1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Analytical Chemistry
  4. Volume 14, 2021
  5. Article

Annual Review of Analytical Chemistry

Volume 14, 2021

Protein Dynamics by Two-Dimensional Infrared Spectroscopy

Abstract

Proteins function as ensembles of interconverting structures. The motions span from picosecond bond rotations to millisecond and longer subunit displacements. Characterization of functional dynamics on all spatial and temporal scales remains challenging experimentally. Two-dimensional infrared spectroscopy (2D IR) is maturing as a powerful approach for investigating proteins and their dynamics. We outline the advantages of IR spectroscopy, describe 2D IR and the information it provides, and introduce vibrational groups for protein analysis. We highlight example studies that illustrate the power and versatility of 2D IR for characterizing protein dynamics and conclude with a brief discussion of the outlook for biomolecular 2D IR.

Keyword(s): 2D IR, infrared spectroscopy, molecular recognition, multidimensional, protein dynamics, vibrational probes
Loading

Article metrics loading...

/content/journals/10.1146/annurev-anchem-091520-091009
2021-07-27
2024-05-02
Loading full text...

Full text loading...

/deliver/fulltext/anchem/14/1/annurev-anchem-091520-091009.html?itemId=/content/journals/10.1146/annurev-anchem-091520-091009&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Frauenfelder H, Sligar SG, Wolynes PG. 1991. The energy landscapes and motions of proteins. Science 254:1598–1603
     [Google Scholar]
  2. 2. 
    Wei G, Xi W, Nussinov R, Ma B. 2016. Protein ensembles: How does nature harness thermodynamic fluctuations for life? The diverse functional roles of conformational ensembles in the cell. Chem. Rev. 116:6516–51
     [Google Scholar]
  3. 3. 
    Campitelli P, Modi T, Kumar S, Ozkan SB. 2020. The role of conformational dynamics and allostery in modulating protein evolution. Annu. Rev. Biophys. 49:267–88
     [Google Scholar]
  4. 4. 
    Ganim Z, Hoi SC, Smith AW, DeFlores LP, Jones KC, Tokmakoff A. 2008. Amide I two-dimensional infrared spectroscopy of proteins. Acc. Chem. Res. 41:432–41
     [Google Scholar]
  5. 5. 
    Kim YS, Hochstrasser RM. 2009. Applications of 2D IR spectroscopy to peptides, proteins, and hydrogen-bond dynamics. J. Phys. Chem. B 113:8231–51
     [Google Scholar]
  6. 6. 
    Hunt NT. 2009. 2D-IR spectroscopy: ultrafast insights into biomolecule structure and function. Chem. Soc. Rev. 38:1837–48
     [Google Scholar]
  7. 7. 
    Le Sueur AL, Horness RE, Thielges MC 2015. Applications of two-dimensional infrared spectroscopy. Analyst 140:4336–49
     [Google Scholar]
  8. 8. 
    Ghosh A, Ostrander JS, Zanni MT. 2017. Watching proteins wiggle: mapping structures with two-dimensional infrared spectroscopy. Chem. Rev. 117:10726–59
     [Google Scholar]
  9. 9. 
    Adhikary R, Zimmermann J, Romesberg FE. 2017. Transparent window vibrational probes for the characterization of proteins with high structural and temporal resolution. Chem. Rev. 117:1927–69
     [Google Scholar]
  10. 10. 
    Hamm P, Lim M, Degrado WF, Hochstrasser RM 1999. The two-dimensional IR nonlinear spectroscopy of a cyclic penta-peptide in relation to its three-dimensional structure. PNAS 96:2036–41
     [Google Scholar]
  11. 11. 
    Mukamel S. 1995. Principles of Nonlinear Optical Spectroscopy New York: Oxford Univ. Press
  12. 12. 
    Hamm P, Zanni M. 2011. Concepts and Methods of 2D Infrared Spectroscopy Cambridge, UK: Cambridge Univ. Press
  13. 13. 
    Park S, Kwak K, Fayer MD. 2007. Ultrafast 2D-IR vibrational echo spectroscopy: a probe of molecular dynamics. Laser Phys. Lett. 4:704–18
     [Google Scholar]
  14. 14. 
    Baiz CR, Błasiak B, Bredenbeck J, Cho M, Choi J-H et al. 2020. Vibrational spectroscopic map, vibrational spectroscopy, and intermolecular interaction. Chem. Rev. 120:7152–218
     [Google Scholar]
  15. 15. 
    Merchant KA, Thompson DE, Fayer MD. 2001. Two-dimensional time-frequency ultrafast infrared vibrational echo spectroscopy. Phys. Rev. Lett. 86:3899–902
     [Google Scholar]
  16. 16. 
    Zanni MT, Hochstrasser RM. 2001. Two-dimensional infrared spectroscopy: a promising new method for the time resolution of structures. Curr. Opin. Struct. Biol. 11:516–22
     [Google Scholar]
  17. 17. 
    Cervetto V, Helbing J, Bredenbeck J, Hamm P. 2004. Double-resonance versus pulsed Fourier transform two-dimensional infrared spectroscopy: an experimental and theoretical comparison. J. Chem. Phys. 121:5935–42
     [Google Scholar]
  18. 18. 
