Structural insights into serine protease inhibition by a marine invertebrate BPTI Kunitz-type inhibitor

Journal of Structural Biology

Volumn 180, Issue 2, 2012, Pages 271-279

  García Fernández, Rossana ^a,b   Pons, Tirso ^c   Perbandt, Markus ^d,e   Valiente, Pedro A ^a   Talavera, Ariel ^f   González González, Yamile ^a,b   Rehders, Dirk ^d   Chávez, María A ^a,b   Betzel, Christian ^d   Redecke, Lars ^d  

^a UNIVERSITY OF HAVANA   (Cuba)

^b Iberoamerican Programme of Science and Technology for Development RED CYTED PROMAL   (Germany)

^c Centro Nacional de Investigations Oncológicas   (Spain)

^d UNIVERSITY OF HAMBURG   (Germany)

^e UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^f CENTER OF MOLECULAR IMMUNOLOGY   (Cuba)

Author keywords

BPTI Kunitz type inhibitor; Crystal structure; Marine invertebrates; Protein inhibitor interaction; Serine protease

Indexed keywords

ALANINE; ARGININE; SERINE PROTEINASE; SERINE PROTEINASE INHIBITOR; STRICHODACTYLA HELIANTHUS PI 1; TRYPSIN; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; DRUG PROTEIN BINDING; DRUG STRUCTURE; ENZYME INHIBITION; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIORITY JOURNAL; SEA ANEMONE; SITE DIRECTED MUTAGENESIS; STRICHODACTYLA HELIANTHUS;

ANIMALS; CATTLE; CRYSTALLOGRAPHY, X-RAY; MUTAGENESIS, SITE-DIRECTED; SEA ANEMONES; SERINE ENDOPEPTIDASES; SERINE PROTEINASE INHIBITORS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TRYPSIN;

ACTINIARIA; BOVINAE; INVERTEBRATA; MAMMALIA; STICHODACTYLA HELIANTHUS;

EID: 84867917659     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2012.08.009     Document Type: Article

References (54)

