Modeling the interface between islet amyloid polypeptide and insulin-based aggregation inhibitors: Correlation to aggregation kinetics and membrane damage

Journal of Chemical Information and Modeling

Volumn 52, Issue 5, 2012, Pages 1298-1307

  Figueroa, Hector ^a   Peddi, Durgaprasad ^a   Osborne, Joshua M ^a   Wilson, Brenan M ^a   Pesaru, Ranadheer Reddy ^a   Kurva, Balakrishna ^a   Ramaraju, Swathi ^a   Milletti, Maria C ^a   Heyl, Deborah L ^a  

^a EASTERN MICHIGAN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEINS; INSULIN; MOLAR CONCENTRATION; MOLAR RATIO; PEPTIDES;

AGGREGATION INHIBITORS; AGGREGATION KINETICS; AGGREGATION PROCESS; COMPUTATIONAL STUDIES; ISLET AMYLOID POLYPEPTIDES; LIPID MEMBRANES; MEMBRANE DAMAGE; SLOW AGGREGATIONS;

DAMAGE DETECTION;

AMYLIN; INSULIN; PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; HUMAN; KINETICS; MOLECULAR GENETICS; PROTEIN SECONDARY STRUCTURE; QUANTUM THEORY; SYNTHESIS;

AMINO ACID SEQUENCE; CELL MEMBRANE; HUMANS; INSULIN; ISLET AMYLOID POLYPEPTIDE; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; PROTEINS; QUANTUM THEORY;

EID: 84861498468     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/ci300119c     Document Type: Article

References (57)

