecz, F. The effect of cyclization on the enzymatic degradation of herpes simplex virus glycoprotein D derived epitope peptide. J. Peptide Sci. 2005, 11, 642-649.
12. Tugyi, R.; Uray, K.; Iván, D.; Fellinger, E.; Perkins, A.; Hudecz, F. Partial D-amino acid substitution: Improved enzymatic stability and preserved Ab recognition of a MUC2 epitope peptide. Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 413-418.
13. Wilkinson, K. A.; Vordermeier, M. H.; Kajtár, J.; Jurcevic, S.; Wilkinson, R.; Ivanyi, J.; Hudecz, F. Modulation of peptide specific T cell responses by non-native flanking regions. Mol. Immunol. 1997, 34, 1237-1246.
14. Mezö, G.; de Oliveira, E.; Krikorian, D.; Feijlbrief, M.; Jakab, A.; Tsikaris, V.; Sakarellos, C.; Welling-Wester, S.; Andreu, D.; Hudecz, F. Synthesis and comparison of antibody recognition of conjugates containing herpes simplex vims type 1 glycoprotein D epitope VII. Bioconjugate Chem. 2003, 14, 1260-1269.
15. Manea, M.; Mezö, G.; Hudecz, F.; Przybylski, M. Polypeptide conjugates comprising a beta-amyloid plaque-specific epitope as new vaccine structures against Alzheimer's disease. Biopolymers 2004, 76, 503-511.
16. Manea, M.; Hudecz, F.; Przybylski, M.; Mezö, G. Synthesis, solution conformation, and antibody recognition of oligotuftsin-based conjugates containing a beta-amyloid(4-10) plaque-specific epitope. Bioconjugate Chem. 2005, 16, 921-928.
17. Hopfinger, A. J.; Wang, S.; Tokarski, J. S.; Jin, B. Q.; Albuquerque, M.; Madhav, P. J.; Duraiswami, C. Construction of 3D-QSAR models using the 4D-QSAR analysis formalism. J. Am. Chem. Soc. 1997, 119, 10509-10524.
18. Vedani, A.; Briem, K.; Dobler, M.; Dollinger, H.; McMasters, D. R. Multiple-conformation and protonation-state representation in 4D-QSAR: The neurokinin-1 receptor system. J. Med. Chem. 2000, 43, 4416-4427.
19. Martinek, T. A.; Ötvös, F.; Dervarics, M.; Tóth, G.; Fülöp, F. Ligand-based prediction of active conformation by 3D-QSAR flexibility descriptors and their application in 3 + 3D-QSAR models. J. Med. Chem. 2005, 48, 3239-3250.
20. Bhonsle, J. B.; Wang, Z. X.; Tamamura, H.; Fujii, N.; Peiper, S. C.; Trent, J. O. A simple, automated quasi-4D-QSAR, quasi-multi way PLS approach to develop highly predictive QSAR models for highly flexible CXCR4 inhibitor cyclic pentapeptide ligands using scripted common molecular modeling tools. QSAR Comb. Sci. 2005, 24, 620-630.
21. Bhonsle, J. B.; Bhattacharjee, A. K.; Gupta, R. K. Novel semiautomated methodology for developing highly predictive QSAR models: application for development of QSAR models for insect repellent amides. J. Mol. Model. 2007, 13, 179-208.
22. Dervarics, M.; Otvos, F.; Martinek, T. A. Development of a chirality-sensitive flexibility descriptor for 3 + 3D-QSAR. J. Chem. Inf. Mod. 2006, 46, 1431-1438.
23. Kalászi, A.; Farkas, Ö. Lead conformer prediction based on a library of flexible molecules. THEOCHEM 2003, 666, 645-649.
24. Kalászi, A.; Imre, G.; Jákli, I.; Farkas, Ö. Identification of the bioactive conformation for mucin epitope peptides. THEOCHEM 2007, 823, 16-27.
