2D IR spectroscopy of histidine: Probing side-chain structure and dynamics via backbone amide vibrations

Journal of Physical Chemistry B

Volumn 118, Issue 28, 2014, Pages 7799-7805

  Ghosh, Ayanjeet ^a   Tucker, Matthew J ^b   Gai, Feng ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF NEVADA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMIDES; CHAINS; ISOTOPES; PEPTIDES; STRUCTURAL DYNAMICS; VIBRATIONS (MECHANICAL);

BIOLOGICAL FUNCTIONS; CONFORMATIONAL TRANSITIONS; FREQUENCY CALCULATIONS; HISTIDINE RESIDUES; SIDE CHAIN STRUCTURE; TIME RESOLUTION; TWO-DIMENSIONAL INFRARED (2D IR); VIBRATIONAL TRANSITIONS;

AMINO ACIDS;

AMIDE; HISTIDINE; PEPTIDE;

CHEMICAL STRUCTURE; CHEMISTRY; INFRARED SPECTROPHOTOMETRY; PROCEDURES;

AMIDES; HISTIDINE; MOLECULAR STRUCTURE; PEPTIDES; SPECTROPHOTOMETRY, INFRARED;

EID: 84904555308     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp411901m     Document Type: Article

References (51)

1. Li, S.; Hong, M. Protonation, Tautomerization, and Rotameric Structure of Histidine: A Comprehensive Study by Magic-Angle-Spinning Solid-State NMR J. Am. Chem. Soc. 2011, 133, 1534-1544
2. Vila, J. A.; Arnautova, Y. A.; Vorobjev, Y.; Scheraga, H. A. Assessing the Fractions of Tautomeric Forms of the Imidazole Ring of Histidine in Proteins as a Function of pH Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 5602-5607
3. Bachovchin, W. W.; Roberts, J. D. N-15 Nuclear Magnetic-Resonance Spectroscopy-State of Histidine in Catalytic Triad of Alpha-Lytic Protease-Implications for Charge-Relay Mechanism of Peptide-Bond Cleavage by Serine Proteases J. Am. Chem. Soc. 1978, 100, 8041-8047
4. Roberts, V. A.; Iverson, B. L.; Iverson, S. A.; Benkovic, S. J.; Lerner, R. A.; Getzoff, E. D.; Tainer, J. A. Antibody Remodeling: A General Solution to the Design of a Metal-Coordination Site in an Antibody Binding Pocket Proc. Natl. Acad. Sci. U.S.A. 1990, 87, 6654-6658
5. Stockel, J.; Safar, J.; Wallace, A. C.; Cohen, F. E.; Prusiner, S. B. Prion Protein Selectively Binds Copper(II) Ions Biochemistry 1998, 37, 7185-7193
6. Wieland, H. A.; Lüddens, H.; Seeburg, P. H. A Single Histidine in GABAA Receptors is Essential for Benzodiazepine Agonist Binding J. Biol. Chem. 1992, 267, 1426-1429
7. Williams, S.; Bledsoe, R. K.; Collins, J. L.; Boggs, S.; Lambert, M. H.; Miller, A. B.; Moore, J.; McKee, D. D.; Moore, L.; Nichols, J.; Parks, D.; Watson, M.; Wisely, B.; Willson, T. M. X-ray Crystal Structure of the Liver X Receptor β Ligand Binding Domain: Regulation by a Histidine-Tryptophan Switch J. Biol. Chem. 2003, 278, 27138-27143
8. Tang, X. S.; Diner, B. A.; Larsen, B. S.; Gilchrist, M. L.; Lorigan, G. A.; Britt, R. D. Identification of Histidine at the Catalytic Site of the Photosynthetic Oxygen-Evolving Complex Proc. Natl. Acad. Sci. U.S.A. 1994, 91, 704-708
9. Shimahara, H.; Yoshida, T.; Shibata, Y.; Shimizu, M.; Kyogoku, Y.; Sakiyama, F.; Nakazawa, T.; Tate, S.; Ohki, S.; Kato, T.; Moriyama, H.; Kishida, K.; Tano, Y.; Ohkubo, T.; Kobayashi, Y. Tautomerism of Histidine 64 Associated with Proton Transfer in Catalysis of Carbonic Anhydrase J. Biol. Chem. 2007, 282, 9646-9656
10. Wang, C.; Lamb, R. A.; Pinto, L. H. Activation of the M2 Ion Channel of Influenza Virus: A Role for the Transmembrane Domain Histidine Residue Biophys. J. 1995, 69, 1363-1371
11. Tu, C. K.; Silverman, D. N.; Forsman, C.; Jonsson, B. H.; Lindskog, S. Role of Histidine-64 in the Catalytic Mechanism of Human Carbonic Anhydrase-Ii Studied with a Site-Specific Mutant Biochemistry 1989, 28, 7913-7918
12. Hong, M.; DeGrado, W. F. Structural Basis for Proton Conduction and Inhibition by the Influenza M2 Protein Protein Sci. 2012, 21, 1620-1633
13. Hu, F. H.; Luo, W. B.; Hong, M. Mechanisms of Proton Conduction and Gating in Influenza M2 Proton Channels from Solid-State NMR Science 2010, 330, 505-508
