Discriminating trpzip2 and trpzip4 peptides' folding landscape using the two-dimensional infrared spectroscopy: A simulation study

Journal of Chemical Physics

Volumn 140, Issue 5, 2014, Pages

  Wu, Tianmin ^a   Zhang, Ruiting ^a   Li, Huanhuan ^a   Yang, Lijiang ^b   Zhuang, Wei ^a  

^a DALIAN INSTITUTE OF CHEMICAL PHYSICS   (China)

^b PEKING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BIOINFORMATICS; ISOTOPES; PEPTIDES;

CONFORMATIONAL ANALYSIS; INFRARED MEASUREMENTS; PROPAGATION METHOD; SAMPLING TECHNIQUE; SIMULATION STUDIES; SPECTROSCOPIC MODELS; THERMAL UNFOLDING; TWO-DIMENSIONAL INFRARED SPECTROSCOPY;

FOURIER TRANSFORM INFRARED SPECTROSCOPY;

PROTEIN; TRPZIP2 PROTEIN;

ARTICLE; CHEMISTRY; CONFORMATION; INFRARED SPECTROPHOTOMETRY; MOLECULAR DYNAMICS; PROTEIN FOLDING;

MOLECULAR CONFORMATION; MOLECULAR DYNAMICS SIMULATION; PROTEIN FOLDING; PROTEINS; SPECTROPHOTOMETRY, INFRARED;

EID: 84905562684     PISSN: 00219606     EISSN: None     Source Type: Journal    
DOI: 10.1063/1.4863562     Document Type: Article

References (87)