    DeFlores LP, Nicodemus RA, Tokmakoff A. 2007. Two-dimensional Fourier transform spectroscopy in the pump-probe geometry. Opt. Lett. 32:2966–68
     [Google Scholar]
  19. 19. 
    Shim SH, Strasfeld DB, Ling YL, Zanni MT 2007. Automated 2D IR spectroscopy using a mid-IR pulse shaper and application of this technology to the human islet amyloid polypeptide. PNAS 104:14197–202
     [Google Scholar]
  20. 20. 
    Bloem R, Garrett-Roe S, Strzalka H, Hamm P, Donaldson P. 2010. Enhancing signal detection and completely eliminating scattering using quasi-phase-cycling in 2D IR experiments. Opt. Express 18:27067–78
     [Google Scholar]
  21. 21. 
    Karthick Kumar SK, Tamimi A, Fayer MD 2012. Comparisons of 2D IR measured spectral diffusion in rotating frames using pulse shaping and in the stationary frame using the standard method. J. Chem. Phys. 137:184201
     [Google Scholar]
  22. 22. 
    Rock W, Li YL, Pagano P, Cheatum CM. 2013. 2D IR spectroscopy using four-wave mixing, pulse shaping, and IR upconversion: a quantitative comparison. J. Phys. Chem. A 117:6073–83
     [Google Scholar]
  23. 23. 
    Ghosh A, Serrano AL, Oudenhoven TA, Ostrander JS, Eklund EC et al. 2016. Experimental implementations of 2D IR spectroscopy through a horizontal pulse shaper design and a focal plane array detector. Opt. Lett. 41:524–27
     [Google Scholar]
  24. 24. 
    Backus EHG, Garrett-Roe S, Hamm P. 2008. Phasing problem of heterodyne-detected two-dimensional infrared spectroscopy. Opt. Lett. 33:2665–67
     [Google Scholar]
  25. 25. 
    Bristow AD, Karaiskaj D, Dai X, Cundiff ST. 2008. All-optical retrieval of the global phase for two-dimensional Fourier-transform spectroscopy. Opt. Express 16:18017–27
     [Google Scholar]
  26. 26. 
    Middleton CT, Strasfeld DB, Zanni MT. 2009. Polarization shaping in the mid-IR and polarization-based balanced heterodyne detection with application to 2D IR spectroscopy. Opt. Express 17:14526–33
     [Google Scholar]
  27. 27. 
    Osborne DG, Kubarych KJ. 2013. Rapid and accurate measurement of the frequency-frequency correlation function. J. Phys. Chem. A 117:5891–98
     [Google Scholar]
  28. 28. 
    Kramer PL, Giammanco CH, Tamimi A, Hoffman DJ, Sokolowsky KP, Fayer MD. 2016. Quasi-rotating frame: accurate line shape determination with increased efficiency in noncollinear 2D optical spectroscopy. J. Opt. Soc. Am. B 33:1143–56
     [Google Scholar]
  29. 29. 
    Lomont JP, Ostrander JS, Ho J-J, Petti MK, Zanni MT. 2017. Not all β-sheets are the same: amyloid infrared spectra, transition dipole strengths, and couplings investigated by 2D IR spectroscopy. J. Phys. Chem. B 121:8935–45
     [Google Scholar]
  30. 30. 
    Grechko M, Zanni MT. 2012. Quantification of transition dipole strengths using 1D and 2D spectroscopy for the identification of molecular structures via exciton delocalization: application to α-helices. J. Chem. Phys. 137:184202
     [Google Scholar]
  31. 31. 
    Dunkelberger EB, Grechko M, Zanni MT. 2015. Transition dipoles from 1D and 2D infrared spectroscopy help reveal the secondary structures of proteins: application to amyloids. J. Phys. Chem. B 119:14065–75
     [Google Scholar]
  32. 32. 
    Ramos S, Basom EJ, Thielges MC. 2018. Conformational change induced by putidaredoxin binding to ferrous CO-ligated cytochrome P450cam characterized by 2D IR spectroscopy. Front. Mol. Biosci. 5:94
     [Google Scholar]
  33. 33. 
    Kim H, Cho M. 2013. Infrared probes for studying the structure and dynamics of biomolecules. Chem. Rev. 113:5817–47
     [Google Scholar]
  34. 34. 
    Kwak K, Park S, Finkelstein IJ, Fayer M. 2007. Frequency-frequency correlation functions and apodization in two-dimensional infrared vibrational echo spectroscopy: a new approach. J. Chem. Phys. 127:124503
     [Google Scholar]
  35. 35. 
    Kwak K, Rosenfeld DE, Fayer MD. 2008. Taking apart the two-dimensional infrared vibrational echo spectra: more information and elimination of distortions. J. Chem. Phys. 128:204505
     [Google Scholar]
  36. 36. 
    Ishikawa H, Kwak K, Chung JK, Kim S, Fayer MD 2008. Direct observation of fast protein conformational switching. PNAS 105:8619–24
     [Google Scholar]
  37. 37. 
