Interaction of Alzheimer's Aβ Peptide with an Engineered Binding Protein-Thermodynamics and Kinetics of Coupled Folding-Binding

Journal of Molecular Biology

Volumn 378, Issue 2, 2008, Pages 398-411

  Hoyer, Wolfgang ^a   Härd, Torleif ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

amyloid; immunotherapy; molecular recognition; protein engineering; protein protein interactions

Indexed keywords

8 ANILINO 1 NAPHTHALENESULFONIC ACID; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; TYROSINE;

ALZHEIMER DISEASE; ARTICLE; BINDING KINETICS; CALORIMETRY; CIRCULAR DICHROISM; COMPLEX FORMATION; CONTROLLED STUDY; DIMERIZATION; FLUORESCENCE; GEL PERMEATION CHROMATOGRAPHY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN PROTEIN INTERACTION; THERMODYNAMICS;

EID: 41249098954     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.02.040     Document Type: Article

References (70)

1. Goedert M., and Spillantini M.G. A century of Alzheimer's disease. Science 314 (2006) 777-781
2. Haass C., and Selkoe D.J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β-peptide. Nat. Rev. Mol. Cell Biol. 8 (2007) 101-112
3. Hardy J., and Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297 (2002) 353-356
4. Lansbury P.T., and Lashuel H.A. A century-old debate on protein aggregation and neurodegeneration enters the clinic. Nature 443 (2006) 774-779
5. Golde T.E. Disease modifying therapy for AD?. J. Neurochem. 99 (2006) 689-707
6. Hamaguchi T., Ono K., and Yamada M. Anti-amyloidogenic therapies: strategies for prevention and treatment of Alzheimer's disease. Cell. Mol. Life Sci. 63 (2006) 1538-1552
7. Roberson E.D., and Mucke L. 100 years and counting: prospects for defeating Alzheimer's disease. Science 314 (2006) 781-784
8. Gelinas D.S., DaSilva K., Fenili D., St George-Hyslop P., and McLaurin J. Immunotherapy for Alzheimer's disease. Proc. Natl Acad. Sci. USA 101 (2004) 14657-14662
9. Weiner H.L., and Frenkel D. Immunology and immunotherapy of Alzheimer's disease. Nat. Rev. Immunol. 6 (2006) 404-416
10. Findeis M.A. Approaches to discovery and characterization of inhibitors of amyloid β-peptide polymerization. Biochim. Biophys. Acta 1502 (2000) 76-84
11. Gervais F., Paquette J., Morissette C., Krzywkowski P., Yu M., Azzi M., et al. Targeting soluble Aβ peptide with tramiprosate for the treatment of brain amyloidosis. Neurobiol. Aging 28 (2007) 537-547
12. Lee V.M. Amyloid binding ligands as Alzheimer's disease therapies. Neurobiol. Aging 23 (2002) 1039-1042
13. Liu D., Xu Y., Feng Y., Liu H., Shen X., Chen K., et al. Inhibitor discovery targeting the intermediate structure of β-amyloid peptide on the conformational transition pathway: implications in the aggregation mechanism of β-amyloid peptide. Biochemistry 45 (2006) 10963-10972
14. Bard F., Cannon C., Barbour R., Burke R.L., Games D., Grajeda H., et al. Peripherally administered antibodies against amyloid β-peptide enter the central nervous system and reduce pathology in a mouse model of Alzheimer disease. Nat. Med. 6 (2000) 916-919
15. Klyubin I., Walsh D.M., Lemere C.A., Cullen W.K., Shankar G.M., Betts V., et al. Amyloid β protein immunotherapy neutralizes Aβ oligomers that disrupt synaptic plasticity in vivo. Nat. Med. 11 (2005) 556-561