1. H. Frauenfelder, S. G. Sligar, and P. G. Wolynes, "The energy landscapes and motions of proteins,"Science 254, 1598-1603 (1991). 10.1126/science.1749933
2. C.-Y. Huang, Z. Getahun, Y. Zhu, J. W. Klemke, W. F. DeGrado, and F. G. Helix, "Formation via conformation diffusion search,"Proc. Natl. Acad. Sci. U.S.A. 99, 2788-2793 (2002). 10.1073/pnas.052700099
3. K. A. Dill, S. B. Ozkan, M. S. Shell, and T. R. Weikl, "The protein folding problem,"Annu. Rev. Biophys. 37, 289-316 (2008). 10.1146/annurev.biophys.37.092707.153558
4. M. Gruebele "The fast protein folding problem,"Annu. Rev. Phys. Chem. 50, 485-516 (1999). 10.1146/annurev.physchem.50.1.485
5. C. B. Anfinsen and H. A. Scheraga, "Experimental and theoretical aspects of protein folding,"Adv. Protein Chem. 29, 205-300 (1975). 10.1016/S0065-3233(08)60413-1
6. J. Kubelka, J. Hofrichter, and W. A. Eaton, "The protein folding "speed limit","Curr. Opin. Struct. Biol. 14, 76-88 (2004). 10.1016/j.sbi.2004.01.013
7. Y. Xu, P. Purkayastha, and F. Gai, "Nanosecond folding dynamics of a three-stranded β-sheet,"J. Am. Chem. Soc. 128, 15836-15842 (2006). 10.1021/ja064865+
8. H. Maity, M. Maity, M. M. Krishna, L. Mayne, and S. W. Englander, "Protein folding: The stepwise assembly of foldon units,"Proc. Natl. Acad. Sci. U.S.A. 102, 4741-4746 (2005). 10.1073/pnas.0501043102
9. P. E. Leopold, M. Montal, and J. N. Onuchic, "Protein folding funnels: A kinetic approach to the sequence-structure relationship,"Proc. Natl. Acad. Sci. U.S.A. 89, 8721-8725 (1992). 10.1073/pnas.89.18.8721
10. C. Cecconi, E. A. Shank, C. Bustamante, and S. Marqusee, "Direct observation of the three-state folding of a single protein molecule, "Science 309, 2057-2060 (2005). 10.1126/science.1116702
11. H. Lei, C. Wu, H. Liu, and Y. Duan, "Folding free-energy landscape of villin headpiece subdomain from molecular dynamics simulations,"Proc. Natl. Acad. Sci. U.S.A. 104, 4925-4930 (2007). 10.1073/pnas.0608432104
12. Y. Levy, S. S. Cho, J. N. Onuchic, and P. G. Wolynes, "A survey of flexible protein binding mechanisms and their transition states using native topology based energy landscapes,"J. Mol. Biol. 346, 1121-1145 (2005). 10.1016/j.jmb.2004.12.021
13. A. Matouschek, J. T. Kellis Jr., L. Serrano, and A. R. Fersht, "Mapping the transition state and pathway of protein folding b protein engineering,"Nature (London) 340, 122-126 (1989). 10.1038/340122a0
14. T. R. Sosnick, R. S. Dothager, and B. A. Krantz, "Differences in the folding transition state of ubiquitin indicated by φ and Ψ analyses,"Proc. Natl. Acad. Sci. U.S.A. 101, 17377-17382 (2004). 10.1073/pnas.0407683101
15. R. Zhou, B. J. Berne, and R. Germain, "The free energy landscape for β hairpin folding in explicit water,"Proc. Natl. Acad. Sci. U.S.A. 98, 14931-14936 (2001). 10.1073/pnas.201543998
16. L. J. Yang, Q. Shao, and Y. Q. Gao, "Thermodynamics and folding pathways of trpzip2: An accelerated molecular dynamics simulation study,"J. Phys. Chem. B 113, 803-808 (2009). 10.1021/jp803160f
17. J. Song, F. Gao, R. Z. Cui, F. Shuang, W. Z. Liang, X. H. Huang, and W. Zhuang, "Investigating the structural origin of trpzip2 temperature dependent unfolding fluorescence line shape based on a Markov state model simulation,"J. Phys. Chem. B 116, 12669-12676 (2012). 10.1021/jp304714q
18. Z. Wei, R. Z. Cui, D.-A. Sliva, and X. Huang, "Simulating the T-jump-triggered unfolding dynamics of trpzip2 peptide and its time-resolved IR and two-dimensional IR signals using the Markov state model approach,"J. Phys. Chem. B 115, 5415-5424 (2011). 10.1021/jp109592b
19. M. Lepage, T. Visser, A. M. J. van der Eerden, F. Soulimani, and B. M. Weckhuysen, "Pore curvature and support composition effects on the electronic properties of supported Pt catalysts: An infrared spectroscopy study with CO as probe molecule,"Vib. Spec. 48 (1), 92-100 (2008). 10.1016/j.vibspec.2007.11.006
20. L. Wang and J. L. Skinner, "Thermally induced protein unfolding probed by isotope-edited IR spectroscopy,"J. Phys. Chem. B 116, 9627-9634 (2012). 10.1021/jp304613b
21. W. Yang, J. Pitera, W. Swope, and M. Gruebele, "Multiple ensembles during trpzip unfolding probed by replica-exchange MD and experiment,"J. Mol. Biol. 336, 241-251 (2004). 10.1016/j.jmb.2003.11.033
