Evidence of π-stacking interactions in the self-assembly of hIAPP22-29

Proteins: Structure, Function and Bioinformatics

Volumn 81, Issue 4, 2013, Pages 690-703

  Profit, Adam A ^a   Felsen, Valentina ^a   Chinwong, Justina ^a   Mojica, Elmer Rico E ^a   Desamero, Ruel Z B ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

stacking; Fluorescence; Islet amyloid polypeptide; Pentafluorophenylalanine; Phenylalanine; Raman spectroscopy; Self assembly

Indexed keywords

AMYLIN; AMYLIN[22-29]; AMYLOID; PHENYLALANINE; UNCLASSIFIED DRUG;

ARTICLE; BETA SHEET; FLUORESCENCE SPECTROSCOPY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; RAMAN SPECTROMETRY; SIMULATION; TRANSMISSION ELECTRON MICROSCOPY; TURBIDITY;

AMYLOID; ELECTRONS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; ISLET AMYLOID POLYPEPTIDE; PHENYLALANINE; PROTEIN STRUCTURE, SECONDARY;

EID: 84874812945     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24229     Document Type: Article

References (61)

1. Westermark P, Wernstedt C, Wilander E, Hayden DW, O'Brien TD, Johnson KH. Amyloid fibrils in human insulinoma and islets of Langerhans of the diabetic cat are derived from a neuropeptide-like protein also present in normal islet cells. Proc Natl Acad Sci USA 1987; 84: 3881-3885.
2. Cooper GJS, Willis AC, Clark A, Turner RC, Sim RB, Reid KBM. Purification and characterization of a peptide from amyloid-rich pancreases of type II diabetic patients. Proc Natl Acad Sci USA 1987; 84: 8628-8632.
3. Clark A, Cooper GJ, Lewis CE, Morris JF, Willis AC, Reid KB, Turner RC. Islet amyloid formed from diabetes-associated peptide may be pathogenic in type-2 diabetes. Lancet 1987; 2: 231-234.
4. Jaikaran E, Clark A. Islet amyloid and type 2 diabetes: from molecular misfolding to islet pathophysiology. Biochim Biophys Acta 2001; 1537: 179-203.
5. Kapurniotu A. Amyloidogenicity and cytotoxicity of islet amyloid polypeptide. Biopolymers 2001; 60: 438-459.
6. Engel MF. Membrane permeabilization by islet amyloid polypeptide. Chem Phys Lipids 2009; 160: 1-10.
7. Lin CY, Gurlo T, Kayed R, Butler AE, Haataja L, Glabe CG, Butler PC. Toxic human islet amyloid polypeptide (h-IAPP) oligomers are intracellular, and vaccination to induce anti-toxic oligomer antibodies does not prevent h-IAPP-induced beta-cell apoptosis in h-IAPP transgenic mice. Diabetes 2007; 56: 1324-1332.
8. 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.
9. Abedini A, Raleigh DP. A critical assessment of the role of helical intermediates in amyloid formation by natively unfolded proteins and polypeptides. Protein Eng Des Sel 2009; 22: 453-459.
10. Soong R, Brender JR, Macdonald PM, Ramamoorthy A. Association of highly compact type II diabetes related islet amyloid polypeptide intermediate species at physiological temperature revealed by diffusion NMR spectroscopy. J Am Chem Soc 2009; 131: 7079-7085.
11. Westermark P, Engstrom U, Johnson KH, Westermark GT, Betsholtz C. Islet amyloid polypeptide: pinpointing amino acid residues linked to amyloid fibril formation. Proc Natl Acad Sci USA 1990; 87: 5036-5040.
12. Jaikaran ET, Higham CE, Serpell LC, Zurdo J, Gross M, Clark A, Fraser PE. Identification of a novel human islet amyloid polypeptide β-sheet domain and factors influencing fibrillogenesis. J Mol Biol 2001; 308: 515-525.
