Two-dimensional infrared spectroscopy of amide I vibrations is increasingly being used to study the structure and dynamics of proteins and peptides. Amide I, a primarily carbonyl stretching vibration of the protein backbone, provides information on secondary structures as a result of vibrational couplings and on hydrogen-bonding contacts when isotope labeling is used to isolate specific sites. In parallel with experiments, computational models of amide I spectra that use atomistic structures from molecular dynamics simulations have evolved to calculate experimental spectra. Mixed quantum-classical models use spectroscopic maps to translate the structural information into a quantum-mechanical Hamiltonian for the spectroscopically observed vibrations. This allows one to model the spectroscopy of large proteins, disordered states, and protein conformational dynamics. With improvements in amide I models, quantitative modeling of time-dependent structural ensembles and of direct feedback between experiments and simulations is possible. We review the advances in developing these models, their theoretical basis, and current and future applications.


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Literature Cited

  1. Frauenfelder H, Sligar SG, Wolynes P. 1.  1991. The energy landscapes and motions of proteins. Science 254:1598–603 [Google Scholar]
  2. Khodadadi S, Sokolov AP. 2.  2015. Protein dynamics: from rattling in a cage to structural relaxation. Soft Matter 11:4984–98 [Google Scholar]
  3. Schneider R, Huang J-R, Yao M, Communie G, Ozenne V. 3.  et al. 2012. Towards a robust description of intrinsic protein disorder using nuclear magnetic resonance spectroscopy. Mol. Biosyst. 8:58–68 [Google Scholar]
  4. Hsu S-TD, Bertoncini CW, Dobson CM. 4.  2009. Use of protonless NMR spectroscopy to alleviate the loss of information resulting from exchange-broadening. J. Am. Chem. Soc. 131:7222–23 [Google Scholar]
  5. Felli IC, Pierattelli R. 5.  2012. Recent progress in NMR spectroscopy: toward the study of intrinsically disordered proteins of increasing size and complexity. IUBMB Life 64:473–81 [Google Scholar]
  6. Kuzmenkina EV, Heyes CD, Nienhaus GU. 6.  2005. Single-molecule Förster resonance energy transfer study of protein dynamics under denaturing conditions. PNAS 102:15471–76 [Google Scholar]
  7. Ferreon ACM, Deniz AA. 7.  2011. Protein folding at single-molecule resolution. Biochim. Biophys. Acta 1814:1021–29 [Google Scholar]
  8. Schuler B, Hofmann H. 8.  2013. Single-molecule spectroscopy of protein folding dynamics—expanding scope and timescales. Curr. Opin. Struct. Biol. 23:36–47 [Google Scholar]
  9. Dunker AK, Cortese MS, Romero P, Iakoucheva LM, Uversky VN. 9.  2005. Flexible nets. FEBS J. 272:5129–48 [Google Scholar]
  10. Tompa P. 10.  2005. The interplay between structure and function in intrinsically unstructured proteins. FEBS Lett. 579:3346–54 [Google Scholar]
  11. Dyson HJ. 11.  2011. Expanding the proteome: disordered and alternatively folded proteins. Q. Rev. Biophys. 44:467–518 [Google Scholar]
  12. Dunker AK, Brown CJ, Lawson JD, Iakoucheva LM, Obradović Z. 12.  2002. Intrinsic disorder and protein function. Biochemistry 41:6573–82 [Google Scholar]
  13. Ganim Z, Chung HS, Smith AW, DeFlores LP, Jones KC, Tokmakoff A. 13.  2008. Amide I two-dimensional infrared spectroscopy of proteins. Acc. Chem. Res. 41:432–41 [Google Scholar]
  14. Woutersen S, Hamm P. 14.  2001. Isotope-edited two-dimensional vibrational spectroscopy of trialanine in aqueous solution. J. Chem. Phys. 114:2727–37 [Google Scholar]
