A Molecular Dynamics Study of the Interaction of d-Peptide Amyloid Inhibitors with Their Target Sequence Reveals a Potential Inhibitory Pharmacophore Conformation

Journal of Molecular Biology

Volumn 383, Issue 1, 2008, Pages 266-280

  Esteras Chopo, Alexandra ^a   Morra, Giulia ^b   Moroni, Elisabetta ^b   Serrano, Luis ^a   Lopez de la Paz, Manuela ^a   Colombo, Giorgio ^b  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b CNR   (Italy)

Author keywords

aggregation; amyloid inhibition; drug design; molecular dynamics; pharmacophore structure

Indexed keywords

AMINO ACID DERIVATIVE; DEXTRO PEPTIDE AMYLOID INHIBITOR; PROTEIN INHIBITOR; SERYLTHREONYLISOLEUCYLISOLEUCILGLUTAMIC ACID; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; MOLECULAR DYNAMICS; PHARMACOPHORE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; SIMULATION;

EID: 52249085846     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.07.076     Document Type: Article

References (63)

1. Chiti F., and Dobson C.M. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75 (2006) 333-366
2. Townsend M., Cleary J.P., Mehta T., Hofmeister J., Lesne S., O'Hare E., et al. Orally available compound prevents deficits in memory caused by the Alzheimer amyloid-beta oligomers. Ann. Neurol. 60 (2006) 668-676
3. Ryu J., Kanapathipillai M., Lentzen G., and Park C.B. Inhibition of beta-amyloid peptide aggregation and neurotoxicity by alpha-d-mannosylglycerate, a natural extremolyte. Peptides 29 (2008) 578-584
4. Durairajan S.S.K., Yuan Q.J., Xie L.X., Chan W.S., Kum W.F., Koo I., et al. Salvianolic acid B inhibits A beta fibril formation and disaggregates preformed fibrils and protects against A beta-induced cytotoxicity. Neurochem. Int. 52 (2008) 741-750
5. Alkam T., Nitta A., Mizoguchi H., Saito K., Seshima M., Itoh A., et al. Restraining tumor necrosis factor-alpha by thalidomide prevents the amyloid beta-induced impairment of recognition memory in mice. Behav. Brain Res. 189 (2008) 100-106
6. Webb S., Lekishvili T., Loeschner C., Sellarajah S., Prelli F., Wisniewski T., et al. Mechanistic insights into the cure of prion disease by novel antiprion compounds. J. Virol. 81 (2007) 10729-10741
7. Hammarstrom P., Wiseman R.L., Powers E.T., and Kelly J.W. Prevention of transthyretin amyloid disease by changing protein misfolding energetics. Science 299 (2003) 713-716
8. Gestwicki J.E., Crabtree G.R., and Graef I.A. Harnessing chaperones to generate small-molecule inhibitors of amyloid beta aggregation. Science 306 (2004) 865-869
9. Barghorn S., Nimmrich V., Striebinger A., Krantz C., Keller P., Janson B., et al. Globular amyloid beta-peptide(1-42) oligomer-a homogenous and stable neuropathological protein in Alzheimer's disease. J. Neurochem. 95 (2005) 834-847
10. Walsh D.M., Hartley D.M., Kusumoto Y., Fezoui Y., Condron M.M., Lomakin A., et al. Amyloid beta-protein fibrillogenesis-structure and biological activity of protofibrillar intermediates. J. Biol. Chem. 274 (1999) 25945-25952
11. Hashimoto M., Rockenstein E., Crews L., and Masliah E. Role of protein aggregation in mitochondrial dysfunction and neurodegeneration in Alzheimer's and Parkinson's diseases. Neuromol. Med. 4 (2003) 21-35
12. Lorenzo A., Razzaboni B., Weir G.C., and Yankner B.A. Pancreatic islet cell toxicity of amylin associated with type-2 diabetes mellitus. Nature 368 (1994) 756-760
13. 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
14. Bucciantini M., Giannoni E., Chiti F., Baroni F., Formigli L., Zurdo J.S., et al. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416 (2002) 507-511
15. Lopez de la Paz M., Goldie K., Zurdo J., Lacroix E., Dobson C.M., Hoenger A., and Serrano L. De novo designed peptide-based amyloid fibrils. Proc. Natl Acad. Sci. USA 99 (2002) 16052-16057
16. Pastor M.T., Kummerer N., Schubert V., Esteras-Chopo A., Dotti C.G., Lopez de la Paz M., and Serrano L. Amyloid toxicity is independent of polypeptide sequence, length and chirality. J. Mol. Biol. 375 (2008) 695-707
17. Sawaya M.R., Sambashivan S., Nelson R., Ivanova M.I., Sievers S.A., Apostol M.I., et al. Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 447 (2007) 453-457