13. Nilsson MR, Raleigh DP. Analysis of amylin cleavage products provides new insights into the amyloidogenic region of human amylin. J Mol Biol 1999; 294: 1375-1385.
14. Goldsbury C, Goldie K, Pellaud J, Seeling J, Frey P, Muller SA, Kistler J, Cooper GJS, Aebi U. Amyloid fibril formation from full-length and fragments of amylin. J Struct Biol 2000; 130: 352-362.
15. Tenidis K, Waldner M, Bernhagen J, Fischle W, Bergmann M, Weber M, Merkle ML, Voelter W, Brunner H, Kapurniotu A. Identification of a penta- and hexa-peptide of islet amyloid polypeptide (IAPP) with amyloidogenic and cytotoxic properties. J Mol Biol 2000; 295: 1055-1071.
16. Azriel R, Gazit E. Analysis of the minimal amyloid-forming fragment of the islet amyloid polypeptide. J Biol Chem 2001; 276: 34156-34161.
17. Porat Y, Stepensky A, Naider F, Gazit E. Completely different amyloidogenic potential of nearly identical peptide fragments. Biopolymers 2003; 69: 161-164.
18. Marshall KE, Morris KL, Charlton D, O'Reilly N, Lewis L, Walden H, Serpell LC. Hydrophobic, aromatic, and electrostatic interactions play a central role in amyloid fibril formation and stability. Biochemistry 2011; 50: 2061-2071.
19. Chelli R, Gervasio FL, Procacci P, Schettino V. Stacking and T-shape competition in aromatic-aromatic amino acid interactions. J Am Chem Soc 2002; 124: 6133-6143.
20. Porat Y, Abramowitz A, Gazit E. Inhibition of amyloid fibril formation by polyphenols: structural similarity and aromatic interactions as a common inhibition mechanism. Chem Biol Drug Des 2006; 67: 27-37.
21. Meng F, Abedini A, Plesner A, Verchere CB, Raleigh DP. The flavanol (-) epigallocatechin 3-gallate inhibits amyloid formation by islet amyloid polypeptide, disaggregates amyloid fibrils and protects cultured cells against IAPP-induced toxicity. Biochemistry 2010; 49: 8127-8133.
22. Levy-Saskin M, Shreberk M, Daniel Y, Gazit E. Targeting insulin amyloid assembly by small aromatic molecules. Islets 2009; 1: 210-215.
23. Convertino M, Pellarin R, Catto M, Carotti A, Caflisch A. 9, 10-Anthraquinone hinders β-aggregation: how does a small molecule interfere with Aβ-peptide amyloid fibrillation? Protein Sci 2009; 18: 792-800.
24. Cao P, Raleigh DP. Analysis of the inhibition and remodeling of islet amyloid polypeptide fibers by flavanols. Biochemistry 2012; 51: 2670-2683.
25. Tracz SM, Abedini A, Driscoll M, Raleigh DP. Role of aromatic interactions in amyloid formation by peptides derived from human amylin. Biochemistry 2004; 43: 15901-15908.
26. Milardi D, Sciacca MFM, Pappalardo M, Grasso DM, La Rosa C. The role of aromatic side-chains in amyloid growth and membrane interaction of the islet amyloid polypeptide fragment LANFLVH. Eur Biophys J 2011; 40: 1-12.
27. Marek P, Abedini A, Song BB, Kanungo M, Johnson ME, Gupta R, Zaman W, Wong SS, Raleigh DP. Aromatic interactions are not required for amyloid fibril formation by islet amyloid polypeptide but do influence the rate of fibril formation and fibril morphology. Biochemistry 2007; 46: 3255-3261.
28. Bemporad F, Taddei N, Stefani M, Chiti F. Assessing the role of aromatic residues in the amyloid aggregation of human muscle acylphosphatase. Protein Sci 2006; 15: 862-870.
