Structural consequences of accommodation of four non-cognate amino acid residues in the S1 pocket of bovine trypsin and chymotrypsin

Journal of Molecular Biology

Volumn 333, Issue 4, 2003, Pages 845-861

  Helland, Ronny ^a   Czapinska, Honorata ^b   Leiros, Ingar ^a,c   Olufsen, Magne ^a   Otlewski, Jacek ^b   Smalås, Arne O ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

^b UNIVERSITY OF WROC AW   (Poland)

^c EUROPEAN SYNCHROTRON RADIATION FACILITY   (France)

Author keywords

Bovine pancreatic trypsin inhibitor; Chymotrypsin; Protein protein interaction; Serine proteinase; Trypsin

Indexed keywords

APROTININ; ASPARTIC ACID; CHYMOTRYPSIN; GLYCINE; LEUCINE; MUTANT PROTEIN; PHENYLALANINE; SERINE PROTEINASE; TRYPSIN; VALINE;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CRYSTAL STRUCTURE; ENERGY; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

BOVINAE;

EID: 0142074764     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.08.059     Document Type: Article

References (38)

1. Schechter I., Berger A. On the size of the active site in proteases. Biochem. Biophys. Res. Commun. 27:1967;157-162.
2. Krowarsch D., Dadlez M., Buczek O., Krokoszynska I., Smalås A.O., Otlewski J. Interscaffolding additivity: binding of P1Variants of bovine pancreatic trypsin inhibitor to four serine proteases. J. Mol. Biol. 289:1999;175-186.
3. Barrett A.J., Rawlings N.D. Families and clans of serine peptidases. Arch. Biochem. Biophys. 318:1995;247-250.
4. Czapinska H., Otlewski J. Structural and energetic determinants of the S1-site specificity in serine proteases. Eur. J. Biochem. 260:1999;571-595.
5. Graf L., Jancso A., Szilagyi L., Hegyi G., Pinter K., Naray-Szabo G., et al. Electrostatic complementarity in the substrate binding pocket of trypsin. Proc. Natl Acad. Sci. USA. 85:1988;4961-4965.
6. Hedstrom L., Perona J.J., Rutter W.J. Converting trypsin to chymotrypsin: residue 172 is a substrate specificity determinant. Biochemistry. 33:1994;8757-8763.
7. Venekei I., Szilagyi L., Graf L., Rutter W.J. Attempts to convert chymotrypsin to trypsin. FEBS Letters. 25:1996;143-147.
8. Hedstrom L., Szilagyi L., Rutter W.J. Converting trypsin to chymotrypsin: the role of the surface loops. Science. 255:1992;1249-1253.
9. Perona J.J., Craik C.S. Structural basis of substrate specificity in the serine proteases. Protein Sci. 4:1995;337-360.
10. Perona J.J., Hedstrom L., Rutter W.J., Fletterick R.J. Structural origins of substrate discrimination in trypsin and chymotrypsin. Biochemistry. 34:1995;1489-1499.
11. Perona J.J., Craik C.S. Evolutionary divergence of substrate specificity within the chymotrypsin-like serine protease fold. J. Biol. Chem. 272:1997;29987-29990.
12. Helland R., Otlewski J., Sundheim O., Dadlez M., Smalås A.O. The crystal structures of the complexes between bovine beta-trypsin and ten P1 variants of BPTI. J. Mol. Biol. 287:1999;923-942.
13. Brandsdal B.O., Aqvist J., Smalås A.O. Computational analysis of binding of P1 variants to trypsin. Protein Sci. 10:2001;1584-1595.
14. Huang K., Lu W., Anderson S., Laskowski M. Jr, James M.N. Water molecules participate in proteinase-inhibitor interactions: crystal structures of Leu18, Ala18, and Gly18 variants of turkey ovomucoid inhibitor third domain complexed with Streptomyces griseus proteinase B. Protein Sci. 4:1995;1985-1997.
15. Bateman K.S., Anderson S., Lu W., Qasim M.A., Laskowski M. Jr, James M.N. Deleterious effects of beta-branched residues in the S1 specificity pocket of Streptomyces griseus proteinase B (SGPB): crystal structures of the turkey ovomucoid third domain variants Ile18I, Val18I, Thr18I, and Ser18I in complex with SGPB. Protein Sci. 9:2000;83-94.
16. Otlewski J., Jaskolski M., Buczek O., Cierpicki T., Czapinska H., Krowarsch D., et al. Structure-function relationship of serine protease-protein inhibitor interaction. Acta Biochim. Pol. 48:2001;419-428.
17. Castro M.J.M., Anderson S. Alanine point-mutations in the reactive region of bovine pancreatic trypsin inhibitor: effects on the kinetics and thermodynamics of binding to β-trypsin and α-chymotrypsin. Biochemistry. 35:1996;11435-11446.