18. Zanuy D., Porat Y., Gazit E., and Nussinov R. Peptide sequence, molecular assembly and amyloid formation: molecular simulations and experimental study of a human islet amyloid polypeptide fragment and its analogues. Structure 12 (2004) 439-455
19. Lopez de la Paz M., and Serrano L. Sequence determinants of amyloid fibril formation. Proc. Natl Acad. Sci. USA 101 (2004) 87-92
20. Esteras-Chopo A., Serrano L., and de la Paz M.L. The amyloid stretch hypothesis: recruiting proteins toward the dark side. Proc. Natl Acad. Sci. USA 102 (2005) 16672-16677
21. Pastor M.T., Kummerer N., Schubert V., Esteras-Chopo A., Dotti C.G., de la Paz M.L., and Serrano L. Amyloid toxicity is independent of polypeptide sequence, length and chirality. J. Mol. Biol. 375 (2008) 695-707
22. Lopez de la Paz M., de Mori G.M.S., Serrano L., and Colombo G. Sequence dependence of amyloid fibril formation: insights from molecular dynamics simulations. J. Mol. Biol. 349 (2005) 583-596
23. Mousseau N., and Derreumaux P. Exploring the early steps of amyloid peptide aggregation by computers. Acc. Chem. Res. 38 (2005) 885-891
24. Melquiond A., Gelly J.C., Mousseau N., and Derreumaux P. Probing amyloid fibril formation of the NFGAIL peptide by computer simulations. J. Chem. Phys. 126 (2007) 065101
25. Soto P., Cladera J., Mark A.E., and Daura X. Stability of SIV gp32 fusion-peptide single-layer protofibrils as monitored by molecular-dynamics simulations. Angew. Chem. Int. Ed. 44 (2005) 1065-1067
26. Baumketner A., and Shea J.E. Folding landscapes of the Alzheimer amyloid-beta(12-28) peptide. J. Mol. Biol. 362 (2006) 567-579
27. Wu C., Lei H.X., and Duan Y. Elongation of ordered peptide aggregate of an amyloidogenic hexapeptide NFGAIL observed in molecular dynamics simulations with explicit solvent. J. Am. Chem. Soc. 127 (2005) 13530-13537
28. Nguyen H.D., and Hall C.K. Molecular dynamics simulations of spontaneous fibril formation by random-coil peptides. Proc. Natl Acad. Sci. USA 101 (2004) 16180-16185
29. Colombo G., Soto P., and Gazit E. Peptide self-assembly at the nanoscale: a challenging target for computational and experimental biotechnology. Trends Biotechnol. 25 (2007) 211-218
30. Wu C., Wang Z., Lei H., Zhang W., and Duan Y. Dual binding modes of Congo red to amyloid protofibril surface observed in molecular dynamics simulations. J. Am. Chem. Soc. 129 (2007) 1225-1232
31. Wu C., Lei H.X., Wang Z.X., Zhang W., and Duan Y. Phenol red interacts with the protofibril-like oligomers of an amyloidogenic hexapeptide NFGAIL through both hydrophobic and aromatic contacts. Biophys. J. 91 (2006) 3664-3672
32. Esteras-Chopo A., Pastor M.T., Serrano L., and Lopez de la Paz M. New strategy for the generation of specific d-peptide amyloid inhibitors. J. Mol. Biol. 377 (2008) 1372-1381
33. Esler W.P., Stimson E.R., Fishman J.B., Ghilardi J.R., Vinters H.V., Mantyh P.W., and Maggio J.E. Stereochemical specificity of Alzheimer's disease beta-peptide assembly. Biopolymers 49 (1999) 505-514
34. Wadai H., Yamaguchi K., Takahashi S., Kanno T., Kawai T., Naiki H., and Goto Y. Stereospecific amyloid-like fibril formation by a peptide fragment of beta2-microglobulin. Biochemistry 44 (2005) 157-164
35. Tjernberg L.O., Lilliehook C., Callaway D.J., Naslund J., Hahne S., Thyberg J., et al. Controlling amyloid beta-peptide fibril formation with protease-stable ligands. J. Biol. Chem. 272 (1997) 12601-12605
36. Chalifour R.J., McLaughlin R.W., Lavoie L., Morissette C., Tremblay N., Boule M., et al. Stereoselective interactions of peptide inhibitors with the beta-amyloid peptide. J. Biol. Chem. 278 (2003) 34874-34881
37. Wiesehan K., Buder K., Linke R.P., Patt S., Stoldt M., Unger E., et al. Selection of d-amino-acid peptides that bind to Alzheimer's disease amyloid peptide beta1-42 by mirror image phage display. ChemBioChem 4 (2003) 748-753
38. Blanchard B.J., Konopka G., Russell M., and Ingram V.M. Mechanism and prevention of neurotoxicity caused by beta-amyloid peptides: relation to Alzheimer's disease. Brain Res. 776 (1997) 40-50
39. Gazit E. Mechanisms of amyloid fibril self-assembly and inhibition. Model short peptides as a key research tool. FEBS J. 272 (2005) 5971-5978
40. Porat Y., Mazor Y., Efrat S., and Gazit E. Inhibition of islet amyloid polypeptide fibril formation: a potential role for heteroaromatic interactions. Biochemistry 43 (2004) 14454-14462
