A new Raman spectroscopic probe of both the protonation state and noncovalent interactions of histidine residues

Journal of Physical Chemistry A

Volumn 117, Issue 29, 2013, Pages 5987-5996

  Hoffman, Kevin W ^a   Romei, Matthew G ^a   Londergan, Casey H ^a  

^a HAVERFORD COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COORDINATION ENVIRONMENT; ENVIRONMENTAL CHANGE; H-BONDING INTERACTION; HIGH-TIME RESOLUTION; NON-COVALENT INTERACTION; RAMAN SPECTROSCOPIC; STRETCHING VIBRATIONS; TRANSMISSION EXPERIMENTS;

AMINO ACIDS; ATOMS; DEUTERIUM; HYDROGEN BONDS; IONS; PH; PROBES; PROTONATION; RAMAN SPECTROSCOPY; STRETCHING;

PROTEINS;

EID: 84880843124     PISSN: 10895639     EISSN: 15205215     Source Type: Journal    
DOI: 10.1021/jp311815k     Document Type: Article

References (59)

1. Carnevale, V.; Fiorin, G.; Levine, B. G.; DeGrado, W. F.; Klein, M. L. Multiple Proton Confinement in the M2 Channel from the Influenza A Virus J. Phys. Chem. C 2010, 114, 20856-20863
2. Day, R. M.; Thalhauser, C. J.; Sudmeier, J. L.; Vincent, M. P.; Torchilin, E. V.; Sanford, D. G.; Bachovchin, C. W.; Bachovchin, W. W. Tautomerism, Acid-Base Equilibria, and H-Bonding of the Six Histidines in Subtilisin BPN ' by NMR Protein Sci. 2003, 12, 794-810
3. Grey, M. J.; Tang, Y. F.; Alexov, E.; McKnight, C. J.; Raleigh, D. P.; Palmer, A. G. Characterizing a Partially Folded Intermediate of the Villin Headpiece Domain under Non-denaturing Conditions: Contribution of His41 to the pH-dependent Stability of the N-Terminal Subdomain J. Mol. Biol. 2006, 355, 1078-1094
4. Hass, M. A. S.; Thuesen, M. H.; Christensen, H. E. M.; Led, J. J. Characterization of μs-ms Dynamics of Proteins Using a Combined Analysis of N-15 NMR Relaxation and Chemical Shift: Conformational Exchange in Plastocyanin Induced by Histidine Protonations J. Am. Chem. Soc. 2004, 126, 753-765
5. Okada, A.; Miura, T.; Takeuchi, H. Protonation of Histidine and Histidine-Tryptophan Interaction in the Activation of the M2 Ion Channel from Influenza A Virus Biochemistry 2001, 40, 6053-6060
6. 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
7. Wang, J.; Qiu, J. X. Y.; Soto, C.; DeGrado, W. F. Structural and Dynamic Mechanisms for the Function and Inhibition of the M2 Proton Channel from Influenza A Virus Curr. Opin. Struct. Biol. 2011, 21, 68-80
8. Hasegawa, K.; Ono, T.; Noguchi, T. Vibrational Spectra and ab initio DFT Calculations of 4-Methylimidazole and its Different Protonation Forms: Infrared and Raman Markers of the Protonation State of a Histidine Side Chain J. Phys. Chem. B 2000, 104, 4253-4265
9. 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
10. 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
11. Markley, J. L. Observation of Histidine Residues in Proteins by Means of Nuclear Magnetic Resonance Spectroscopy Acc. Chem. Res. 1975, 8, 70-80
12. Arata, Y.; Shimizu, A.; Matsuo, H. Deuterium-Labeling Method for Assignment of Histidine Nuclear Magnetic Resonance Peaks of Proteins J. Am. Chem. Soc. 1978, 100, 3230-3232
