A vibrational spectral maker for probing the hydrogen-bonding status of protonated Asp and Glu residues

Biophysical Journal

Volumn 88, Issue 4, 2005, Pages 2833-2847

  Nie, Beining ^a   Stutzman, Jerrod ^a   Xie, Aihua ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; CARBOXYL GROUP; FUNCTIONAL GROUP; GLUTAMIC ACID; PROTON;

AB INITIO CALCULATION; ARTICLE; CHEMICAL BOND; DENSITY FUNCTIONAL THEORY; DOUBLE BOND; HYDROGEN BOND; HYDROGEN BOND NUMBER; HYDROGEN BOND STRENGTH; INFRARED SPECTROSCOPY; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE; SPECTROSCOPY; STRETCHING; STRETCHING FREQUENCY; STRUCTURE ANALYSIS; TWO DIMENSIONAL INFRARED SPECTROSCOPTY; VACUUM; VIBRATION; VIBRATIONAL SPECTRAL MARKER;

EID: 22144464025     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.047639     Document Type: Article

References (74)

1. Acharya, S., and S. S. Karnik. 1996. Modulation of GDP release from transducin by the conserved Glu134-Arg135 sequence in rhodopsin. J. Biol. Chem. 271:25406-25411.
2. Arnis, S., K. Fahmy, K. P. Hofmann, and T. P. Sakmar. 1994. A conserved carboxylic acid group mediates light-dependent proton uptake and signaling by rhodopsin. J. Biol. Chem. 269:23879-23881.
3. Barber-Armstrong, W., T. Donaldson, H. Wijesooriya, R. A. Silva, and S. M. Decatur. 2004. Empirical relationships between isotope-edited IR spectra and helix geometry in model peptides. J. Am. Chem. Soc. 126:2339-2345.
4. Barth, A. 2000. The infrared absorption of amino acid side chains. Prog. Biophys. Mol. Bio. 74:141-173.
5. Bergo, V., E. N. Spudich, J. Spudich, and K. J. Rothschild. 2003. Conformational changes detected in a sensory rhodopsin II-transducer complex. J. Biol. Chem. 278:36556-36562.
6. Borgstahl, G. E., D. R. Williams, and E. D. Getzoff. 1995. 1.4 A structure of photoactive yellow protein, a cytosolic photoreceptor: unusual fold, active site, and chromophore. Biochemistry. 34:6278-6287.
7. Bousche, O., S. Sonar, M. P. Krebs, H. G. Khorana, and K. J. Rothschild. 1992. Time-resolved Fourier transform infrared spectroscopy of the bacteriorhodopsin mutant Tyr-185 → Phe: Asp-96 reprotonates during O formation; Asp-85 and Asp-212 deprotonate during O decay. Photochem. Photobiol. 56:1085-1095.
8. Braiman, M. S., T. Mogi, T. Marti, L. J. Stern, H. G. Khorana, and K. J. Rothschild. 1988. Vibrational spectroscopy of bacteriorhodopsin mutants: light-driven proton transport involves protonation charges of aspartic acid residues 85, 96, and 212. Biochemistry. 27:8516-8520.
9. Breton, J., E. Nabedryk, J. P. Allen, and J. C. Williams. 1997. Electrostatic influence of QA reduction on the IR vibrational mode of the 10a-ester C==O of HA demonstrated by mutations at residues Glu L104 and Trp L100 in reaction centers from Rhodobacter sphaeroides. Biochemistry. 36:4515-4525.
10. Brown, L. S., A. K. Dioumaev, R. Needleman, and J. K. Lanyi. 1998. Local-access model for proton transfer in bacteriorhodopsin. Biochemistry. 37:3982-3993.
11. Brown, L. S., J. Sasaki, H. Kandori, A. Maeda, R. Needleman, and J. K. Lanyi. 1995. Glutamic acid 204 is the terminal proton release group at the extracellular surface of bacteriorhodopsin. J. Biol. Chem. 270:27122-27126.
