Conformations of alanine-based peptides in water probed by FTIR, raman, vibrational circular dichroism, electronic circular dichroism, and NMR spectroscopy

Biochemistry

Volumn 46, Issue 6, 2007, Pages 1587-1596

  Schweitzer Stenner, Reinhard ^a   Measey, Thomas ^a   Kakalis, Lazaros ^b   Jordan, Frank ^b   Pizzanelli, Silvia ^c   Forte, Claudia ^c   Griebenow, Kai ^d  

^a DREXEL UNIVERSITY   (United States)

^b RUTGERS UNIVERSITY   (United States)

^c AREA DELLA RICERCA   (Italy)

^d UNIVERSITY OF PUERTO RICO   (Puerto Rico)

Author keywords

[No Author keywords available]

Indexed keywords

POLYLYSINE; POLYPROLINE II; RIGHT-HANDED HELICAL; VIBRATIONAL SPECTROSCOPY;

ANISOTROPY; COMPUTER SIMULATION; CONFORMATIONS; FOURIER TRANSFORM INFRARED SPECTROSCOPY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROBES; RAMAN SPECTROSCOPY;

AMINO ACIDS;

ALANINE; ALANINE DERIVATIVE; ALANYLALANYLLYSYLALANINE; AMIDE; LYSINE; POLYPROLINE II; PROLINE DERIVATIVE; TETRAPEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; ELECTRONIC CIRCULAR DICHROISM; INFRARED SPECTROSCOPY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; RAMAN SPECTROMETRY; STRUCTURE ANALYSIS; VIBRATIONAL CIRCULAR DICHROISM;

ALANINE; CIRCULAR DICHROISM; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OLIGOPEPTIDES; PROTEIN CONFORMATION; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SPECTRUM ANALYSIS, RAMAN; VIBRATION;

TETRA;

EID: 33847029566     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi062224l     Document Type: Article

References (73)

