A novel subclassification for Kunitz proteinase inhibitors from leguminous seeds

Biochimie

Volumn 92, Issue 11, 2010, Pages 1667-1673

  Oliva, Maria Luiza V ^a   Silva, Mariana C C ^a   Sallai, Roberto C ^a   Brito, Marlon V ^a   Sampaio, Misako U ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Chymotrypsin; Kunitz inhibitors; Plant inhibitors; Primary structure; Trypsin inhibitors

Indexed keywords

CYSTEINE; CYSTEINE PROTEINASE INHIBITOR; DISULFIDE; HERBACEOUS AGENT; KALLIKREIN INHIBITOR; KUNITZ PROTEINASE INHIBITOR; PROTEINASE INHIBITOR; PROTEINASE INHIBITOR ACTI; PROTEINASE INHIBITOR AETI; PROTEINASE INHIBITOR AKTI; PROTEINASE INHIBITOR APTI; PROTEINASE INHIBITOR AVTI; PROTEINASE INHIBITOR BBCI; PROTEINASE INHIBITOR BBKI; PROTEINASE INHIBITOR BRTI; PROTEINASE INHIBITOR BUXI; PROTEINASE INHIBITOR BVCTI 3; PROTEINASE INHIBITOR BVTI; PROTEINASE INHIBITOR CEKI; PROTEINASE INHIBITOR CSTI; PROTEINASE INHIBITOR DTTCI; PROTEINASE INHIBITOR ECTI; PROTEINASE INHIBITOR GBREI; PROTEINASE INHIBITOR LLTI; PROTEINASE INHIBITOR PDTI; PROTEINASE INHIBITOR PTPKI; PROTEINASE INHIBITOR SWTI; PROTEINASE INHIBITOR TDI I; TRYPSIN INHIBITOR; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ACACIA CONFUSA; ALPHA HELIX; AMINO ACID SEQUENCE; BAUHINIA; CANAVALIA LINEATA; CASSIA OBTUSIFOLIA; DISULFIDE BOND; DRUG CLASSIFICATION; DRUG ISOLATION; ENTEROLOBIUM CONTORTISILIQUUM; ENZYME ACTIVE SITE; ENZYME INHIBITOR COMPLEX; ENZYME INHIBITOR INTERACTION; ENZYME SUBSTRATE COMPLEX; LEGUME; MEDICINAL PLANT; MOLECULAR STABILITY; NONHUMAN; PLANT SEED; PLANT TAXONOMY; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; REVIEW; SEQUENCE HOMOLOGY; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; CYSTEINE; FABACEAE; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDE HYDROLASES; PEPTIDES; PLANT PROTEINS; PROTEIN CONFORMATION; SEEDS;

EID: 78149358882     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2010.03.021     Document Type: Review

References (109)

1. Lopez-Otin C., Bond J.S. Proteases: multifunctional enzymes in life and disease. J. Biol. Chem. 2008, 283:30433-30437.
2. Richardson M. Seed storage proteins: the enzymes inhibitors. Meth. Plant Biochem. 1991, 5:259-305.
3. Birk Y. Plant Protease Inhibitors: Significance in Nutrition, Plant Protection, Cancer Prevention and Genetic Engineering 2003, Springer-Verlag, Berlin, 170 pp.
4. Bode W., Huber R. Structural basis of the endoproteinase-protein inhibitor interaction. Biochim. Biophys. Acta 2000, 1477:241-252.
5. Kunitz M. Crystalline soybean trypsin inhibitor. J. Gen. Physiol. 1946, 29:149-154.
6. Breiteneder H., Radauer C. A classification of plant food allergens. J. Allergy Clin. Immunol. 2004, 113:821-830.
7. Mosolov V.V., Valueva T.A. Proteinase inhibitors and their function in plants: a review. Appl. Biochem. Microbiol. 2005, 41:227-246.