  15. Decatur SM. 15.  2006. Elucidation of residue-level structure and dynamics of polypeptides via isotope-edited infrared spectroscopy. Acc. Chem. Res. 39:169–75 [Google Scholar]
  16. Middleton CT, Woys AM, Mukherjee SS, Zanni MT. 16.  2010. Residue-specific structural kinetics of proteins through the union of isotope labeling, mid-IR pulse shaping, and coherent 2D IR spectroscopy. Methods 52:12–22 [Google Scholar]
  17. Hamm P, Helbing J, Bredenbeck J. 17.  2008. Two-dimensional infrared spectroscopy of photoswitchable peptides. Annu. Rev. Phys. Chem. 59:291–317 [Google Scholar]
  18. Panman MR, van Dijk CN, Meuzelaar H, Woutersen S. 18.  2015. Communication. Nanosecond folding dynamics of an alpha helix: time-dependent 2D-IR cross peaks observed using polarization-sensitive dispersed pump-probe spectroscopy. J. Chem. Phys. 142:041103 [Google Scholar]
  19. Khalil M, Demirdöven N, Tokmakoff A. 19.  2003. Coherent 2D IR spectroscopy: molecular structure and dynamics in solution. J. Phys. Chem. A 107:5258 [Google Scholar]
  20. Hochstrasser RM. 20.  2007. Two-dimensional spectroscopy at infrared and optical frequencies. PNAS 104:14190–96 [Google Scholar]
  21. Hamm P, Lim M, Hochstrasser RM. 21.  1998. Structure of the amide I band of peptides measured by femtosecond nonlinear-infrared spectroscopy. J. Phys. Chem. B 102:6123–38 [Google Scholar]
  22. Chung HS, Ganim Z, Jones KC, Tokmakoff A. 22.  2007. Transient 2D IR spectroscopy of ubiquitin unfolding dynamics. PNAS 104:14237–42 [Google Scholar]
  23. Ganim Z, Jones KC, Tokmakoff A. 23.  2010. Insulin dimer dissociation and unfolding revealed by amide I two-dimensional infrared spectroscopy. Phys. Chem. Chem. Phys. 12:3579–88 [Google Scholar]
  24. DeFlores LP, Ganim Z, Nicodemus RA, Tokmakoff A. 24.  2009. Amide I′−II′ 2D IR spectroscopy provides enhanced protein secondary structural sensitivity. J. Am. Chem. Soc. 131:3385–91 [Google Scholar]
  25. Demirdöven N, Cheatum CM, Chung HS, Khalil M, Knoester J, Tokmakoff A. 25.  2004. Two-dimensional infrared spectroscopy of antiparallel β-sheet secondary structure. J. Am. Chem. Soc. 126:7981–90 [Google Scholar]
  26. Woys AM, Almeida AM, Wang L, Chiu C-C, McGovern M. 26.  et al. 2012. Parallel β-sheet vibrational couplings revealed by 2D IR spectroscopy of an isotopically labeled macrocycle: quantitative benchmark for the interpretation of amyloid and protein infrared spectra. J. Am. Chem. Soc. 134:19118–28 [Google Scholar]
  27. Fang C, Senes A, Cristian L, DeGrado WF, Hochstrasser RM. 27.  2006. Amide vibrations are delocalized across the hydrophobic interface of a transmembrane helix dimer. PNAS 103:16740–45 [Google Scholar]
  28. Mukherjee P, Kass I, Arkin IT, Zanni MT. 28.  2006. Structural disorder of the CD3ζ transmembrane domain studied with 2D IR spectroscopy and molecular dynamics simulations. J. Phys. Chem. B 110:24740–49 [Google Scholar]
  29. Manor J, Mukherjee P, Lin Y-S, Leonov H, Skinner JL. 29.  et al. 2009. Gating mechanism of the influenza A M2 channel revealed by 1D and 2D IR spectroscopies. Structure 17:247–54 [Google Scholar]
  30. Ghosh A, Qiu J, DeGrado WF, Hochstrasser RM. 30.  2011. Tidal surge in the M2 proton channel, sensed by 2D IR spectroscopy. PNAS 108:6115–20 [Google Scholar]
  31. Stevenson P, Tokmakoff A. 31.  2015. Distinguishing gramicidin D conformers through two-dimensional infrared spectroscopy of vibrational excitons. J. Chem. Phys. 142:212424 [Google Scholar]
  32. Woutersen S, Hamm P. 32.  2002. Nonlinear two-dimensional vibrational spectroscopy of peptides. J. Phys. Condens. Matter 14:R1035–62 [Google Scholar]
