In situ molecular-level insights into the interfacial structure changes of membrane-associated prion protein fragment [118-135] investigated by sum frequency generation vibrational spectroscopy

Langmuir

Volumn 28, Issue 49, 2012, Pages 16979-16988

  Li, Hongchun ^a   Ye, Shuji ^a   Wei, Feng ^a   Ma, Sulan ^a   Luo, Yi ^a  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER'S; AMYLOID PEPTIDES; C-TERMINAL DOMAINS; CONFORMATION CHANGE; CONFORMATIONAL TRANSITIONS; HELICAL STRUCTURES; INTERFACIAL STRUCTURES; ISOFORMS; LOW CONCENTRATIONS; MEMBRANE-ASSOCIATED PROTEINS; MOLECULAR-LEVEL INSIGHTS; POTENTIAL MODEL; PRION PROTEIN; PROTEIN AGGREGATION; PROTEIN DEPOSITION; SHEET STRUCTURE; SUM FREQUENCY GENERATION VIBRATIONAL SPECTROSCOPIES; SUM FREQUENCY GENERATION VIBRATIONAL SPECTROSCOPY; SURFACE NORMALS; TILT ANGLE; TWIST ANGLES;

CELL MEMBRANES; CYTOLOGY; GLYCEROL; NEURODEGENERATIVE DISEASES; PEPTIDES; VIBRATIONAL SPECTROSCOPY;

LIPID BILAYERS;

1 PALMITOYL 2 OLEOYLGLYCERO 3 PHOSPHOGLYCEROL; 1-PALMITOYL-2-OLEOYLGLYCERO-3-PHOSPHOGLYCEROL; PEPTIDE FRAGMENT; PHOSPHATIDYLGLYCEROL; PRION PROTEIN (118 135); PRION PROTEIN (118-135);

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; INFRARED SPECTROSCOPY; LIPID BILAYER; MOLECULAR GENETICS; PRION; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; VIBRATION;

AMINO ACID SEQUENCE; LIPID BILAYERS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PHOSPHATIDYLGLYCEROLS; PRIONS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; VIBRATION;

EID: 84870858388     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la302655p     Document Type: Article

References (94)