    Tokmakoff A. 2000. Two-dimensional line shapes derived from coherent third-order nonlinear spectroscopy. J. Phys. Chem. A 104:4247–55
     [Google Scholar]
  38. 38. 
    Demirdöven N, Khalil M, Tokmakoff A. 2002. Correlated vibrational dynamics revealed by two-dimensional infrared spectroscopy. Phys. Rev. Lett. 89:237401
     [Google Scholar]
  39. 39. 
    Asbury JB, Steinel T, Stromberg C, Corcelli SA, Lawrence CP et al. 2004. Water dynamics: vibrational echo correlation spectroscopy and comparison to molecular dynamics simulations. J. Phys. Chem. A 108:1107–19
     [Google Scholar]
  40. 40. 
    Roberts ST, Loparo JJ, Tokmakoff A. 2006. Characterization of spectral diffusion from two-dimensional line shapes. J. Chem. Phys. 125:084502
     [Google Scholar]
  41. 41. 
    Eaves JD, Loparo JJ, Fecko CJ, Roberts ST, Tokmakoff A, Geissler PL 2005. Hydrogen bonds in liquid water are broken only fleetingly. PNAS 102:13019–22
     [Google Scholar]
  42. 42. 
    Kwac K, Cho M. 2003. Two-color pump–probe spectroscopies of two- and three-level systems:2-dimensional line shapes and solvation dynamics. J. Phys. Chem. A 107:5903–12
     [Google Scholar]
  43. 43. 
    Golonzka O, Tokmakoff A. 2001. Polarization-selective third-order spectroscopy of coupled vibronic states. J. Chem. Phys. 115:297–309
     [Google Scholar]
  44. 44. 
    Zanni MT, Ge N-H, Kim YS, Hochstrasser RM 2001. Two-dimensional IR spectroscopy can be designed to eliminate the diagonal peaks and expose only the crosspeaks needed for structure determination. PNAS 98:11265–70
     [Google Scholar]
  45. 45. 
    Chalyavi F, Gilmartin PH, Schmitz AJ, Fennie MW, Tucker MJ. 2018. Synthesis of 5-cyano-tryptophan as a two-dimensional infrared spectroscopic reporter of structure. Angew. Chem. Int. Ed. 57:7528–32
     [Google Scholar]
  46. 46. 
    Merchant KA, Thompson DE, Xu Q-H, Williams RB, Loring RF, Fayer MD. 2002. Myoglobin-CO conformational substate dynamics: 2D vibrational echoes and MD simulations. Biophys. J. 82:3277–88
     [Google Scholar]
  47. 47. 
    Merchant KA, Noid WG, Akiyama R, Finkelstein IJ, Goun A et al. 2003. Myoglobin-CO substate structures and dynamics: multidimensional vibrational echoes and molecular dynamics simulations. J. Am. Chem. Soc. 125:13804–18
     [Google Scholar]
  48. 48. 
    Thielges MC, Fayer MD. 2012. Protein dynamics studied with ultrafast two-dimensional infrared vibrational echo spectroscopy. Acc. Chem. Res. 45:1866–74
     [Google Scholar]
  49. 49. 
    Maj M, Oh Y, Park K, Lee J, Kwak KW, Cho M. 2014. Vibrational dynamics of thiocyanate and selenocyanate bound to horse heart myoglobin. J. Chem. Phys. 140:235104
     [Google Scholar]
  50. 50. 
    Van Wilderen LJGW, Kern-Michler D, Müller-Werkmeister HM, Bredenbeck J. 2014. Vibrational dynamics and solvatochromism of the label SCN in various solvents and hemoglobin by time dependent IR and 2D-IR spectroscopy. Phys. Chem. Chem. Phys. 16:19643–53
     [Google Scholar]
  51. 51. 
    Basom EJ, Spearman JW, Thielges MC. 2015. Conformational landscape and the selectivity of cytochrome P450cam. J. Phys. Chem. B 119:6620–27
     [Google Scholar]
  52. 52. 
    Maj M, Kwak K, Cho M. 2015. Ultrafast structural fluctuations of myoglobin-bound thiocyanate and selenocyanate ions measured with two-dimensional infrared photon echo spectroscopy. Chem. Phys. Chem. 16:3468–76
     [Google Scholar]
  53. 53. 
    Horch M, Schoknecht J, Wrathall SLD, Greetham GM, Lenz O, Hunt NT. 2019. Understanding the structure and dynamics of hydrogenases by ultrafast and two-dimensional infrared spectroscopy. Chem. Sci. 10:8981–89
     [Google Scholar]
  54. 54. 
    Fang C, Bauman JD, Das K, Remorino A, Arnold E, Hochstrasser RM 2007. Two-dimensional infrared spectra reveal relaxation of the nonnucleoside inhibitor TMC278 complexed with HIV-1 reverse transcriptase. PNAS 105:1472–77
     [Google Scholar]
  55. 55. 
    Bandaria JN, Dutta S, Hill SE, Kohen A, Cheatum CM. 2008. Fast enzyme dynamics at the active site of formate dehydrogenase. J. Am. Chem. Soc. 130:22–23
     [Google Scholar]
  56. 56. 