13. Bradbury, J. H.; Chapman, B. E.; Crompton, M. W.; Norton, R. S.; Teh, J. S. Hydrogen-Deuterium Exchange of the C-2 Protons of Histidine and Histidine Peptides and Proteins J. Chem. Soc., Perkin Trans. 2 1980, 693-699
14. Bradbury, J. H.; Chapman, B. E.; Pellegri, Fa Hydrogen-Deuterium Exchange Kinetics of C-2 Protons of Imidazole and Histidine Compounds J. Am. Chem. Soc. 1973, 95, 6139-6140
15. Matsuo, H.; Ohe, M.; Narita, K.; Sakiyama, F. New Approach to Determination of pKas of Histidine Residues in Proteins J. Biochem. 1972, 72, 1057
16. Takesada, H.; Nakanishi, M.; Tsuboi, M.; Ajisaka, K. Hydrogen-Deuterium Exchange in Histidine Residues of Bovine α-Lactalbumin J. Biochem. 1976, 80, 969-974
17. Li, S. H.; 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
18. Lindquist, B. A.; Furse, K. E.; Corcelli, S. A. Nitrile Groups as Vibrational Probes of Biomolecular Structure and Dynamics: an Overview Phys. Chem. Chem. Phys. 2009, 11, 8119-8132
19. Waegele, M. M.; Culik, R. M.; Gai, F. Site-Specific Spectroscopic Reporters of the Local Electric Field, Hydration, Structure, and Dynamics of Biomolecules J. Phys. Chem. Lett. 2011, 2, 2598-2609
20. Hamm, P.; Zanni, M. T.: Concepts and Methods of 2D Infrared Spectroscopy; Cambridge University Press: Cambridge, 2011.
21. Chin, J. K.; Jimenez, R.; Romesberg, F. E. Direct Observation of Protein Vibrations by Selective Incorporation of Spectroscopically Observable Carbon-Deuterium Bonds in Cytochrome C J. Am. Chem. Soc. 2001, 123, 2426-2427
22. Cremeens, M.; Fujisaki, H.; Zhang, Y.; Zimmermann, J.; Sagle, L.; Matsuda, S.; Dawson, P.; Straub, J.; Romesberg, F. Efforts toward Developing Direct Probes of Protein Dynamics J. Am. Chem. Soc. 2006, 6028-6029
23. Cremeens, M. E.; Zimmermann, J.; Yu, W.; Dawson, P. E.; Romesberg, F. E. Direct Observation of Structural Heterogeneity in a beta-Sheet J. Am. Chem. Soc. 2009, 131, 5726
24. Groff, D.; Thielges, M. C.; Cellitti, S.; Schultz, P. G.; Romesberg, F. E. Efforts Toward the Direct Experimental Characterization of Enzyme Microenvironments: Tyrosine100 in Dihydrofolate Reductase Angew. Chem., Int. Ed. 2009, 48, 3478-3481
25. Kinnaman, C. S.; Cremeens, M. E.; Romesberg, F. E.; Corcelli, S. A. Infrared Line Shape of an Alpha-carbon Deuterium-labeled Amino Acid J. Am. Chem. Soc. 2006, 128, 13334-13335
26. Naraharisetty, S. R. G.; Kasyanenko, V. M.; Zimmermann, J.; Thielges, M. C.; Romesberg, F. E.; Rubtsov, I. V. C-D Modes of Deuterated Side Chain of Leucine as Structural Reporters via Dual-frequency Two-dimensional Infrared Spectroscopy J. Phys. Chem. B 2009, 113, 4940-4946
27. Nydegger, M. W. N. M. W.; Rock, W.; Cheatum, C. M. 2D IR Spectroscopy of the C-D Stretching Vibration of the Deuterated Formic Acid Dimer Phys. Chem. Chem. Phys. 2011, 13, 6098-6104
28. Sagle, L.; Zimmerman, J.; Baldridge, K.; Dawson, P.; Romesberg, F. Carbon-deuterium Bonds as an IR Probe in Cytochrome C Protein Sci. 2004, 216-216
29. Sagle, L. B.; Zimmermann, J.; Dawson, P. E.; Romesberg, F. E. A High-resolution Probe of Protein Folding J. Am. Chem. Soc. 2004, 126, 3384-3385