12. Brudler, R., R. Rammelsberg, T. T. Woo, E. D. Getzoff, and K. Gerwert. 2001. Structure of the II early intermediate of photoactive yellow protein by FTIR spectroscopy. Nat. Struct. Biol. 8:265-270.
13. Camara-Artigas, A., D. Brune, and J. P. Allen. 2002. Interactions between lipids and bacterial reaction centers determined by protein crystallography. Proc. Natl. Acad. Sci. USA. 99:11055-11060.
14. Cammi, R., C. Cappelli, S. Corni, and J. Tomasi. 2000. On the calculation of infrared intensities in solution within the polarizable continuum model. J. Phys. Chem. 104:9874-9879.
15. Cappelli, C., S. Corni, R. Cammi, B. Mennucci, and J. Tomasi. 2000. Nonequilibrium formulation of infrared frequencies and intensities in solution: analytical evaluation within the polarizable continuum model. J. Chem. Phys. 113:11270-11279.
16. Creighton, T. E. 1997. Protein Structures and Molecular Properties. W. H. Freeman and Company, New York.
17. DeLange, F., P. H. M. Bovee-Geurts, A. M. A. Pistorius, K. J. Rothschild, and W. J. DeGrip. 1999. Probing intramolecular orientations in rhodopsin and metarhodopsin II by polarized infrared difference spectroscopy. Biochemistry. 38:13200-13209.
18. Dioumaev, A. K. 2001. Infrared methods for monitoring the protonation state of carboxylic amino acids in the photocycle of bacteriorhodopsin. Biochemistry (Mosc.). 66:1269-1276.
19. Dioumaev, A. K., and M. S. Braiman. 1995. Modeling vibrational spectra of amino acid side chains in proteins: the carbonyl stretch frequency of buried carboxylic residues. J. Am. Chem. Soc. 117:10572-10574.
20. Dwyer, J., A. G. Gittis, D. Karp, E. Lattman, D. S. Spencer, W. Stites, and B. Garcia-Moreno. 2000. High apparent dielectric constants in the interior of a protein reflect water penetration. Biophys. J. 79:1610-1620.
21. Engelhard, M., K. Gerwert, B. Hess, W. Kreutz, and F. Siebert. 1985. Light-driven protonation changes of internal aspartic acids of bacteriorhodopsin: an investigation by static and time-resolved infrared difference spectroscopy using [4-13C] aspartic acid labeled purple membrane. Biochemistry. 24:400-407.
22. Fahmy, K., F. Jager, M. Beck, T. A. Zvyaga, T. P. Sakmar, and F. Siebert. 1993. Protonation states of membrane-embedded carboxylic acid groups in rhodopsin and metarhodopsin II: a Fourier-transform infrared spectroscopy study of site-directed mutants. Proc. Natl. Acad. Sci. USA. 90:10206-10210.
23. Fahmy, K., T. P. Sakmar, and F. Siebert. 2000. Transducin-dependent protonation of glutamic acid 134 in rhodopsin. Biochemistry. 39:10607-10612.
24. Foresman, I. B., and Æ. Frisch. 1996. Exploring Chemistry with Electronic Structure Methods. Gaussian, Pittsburgh, PA.
25. Friedrich, T., S. Geibel, R. Kalmbach, I. Chizhov, K. Ataka, I. Heberle, M. Engelhard, and E. Bamberg. 2002. Proteorhodopsin is a light-driven proton pump with variable vectoriality. J. Mol. Biol. 321:821-838.
26. Frisch, M. I., G. W. Trucks, H. B. Schlegel, G. E. Scuseria, M. A. Robb, I. R. Cheeseman, I. A. Montgomery, I. Vreven, K. N. Kudin, I. C. Burant, J. M. Milliam, S. S. Iyengar, et al. 2003. Gaussian03, Revision A.1. Gaussian, Pittsburgh, PA.
27. Garcia-Moreno, B. E., J. J. Dwyer, A. G. Gittis, E. E. Lattman, D. S. Spencer, and W. E. Stites. 1997. Experimental measurement of the effective dielectric in the hydrophobic core of a protein. Biophys. Chem. 64:211-224.
28. Gerwert, K. 1999. Molecular reaction mechanisms of proteins monitored by time-resolved FTTR-spectroscopy. Biol. Chem. 380:931-935.
29. Getzoff, E. D., K. N. Gutwin, and U. K. Genick. 2003. Anticipatory activesite motions and chromophore distortion prime photoreceptor PYP for light activation. Nat. Struct. Biol. 10:663-668.
30. Griffiths, D. I. 1999. Introduction to Electrodynamics. Prentice-Hall, Saddle River, NI.
31. Heberle, I. 2000. Proton transfer reactions across bacteriorhodopsin and along the membrane. Biochim. Biophys. Acta. 1458:135-147.
32. Hering, I. A., P. R. Innocent, and P. I. Haris. 2002. Automatic amide I frequency selection for rapid quantification of protein secondary structure from Fourier transform infrared spectra of proteins. Proteomics. 2:839-849.
33. Hibbert, F., and I. Emsley. 1990. Hydrogen bonding and chemical reactivity. Adv. Phys. Org. Chem. 26:255-379.
34. Honig, B., and A. S. Yang. 1995. Free energy balance in protein folding. Adv. Protein Chem. 46:27-58.
35. Hoppe, W., W. Lohmann, H. Markl, and H. Ziegler. 1983. Biophysics. Springer-Verlag, New York.
36. Hutson, M. S., S. V. Shilov, R. Krebs, and M. S. Braiman. 2001. Halide dependence of the halorhodopsin photocycle as measured by time-resolved infrared spectra. Biophys. J. 80:1452-1465.
37. Imamoto, Y., K. Mihara, O. Hisatomi, M. Kataoka, F. Tokunaga, N. Bojkova, and K. Yoshihara. 1997. Evidence for proton transfer from Glu-46 to the chromophore during the photocycle of photoactive yellow protein. J. Biol. Chem. 272:12905-12908.
38. Jager, F., K. Fahmy, T. P. Sakmar, and F. Siebert. 1994. Identification of glutamic acid 113 as the Schiff base proton acceptor in the metarhodopsin II photointermediate of rhodopsin. Biochemistry. 33:10878-10882.
39. Kolbe, M., H. Besir, L. O. Essen, and D. Oesterhelt. 2000. Structure of the light-driven chloride pump halorhodopsin at 1.8 A resolution. Science. 288:1390-1396.
40. Koutsoupakis, C., T. Soulimane, and C. Varotsis. 2004. Probing the Q-proton pathway of ba3-cytochrome c oxidase by time-resolved Fourier transform infrared spectroscopy. Biophys. J. 86:2438-2444.
41. Krebs, M. P., and H. G. Khorana. 1993. Mechanism of light-dependent proton translocation by bacteriorhodopsin. J. Bacteriol. 175:1555-1560.
42. Lanyi, J. K., and B. Schobert. 2002. Crystallographic structure of the retinal and the protein after deprotonation of the Schiff base: the switch in the bacteriorhodopsin photocycle. J. Mol. Biol. 321:727-737.
43. C=O de quelques acides monocarboxyliques: etude par spectroscopie infrarouge. [in French]. J. Chim. Phys. 59:1233-1246.
44. Lide, D. R. 1997. CRC Handbook of Chemistry and Physics. CRC Press, New York.
45. Lubben, M., A. Prutsch, B. Mamat, and K. Gerwert. 1999. Electron transfer induces side-chain conformational changes of glutamate-286 from cytochrome bo3. Biochemistry. 38:2048-2056.