8. Oliva M.L., Sampaio U.M. Bauhinia Kunitz-type proteinase inhibitors: structural characteristics and biological properties. Biol. Chem. 2008, 389:1007-1013.
9. Turk B. Targeting proteases: successes, failures and future prospects. Nat. Rev. Drug Discov. 2006, 5:785-799.
10. Laskowski M., Kato I. Protein inhibitors of proteinases. Annu. Rev. Biochem. 1980, 49:593-626.
11. Rawlings N.D., Tolle D.P., Barrett A.J. MEROPS: the peptidase database. Nucleic Acids Res. 2004, 32:D160-D164.
12. Koide T., Tsunasawa S., Ikenaka T. Studies on soybean trypsin inhibitors. 2. Amino-acid sequence around the reactive site of soybean trypsin inhibitor (Kunitz). Eur. J. Biochem. 1973, 32:408-416.
13. Lehle K., Wrba A., Jaenicke R. Erythrina caffra trypsin inhibitor retains its native structure and function after reducing its disulfide bonds. J. Mol. Biol. 1994, 239:276-284.
14. Hung C.H., Lee M.C., Lin J.Y. Inactivation of Acacia confusa trypsin inhibitor by site-specific mutagenesis. FEBS Lett. 1994, 353:312-314.
15. Lin J.Y., Chu S.C., Wu H.C., Hsieh Y.S. Trypsin inhibitor from the seeds of Acacia confusa. J. Biochem. 1991, 110:879-883.
16. Negreiros A.N., Carvalho M.M., Xavier Filho J., Blanco-Labra A., Shewry P.R., Richardson M. The complete amino acid sequence of the major Kunitz trypsin inhibitor from the seeds of Prosopsis juliflora. Phytochemistry 1991, 30:2829-2833.
17. Terada S., Katayama H., Noda K., Fujimura S., Kimoto E. Amino acid sequences of Kunitz family subtilisin inhibitors from seeds of Canavalia lineata. J. Biochem. 1994, 115:397-404.
18. Batista I.F., Oliva M.L., Araujo M.S., Sampaio M.U., Richardson M., Fritz H., Sampaio C.A. Primary structure of a Kunitz-type trypsin inhibitor from Enterolobium contortisiliquum seeds. Phytochemistry 1996, 41:1017-1022.
19. Oliva M.L., Souza-Pinto J.C., Batista I.F., Araujo M.S., Silveira V.F., Auerswald E.A., Mentele R., Eckerskorn C., Sampaio M.U., Sampaio C.A. Leucaena leucocephala serine proteinase inhibitor: primary structure and action on blood coagulation, kinin release and rat paw edema. Biochim. Biophys. Acta 2000, 1477:64-74.
20. Souza-Pinto J.C., Oliva M.L., Sampaio C.A., Damas J., Auerswald E.A., Limaos E., Fritz H., Sampaio M.U. Effect of a serine proteinase inhibitor from Leucaena leucocephala on plasma kallikrein and plasmin. Immunopharmacology 1996, 33:330-332.
21. Macedo M.L., de Sa C.M., Freire M.D., Parra J.R. A Kunitz-type inhibitor of coleopteran proteases, isolated from Adenanthera pavonina L. seeds and its effect on Callosobruchus maculatus. J. Agric. Food Chem. 2004, 52:2533-2540.
22. Delgado-Vargas F., Lopez-Valdes H.E., Valdes-Rodriguez S., Blanco-Labra A., Chagolla-Lopez A., Lopez-Valenzuela Ede J. Isolation and properties of a Kunitz-type protein inhibitor obtained from Pithecellobium dulce seeds. J. Agric. Food Chem. 2004, 52:6115-6121.
23. Bhattacharyya A., Babu C.R. Exploring the protease mediated conformational stability in a trypsin inhibitor from Archidendron ellipticum seeds. Plant Physiol. Biochem. 2006, 44:637-644.