    Bandaria JN, Dutta S, Nydegger MW, Rock W, Kohen A, Cheatum CM 2010. Characterizing the dynamics of functionally relevant complexes of formate dehydrogenase. PNAS 107:17974–79
     [Google Scholar]
  57. 57. 
    Pagano P, Guo Q, Kohen A, Cheatum CM. 2016. Oscillatory enzyme dynamics revealed by two-dimensional infrared spectroscopy. J. Phys. Chem. Lett. 7:2507–11
     [Google Scholar]
  58. 58. 
    Demirdöven N, Cheatum CM, Chung HS, Khalil M, Knoester J, Tokmakoff A. 2004. Two-dimensional infrared spectroscopy of antiparallel β-sheet secondary structure. J. Am. Chem. Soc. 126:7981–90
     [Google Scholar]
  59. 59. 
    Maekawa H, Poli MD, Moretto A, Toniolo C, Ge N-H. 2009. Toward detecting the formation of a single helical turn by 2D IR cross peaks between the amide-I and -II modes. J. Phys. Chem. B 113:11775–86
     [Google Scholar]
  60. 60. 
    DeFlores LP, Ganim Z, Nicodemus RA, Tokmakoff A. 2009. Amide I′−II′ 2D IR spectroscopy provides enhanced protein secondary structural sensitivity. J. Am. Chem. Soc. 131:3385–91
     [Google Scholar]
  61. 61. 
    Buchanan LE, Dunkelberger EB, Tran HQ, Cheng P-N, Chiu C-C et al. 2013. Mechanism of IAPP amyloid fibril formation involves an intermediate with a transient β-sheet. PNAS 110:19285–90
     [Google Scholar]
  62. 62. 
    Stevenson P, Tokmakoff A. 2015. Distinguishing gramicidin D conformers through two-dimensional infrared spectroscopy of vibrational excitons. J. Chem. Phys. 142:212424
     [Google Scholar]
  63. 63. 
    Zhang X-X, Jones KC, Fitzpatrick A, Peng CS, Feng C-J et al. 2016. Studying protein–protein binding through T-jump induced dissociation: transient 2D IR spectroscopy of insulin dimer. J. Phys. Chem. B 120:5134–45
     [Google Scholar]
  64. 64. 
    Woutersen S, Pfister R, Hamm P, Mu Y, Kosov DS, Stock G. 2002. Peptide conformational heterogeneity revealed from nonlinear vibrational spectroscopy and molecular-dynamics simulations. J. Chem. Phys. 117:6833–40
     [Google Scholar]
  65. 65. 
    Fang C, Senes A, Cristian L, DeGrado WF, Hochstrasser RM 2006. Amide vibrations are delocalized across the hydrophobic interface of a transmembrane helix dimer. PNAS 103:16740–45
     [Google Scholar]
  66. 66. 
    Remorino A, Hochstrasser RM. 2012. Three-dimensional structures by two-dimensional vibrational spectroscopy. Acc. Chem. Res. 45:1896–905
     [Google Scholar]
  67. 67. 
    Kratochvil HT, Carr JK, Matulef K, Annen AW, Li H et al. 2016. Instantaneous ion configurations in the K+ ion channel selectivity filter revealed by 2D IR spectroscopy. Science 353:1040–44
     [Google Scholar]
  68. 68. 
    Andresen ER, Hamm P. 2009. Site-specific difference 2D-IR spectroscopy of bacteriorhodopsin. J. Phys. Chem. B 113:6520–27
     [Google Scholar]
  69. 69. 
    Edington SC, Gonzalez A, Middendorf TR, Halling DB, Aldrich RW, Baiz CR 2018. Coordination to lanthanide ions distorts binding site conformation in calmodulin. PNAS 115:E3126–34
     [Google Scholar]
  70. 70. 
    Torres J, Kukol A, Goodman JM, Arkin IT. 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]
  71. 71. 
    Mukherjee P, Kass I, Arkin IT, Arkin I, Zanni MT 2006. Picosecond dynamics of a membrane protein revealed by 2D IR. PNAS 103:3528–33
     [Google Scholar]
  72. 72. 
    Backus EHG, Bloem R, Donaldson PM, Ihalainen JA, Pfister R et al. 2010. 2D-IR study of a photoswitchable isotope-labeled α-helix. J. Phys. Chem. B 114:3735–40
     [Google Scholar]
  73. 73. 
    Moran SD, Woys AM, Buchanan LE, Bixby E, Decatur SM, Zanni MT 2012. Two-dimensional IR spectroscopy and segmental 13C labeling reveals the domain structure of human γD-crystallin amyloid fibrils. PNAS 109:3329–34
     [Google Scholar]
  74. 74. 
    Maj M, Lomont JP, Rich KL, Alperstein AM, Zanni MT. 2018. Site-specific detection of protein secondary structure using 2D IR dihedral indexing: a proposed assembly mechanism of oligomeric hIAPP. Chem. Sci. 9:463–74
     [Google Scholar]
  75. 75. 