22. J. W. Pitera, I. Haque, and W. C. Swope, "Absence of reptation in the high-temperature folding of the trpzip2 β-hairpin peptide,"J. Chem. Phys. 124, 141102 (2006). 10.1063/1.2190226
23. Y. Xiao, C. Chen, and Y. He, "Folding mechanism of beta-hairpin trpzip2: Heterogeneity, transition state and folding pathways,"Int. J. Mol. Sci. 10 (6), 2838-2848 (2009). 10.3390/ijms10062838
24. W. Zhuang, T. Hayashi, and S. Mukamel, "Coherent multidimensional vibrational spectroscopy of biomolecules: Concepts, simulations, and challenges,"Angew Chem., Int. Ed. 48, 3750-3781 (2009). 10.1002/anie.200802644
25. Infrared Spectroscopy of Biomolecules, edited by H. H. Mantsch and D. Chapman (Wiley-Liss, New York, 1996), p. 359.
26. S. Hahn, S. Ham, and M. Cho, "Simulation studies of amide I IR absorption and two-dimensional IR spectra of β hairpins in liquid water,"J. Phys. Chem. B 109, 11789-11801 (2005). 10.1021/jp050450j
27. T. L. C. Jansen and J. Knoester, "Two-dimensional infrared population transfer spectroscopy for enhancing structural markers of proteins,"Biophys. J. 94, 1818-1825 (2008). 10.1529/biophysj.107.118851
28. Y. Mu, D. S. Kosov, and G. Stock, "Conformational dynamics of trialanine in water. 2. Comparison of AMBER, CHARMM, GROMOS, and OPLS force fields to NMR and infrared experiments,"J. Phys. Chem. B 107, 5064-5073 (2003). 10.1021/jp022445a
29. R. Santanu, T. L. C. Jansen, and K. Jasper, "Structural classification of the amide I sites of a β-hairpin with isotope label 2DIR spectroscopy,"Phys. Chem. Chem. Phys. 12, 9347-9357 (2010). 10.1039/b925645h
30. K. Y. Sam and R. M. Hochstrasser, "The 2D IR responses of amide and carbonyl modes in water cannot be described by Gaussian frequency fluctuations,"J. Phys. Chem. B 111, 9697-9701 (2007). 10.1021/jp074267x
31. Z. Ganim, H. S. Chung, A. Smith, L. P. DeFlores, K. C. Jones, A. Tokmakoff, and I. Amide, "Two-dimensional infrared spectroscopy of proteins,"Acc. Chem. Res. 41, 432-441 (2008). 10.1021/ar700188n
32. H. Torii and M. Tasumi, "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 (1998). 10.1002/(SICI)1097- 4555(199801)29:1<81::AID-JRS214>3.0.CO;2-H
33. S. Krimm and J. Bandekar, "Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins,"Adv. Protein Chem. 38, 181-364 (1986). 10.1016/S0065-3233(08)60528-8
34. P. Hamm, M. Lim, and R. M. Hochstrasser, "Structure of the amide I band of peptides measured by femtosecond nonlinear-infrared spectroscopy, "J. Phys. Chem. B 102, 6123-6138 (1998). 10.1021/jp9813286
35. T. L. Jansen and J. A. Knoester, "Transferable electrostatic map for solvation effects on amide I vibrations and Its application to linear and two-dimensional spectroscopy,"J. Chem. Phys. 124, 044502 (2006). 10.1063/1.2148409
36. M. Cho, "Coherent two-dimensional optical spectroscopy,"Chem. Rev. 108, 1331-1418 (2008). 10.1021/cr078377b
37. A. Smith and A. Tokmakoff, "Probing local structural events in β-hairpin unfolding with transient nonlinear infrared spectroscopy, "Angew. Chem., Int. Ed. 46, 7984-7987 (2007). 10.1002/anie.200701172
38. M. C. Asplund, M. T. Zanni, and R. M. Hochstrasser, "Two dimensional infrared spectroscopy of peptides by phase-controlled femtosecond vibrational photon echoes,"Proc. Natl. Acad. Sci. U.S.A. 97, 8219-8224 (2000). 10.1073/pnas.140227997
39. S. Mukamel and D. Abramavicius, "Many-body approaches for simulating coherent nonlinear spectroscopies of electronic and vibrational excitons,"Chem. Rev. 104, 2073-2098 (2004). 10.1021/cr020681b
40. J. Wang, "Conformational dependence of anharmonic vibrations in peptides: Amide-I modes in model dipeptide,"J. Phys. Chem. B 112, 4790-4800 (2008). 10.1021/jp710641x
41. Z. Junrong, K. Kyungwon, and M. D. Fayer, "Ultrafast 2D IR vibrational echo spectroscopy,"Acc. Chem. Res. 40, 75-83 (2006). 10.1021/ar068010d
42. I. J. Finkelstein, I. Haruto, K. Seongheun, A. M. Massari, and M. D. Fayer, "Substrate binding and protein conformational dynamics measured via 2D-IR vibrational echo spectroscopy,"Proc. Natl. Acad. Sci. U.S.A. 2007 (104), 2637-2642. 10.1073/pnas.0610027104
