Molecular engineering of a small trypsin inhibitor based on the binding loop of horsegram seed Bowman-Birk inhibitor

References

• Steiner RF. The interaction of the Bowman-Birk inhibitor with trypsin and chymotrypsin. Eur J Biochem 1972;27:87–92.
   PubMedGoogle Scholar
• Galasso I, Piergiovanni AR, Lioi L, Campion B, Bollini R, Sparvoli F. Genome organization of Bowman–Birk inhibitor in common bean (Phaseolus vulgaris L.). Mol Breeding 2009;23:617–624.
   Google Scholar
• Chen P, Rose J, Love R, Wei CH, Wang BC. Reactive sites of an anticarcinogenic Bowman-Birk proteinase inhibitor are similar to other trypsin inhibitors. J Biol Chem 1992;267:1990–1994.
   PubMed Web of Science ®Google Scholar
• Terada S, Sato K, Kato T, Izumiya N. Inhibitory properties of nonapeptide loop structures related to reactive sites of soybean Bowman-Birk inhibitor. FEBS Lett 1978;90:89–92.
   PubMedGoogle Scholar
• Odani S, Ikenaka T. Scission of soybean Bowman-Birk proteinase inhibitor into two small fragments having either trypsin or chymotrypsin inhibitory activity. J Biochem (Tokyo). 1973;74:697–715.
   PubMed Web of Science ®Google Scholar
• Luckett S, Garcia RS, Barker JJ, Konarev AV, Shewry PR, Clarke AR et al. High-resolution structure of a potent, cyclic proteinase inhibitor from sunflower seeds. J Mol Biol 1999;290:525–533.
   PubMed Web of Science ®Google Scholar
• Bode W, Huber R. Structural basis of the endoproteinase-protein inhibitor interaction. Biochim Biophys Acta 2000;1477:241–252.
   PubMed Web of Science ®Google Scholar
• Qi RF, Song ZW, Chi CW. Structural features and molecular evolution of Bowman-Birk protease inhibitors and their potential application. Acta Biochim Biophys Sin (Shanghai) 2005;37:283–292.
   PubMed Web of Science ®Google Scholar
• Barbosa JA, Silva LP, Teles RC, Esteves GF, Azevedo RB, Ventura MM et al. Crystal structure of the Bowman-Birk Inhibitor from Vigna unguiculata seeds in complex with beta-trypsin at 1.55 A resolution and its structural properties in association with proteinases. Biophys J 2007;92:1638–1650.
   PubMed Web of Science ®Google Scholar
• Capaldi S, Perduca M, Faggion B, Carrizo ME, Tava A, Ragona L et al. Crystal structure of the anticarcinogenic Bowman-Birk inhibitor from snail medic (Medicago scutellata) seeds complexed with bovine trypsin. J Struct Biol 2007;158:71–79.
   PubMedGoogle Scholar
• Catalano M, Ragona L, Molinari H, Tava A, Zetta L. Anticarcinogenic Bowman Birk inhibitor isolated from snail medic seeds (Medicago scutellata): solution structure and analysis of self-association behavior. Biochemistry 2003;42:2836–2846.
   PubMedGoogle Scholar
• Koepke J, Ermler U, Warkentin E, Wenzl G, Flecker P. Crystal structure of cancer chemopreventive Bowman-Birk inhibitor in ternary complex with bovine trypsin at 2.3 A resolution. Structural basis of Janus-faced serine protease inhibitor specificity. J Mol Biol 2000;298:477–491.
   PubMed Web of Science ®Google Scholar
• Li Y, Huang Q, Zhang S, Liu S, Chi C, Tang Y. Studies on an artificial trypsin inhibitor peptide derived from the mung bean trypsin inhibitor: chemical synthesis, refolding, and crystallographic analysis of its complex with trypsin. J Biochem 1994;116:18–25.
   PubMed Web of Science ®Google Scholar
• Lin G, Bode W, Huber R, Chi C, Engh RA. 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 1993;212:549–555.
   PubMedGoogle Scholar
• Park EY, Kim JA, Kim HW, Kim YS, Song HK. Crystal structure of the Bowman-Birk inhibitor from barley seeds in ternary complex with porcine trypsin. J Mol Biol 2004;343:173–186.
