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Structure and ligand-binding modes of human serum albumin studied by UV resonance raman spectroscopy
Shinji Hashimoto,
Takahiko Yabusaki,
Hideo Takeuchi,
Issei Harada,
Shinji Hashimoto
Pharmaceutical Institute, Tohoku University, Aobayama, Sendai 980-77, Japan
Search for more papers by this authorTakahiko Yabusaki
Pharmaceutical Institute, Tohoku University, Aobayama, Sendai 980-77, Japan
Search for more papers by this authorCorresponding Author
Hideo Takeuchi
Pharmaceutical Institute, Tohoku University, Aobayama, Sendai 980-77, Japan
Pharmaceutical Institute, Tohoku University, Aobayama, Sendai 980-77, JapanSearch for more papers by this authorIssei Harada
Pharmaceutical Institute, Tohoku University, Aobayama, Sendai 980-77, Japan
Deceased August 10, 1992.
Search for more papers by this authorShinji Hashimoto,
Takahiko Yabusaki,
Hideo Takeuchi,
Issei Harada,
Shinji Hashimoto
Pharmaceutical Institute, Tohoku University, Aobayama, Sendai 980-77, Japan
Search for more papers by this authorTakahiko Yabusaki
Pharmaceutical Institute, Tohoku University, Aobayama, Sendai 980-77, Japan
Search for more papers by this authorCorresponding Author
Hideo Takeuchi
Pharmaceutical Institute, Tohoku University, Aobayama, Sendai 980-77, Japan
Pharmaceutical Institute, Tohoku University, Aobayama, Sendai 980-77, JapanSearch for more papers by this authorIssei Harada
Pharmaceutical Institute, Tohoku University, Aobayama, Sendai 980-77, Japan
Deceased August 10, 1992.
Search for more papers by this authorAbstract
Ultraviolet resonance Raman spectra have been measured for human serum albumin (HSA) and its complexes with three types of ligands. Tyr and Trp Raman bands of ligand-free HSA are strongly enhanced with 240-nm excitation compared with those of aqueous amino acids, indicating that the side chains of some Tyr residues and the unique Trp at position 214 are hydrogen bonded in hydrophobic environments. The high intensity of Tyr and Trp Raman scattering remains unchanged in a wide pH range of 3.5–9.0 and the microenvironments of the Tyr and Trp residues seem conserved in this pH range. The Tyr Raman intensity of HSA increases upon binding of palmitic acid, indicating hydrophobic interactions between the Tyr phenol ring and the aliphatic chain of the bound fatty acid. Binding of warfarin, on the other hand, does not affect the Tyr Raman intensity. Instead, an increase is observed for the Raman intensity of Trp-214, which is located at the opening of the warfarin binding site. Concomitantly a conformation-marker Raman band of Trp-214 changes in frequency and the warfarin Raman intensity increases, suggesting direct hydrophobic interactions between Trp-214 and warfarin. Complexation of ibuprofen and HSA increases the Raman intensity of Tyr but not of ibuprofen, which is ascribed to the formation of a hydrogen bond between the carboxylate of ibuprofen and the phenolic OH of Tyr-411, the unique Tyr residue at the ibuprofen binding site. Hydrophobic interactions and hydrogen bonding of Tyr and Trp residues play a key role in ligand binding of HSA. © 1995 John Wiley & Sons, Inc.
References
- 1 W. E. Lindup, “Plasma protein binding of drugs—some basic and clinical aspects,” Prog. Drug Metab., 10, 141–185 (1987).
- 2 T. Peters, Jr., “Serum albumin,” Adv. Protein Chem., 37, 161–245 (1985).
- 3 U. Kragh-Hansen, “Molecular aspects of ligand binding to serum albumin,” Pharmacol. Rev., 33, 17–53 (1981).
- 4 K. J. Fehske, W. E. Müller, and U. Wollert, “The location of drug binding sites in human serum albumin,” Biochem. Pharmacol., 30, 687–692 (1981).
- 5 G. Sudlow, D. J. Birkett, and D. N. Wade, “The characterization of two specific drug binding sites on human serum albumin,” Mol. Pharmacol., 11, 824–832 (1975).
- 6 G. Sudlow, D. J. Birkett, and D. N. Wade, “Further characterization of specific drug binding sites on human serum albumin,” Mol. Pharmacol., 12, 1052–1061 (1976).
- 7 I. Sjöholm, B. Ekman, A. Kober, I. Ljungstedt-Påhlman, B. Seiving, and T. Sjödin, “Binding of drugs to human serum albumin: XI. The specificity of three binding sites as studied with albumin immobilized in microparticles,” Mol. Pharmacol., 16, 767–777 (1979).
- 8 U. Kragh-Hansen, “Evidence for a large and flexible region of human serum albumin possessing high affinity binding sites for salicylate, warfarin, and other ligands,” Mol. Pharmacol., 34, 160–171 (1988).
- 9 K. J. Fehske, U. Schläfer, U. Wollert, and W. E. Müller, “Characterization of an important drug binding area on human serum albumin including the high-affinity binding sites of warfarin and azapropazone,” Mol. Pharmacol., 21, 387–393 (1982).
- 10 G. E. Means and M. L. Bender, “Acetylation of human serum albumin by p-nitrophenyl acetate,” Biochemistry, 14, 4989–4994 (1975).
- 11 K. J. Fehske, W. E. Müller, and U. Wollert, “A highly reactive tyrosine residue as part of the indole and benzodiazepine binding site of human serum albumin,” Biochim. Biophys. Acta, 577, 346–359 (1979).
- 12 O. J. M. Bos, M. J. E. Fischer, J. Wilting, and L. H. M. Janssen, “Drug-binding and other physico-chemical properties of a large tryptic and a large peptic fragment of human serum albumin,” Biochim. Biophys. Acta, 953, 37–47 (1988).
- 13 X. M. He and D. C. Carter, “Atomic structure and chemistry of human serum albumin,” Nature, 358, 209–215 (1992).
- 14 F. B. Edwards, R. B. Rombauer, and B. J. Campbell, “Thiol-disulfide interchange reactions between serum albumin and disulfides,” Biochim. Biophys. Acta, 194, 234–245 (1969).
- 15 S. Hashimoto, T. Ikeda, H. Takeuchi, and I. Harada, “Utilization of a prism monochromator as a sharpcut bandpass filter in ultraviolet Raman spectroscopy,” Appl. Spectrosc., 47, 1283–1285 (1993).
- 16 C. Su, Y. Wang, and T. G. Spiro, “Saturation effects on ultraviolet resonance Raman intensities: Excimer/YAG laser comparison and aromatic amino acid cross-sections,” J. Raman Spectrosc., 21, 435–440 (1990).
- 17 N. Cho, S. Song, and S. A. Asher, “UV resonance Raman and excited-state relaxation rate studies of hemoglobin,” Biochemistry, 33, 5932–5941 (1994).
- 18 I. Harada and H. Takeuchi, Raman and ultraviolet resonance Raman spectra of proteins and related compounds, in Spectroscopy of Biological Systems, ed. by R. J. H. Clark and R. H. Hester, John Wiley & Sons, Chichester, 1986, pp. 113–175.
- 19 D. C. Carter and J. X. Ho, “Structure of serum albumin,” Adv. Protein Chem., 45, 153–203 (1994).
- 20 R. A. Copeland and T. G. Spiro, “Secondary structure determination in proteins from deep (192–223-nm) ultraviolet Raman spectroscopy,” Biochemistry, 26, 2134–2139 (1987).
- 21 S. A. Asher, M. Ludwig, and C. R. Johnson, “UV resonance Raman excitation profiles of the aromatic amino acids,” J. Am. Chem. Soc., 108, 3186–3197 (1986).
- 22 H. Takeuchi, Y. Ohtsuka, and I. Harada, “Ultraviolet resonance Raman study on the binding mode of enkephalin to phospholipid membranes,” J. Am. Chem. Soc., 114, 5321–5328 (1992).
- 23 D. A. Chignell and W. B. Gratzer, “Solvent effects on aromatic chromophores and their relation to ultraviolet difference spectra of proteins,” J. Phys. Chem., 72, 2934–2941 (1968).
- 24 K. R. Rodgers, C. Su, S. Subramaniam, and T. G. Spiro, “Hemoglobin R → T structural dynamics from simultaneous monitoring of tyrosine and tryptophan time-resolved UV resonance Raman signals,” J. Am. Chem. Soc., 114, 3697–3709 (1992).
- 25 H. Takeuchi, N. Watanabe, and I. Harada, “Vibrational spectra and normal coordinate analysis of p-cresol and its deuterated analogs,” Spectrochim. Acta, 44A, 749–761 (1988).
- 26 H. Takeuchi, N. Watanabe, Y. Sato, and I. Harada, “Effects of hydrogen bonding on the tyrosine Raman bands in the 1300–1150 cm−1 region,” J. Raman Spectrosc., 20, 233–237 (1989).
- 27 M. J. Kamlet and R. W. Taft, “The solvatochromic comparison method. I. The β-scale of solvent hydrogen-bond acceptor (HBA) basicities,” J. Am. Chem. Soc., 98, 377–383 (1976).
- 28 T. Yokoyama, R. W. Taft, and M. J. Kamlet, “The solvatochromic comparison method. 3. Hydrogen bonding by some 2-nitroaniline derivatives,” J. Am. Chem. Soc., 98, 3233–3237 (1976).
- 29 M. N. Siamwiza, R. C. Lord, M. C. Chen, et al., “Interpretation of the doublet at 850 and 830 cm−1 in the Raman spectra of tyrosyl residues in proteins and certain model compounds,” Biochemistry, 14, 4870–4876 (1975).
- 30 I. Harada, T. Miura, and H. Takeuchi, “Origin of the doublet at 1360 and 1340 cm−1 in the Raman spectra of tryptophan and related compounds,” Spectrochim. Acta, 42A, 307–312 (1986).