24. Yoshizaki L., Troncoso M.F., Lopes J.L., Hellman U., Beltramini L.M., Wolfenstein-Todel C. Calliandra selloi macbride trypsin inhibitor: isolation, characterization, stability, spectroscopic analyses. Phytochemistry 2007, 68:2625-2634.
25. Zhou J.Y., Liao H., Zhang N.H., Tang L., Xu Y., Chen F. Identification of a Kunitz inhibitor from Albizzia kalkora and its inhibitory effect against pest midgut proteases. Biotechnol. Lett. 2008, 30:1495-1499.
26. Ee K.Y., Zhao J., Rehman A.U., Agboola S.O. Purification and characterization of a Kunitz-type trypsin inhibitor from Acacia victoriae Bentham seeds. J. Agric. Food Chem. 2009, 57:7022-7029.
27. Lopes J.L., Valadares N.F., Moraes D.I., Rosa J.C., Araujo H.S., Beltramini L.M. Physico-chemical and antifungal properties of protease inhibitors from Acacia plumosa. Phytochemistry 2009, 70:871-879.
28. Oliva M.L., Sallai R.C., Sampaio C.A., Fritz H., Auerswald E.A., Tanaka A.S., Torquato R.J., Sampaio M.U. Bauhinia serine proteinase inhibitors: effect on factor X, factor XII and plasma kallikrein. Immunopharmacology 1996, 32:85-87.
29. Oliva M.L., Andrade S.A., Batista I.F., Sampaio M.U., Juliano M., Fritz H., Auerswald E.A., Sampaio C.A. Human plasma kallikrein and tissue kallikrein binding to a substrate based on the reactive site of a factor Xa inhibitor isolated from Bauhinia ungulata seeds. Immunopharmacology 1999, 45:145-149.
30. Oliva M.L., Mendes C.R., Santomauro-Vaz E.M., Juliano M.A., Mentele R., Auerswald E.A., Sampaio M.U., Sampaio C.A. Bauhinia bauhinioides plasma kallikrein inhibitor: interaction with synthetic peptides and fluorogenic peptide substrates related to the reactive site sequence. Curr. Med. Chem. 2001, 8:977-984.
31. Oliva M.L., Santomauro-Vaz E.M., Andrade S.A., Juliano M.A., Pott V.J., Sampaio M.U., Sampaio C.A. Synthetic peptides and fluorogenic substrates related to the reactive site sequence of Kunitz-type inhibitors isolated from Bauhinia: interaction with human plasma kallikrein. Biol. Chem. 2001, 382:109-113.
32. Oliva M.L., Andrade S.A., Juliano M.A., Sallai R.C., Torquato R.J., Sampaio M.U., Pott V.J., Sampaio C.A. Kinetic characterization of factor Xa binding using a quenched fluorescent substrate based on the reactive site of factor Xa inhibitor from Bauhinia ungulata seeds. Curr. Med. Chem. 2003, 10:1085-1093.
33. Di Ciero L., Oliva M.L., Torquato R., Kohler P., Weder J.K., Camillo Novello J., Sampaio C.A., Oliveira B., Marangoni S. The complete amino acid sequence of a trypsin inhibitor from Bauhinia variegata var. candida seeds. J. Protein Chem. 1998, 17:827-834.
34. Cruz-Silva I., Gozzo A.J., Nunes V.A., Carmona A.K., Faljoni-Alario A., Oliva M.L., Sampaio M.U., Sampaio C.A., Araujo M.S. A proteinase inhibitor from Caesalpinia echinata (pau-brasil) seeds for plasma kallikrein, plasmin and factor XIIa. Biol. Chem. 2004, 385:1083-1086.
35. Bhattacharyya A., Babu C.R. Purification and biochemical characterization of a serine proteinase inhibitor from Derris trifoliata Lour. seeds: insight into structural and antimalarial features. Phytochemistry 2009, 70:703-712.