1. Abbenante G., Fairlie D.P. Protease inhibitors in the clinic. Med. Chem. 2005, 1:71-104.
2. Alonso del Rivero M., Trejo S.A., Reytor M.L., Rodríguez de la Vega M., Delfín J., González Y., Canals F., Chávez M.A., Avilés F.X. A tri-domain bifunctional inhibitor of metallocarboxypeptidases A and serine proteases isolated from the marine annelid Sabellastarte magnifica. J. Biol. Chem. 2012, 287(19):15427-15438.
3. Antuch W., Berndt K.D., Chávez M.A., Delfín J., Wuethrich K. The NMR solution structure of a Kunitz-type proteinase inhibitor from the sea anemone Stichodactyla helianthus. Eur. J. Biochem. 1993, 212:675-684.
4. Bieth J. Some kinetic consequences of the tight binding of protein-proteinase inhibitor to proteolytic enzymes and their application to the determination of dissociation constants. Bayer Symposium V " Proteinase Inhibitor" 1974, Springer-Verlag, Berlin, pp. 463-469.
5. Brusca R.C., Brusca G.J. Invertebrates 2003, Sinauer Associates Inc, Publishers Sunderland, Massachusetts. second ed.
6. Burgering M.J., Orbons L.P., van der Doelen A., Mulders J., Theunissen H.J., Grootenhuis P.D., Bode W., Huber R., Stubbs M.T. The second Kunitz domain of human tissue factor pathway inhibitor: cloning, structure determination and interaction with factor Xa. J. Mol. Biol. 1997, 269:395-407.
7. Chand H.S., Schmidt A.E., Bajaj S.P., Kisiel W. Structure-function analysis of the reactive site in the first Kunitz-type domain of human tissue factor pathway inhibitor-2. J. Biol. Chem. 2004, 279:17500-17507.
8. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography. Acta Crystallogr. 1994, D50:760-763.
9. Czapinska H., Otlewski J., Krzywda S., Sheldrick G.M., Jaskólski M. High-resolution structure of bovine pancreatic trypsin inhibitor with altered binding loop sequence. J. Mol. Biol. 2000, 295:1237-1249.
10. Deisenhofer J., Steigemann W. Crystallographic refinement of the structure of bovine pancreatic trypsin inhibitor at l.5å resolution. Acta Crystallogr. 1975, B31:238-250.
11. Delfín J., Morera V., González Y., Díaz J., Márquez M., Larionova N., Saroyán A., Padrón G., Chávez M.A. Purification, characterization and immobilization of proteinase inhibitors from Stichodactyla helianthus. Toxicon 1996, 34:1367-1376.
12. Dennis M.S., Lazarus R.A. Kunitz domain inhibitors of tissue factor-factor VIIa: potents and specific inhibitors by competitive phage selection. J. Biol. Chem. 1994, 269:22137-22144.
13. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. 2004, D60:2126-2132.
14. Erlanger B.F., Kokowsky N., Cohen E. Preparation and properties of two new chromogenic substrates of trypsin. Arch. Biochem. Biophys. 1961, 95:271-278.
15. Fiedler F. Effects of secondary interactions on the kinetics of peptide and peptide ester hydrolysis by tissue kallikrein and trypsin. Eur. J. Biochem. 1987, 163:303-312.
16. Fischer H., Polikarpov I., Craievich A.F. Average protein density is a molecular-weight-dependent function. Protein Sci. 2004, 13:2825-2828.
17. Fritz H., Wunderer G. Biochemistry and applications of aprotinin, the kallikrein inhibitor from bovine organs. Arzneimittelforschung 1983, 33:479-494.
18. Gasteiger E., Hoogland C., Gattiker A., Duvaud S., Wilkins M.R., Appel R.D., Bairoch A. Protein Identification and Analysis Tools on the ExPASy Server;. The Proteomics Protocols Handbook 2005, 571-607. Humana Press. J.M. Walker (Ed.).
19. Gil D., García-Fernández R., Alonso-del-Rivero M., Lamazares E., Pérez M., Varas L., Díaz J., Chávez M.A., González-González Y., Mansur M. Recombinant expression of ShPI-1A, a non-specific BPTI-Kunitz-type inhibitor, and its protection effect on proteolytic degradation of recombinant human miniproinsulin expressed in Pichia pastoris. FEMS Yeast Res. 2011, 7:575-586.
20. Goette M., Grubmüller H. Accuracy and convergence of free energy differences calculated from nonequilibrium switching processes. J. Comp. Chem. 2009, 30:447-456.
21. González Y., Pons T., Gil J., Besada V., Alonso-del-Rivero M., Tanaka A.S., Araujo M.S., Chávez M.A. Characterization and comparative 3D modeling of CmPI-II, a novel 'non-classical' Kazal-type inhibitor from the marine snail Cenchritis muricatus (Mollusca). Biol. Chem. 2007, 388:1183-1194.
22. Grzesiak A., Krokoszynska I., Krowarchsch D., Dadlez M., Otlewski J. Inhibition of six serine proteinases of the human coagulation system by mutants of bovine pancreatic trypsin inhibitor. J. Biol. Chem. 2000, 321:647-658.
23. Hanson W.M., Domek G.J., Horvath M.P., Goldenberg D.P. Rigidification of a flexible protease inhibitor variant upon binding to trypsin. J. Mol. Biol. 2007, 366:230-243.
24. Helland R., Leiros I., Berglund G., Willassen N.P., Smala A. The crystal structure of anionic salmon trypsin in complex with bovine pancreatic trypsin inhibitor. Eur. J. Biochem. 1998, 256:317-324.
25. Hess B., Kutzner C., Van der Spoel D., Lindahl E. GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation. J. Chem. Theory Comput. 2008, 4:435-447.
26. Huber R., Kukla D., Bode W., Schwager P., Bartels K., Deisenhofer J., Steigemann W. Structure of the complex formed by bovine trypsin and bovine pancreatic trypsin inhibitor. Crystallographic refinement at 1.9å resolution. J. Mol. Biol. 1974, 89:73-101.