  33. Wang J, Chen J, Hochstrasser RM. 33.  2006. Local structure of β-hairpin isotopomers by FTIR, 2D IR, and ab initio theory. J. Phys. Chem. B 110:7545–55 [Google Scholar]
  34. Kim YS, Hochstrasser RM. 34.  2009. Applications of 2D IR spectroscopy to peptides, proteins, and hydrogen-bond dynamics. J. Phys. Chem. B 113:8231–51 [Google Scholar]
  35. Smith AW, Lessing J, Ganim Z, Peng CS, Tokmakoff A. 35.  et al. 2010. Melting of a β-hairpin peptide using isotope-edited 2D IR spectroscopy and simulations. J. Phys. Chem. B 114:10913–24 [Google Scholar]
  36. Buchanan LE, Dunkelberger EB, Tran HQ, Cheng P-N, Chiu C-C. 36.  et al. 2013. Mechanism of IAPP amyloid fibril formation involves an intermediate with a transient β-sheet. PNAS 110:19285–90 [Google Scholar]
  37. Shim S-H, Gupta R, Ling YL, Strasfeld DB, Raleigh DP, Zanni MT. 37.  2009. Two-dimensional IR spectroscopy and isotope labeling defines the pathway of amyloid formation with residue-specific resolution. PNAS 106:6614–19 [Google Scholar]
  38. Kim YS, Liu L, Axelsen PH, Hochstrasser RM. 38.  2009. 2D IR provides evidence for mobile water molecules in β-amyloid fibrils. PNAS 106:17751–56 [Google Scholar]
  39. Londergan CH, Wang J, Axelsen PH, Hochstrasser RM. 39.  2006. Two-dimensional infrared spectroscopy displays signatures of structural ordering in peptide aggregates. Biophys. J. 90:4672–85 [Google Scholar]
  40. Moran SD, Zanni MT. 40.  2014. How to get insight into amyloid structure and formation from infrared spectroscopy. J. Phys. Chem. Lett. 5:1984–93 [Google Scholar]
  41. Bredenbeck J, Helbing J, Behrendt R, Renner C, Moroder L. 41.  et al. 2003. Transient 2D-IR spectroscopy: snapshots of the nonequilibrium ensemble during the picosecond conformational transition of a small peptide. J. Phys. Chem. B 107:8654–60 [Google Scholar]
  42. Ihalainen JA, Paoli B, Muff S, Backus EHG, Bredenbeck J. 42.  et al. 2008. α-Helix folding in the presence of structural constraints. PNAS 105:9588–93 [Google Scholar]
  43. Bredenbeck J, Helbing J, Kumita JR, Woolley GA, Hamm P. 43.  2005. α-Helix formation in a photoswitchable peptide tracked from picoseconds to microseconds by time-resolved IR spectroscopy. PNAS 102:2379–84 [Google Scholar]
  44. Chung HS, Khalil M, Smith AW, Ganim Z, Tokmakoff A. 44.  2005. Conformational changes during the nanosecond-to-millisecond unfolding of ubiquitin. PNAS 102:612–17 [Google Scholar]
  45. Kolano C, Helbing J, Kozinski M, Sander W, Hamm P. 45.  2006. Watching hydrogen-bond dynamics in a β-turn by transient two-dimensional infrared spectroscopy. Nature 444:469–72 [Google Scholar]
  46. Buchli B, Waldauer SA, Walser R, Donten ML, Pfister R. 46.  et al. 2013. Kinetic response of a photoperturbed allosteric protein. PNAS 110:11725–30 [Google Scholar]
  47. Jones KC, Peng CS, Tokmakoff A. 47.  2013. Folding of a heterogeneous β-hairpin peptide from temperature-jump 2D IR spectroscopy. PNAS 110:2828–33 [Google Scholar]
  48. Tucker MJ, Abdo M, Courter JR, Chen J, Brown SP. 48.  et al. 2013. Nonequilibrium dynamics of helix reorganization observed by transient 2D IR spectroscopy. PNAS 110:17314–19 [Google Scholar]
  49. Bredenbeck J, Helbing J, Nienhaus K, Nienhaus GU, Hamm P. 49.  2007. Protein ligand migration mapped by nonequilibrium 2D-IR exchange spectroscopy. PNAS 104:14243–48 [Google Scholar]
  50. Ma JQ, Pazos IM, Zhang WK, Culik RM, Gai F. 50.  2015. Site-specific infrared probes of proteins. Annu. Rev. Phys. Chem. 66:357–77 [Google Scholar]