43. M. J. Tucker, J. Tang, and F. Gai, "Probing the kinetics of membrane-mediated helix folding,"J. Phys. Chem. B 110, 8105-8109 (2006). 10.1021/jp060900n
44. K. Girdhar, G. Scott, Y. Chemla, and M. Gruebele, "Better biomolecule thermodynamics from kinetics,"J. Chem. Phys. 135, 015102 (2011). 10.1063/1.3607605
45. D. G. Du, Y. J. Zhu, C.-Y. Huang, and F. Gai, "Understanding the key factors that control the rate of β-hairpin folding,"Proc. Natl. Acad. Sci. U.S.A. 101, 15915-15920 (2004). 10.1073/pnas.0405904101
46. G. Martin, "Weighing up protein folding,"Nature (London) 468, 640-641 (2010). 10.1038/468640a
47. A. L. Serrano, M. M. Waegele, and F. Gai, "Spectroscopic studies of protein folding: Linear and nonlinear methods,"Protein Sci. 21, 157-170 (2012). 10.1002/pro.2006
48. W. Zhuang, D. Abramavicius, T. Hayashi, and S. Mukamel, "Simulation protocols for coherent femtosecond vibrational spectra of peptides,"J. Phys. Chem. B 110, 3362-3374 (2006). 10.1021/jp055813u
49. H. Torii, "Effects of intermolecular vibrational coupling and liquid dynamics on the polarized raman and two-dimensional infrared spectral profiles of liquid N,N-dimethylformamide analyzed with a timedomain computational method,"J. Phys. Chem. A 110, 4822-4832 (2006). 10.1021/jp060014c
50. B. M. Auer and J. L. Skinner, "IR and raman spectra of liquid water: Theory and interpretation,"J. Chem. Phys. 128, 224511 (2008). 10.1063/1.2925258
51. K. Kijeong and C. Minhaeng, "Molecular dynamics simulation study of N-methylacetamide in water. II. Two-dimensional infrared pump-probe spectra,"J. Chem. Phys. 119, 2256-2263 (2003). 10.1063/1.1580808
52. W. Tianmin, Y. Lijiang, Z. Ruiting, S. Qiang, and W. Zhuang, "Modeling the thermal unfolding 2DIR spectra of a β-hairpin peptide based on the implicit solvent MD simulation,"J. Phys. Chem. A 117, 6256-6263 (2013). 10.1021/jp400625a
53. B. Christian and K. Martin, "Probability distributions for complex systems: Adaptive umbrella sampling of the potential energy,"J. Phys. Chem. B 102 (5), 865-880 (1998). 10.1021/jp972280j
54. Y. Sugitaa and Y. Okamoto, "Replica-exchange molecular dynamics method for protein folding,"Chem. Phys. Lett. 314, 141-151 (1999). 10.1016/S0009-2614(99)01123-9
55. B. A. Berg and T. Neuhaus, "Multicanonical algorithms for first order phase transitions,"Phys. Lett. B 267, 249-253 (1991). 10.1016/0370-2693(91)91256-U
56. E. Darvea, M. A. Wilson, and A. Pohorille, "Calculating free energies using a scaled-force molecular dynamics algorithm,"Mol. Simul. 28, 113-144 (2002). 10.1080/08927020211975
57. Y. Q. Gao, "An integrate-over-temperature approach for enhanced sampling,"J. Chem. Phys. 128, 064105-1 064105-5 (2008). 10.1063/1.2825614
58. Q. Shao and Y. Q. Gao, "Temperature dependence of hydrogen-bond stability in β-hairpin structures,"J. Chem. Theory Comput. 6, 3750-3760 (2010). 10.1021/ct100436r
59. A. G. Cochran, N. J. Skelton, and M. A. Starovasnik, "Tryptophan zippers: Stable, monomeric β-hairpins,"Proc. Natl. Acad. Sci. U.S.A. 98, 5578-5583 (2001). 10.1073/pnas.091100898
60. H. Soyoun and H. Christian, "Folding of a tryptophan zipper peptide investigated on the basis of the nuclear overhauser effect and thermal denaturation,"J. Phys. Chem. B 115, 15355-15361 (2011). 10.1021/jp206405b
61. H. Nymeyer, "Energy landscape of the trpzip2 peptide,"J. Phys. Chem. B 113 (24), 8288-8295 (2009). 10.1021/jp806749b
62. A. W. Smith, J. Lessing, Z. Ganim, C. S. Peng, A. Tokmakoff, R. Santanu, T. L. C. Jansen, and J. Knoester, "Melting of β-hairpin peptide using isotope-edited 2 D IR spectroscopy and simulations,"J. Phys. Chem. B 114, 10913-10924 (2010). 10.1021/jp104017h
63. D. Deguo, J. Matthew, and F. G. Tucker, "Understanding the mechanism of â-hairpin folding via -value analysis,"Biochemistry 45, 2668-2678 (2006). 10.1021/bi052039s
64. L. J. Yang, Q. Shao, and Y. Q. Gao, "Thermodynamics and folding pathways of trpzip2: An accelerated molecular dynamics simulation study,"J. Chem. Phys. 130, 124111 (2009). 10.1063/1.3097129
65. Q. Shao, L. J. Yang, and Y. Q. Gao, "A test of implicit solvent models on the folding simulation of the GB1 peptide,"J. Chem. Phys. 130, 195104 (2009). 10.1063/1.3132850