16. Solomon B., Koppel R., Frenkel D., and Hanan-Aharon E. Disaggregation of Alzheimer β-amyloid by site-directed mAβ. Proc. Natl Acad. Sci. USA 94 (1997) 4109-4112
17. Wilcock D.M., Munireddy S.K., Rosenthal A., Ugen K.E., Gordon M.N., and Morgan D. Microglial activation facilitates Aβ plaque removal following intracranial anti-Aβ antibody administration. Neurobiol. Dis. 15 (2004) 11-20
18. DeMattos R.B., Bales K.R., Cummins D.J., Dodart J.C., Paul S.M., and Holtzman D.M. Peripheral anti-Aβ antibody alters CNS and plasma Aβ clearance and decreases brain Aβ burden in a mouse model of Alzheimer's disease. Proc. Natl Acad. Sci. USA 98 (2001) 8850-8855
19. DeMattos R.B., Bales K.R., Cummins D.J., Paul S.M., and Holtzman D.M. Brain to plasma amyloid-β efflux: a measure of brain amyloid burden in a mouse model of Alzheimer's disease. Science 295 (2002) 2264-2267
20. Lemere C.A., Spooner E.T., LaFrancois J., Malester B., Mori C., Leverone J.F., et al. Evidence for peripheral clearance of cerebral Aβ protein following chronic, active Aβ immunization in PSAPP mice. Neurobiol. Dis. 14 (2003) 10-18
21. Tanzi R.E., Moir R.D., and Wagner S.L. Clearance of Alzheimer's Aβ peptide: the many roads to perdition. Neuron 43 (2004) 605-608
22. Wang Y.J., Zhou H.D., and Zhou X.F. Clearance of amyloid-β in Alzheimer's disease: progress, problems and perspectives. Drug Discovery Today 11 (2006) 931-938
23. Frenkel D., Balass M., Katchalski-Katzir E., and Solomon B. High affinity binding of monoclonal antibodies to the sequential epitope EFRH of β-amyloid peptide is essential for modulation of fibrillar aggregation. J. Neuroimmunol. 95 (1999) 136-142
24. Lührs T., Ritter C., Adrian M., Riek-Loher D., Bohrmann B., Döbeli H., et al. 3D structure of Alzheimer's amyloid-β(1-42) fibrils. Proc. Natl Acad. Sci. USA 102 (2005) 17342-17347
25. Petkova A.T., Yau W.M., and Tycko R. Experimental constraints on quaternary structure in Alzheimer's β-amyloid fibrils. Biochemistry 45 (2006) 498-512
26. Etienne M.A., Aucoin J.P., Fu Y., McCarley R.L., and Hammer R.P. Stoichiometric inhibition of amyloid β-protein aggregation with peptides containing alternating α,α-disubstituted amino acids. J. Am. Chem. Soc. 128 (2006) 3522-3523
27. Gordon D.J., Sciarretta K.L., and Meredith S.C. Inhibition of β-amyloid(40) fibrillogenesis and disassembly of β-amyloid(40) fibrils by short β-amyloid congeners containing N-methyl amino acids at alternate residues. Biochemistry 40 (2001) 8237-8245
28. Soto C., Sigurdsson E.M., Morelli L., Kumar R.A., Castano E.M., and Frangione B. β-Sheet breaker peptides inhibit fibrillogenesis in a rat brain model of amyloidosis: implications for Alzheimer's therapy. Nat. Med. 4 (1998) 822-826
29. Tjernberg L.O., Näslund J., Lindqvist F., Johansson J., Karlström A.R., Thyberg J., et al. Arrest of β-amyloid fibril formation by a pentapeptide ligand. J. Biol. Chem. 271 (1996) 8545-8548
30. Alexandrescu A.T. Amyloid accomplices and enforcers. Protein Sci. 14 (2005) 1-12
31. Webster S., and Rogers J. Relative efficacies of amyloid β peptide (Aβ) binding proteins in Aβ aggregation. J. Neurosci. Res. 46 (1996) 58-66
32. Nord K., Gunneriusson E., Ringdahl J., Ståhl S., Uhlén M., and Nygren P.Å. Binding proteins selected from combinatorial libraries of an α-helical bacterial receptor domain. Nat. Biotechnol. 15 (1997) 772-777