25. Janssen, L. H. M. Conformational flexibility and receptor interaction. Bioorg. Med. Chem. 1998, 6, 785-788.
26. Yung-Chi, Cheng.; Prusoff, W. H. Relationship between the inhibition constant (Ki) and the concentration of inhibitor which causes 50% inhibition (150) of an enzymatic reaction. Biochem. Pharmacol. 1973, 22, 3099-3108.
27. Nicklaus, M. C.; Wang, S. M.; Driscoll, J. S.; Milne, G. W. A. Conformational-changes of small molecules binding to proteins. Bioorg. Med. Chem. 1995, 3, 411-428.
28. Perola, E.; Charifson, P. S. Conformational analysis of drag-like molecules bound to proteins: An extensive study of ligand reorganization upon binding. J. Med. Chem. 2004, 47, 2499-2510.
29. Stockwell, G. R.; Thornton, J. M. Conformational diversity of ligands bound to proteins. J. Mol. Biol. 2006, 356, 928-944.
30. Steer, D.; Lew, R.; Perlmutter, P.; Smith, A. I.; Aguilar, M. I. Inhibitors of metalloendopeptidase EC 3.4.24.15 and EC 3.4.24.16 stabilized against proteolysis by the incorporation of beta-amino acids. Biochemistry 2002, 41, 10819-10826.
31. Briand, J. P.; Benkirane, N.; Guichard, G.; Newman, J. F. E.; vanRegenmortel, M. H. V.; Brown, F.; Muller, S. A retro-inverso peptide corresponding to the GH loop of foot-and-mouth disease virus elicits high levels of long-lasting protective neutralizing antibodies. Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 12545-12550.
32. Hamamoto, K.; Kida, Y.; Zhang, Y.; Shimizu, T.; Kuwano, K. Antimicrobial activity and stability to proteolysis of small linear cationic peptides with D-amino acid substitutions. Microbiol. Immunol. 2002, 46, 741-749.
33. Conley, A. J.; Conard, P.; Bondy, S.; Dolan, C. A.; Hannah, J.; Leanza, W. J.; Marburg, S.; Rivetna, M.; Rusiecki, V. K.; Sugg, E. E.; Vanmiddlesworth, F.; Warne, S. A.; Ulrich, J. T.; Rudbach, J. A.; Tolman, R. L.; Emini, E. A. Immunogenicity of Synthetic Hiv-1 Gp120 V3-Loop Peptide-Conjugate Immunogens. Vaccine 1994, 12, 445-451.
34. Muller, S.; Plaue, S.; Samama, J. P.; Valette, M.; Briand, J. P.; van Regenmortel, M. H. V. Antigenic properties and protective capacity of a cyclic peptide corresponding to site-A of Influenza-virus hemagglutinin. Vaccine 1990, 8, 308-314.
35. Schulzegahmen, U.; Klenk, H. D.; Beyreuther, K. Immunogenicity of loop-structured short synthetic peptides mimicking the antigenic site A of Influenza-virus hemagglutinin. Eur. J. Biochem. 1986, 159, 283-289.
36. Williams, W. V.; Kieberemmons, T.; Vonfeldt, J.; Greene, M. I.; Weiner, D. B. Design of bioactive peptides based on antibody hypervariable region structures - development of conformationally constrained and dimeric peptides with enhanced affinity. J. Biol. Chem. 1991, 266, 5182-5190.
37. Schlosser, G.; Mezö, G.; Kiss, R.; Vass, E.; Majer, Z.; Feijlbrief, M.; Perczel, A.; Bösze, S.; Welling-Wester, S.; Hudecz, F. Synthesis, solution structure analysis and antibody binding of cyclic epitope peptides from glycoprotein D of Herpes simplex virus type I. Biophys. Chem. 2003, 106, 155-171.
38. Valero, M. L.; Camarero, J. A.; Haack, T.; Mateu, M. G.; Domingo, E.; Giralt, E.; Andreu, D. Native-like cyclic peptide models of a viral antigenic site: finding a balance between rigidity and flexibility. J. Mol. Recognit. 2000, 13, 5-13.
39. van Regelmortel M. H. V.; Briand, J. P.; Muller, S.; Plaue, S. In Laboratory techniques in biochemistry and molecular biology; Burdon, R. H., Knippenberg, P. H., Eds.; Elsevier: Amsterdam, The Netherlands: 1988; pp 145-158.