46. Maeda, A. 2001. Internal water molecules as mobile polar groups for light-induced proton translocation in bacteriorhodopsin and rhodopsin as studied by difference FTIR spectroscopy. Biochemistry (Mosc.). 66:1256-1268.
47. Maeda, A., J. Sasaki, Y. Shichida, T. Yoshizawa, M. Chang, B. Ni, R. Needleman, and J. K. Lanyi. 1992. Structures of aspartic acid-96 in the L and N intermediates of bacteriorhodopsin: analysis by Fourier transform infrared spectroscopy. Biochemistry. 31:4684-4690.
48. Maeda, A., F. L. Tomson, R. B. Gennis, S. P. Baiashov, and T. G. Ebrey. 2003. Water molecule rearrangements around Leu93 and Trp182 in the formation of the L intermediate in bacteriorhodopsin's photocycle. Biochemistry. 42:2535-2541.
49. Marti, T., H. Otto, S. J. Rosselet, M. P. Heyn, and H. G. Khorana. 1992. Anion binding to the Schiff base of the bacteriorhodopsin mutants Asp-85-Asn/Asp-212-Asn and Arg-82-Gln/Asp-85-Asn/Asp-212-Asn. J. Biol. Chem. 267:16922-16927.
50. Meyer, T. E., S. Devanathan, T. T. Woo, E. D. Getzoff, G. Tollin, and M. A. Cusanovich. 2003. Site-specific mutations provide new insights into the origin of pH effects and alternative spectral forms in the photo-active yellow protein from Halorhodospira halophilia. Biochemistry. 42:3319-3325.
51. Nabedryk, E., J. Breton, H. M. Joshi, and D. K. Hanson. 2000. Fourier transform infrared evidence of proton uptake by glutamate L212 upon reduction of the secondary quinone QB in the photosynthetic reaction center from Rhodobacter capsulatus. Biochemistry. 39:14654-14663.
52. Nabedryk, E., J. Breton, M. Y. Okamura, and M. L. Paddock. 2001. Simultaneous replacement of Asp-L210 and Asp-M17 with Asn increases proton uptake by Glu-L212 upon first electron transfer to QB in reaction centers from Rhodobacter sphaeroides. Biochemistry. 40:13826-13832.
53. Nie, B. 2002. Vibrational band assignment and electrostatic properties of biomolecules based on ab initio computational studies. Master thesis. Oklahoma State University, Stillwater, OK
54. Okada, T., Y. Fujiyoshi, M. Silow, J. Navarro, E. M. Landau, and Y. Shichida. 2002. Functional role of internal water molecules in rhodopsin revealed by X-ray crystallography. Proc. Natl. Acad. Sci. USA. 99:5982-5987.
55. Otto, H., T. Marti, M. Holz, T. Mogi, L. J. Stem, F. Engel, H. G. Khorana, and M. P. Heyn. 1990. Substitution of amino acids Asp-85, Asp-212, and Arg-82 in bacteriorhodopsin affects the proton release phase of the pump and the pK of the Schiff base. Proc. Natl. Acad. Sci. USA. 87:1018-1022.
56. Pebay-Peyroula, E., G. Rummel, J. P. Rosenbusch, and E. M. Landau. 1997. X-ray structure of bacteriorhodopsin at 2.5 angstroms from microcrystals grown in lipidic cubic phases. Science. 277:1676-1681.
57. Perrin, C. L., and J. B. Nielson. 1997. "Strong" hydrogen bonds in chemistry and biology. Annu. Rev. Phys. Chem. 48:511-544.
58. Puustinen, A., J. A. Bailey, R. B. Dyer, S. L. Mecklenburg, M. Wikstrom, and W. H. Woodruff. 1997. Fourier transform infrared evidence for connectivity between CuB and glutamic acid 286 in cytochrome bo3 from Escherichia coli. Biochemistry. 36:13195-13200.