36. Silva J.A., Macedo M.L., Novello J.C., Marangoni S. Biochemical characterization and N-terminal sequences of two new trypsin inhibitors from Copaifera langsdorffii seeds. J. Protein Chem. 2001, 20:1-7.
37. Krauchenco S., Silva J.A., Nagem R.A., Brandao Neto J.R., Forrer V.P., Carmona E.F.R., Macedo M.L., Novello J.C., Marangoni S., Polikarpov I. Crystallization and preliminary X-ray diffraction analysis of a novel trypsin inhibitor from seeds of Copaifera langsdorffii. Acta Crystallogr. D Biol. Crystallogr. 2001, 57:1316-1318.
38. Krauchenco S., Nagem R.A., da Silva J.A., Marangoni S., Polikarpov I. Three-dimensional structure of an unusual Kunitz (STI) type trypsin inhibitor from Copaifera langsdorffii. Biochimie 2004, 86:167-172.
39. do Socorro M.C.M., Oliva M.L., Fritz H., Jochum M., Mentele R., Sampaio M., Coelho L.C., Batista I.F., Sampaio C.A. Characterization of a Kunitz trypsin inhibitor with one disulfide bridge purified from Swartzia pickellii. Biochem. Biophys. Res. Commun. 2002, 291:635-639.
40. Sumikawa J.T., Nakahata A.M., Fritz H., Mentele R., Sampaio M.U., Oliva M.L. A Kunitz-type glycosylated elastase inhibitor with one disulfide bridge. Planta Med. 2006, 72:393-397.
41. Macedo M.L., Garcia V.A., Freire M.G., Richardson M. Characterization of a Kunitz trypsin inhibitor with a single disulfide bridge from seeds of Inga laurina (SW.) willd. Phytochemistry 2007, 68:1104-1111.
42. Lingaraju M.H., Gowda L.R. A Kunitz trypsin inhibitor of Entada scandens seeds: another member with single disulfide bridge. Biochim. Biophys. Acta 2008, 1784:850-855.
43. de Oliveira C., Santana L.A., Carmona A.K., Cezari M.H., Sampaio M.U., Sampaio C.A., Oliva M.L. Structure of cruzipain/cruzain inhibitors isolated from Bauhinia bauhinioides seeds. Biol. Chem. 2001, 382:847-852.
44. Nakahata A.M., Bueno N.R., Rocha H.A., Franco C.R., Chammas R., Nakaie C.R., Jasiulionis M.G., Nader H.B., Santana L.A., Sampaio M.U., Oliva M.L. Structural and inhibitory properties of a plant proteinase inhibitor containing the RGD motif. Int. J. Biol. Macromol 2006, 40:22-29.
45. Haq S.K., Khan R.H. Characterization of a proteinase inhibitor from Cajanus cajan (L.). J. Protein Chem. 2003, 22:543-554.
46. Rawlings N.D., Barrett A.J., Bateman A. MEROPS: the peptidase database. Nucleic Acids Res. 2010, 38:D227-D233.
47. de Souza A.F., Torquato R.J., Tanaka A.S., Sampaio C.A. Cloning, expression and characterization of Bauhinia variegata trypsin inhibitor BvTI. Biol. Chem. 2005, 386:1185-1189.
48. Sumikawa J.T., Brito M.V., Macedo M.L., Uchoa A.F., Miranda A., Araujo A.P., Silva-Lucca R.A., Sampaio M.U., Oliva M.L. The defensive functions of plant inhibitors are not restricted to insect enzyme inhibition. Phytochemistry 2010, 71:214-220.
49. Oliva M.L., Sampaio M.U. Action of plant proteinase inhibitors on enzymes of physiopathological importance. Acad. Bras. Cienc. 2009, 81:615-621.