33. Grönwall C., Jonsson A., Lindström S., Gunneriusson E., Ståhl S., and Herne N. Selection and characterization of affibody ligands binding to Alzheimer amyloid β peptides. J. Biotechnol. 128 (2007) 162-183
34. Hou L., Shao H., Zhang Y., Li H., Menon N.K., Neuhaus E.B., et al. Solution NMR studies of the Aβ(1-40) and Aβ(1-42) peptides establish that the Met35 oxidation state affects the mechanism of amyloid formation. J. Am. Chem. Soc. 126 (2004) 1992-2005
35. Lendel C., Dogan J., and Härd T. Structural basis for molecular recognition in an affibody:affibody complex. J. Mol. Biol. 359 (2006) 1293-1304
36. Wahlberg E., Lendel C., Helgstrand M., Allard P., Dincbas-Renqvist V., Hedqvist A., et al. An affibody in complex with a target protein: structure and coupled folding. Proc. Natl Acad. Sci. USA 100 (2003) 3185-3190
37. Wishart D.S., Sykes B.D., and Richards F.M. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J. Mol. Biol. 222 (1991) 311-333
38. Wishart D.S., Sykes B.D., and Richards F.M. The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry 31 (1992) 1647-1651
39. Dincbas-Renqvist V., Lendel C., Dogan J., Wahlberg E., and Härd T. Thermodynamics of folding, stabilization, and binding in an engineered protein-protein complex. J. Am. Chem. Soc. 126 (2004) 11220-11230
40. Baker B.M., and Murphy K.P. Evaluation of linked protonation effects in protein binding reactions using isothermal titration calorimetry. Biophys. J. 71 (1996) 2049-2055
41. a of histidine side-chains correlates with burial within proteins. Proteins 49 (2002) 1-6
42. Markley J.L. Observation of histidine residues in proteins by means of nuclear magnetic resonance spectroscopy. Acc. Chem. Res. 8 (1975) 70-80
43. Hortschansky P., Schroeckh V., Christopeit T., Zandomeneghi G., and Fändrich M. The aggregation kinetics of Alzheimer's β-amyloid peptide is controlled by stochastic nucleation. Protein Sci. 14 (2005) 1753-1759
44. Kumar M.D., and Gromiha M.M. PINT: Protein-protein Interactions Thermodynamic Database. Nucleic Acids Res. 34 (2006) D195-D198
45. Cliff M.J., Williams M.A., Brooke-Smith J., Barford D., and Ladbury J.E. Molecular recognition via coupled folding and binding in a TPR domain. J. Mol. Biol. 346 (2005) 717-732
46. Murphy K.P., and Freire E. Thermodynamics of structural stability and cooperative folding behavior in proteins. Adv. Protein Chem. 43 (1992) 313-361
47. Spolar R.S., Livingstone J.R., and Record Jr. M.T. Use of liquid hydrocarbon and amide transfer data to estimate contributions to thermodynamic functions of protein folding from the removal of nonpolar and polar surface from water. Biochemistry 31 (1992) 3947-3955
48. Semisotnov G.V., Rodionova N.A., Razgulyaev O.I., Uversky V.N., Gripas A.F., and Gilmanshin R.I. Study of the "molten globule" intermediate state in protein folding by a hydrophobic fluorescent probe. Biopolymers 31 (1991) 119-128
49. Berger C., Weber-Bornhauser S., Eggenberger J., Hanes J., Plückthun A., and Bosshard H.R. Antigen recognition by conformational selection. FEBS Lett. 450 (1999) 149-153
50. Foote J., and Milstein C. Conformational isomerism and the diversity of antibodies. Proc. Natl Acad. Sci. USA 91 (1994) 10370-10374
