Spontaneous formation of hydrophobic domains in isolated peptides

Journal of Physical Chemistry B

Volumn 117, Issue 17, 2013, Pages 4945-4955

  Gloaguen, Eric ^a,b   Loquais, Yohan ^a,b   Thomas, Jessica A ^c   Pratt, David W ^d   Mons, Michel ^a,b  

^a Centre National de la Recherche Scientifique   (France)

^b CNRS UMR 3299   (France)

^c PURDUE UNIVERSITY CALUMET   (United States)

^d UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; AROMATIC COMPOUNDS; AROMATIZATION; DENSITY FUNCTIONAL THEORY; LASER SPECTROSCOPY; PEPTIDES; PROTEIN FOLDING;

AROMATIC AMINO ACID; DISPERSION-CORRECTED DENSITY FUNCTIONAL; HYDROPHOBIC CLUSTERS; HYDROPHOBIC COLLAPSE; HYDROPHOBIC DOMAINS; SECONDARY STRUCTURES; SPONTANEOUS FORMATION; TERTIARY STRUCTURES;

HYDROPHOBICITY;

EID: 84877021804     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp401499x     Document Type: Article

References (56)

1. Burley, S. K.; Petsko, G. A. Aromatic-Aromatic Interaction: a Mechanism of Protein-Structure Stabilization Science 1985, 229, 23-28
2. Butterfield, S. M.; Patel, P. R.; Waters, M. L. Contribution of Aromatic Interactions to α-Helix Stability J. Am. Chem. Soc. 2002, 124, 9751-9755
3. Chelli, R.; Gervasio, F. L.; Procacci, P.; Schettino, V. Stacking and T-Shape Competition in Aromatic-Aromatic Amino Acid Interactions J. Am. Chem. Soc. 2002, 124, 6133-6143
4. Thomas, A.; Meurisse, R.; Brasseur, R. Aromatic Side-Chain Interactions in Proteins. II. Near- and Far-Sequence Phe-X Pairs Proteins-Struct. Funct. Genet. 2002, 48, 635-644
5. Frank, B. S.; Vardar, D.; Buckley, D. A.; McKnight, C. J. The Role of Aromatic Residues in the Hydrophobic Core of the Villin Headpiece Subdomain Protein Sci. 2002, 11, 680-687
6. Tatko, C. D.; Waters, M. L. Selective Aromatic Interactions in β-Hairpin Peptides J. Am. Chem. Soc. 2002, 124, 9372-9373
7. Waters, M. L. Aromatic Interactions in Model Systems Curr. Opin. Chem. Biol. 2002, 6, 736-741
8. Meyer, E. A.; Castellano, R. K.; Diederich, F. Interactions with Aromatic Rings in Chemical and Biological Recognition Angew. Chem., Int. Ed. 2003, 42, 1210-1250
9. Salonen, L. M.; Ellermann, M.; Diederich, F. Aromatic Rings in Chemical and Biological Recognition: Energetics and Structures Angew. Chem., Int. Ed. 2011, 50, 4808-4842
10. Martin-Gago, P.; Gomez-Caminals, M.; Ramon, R.; Verdaguer, X.; Martin-Malpartida, P.; Aragon, E.; Fernandez-Carneado, J.; Ponsati, B.; Lopez-Ruiz, P.; Cortes, M. A. Fine-Tuning the π-π Aromatic Interactions in Peptides: Somatostatin Analogues Containing Mesityl Alanine Angew. Chem., Int. Ed. 2012, 51, 1820-1825
11. Kauzmann, W. Some Factors in the Interpretation of Protein Denaturation Adv. Protein Chem. 1959, 14, 1-63
12. Mellor, B. L.; Cortes, E. C.; Busath, D. D.; Mazzeo, B. A. Method for Estimating the Internal Permittivity of Proteins Using Dielectric Spectroscopy J. Phys. Chem. B 2011, 115, 2205-2213
13. Tanford, C. Hydrophobic Effect and Organization of Living Matter Science 1978, 200, 1012-1018
14. Chandler, D. Interfaces and the Driving Force of Hydrophobic Assembly Nature 2005, 437, 640-647
15. Huang, J. J.-T.; Larsen, R. W.; Chan, S. I. The Interplay of Turn Formation and Hydrophobic Interactions on the Early Kinetic Events in Protein Folding Chem. Commun. 2012, 48, 487-497
16. Baldwin, R. L. Protein Folding-Making a Network of Hydrophobic Clusters Science 2002, 295, 1657-1658
17. Simons, J. P. Good Vibrations: Probing Biomolecular Structure and Interactions through Spectroscopy in the Gas Phase Mol. Phys. 2009, 107, 2435-2458
18. Schermann, J.-P. Spectroscopy and Modeling of Biomolecular Building Blocks; Elsevier: New York, 2008.
