Crystal structure of the anticarcinogenic Bowman-Birk inhibitor from snail medic (Medicago scutellata) seeds complexed with bovine trypsin

Journal of Structural Biology

Volumn 158, Issue 1, 2007, Pages 71-79

  Capaldi, Stefano ^a   Perduca, Massimiliano ^a   Faggion, Beniamino ^a   Carrizo, Maria E ^a   Tava, Aldo ^b   Ragona, Laura ^c   Monaco, Hugo L ^a  

^a UNIVERSITY OF VERONA   (Italy)

^b ISTITUTO NAZIONALE DELLA NUTRIZIONE   (Italy)

^c CNR   (Italy)

Author keywords

Bowman Birk inhibitor; Medicago scutellata; Protease inhibitor; Ternary complex; Trypsin; X ray structure

Indexed keywords

ARGININE; ASPARTIC ACID; BOWMAN BIRK INHIBITOR; HISTIDINE; POLYPEPTIDE; TERNARY COMPLEX FACTOR; TRYPSIN; TRYPSIN INHIBITOR;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CRYSTAL STRUCTURE; ENZYME BINDING; MEDICAGO; NUCLEAR MAGNETIC RESONANCE; OPTICAL RESOLUTION; PRIORITY JOURNAL; SOYBEAN; X RAY DIFFRACTION;

AMINO ACID SEQUENCE; ANIMALS; CATTLE; CRYSTALLOGRAPHY, X-RAY; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN CONFORMATION; SEEDS; SOLUTIONS; TRYPSIN; TRYPSIN INHIBITORS;

BOVINAE; GASTROPODA; GLYCINE MAX; MEDICAGO SCUTELLATA;

EID: 33947319328     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2006.10.017     Document Type: Article

References (46)