1. + salt bridges in short peptides of de novo design, Proc. Natl. Acad. Sci. U.S.A. 84, 8898-8902.
2. Scholtz, J. M., Marqusee, S., Baldwin, R. L., York, E. J., Stewart, J. M., Santoro, M., and Bolen. D. W. (1991) Calorimetric determination of the enthalpy change for the alpha-helix to coil transition of an alanine peptide in water, Proc. Natl. Acad. Sci. U.S.A. 88, 2854-2860.
3. Scholtz, J. M., and Baldwin, R. L. (1992) The mechanism of alpha-helix formation by peptides, Annu. Rev. Biophys. Biomol. Struct. 21, 95-118.
4. Lednev, I. K., Karnoup, A. S., Sparrow, M. C., and Asher, S. A. (1999) R-Helix peptide folding and unfolding activation barriers: A nanosecond UV resonance Raman study, J. Am. Chem. Soc. 121, 8074-8086.
5. Tanford, C. (1998) Protein denaturation, Adv. Protein Chem. 23, 121-282.
6. Flory, P. J. (1969) Statistical Mechanics of Chain Molecules, Wiley, New York.
7. Shi, Z., Olson, C. A., Rose, G. D., Baldwin, R. L., and Kallenbach, N. R. (2002) Polyproline II structure in a sequence of seven alanine residues, Proc. Natl. Acad. Sci. U.S.A. 99, 9190-9195.
8. Cowan, P. M., and McGavin, S. (1955) Structure of poly-L- proline, Nature 176, 501-503.
9. Kentsis, A., Mezei, M., and Osman, R. (2005) Origin of the sequence dependent polyproline II structure in unfolded proteins, Proteins 61, 769-776.
10. Shi, Z., Olson, C. A., Rose, G. A., Baldwin, R. L., and Kallenbach, N. R. (2005) Pcilyproline II propensities from GGXGG peptides reveal an anticorrelation with β-sheet scales, Proc. Natl. Acad. Sci. U.S.A. 102, 17964-17968.
11. Kelly, M. A., Chellgren, B. W., Rucker, A. L., Troutman, J. M., Fried, M. G., Miller, A., and Creamer, T. P. (2001) Host-guest study of left handed polyproline II helix formation, Biochemistry 40, 14376-14383.
12. McColl, I. H., Blanch, E. W., Hecht, L., Kalenbach, N. R., and Barron, L. D. (2004) Vibrational Raman optical activity characterization of poly(L-proline II) helix in alanine oligopeptides, J. Am. Chem. Soc. 126, 5076-5077.
13. Makowska, J., Rodziewicz-Motowidło, S., Bagińska, K., Vila, J. A., Liwo, A., Chmurzyński, L., and Scheraga, H. A. (2006) Polyproline II conformation is one of many local conformational states and is not an overall conformation of unfolded peptides and proteins, Proc. Natl. Acad. Sci. U.S.A. 103, 1744-1749.
14. Zimmermann, S. S., Pottle, M. S., Nemethy, G., and Scheraga, H. A. (1976) Conformational analysis of the 20 naturally occurring amino acid residues using ECEPP, Macromolecules 9, 408-416.
15. Zagrovic, B., Lipfert, J., Sorin, E. J., Millett, I. S., van Gunsteren, W. F., Doniach, S., and Pande, V. S. (2005) Unusual compactness of a polyproline II structure, Proc. Natl. Acad. Sci. U.S.A. 102, 11698-11703.
16. Gnanakaran, S., and Garcia, A. (2003) Validation of an all-atom protein force field: from dipeptides to larger peptides, J. Phys. Chem. B 107, 12555-12557.
17. Duan, Y., Wu, C., Chowdhury, S., Lee, M. C., Xiong, G., Zhang, W., Yang, R., Cieplak, P., Luo, R., Lee, T., Caldwell, J., Wang, J., and Kollman, P. (2003) A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations, J. Comput. Chem. 24, 1999-2012.
18. Gnanakaran, S., and Hochstrasser, R. M. (2001) Conformational preferences and vibrational frequency distributions of short peptides in relation to multidimensional infrared spectroscopy, J. Am. Chem. Soc. 123, 12886-12898.
19. Gnanakarna, S., and Garcia, A. E. (2005) Helix-coil transition of alanine peptides in water: Force field dependence on the folded and unfolded structures, Proteins 59, 773-782.
20. Serrano, L. (1995) Comparison between the φ-distribution of the amino acids in the Protein Data Base and NMR data indicates that amino acids have various φ propensities in the random coil conformation, J. Mol. Biol. 254, 322-333.
21. Tiffany, M. L., and Krimm, S. (1968) New chain conformations of poly(glutamic acid) and polylysine, Biopolymers 6, 1379-1382.
22. Rucker, A. L., and Creamer, T. P. (2002) Polyproline II helical structure in protein unfolded states: Lysine peptides revisited, Protein Sci. 11, 980-985.
23. Eker, F., Griebenow, K., Cao, X., Nafie, L. A., and Schweitzer-Stenner, R. (2004) Preferred backbone conformations in the unfolded state revealed by the structure analysis of alanine based (AXA) tripeptides in solution, Proc. Natl. Acad. Sci. U.S.A. 101, 10054-10059.
24. Tompa, P. (2002) Intrinsically unstructured proteins, Trends Biochem. Sci. 27, 527-533.