41. Necula M., Breydo L., Milton S., Kayed R., van der Veer W.E., Tone P., and Glabe C.G. Methylene blue inhibits amyloid A beta oligomerization by promoting fibrillization. Biochemistry 46 (2007) 8850-8860
42. Gazit E., della Bruna P., Pieraccini S., and Colombo G. The molecular dynamics of assembly of the ubiquitous aortic medial amyloidal medin fragment. J. Mol. Graphics Modell. 25 (2007) 903-911
43. Aitken J.F., Loomes K.M., Konarkowska B., and Cooper G.J. Suppression by polycyclic compounds of the conversion of human amylin into insoluble amyloid. Biochem. J. 374 (2003) 779-784
44. Clement O.O., and Mehl A.T. Pharmacophores based on multiple common-feature alignments. Pharmacophore Perception, Development, and Use in Drug Design (2000), International University Line, La Jolla, CA
45. Accelrys. Catalyst (2005), Accelrys, San Diego, CA, USA
46. Ernhoefer D.E., Bieschke J., Boeddrich A., Herbst M., Masino L., Lurz R., et al. EGCG redirects amyloidogenic polypeptides into unstructured, off-pathway oligomers. Nat. Struct. Mol. Biol. 15 (2008) 558-565
47. Porat Y., Abramowitz A., and Gazit E. Inhibition of amyloid fibril formation by polyphenols: structural similarity and aromatic interactions as a common inhibition mechanism. Chem. Biol. Drug Des. 67 (2006) 27-37
48. Meli M., Pennati M., Curto M., Daidone M.G., Plescia J., Toba S., et al. Small-molecule targeting of heat shock protein 90 chaperone function: rational identification of a new anticancer lead. J. Med. Chem. 49 (2006) 7721-7730
49. Lerner M.G., Bowman A.L., and Carlson H.A. Incorporating dynamics in E. coli dihydrofolate reductase enhances structure-based drug discovery. J. Chem. Inf. Mod. 47 (2007) 2358-2365
50. Findeis M.A., Musso G.M., Arico-Muendel C.C., Benjamin H.W., Hundal A.M., Lee J.J., et al. Modified-peptide inhibitors of amyloid beta-peptide polymerization. Biochemistry 38 (1999) 6791-6800
51. Soto C., Kindy M.S., Baumann M., and Frangione B. Inhibition of Alzheimer's amyloidosis by peptides that prevent beta-sheet conformation. Biochem. Biophys. Res. Commun. 226 (1996) 672-680
52. Permanne B., Adessi C., Saborio G.P., Fraga S., Frossard M.J., Van Dorpe J., et al. Reduction of amyloid load and cerebral damage in a transgenic mouse model of Alzheimer's disease by treatment with a beta-sheet breaker peptide. FASEB J. 16 (2002) 860-862
53. Adessi C., Frossard M.J., Boissard C., Fraga S., Bieler S., Ruckle T., et al. Pharmacological profiles of peptide drug candidates for the treatment of Alzheimer's disease. J. Biol. Chem. 278 (2003) 13905-13911
54. Soto-Jara, C., Baumann, M. H. & Frangione, B. (2002). Peptides and pharmaceutical compositions thereof for treatment of disorders or diseases associated with abnormal protein folding into amyloid or amyloid-like deposits. US Patent 6,462,171.
55. Berendsen H.J.C., Postma J.P.M., van Gunsteren W.F., Di Nola A., and Haak J.R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81 (1984) 3684-3690
56. Scott W.R.P., Hunenberger P.H., Tironi I.G., Mark A.E., Billeter S.R., Fennen J., et al. The GROMOS biomolecular simulation program package. J. Phys. Chem. A 103 (1999) 3596-3607
57. van Gunsteren W.F., Billeter S.R., Eising A.A., Hunenberger P.H., Kruger P., Mark A.E., et al. Biomolecular Simulation: The GROMOS96 Manual and User Guide (1996), vdf Hochschulverlag, ETH Zurich, Switzerland
58. Berendsen H.J.C., Grigera J.R., and Straatsma P.R. The missing term in effective pair potentials. J. Phys. Chem. 91 (1987) 6269-6271
59. Hess B., Bekker H., Fraaije J.G.E.M., and Berendsen H.J.C. A linear constraint solver for molecular simulations. J. Comput. Chem. 18 (1997) 1463-1472
60. Miyamoto S., and Kollman P.A. SETTLE: an analytical version of the SHAKE and RATTLE algorithms for rigid water models. J. Comput. Chem. 13 (1992) 952-962
61. Lindahl E., Hess B., and van der Spoel D. Gromacs 3.0: A package for molecular simulation and trajectory analysis. J. Mol. Mod. 7 (2001) 306-317
62. Daura X., Gademann K., Jaun B., Seebach D., van Gunsteren W.F., and Mark A.E. Peptide folding: when simulation meets experiment. Angew. Chem. Int. Ed. 38 (1999) 236-240
63. MacroModel, version 9.0 (2005), Schrödinger LLC, New York