1. Chiti, F.; Dobson, C. M. Amyloid formation by globular proteins under native conditions Nat. Chem. Biol. 2009, 5, 15-22
2. Outeiro, T. F. FlAsH illuminates Aβ aggregation Nat. Chem. Biol. 2011, 7, 581-582
3. Chiti, F.; Dobson, C. M. Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 2006, 75, 333-366
4. Bates, G. P. One misfolded protein allows others to sneak by Science 2006, 311, 1385-1386
5. Dobson, C. M. Protein folding and misfolding Nature 2003, 426, 884-890
6. Prusiner, S. B. Prions Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 13363-13383
7. Caughey, B.; Raymond, G. J.; Callahan, M. A.; Wong, C. N.; Baron, G. S.; Xiong, L. W. Interactions and conversions of prion protein isoforms Adv. Protein Chem. 2001, 57, 139-169
8. Pan, K.-M.; Baldwin, M.; Nguyen, J.; Gasset, M.; Serban, A.; Groth, D.; Mehlhorn, I.; Huang, Z.; Fletterick, R. J.; Cohen, F. E.; Prusiner, S. B. Conversion of α-helices into β-sheets features in the formation of the scrapie prion proteins Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 10962-10966
9. Meyer, R. K.; McKinley, M. P.; Bowman, K. A.; Braunfeld, M. B.; Barry, R. A.; Prusiner, S. B. Separation and properties of cellular and scrapie prion proteins Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 2310-2314
10. Murphy, R. M. Peptide aggregation in neurodegenerative disease Annu. Rev. Biomed. Eng. 2002, 4, 155-174
11. Caughey, B.; Lansbury, P. T. Protofibrils, pores fibrils, and neurodegeneration: Separating the responsible protein aggregates from the innocent bystanders Annu. Rev. Neurosci. 2003, 26, 267-298
12. Lashuel, H. A.; Lansbury, P. T. Are amyloid diseases caused by protein aggregates that mimic bacterial pore-forming toxins? Q. Rev. Biophys. 2006, 39, 167-201
13. Soto, C. Diagnosing prion diseases: Needs, challenges and hopes Nat. Rev. Micro 2004, 2, 809-819
14. Orte, A.; Birkett, N. R.; Clarke, R. W.; Devlin, G. L.; Dobson, C. M.; Klenerman, D. Direct characterization of amyloidogenic oligomers by single-molecule fluorescence Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 14424-14429
15. Collins, S. R.; Douglass, A.; Vale, R. D.; Weissman, J. S. Mechanism of prion propagation: Amyloid growth occurs by monomer addition PLOS Bio. 2004, 2, 1582-1590
16. King, C. -Y.; Diaz-Avalos, R. Protein-only transmission of three yeast prion strains Nature 2004, 428, 319-323
17. Paravastu, A. K.; Leapman, R. D.; Yau, W. -M.; Tycko, R. Molecular structural basis for polymorphism in Alzheimer's β-amyloid fibrils Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 18349-18354
18. Decatur, S. M. Elucidation of residue-level structure and dynamics of polypeptides via isotope-edited infrared spectroscopy Acc. Chem. Res. 2006, 39, 169-175
19. Elfrink, K.; Ollesch, J.; Stohr, J.; Willbold, D.; Riesner, D.; Gerwert, K. Structural changes of membrane-anchored native PrPc Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 10815-10819
20. Measey, T. J.; Schweitzer-Stenner, R. Vibrational circular dichroism as a probe of fibrillogenesis: The origin of the anomalous intensity enhancement of amyloid-like fibrils J. Am. Chem. Soc. 2011, 133, 1066-1076
21. Grabenauer, M.; Wu, C.; Soto, P.; Shea, J. -E.; Bowers, M. T. Oligomers of the prion protein fragment 106-126 are likely assembled from β-hairpins in solution, and methionine oxidation inhibits assembly without altering the peptide's monomeric conformation J. Am. Chem. Soc. 2010, 132, 532-539
22. Stahl, N.; Borchelt, D. R.; Hsiao, K.; Prusiner, S. B. Scrapie prion protein contains a phosphatidylinositol glycolipid Cell 1987, 51, 229-240