1. Jaikaran, E.; Clark, A. Islet amyloid and type 2 diabetes: from molecular misfolding to islet pathophysiology Biochim. Biophys. Acta 2001, 1537, 179-203 (Pubitemid 33139801)
2. Larson, J. L.; Miranker, A. D. The mechanism of insulin action on islet amyloid polypeptide fiber formation J. Mol. Biol. 2004, 335, 221-231 (Pubitemid 37494974)
3. Padrick, S. B.; Miranker, A. D. Islet amyloid: phase partitioning and secondary nucleation are central to the mechanism of fibrillogenesis Biochemistry. 2002, 41, 4694-4703 (Pubitemid 34275671)
4. Hutton, J. C. The insulin secretory granule Diabetologia. 1989, 32, 271-281 (Pubitemid 19166479)
5. Gilead, S.; Wolfenson, H.; Gazit, E. Molecular mapping of the recognition interface between the islet amyloid polypeptide and insulin Angew. Chem., Int. Ed. 2006, 45, 6476-6480 (Pubitemid 44563600)
6. Glenner, G. G.; Eanes, E. D.; Wiley, C. A. Amyloid fibrils formed from a segment of the pancreatic-islet amyloid protein Biochem. Biophys. Res. Commun. 1988, 155, 608-614
7. Westermark, P.; Engstrom, U.; Johnson, K. H.; Westermark, G. T.; Betsholtz, C. Islet amyloid polypeptide: pinpointing amino acid residues linked to amyloid fibril formation Proc. Natl. Acad. Sci. U.S.A. 1990, 87, 5036-5040
8. Nilsson, M.; Raleigh, D. Analysis of amylin cleavage products provides new insights into the amyloidogenic region of human amylin J. Mol. Biol. 1999, 294, 1375-1395
9. Jaikaran, E.; Higham, C. E.; Serpell, L. C.; Zurdo, J.; Gros, M.; Clark, A.; Fraser, P. E. Identification of a novel human islet amyloid polypeptide β-sheet domain and factors influencing fibrillogenesis J. Mol. Biol. 2001, 308, 515-525 (Pubitemid 33027616)
10. Gilead, S.; Gazit, E. The role of the 14-20 domain of the islet amyloid polypeptide in amyloid formation Exp. Diabetes Res. 2008, 256954 10.1155/2008/256954
11. Kayed, R.; Bernhagen, J.; Greenfield, N.; Sweimeh, K.; Brunner, H.; Voelter, W.; Kapurniotu, A. Conformational transitions of islet amyloid polypeptide (IAPP) in amyloid formation in vitro J. Mol. Biol. 1999, 287, 781-796 (Pubitemid 29176513)
12. Jiang, P.; Wei, L.; Pervushin, K.; Mu, Y. pH-Dependent interactions of human islet amyloid polypeptide segments with insulin studied by replica exchange molecular dynamics simulations J. Phys. Chem. 2010, 114, 10176-10183
13. Wiltzius, J.; Sievers, S.; Sawaya, M.; Eisenberg, D. Atomic structures of IAPP (amylin) fusions suggest a mechanism for fibrillation and the role of insulin in the process Protein Sci. 2009, 18, 1521-1530
14. Wei, L.; Jiang, P.; Yau, Y. H.; Summer, H.; Shochat, S. G.; Mu, Y.; Pervushin, K. Residual structure in islet amyloid polypeptide mediates its interactions with soluble insulin Biochemistry 2009, 48, 2368-2376
15. Brender, J. R.; Lee, E. L.; Cavitt, M. A.; Gafni, A.; Steel, D. G.; Ramamoorthy, A. Amyloid fiber formation and membrane disruption are separate processes localized in two distinct regions of IAPP, the type-2-diabetes-related peptide J. Am. Chem. Soc. 2008, 130, 6424-6429 (Pubitemid 351706103)
16. Khemtémourian, L.; Killian, J. A.; Höppener, J. W. M.; Engel, M. F. M. Recent insights in islet amyloid polypeptide-induced membrane disruption and its role in β-cell death in Type 2 Diabetes Mellitus Exp. Diabetes Res. 2008, 421287 10.1155/2008/421287
17. Smith, P. E. S.; Brender, J. R.; Ramamoorthy, A. Induction of negative curvature as a mechanism of cell toxicity by amyloidogenic peptides: the case of islet amyloid polypeptide J. Am. Chem. Soc. 2008, 131, 4470-4478
18. Heyl, D. L.; Osbourne, J. M.; Pamarthy, S.; Samisetti, S.; Gray, A. W.; Jayaprakash, A.; Konda, S. R.; Brown, D. J.; Miller, S. R.; Eizadkhah, R.; Milletti, M. C. Liposome damage and modeling of fragments of human islet amyloid polypeptide (IAPP) support a two-step model of membrane destruction Int. J. Peptide Res. Ther. 2010, 16, 43-54