  51. Fayer MD. 51.  2009. Dynamics of liquids, molecules, and proteins measured with ultrafast 2D IR vibrational echo chemical exchange spectroscopy. Annu. Rev. Phys. Chem. 60:21–38 [Google Scholar]
  52. Thielges MC, Fayer MD. 52.  2012. Protein dynamics studied with ultrafast two-dimensional infrared vibrational echo spectroscopy. Acc. Chem. Res. 45:1866–74 [Google Scholar]
  53. Cheatum CM, Kohen A. 53.  2013. Relationship of femtosecond-picosecond dynamics to enzyme-catalyzed H-transfer. Dynamics in Enzyme Catalysis J Klinman, S Hammes-Schiffer 1–39 Berlin: Springer [Google Scholar]
  54. Adamczyk K, Candelaresi M, Robb K, Gumiero A, Walsh MA. 54.  et al. 2012. Measuring protein dynamics with ultrafast two-dimensional infrared spectroscopy. Meas. Sci. Technol. 23:062001 [Google Scholar]
  55. King JT, Kubarych KJ. 55.  2012. Site-specific coupling of hydration water and protein flexibility studied in solution with ultrafast 2D-IR spectroscopy. J. Am. Chem. Soc. 134:18705–12 [Google Scholar]
  56. Baiz C, Reppert M, Tokmakoff A. 56.  2013. An introduction to protein 2D IR spectroscopy. Ultrafast Infrared Vibrational Spectroscopy MD Fayer 361–404 New York: Taylor & Francis [Google Scholar]
  57. Byler DM, Susi H. 57.  1986. Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers 25:469–87 [Google Scholar]
  58. Krimm S, Bandekar J. 58.  1986. Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins. Adv. Protein Chem. 38:181–364 [Google Scholar]
  59. Barth A, Zscherp C. 59.  2002. What vibrations tell us about proteins. Q. Rev. Biophys. 35:369–430 [Google Scholar]
  60. Miyazawa T. 60.  1960. Perturbation treatment of the characteristic vibrations of polypeptide chains in various configurations. J. Chem. Phys. 32:1647–52 [Google Scholar]
  61. Miyazawa T, Blout ER. 61.  1961. The infrared spectra of polypeptides in various conformations: amide I and II bands. J. Am. Chem. Soc. 83:712–19 [Google Scholar]
  62. Krimm S, Abe Y. 62.  1972. Intermolecular interaction effects in the amide I vibrations of β polypeptides. PNAS 69:2788–92 [Google Scholar]
  63. Torii H, Tasumi M. 63.  1992. Model calculations on the amide-I infrared bands of globular proteins. J. Chem. Phys. 96:3379–87 [Google Scholar]
  64. De Marco L, Thämer M, Reppert M, Tokmakoff A. 64.  2014. Direct observation of intermolecular interactions mediated by hydrogen bonding. J. Chem. Phys. 141:034502 [Google Scholar]
  65. Torres J, Kukol A, Goodman JM, Arkin IT. 65.  2001. Site-specific examination of secondary structure and orientation determination in membrane proteins: the peptidic 13C=18O group as a novel infrared probe. Biopolymers 59:396–401 [Google Scholar]
  66. Marecek J, Song B, Brewer S, Belyea J, Dyer RB, Raleigh DP. 66.  2007. A simple and economical method for the production of 13C,18O-labeled fmoc-amino acids with high levels of enrichment: applications to isotope-edited IR studies of proteins. Org. Lett. 9:4935–37 [Google Scholar]
  67. Hamm P. 67.  2009. For structural biology, try infrared instead. Structure 17:149–50 [Google Scholar]
  68. Baiz CR, Tokmakoff A. 68.  2015. Structural disorder of folded proteins: isotope-edited 2D IR spectroscopy and Markov state modeling. Biophys. J. 108:1747–57 [Google Scholar]
  69. Baiz CR, Lin YS, Peng CS, Beauchamp KA, Voelz VA. 69.  et al. 2014. A molecular interpretation of 2D IR protein folding experiments with Markov state models. Biophys. J. 106:1359–70 [Google Scholar]
  70. Lessing J, Roy S, Reppert M, Baer M, Marx D. 70.  et al. 2012. Identifying residual structure in intrinsically disordered systems: a 2D IR spectroscopic study of the GVGXPGVG peptide. J. Am. Chem. Soc. 134:5032–35 [Google Scholar]