27. Kohfeldt E., Gohring W., Mayer U., Zweckstetter M., Holak T.A., Chu M.L., Timpl R. Conversion of the Kunitz-type module of collagen VI into a highly active trypsin inhibitor by site-directed mutagenesis. Eur. J. Biochem. 1996, 238:333-340.
28. Krissinel E., Henrick K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 2007, 372:774-797.
29. Krowarsch D., Zakrzewska M., Smalas A.O., Otlewski J. Structure-function relationships in serine protease-bovine pancreatic trypin inhibitor interaction. Protein Pept. Lett. 2005, 12:403-407.
30. Kunitz M., Northrop J.H. Isolation from beef pancreas of crystalline trypsinogen, trypsin, a trypsin inhibitor, and an inhibitor-trypsin compound. J. Gen. Physiol. 1936, 19:991-1007.
31. Laskowski M., Qasim M.A., Lu S.M. 2000, 228-279. Oxford University Press, Oxford.
32. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK - a program to check the stereochemical quality of protein structures. J. App. Cryst. 1993, 26:283-291.
33. Lenarčič B., Turk V. Thyroglobulin type-1 domains in equistatin inhibit both papain-like cysteine proteinases and cathepsin D. J. Biol. Chem. 1999, 274:563-566.
34. Lüthy R., Bowie J.U., Eisenberg D. Assessment of protein models with three-dimensional profiles. Nature 1992, 356:83-85.
35. Navaneetham D., Jin L., Pandey P., Strickler J.E., Babine R.E., Abdel-Meguid S.S., Walsh P.N. Structural and mutational analyses of the molecular interactions between the catalytic domain of factor XIa and the Kunitz protease inhibitor domain of protease nexin 2. J. Biol. Chem. 2005, 280:36165-36175.
36. Navaneetham D., Sinha D., Walsh P.N. Mechanisms and specificity of factor XIa and trypsin inhibition by protease nexin 2 and basic pancreatic trypsin inhibitor. J. Biochem. 2010, 148:467-479.
37. McBride J.D., Freeman H.N.M., Leatherbarrow R.J. Selection of human elastase inhibitors from a conformationally constrained combinatorial peptide library. Eur. J. Biochem. 1999, 266:403-412.
38. Minagawa S., Ishida M., Shimakura K., Nagashima Y., Shiomi K. Isolation and amino acid sequences of two Kunitz-type protease inhibitors from the sea anemone Anthopleura aff Xanthogrammica. Comp. Biochem. Physiol. 1997, 118B:381-386.
39. Murshudov G.N. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. 1997, D53:240-255.
40. Otlewski J., Jaskolski M., Buseck O., Cierpicki T., Czapiñska H., et al. Structure-function relationship of serine protease-protein inhibitor interaction. Acta Biochim. Pol. 2001, 38:419-428.
41. Perona J.J., Craik C.S. Evolutionary divergence of substrate specificity within the chymotrypsin-like serine protease fold. J. Biol. Chem. 1997, 272:29987-29990.
42. Reynolds C., Damerell D., Jones S. Protorp: a protein-protein interaction analysis tool. Bioinformatics 2009, 25:413-414.
43. Sasaki S.D., Cotrin S.S., Carmona A.K., Tanaka A.S. An unexpected inhibitory activity of Kunitz-type serine proteinase inhibitor derived from Boophilus microplus trypsin inhibitor of Cathepsin L. Biochem. Biophys. Res. Comm. 2006, 341:266-272.
44. Schechter I., Berger A. On the size of the active site in proteases. Biochem. Biophys. Res. Commun. 1967, 27:157-162.
45. 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 β-protein precursor (APPI) and basic trypsin inhibitor (BPTI): engineering of inhibitors with altered specificities. Protein Sci. 1997, 6:1806-1824.
46. Schmidt A.E., Chand H.S., Cascio D., Kisiel W., Bajaj S.P. Crystal structure of Kunitz domain 1 (KD1) of tissue factor pathway inhibitor-2 in complex with trypsin. J. Biol. Chem. 2005, 280:27832-27838.
47. Schweitz H., Bruhn T., Guillemare E., Moinier D., Lancelin J.M., Beress L., Lazdunski M. Kalicludines and kaliseptine. Two different classes of sea anemone toxins for voltage sensitive K+ channels. J. Biol. Chem. 1995, 270:25121-25126.
48. Seeliger D., de Groot B.L. Protein thermostability calculations using alchemical free energy simulations. Biophys. J. 2010, 98:2309-2316.
49. Shimomura T., Denda K., Kitamura A., Kawaguchi T., Kito M., Kondo J., Kagaya S., Qin L., Takata H., Miyazawa K., Kitamura N. Hepatocyte growth factor activator inhibitor, a novel Kunitz-type serine protease inhibitor. J. Biol. Chem. 1997, 272:6370-6376.
50. Sobolev V., Eyal E., Gerzon S., Potapov V., Babor M., et al. SPACE: a suite of tools for protein structure prediction and analysis based on complementarity and environment. Nucleic Acids Res. 2005, 33:W39-W43.
51. Van Nostrand W.E., Schmaier A.H., Siegel R.S., Wagner S.L., Raschke W.C. enhanced plasmin inhibition by a reactive center lysine mutant of the Kunitz-type protease inhibitor domain of the amyloid β-protein precursor. J. Biol. Chem. 1995, 270:22827-22830.
52. Vriend G. WHAT IF, a molecular modeling and drug design program. J. Mol. Graph. 1990, 8:52-56.
53. Xue Q., Itoh N., Schey K.L., Cooper R.K., La Peyre J.F. Evidence indicating the existence of a novel family of serine protease inhibitors that may be involved in marine invertebrate immunity. Fish Shellfish Immunol. 2009, 27:250-259.
54. Yanes O., Villanueva J., Querol E., Avilés F.X. Detection of non-covalent protein interactions by 'intensity fading' MALDI-TOF mass spectrometry: applications to proteases and protease inhibitors. Nat. Protoc. 2007, 2:119-130.