30. Sagle, L. B.; Zimmermann, J.; Dawson, P. E.; Romesberg, F. E. Direct and High Resolution Characterization of Cytochrome C Equilibrium Folding J. Am. Chem. Soc. 2006, 128, 14232-14233
31. Thielges, M. C.; Case, D. A.; Romesberg, F. E. Carbon-deuterium Bonds as Probes of Dihydrofolate Reductase J. Am. Chem. Soc. 2008, 130, 6597-6603
32. Weinkam, P.; Zimmermann, J.; Sagle, L. B.; Matsuda, S.; Dawson, P. E.; Wolynes, P. G.; Romesberg, F. E. Characterization of Alkaline Transitions in Ferricytochrome c Using Carbon-Deuterium Infrared Probes Biochemistry 2008, 47, 13470-13480
33. Zimmermann, J.; Gundogdu, K.; Cremeens, M. E.; Bandaria, J. N.; Hwang, G. T.; Thielges, M. C.; Cheatum, C. M.; Romesberg, F. E. Efforts toward Developing Probes of Protein Dynamics: Vibrational Dephasing and Relaxation of Carbon-Deuterium Stretching Modes in Deuterated Leucine J. Phys. Chem. B 2009, 113, 7991-7994
34. Zimmermann, J.; Thielges, M. C.; Yu, W.; Dawson, P. E.; Romesberg, F. E. Carbon-Deuterium Bonds as Site-Specific and Nonperturbative Probes for Time-Resolved Studies of Protein Dynamics and Folding J. Phys. Chem. Lett. 2011, 2, 412-416
35. Miller, C. S.; Corcelli, S. A. Carbon-Deuterium Vibrational Probes of Amino Acid Protonation State J. Phys. Chem. B 2009, 113, 8218-8221
36. Miller, C. S.; Corcelli, S. A. Carbon-Deuterium Vibrational Probes of the Protonation State of Histidine in the Gas-Phase and in Aqueous Solution J. Phys. Chem. B 2010, 114, 8565-8573
37. Mesu, J. G.; Visser, T.; Soulimani, F.; Weckhuysen, B. M. Infrared and Raman Spectroscopic Study of pH-induced Structural Changes of L-Histidine in Aqueous Environment Vib. Spectrosc. 2005, 39, 114-125
38. Miura, T.; Satoh, T.; Hori-i, A.; Takeuchi, H. Raman Marker Bands of Metal Coordination Sites of Histidine Side Chains in Peptides and Proteins J. Raman Spectrosc. 1998, 29, 41-47
39. Pfluger, F.; Hernandez, B.; Ghomi, M. Vibrational Analysis of Amino Acids and Short Peptides in Hydrated Media. VII. Energy Landscapes, Energetic and Geometrical Features of L-Histidine with Protonated and Neutral Side Chains J. Phys. Chem. B 2010, 114, 9072-9083
40. Takeuchi, H. Raman Structural Markers of Tryptophan and Histidine Side Chains in Proteins Biopolymers 2003, 72, 305-317
41. Takeuchi, H.; Kimura, Y.; Koitabashi, I.; Harada, I. Raman Bands of N-deuterated Histidinium as Markers of Conformation and Hydrogen Bonding J. Raman Spectrosc. 1991, 22, 233-236
42. Tasumi, M.; Harada, I.; Takamatsu, T.; Takahashi, S. Raman Studies of L-Histidine and Related Compounds in Aqueous Solutions J. Raman Spectrosc. 1982, 12, 149-151
43. Toyama, A.; Ono, K.; Hashimoto, S.; Takeuchi, H. Raman Spectra and Normal Coordinate Analysis of the N1-H and N3-H Tautomers of 4-Methylimidazole: Vibrational Modes of Histidine Tautomer Markers J. Phys. Chem. A 2002, 106, 3403-3412
44. Harada, I.; Takamatsu, T.; Tasumi, M.; Lord, R. C. Raman Spectroscopic Study of the Interactions Between Sulfate Anion and an Imidazolium Ring in Ribonuclease A Biochemistry 1982, 21, 3674-3677