50. Araujo A.P., Hansen D., Vieira D.F., Oliveira C., Santana L.A., Beltramini L.M., Sampaio C.A., Sampaio M.U., Oliva M.L. Kunitz-type Bauhinia bauhinioides inhibitors devoid of disulfide bridges: isolation of the cDNAs, heterologous expression and structural studies. Biol. Chem. 2005, 386:561-568.
51. Sattar R., Ali S.A., Kamal M., Khan A.A., Abbasi A. Molecular mechanism of enzyme inhibition: prediction of the three-dimensional structure of the dimeric trypsin inhibitor from Leucaena leucocephala by homology modelling. Biochem. Biophys. Res. Commun. 2004, 314:755-765.
52. Song H.K., Suh S.W. Kunitz-type soybean trypsin inhibitor revisited: refined structure of its complex with porcine trypsin reveals an insight into the interaction between a homologous inhibitor from Erythrina caffra and tissue-type plasminogen activator. J. Mol. Biol. 1998, 275:347-363.
53. Teles R.C., de Souza E.M., Calderon Lde A., de Freitas S.M. Purification and pH stability characterization of a chymotrypsin inhibitor from Schizolobium parahyba seeds. Phytochemistry 2004, 65:793-799.
54. Hansen D., Macedo-Ribeiro S., Verissimo P., Yoo Im S., Sampaio M.U., Oliva M.L. Crystal structure of a novel cysteinless plant Kunitz-type protease inhibitor. Biochem. Biophys. Res. Commun. 2007, 360:735-740.
55. Onesti S., Brick P., Blow D.M. Crystal structure of a Kunitz-type trypsin inhibitor from Erythrina caffra seeds. J. Mol. Biol. 1991, 217:153-176.
56. Laskowski M., Qasim M.A. What can the structures of enzyme-inhibitor complexes tell us about the structures of enzyme substrate complexes?. Biochim. Biophys. Acta 2000, 1477:324-337.
57. Otlewski J., Jaskolski M., Buczek O., Cierpicki T., Czapinska H., Krowarsch D., Smalas A.O., Stachowiak D., Szpineta A., Dadlez M. Structure-function relationship of serine protease-protein inhibitor interaction. Acta Biochim. Pol. 2001, 48:419-428.
58. Navia M.A., McKeever B.M., Springer J.P., Lin T.Y., Williams H.R., Fluder E.M., Dorn C.P., Hoogsteen K. Structure of human neutrophil elastase in complex with a peptide chloromethyl ketone inhibitor at 1.84-A resolution. Proc. Natl. Acad. Sci. U S A 1989, 86:7-11.
59. Liao H., Ren W., Kang Z., Jiang J.H., Zhao X.J., Du L.F. A trypsin inhibitor from Cassia obtusifolia seeds: isolation, characterization and activity against Pieris rapae. Biotechnol. Lett. 2007, 29:653-658.
60. Dattagupta J.K., Podder A., Chakrabarti C., Sen U., Mukhopadhyay D., Dutta S.K., Singh M. Refined crystal structure (2.3 A) of a double-headed winged bean alpha-chymotrypsin inhibitor and location of its second reactive site. Proteins 1999, 35:321-331.
61. Srinivasan A., Giri A.P., Harsulkar A.M., Gatehouse J.A., Gupta V.S. A Kunitz trypsin inhibitor from chickpea (Cicer arietinum L.) that exerts anti-metabolic effect on podborer (Helicoverpa armigera) larvae. Plant Mol. Biol. 2005, 57:359-374.
62. Khamrui S., Dasgupta J., Dattagupta J.K., Sen U. Single mutation at P1 of a chymotrypsin inhibitor changes it to a trypsin inhibitor: X-ray structural (2.15 A) and biochemical basis. Biochim. Biophys. Acta 2005, 1752:65-72.
63. Souza E.M., Mizuta K., Sampaio M.U., Sampaio C.A. Purification and partial characterization of a Schizolobium parahyba chymotrypsin inhibitor. Phytochemistry 1995, 39:521-525.
64. