Incorporation of the fluorescent amino acid 7-azatryptophan into the core domain 1-47 of hirudin as a probe of hirudin folding and thrombin recognition

Protein Science

Volumn 13, Issue 6, 2004, Pages 1489-1502

  De Filippis, Vincenzo ^a   De Boni, Silvia ^a,b   De Dea, Elisa ^a   Dalzoppo, Daniele ^a   Grandi, Claudio ^a   Fontana, Angelo ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

7 azatryptophan; Anticoagulants; Folding; Hirudin; Noncoded amino acids; Spectroscopy; Thrombin

Indexed keywords

7 AZATRYPTOPHAN; AMINO ACID; HIRUDIN; HIRUDIN DERIVATIVE; NITROGEN; THROMBIN; THROMBIN INHIBITOR; UNCLASSIFIED DRUG;

ABSORPTION; AMINO TERMINAL SEQUENCE; ARTICLE; COMPLEX FORMATION; DISULFIDE BOND; ENERGY TRANSFER; FLUORESCENCE; HYDROPHOBICITY; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SPECTROSCOPY; STRUCTURE ANALYSIS; SYNTHESIS;

AMINO ACID SEQUENCE; ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; HIRUDINS; LEECHES; MODELS, MOLECULAR; MOLECULAR PROBES; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN FOLDING; SPECTROMETRY, FLUORESCENCE; THERMODYNAMICS; THROMBIN; TRYPTOPHAN;

EID: 2442708919     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.03542104     Document Type: Article

References (80)

1. Allenmark, S. and Bomgren, B. 1982. Resolution of enantiomers by liquid affinity chromatography on albumin-agarose under isocratic conditions. J. Chromatogr. 237: 473-477.
2. Atherton, E. and Sheppard, R.C. 1989. Solid phase peptide synthesis: A practical approach. IRL Press, Oxford, UK.
3. Ayala, Y. and Di Cera, E. 1994. Molecular recognition by thrombin. Role of the slow → fast transition, site-specific ion binding energetics and thermodynamic mapping of structural components. J. Mol. Biol. 235: 733-746.
4. Berliner, L.J. and Shen, Y.Y.L. 1977. Physical evidence for an apolar binding site near the catholytic center of human α-thrombin. Biochemistry 16: 4622-4626.
5. Betz, A., Hofsteenge, J., and Stone, S.R. 1992. Interaction of the N-terminal region of hirudin with the active-site cleft of thrombin. Biochemistry 31: 4557-4562.
6. Blouse, G.E., Perron, M.J., Thompson, J.H., Day, D.E., Link, C.A., and Shore, J.D. 2002. A concerted structural transition in the plasminogen activator inhibitor-1 mechanism of inhibition. Biochemistry 41: 11997-12009.
7. Bode, W., Turk, D., and Karshikov, A. 1992. The refined 1.9-Å X-ray crystal structure of D-Phe-Pro-Arg chloromethylketone-inhibited human α-thrombin: Structure analysis, overall structure, electrostatic properties, detailed active-site geometry, and structure-function relationships. Protein Sci. 1: 426-471.
8. Buckler, D.R., Haas, E., and Scheraga, H.A. 1995. Analysis of the structure of ribonuclease A in native and partially denatured states by time-resolved nonradiative dynamic excitation energy transfer between site-specific extrinsic probes. Biochemistry 34: 15965-15978.
9. Budisa, N., Minks, C., Medrano, F.J., Lutz, J., Huber, R., and Moroder, L. 1998. Residue-specific bioincorporation of non-natural, biologically active amino acid into proteins as possible drug carriers: Structure and stability of the per-thiaproline mutant of annexin V. Proc. Natl. Acad. Sci. 95: 455-459.
10. Chapman, C.F. and Maroncelli, M. 1992. Excited-state tautomerization of 7-azaindole in water. J. Phys. Chem. 96: 8430-8441.
11. Chatrenet, B. and Chang, J.-Y. 1992. The folding of hirudin adopts a mechanism of trial and error. J. Biol. Chem. 267: 3038-3043.
12. Chen, Y., Rich, R.L., Gai, F., and Petrich, J.W. 1993. Fluorescent species of 7-azaindole and 7-azatryptophan in water. J. Phys. Chem. 97: 1770-1780.
13. Chen, Y., Gai, F., and Petrich, J.W. 1994. Single-exponential fluorescence decay of the nonnatural amino acid 7-azatryptophan and the nonexponential decay of tryptophan in water. J. Phys. Chem. 98: 2203-2209.
14. Chenault, H.K., Dahmer, J., and Whitesides, G.M. 1989. Kinetic resolution of unnatural and rarely occurring amino acids: Enantioselective hydrolysis of N-acyl amino acids catalyzed by acylase I. J. Am. Chem. Soc. 111: 6354-6364.
15. Chou, P.-T., Martinez, M.L., Cooper, W.C., McMorrow, D., Collins, S.T., and Kasha, M. 1992. Monohydrate catalysis of excited-state double-proton transfer in 7-azaindole. J. Phys. Chem. 96: 5203-5205.
16. Cohen, B.E., McAnaney, T.B., Park, E.S., Jan, Y.N., Boxer, S.G., and Jan, L.Y. 2002. Probing protein electrostatics with a synthetic fluorescent amino acid. Science 296: 1700-1703.
17. Cornish, V.W., Benson, D.R., Altenbach, C.A., Hideg, K., Hubbell, W.L., and Schultz, P.G. 1994. Site-specific incorporation of biophysical probes into proteins. Proc. Natl. Acad. Sci. 91: 2910-2924.
18. Cornish, V.W., Mendel, D., and Schultz, P.G. 1995. Probing protein structure and function with an expanded genetic code. 1995. Angew. Chem. Int. Ed. Engl. 34: 621-633.
19. Davie, E.W., Fujikawa, K., and Kisiel, W. 1991. The coagulation cascade: Initiation, maintenance, and regulation. Biochemistry 30: 10363-10370.
20. De Filippis, V., Vindigni, A., Altichieri, L., and Fontana A. 1995. Core domain of hirudin from leech Hirudinaria manillensis: Chemical synthesis, purification and characterization of a Trp3 analog of fragment 1-47. Biochemistry 34: 9552-9564.
21. De Filippis, V., Quarzago, D., Vindigni, A., Di Cera, E., and Fontana, A. 1998a. Synthesis and characterization of more potent analogues of hirudin fragment 1-47 containing non-natural amino acids. Biochemistry 37: 13507-13515.
22. De Filippis, V., De Antoni, F., Frigo, M., Polverino de Laureto, P., and Fontana, A. 1998b. Protein stabilization by Ala→Aib replacements. Biochemistry 37: 1686-1696.
23. De Filippis, V., Colombo, G., Russo, I., Spadari, B., and Fontana, A. 2002. Probing hirudin-thrombin interaction by incorporation of noncoded amino acids and molecular dynamics simulation. Biochemistry 43: 1537-1550.
24. Desinov, V.P., Peters, J., Hörlein, H.D., and Halle, B. 1996. Using buried water molecules to explore the energy landscape of proteins. Nat. Struct. Biol. 3: 505-509.
25. Di Cera, E., Dang, Q.D., and Ayala, Y.M. 1997. Molecular mechanisms of thrombin function. Cell. Mol. Life Sci. 53: 701-730.
26. Dougherty, D.A. 2000. Unnatural amino acids as probes of protein structure and function. Curr. Opin. Chem. Biol. 4: 645-652.
27. Eftink, M.R. 1997. Fluorescence methods for studying equilibrium macromolecule-ligand interactions. Methods Enzymol. 278: 221-257.
28. Eftink, M.R. and Shastry, M.C.R. 1997. Fluorescence methods for studying kinetics of protein folding reactions. Methods Enzymol. 278: 258-286.
29. Esmon, C.T., Fukudome, K., Mather, T., Bode, W., Regan, L.M., Stearns-Kurosawa, D.J., and Kurosawa, S. 1999. Inflammation, sepsis, and coagulation. Trends Hematol. 84: 254-259.
30. Fenton II, J.W., Fasco, M.J., and Stackrow, A.B. 1977. Human thrombins: Production, evaluation, and properties of α-thrombin. J. Biol. Chem. 252: 3587-3598.
31. Fersht, A. and Winter, G. 1992. Protein engineering. Trends Biochem. Sci. 17: 292-294.
32. Freedman, R.B. 1971. Applications of the chemical reactions of proteins in studies of their structure and function. Q. Rev. Chem. Soc. 25: 431-462.
33. Garcia, A.E. and Hummer, G. 2000. Water penetration and escape in proteins. Proteins 38: 261-272.
34. Gill, S.G. and von Hippel, P.H. 1989. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182: 319-326.
35. Gordon, M.S. 1996. Hydrogen transfer in 7-azaindole. J. Phys. Chem. 100: 3974-3979.
36. Greenstein, J.P. 1957. Resolution of DL mixtures of α-amino acids. Methods Enzymol. 3: 554-570.
37. Haruyama, H. and Wüthrich, K. 1989. Conformation of recombinant desulfatohirudin in aqueous solution determined by nuclear magnetic resonance. Biochemistry 28: 4301-4312.
38. Hu, Z., Ma, B., Wolfson, H., and Nussinov, R. 2000. Conservation of polar residues as hot spots at protein interfaces. Proteins 39: 331-342.
39. Huang, K., Lu, W., Anderson, S., Laskowski Jr., M., and James, M.N.G. 1995. Water molecules participate in proteinase-inhibitor interactions. Protein Sci. 4: 1985-1997.
40. Ittah, V. and Haas, E. 1995. Nonlocal interactions stabilize long range loops in the initial folding intermediates of reduced bovine pancreatic trypsin inhibitor. Biochemistry 34: 4493-4506.
41. Josefsson, B., Einarsson, S., Moller, P., and Sanchez, D. 1987. Separation of amino acid enantiomers and chiral amines using precolumn derivatization with (+)-1-(9-fluorenyl)ethylchloroformate and reversed-phase liquid chromatography. Anal. Chem. 59: 1191-1195.
42. Kahn, P.C. 1979. The interpretation of near-ultraviolet circular dichroism. Methods Enzymol. 61: 339-378.
43. Kay, L.E. 1998. Protein dynamics from NMR. Nat. Struct. Biol. Suppl: 513-517.
44. Kelley, L.A. and Sutcliffe, M.J. 1997. OLDERADO: On-line database of ensemble representatives and domains. Protein Sci. 6: 2628-2630.
45. Kent, S.B. 1988. Chemical synthesis of peptides and proteins. Annu. Rev. Biochem. 57: 957-989.
46. Lacowicz, J.R. 1999. Principles of fluorescence spectroscopy, 2nd ed. Kluwer Academic/Plenum, New York.
47. Lecointe, L., Rolland-Fulcrand, V., Roumestant, M.L., Viallefont, P., and Martinez, J. 1998. Chemoenzymatic synthesis of the two enantiomers of 7-azatryptophan. Tetrahedron 9: 1753-1758.
48. Leo, A., Hansch, C., and Elkins, D. 1971. Partition coefficients and their uses. Chem. Rev. 71: 525-555.
49. Lo Conte. L., Chothia, C., and Janin, J. 1999. The atomic structure of protein-protein recognition sites. J. Mol. Biol. 285: 2177-2198.
50. Markwardt, F. 1994. The development of hirudin as an antithrombotic drug. Thromb. Res. 74: 1-23.
51. Mente, S. and Maroncelli, M. 1998. Solvation and the excited-state tautomerization of 7-azaindole and 1-azacarbazole: Computer simulations in water and alcohol solvents. J. Phys. Chem. 102: 3860-3876.
52. Mohammadi, F., Prentice, G.A., and Merrill, A.R. 2001. Protein-protein interaction using tryptophan analogues: Novel spectroscopic probes for toxin-elongation factor-2 interactions. Biochemistry 40: 10273-10283.
53. Nakajima, A., Hirano, M., Hasumi, R., Kaya, K., Watanabe, H., Carter, C.C., Williamson, J.M., and Miller, T.A. 1997. High-resolution laser-induced fluorescence spectra of 7-azaindole-water complexes and 7-azaindole dimmer. J. Phys. Chem. A 101: 392-398.
54. Negrerie, M., Gai, F., Bellefeuille, S.M., and Petrich, J.W. 1991. Photophysics of a novel optical probe: 7-Azaindole. J. Phys. Chem. 95: 8663-8670.
55. Nicastro, G., Baumer, L., Bolis, G., and Tatò, M. 1997. NMR solution structure of a novel hirudin variant HM2, N-terminal 1-47 and N64 → V + G mutant. Biopolymers 41: 731-749.
56. Rich, R.L., Negrerie, M., Li, J., Elliott, S., Thornburg, R.W., and Petrich, J.W. 1993. The photophysical probe, 7-azatryptophan, in synthetic peptides. Photochem. Photobiol. 58: 28-30.
57. Rich, R.L., Gai, F., Lane, J.W., Petrich, J.W., and Schwabacher, A.W. 1995. Using 7-azatryptophan to probe small molecule-protein interactions on the picosecond time scale: The complex of avidin and biotinylated 7-azatryptophan. J. Am. Chem. Soc. 117: 733-739.
58. Rischel, C. and Poulsen, F.M. 1995. Modification of a specific tyrosine enables tracing of the end-to-end distance during apomyoglobin folding. FEBS Lett. 374: 105-109.
59. Ross, A., Szabo, A.G., and Hogue, C.W.V. 1997. Enhancement of protein spectra with tryptophan analogs: Fluorescence spectroscopy of protein-protein and protein-nucleic acid interactions. Methods Enzymol. 278: 151-190.
60. Rydel, T.J., Tulinsky, A., Bode, W., and Huber, R. 1991. Refined structure of the hirudin-thrombin complex. J. Mol. Biol. 221: 583-601.
61. Scacheri, E., Nitti, G., Valsasina, B., Orsini, G., Visco, C., Ferreia, M., Sawyer, R.T., and Sarmientos, P. 1993. Novel hirudin variants from the leech Hirudinaria manillensis. Amino acid sequence, cDNA cloning and genomic organization. Eur. J. Biochem. 214: 295-304.
62. Schlesinger, S. 1968. The effect of amino acid analogues on alkaline phosphatase formation in Escherichia coli K-12. J. Biol. Chem. 243: 3877-3883.
63. Scott, D.J., Leejeerajumnean, S., Brannigan, J.A., Lewis, R.J., Wilkinson, A.J., and Hoggett, J.G. 1999. Quaternary re-arrangement analysed by spectral enhancement: The interaction of sporulation repressor with its antagonist. J. Mol. Biol. 293: 997-1004.
64. Shaltiel, A., Cox, S., and Taylor, S.S. 1998. Conserved water molecules contribute to the extensive network of interactions at the active site of protein kinase A. Proc. Natl. Acad. Sci. 95: 484-491.
65. Smirnov, A.V., English, D.S., Rich, R.L., Lane, J., Teyton, L., Schwabacher, A.W., Luo, S., Thorburg, R.W., and Petrich, J.W. 1997. Photophysics and biological applications of 7-azaindole and its analogs. J. Phys. Chem. B 101: 2758-2769.
66. Soumillon, P., Jespers, L., Vervoort, J., and Fastrez, J. 1995. Biosynthetic incorporation of 7-azatryptophan into the phage lambda lysozyme: Estimation of tryptophan accessibility, effect on enzymatic activity and protein stability. Protein Eng. 8: 451-456.
67. Stewart, K.K. and Doherty, R.F. 1973. Resolution of D,L-tryptophan by affinity chromatography on bovine-serum albumin-agarose columns. Proc. Natl. Acad. Sci. 70: 2850-2852.
68. Strickland, E.H. 1974. Aromatic contributions to circular dichroism spectra of proteins. CRC Crit. Rev. Biochem. 3: 113-175.
69. Szyperski, T., Güntert, P., Stone, S.R., and Wütrich, K. 1992. Nuclear magnetic resonance solution structure of hirudin (1-51) and comparison with corresponding tridimensional structures determined using the complete 65-residue hirudin polypeptide chain. J. Mol. Biol. 228: 1193-1205.
70. Taylor, C.A., El-Boyoumi, M.A., and Kasha, M. 1969. Excited-state two proton tautomerism in hydrogen-bonded N-heterocyclic base pairs. Proc. Natl. Acad. Sci. 63: 253-260.
71. Tcherkasskaya, O. and Ptitsyn, O.B. 1999. Direct energy transfer to study the 3D structure of non-native proteins: AGH complex in the molten globule state of apomyoglobin. Protein Eng. 12: 485-490.
72. Ten-Kortenaar, P.B.W., Van Dijk, B.G., Peeters, M.J., Raabe, B.J., Adams, P.J., and Tesser, G.I. 1986. Rapid and efficient method for the preparation of Fmoc-amino acids starting from 9-fluorenylmethanol. Int. J. Pept. Protein Res. 27: 398-400.
73. Twine, S.M. and Szabo, A.G. 2003. Fluorescent amino acid analogs. Methods Enzymol. 360: 104-127.
74. Vijayalakshmi, J., Padmanabhan, K.P., Mann, K.G., and Tulinsky, A. 1994. The isomorphous structures of prethrombin2, hirugen-, and PPACK-thrombin: Changes accompanying activation and exosite binding to thrombin. Protein Sci. 3: 2254-2271.
75. Vindigni, A., De Filippis, V., Zanotti, G., Visco, C., Orsini, G., and Fontana, A. 1994. Probing the structure of hirudin from Hirudinaria manillensis by limited proteolysis: Isolation, characterization and thrombin-inhibitory properties of N-terminal fragments. Eur. J. Biochem. 226: 323-333.
76. Wallace, C.J. 1993. Understanding cytochrome c function: Engineering protein structure by semisynthesis. FASEB J. 7: 505-515.
77. Wong, C.-Y. and Eftink, M.R. 1997. Biosynthetic incorporation of tryptophan analogues into staphylococcal nuclease: Effect of 5-hydroxytryptophan and 7-azatryptophan on structure and stability. Protein Sci. 6: 689-697.
78. -. 1998. Incorporation of tryptophan analogues into staphylococcal nuclease: Stability toward thermal and guanidine-HCl induced unfolding. Biochemistry 37: 8947-8953.
79. Wu, P. and Brand, L. 1994. Resonance energy transfer: Methods and applications. Anal. Biochem. 18: 1-13.
80. Yamashita, S., Nishimoto, E., Szabo, A.G., and Yamasaki, N. 1996. Steady-state and time-resolved fluorescence studies on the ligand-induced conformational change in an active derivative, Kyn62-lysozyme. Biochemistry 35: 531-537.