    Abaskharon RM, Brown SP, Zhang W, Chen J, Smith AB, Gai F. 2017. Isotope-labeled aspartate sidechain as a non-perturbing infrared probe: application to investigate the dynamics of a carboxylate buried inside a protein. Chem. Phys. Lett. 683:193–98
     [Google Scholar]
  76. 76. 
    Kozinski M, Garrett-Roe S, Hamm P. 2008. 2D-IR spectroscopy of the sulfhydryl band of cysteines in the hydrophobic core of proteins. J. Phys. Chem. B 112:7645–50
     [Google Scholar]
  77. 77. 
    Chalyavi F, Hogle DG, Tucker MJ. 2017. Tyrosine as a non-perturbing site-specific vibrational reporter for protein dynamics. J. Phys. Chem. B 121:6380–89
     [Google Scholar]
  78. 78. 
    Ghosh A, Tucker MJ, Hochstrasser RM. 2011. Identification of arginine residues in peptides by 2D-IR echo spectroscopy. J. Phys. Chem. A 115:9731–38
     [Google Scholar]
  79. 79. 
    Huerta-Viga A, Amirjalayer S, Domingos SR, Meuzelaar H, Rupenyan A, Woutersen S. 2015. The structure of salt bridges between Arg+ and Glu− in peptides investigated with 2D-IR spectroscopy: evidence for two distinct hydrogen-bond geometries. J. Chem. Phys. 142:212444
     [Google Scholar]
  80. 80. 
    Thielges MC, Axup JY, Wong D, Lee HS, Chung JK et al. 2011. Two-dimensional IR spectroscopy of protein dynamics using two vibrational labels: a site-specific genetically encoded unnatural amino acid and an active site ligand. J. Phys. Chem. B 115:11294–304
     [Google Scholar]
  81. 81. 
    King JT, Kubarych KJ. 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]
  82. 82. 
    King JT, Arthur EJ, Brooks CL, Kubarych KJ. 2012. Site-specific hydration dynamics of globular proteins and the role of constrained water in solvent exchange with amphiphilic cosolvents. J. Phys. Chem. B 116:5604–11
     [Google Scholar]
  83. 83. 
    Bloem R, Koziol K, Waldauer SA, Buchli B, Walser R et al. 2012. Ligand binding studied by 2D IR spectroscopy using the azidohomoalanine label. J. Phys. Chem. B 116:13705–12
     [Google Scholar]
  84. 84. 
    Woys AM, Mukherjee SS, Skoff DR, Moran SD, Zanni MT. 2013. A strongly absorbing class of non-natural labels for probing protein electrostatics and solvation with FTIR and 2D IR spectroscopies. J. Phys. Chem. B 117:5009–18
     [Google Scholar]
  85. 85. 
    King JT, Arthur EJ, Brooks CL 3rd, Kubarych KJ 2014. Crowding induced collective hydration of biological macromolecules over extended distances. J. Am. Chem. Soc. 136:188–94
     [Google Scholar]
  86. 86. 
    Ross MR, White AM, Yu F, King JT, Pecoraro VL, Kubarych KJ. 2015. Histidine orientation modulates the structure and dynamics of a de novo metalloenzyme active site. J. Am. Chem. Soc. 137:10164–76
     [Google Scholar]
  87. 87. 
    Stucki-Buchli B, Johnson PJM, Bozovic O, Zanobini C, Koziol KL et al. 2017. 2D-IR spectroscopy of an AHA labeled photoswitchable PDZ2 domain. J. Phys. Chem. A 121:9435–45
     [Google Scholar]
  88. 88. 
    Johnson PJM, Koziol KL, Hamm P. 2017. Quantifying biomolecular recognition with site-specific 2D infrared probes. J. Phys. Chem. Lett. 8:2280–84
     [Google Scholar]
  89. 89. 
    Zanobini C, Bozovic O, Jankovic B, Koziol KL, Johnson PJM et al. 2018. Azidohomoalanine: a minimally invasive, versatile, and sensitive infrared label in proteins to study ligand binding. J. Phys. Chem. B 122:10118–25
     [Google Scholar]
  90. 90. 
    Ramos S, Le Sueur AL, Horness RE, Specker JT, Collins JA et al. 2019. Heterogeneous and highly dynamic interface in plastocyanin-cytochrome F complex revealed by site-specific 2D-IR spectroscopy. J. Phys. Chem. B 123:2114–22
     [Google Scholar]
  91. 91. 
    Ramos S, Horness RE, Collins JA, Haak D, Thielges MC. 2019. Site-specific 2D IR spectroscopy: a general approach for the characterization of protein dynamics with high spatial and temporal resolution. Phys. Chem. Chem. Phys. 21:780–88
     [Google Scholar]
  92. 92. 
    Schmidt-Engler JM, Zangl R, Guldan P, Morgner N, Bredenbeck J. 2020. Exploring the 2D-IR repertoire of the −SCN label to study site-resolved dynamics and solvation in the calcium sensor protein calmodulin. Phys. Chem. Chem. Phys. 22:5463–75
     [Google Scholar]
  93. 93. 
    Ramos S, Mammoser CC, Thibodeau KE, Thielges MC. 2021. Dynamics underlying hydroxylation selectivity of cytochrome P450cam. Biophys. J. 120:912–23
     [Google Scholar]
  94. 94. 
    Merrifield RB. 1963. Solid phase peptide synthesis. I. The synthesis of a tetrapeptide. J. Am. Chem. Soc. 85:2149–54
     [Google Scholar]
  95. 95. 
    Chung JK, Thielges MC, Fayer MD. 2012. Conformational dynamics and stability of HP35 studied with 2D IR vibrational echoes. J. Am. Chem. Soc. 134:12118–24
     [Google Scholar]
  96. 96. 
    Chung JK, Thielges MC, Lynch SR, Fayer MD. 2012. Fast dynamics of HP35 for folded and urea-unfolded conditions. J. Phys. Chem. B 116:11024–31
     [Google Scholar]
  97. 97. 
    Urbanek DC, Vorobyev DY, Serrano AL, Gai F, Hochstrasser RM. 2010. The two dimensional vibrational echo of a nitrile probe of the villin HP35 protein. J. Phys. Chem. Lett. 1:3311–15
     [Google Scholar]
  98. 98. 
    Bagchi S, Boxer SG, Fayer MD. 2012. Ribonuclease S dynamics measured using a nitrile label with 2D IR vibrational echo spectroscopy. J. Phys. Chem. B 116:4034–42
     [Google Scholar]
  99. 99. 
    Beligere GS, Dawson PE. 1999. Conformationally assisted protein ligation using C-terminal thioester peptides. J. Am. Chem. Soc. 121:6332–33
     [Google Scholar]
  100. 100. 
    Dawson PE, Kent SBH. 2000. Synthesis of native proteins by chemical ligation. Annu. Rev. Biochem. 69:923–60
     [Google Scholar]
  101. 101. 
    Muir TW. 2003. Semisynthesis of proteins by expressed protein ligation. Annu. Rev. Biochem. 72:249–89
     [Google Scholar]
  102. 102. 
    Fafarman AT, Webb LJ, Chuang JI, Boxer SG. 2006. Site-specific conversion of cysteine thiols into thiocyanate creates an IR probe for electric fields in proteins. J. Am. Chem. Soc. 128:13356–57
     [Google Scholar]
  103. 103. 
    Liu CC, Schultz PG. 2010. Adding new chemistries to the genetic code. Annu. Rev. Biochem. 79:413–44
     [Google Scholar]
  104. 104. 
    Peuker S, Andersson H, Gustavsson E, Maiti KS, Kania R et al. 2016. Efficient isotope editing of proteins for site-directed vibrational spectroscopy. J. Am. Chem. Soc. 138:2312–18
     [Google Scholar]
  105. 105. 
    Park JY, Kwon H-J, Mondal S, Han H, Kwak K, Cho M. 2020. Two-dimensional IR spectroscopy reveals a hidden Fermi resonance band in the azido stretch spectrum of β-azidoalanine. Phys. Chem. Chem. Phys. 22:19223–29
     [Google Scholar]
  106. 106. 
    Schmidt-Engler JM, Blankenburg L, Błasiak B, van Wilderen LJGW, Cho M, Bredenbeck J. 2020. Vibrational lifetime of the SCN protein label in H2O and D2O reports site-specific solvation and structure changes during PYP's photocycle. Anal. Chem. 92:1024–32
     [Google Scholar]
  107. 107. 
    Chung HS, Khalil M, Tokmakoff A. 2004. Nonlinear infrared spectroscopy of protein conformational change during thermal unfolding. J. Phys. Chem. B 108:15332–42
     [Google Scholar]
  108. 108. 
    Huerta-Viga A, Woutersen S. 2013. Protein denaturation with guanidinium: a 2D-IR study. J. Phys. Chem. Lett. 4:3397–401
     [Google Scholar]
  109. 109. 
    Minnes L, Shaw DJ, Cossins BP, Donaldson PM, Greetham GM et al. 2017. Quantifying secondary structure changes in calmodulin using 2D-IR spectroscopy. Anal. Chem. 89:10898–906
     [Google Scholar]
  110. 110. 
    Chung HS, Khalil M, Smith AW, Ganim Z, Tokmakoff A 2005. Conformational changes during the nanosecond-to-millisecond unfolding of ubiquitin. PNAS 102:612–17
     [Google Scholar]
  111. 111. 
    Kolano C, Helbing J, Kozinski M, Sander W, Hamm P. 2006. Watching hydrogen-bond dynamics in a β-turn by transient two-dimensional infrared spectroscopy. Nature 444:469–72
     [Google Scholar]
  112. 112. 
    Causgrove TP, Dyer RB. 2006. Nonequilibrium protein folding dynamics: laser-induced pH-jump studies of the helix–coil transition. Chem. Phys. 323:2–10
     [Google Scholar]
  113. 113. 
    Chung HS, Ganim Z, Jones KC, Tokmakoff A 2007. Transient 2D IR spectroscopy of ubiquitin unfolding dynamics. PNAS 104:14237–42
     [Google Scholar]
  114. 114. 