59. Riistama, S., G. Hummer, A. Puustinen, R. B. Dyer, W. H. Woodruff, and M. Wikstrom. 1997. Bound water in the proton translocation mechanism of the haem-copper oxidases. FEBS Lett. 414:275-280.
60. Rothschild, K. J. 1992. FTIR difference spectroscopy of bacteriorhodopsin: toward a molecular model. J. Bioenerg. Biomembr. 24:147-167.
61. Sasaki, J., J. K. Lanyi, R. Needleman, T. Yoshizawa, and A. Maeda. 1994. Complete identification of C=O stretching vibrational bands of protonated aspartic acid residues in the difference infrared spectra of M and N intermediates versus bacteriorhodopsin. Biochemistry. 33:3178-3184.
62. Schmidt, B., W. Hillier, J. McCracken, and S. Ferguson-Miller. 2004. The use of stable isotopes and spectroscopy to investigate the energy transducing function of cytochrome c oxidase. Biochim. Biophys. Acta. 1655:248-255.
63. Song, Y., J. Mao, and M. R. Gunner. 2003. Calculation of proton transfers in bacteriorhodopsin bR and M intermediates. Biochemistry. 42:9875-9888.
64. Soulimane, T., G. Buse, G. P. Bourenkov, H. D. Bartunik, R. Huber, and M. E. Than. 2000. Structure and mechanism of the aberrant ba(3)-cytochrome c oxidase from Thermus thermophilus. EMBO J. 19:1766-1776.
65. Steiner, T. 2002. The hydrogen bond in the solid state. Angew. Chem. Int. Ed. Engl. 41:49-76.
66. Subramaniam, S., D. A. Greenhalgh, and H. G. Khorana. 1992. Aspartic acid 85 in bacteriorhodopsin functions both as proton acceptor and negative counterion to the Schiff base. J. Biol. Chem. 267:25730-25733.
67. Subramaniam, S., and R. Henderson. 2000. Molecular mechanism of vectorial proton translocation by bacteriorhodopsin. Nature. 406:653-657.
68. Susi, H., S. N. Timasheff, and L. Stevens. 1967. Infrared spectra and protein conformations in aqueous solutions. I. The amide I band in H2O and D20 solutions. J. Biol. Chem. 242:5460-5466.
69. Svensson-Ek, M., J. Abramson, G. Larsson, S. Tornroth, P. Brezezinski, and S. Iwata. 2002. The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides. J. Mol. Biol. 321:329-339.
70. Szaraz, S., D. Oesterhelt, and P. Ormos. 1994. pH-induced structural changes in bacteriorhodopsin studied by Fourier transform infrared spectroscopy. Biophys. J. 67:1706-1712.
71. Tsukihara, T., K. Shimokata, Y. Katayama, H. Shimada, K. Muramoto, H. Aoyama, M. Mochizuki, K. Shinzawa-Itoh, E. Yamashita, M. Yao, Y. Ishimura, and S. Yoshikawa. 2003. The low-spin heme of cytochrome c oxidase as the driving element of the proton-pumping process. Proc. Natl. Acad. Sci. USA. 100:15304-15309.
72. Xie, A., W. D. Hoff, A. R. Kroon, and K. J. Hellingwerf. 1996. Glu46 donates a proton to the 4-hydroxycinnamate anion chromophore during the photocycle of photoactive yellow protein. Biochemistry. 35:14671-14678.
73. Xie, A., L. Kelemen, J. Hendriks, B. J. White, K. J. Hellingwerf, and W. D. Hoff. 2001. Formation of a new buried charge drives a large-amplitude protein quake in photoreceptor activation. Biochemistry. 40:1510-1517.
74. Zscherp, C., R. Schlesinger, J. Tittor, D. Oesterhelt, and J. Heberle. 1999. In situ determination of transient pK changes of internal amino acids of bacteriorhodopsin by using time-resolved attenuated total reflection Fourier-transform infrared spectroscopy. Proc. Natl. Acad. Sci. USA. 96:5498-5503.