14. Hu, J.; Fu, R.; Nishimura, K.; Zhang, L.; Zhou, H. X.; Busath, D. D.; Vijayvergiya, V.; Cross, T. A. Histidines, Heart of the Hydrogen Ion Channel from Influenza A Virus: Toward an Understanding of Conductance and Proton Selectivity Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 6865-6870
15. Pinto, L. H.; Lamb, R. A. The M2 Proton Channels of Influenza A and B Viruses J. Biol. Chem. 2006, 281, 8997-9000
16. Tu, C.; Silverman, D. N.; Forsman, C.; Jonsson, B. H.; Lindskog, S. Role of Histidine 64 in the Catalytic Mechanism of Human Carbonic Anhydrase II Studied with a Site-Specific Mutant Biochemistry 1989, 28, 7913-7918
17. Vila, J. A.; Arnautova, Y. A.; Vorobjev, Y.; Scheraga, H. A. Assessing the Fractions of Tautomeric Forms of the Imidazole Ring of Histidine in Proteins as a Function of pH Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 5602-5607
18. Hass, M. A. S.; Hansen, D. F.; Christensen, H. E. M.; Led, J. J.; Kay, L. E. Characterization of Conformational Exchange of a Histidine Side Chain: Protonation, Rotamerization, and Tautomerization of His61 in Plastocyanin from Anabaena Variabilis J. Am. Chem. Soc. 2008, 130, 8460-8470
19. Shimba, N.; Takahashi, H.; Sakakura, M.; Fujii, I.; Shimada, I. Determination of Protonation and Deprotonation Forms and Tautomeric States of Histidine Residues in Large Proteins using Nitrogen-Carbon J Couplings in Imidazole Ring J. Am. Chem. Soc. 1998, 120, 10988-10989
20. Hass, M. A. S.; Yilmaz, A.; Christensen, H. E. M.; Led, J. J. Histidine Side-Chain Dynamics and Protonation Monitored by C-13 CPMG NMR Relaxation Dispersion J. Biomol. NMR 2009, 44, 225-233
21. Harbison, G.; Herzfeld, J.; Griffin, R. G. N-15 Chemical-Shift Tensors in L-Histidine Hydrochlorid Monohydrate J. Am. Chem. Soc. 1981, 103, 4752-4754
22. Pelton, J. G.; Torchia, D. A.; Meadow, N. D.; Roseman, S. Tautomeric States of the Active-Site Histidines of Phosphorylated and Unphosphorylated III(GLC), a Signal-Transducing Protein from Escherichia-Coli, using Two-Dimentional Heteronuclear NMR Techniques Protein Sci. 1993, 2, 543-558
23. Cheng, F.; Sun, H.; Zhang, Y.; Mukkamala, D.; Oldfield, E. A Solid State 13C NMR, Crystallographic, and Quantum Chemical Investigation of Chemical Shifts and Hydrogen Bonding in Histidine Dipeptides J. Am. Chem. Soc. 2005, 127, 12544-12554
24. Nydegger, M. W.; Dutta, S.; Cheatum, C. M. Two-Dimensional Infrared Study of 3-Azidopyridine as a Potential Spectroscopic Reporter of Protonation State J. Chem. Phys. 2010, 133, 134506
25. Roberts, S. T.; Loparo, J. J.; Tokmakoff, A. Characterization of Spectral Diffusion from Two-Dimensional Line Shapes J. Chem. Phys. 2006, 125, 084502
26. Ghosh, A.; Hochstrasser, R. M. A Peptide's Perspective of Water Dynamics Chem. Phys. 2011, 390, 1-13
27. Remorino, A.; Korendovych, I. V.; Wu, Y. B.; DeGrado, W. F.; Hochstrasser, R. M. Residue-Specific Vibrational Echoes Yield 3D Structures of a Transmembrane Helix Dimer Science 2011, 332, 1206-1209
28. Peng, C. S.; Tokmakoff, A. Identification of Lactam-Lactim Tautomers of Aromatic Heterocycles in Aqueous Solution Using 2D IR Spectroscopy J. Phys. Chem. Lett. 2012, 3, 3302-3306
29. Barth, A.; Zscherp, C. What Vibrations Tell Us About Proteins Q. Rev. Biophys. 2002, 35, 369-430
30. Tucker, M. J.; Gai, X. S.; Fenlon, E. E.; Brewer, S. H.; Hochstrasser, R. M. 2D IR Photon Echo of Azido-Probes for Biomolecular Dynamics Phys. Chem. Chem. Phys. 2011, 13, 2237-2241
31. Tucker, M. J.; Getahun, Z.; Nanda, V.; DeGrado, W. F.; Gai, F. A New Method for Determining the Local Environment and Orientation of Individual Side Chains of Membrane-Binding Peptides J. Am. Chem. Soc. 2004, 126, 5078-5079
32. Hoffman, K. W.; Romei, M. G.; Londergan, C. H. A New Raman Spectroscopic Probe of Both the Protonation State and Noncovalent Interactions of Histidine Residues J. Phys. Chem. A 2013, 117, 5987-5996
33. Romei, M. G.; Hoffman, K. W.; Londergan, C. H. 2-Deuterated Histidine is a Raman Reporter of Histidine's Protonation State, Hydrogen Bonding, and Metal Coordination Biophys. J. 2013, 104, 685a-685a
34. Kim, Y. S.; Hochstrasser, R. M. Applications of 2D IR Spectroscopy to Peptides, Proteins, and Hydrogen-Bond Dynamics J. Phys. Chem. B 2009, 113, 8231-8251
35. Ganim, Z.; Chung, H. S.; Smith, A. W.; Deflores, L. P.; Jones, K. C.; Tokmakoff, A. Amide I Two-Dimensional Infrared Spectroscopy of Proteins Acc. Chem. Res. 2008, 41, 432-441
36. Zheng, J.; Kwak, K.; Fayer, M. D. Ultrafast 2D IR Vibrational Echo Spectroscopy Acc. Chem. Res. 2007, 40, 75-83
37. Bagchi, S.; Charnley, A. K.; Smith, A. B.; Hochstrasser, R. M. Equilibrium Exchange Processes of the Aqueous Tryptophan Dipeptide J. Phys. Chem. B 2009, 113, 8412-8417
38. Ghosh, A.; Qiu, J.; DeGrado, W. F.; Hochstrasser, R. M. Tidal Surge in the M2 Proton Channel, Sensed by 2D IR Spectroscopy Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 6115-6120
39. Fang, C.; Bauman, J. D.; Das, K.; Remorino, A.; Arnold, E.; Hochstrasser, R. M. Two-Dimensional Infrared Spectra Reveal Relaxation of the Nonnucleoside Inhibitor TMC278 Complexed with HIV-1 Reverse Transcriptase Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 1472-1477
40. Wang, L.; Middleton, C. T.; Singh, S.; Reddy, A. S.; Woys, A. M.; Strasfeld, D. B.; Marek, P.; Raleigh, D. P.; de Pablo, J. J.; Zanni, M. T.; Skinner, J. L. 2DIR Spectroscopy of Human Amylin Fibrils Reflects Stable Beta-Sheet Structure J. Am. Chem. Soc. 2011, 133, 16062-16071
41. Middleton, C. T.; Marek, P.; Cao, P.; Chiu, C. C.; Singh, S.; Woys, A. M.; de Pablo, J. J.; Raleigh, D. P.; Zanni, M. T. Two-Dimensional Infrared Spectroscopy Reveals the Complex Behaviour of an Amyloid Fibril Inhibitor Nat. Chem. 2012, 4, 355-360
42. Kim, Y. S.; Liu, L.; Axelsen, P. H.; Hochstrasser, R. M. 2D IR Provides Evidence for Mobile Water Molecules in Beta-Amyloid Fibrils Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 17751-17756
43. 18O-Labeled Fmoc-Amino Acids with High Levels of Enrichment: Applications to Isotope-Edited IR Studies of Proteins Org. Lett. 2007, 9, 4935-4937
44. Reppert, M.; Tokmakoff, A. Electrostatic Frequency Shifts in Amide I Vibrational Spectra: Direct Parameterization Against Experiment J. Chem. Phys. 2013, 138, 134116
45. Kim, Y. S.; Hochstrasser, R. M. Dynamics of Amide-I Modes of the Alanine Dipeptide in D2O J. Phys. Chem. B 2005, 109, 6884-6891
46. Falvo, C.; Zhuang, W.; Kim, Y. S.; Axelsen, P. H.; Hochstrasser, R. M.; Mukamel, S. Frequency Distribution of the Amide-I Vibration Sorted by Residues in Amyloid Fibrils Revealed by 2D-IR Measurements and Simulations J. Phys. Chem. B 2012, 116, 3322-3330
47. Zheng, J. R.; Kwak, K.; Asbury, J.; Chen, X.; Piletic, I. R.; Fayer, M. D. Ultrafast Dynamics of Solute-Solvent Complexation Observed at Thermal Equilibrium in Real Time Science 2005, 309, 1338-1343
48. Kwak, K.; Zheng, J. R.; Cang, H.; Fayer, M. D. Ultrafast Two-Dimensional Infrared Vibrational Echo Chemical Exchange Experiments and Theory J. Phys. Chem. B 2006, 110, 19998-20013
49. Kim, Y. S.; Hochstrasser, R. M. Chemical Exchange 2D IR of Hydrogen-Bond Making and Breaking Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 11185-11190
50. Woutersen, S.; Mu, Y.; Stock, G.; Hamm, P. Hydrogen-Bond Lifetime Measured by Time-Resolved 2D-IR Spectroscopy: N-Methylacetamide in Methanol Chem. Phys. 2001, 266, 137-147
51. Pazos, I. M.; Gai, F. Solute's Perspective on How Trimethylamine Oxide, Urea, and Guanidine Hydrochloride Affect Water's Hydrogen Bonding Ability J. Phys. Chem. B 2012, 116, 12473-12478