1. Balestrazzi A., Confalonieri M., Odoardi M., Ressegotti V., Allegro G., Tava A., and Carbonera D. A trypsin inhibitor cDNA from a novel source, snail medic (Medicago scutellata L.): cloning and functional expression in response to wounding, herbivore, jasmonic and salicylic acid. Plant Sci. 167 (2004) 337-346
2. Billings P.C., and Habres J.M. A growth-regulated protease activity that is inhibited by the anticarcinogenic Bowman-Birk protease inhibitor. Proc. Natl. Acad. Sci. USA 89 (1992) 3120-3124
3. Billings P.C., St Clair W., Owen A.J., and Kennedy A.R. Potential intracellular target proteins of the anticarcinogenic Bowman Birk protease inhibitor identified by affinity chromatography. Cancer Res. 48 (1988) 1798-1802
4. Bode W., and Huber R. Structural basis of the endoproteinase-protein inhibitor interaction. Biochim. Biophys. Acta 1477 (2000) 241-252
5. Catalano M., Ragona L., Molinari H., Tava A., and Zetta L. Anticarcinogenic Bowman Birk inhibitor isolated from snail medic seeds (Medicago scutellata): solution structure and analysis of self-association behavior. Biochemistry 42 (2003) 2836-2846
6. Ceciliani F., Tava A., Iori R., Mortarino M., Odoardi M., and Ronchi S. A trypsin inhibitor from snail medic seeds active against pest proteases. Phytochemistry 44 (1997) 393-398
7. Chen P., Rose J., Love R., Wei C.H., and an Wang B.C. Reactive sites of an anticarcinogenic Bowman-Birk proteinase inhibitor are similar to other trypsin inhibitors. J. Biol. Chem. 267 (1992) 1990-1994
8. Collaborative Computational Project Number 4 (1994). Acta Cryst. D50, 760-767.
9. Dittmann K.H., Dikomey E., Mayer C., and Rodemann H.P. The Bowman-Birk protease inhibitor enhances clonogenic cell survival of ionizing radiation-treated nucleotide excision repair-competent cells but not of xeroderma pigmentosum cells. Int. J. Radiat. Biol. 76 (2000) 223-229
10. Dittmann K.H., Mayer C., and Rodemann H.P. Radioprotection of normal tissue to improve radiotherapy: the effect of the Bowman Birk protease inhibitor. Curr. Med. Chem. Anticancer Agents 3 (2003) 360-363
11. Hutchinson E.G., and Thornton J.M. PROMOTIF-a program to identify and analyze structural motifs in proteins. Protein Sci. 5 (1995) 212-220
12. Kabsch W. A solution for the best rotation to relate two sets of vectors. Acta Cryst. A 32 (1978) 922-923
13. Kennedy A.R. Chemopreventive agents: protease inhibitors. Pharmacol. Ther. 78 (1998) 167-209
14. Kennedy A.R. The Bowman-Birk inhibitor from soybeans as an anticarcinogenic agent. Am. J. Clin. Nutr. 68 (1998) 1406S-1412S
15. Kennedy A.R., and Wan X.S. Effects of the Bowman-Birk inhibitor on growth, invasion, and clonogenic survival of human prostate epithelial cells and prostate cancer cells. Prostate 50 (2002) 125-133
16. Koepke J., Ermler U., Warkentin E., Wenzl G., and Flecker P. Crystal structure of cancer chemopreventive Bowman.Birk inhibitor in ternary complex with bovine trypsin. J. Mol. Biol. 298 (2000) 477-491
17. Kraulis P.J. Molscript: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24 (1991) 946-950
18. Krishna Murthy H.M., Judge K., DeLucas L., and Padmanabhan R. Crystal structure of Dengue virus NS3 protease in complex with a Bowman-Birk inhibitor: implications for flaviviral polyprotein processing and drug design. J. Mol. Biol. 301 (2000) 759-767
19. Lanza A., Tava A., Catalano M., Ragona L., Singuaroli I., Robustelli della Cuna F.S., and Robustelli della Cuna G. Effects of the Medicago scutellata trypsin inhibitor (MsTI) on cisplatin-induced cytotoxicity in human breast and cervical cancer cells. Anticancer Res. 24 (2004) 227-233
20. Laskowski Jr. M., and Kato I. Protein inhibitors of proteinases. Annu. Rev. Biochem. 49 (1980) 593-626
21. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. Procheck: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291
22. Leslie A.G.W. Recent changes to the MOSFLM package for processing film and image plate data Jnt. CCP4/ESF-EACMB Newslett. Protein Crystallogr. (1992) 26
23. Li de la Sierra I., Quillien L., Flecker P., Gueguen J., and Brunie S. Dimeric crystal structure of a Bowman-Birk protease inhibitor from pea seeds. J. Mol. Biol. 285 (1999) 1195-1207
24. Lin G., Bode W., Huber R., Chi C., and Engh R.A. The 0.25 nm X-ray structure of the Bowman-Birk type inhibitor from mung bean in ternary complex with porcine trypsin. Eur. J. Biochem. 212 (1993) 549-555