45. IUPAC. Compendium of Chemical Terminology, 2 nd ed. (the "Gold Book"); Compiled by McNaught, A. D.; Wilkinson, A.; Blackwell Scientific Publications: Oxford, 1997; XML on-line corrected version: http://goldbook. iupac.org (2006-) created by M. Nic, J. Jirat, B. Kosata; updates compiled by A. Jenkins.
46. Miyagi, M.; Nakazawa, T. Determination of pKa Values of Individual Histidine Residues in Proteins Using Mass Spectrometry Anal. Chem. 2008, 80, 6481-6487
47. Fairman, R.; Shoemaker, K. R.; York, E. J.; Stewart, J. M.; Baldwin, R. L. Further Studies of the Helix Dipole Model- Effects of a Free α-NH3+ or α-COO- Group on Helix Stability Proteins 1989, 5, 1-7
48. Balakrishnan, G.; Jarzecki, A. A.; Wu, Q.; Kozlowski, P. M.; Wang, D. J.; Spiro, T. G. Mode Recognition in UV Resonance Raman Spectra of Imidazole: Histidine Monitoring in Proteins J. Phys. Chem. B 2012, 116, 9387-9395
49. Kamlet, M. J.; Abboud, J. L. M.; Abraham, M. H.; Taft, R. W. Linear Solvation Energy Relationships. 23. A Comprehesive Collection of the Solvatochromic Parameters π*, α and β, and Some Methods for Simplifying the Generalized Solvatochromic Equation J. Org. Chem. 1983, 48, 2877-2887
50. Taft, R. W.; Kamlet, M. J. Linear Solvation Energy Relationships. 4. Correlations with and Limitations of the α-scale of Solvent Hydrogen Bond Donor Acidities J. Chem. Soc., Perkin Trans. 2 1979, 1723-1729
51. Taft, R. W.; Pienta, N. J.; Kamlet, M. J.; Arnett, E. M. Linear Solvation Energy Relationships. 7. Correlations beween the Solvent-Donicity and Acceptor-Number Scales and the Solvatochromic Parameters π*, α and β J. Org. Chem. 1981, 46, 661-667
52. Yu, N. T. Resonance Raman Studies of Ligand Binding Meth. Enzymol. 1986, 130, 350-409
53. Mukherji, I.: Resonance raman spectroscopy. In Handbook of Proteins; John Wiley & Sons Ltd.: Chichester, UK, 2007; Vol. 2, pp 1167-1171.
54. Andrews, S.; Boxer, S. Vibrational Stark Effects of Nitriles II. Physical Origins of Stark Effects from Experiment and Perturbation Models J. Phys. Chem. A 2002, 469-477
55. Andrews, S. S.; Boxer, S. G. Vibrational Stark Effects of Nitriles I. Methods and Experimental Results J. Phys. Chem. A 2000, 104, 11853-11863
56. Fafarman, A. T.; Sigala, P. A.; Schwans, J. P.; Fenn, T. D.; Herschlag, D.; Boxer, S. G. Quantitative, Directional Measurement of Electric Field Heterogeneity in the Active Site of Ketosteroid Isomerase Proc. Natl. Acad. Sci. U.S.A. 2012, 109, E299-E308
57. Suydam, I. T.; Boxer, S. G. Vibrational Stark Effects Calibrate the Sensitivity of Vibrational Probes for Electric Fields in Proteins Biochemistry 2003, 42, 12050-12055
58. Wright, J. C. Multiresonant Coherent Multidimensional Spectroscopy Annu. Rev. Phys. Chem. 2011, 62, 209-230
59. Pakoulev, A. V.; Rickard, M. A.; Kornau, K. M.; Mathew, N. A.; Yurs, L. A.; Block, S. B.; Wright, J. C. Mixed Frequency-/Time-Domain Coherent Multidimensional Spectroscopy: Research Tool or Potential Analytical Method? Acc. Chem. Res. 2009, 42, 1310-1321