    Tucker MJ, Abdo M, Courter JR, Chen J, Brown SP et al. 2013. Nonequilibrium dynamics of helix reorganization observed by transient 2D IR spectroscopy. PNAS 110:17314–19
     [Google Scholar]
  115. 115. 
    Meuzelaar H, Panman MR, Woutersen S. 2015. Guanidinium-induced denaturation by breaking of salt bridges. Angew. Chem. Int. Ed. 54:15255–59
     [Google Scholar]
  116. 116. 
    Stevenson P, Tokmakoff A 2017. Time-resolved measurements of an ion channel conformational change driven by a membrane phase transition. PNAS 114:10840–45
     [Google Scholar]
  117. 117. 
    Chiti F, Dobson CM. 2006. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75:333–66
     [Google Scholar]
  118. 118. 
    Shim SH, Gupta R, Ling YL, Strasfeld DB, Raleigh D, Zanni MT 2009. Two-dimensional IR spectroscopy and isotope labeling defines the pathway of amyloid formation with residue-specific resolution. PNAS 106:6614–19
     [Google Scholar]
  119. 119. 
    Ling YL, Strasfeld DB, Shim SH, Raleigh DP, Zanni MT. 2009. Two-dimensional infrared spectroscopy provides evidence of an intermediate in the membrane-catalyzed assembly of diabetic amyloid. J. Phys. Chem. B 113:2498–505
     [Google Scholar]
  120. 120. 
    Dunkelberger EB, Buchanan LE, Marek P, Cao P, Raleigh DP, Zanni MT. 2012. Deamidation accelerates amyloid formation and alters amylin fiber structure. J. Am. Chem. Soc. 134:12658–67
     [Google Scholar]
  121. 121. 
    Iyer A, Roeters SJ, Schilderink N, Hommersom B, Heeren RMA et al. 2016. The impact of N-terminal acetylation of α-synuclein on phospholipid membrane binding and fibril structure. J. Biol. Chem. 291:21110–22
     [Google Scholar]
  122. 122. 
    Zhang TO, Alperstein AM, Zanni MT. 2017. Amyloid β-sheet secondary structure identified in UV-induced cataracts of porcine lenses using 2D IR spectroscopy. J. Mol. Biol. 429:1705–21
     [Google Scholar]
  123. 123. 
    Roeters SJ, Sawall M, Eskildsen CE, Panman MR, Tordai G et al. 2020. Unraveling vealyl amyloid formation using advanced vibrational spectroscopy and microscopy. Biophys. J. 119:87–98
     [Google Scholar]
  124. 124. 
    Fields CR, Dicke SS, Petti MK, Zanni MT, Lomont JP. 2020. A different hIAPP polymorph is observed in human serum than in aqueous buffer: demonstration of a new method for studying amyloid fibril structure using infrared spectroscopy. J. Phys. Chem. Lett. 11:6382–88
     [Google Scholar]
  125. 125. 
    Iyer A, Roeters SJ, Kogan V, Woutersen S, Claessens MMAE, Subramaniam V. 2017. C-terminal truncated α-synuclein fibrils contain strongly twisted β-sheets. J. Am. Chem. Soc. 139:15392–400
     [Google Scholar]
  126. 126. 
    Buchanan LE, Maj M, Dunkelberger EB, Cheng P-N, Nowick JS, Zanni MT. 2018. Structural polymorphs suggest competing pathways for the formation of amyloid fibrils that diverge from a common intermediate species. Biochemistry 57:6470–78
     [Google Scholar]
  127. 127. 
    Lomont JP, Rich KL, Maj M, Ho J-J, Ostrander JS, Zanni MT. 2018. Spectroscopic signature for stable β-amyloid fibrils versus β-sheet-rich oligomers. J. Phys. Chem. B 122:144–53
     [Google Scholar]
  128. 128. 
    Ostrander JS, Lomont JP, Rich KL, Saraswat V, Feingold BR et al. 2019. Monolayer sensitivity enables a 2D IR spectroscopic immuno-biosensor for studying protein structures: application to amyloid polymorphs. J. Phys. Chem. Lett. 10:3836–42
     [Google Scholar]
  129. 129. 
    Roeters SJ, Iyer A, Pletikapiä G, Kogan V, Subramaniam V, Woutersen S. 2017. Evidence for intramolecular antiparallel beta-sheet structure in alpha-synuclein fibrils from a combination of two-dimensional infrared spectroscopy and atomic force microscopy. Sci. Rep. 7:41051
     [Google Scholar]
  130. 130. 
    Coates L. 2020. Ion permeation in potassium ion channels. Acta Crystallogr. D Struct. Biol. 76:326–31
     [Google Scholar]
  131. 131. 
    Zhou Y, MacKinnon R. 2003. The occupancy of ions in the K+ selectivity filter: charge balance and coupling of ion binding to a protein conformational change underlie high conduction rates. J. Mol. Biol. 333:965–75
     [Google Scholar]
  132. 132. 
    Köpfer DA, Song C, Gruene T, Sheldrick GM, Zachariae U, de Groot BL. 2014. Ion permeation in K+ channels occurs by direct coulomb knock-on. Science 346:352–55
     [Google Scholar]
  133. 133. 