29. Frisch M, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Mennucci B, Petersson GA, Nakatsuji H, Caricato M, Li X, Hratchian HP, Izmaylov AF, Bloino J, Zheng G, Sonnenberg JL, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Vreven T, Montgomery JA, Jr, Peralta JE, Ogliaro F, Bearpark M, Heyd JJ, Brothers E, Kudin KN, Staroverov VN, Kobayashi R, Normand J, Raghavachari K, Rendell A, Burant JC, Iyengar SS, Tomasi J, Cossi M, Rega N, Millam JM, Klene M, Knox JE, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Martin RL, Morokuma K, Zakrzewski VG, Voth GA, Salvador P, Dannenberg JJ, Dapprich S, Daniels AD, Farkas Ö, Foresman JB, Ortiz JV, Cioslowski J, Fox DJ. Gaussian 09, Revision A.1. Wallingford, CT: Gaussian Inc.; 2009.
30. Becke AD. Density-functional thermochemistry. III. The role of exact exchange. J Chem Phys 1993; 98: 5648-5652.
31. Lee C, Yang W, Parr RG. Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density. Phys Rev B 1988; 41: 785-789.
32. Rauhut G, Pulay P. Transferable scaling factors for density functional derived vibrational force fields. J Phys Chem 1995; 99: 3093-3100.
33. Stephens PJ, Devlin FJ, Chabalowski CF, Frisch MJ. Ab initio calculations of vibrational absorption and circular dichroism spectra using density functional force fields. J Phys Chem 1994; 98: 11623-11627.
34. Pulay P, Fogarasi G, Pongor G, Boggs JE, Vargha A. Combination of theoretical ab initio and experimental information to obtain reliable harmonic force constants. Scaled quantum mechanical (QM) force fields for glyoxal, acrolein, butadiene, formaldehyde, and ethylene. J Am Chem Soc 1983; 105: 7037-7047.
35. Dennington R, Keith T, Millam, J. GaussView, Version 5. Shawnee Mission, KS: Semichem, Inc.; 2009.
36. Porat Y, Mazor Y, Efrat S, Gazit E. Inhibition of islet amyloid polypeptide fibril formation: a potential role for heteroaromatic interactions. Biochemistry 2004; 43: 14454-14462.
37. Ashburn TT, Lansbury PT. Interspecies sequence variations affect kinetics and thermodynamics of amyloid formation: peptide models of pancreatic amyloid. J Am Chem Soc 1993; 115: 11012-11013.
38. Woll MG, Hadley EB, Mecozzi S, Gellman SH. Stabilizing and destabilizing effects of phenylalanine --> F5-phenylalanine mutations on the folding of a small protein. J Am Chem Soc 2006; 128: 15932-15933.
39. Bowerman CJ, Liyanage W, Federation AJ, Nilsson BL. Tuning β-sheet peptide self-assembly and hydrogelation behavior by modification of sequence hydrophobicity and aromaticity. Biomacromolecules 2011; 12: 2735-2745.
40. Ryan DM, Doran TM, Anderson SB, Nilsson BL. Effect of C-terminal modification on the self-assembly and hydrogelation of fluorinated Fmoc-Phe derivatives. Langmuir 2011; 27: 4029-4039.
41. Marek P, Mukherjee S, Zanni MT, Raleigh DP. Residue-specific, real-time characterization of lag-phase species and fibril growth during amyloid formation: a combined fluorescence and IR study of p-cyanophenylalanine analogs of islet amyloid polypeptide. J Mol Biol 2010; 400: 878-888.
42. Hirata A, Sugimoto K, Konnob T, Moriia T. Amyloid-forming propensity of the hydrophobic non-natural amino acid on the fibril-forming core peptide of human tau. Bioorg Med Chem Lett 2007; 17: 2971-2974.
43. Profit AA, Lee TR, Niu J, Lawrence DS. Molecular rulers: an assessment of distance and spatial relationships of Src tyrosine kinase SH2 and active site regions. J Biol Chem 2001; 276: 9446-9451.