- 31 I. Harada, T. Yamagishi, K. Uchida, and H. Takeuchi, “Ultraviolet resonance Raman spectra of bacteriorhodopsin in the light-adapted and darkadapted states,” J. Am. Chem. Soc., 112, 2443–2445 (1990).
- 32 S. Hashimoto, K. Miura, T. Yamagishi, H. Takeuchi, and I. Harada, “Ultraviolet resonance Raman study on purple and blue membranes of Halobacterium halobium,” Photochem. Photobiol., 56, 1097–1103 (1992).
- 33 M. R. Eftink and C. A. Ghiron, “Exposure of tryptophanyl residues and protein dynamics,” Biochemistry, 16, 5546–5551 (1977).
- 34 K. L. Bell and H. C. Brenner, “Phosphorescence and optically detected magnetic resonance study of the tryptophan residue in human serum albumin,” Biochemistry, 21, 799–804 (1982).
- 35 R. P. Rava and T. G. Spiro, “Resonance enhancement in the ultraviolet Raman spectra of aromatic amino acids,” J. Phys. Chem., 89, 1856–1861 (1985).
- 36 H. Takeuchi and I. Harada, “Ultraviolet resonance Raman spectroscopy of X-Proline bonds: A new marker band of hydrogen bonding at the imide CO site,” J. Raman Spectrosc., 21, 509–515 (1990).
- 37 A. O. Obaseki, W. R. Porter, and W. F. Trager, “4-Hydroxycoumarin/2-hydroxychromone tautomerism: Infrared spectra of 2- 13C and 3-D labeled 4-hydroxycoumarin and its anion,” J. Heterocyclic Chem., 19, 385–390 (1982).
- 38 T. Miura, H. Takeuchi, and I. Harada, “Tryptophan Raman bands sensitive to hydrogen bonding and side-chain conformation,” J. Raman Spectrosc., 20, 667–671 (1989).
- 39 A. Hvidt and K. Wallevik, “Conformational changes in human serum albumin as revealed by hydrogen–deuterium exchange studies,” J. Biol. Chem., 247, 1530–1535 (1972).
- 40 S. Era, H. Ashida, S. Nagaoka, H. Inouye, and M. Sogami, “CD-resolved secondary structure of bovine plasma albumin in acid-induced isomerization.” Int. J. Peptide Protein Res., 22, 333–340 (1983).
- 41 O. J. M. Bos, J. F. A. Labro, M. J. E. Fischer, J. Wilting, and L. H. M. Janssen, “The molecular mechanism of the neutral-to-base transition of human serum albumin,” J. Biol. Chem., 264, 953–959 (1989).
- 42 J. D. Ashbrook, A. A. Spector, E. C. Santos, and J. E. Fletcher, “Long chain fatty acid binding to human serum albumin,” J. Biol. Chem., 250, 2333–2338 (1975).
- 43 M. W. Yu and J. S. Finlayson, “Stabilization of human albumin by caprylate and acetyltryptophanate,” Vox Sang., 47, 28–40 (1984).
- 44 J. A. Klapper, Jr. and J. R. Cann, “Inhibition of peptic digestion of serum albumin by fatty acids,” Arch. Biochem. Biophys., 108, 531–534 (1964).
- 45 K. J. Fehske, W. E. Müller, U. Wollert, and L. M. Velden, “The lone tryptophan residue of human serum albumin as part of the specific warfarin binding site. Binding of dicoumarol to the warfarin, indole, and benzodiazepine binding sites,” Mol. Pharmacol., 16, 778–789 (1979).
- 46 C. F. Chignell, “Optical studies of drug–protein complexes. IV. The interaction of warfarin and dicoumarol with human serum albumin,” Mol. Pharmacol., 6, 1–12 (1970).
- 47 K. J. Fehske, W. E. Müller, and U. Wollert, “Direct demonstration of the highly reactive tyrosine residue of human serum albumin located in fragment 299–585,” Arch. Biochem. Biophys., 205, 217–221 (1980).
- 48 T. Maruyama, C. C. Lin, K. Yamasaki, et al., “Binding of suprofen to human serum albumin. Role of the suprofen carboxyl group,” Biochem. Pharmacol., 45, 1017–1026 (1993).
- 49 M. H. Rahman, T. Maruyama, T. Okada, K. Yamasaki, and M. Otagiri, “Study of interaction of carprofen and its enantiomers with human serum albumin—I. Mechanism of binding studied by dialysis and spectroscopic methods,” Biochem. Pharmacol., 46, 1721–1731 (1993).
- 50 N. P. Sollenne and G. E. Means, “Characterization of a specific drug binding site of human serum albumin,” Mol. Pharmacol., 15, 754–757 (1979).
- 51 K. Ikeda, Y. Kurono, Y. Ozeki, and T. Yotsuyanagi, “Effects of drug bindings on esterase activity of human serum albumin. Dissociation constants of the complexes between the protein and drugs such as N-arylanthranilic acids, coumarin derivatives and prostaglandins,” Chem. Pharm. Bull., 27, 80–87 (1979).