23. Morillas, M.; Swietnicki, W.; Gambetti, P.; Surewicz, W. K. Membrane environment alters the conformational structure of the recombinant human prion protein J. Biol. Chem. 1999, 274, 36859-36865
24. Eberl, H.; Tittmann, P.; Glockshuber, R. Characterization of recombinant, membrane-attached full-length prion protein J. Biol. Chem. 2004, 279, 25058-25065
25. Stahl, N.; Borchelt, D. R.; Prusiner, S. B. Differential release of cellular and scrapie prion proteins from cellular membranes by phosphatidylinositol-specific phospholipase C Biochemistry 1990, 29, 5405-5412
26. Sanghera, N.; Pinheiro, T. J. T. Binding of prion protein to lipid membranes and implications for prion conversion J. Mol. Biol. 2002, 315, 1241-1256
27. Robinson, P. J.; Pinheiro, T. J. T. Phospholipid composition of membranes directs prions down alternative aggregation pathways Biophys. J. 2010, 98, 1520-1528
28. Hegde, R. S. A transmembrane form of the prion protein in neurodegenerative disease Science 1998, 279, 827-834
29. Come, J. H.; Fraser, P. E.; Lansbury, P. T. A kinetic model for amyloid formation in the prion diseases: Importance of seeding Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 5959-5963
30. Pillot, T.; Lins, L.; Goethals, M.; Vanloo, B.; Baert, J.; Vandekerckhove, J.; Rosseneu, M.; Brasseur, R. The 118-135 peptide of the human prion protein forms amyloid fibrils and induces liposome fusion J. Mol. Biol. 1997, 274, 381-393
31. Pillot, T.; Drouet, B.; Pincon-Raymond, M.; Vandekerckhove, J.; Rosseneu, M.; Chambaz, J. A nonfibrillar form of the fusogenic prion protein fragment [118-135] induces apoptotic cell death in rat cortical neurons J. Neurochem. 2000, 75, 2298-2308
32. Cho, K. R.; Huang, Y.; Yu, S.; Yin, S.; Plomp, M.; Qiu, S. R.; Lakshminarayanan, R.; Moradian-Oldak, J.; Sy, M. -S.; De Yoreo, J. J. A multistage pathway for human prion protein aggregation in vitro: From multimeric seeds to β-oligomers and nonfibrillar structures J. Am. Chem. Soc. 2011, 133, 8586-8593
33. Jarrett, J. T.; Lansbury, P. T. Seeding "one-dimensional crystallization" of amyloid: A pathogenic mechanism in Alzheimer's disease and scrapie? Cell 1993, 73, 1055-1058
34. Forloni, G.; Angeretti, N.; Chiesa, R.; Monzani, E.; Salmona, M.; Bugiani, O.; Tagliavini, F. Neurotoxicity of a prion protein fragment Nature 1993, 362, 543-546
35. Salmona, M.; Malesani, P.; De Gioia, L.; Gorla, S.; Bruschi, M.; Molinari, A.; Della Vedova, F.; Pedrotti, B.; Marrari, M. A.; Awan, T.; Bugiani, O.; Forloni, G.; Tagliavini, F. Molecular determinants of the physicochemical properties of a critical prion protein region comprising residues 106-126 Biochem. J. 1999, 342, 207-214
36. Brown, D. R.; Schmidt, B.; Kretzschmar, H. A. Role of microglia and host prion protein in neurotoxicity of a prion protein fragment Nature 1996, 380, 345-347
37. Shen, Y. R. The Principles of Nonlinear Optics; Wiley: New York, 1984.
38. Castellana, E. T.; Cremer, P. S. Solid supported lipid bilayers: From biophysical studies to sensor design Surf. Sci. Rep. 2006, 61, 429-444
39. Lambert, A. G.; Davies, P. B.; Neivandt, D. J. Implementing the theory of sum frequency generation vibrational spectroscopy: A tutorial review Appl. Spectrosc. Rev. 2005, 40, 103-145
40. Gopalakrishnan, S.; Liu, D. F.; Allen, H. C.; Kuo, M.; Shultz, M. J. Vibrational spectroscopic studies of aqueous interfaces: Salts, acids, bases, and nanodrops Chem. Rev. 2006, 106, 1155-1175
41. Wang, H. F.; Gan, W.; Lu, R.; Rao, Y.; Wu, B. H. Quantitative spectral and orientational analysis in surface sum frequency generation vibrational spectroscopy (SFG-VS) Int. Rev. Phys. Chem. 2005, 24, 191-256