66. D. A. Case, T. E. Cheatham III, T. Darden, H. Gohlke, R. Luo, K. M. Merz Jr., A. Onufriev, C. Simmerling, B. Wang, and R. J. Woods, "The amber biomolecular simulation programs,"J. Comput. Chem. 26, 1668-1688 (2005). 10.1002/jcc.20290
67. W. D. Cornell, P. Cieplak, C. I. Bayly, I. R. Gould, K. M. Merz, D. M. Ferguson, D. C. Spellmeyer, T. Fox, J. W. Caldwell, and P. A. Kollman, "A second generation force field for the simulation of proteins, nucleic acids, and organic molecules,"J. Am. Chem. Soc. 117, 5179-5197 (1995). 10.1021/ja00124a002
68. A. Onufriev, D. Bashford, and D. A. Case, "Exploring native states and large-scale conformational changes with a modified generalized born model,"Proteins 55, 383-394 (2004). 10.1002/prot.20033
69. W. L. Jorgensen, J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein, "Comparison of simple potential functions for simulating liquid water,"J. Chem. Phys. 79, 926-935 (1983). 10.1063/1.445869
70. R. Fletcher and C. M. Reeves, "A rapidly convergent descent method for minimization,"Comput. J. 6, 163-168 (1963). 10.1093/comjnl/6.2.163
71. R. Fletcher and M. J. D. Powell, "Function minimization by conjugate gradients,"Comput J. 7, 149-154 (1964). 10.1093/comjnl/7.2.149
72. P. Langevin, "On the theory of brownian motion,"C. R. Acad. Sci. 146, 530-533 (1908).
73. H. J. C. Berendsen, J. P. M. Postma, W. F. van Gunsteren, A. DiNola, and J. R. Haak, "Molecular dynamics with coupling to an external bath,"J. Chem. Phys. 81, 3684-3690 (1984). 10.1063/1.448118
74. U. Essmann, L. Perela, M. L. Berkowitz, T. Darden, H. Lee, and L. G. Pedersen, "A smooth particle mesh ewald method,"J. Chem. Phys. 103, 8577-8593 (1995). 10.1063/1.470117
75. J. P. Ryckaert, G. Ciccotti, and H. J. C. Berendsen, "Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes,"J. Comput. Phys. 23, 327-341 (1977). 10.1016/0021-9991(77)90098-5
76. C. Falvo, B. Palmieri, and S. Mukamel "Coherent infrared multidimensional spectra of the OH stretching band in liquid water simulated by direct nonlinear exciton propagation,"J. Chem. Phys. 130, 184501 (2009). 10.1063/1.3120771
77. T. L. C. Jansen, A. G. Dijkstra, T. M. Watson, J. D. Hirst, and J. Knoester, "Modeling the amide I bands of small peptides,"J. Chem. Phys. 125, 044312 (2006). 10.1063/1.2218516
78. T. L. C. Jansen and J. Knoester, "Nonadiabatic effects in the two-dimensional infrared spectra of peptides: Application to alanine dipeptide,"J. Phys. Chem. B 110, 22910-22916 (2006). 10.1021/jp064795t
79. R. M. Hochstrasser, "Two-dimensional IR-spectroscopy: Polarization anisotropy effects,"Chem. Phys. 266, 273-284 (2001). 10.1016/S0301-0104(01) 00232-4
80. S. Ham and C. Minhaeng, "Amide I modes in the N-methylacetamide dimer and glycine dipeptide analog: Diagonal force constants,"J. Chem. Phys. 118, 6915-6922 (2003). 10.1063/1.1559681
81. A. W. Smith and A. Tokmakoff, "Amide I two-dimensional infrared spectroscopy of β-hairpin peptides,"J. Chem. Phys. 126, 045109 (2007). 10.1063/1.2428300
82. W. Zhuang, D. Abramavicius, and S. Mukamel, "Two-dimensional vibrational optical probes for peptide fast folding investigation,"Proc. Natl. Acad. Sci. U.S.A. 103, 18934-18938 (2006). 10.1073/pnas.0606912103
83. J. J. Loparo, S. T. Roberts, and A. Tokmakoff, "Multidimensional infrared spectroscopy of water. II. Hydrogen bond switching dynamics,"J. Chem. Phys. 125, 194522 (2006). 10.1063/1.2382896
84. K. Lazonder, M. S. Pshenichnikov, and D. A. Wiersma "Easy interpretation of optical two-dimensional correlation spectra,"Opt. Lett. 31 (22), 3354-3356 (2006). 10.1364/OL.31.003354
85. M. S. Shell, R. Ritterson, and K. A. Dill, "A test on peptide stability of AMBER force fields with implicit solvation,"J. Phys. Chem. B 112, 6878-6886 (2008). 10.1021/jp800282x
86. I. Shub, E. Schreiber, and Y. Kliger "Saving significant amount of time in MD simulations by using an implicit solvent model and elevated temperatures computational biology,"ISRN Comput. Biol. 2013, 640125 (2013). 10.1155/2013/640125
87. S. B. Ozkan, G. A. Wu, J. D. Chodera, and K. A. Dill, "Protein folding by zipping and assembly,"Proc. Natl. Acad. Sci. U.S.A. 104, 11987-11992 (2007). 10.1073/pnas.0703700104