40. Buck, M. Trifluoroethanol and colleagues: cosolvents come of age. Recent studies with peptides and proteins. Q. Rev. Biophys. 1998, 31, 297-355.
41. Goodman, M.; Listowsky, I. Conformational aspects of synthetic polypeptides VI. Hypochromic spectral studies of oligo-γ-methyl-L- glutamate peptides. J. Am. Chem. Soc. 1962, 84, 3770-3771.
42. Nelson, J. W.; Kallenbach, N. R. Stabilization of the ribonuclease S-peptide α helix by trifluoroethanol. Proteins 1986, 1, 211-217.
43. Woody, R. W. In Circular dichroism - Principles and applications; Woody, R. W., Nakanishi, K., Berova, N., Eds.; VCH Publishers, Inc.: New York, 1996; pp 473-496.
44. Vass, E.; Hollósi, M.; Besson, F.; Buchet, R. Vibrational spectroscopic detection of beta- and gamma-turns in synthetic and natural peptides and proteins. Chem. Rev. 2003, 103, 1917-1954.
45. Woody, R. W. In The peptides-Analysis, Synthesis, Biology; Udenfriend, S. Meienhofer, J., Eds.; Academic Press, Inc.: New York, 1985; pp 15-114.
46. Uray, K.; Kajtár, J.; Vass, E.; Price, M. R.; Hollósi, M.; Hudecz, F. Effect of D-amino acid substitution in a mucin 2 epitope on mucin-specific monoclonal antibody recognition. Arch. Biochem. Biophys. 2000, 378, 25-32.
47. Cheng, R. P.; Gellman, S. H.; DeGrado, W. F. beta-peptides: From structure to function. Chem. Rev. 2001, 101, 3219-3232.
48. Iverson, H. A.; Fox, D., III; Nadler, L. S.; Klevit, R. E.; Nathanson, N. M. Identification and structural determination of the M3 muscarinic acetylcholine receptor baselatoral sorting signal. J. Biol. Chem. 2005, 280, 24568-24575.
49. Heisterberg, D. J. Quaternion fit source code. http://www.ccl.net/cca/ software/SOURCES/C/quaternion-mol-fit/quatfit. 1990.
50. Barnard, J. M.; Downs, G. M. Chemical fragment generation and clustering software. J. Chem. Inf. Comput. Sci. 1997, 37, 141-142.
51. Brown, R. D.; Martin, Y. C. Use of structure Activity data to compare structure-based clustering methods and descriptors for use in compound selection. J. Chem. Inf. Comput. Sci. 1996, 36, 572-584.
52. Berendsen, H. J. C.; Postma, J. P. M.; Vangunsteren, W. F.; Dinola, A.; Haak, J. R. Molecular-dynamics with coupling to an external bath. J. Chem. Phys. 1984, 81, 3684-3690.
53. Hess, B.; Bekker, H.; Berendsen, H. J. C.; Fraaije, J. G. E. M. LINCS: A linear constraint solver for molecular simulations. J. Comput. Chem. 1997, 18, 1463-1472.
54. Berendsen, H. J. C.; Vanderspoel, D.; Vandranen, R. Gromacs - A message-passing parallel molecular-dynamics implementation. Comput. Phys. Commun. 1995, 91, 43-56.
55. Lindahl, E.; Hess, B.; van der Spoel, D. GROMACS 3.0: a package for molecular simulation and trajectory analysis. J. Mol. Modeling 2001, 7, 306-317.
56. van der Spoel, D.; Lindahl, E.; Hess, B.; Groenhof, G.; Mark, A. E.; Berendsen, H. J. C. GROMACS: Fast, flexible, and free. J. Comput. Chem. 2005, 26, 1701-1718.
57. Miyamoto, S.; Kollman, P. A. Settle - an analytical version of the shake and rattle algorithm for rigid water models. J. Comput. Chem. 1992, 13, 952-962.
58. ChemAxon MarvinBeans 4.1.0. http://www.chemaxon.com, 2007.