  71. Reppert M, Tokmakoff A. 71.  2013. Electrostatic frequency shifts in amide I vibrational spectra: direct parameterization against experiment. J. Chem. Phys. 138:134116 [Google Scholar]
  72. Smith AW, Tokmakoff A. 72.  2007. Probing local structural events in β-hairpin unfolding with transient nonlinear infrared spectroscopy. Angew. Chem. 46:7984–87 [Google Scholar]
  73. Torii H, Tasumi M. 73.  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 [Google Scholar]
  74. Choi J-H, Ham S, Cho M. 74.  2003. Local amide I mode frequencies and coupling constants in polypeptides. J. Phys. Chem. B 107:9132–38 [Google Scholar]
  75. Ham S, Cha S, Choi J-H, Cho M. 75.  2003. Amide I modes of tripeptides: Hessian matrix reconstruction and isotope effects. J. Chem. Phys. 119:1451–61 [Google Scholar]
  76. Ham S, Cho M. 76.  2003. Amide I modes in the N-methylacetamide dimer and glycine dipeptide analog: diagonal force constants. J. Chem. Phys. 118:6915–22 [Google Scholar]
  77. Watson TM, Hirst JD. 77.  2005. Theoretical studies of the amide I vibrational frequencies of [Leu]-enkephalin. Mol. Phys. 103:1531–46 [Google Scholar]
  78. Gorbunov RD, Kosov DS, Stock G. 78.  2005. Ab initio-based exciton model of amide I vibrations in peptides: definition, conformational dependence, and transferability. J. Chem. Phys. 122:224904 [Google Scholar]
  79. Buchanan EG, James WH, Choi SH, Guo L, Gellman SH. 79.  et al. 2012. Single-conformation infrared spectra of model peptides in the amide I and amide II regions: experiment-based determination of local mode frequencies and inter-mode coupling. J. Chem. Phys. 137:094301 [Google Scholar]
  80. Lakhani A, Roy A, De Poli M, Nakaema M, Formaggio F. 80.  et al. 2011. Experimental and theoretical spectroscopic study of 310-helical peptides using isotopic labeling to evaluate vibrational coupling. J. Phys. Chem. B 115:6252–64 [Google Scholar]
  81. Chi H, Lakhani A, Roy A, Nakaema M, Keiderling TA. 81.  2010. Inter-residue coupling and equilibrium unfolding of PPII helical peptides. Vibrational spectra enhanced with 13C isotopic labeling. J. Phys. Chem. B 114:12744–53 [Google Scholar]
  82. Kubelka J, Bour P, Kiederling TA. 82.  2009. Quantum mechanical calculations of peptide vibrational force fields and spectral intensities. Advances in Biomedical Spectroscopy, Biological and Biomedical Infrared Spectroscopy PI Haris, A Barth 178–223 Amsterdam: IOS [Google Scholar]
  83. Gaigeot M-P. 83.  2010. Theoretical spectroscopy of floppy peptides at room temperature. A DFTMD perspective: gas and aqueous phase. Phys. Chem. Chem. Phys. 12:3336–59 [Google Scholar]
  84. Jansen TLC, Dijkstra AG, Watson TM, Hirst JD, Knoester J. 84.  2006. Modeling the amide I bands of small peptides. J. Chem. Phys. 125:044312 [Google Scholar]
  85. Jansen TLC, Knoester J. 85.  2006. Nonadiabatic effects in the two-dimensional infrared spectra of peptides: application to alanine dipeptide. J. Phys. Chem. B 110:22910–16 [Google Scholar]
  86. Bour P, Keiderling TA. 86.  2003. Empirical modeling of the peptide amide I band IR intensity in water solution. J. Chem. Phys. 119:11253–62 [Google Scholar]
  87. Wang L, Middleton CT, Zanni MT, Skinner JL. 87.  2011. Development and validation of transferable amide I vibrational frequency maps for peptides. J. Phys. Chem. B 115:3713–24 [Google Scholar]
  88. Lin YS, Shorb JM, Mukherjee P, Zanni MT, Skinner JL. 88.  2009. Empirical amide I vibrational frequency map: application to 2D-IR line shapes for isotope-edited membrane peptide bundles. J. Phys. Chem. B 113:592–602 [Google Scholar]