19. Biswal, H. S.; Gloaguen, E.; Loquais, Y.; Tardivel, B.; Mons, M. Strength of NH⋯S Hydrogen Bonds in Methionine Residues Revealed by Gas-Phase IR/UV Spectroscopy J. Phys. Chem. Lett. 2012, 755-759
20. Arunan, E.; Gutowsky, H. S. The Rotational Spectrum, Structure and Dynamics of a Benzene Dimer J. Chem. Phys. 1993, 98, 4294-4296
21. Hobza, P.; Selzle, H. L.; Schlag, E. W. Potential Energy Surface for the Benzene Dimer. Results of Ab Initio CCSD(T) Calculations Show Two Nearly Isoenergetic Structures: T-Shaped and Parallel-Displaced J. Phys. Chem. 1996, 100, 18790-18794
22. Bandyopadhyay, B.; Cheng, T. C.; Wheeler, S. E.; Duncan, M. A. Vibrational Spectroscopy and Theory of the Protonated Benzene Dimer and Trimer J. Phys. Chem. A 2012, 116, 7065-7073
23. Pillsbury, N. R.; Stearns, J. A.; Muller, C. W.; Plusquellic, D. F.; Zwier, T. S. State-Specific Studies of Internal Mixing in a Prototypical Flexible Bichromophore: Diphenylmethane J. Chem. Phys. 2008, 129, 114301
24. 12 Isotopologue J. Chem. Phys. 2008, 129
25. Thomas, A.; Meurisse, R.; Charloteaux, B.; Brasseur, R. Aromatic Side-Chain Interactions in Proteins. I. Main Structural Features Proteins-Structure Function and Genetics 2002, 48, 628-634
26. Baquero, E. E.; James, W. H., III; Choi, T. H.; Jordan, K. D.; Zwier, T. S. Single Conformation Spectroscopy of a Flexible Bichromophore: 3-(4-Hydroxyphenyl)-N-Benzylpropionamide J. Phys. Chem. A 2008, 112, 11115-11123
27. Abo-Riziq, A. G.; Bushnell, J. E.; Crews, B.; Callahan, M. P.; Grace, L.; De Vries, M. S. Discrimination between Diastereoisomeric Dipeptides by IR-UV Double Resonance Spectroscopy and Ab Initio Calculations Int. J. Quantum Chem. 2005, 105, 437-445
28. Schwing, K.; Fricke, H.; Bartl, K.; Polkowska, J.; Schrader, T.; Gerhards, M. Isolated β-Turn Model Systems Investigated by Combined IR/UV Spectroscopy ChemPhysChem 2012, 13, 1576-1582
29. Gloaguen, E.; Valdes, H.; Pagliarulo, F.; Pollet, R.; Tardivel, B.; Hobza, P.; Piuzzi, F.; Mons, M. Experimental and Theoretical Investigation of the Aromatic-Aromatic Interaction in Isolated Capped Dipeptides J. Phys. Chem. A 2010, 114, 2973-2982
30. Gloaguen, E.; Pagliarulo, F.; Brenner, V.; Chin, W.; Piuzzi, F.; Tardivel, B.; Mons, M. Intramolecular Recognition in a Jet-Cooled Short Peptide Chain: γ-Turn Helicity Probed by a Neighbouring Residue Phys. Chem. Chem. Phys. 2007, 9, 4491-4497
31. Case, D. A. Amber 9; University of California: San Francisco, 2006.
32. Hyperchem Professional 7.51; Hypercube, Inc.: Gainesville, FL, 2002.
33. Grimme, S. Semiempirical GGA-Type Density Functional Constructed with a Long-Range Dispersion Correction J. Comput. Chem. 2006, 27, 1787-1799
34. Ahlrichs, R.; Bär, M.; Häser, M.; Horn, H.; Kölmel, C. Electronic-Structure Calculations on Workstation Computers: the Program System Turbomole Chem. Phys. Lett. 1989, 162, 165-169
35. Morgado, C.; Vincent, M. A.; Hillier, I. H.; Shan, X. Can the DFT-D Method Describe the Full Range of Noncovalent Interactions Found in Large Biomolecules? Phys. Chem. Chem. Phys. 2007, 9, 448-451
36. n Clusters from Resonant Ion-Dip Infrared Spectroscopy J. Chem. Phys. 1998, 108, 3379-3382
37. Inokuchi, Y.; Kobayashi, Y.; Ito, T.; Ebata, T. Conformation of L-Tyrosine Studied by Fluorescence-Detected UV-UV and IR-UV Double-Resonance Spectroscopy J. Phys. Chem. A 2007, 111, 3209-3215
38. Plowright, R. J.; Gloaguen, E.; Mons, M. Compact Folding of Isolated Four-Residue Neutral Peptide Chains: H-Bonding Patterns and Entropy Effects ChemPhysChem 2011, 12, 1889-1899
39. Johnson, E. R.; Keinan, S.; Mori-Sanchez, P.; Contreras-Garcia, J.; Cohen, A. J.; Yang, W. Revealing Noncovalent Interactions J. Am. Chem. Soc. 2010, 132, 6498-6506