19. 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.; Nakatsuji, H.; Caricato, M.; Li, X.; Hratchian, H. P.; Izmaylov, A. F.; Bloino, J.; Zheng, G.; Sonnenberg, J. L.; Hada, M.; Ehara, M.; Toyota, K.; Fukuda, R.; Hasegawa, J.; Ishida, M.; Nakajima, T.; Honda, Y.; Kitao, O.; Nakai, H.; Vreven, T.; Montgomery, Jr., J. A.; Peralta, J. E.; Ogliaro, F.; Bearpark, M.; Heyd, J. J.; Brothers, E.; Kudin, K. N.; Staroverov, V. N.; Kobayashi, R.; Normand, J.; Raghavachari, K.; Rendell, A.; Burant, J. C.; Iyengar, S. S.; Tomasi, J.; Cossi, M.; Rega, N.; Millam, N. J.; Klene, M.; Knox, J. E.; Cross, J. B.; Bakken, V.; Adamo, C.; Jaramillo, J.; Gomperts, R.; Stratmann, R. E.; Yazyev, O.; Austin, A. J.; Cammi, R.; Pomelli, C.; Ochterski, J. W.; Martin, R. L.; Morokuma, K.; Zakrzewski, V. G.; Voth, G. A.; Salvador, P.; Dannenberg, J. J.; Dapprich, S.; Daniels, A. D.; Farkas, Ö.; Foresman, J. B.; Ortiz, J. V.; Cioslowski, J.; Fox, D. J. Gaussian 09, Revision C.02; Gaussian, Inc., Wallingford CT, 2009.
20. GaussView, version 2.1; Gaussian, Inc.: Wallingford, CT, 2000.
21. Hohenberg, P.; Kohn, W. Inhomogeneous Electron Gas Phys. Rev. 1964, 136, B864-B871
22. Kohn, W.; Sham, L. J. Self-Consistent Equations Including Exchange and Correlation Effects Phys. Rev. 1965, 140, A1133-A1138
23. Parr, R. G.; Yang, W. Density-functional theory of atoms and molecules; Oxford Univ. Press: Oxford, 1989.
24. The Challenge of d and f Electrons; Salahub, D. R.,; Zerner, M. C., Eds.; American Chemical Society: Washington, D.C., 1989.
25. Becke, A. D. Density-functional thermochemistry. III. The role of exact exchange J. Chem. Phys. 1993, 98, 5648-5652
26. Lee, C.; Yang, W.; Parr, R. G. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density Phys. Rev. B. 1988, 37, 785-789
27. Miehlich, B.; Savin, A.; Stoll, H.; Preuss, H. Results obtained with the correlation-energy density functionals of Becke and Lee, Yang and Parr Chem. Phys. Lett. 1989, 157, 200-206
28. Vosko, S. H.; Wilk, L.; Nusair, M. Accurate spin-dependent electron liquid correlation energies for local spin density calculations: A critical analysis Can. J. Phys. 1980, 58, 1200-1211
29. Binkley, J. S.; Pople, J. A.; Hehre, W. J. Self-Consistent Molecular Orbital Methods. 21. Small Split-Valence Basis Sets for First-Row Elements J. Am. Chem. Soc. 1980, 102, 939-947
30. Gordon, M. S.; Binkley, J. S.; Pople, J. A.; Pietro, W. J.; Hehre, W. J. Self-Consistent Molecular Orbital Methods. 22. Small Split-Valence Basis Sets for Second-Row Elements J. Am. Chem. Soc. 1982, 104, 2797-2803
31. Pietro, W. J.; Francl, M. M.; Hehre, W. J.; Defrees, D. J.; Pople, J. A.; Binkley, J. S. Self-Consistent Molecular Orbital Methods. 24. Supplemented small split-valence basis-sets for 2nd-row elements J. Am. Chem. Soc. 1982, 104, 5039-5048
32. Dobbs, K. D.; Hehre, W. J. Molecular-orbital theory of the properties of inorganic and organometallic compounds. 4. Extended basis-sets for 3rd row and 4th row, main-group elements J. Comput. Chem. 1986, 7, 359-378
33. Dobbs, K. D.; Hehre, W. J. Molecular-orbital theory of the properties of inorganic and organometallic compounds. 5. Extended basis-sets for 1st-row transition-metals J. Comput. Chem. 1987, 8, 861-879
34. Dobbs, K. D.; Hehre, W. J. Molecular-orbital theory of the properties of inorganic and organometallic compounds. 6. Extended basis-sets for 2nd-row transition-metals J. Comput. Chem. 1987, 8, 880-893
35. Foster, J. P.; Weinhold, F. Natural hybrid orbitals J. Am. Chem. Soc. 1980, 102, 7211-7218
36. Reed, A. E.; Weinhold, F. Natural bond orbital analysis of near-Hartree-Fock water dimer J. Chem. Phys. 1983, 78, 4066-4073
37. Reed, A. E.; Weinstock, R. B.; Weinhold, F. Natural-population analysis J. Chem. Phys. 1985, 83, 735-746
38. Reed, A. E.; Weinhold, F. Natural Localized Molecular Orbitals J. Chem. Phys. 1985, 83, 1736-1740
39. Carpenter, J. E. Extension of Lewis structure concepts to open-shell and excited-state molecular species. Ph. D. thesis, University of Wisconsin, Madison, WI, 1987.