42. Ye, S. J.; Nguyen, K. T.; Le Clair, S.; Chen, Z. In situ molecular level studies on membrane related peptides and proteins in real time using sum frequency generation vibrational spectroscopy J. Struct. Biol. 2009, 168, 61-77
43. Chen, X.; Wang, J.; Boughton, A. P.; Kristalyn, C. B.; Chen, Z. Multiple orientation of melittin inside a single lipid bilayer determined by combined vibrational spectroscopic studies J. Am. Chem. Soc. 2007, 129, 1420-1427
44. Nguyen, K. T.; Le Clair, S.; Ye, S. J.; Chen, Z. Orientation determination of protein helical secondary structures using linear and nonlinear vibrational spectroscopy J. Phys. Chem. B 2009, 113, 12169-12180
45. Ye, S. J.; Nguyen, K. T.; Chen, Z. Interactions of alamethicin with model cell membranes Investigated using sum frequency generation vibrational spectroscopy in real time in situ J. Phys. Chem. B 2010, 114, 3334-3340
46. Chen, X.; Boughton, A. P.; Tesmer, J. J. G.; Chen, Z. In situ investigation of heterotrimeric G protein βγ subunit binding and orientation on membrane bilayers J. Am. Chem. Soc. 2007, 129, 12658-12659
47. Ye, S. J.; Li, H. C.; Wei, F.; Jasensky, J.; Boughton, A. P.; Yang, P.; Chen, Z. Observing a model ion channel gating action in model cell membranes in real time in situ: Membrane potential change induced alamethicin orientation change J. Am. Chem. Soc. 2012, 134, 6237-6243
48. Fu, L.; Ma, G.; Yan, E. C. Y. In situ misfolding of human islet amyloid polypeptide at interfaces probed by vibrational sum frequency generation J. Am. Chem. Soc. 2010, 132, 5405-5412
49. Fu, L.; Liu, J.; Yan, E. C. Y. Chiral sum frequency generation spectroscopy for characterizing protein secondary structures at interfaces J. Am. Chem. Soc. 2011, 133, 8094-8097
50. Liu, C.; Monson, C. F.; Yang, T.; Pace, H.; Cremer, P. S. Protein separation by electrophoretic-electroosmotic focusing on supported lipid bilayers Anal. Chem. 2011, 83, 7876-7880
51. Clarke, M. L.; Wang, J.; Chen, Z. Conformational changes of fibrinogen after adsorption J. Phys. Chem. B 2005, 109, 22027-22035
52. Phillips, D. C.; York, R. L.; Mermut, O.; McCrea, K. R.; Ward, R. S.; Somorjai, G. A. Side chain, chain length, and sequence effects on amphiphilic peptide adsorption at hydrophobic and hydrophilic surfaces studied by sum-frequency generation vibrational spectroscopy and quartz crystal microbalance J. Phys. Chem. C 2007, 111, 255-261
53. York, R. L.; Mermut, O.; Phillips, D. C.; McCrea, K. R.; Ward, R. S.; Somorjai, G. A. Influence of ionic strength on the adsorption of a model peptide on hydrophilic silica and hydrophobic polystyrene surfaces: Insight from SFG vibrational spectroscopy J. Phys. Chem. C 2007, 111, 8866-8871
54. Jung, S. -Y.; Lim, S. -M.; Albertorio, F.; Kim, G.; Gurau, M. C.; Yang, R. D.; Holden, M. A.; Cremer, P. S. The vroman effect: A molecular level description of fibrinogen displacement J. Am. Chem. Soc. 2003, 125, 12782-12786
55. Mermut, O.; Phillips, D. C.; York, R. L.; McCrea, K. R.; Ward, R. S.; Somorjai, G. A. In situ adsorption studies of a 14-amino acid leucine-lysine peptide onto hydrophobic polystyrene and hydrophilic silica surfaces using quartz crystal microbalance, atomic force microscopy, and sum frequency generation vibrational spectroscopy J. Am. Chem. Soc. 2006, 128, 3598-3607
56. 15N isotope labels J. Phy. Chem. B 2009, 113, 15423-15426
57. Ye, S. J.; Wei, F. An approach to compatible multiple nonlinear vibrational spectroscopy measurements using a commercial sum frequency generation system Analyst 2011, 136, 2489-2494
58. (3) contribution to sum frequency generation signal Langmuir 2012, 28, 1374-1380