   PubMedGoogle Scholar
• Tsunogae Y, Tanaka I, Yamane T, Kikkawa J, Ashida T, Ishikawa C et al. Structure of the trypsin-binding domain of Bowman-Birk type protease inhibitor and its interaction with trypsin. J Biochem 1986;100:1637–1646.
   PubMed Web of Science ®Google Scholar
• Kennedy AR. The Bowman-Birk inhibitor from soybeans as an anticarcinogenic agent. Am J Clin Nutr 1998;68:1406S–1412S.
   PubMed Web of Science ®Google Scholar
• Ware JH, Wan XS, Rubin H, Schechter NM, Kennedy AR. Soybean Bowman-Birk protease inhibitor is a highly effective inhibitor of human mast cell chymase. Arch Biochem Biophys 1997;344:133–138.
   PubMed Web of Science ®Google Scholar
• Larionova NI, Gladysheva IP, Tikhonova TV, Kazanskaia NF. Inhibition of cathepsin G and elastase from human granulocytes by multiple forms of the Bowman-Birk type of soy inhibitor. Biokhimiia 1993;58:1437–1444.
   PubMedGoogle Scholar
• Lichtenstein GR, Deren JJ, Katz S, Lewis JD, Kennedy AR, Ware JH. Bowman-Birk inhibitor concentrate: a novel therapeutic agent for patients with active ulcerative colitis. Dig Dis Sci 2008;53:175–180.
   PubMed Web of Science ®Google Scholar
• Murthy HM, Judge K, DeLucas L, 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 2000;301:759–767.
   PubMed Web of Science ®Google Scholar
• Caccialupi P, Ceci LR, Siciliano RA, Pignone D, Clemente A, Sonnante G. Bowman-Birk Inhibitors in Lentil: Heterologous Expression, Functional Characterisation and anti-proliferative Properties in Human Colon Cancer Cells. Food Chemistry 2010;120:1058–1066.
   Web of Science ®Google Scholar
• Joanitti GA, Azevedo RB, Freitas SM. Apoptosis and lysosome membrane permeabilization induction on breast cancer cells by an anticarcinogenic Bowman-Birk protease inhibitor from Vigna unguiculata seeds. Cancer Lett 2010;293:73–81.
   PubMed Web of Science ®Google Scholar
• Clemente A, Moreno FJ, Marín-Manzano Mdel C, Jiménez E, Domoney C. The cytotoxic effect of Bowman-Birk isoinhibitors, IBB1 and IBBD2, from soybean (Glycine max) on HT29 human colorectal cancer cells is related to their intrinsic ability to inhibit serine proteases. Mol Nutr Food Res 2010;54:396–405.
   PubMed Web of Science ®Google Scholar
• Lanza A, Tava A, Catalano M, Ragona L, Singuaroli I, Robustelli della Cuna FS et al. Effects of the Medicago scutellata trypsin inhibitor (MsTI) on cisplatin-induced cytotoxicity in human breast and cervical cancer cells. Anticancer Res 2004;24:227–233.
   PubMed Web of Science ®Google Scholar
• Birk Y. The Bowman-Birk inhibitor. Trypsin- and chymotrypsin-inhibitor from soybeans. Int J Pept Protein Res 1985;25:113–131.
   PubMedGoogle Scholar
• Yavelow J, Finlay TH, Kennedy AR, Troll W. Bowman-Birk soybean protease inhibitor as an anticarcinogen. Cancer Res 1983;43:2454s–2459s.
   PubMed Web of Science ®Google Scholar
• Blanca HL, Hsieh CC, Lumen BO. Lunasin and Bowman-Birk protease inhibitor (BBI) in US commercial soy foods. Food Chem 2009;115:574–580.
   Google Scholar
• Billings PC, St Clair WH, Maki PA, Kennedy AR. Distribution of the Bowman Birk protease inhibitor in mice following oral administration. Cancer Lett 1992;62:191–197.
   PubMed Web of Science ®Google Scholar
• Fernandez JH, Mello MO, Galgaro L, Tanaka AS, Silva-Filho MC, Neshich G. Proteinase inhibition using small Bowman-Birk-type structures. Genet Mol Res 2007;6:846–858.