  89. Maekawa H, Ge N-H. 89.  2010. Comparative study of electrostatic models for the amide-I and -II modes: linear and two-dimensional infrared spectra. J. Phys. Chem. B 114:1434–46 [Google Scholar]
  90. Ham S, Kim J-H, Lee H, Cho M. 90.  2003. Correlation between electronic and molecular structure distortions and vibrational properties. II. Amide I modes of NMA-nD2O complexes. J. Chem. Phys. 118:3491–98 [Google Scholar]
  91. Jansen TLC, Knoester J. 91.  2006. A transferable electrostatic map for solvation effects on amide I vibrations and its application to linear and two-dimensional spectroscopy. J. Chem. Phys. 124:044502 [Google Scholar]
  92. Schmidt JR, Corcelli SA, Skinner JL. 92.  2004. Ultrafast vibrational spectroscopy of water and aqueous N-methylacetamide: comparison of different electronic structure/molecular dynamics approaches. J. Chem. Phys. 121:8887–96 [Google Scholar]
  93. Reppert M, Roy AR, Tokmakoff A. 93.  2015. Isotope-enriched protein standards for computational amide I spectroscopy. J. Chem. Phys. 142:125104 [Google Scholar]
  94. Fecko CJ, Eaves JD, Loparo JJ, Tokmakoff A, Geissler P. 94.  2003. Ultrafast hydrogen-bond dynamics in the infrared spectroscopy of water. Science 301:1698–702 [Google Scholar]
  95. Corcelli SA, Lawrence CP, Skinner JL. 95.  2004. Combined electronic structure/molecular dynamics approach for ultrafast infrared spectroscopy of dilute HOD in liquid H2O and D2O. J. Chem. Phys. 120:8107 [Google Scholar]
  96. Rey R, Møller KB, Hynes JT. 96.  2002. Hydrogen bond dynamics in water and ultrafast infrared spectroscopy. J. Phys. Chem. A 106:11993–96 [Google Scholar]
  97. Cho M. 97.  2003. Correlation between electronic and molecular structure distortions and vibrational properties. I. Adiabatic approximations. J. Chem. Phys. 118:3480–90 [Google Scholar]
  98. Małolepsza E, Straub JE. 98.  2014. Empirical maps for the calculation of amide I vibrational spectra of proteins from classical molecular dynamics simulations. J. Phys. Chem. B 118:7848–55 [Google Scholar]
  99. Eaves JD, Tokmakoff A, Geissler P. 99.  2005. Electric field fluctuations drive vibrational dephasing in water. J. Phys. Chem. A 109:9424–36 [Google Scholar]
  100. Cho M. 100.  2009. Vibrational solvatochromism and electrochromism: coarse-grained models and their relationships. J. Chem. Phys. 130:094505 [Google Scholar]
  101. Torii H, Tasumi M. 101.  1997. Charge fluxes and changes in electronic structures as the origin of infrared intensities in the ground and excited electronic states. J. Phys. Chem. B 101:466–71 [Google Scholar]
  102. Torii H, Tasumi M. 102.  1993. Infrared intensities of vibrational modes of an α-helical polypeptide: calculations based on the equilibrium charge/charge flux (ECCF) model. J. Mol. Struct. 300:171–79 [Google Scholar]
  103. Cheam TC, Krimm S. 103.  1985. Infrared intensities of amide modes in N-methylacetamide and poly(glycine I) from ab initio calculations of dipole moment derivatives of N-methylacetamide. J. Chem. Phys. 82:1631–41 [Google Scholar]
  104. Ackels L, Stawski P, Amunson KE, Kubelka J. 104.  2009. On the temperature dependence of amide I intensities of peptides in solution. Vib. Spectrosc. 50:2–9 [Google Scholar]
  105. Wang J, Hochstrasser RM. 105.  2004. Characteristics of the two-dimensional infrared spectroscopy of helices from approximate simulations and analytic models. Chem. Phys. 297:195–219 [Google Scholar]
  106. Ganim Z, Tokmakoff A. 106.  2006. Spectral signatures of heterogeneous protein ensembles revealed by MD simulations of 2D IR spectra. Biophys. J. 91:2636–46 [Google Scholar]