    Chin D, Means AR. 2000. Calmodulin: a prototypical calcium sensor. Trends Cell Biol 10:322–28
     [Google Scholar]
  134. 134. 
    Denisov IG, Makris TM, Sligar SG, Schlichting I. 2005. Structure and chemistry of cytochrome P450. Chem. Rev. 105:2253–78
     [Google Scholar]
  135. 135. 
    Atkins WM, Sligar SG. 1989. Molecular recognition in cytochrome P-450: alteration of regioselective alkane hydroxylation via protein engineering. J. Am. Chem. Soc. 111:2715–17
     [Google Scholar]
  136. 136. 
    Lee Y-T, Wilson RF, Rupniewski I, Goodin DB. 2010. P450cam visits an open conformation in the absence of substrate. Biochemistry 49:3412–19
     [Google Scholar]
  137. 137. 
    Fournier F, Guo R, Gardner EM, Donaldson PM, Loeffeld C et al. 2009. Biological and biomedical applications of two-dimensional vibrational spectroscopy: proteomics, imaging, and structural analysis. Acc. Chem. Res. 42:1322–31
     [Google Scholar]
  138. 138. 
    Hume S, Hithell G, Greetham GM, Donaldson PM, Towrie M et al. 2019. Measuring proteins in H2O with 2D-IR spectroscopy. Chem. Sci. 10:6448–56
     [Google Scholar]
  139. 139. 
    Hume S, Greetham GM, Donaldson PM, Towrie M, Parker AW et al. 2020. 2D-infrared spectroscopy of proteins in water: using the solvent thermal response as an internal standard. Anal. Chem. 92:3463–69
     [Google Scholar]
  140. 140. 
    Le Sueur AL, Ramos S, Ellefsen JD, Cook SP, Thielges MC 2017. Evaluation of p-(13C,15N-cyano)phenylalanine as an extended timescale 2D IR probe of proteins. Anal. Chem. 89:5254–60
     [Google Scholar]
  141. 141. 
    Park K-H, Jeon J, Park Y, Lee S, Kwon H-J et al. 2013. Infrared probes based on nitrile-derivatized prolines: thermal insulation effect and enhanced dynamic range. J. Phys. Chem. Lett. 4:2105–10
     [Google Scholar]
  142. 142. 
    Levin DE, Schmitz AJ, Hines SM, Hines KJ, Tucker MJ et al. 2016. Synthesis and evaluation of the sensitivity and vibrational lifetimes of thiocyanate and selenocyanate infrared reporters. RSC Adv 6:36231–37
     [Google Scholar]
  143. 143. 
    Ramos S, Scott KJ, Horness RE, Le Sueur AL, Thielges MC 2017. Extended timescale 2D IR probes of proteins: p-cyanoselenophenylalanine. Phys. Chem. Chem. Phys. 19:10081–86
     [Google Scholar]
  144. 144. 
    Chalyavi F, Schmitz AJ, Fetto NR, Tucker MJ, Brewer SH, Fenlon EE. 2020. Extending the vibrational lifetime of azides with heavy atoms. Phys. Chem. Chem. Phys. 22:18007–13
     [Google Scholar]
  145. 145. 
    Baiz CR, Kubarych KJ. 2011. Ultrabroadband detection of a mid-IR continuum by chirped-pulse upconversion. Opt. Lett. 36:187–89
     [Google Scholar]
  146. 146. 
    De Marco L, Ramasesha K, Tokmakoff A. 2013. Experimental evidence of Fermi resonances in isotopically dilute water from ultrafast broadband IR spectroscopy. J. Phys. Chem. B 117:15319–27
     [Google Scholar]
  147. 147. 
    Stingel AM, Calabrese C, Petersen PB. 2013. Strong intermolecular vibrational coupling through cyclic hydrogen-bonded structures revealed by ultrafast continuum mid-IR spectroscopy. J. Phys. Chem. B 117:15714–19
     [Google Scholar]
  148. 148. 
    Singh V, Peng CS, Li D, Mitra K, Silvestre KJ et al. 2014. Direct observation of multiple tautomers of oxythiamine and their recognition by the thiamine pyrophosphate riboswitch. ACS Chem. Biol. 9:227–36
     [Google Scholar]
  149. 149. 
    Bruening EM, Schauss J, Siebert T, Fingerhut BP, Elsaesser T. 2018. Vibrational dynamics and couplings of the hydrated RNA backbone: a two-dimensional infrared study. J. Phys. Chem. Lett. 9:583–87
     [Google Scholar]
  150. 150. 
    Sanstead PJ, Tokmakoff A. 2018. Direct observation of activated kinetics and downhill dynamics in DNA dehybridization. J. Phys. Chem. B 122:3088–100
     [Google Scholar]
/content/journals/10.1146/annurev-anchem-091520-091009
Loading
Protein Dynamics by Two-Dimensional Infrared Spectroscopy
Annual Review of Analytical Chemistry 14, 299 (2021); https://doi.org/10.1146/annurev-anchem-091520-091009
/content/journals/10.1146/annurev-anchem-091520-091009
/content/journals/10.1146/annurev-anchem-091520-091009
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error