25. Luckett S., Garcia R.S., Barker J.J., Konarev A.V., Shewry P.R., Clarke A.R., and Brady R.L. High-resolution structure of a potent, cyclic proteinase inhibitor from sunflower seeds. J. Mol. Biol. 290 (1999) 525-533
26. McRee D.E. XtalView/Xfit-A versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125 (1999) 156-165
27. Mello M.O., Tanaka A.S., and Silva-Filho M.C. Molecular evolution of Bowman-Birk type proteinase inhibitors in flowering plants. Mol. Phylogenet. Evol. 27 (2003) 103-112
28. Meyskens F.L. Development of Bowman-Birk inhibitor for chemoprevention of oral head and neck cancer. Ann. N.Y. Acad. Sci. 952 (2001) 116-123
29. Miyata S., Koshikawa N., Yasumitsu H., and Miyazaki K. Trypsin stimulates integrin alpha(5)beta(1)-dependent adhesion to fibronectin and proliferation of human gastric carcinoma cells through activation of proteinase-activated receptor-2. J. Biol. Chem. 275 (2000) 4592-4598
30. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum likelihood method. Acta Crystallogr., D Biol. Crystallogr. 53 (1997) 240-255
31. Odani S., and Ikenaka T. Studies on soybean trypsin inhibitors. 8. Disulfide bridges in soybean Bowman-Birk proteinase inhibitor. J. Biochem. (Tokyo) 74 (1973) 697-715
32. Park E.Y., Kim J.A., Kim H.W., Kim Y.S., and Song H.K. Crystal structure of the Bowman-Birk inhibitor from barley seeds in ternary complex with porcine trypsin. J. Mol. Biol. 343 (2004) 173-186
33. Qi R.F., Song Z.W., and Chi C.W. Structural features and molecular evolution of Bowman-Birk protease inhibitors and their potential application. Acta Biochim. Biophys. Sin. 37 (2005) 283-292
34. Sanner, M.F., Olson, A.J., and Spehner, J.C. (1995). Fast and robust computation of molecular surfaces. Presented at the 11th Symposium on Computational Geometry held in Vancouver, BC, Canada.
35. Sibanda B.L., Blundell T.L., and Thornton J.M. Conformation of beta-hairpins in protein structures. A systematic classification with applications to modelling by homology, electron density fitting and protein engineering. J. Mol. Biol. 206 (1989) 759-777
36. Suzuki A., Yamane T., Ashida T., Norioka S., Hara S., and Ikenazka T. Crystallographic refinement of Bowman-Birk type protease inhibitor A-II from peanut (Arachis hypogaea) at 2.3 Å resolution. J. Mol. Biol. 234 (1993) 722-734
37. Thompson J.D., Higgins D.G., and Gibson T.J. Clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22 (1994) 4673-4680
38. Tsunogae Y., Tanaka I., Yamane T., Kikkawa J., Ashida T., Ishikawa C., Watanabe K., Nakamura S., and Takahashi K. Structure of the trypsin-binding domain of Bowman-Birk type protease inhibitor and its interaction with trypsin. J. Biochem. 100 (1986) 1637-1646
39. Vagin A., and Teplyakov A. An approach to multi-copy search in molecular replacement. Acta Crystallogr. D Biol. Crystallogr. 56 (2000) 1622-1624
40. Voss R.H., Ermler U., Essen L.O., Wenzl G., Kim Y.M., and Flecker P. Crystal structure of the bifunctional soybean Bowman-Birk inhibitor at 0.28-nm resolution. Structural peculiarities in a folded protein conformation. Eur. J. Biochem. 242 (1996) 122-131
41. Ware J.H., Wan X.S., Rubin H., Schechter N.M., and Kennedy A.R. Soybean Bowman-Birk protease inhibitor is a highly effective inhibitor of human mast cell chymase. Arch. Biochem. Biophys. 344 (1997) 133-138
42. Ware J.H., Wan X.S., and Kennedy A.R. Bowman-Birk inhibitor suppresses production of superoxide anion radicals in differentiated HL-60 cells. Nutr. Cancer. 33 (1999) 174-177
43. Werner M.H., and Wemmer D.E. Three-dimensional structure of soybean trypsin/chymotrypsin Bowman-Birk inhibitor in solution. Biochemistry 31 (1992) 999-1010
44. Wishart D.S., and Sykes B.D. The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data. J. Biomol. NMR 4 (1994) 171-180
45. Yavelow J., Collins M., Birk Y., Troll W., and Kennedy A.R. Nanomolar concentrations of Bowman-Birk soybean protease inhibitor suppress x-ray-induced transformation in vitro. Proc. Natl. Acad. Sci. USA 82 (1985) 5395-5399
46. Zhang L., Wan X.S., Donahue J.J., Ware J.H., and Kennedy A.R. Effects of the Bowman-Birk inhibitor on clonogenic survival and cisplatin- or radiation-induced cytotoxicity in human breast, cervical, and head and neck cancer cells. Nutr. Cancer 33 (1999) 165-173