  107. Auer BM, Skinner JL. 107.  2007. Dynamical effects in line shapes for coupled chromophores: time-averaging approximation. J. Chem. Phys. 127:104105 [Google Scholar]
  108. Torii H. 108.  2006. 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 time-domain computational method. J. Phys. Chem. A 110:4822–32 [Google Scholar]
  109. Liang C, Jansen TLC. 109.  2012. An efficient N3-scaling propagation scheme for simulating two-dimensional infrared and visible spectra. J. Chem. Theory Comput. 8:1706–13 [Google Scholar]
  110. Jansen TLC, Auer BM, Yang M, Skinner JL. 110.  2010. Two-dimensional infrared spectroscopy and ultrafast anisotropy decay of water. J. Chem. Phys. 132:224503 [Google Scholar]
  111. Paarmann A, Hayashi T, Mukamel S, Miller RJD. 111.  2009. Nonlinear response of vibrational excitons: simulating the two-dimensional infrared spectrum of liquid water. J. Chem. Phys. 130:204110 [Google Scholar]
  112. Chirgadze YN, Nevskaya NA. 112.  1976. Infrared spectra and resonance interaction of amide-I vibration of the antiparallel-chain pleated sheet. Biopolymers 15:607–25 [Google Scholar]
  113. Hamm P, Lim M, DeGrado WF, Hochstrasser RM. 113.  1999. The two-dimensional infrared nonlinear spectroscopy of a cyclic penta-peptide in relation to its three-dimensional structure. PNAS 96:2036–41 [Google Scholar]
  114. Scheurer C, Piryatinski A, Mukamel S. 114.  2001. Signatures of β-peptide unfolding in two-dimensional vibrational echo spectroscopy: a simulation study. J. Am. Chem. Soc. 123:3114 [Google Scholar]
  115. Krimm S, Reisdorf WC. 115.  1994. Understanding normal modes of proteins. Faraday Discuss. 99:181–97 [Google Scholar]
  116. Torii H, Tatsumi T, Tasumi M. 116.  1997. Effect of hydrogen bonding and solvation in dielectric media on the amide I frequencies: ab initio molecular orbital study. Mikrochim. Acta 14:Suppl.531–33 [Google Scholar]
  117. Hayashi T, Zhuang W, Mukamel S. 117.  2005. Electrostatic DFT map for the complete vibrational amide band of NMA. J. Phys. Chem. A 109:9747–59 [Google Scholar]
  118. Torii H. 118.  2015. Amide I vibrational properties affected by hydrogen bonding out-of-plane of the peptide group. J. Phys. Chem. Lett. 6:727–33 [Google Scholar]
  119. Cai K, Han C, Wang J. 119.  2009. Molecular mechanics force field-based map for peptide amide-I mode in solution and its application to alanine di- and tripeptides. Phys. Chem. Chem. Phys. 11:9149–59 [Google Scholar]
  120. Hamm P, Woutersen S. 120.  2002. Coupling of the amide I modes of the glycine dipeptide. Bull. Chem. Soc. Jpn. 75:985–88 [Google Scholar]
  121. Bondarenko AS, Jansen TLC. 121.  2015. Application of two-dimensional infrared spectroscopy to benchmark models for the amide I band of proteins. J. Chem. Phys. 142:212437 [Google Scholar]
  122. Carr JK, Zabuga AV, Roy S, Rizzo TR, Skinner JL. 122.  2014. Assessment of amide I spectroscopic maps for a gas-phase peptide using IR-UV double-resonance spectroscopy and density functional theory calculations. J. Chem. Phys. 140:224111 [Google Scholar]
  123. Nauli S, Kuhlman B, Baker D. 123.  2001. Computer-based redesign of a protein folding pathway. Nat. Struct. Mol. Biol. 8:602–5 [Google Scholar]
  124. Reppert M, Tokmakoff A. 124.  2015. Quantitative multi-site frequency maps for amide I vibrational spectroscopy. J. Chem. Phys. 143:061102 [Google Scholar]
  125. Nauli S, Kuhlman B, Le Trong I, Stenkamp RE, Teller D, Baker D. 125.  2002. Crystal structures and increased stabilization of the protein g variants with switched folding pathways NuG1 and NuG2. Protein Sci. 11:2924–31 [Google Scholar]