   PubMedGoogle Scholar
• Jaulent AsM Leatherbarrow, RJ. Design, synthesis and analysis of novel bicyclic and bifunctional protease inhibitors. Protein Eng Des Sel 2004;17:681–687.
   PubMedGoogle Scholar
• Scarpi D, McBride JD, Leatherbarrow RJ. Inhibition of human beta-tryptase by Bowman-Birk inhibitor derived peptides: creation of a new tri-functional inhibitor. Bioorg Med Chem 2004;12:6045–6052.
   PubMedGoogle Scholar
• Zablotna E, Jaskiewicz A, Legowska A, Miecznikowska H, Lesner A, Rolka K. Design of serine proteinase inhibitors by combinatorial chemistry using trypsin inhibitor SFTI-1 as a starting structure. J Pept Sci 2007;13:749–755.
   PubMed Web of Science ®Google Scholar
• Sreerama YN, Das JR, Rao DR, Gowda LR. Double-headed trypsin/chymotrypsin inhibitors from horse gram (Dolichos biflorus): purification, molecular and kinetic properties. J Food Biochem 1997;21:461–477.
   Google Scholar
• Muricken DG, Gowda LR. Functional expression of Horsegram (Dolichos biflorus) Bowman-Birk inhibitor and its self association. Biochim Biophys Acta 2010;1804:1413–1423.
   PubMedGoogle Scholar
• Kakade ML, Simons N, Liener IE. An evolution of natural vs. synthetic substrate for measuring the antitryptic activity of soybean samples. Cereal Chem 1969;46:518–526.
   Web of Science ®Google Scholar
• Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970;227:680–685.
   PubMed Web of Science ®Google Scholar
• Lineweaver H, Burk D. The determination of enzyme dissociation constants. J Am Chem Soc 1934;56:658–666.
   Web of Science ®Google Scholar
• Dixon M. The determination of enzyme inhibitor constants. Biochem J 1953;55:170–171.
   PubMed Web of Science ®Google Scholar
• Fear G, Komarnytsky S, Raskin I. Protease inhibitors and their peptidomimetic derivatives as potential drugs. Pharmacol Ther 2007;113:354–368.
   PubMed Web of Science ®Google Scholar
• McBride JD, Leatherbarrow RJ. Synthetic peptide mimics of the Bowman-Birk inhibitor protein. Curr Med Chem 2001;8:909–917.
   PubMed Web of Science ®Google Scholar
• Prakash B, Selvaraj S, Murthy MR, Sreerama YN, Rao DR, Gowda LR. Analysis of the amino acid sequences of plant Bowman-Birk inhibitors. J Mol Evol 1996;42:560–569.
   PubMed Web of Science ®Google Scholar
• Qi RF, Liu ZX, Xu SQ, Zhang L, Shao XX, Chi CW. Small peptides derived from the Lys active fragment of the mung bean trypsin inhibitor are fully active against trypsin. Febs J 2010;277:224–232.
   PubMedGoogle Scholar
• Stubbs MT, Morenweiser R, Stürzebecher J, Bauer M, Bode W, Huber R et al. The three-dimensional structure of recombinant leech-derived tryptase inhibitor in complex with trypsin. Implications for the structure of human mast cell tryptase and its inhibition. J Biol Chem 1997;272:19931–19937.
   PubMed Web of Science ®Google Scholar
• Sommerhoff CP, Söllner C, Mentele R, Piechottka GP, Auerswald EA, Fritz H. A Kazal-type inhibitor of human mast cell tryptase: isolation from the medical leech Hirudo medicinalis, characterization, and sequence analysis. Biol Chem Hoppe-Seyler 1994;375:685–694.
   PubMed Web of Science ®Google Scholar
• Marín-Manzano MC, Ruiz R, Jiménez E, Rubio LA, Clemente A. Anti-carcinogenic soyabean Bowman-Birk inhibitors survive faecal fermentation in their active form and do not affect the microbiota composition in vitro. Br J Nutr 2009;101:967–971.
   PubMedGoogle Scholar