25. Vila, J. A., Ripoll, D. R., and Scheraga, H. A. (2001) Influence of lysine content and pH on the stability of alanine-based copolypeptide, Biopolymers 58, 235-246.
26. Schweitzer-Stenner, R., Eker, F., Griebenow, K., Cao, X., and Nafie, L. A. (2004) The conformation of tetraalanine in water determined by polarized Raman, FTIR and VCD spectroscopy, J. Am. Chem. Soc. 126, 2768-2776.
27. Sieler, G., and Schweitzer-Stenner, R. (1997) The amide I mode of peptides in aqueous solution involves vibrational coupling between the peptide group and water molecules of the hydration shell, J. Am. Chem. Soc. 119, 1720-1726.
28. Aue, W. P., Bartholdi, E., and Ernst, R. R. (1976) Two-dimensional spectroscopy. Application to nuclear magnetic resonance, J. Chem. Phys. 64, 2229-2246.
29. Bax, A., and Freeman, R. (1981) Investigation of complex networks of spin-spin coupling by two-dimensional NMR, J. Magn. Reson. 44, 542-561.
30. Jeener, J., Meier, B. H., Bachmann, P., and Ernst, R. R. (1979) Investigation of exchange processes by two-dimensional NMR spectroscopy, J. Chem. Phys. 71, 4546-4553.
31. Macura, S., and Ernst, R. R. (1980) Elucidation of cross relaxation in liquids by two-dimensional N.M.R. spectroscopy, Mol. Phys. 41, 95-117.
32. Redfield, A. G., and Kunz, S. D. (1975) Quadrature Fourier NMR detection: Simple multiplex for dual detection and discussion, J. Magn. Reson. 19, 250-254.
33. 1H spin-spin coupling constants in proteins, Biochem. Biophys. Res. Commun. 113, 967-974.
34. States, D. J., Haberkorn, R. A., and Ruben, D. J. (1982) A two-dimensional nuclear overhauser experiment with pure absorption phase in four quadrants, J. Magn. Reson. 48, 286-292.
35. Hoult, D. I. (1976) Solvent peak saturation with single phase and quadrature fourier transformation, J. Magn. Reson. 21, 337-347.
36. Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum, a. NMR spectroscopy of aqueous solutions, J. Biomol. NMR 2, 661-665.
37. Sklenar, V., Piotto, M., Leppik, R., and Saudek, V. (1993) Gradient-tailored water suppresion for H1-N15. HSQC experiments optimized to retain full sensitivity, J. Magn. Reson. A 102, 241-245.
38. 2 ridges in 2D a: NMR spectra and procedures for suppression, J. Magn. Reson. 66, 187-193.
39. Wüthrich, K. (1986) NMR of Proteins and Nucleic Acids, Wiley-Interscience, New York.
40. Jentten, W., Unger, E., Karvounis, G., Shelnutt, J. A., Dreybrodt, W., and Schweitzer-Stenner, R. (1996) Conformational properties of nickel(II) octaethylporphyrin in solution. 1. Resonance excitation profiles and temperature dependence of structure-sensitive Raman lines, J. Phys. Chem. 100, 14184-14191.
41. Measey, T., and Schweitzer-Stenner, R. (2005) Simulation of amide I′ band profiles of trans polyproline based on an excitonic coupling model, Chem. Phys. Lett. 408, 123-127.
42. Schweitzer-Stenner, R. (2004) Secondary structure analysis of polypeptides based on an excitonic coupling model to describe the band profile of amide I of IR, Raman and vibrational circular dichroism spectra, J. Phys. Chem. B 108, 16965-16975.
43. 1-28 fragment of the amyloid peptide predominantly adopts a polyproline II conformation in an acidic solution, Biochemistry 43, 6893-6898.
44. Woutersen, S., and Hamm, P. (2000) Structure determination of trialanine in water using polarized sensitive two-dimensional vibrational spectroscopy, J. Phys. Chem. B 104, 11316-11320.
45. Measey, T., Hagarman, A., Eker, F., Griebenow, K., and Schweitzer-Stenner, R. (2005) Side chain dependence of intensity and wavenumber position of amide I′ in IR and visible Raman spectra of XA and AX dipeptides, J. Phys. Chem. B 109, 8195-8205.
46. Eker, F., Cao, X., Nafie, L., and Schweitzer-Stenner, R. (2002) Tripeptides adopt stable structures in water. A combined polarized visible Raman, FTIR and VCD spectroscopy study, J. Am. Chem. Soc. 124, 14330-14341.
47. Hamm, P., Lim, M., and Hochstrasser, R. (1998) Structure of the amide I band of peptides measured by femtosecond nonlinear-infrared spectroscopy, J. Phys. Chem. B 102, 6123-6138.
48. Avbelj, F., and Baldwin, R. L. (2003) Role of backbone solvation and electrostatics in generating preferred peptide backbone conformations: Distributions of φ, Proc. Natl. Acad. Sci. U.S.A. 100, 5742-5747.
49. Muggins, M. L. (1943) The structure of fibrous proteins, Chem. Rev. 32, 195-218.
50. Torii, H., and Tasumi, M. (1998) Ab Initio molecular orbital study of the amide I vibrational interactions between the peptide groups in di- and tripeptides and considerations on the conformation of the extended helix, J. Raman Spectrosc. 29, 81-86.