40. Chin, W.; Piuzzi, F.; Dimicoli, I.; Mons, M. Probing the Competition between Secondary Structures and Local Preferences in Gas Phase Isolated Peptide Backbones Phys. Chem. Chem. Phys. 2006, 8, 1033-1048
41. Chin, W.; Piuzzi, F.; Dognon, J.-P.; Dimicoli, I.; Mons, M. Gas Phase Models of γ-Turns: Effects of Side-Chain/Backbone Interactions Investigated by IR/UV Spectroscopy and Quantum Chemistry J. Chem. Phys. 2005, 123, 084301
42. Albrecht, M.; Rice, C. A.; Suhm, M. A. Elementary Peptide Motifs in the Gas Phase: FTIR Aggregation Study of Formamide, Acetamide, N-Methylformamide, and N-Methylacetamide J. Phys. Chem. A 2008, 112, 7530-7542
43. 2, and Benzene-Toluene J. Chem. Phys. 1984, 81, 4871-4882
44. Carney, J. R.; Zwier, T. S. Infrared and Ultraviolet Spectroscopy of Water-Containing Clusters of Indole, 1-Methylindole, and 3-Methylindole J. Phys. Chem. A 1999, 103, 9943-9957
45. Biswal, H. S.; Loquais, Y.; Tardivel, B.; Gloaguen, E.; Mons, M. Isolated Monohydrates of a Model Peptide Chain: Effect of a First Water Molecule on the Secondary Structure of a Capped Phenylalanine J. Am. Chem. Soc. 2011, 133, 3931-3942
46. Mališ, M.; Loquais, Y.; Gloaguen, E.; Biswal, H. S.; Piuzzi, F.; Tardivel, B.; Brenner, V.; Broquier, M.; Jouvet, C.; Mons, M. Unraveling the Mechanisms of Nonradiative Deactivation in Model Peptides Following Photoexcitation of a Phenylalanine Residue J. Am. Chem. Soc. 2012, 134, 20340-20351
47. Gloaguen, E.; de Courcy, B.; Piquemal, J. P.; Pilmé, J.; Parisel, O.; Pollet, R.; Biswal, H. S.; Piuzzi, F.; Tardivel, B.; Broquier, M. Gas-Phase Folding of a Two-Residue Model Peptide Chain: On the Importance of an Interplay between Experiment and Theory J. Am. Chem. Soc. 2010, 132, 11860-11863
48. Handschuh, M.; Nettesheim, S.; Zenobi, R. Is Infrared Laser-Induced Desorption a Thermal Process? The Case of Aniline J. Phys. Chem. B 1999, 103, 1719-1726
49. Hutchinson, E. G.; Thornton, J. M. A Revised Set of Potentials for β-Turn Formation in Proteins Protein Sci. 1994, 3, 2207-2216
50. Chin, W.; Mons, M.; Dognon, J.-P.; Piuzzi, F.; Tardivel, B.; Dimicoli, I. Competition between Local Conformational Preferences and Secondary Structures in Gas-Phase Model Tripeptides as Revealed by Laser Spectroscopy and Theoretical Chemistry Phys. Chem. Chem. Phys. 2004, 6, 2700-2709
51. Perczel, A.; Angyan, J. G.; Kajtar, M.; Viviani, W.; Rivail, J. L.; Marcoccia, J. F.; Csizmadia, I. G. Peptide Models. 1. Topology of Selected Peptide Conformational Potential-Energy Surfaces (Glycine and Alanine Derivatives) J. Am. Chem. Soc. 1991, 113, 6256-6265
52. Chin, W.; Dognon, J.-P.; Canuel, C.; Piuzzi, F.; Dimicoli, I.; Mons, M.; Compagnon, I.; von Helden, G.; Meijer, G. Secondary Structures of Short Peptide Chains in the Gas Phase: Double Resonance Spectroscopy of Protected Dipeptides J. Chem. Phys. 2005, 122, 054317
53. Atwood, R. E.; Urban, J. J. Conformations of the Glycine Tripeptide Analog Ac-Gly-Gly-NHMe: A Computational Study Including Aqueous Solvation Effects J. Phys. Chem. A 2012, 116, 1396-1408
54. Ottiger, P.; Pfaffen, C.; Leist, R.; Leutwyler, S.; Bachorz, R. A.; Klopper, W. Strong N-H⋯π Hydrogen Bonding in Amide-Benzene Interactions J. Phys. Chem. B 2009, 113, 2937-2943
55. 10-Helix in a Three-Residue Peptide Chain: Role of Side Chain-Backbone Interactions as Evidenced by IR-UV Double Resonance Experiments J. Am. Chem. Soc. 2005, 127, 11900-11901
56. Klein-Seetharaman, J.; Oikawa, M.; Grimshaw, S. B.; Wirmer, J.; Duchardt, E.; Ueda, T.; Imoto, T.; Smith, L. J.; Dobson, C. M.; Schwalbe, H. Long-Range Interactions within a Nonnative Protein Science 2002, 295, 1719-1722