40. Carpenter, J. E.; Weinhold, F. Analysis of the geometry of the hydroxymethyl radical by the different hybrids for different spins natural bond orbital procedure J. Mol. Struct. (Theochem) 1988, 46, 41-62
41. Reed, A. E.; Curtiss, L. A.; Weinhold, F. Intermolecular interactions from a natural bond orbital, donor-acceptor viewpoint Chem. Rev. 1988, 88, 899-926
42. Weinhold, F.; Carpenter, J. E. In The Structure of Small Molecules and Ions; Naaman, R.; Vager, Z., Eds.; Plenum: New York, 1988; pp 227-236.
43. Scrocchi, L. A.; Chen, Y.; Waschuk, S.; Wang, F.; Cheung, S.; Darabie, A. A.; McLaurin, J.; Fraser, P. E. Design of peptide-based inhibitors of human islet amyloid polypeptide fibrillogenesis J. Mol. Biol. 2002, 318, 697-706 (Pubitemid 34729362)
44. Scrocchi, L. A.; Chen, Y.; Wang, F.; Han, K.; Ha, K.; Wu, L.; Fraser, P. E. Inhibitors of islet amyloid polypeptide fibrillogenesis, and the treatment of typ-2 diabetes Lett. Peptide Sci. 2003, 10, 545-551 (Pubitemid 40379046)
45. Yan, L. M.; Tatarek-Nossol, M.; Velkova, A.; Kazantzis, A.; Kapurniotu, A. Design of a mimic of nonamyloidogenic and bioactive human islet amyloid polypeptide (IAPP) as nanomolar affinity inhibitor of IAPP cytotoxic fibrillogenesis Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 2046-2051 (Pubitemid 43271620)
46. Martinek, V.; Bren, U.; Goodman, M. F.; Warshel, A.; Florian, J. DNA polymerase β catalytic efficiency mirrors the Asn279-dCTP H-bonding strength FEBS Lett. 2007, 581, 775-780 (Pubitemid 46216300)
47. Zhang, H.; Bren, U.; Kozekov, I. D.; Rizzo, C. J.; Stec, D. F.; Guengerich, F. P. Steric and electrostatic effects at the C2 atom substituent influence replication and miscoding of the DNA deamination product deoxyxanthosine and analogs by DNA polymerases J. Mol. Biol. 2009, 392, 251-269
48. Gazit, E. A possible role for π-stacking in the self-assembly of amyloid fibrils FASEB J. 2002, 16, 77-83 (Pubitemid 34027953)
49. Milardi, D.; Sciacca, M.; Pappalardo, M.; Grasso, D. M.; La Rosa, C. The role of aromatic side-chains in amyloid growth and membrane interaction of the islet amyloid polypeptide fragments LANFLVH Eur. Biophys. J. 2011, 40, 1-12
50. Cecchini, M.; Curcio, R.; Pappalardo, M.; Melki, R.; Caflisch, A. A molecular dynamics approach to the structural characterization of amyloid aggregation J. Mol. Biol. 2006, 357, 1306-1321 (Pubitemid 43357990)
51. Hebda, J. A.; Saraogi, I.; Magzoub, M.; Hamilton, A. D.; Miranker, A. D. A peptidomimetic approach to targeting pre-amyloidogenic states in Type II Diabetes Chem. Biol. 2009, 16, 943-950
52. Udommaneethanakit, T.; Rungrotmongkol, T.; Bren, U.; Frecer, V.; Stanislav, M. Dynamic behavior of avian influenza A virus neuraminidase subtype H5N1 in complex with oseltamivir, zanamivir, peramivir, and their phosphonate analogues J. Chem. Info. Model. 2009, 49, 2323-2332
53. Bren, U.; Lah, J.; Bren, M.; Martinek, V.; Florian, J. DNA duplex stability: the role of preorganized electrostatics J. Phys. Chem. 2010, 114, 2876-2885
54. Zhao, H.; Zhu, Y.; Tong, M.; He, J.; Liu, C.; Tang, M. Density functional theory studies on the inclusion complexes of cyclic decapeptide with 1-phenyl-1-propanol enantiomers J. Mol. Model. 2012, 18, 851-858
55. Lo Verso, F.; Egorov, S. A.; Milchev, A.; Binder, K. Spherical polymer brushes under good solvent conditions: molecular dynamics results compared to density functional theory J. Phys. Chem. 2010, 184901 10.1063/1.3494902
56. Buhl, M.; Sieffert, N.; Chaumont, A.; Wipff, G. Water versus acetonitrile coordination to uranyl. Density functional study of cooperative polarization effects in solution Inorg. Chem. 2011, 50, 299-308
57. Cui, W.; Ma, J. W.; Lei, P.; Wu, W. H.; Yu, Y. P.; Xiang, Y.; Tong, A. J.; Zhao, Y. F.; Li, Y. M. Insulin is a kinetic but not a thermodynamic inhibitor of amylin aggregation FEBS J. 2009, 276, 3365-3371