59. Ollesch, J.; Nnemann, E. K.; Glockshuber, R.; Gerwert, K. Prion protein α-to-β transition monitored by time-resolved fourier transform infrared spectroscopy Appl. Spectrosc. 2007, 61, 1025-1031
60. Baron, G. S.; Hughson, A. G.; Raymond, G. J.; Offerdahl, D. K.; Barton, K. A.; Raymond, L. D.; Dorward, D. W.; Caughey, B. Effect of glycans and the glycophosphatidylinositol anchor on strain dependent conformations of scrapie prion protein: Improved purifications and infrared spectra Biochemistry 2011, 50, 4479-4490
61. Ostapchenko, V. G.; Sawaya, M. R.; Makarava, N.; Savtchenko, R.; Nilsson, K. P. R.; Eisenberg, D.; Baskakov, I. V. Two amyloid states of the prion protein display significantly different folding patterns J. Mol. Biol. 2010, 400, 908-921
62. Didonna, A.; Vaccari, L.; Bek, A.; Legname, G. Infrared microspectroscopy: A multiple-screening platform for investigating single-cell biochemical perturbations upon prion infection ACS Chem. Neurosci. 2011, 2, 160-174
63. Cordeiro, Y.; Kraineva, J.; Gomes, M. P. B.; Lopes, M. H.; Martins, V. R.; Lima, L. M. T. R.; Foguel, D.; Winter, R.; Silva, J. L. The amino-terminal PrP domain is crucial to modulate prion misfolding and aggregation Biophys. J. 2005, 89, 2667-2676
64. Middleton, C. T.; Marek, P.; Cao, P.; Chiu, C. C.; Singh, S.; Woys, A. M.; de Pablo, J. J.; Raleigh, D. P.; Zanni, M. T. Two-dimensional infrared spectroscopy reveals the complex behaviour of an amyloid fibril inhibitor Nature Chem. 2012, 4, 355-360
65. Wang, L.; Middleton, C. T.; Singh, S.; Reddy, A. S.; Woys, A. M.; Strasfeld, D. B.; Marek, P.; Raleigh, D. P.; de Pablo, J. J.; Zanni, M. T.; Skinner, J. L. 2DIR spectroscopy of human amylin fibrils reflects stable β-sheet structure J. Am. Chem. Soc. 2011, 133, 16062-16071
66. Kim, Y. S.; Liu, L.; Axelsen, P. H.; Hochstrasser, R. M. Two-dimensional infrared spectra of isotopically diluted amyloid fibrils from Aβ40 Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 7720-7725
67. Baiz, C. R.; Peng, C. S.; Reppert, M. E.; Jones, K. C.; Tokmakoff, A. Coherent two-dimensional infrared spectroscopy: Quantitative analysis of protein secondary structure in solution Analyst 2012, 137, 1793-1799
68. Tamm, L. K.; Tatulian, U. A. Infrared spectroscopy of proteins and peptides in lipid bilayers Q. Rev. Biophys. 1997, 30, 365-429
69. Schladitz, C.; Vieira, E. P.; Hermel, H.; Mohwald, H. Amyloid-β-sheet formation at the air-water interface Biophys. J. 1999, 77, 3305-3310
70. Nguyen, K. T.; King, J. T.; Chen, Z. Orientation determination of interfacial β-sheet structures in situ J. Phys. Chem. B 2010, 114, 8291-8300
71. Lopes, D. H. J.; Meister, A.; Gohlke, A.; Hauser, A.; Blume, A.; Winter, R. Mechanism of islet amyloid polypeptide fibrillation at lipid interfaces studied by infrared reflection absorption spectroscopy Biophys. J. 2007, 93, 3132-3141
72. Ling, Y. L.; Strasfeld, D. B.; Shim, S. H.; Raleigh, D. P.; Zanni, M. T. Two-dimensional infrared spectroscopy provides evidence of an intermediate in the membrane-catalyzed assembly of diabetic amyloid J. Phys. Chem. B 2009, 113, 2498-2505
73. Cerf, E.; Sarroukh, R.; Tamamizu-kato, S.; Breydo, L.; Derclaye, S.; Dufrene, Y. F.; Narayanaswami, V.; Goormaghtigh, E.; Ruysschaert, J. M.; Raussens, V. Antiparallel beta-sheet: A signature structure of the oligomeric amyloid beta-peptide Biochem. J. 2009, 421, 415-423
74. Khurana, R.; Fink, A. L. Do parallel β-helix proteins have a unique Fourier transform infrared spectrum? Biophys. J. 2000, 78, 994-1000
75. Saracino, G. A. A.; Villa, A.; Moro, G.; Cosentino, U.; Salmona, M. Spontaneous β-helical fold in prion protein: The case of PrP(82-146) Proteins 2009, 75, 964-976