44. Colthup NB, Daly LH, Wiberley SE. Introduction to infrared and Raman spectroscopy. San Diego: Academic Press; 1990.
45. Lin-Vien D, Colthup NB, Fateley WG, Grasselli JG. The handbook of infrared and Raman characteristic frequencies of organic molecules. San Diego: Academic Press; 1991.
46. Deng H, Schindler JF, Berst KB, Plapp BV, Callender R. A Raman spectroscopic characterization of bonding in the complex of horse liver alcohol dehydrogenase with NADH and N-cyclohexylformamide. Biochemistry 1998; 37: 14267-14278.
47. Fodor SPA, Copeland RA, Grygon CA, Spiro TG. Deep-ultraviolet Raman excitation profiles and vibronic scattering mechanisms of phenylalanine, tyrosine, and tryptophan. J Am Chem Soc 1989; 111: 5509-5518.
48. Desamero RZB, Kang J, Dol C, Chinwong J, Walterd K, Sivarajah T, Profit AA. Spectroscopic characterization of the SH-2 and active site-directed peptide sequences of a bivalent Src kinase inhibitor. Appl Spectrosc 2009; 63: 767-774.
49. Getahun Z, Huang C-Y, Wang T, De Leon B, DeGrado WF, Gai F. Using nitrile-derivatized amino acids as infrared probes of local environment. J Am Chem Soc 2003; 125: 405-411.
50. Weeks CL, Polishchuk A, Getahun Z, DeGrado WF, Spiro TG. Investigation of an unnatural amino acid for use as a resonance Raman probe: detection limits and solvent and temperature dependence of the νC≡N band of 4-cyanophenylalanine. J Raman Spectrosc 2008; 39: 1606-1613.
51. Schmid ED, Moschallski M, Peticolas WL. Solvent effects on the absorption and Raman spectra of aromatic nitro compounds. 1. Calculation of preresonance Raman intensities. J Phys Chem 1986; 90: 2340-2346.
52. Smith EE, Linderman BY, Luskin AC, Brewer SH. Probing local environments with the infrared probe: L-4-Nitrophenylalanine. J Phys Chem B 2011; 115: 2380-2385.
53. Desamero RZB, Cheng H, Cahill S, Girvin M, Deng H, Callender R, Rath P, Variano B, Smart JE. Physical properties of compounds promoting oral delivery of macromolecular drugs. Biopolymers (Biospectroscopy) 2002; 67: 26-40.
54. Takeuchi H. UV Raman markers for structural analysis of aromatic side chains in proteins. Anal Sci 2011; 27: 1077-1086.
55. Barnes AJ. Blue-shifting hydrogen bonds-are they proper or improper? J Mol Struct 2004; 704: 3-9.
56. Madine J, Jack E, Stockley PG, Radford SE, Serpell LC, Middleton DA. Structural insights into the polymorphism of amyloid-like fibrils formed by region 20-29 of amylin revealed by solid-state NMR and X-ray fiber diffraction. J Am Chem Soc 2008; 130: 14990-15001.
57. Nielsen JT, Bjerring M, Jeppesen MD, Pedersen RO, Pedersen JM, Hein KL, Vosegaard T, Skrydstrup T, Otzen DE, Nielsen NC. Unique identification of supramolecular structures in amyloid fibrils by solid-state NMR spectroscopy. Angew Chem Int Ed Engl 2009; 48: 2118-2121.
58. Doran TM, Kamens AJ, Byrnes NK, Nilsson BL. Role of amino acid hydrophobicity, aromaticity, and molecular volume on IAPP(20-29) amyloid self-assembly. Proteins 2012; 80: 1053-1065.
59. Hunter CA, Sanders JKM. The nature of π-π interactions. J Am Chem Soc 1990; 112: 5525-5534.
60. Cockroft SL, Hunter CA, Lawson KR, Perkins J, Urch CJ. Electrostatic control of aromatic stacking interactions. J Am Chem Soc 2005; 127: 8594-8595.
61. Gazit E. A possible role for π-stacking in the self-assembly of amyloid fibrils. FASEB J 2002; 16: 77-83.