18. Lu W., Apostol I., Qasim M.A., Warne N., Wynn R., Zhang W.L., et al. Binding of amino acid side-chains to S1 cavities of serine proteinases. J. Mol. Biol. 266:1997;441-461.
19. Schrauber H., Eisenhaber F., Argos P. Rotamers: to be or not to be? An analysis of amino acid side-chain conformations in globular proteins. J. Mol. Biol. 230:1993;592-612.
20. Cornell W.D., Cieplak P., Bayly C.I., Gould I.R., Merz K.M., Ferguson D.M., et al. A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117:1995;5179-5197.
21. Bode W., Meyer E. Jr, Powers J.C. Human leukocyte and porcine pancreatic elastase: X-ray crystal structures, mechanism, substrate specificity, and mechanism-based inhibitors. Biochemistry. 28:1989;1951-1963.
22. Wei A.Z., Mayr I., Bode W. The refined 2.3 Å crystal structure of human leukocyte elastase in a complex with a valine chloromethyl ketone inhibitor. FEBS Letters. 234:1988;367-373.
23. Cregge R.J., Durham S.L., Farr R.A., Gallion S.L., Hare C.M., Hoffman R.V., et al. Inhibition of human neutrophil elastase. 4. Design, synthesis, X-ray crystallographic analysis, and structure-activity relationships for a series of P2-modified, orally active peptidyl pentafluoroethyl ketones. J. Med. Chem. 41:1998;2461-2480.
24. Macdonald S.J., Dowle M.D., Harrison L.A., Clarke G.D., Inglis G.G., Johnson M.R., et al. Discovery of further pyrrolidine trans-lactams as inhibitors of human neutrophil elastase (HNE) with potential as development candidates and the crystal structure of HNE complexed with an inhibitor (GW475151). J. Med. Chem. 45:2002;3878-3890.
25. Frigerio F., Coda A., Pugliese L., Lionetti C., Menegatti E., Amiconi G., et al. Crystal and molecular structure of the bovine alpha-chymotrypsin-eglin c complex at 2.0 Å resolution. J. Mol. Biol. 225:1992;107-123.
26. Fujinaga M., Sielecki A.R., Read R.J., Ardelt W., Laskowski M. Jr, James M.N. Crystal and molecular structures of the complex of alpha-chymotrypsin with its inhibitor turkey ovomucoid third domain at 1.8 Å resolution. J. Mol. Biol. 195:1987;397-418.
27. Roussel A., Mathieu M., Dobbs A., Luu B., Cambillau C., Kellenberger C. Complexation of two proteic insect inhibitors to the active site of chymotrypsin suggests decoupled roles for binding and selectivity. J. Biol. Chem. 276:2001;38893-38898.
28. Read R.J., Fujinaga M., Sielecki A.R., James M.N. Structure of the complex of Streptomyces griseus protease B and the third domain of the turkey ovomucoid inhibitor at 1.8 Å resolution. Biochemistry. 22:1983;4420-4433.
29. Greenblatt H.M., Ryan C.A., James M.N. Structure of the complex of Streptomyces griseus proteinase B and polypeptide chymotrypsin inhibitor-1 from Russet Burbank potato tubers at 2.1 Å resolution. J. Mol. Biol. 205:1989;201-228.
30. Krokoszynska I., Dadlez M., Otlewski J. Structure of single-disulfide variants of bovine pancreatic trypsin inhibitor (BPTI) as probed by their binding to bovine beta-trypsin. J. Mol. Biol. 275:1998;503-513.
31. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
32. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D. 50(5):1994;760-763.
33. Sundheim, O. (1999). Structural studies on pancreatic serine proteinases. Cand. scient. thesis, University of Tromsø, Norway.
34. Scheidig A.J., Hynes T.R., Pelletier L.A., Wells J.A., Kossiakoff A.A. Crystal structures of bovine chymotrypsin and trypsin complexed to the inhibitor domain of Alzheimer's amyloid beta-protein precursor (APPI) and basic pancreatic trypsin inhibitor (BPTI): engineering of inhibitors with altered specificities. Protein Sci. 6:1997;1806-1824.
35. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921.
36. Sheldrick G.M., Schneider T.R. SHELXL: high resolution refinement. Methods Enzymol. 277:1997;319-343.
37. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for binding protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
38. Kleywegt G.J., Brünger A.T. Checking your imagination: applications of the free R value. Structure. 4:1996;897-904.