51. Grünberg R., Leckner J., and Nilges M. Complementarity of structure ensembles in protein-protein binding. Structure 12 (2004) 2125-2136
52. Kumar S., Ma B., Tsai C.J., Sinha N., and Nussinov R. Folding and binding cascades: dynamic landscapes and population shifts. Protein Sci. 9 (2000) 10-19
53. Jackson G.S., Staniforth R.A., Halsall D.J., Atkinson T., Holbrook J.J., Clarke A.R., et al. Binding and hydrolysis of nucleotides in the chaperonin catalytic cycle: implications for the mechanism of assisted protein folding. Biochemistry 32 (1993) 2554-2563
54. Keeble A.H., and Kleanthous C. The kinetic basis for dual recognition in colicin endonuclease-immunity protein complexes. J. Mol. Biol. 352 (2005) 656-671
55. Wedemeyer W.J., Welker E., and Scheraga H.A. Proline cis-trans isomerization and protein folding. Biochemistry 41 (2002) 14637-14644
56. Ladbury J.E., Wright J.G., Sturtevant J.M., and Sigler P.B. A thermodynamic study of the trp repressor-operator interaction. J. Mol. Biol. 238 (1994) 669-681
57. Sturtevant J.M. Heat capacity and entropy changes in processes involving proteins. Proc. Natl Acad. Sci. USA 74 (1977) 2236-2240
58. Williams D.H., Stephens E., O'Brien D.P., and Zhou M. Understanding noncovalent interactions: ligand binding energy and catalytic efficiency from ligand-induced reductions in motion within receptors and enzymes. Angew. Chem. Int. Ed. 43 (2004) 6596-6616
59. Cooper A. Heat capacity effects in protein folding and ligand binding: a re-evaluation of the role of water in biomolecular thermodynamics. Biophys. Chem. 115 (2005) 89-97
60. Dogan J., Lendel C., and Härd T. Thermodynamics of folding and binding in an affibody:affibody complex. J. Mol. Biol. 359 (2006) 1305-1315
61. Lo Conte L., Chothia C., and Janin J. The atomic structure of protein-protein recognition sites. J. Mol. Biol. 285 (1999) 2177-2198
62. Koshland D.E. Application of a theory of enzyme specificity to protein synthesis. Proc. Natl Acad. Sci. USA 44 (1958) 98-104
63. Razai A., Garcia-Rodriguez C., Lou J., Geren I.N., Forsyth C.M., Robles Y., et al. Molecular evolution of antibody affinity for sensitive detection of botulinum neurotoxin type A. J. Mol. Biol. 351 (2005) 158-169
64. Wu H., Pfarr D.S., Tang Y., An L.L., Patel N.K., Watkins J.D., et al. Ultra-potent antibodies against respiratory syncytial virus: effects of binding kinetics and binding valence on viral neutralization. J. Mol. Biol. 350 (2005) 126-144
65. Pace C.N., Hebert E.J., Shaw K.L., Schell D., Both V., Krajcikova D., et al. Conformational stability and thermodynamics of folding of ribonucleases Sa, Sa2 and Sa3. J. Mol. Biol. 279 (1998) 271-286
66. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6 (1995) 277-293
67. Vranken W.F., Boucher W., Stevens T.J., Fogh R.H., Pajon A., Llinas M., et al. The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins 59 (2005) 687-696
68. Cavanagh J., Fairbrother W.J., Palmer A.G., and Skelton N.J. Protein NMR Spectroscopy: Principles and Practice (1996), Academic Press, London
69. Fukada H., and Takahashi K. Enthalpy and heat capacity changes for the proton dissociation of various buffer components in 0.1 M potassium chloride. Proteins 33 (1998) 159-166
70. Morin P.E., and Freire E. Direct calorimetric analysis of the enzymatic activity of yeast cytochrome c oxidase. Biochemistry 30 (1991) 8494-8500