76. Shewmaker, F.; Wickner, R. B.; Tycko, R. Amyloid of the prion domain of Sup35p has an in-register parallel β-sheet structure Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 19754-19759
77. Cobb, N. J.; Sönnichsen, F. D.; Mchaourab, H.; Surewicz, W. K. Molecular architecture of human prion protein amyloid: A parallel, in-register β-structure Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 18946-18951
78. +] prion, has a parallel in-register β-sheet structure Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 2403-2408
79. Helmus, J. J.; Surewicz, K.; Apostol, M. I.; Surewicz, W. K.; Jaroniec, C. P. Intermolecular alignment in Y145Stop human prion protein amyloid fibrils probed by solid-state NMR spectroscopy J. Am. Chem. Soc. 2011, 133, 13934-13937
80. Xiao, D.; Fu, L.; Liu, J.; Batista, V. S.; Yan, E. C. Y. Amphiphilic adsorption of human islet amyloid polypeptide aggregates to lipid/aqueous interfaces J. Mol. Bio. 2012, 421, 537-547
81. Fu, L.; Wang, Z. G.; Yan, E. C. Y. Chiral vibrational structures of proteins at interfaces probed by sum frequency generation spectroscopy Int. J. Mol. Sci. 2011, 12, 9404-9425
82. Critchley, P.; Kazlauskaite, J.; Eason, R.; Pinheiro, T. J. T. Binding of prion proteins to lipid membranes Biochem. Biophys. Res. Commun. 2004, 313, 559-567
83. Thompsett, A. R.; Brown, D. R. Dual polarisation interferometry analysis of copper binding to the prion protein: Evidence for two folding states Biochim. Biophys. Acta 2007, 1774, 920-927
84. Kazlauskaite, J.; Sanghera, N.; Sylester, I.; Venien-Bryan, C.; Pinheiro, T. J. T. Structural changes of the prion protein in lipid membranes leading to aggregation and fibrillization Biochemistry 2003, 42, 3295-3304
85. Booth, D. R.; Sunde, M.; Bellotti, V.; Robinson, C. V.; Hutchinson, W. L.; Fraser, P. E.; Hawkins, P. N.; Dobson, C. M.; Radford, S. E.; Blake, C. F.; Pepys, M. B. Instability, unfolding and aggregation of human lysozyme variants underlying amyloid fibrillogenesis Nature 1997, 385, 787-793
86. Strasfeld, D. N.; Ling, Y. L.; Shim, S. -H.; Zanni, M. T. Tracking fiber formation in human islet amyloid polypeptide with automated 2D-IR spectroscopy J. Am. Chem. Soc. 2008, 130, 6698-6699
87. Glover, K. J.; Whiles, J. A.; Wood, M. J.; Melacini, G.; Komives, E. A.; Vold, R. R. Conformational dimorphism and transmembrane orientation of prion protein residues 110-136 in bicelles Biochemistry 2001, 40, 13137-13142
88. Moad, A. J.; Simpson, G. J. A unified treatment of selection rules and symmetry relations for sum-frequency and second harmonic spectroscopies J. Phys. Chem. B 2004, 108, 3548-3562
89. Tsuboi, M.; Kubo, Y.; Akahane, K.; Benevides, J. M.; Thomas, G. J., Jr. Determination of the amide I Raman tensor for the antiparallel β-sheet: Application to silkworm and spider silks J. Raman. Spectrosc. 2006, 37, 240-247
90. Pauling, L.; Corey, R. B. Two rippled-sheet configurations of polypeptide chains, and a note about the pleated sheets Proc. Natl. Acad. Sci. U.S.A. 1953, 39, 253-256
91. Marsh, D. Dichroic ratios in polarized Fourier transform infrared for nonaxial symmetry of β-sheet structures Biophys. J. 1997, 72, 2710-2718
92. Marsh, D. Infrared dichroism of isotope-edited α-helices and β-sheets J. Mol. Biol. 2004, 338, 353-367
93. Schweitzer-Stenner, R. Simulated IR, isotropic and anisotropic Raman, and vibrational circular dichroism amide I band profiles of stacked β-sheets J. Phys. Chem. B 2012, 116, 4141-4153
94. Lee, C.; Cho, M. Local amide I mode frequencies and coupling constants in multiple-stranded antiparallel β-sheet polypeptides J. Phys. Chem. B 2004, 108, 20397-20407