51. Krimm, S., and Badekar, J. (1986) Vibrational spectroscopy or peptides and proteins, Adv. Protein Chem. 38, 181-363.
52. Schweitzer-Stenner, R., Measey, T., Hagarman, A., Eker, F., and Griebenow, K. (2006) Salmon calcitonin and amyloid beta: Two peptides with amyloidogenic capacity adopt different conformational manifolds in their unfolded states, Biochemistry 45, 2810-2819.
53. Eker, F., Griebenow, K., Cao, X., Nafie, L., and Schweitzer-Stenner, R. (2004) Tripeptides with ionizable side chains adopt a perturbed polyproline II structure in water, Biochemistry 43, 613-621.
54. Garcia, A. (2004) Characterization of non-alpha conformations in Ala peptides, Polymer 45, 669-676.
55. Vuister, G. W., and Bax, A. (1993) Quantitative J correlation: a new approach for measuring homonuclear three-bond J (HN Ha) coupling, J. Am. Chem. Soc. 115, 7772-7777.
56. Sreerama, N., and Woody, R. W. (1994) Poly(Pro)II helices in globular proteins: identification and circular dichroic analysis, Biochemistry 33, 10022-10025.
57. Ramachandran, G. N., Ramakrishnan, C., and Sasisekharan, V. (1963) Stereochemistry of polypeptide chain configurations, J Mol. Biol. 7, 95-99.
58. Brant, D. A., and Flory, P. J. (1965) The configuration of random polypeptide chains. II. Theory, J. Am. Chem. Soc. 87, 2791-2800.
59. Hagarman, A., Measey, T., Doddasomayajula, R. S., Dragomir, S., Eker, F., Griebenow, K., and Schweitzer-Stenner, R. (2006) Conformational analysis of XA and AX dipeptides in water by electronic circular spectroscopy, J. Phys. Chem. B 110, 6979-6986.
60. Dragomir, I., Measey, T. J., Hagarman, A. M., and Schweitzer-Stenner, R. (2006) Environment-controlled interchromophore charge transfer transitions in dipeptides probed by UV absorption and electronic circular dichroism spectroscopy, J. Phys. Chem. B 110, 13235-13241.
61. Vila, J. A., Baldoni, H. A., Ripoll, D. R., Ghosh, A., and Scheraga, H. A. (2004) Polyproline II helix conformation in a proline-rich environment: A theoretical study, Biophys. J. 86, 731-742.
62. Woutersen, S., Pfister, R., Hamm, P., Mu, Y., Kosov, D. S., and Stock, G. (2002) Peptide conformational heterogeneity revealed from nonlinear vibrational spectroscopy and molecular dynamics simulations, J. Chem. Phys. 117, 6833-6840.
63. Mu, Y., and Stock, G. (2002) Conformational dynamics of trialanine in water: A water dynamics study, J. Phys. Chem. B 106, 5294-5301.
64. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Jr., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W., and Kollman, P. A. (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules, J. Am. Chem. Soc. 117, 5179-5197.
65. Hu, H., Elstner, M., and Hermans, J. (2003) Comparison of a QM/MM force field and molecular mechanics force fields in simulations of alanine and glycine "dipeptides" (Ace-Ala-Nme and Ace-Gly-Nme) in water in relation to the problem of modeling the unfolded peptide backbone in solution, Proteins 50, 451-463.
66. Tran, H. T., Wang, X., and Pappu, R. V. (2005) Reconciling observations of sequence-specific conformational propensities with the generic polymeric behavior of denatured proteins, Biochemistry 44, 11369-11380.
67. Fiebig, K. M., Schwalbe, H., Buck, M., Smith, L. J., and Dobson, C. M. (1996) Toward a description of the conformations of denatured states of proteins, comparison of a random coil model with NMR measurements, J. Phys. Chem. B 100, 2661-2666.
68. Pizzanelli, S., Monti, S., and Forte, C. (2005) Conformation and orientation of tetralanine in a lyotropic liquid crystal studied by nuclear magnetic resonance, J. Phys. Chem. B 109, 21102-21109.
69. 2 in aqueous solution probed by FTIR and polarized Raman spectroscopy, J. Raman Spectrosc. 37, 248-254.
70. Pappu, R. V., and Rose, G. D. (2002) A simple model for polyproline II structure in unfolded states of alanine-based peptides, Protein Sci. 11, 2437-2455.
71. Asher, S. A., Mikhonin, A. V., and Bykov, S. (2004) UV Raman demonstrates that α-helical polyalanine peptides melt to polyproline II conformations, J. Am. Chem. Soc. 126, 8433-8440.
72. Swindells, M. B., MacArthur, M. W., and Thornton, J. M. (1995) Intrinsic φ,ψ propensities of amino acids, derived from the coil regions of known structures, Nat. Struct. Biol. 2, 596-603.
73. Graf, J., Nguyen, P. H., Stock, G., and Schwalbe, H. (2007) Structure and dynamics of the homologous series of alanine peptides: a joint molecular-dynamics/NMR study, J. Am. Chem. Soc. (in press).