  126. Karjalainen EL, Ersmark T, Barth A. 126.  2012. Optimization of model parameters for describing the amide I spectrum of a large set of proteins. J. Phys. Chem. B 116:4831–42 [Google Scholar]
  127. Wüthrich K. 127.  1990. Protein structure determination in solution by NMR spectroscopy. J. Biol. Chem. 265:22059–62 [Google Scholar]
  128. Pande VS, Beauchamp K, Bowman GR. 128.  2010. Everything you wanted to know about Markov state models but were afraid to ask. Methods 52:99–105 [Google Scholar]
  129. Prinz J-H, Keller B, Noe F. 129.  2011. Probing molecular kinetics with Markov models: metastable states, transition pathways and spectroscopic observables. Phys. Chem. Chem. Phys. 13:16912–27 [Google Scholar]
  130. Keller BG, Prinz J-H, Noé F. 130.  2012. Markov models and dynamical fingerprints: unraveling the complexity of molecular kinetics. Chem. Phys. 396:92–107 [Google Scholar]
  131. Chodera JD, Singhal N, Pande VS, Dill KA, Swope WC. 131.  2007. Automatic discovery of metastable states for the construction of Markov models of macromolecular conformational dynamics. J. Chem. Phys. 126:155101 [Google Scholar]
  132. Yang WY, Pitera JW, Swope WC, Gruebele M. 132.  2004. Heterogeneous folding of the TrpZip hairpin: full atom simulation and experiment. J. Mol. Biol. 336:241–51 [Google Scholar]
  133. Piana S, Klepeis JL, Shaw DE. 133.  2014. Assessing the accuracy of physical models used in protein-folding simulations: quantitative evidence from long molecular-dynamics simulations. Curr. Opin. Struct. Biol. 24:98–105 [Google Scholar]
  134. Skinner JJ, Yu W, Gichana EK, Baxa MC, Hinshaw JR. 134.  et al. 2014. Benchmarking all-atom simulations using hydrogen exchange. PNAS 111:15975–80 [Google Scholar]
  135. Fitzgerald JE, Jha AK, Colubri A, Sosnick TR, Freed KF. 135.  2007. Reduced C(β) statistical potentials can outperform all-atom potentials in decoy identification. Protein Sci. 16:2123–39 [Google Scholar]
  136. Wu Y, Lu M, Chen M, Li J, Ma J. 136.  2007. OPUS-Ca: a knowledge-based potential function requiring only Cα positions. Protein Sci. 16:1449–63 [Google Scholar]
  137. Adhikari AN, Freed KF, Sosnick TR. 137.  2013. Simplified protein models: predicting folding pathways and structure using amino acid sequences. Phys. Rev. Lett. 111:028103 [Google Scholar]
  138. Haddadian EJ, Gong H, Jha AK, Yang X, DeBartolo J. 138.  et al. 2011. Automated real-space refinement of protein structures using a realistic backbone move set. Biophys. J. 101:899–909 [Google Scholar]
  139. Boomsma W, Ferkinghoff-Borg J, Lindorff-Larsen K. 139.  2014. Combining experiments and simulations using the maximum entropy principle. PLOS Comput. Biol. 10:e1003406 [Google Scholar]
  140. White AD, Voth GA. 140.  2014. Efficient and minimal method to bias molecular simulations with experimental data. J. Chem. Theory Comput. 10:3023–30 [Google Scholar]
  141. White AD, Dama JF, Voth GA. 141.  2015. Designing free energy surfaces that match experimental data with metadynamics. J. Chem. Theory Comput. 11:2451–60 [Google Scholar]
  142. Beauchamp Kyle A, Pande Vijay S, Das R. 142.  2014. Bayesian energy landscape tilting: towards concordant models of molecular ensembles. Biophys. J. 106:1381–90 [Google Scholar]
  143. MacCallum JL, Perez A, Dill KA. 143.  2015. Determining protein structures by combining semireliable data with atomistic physical models by Bayesian inference. PNAS 112:6985–90 [Google Scholar]

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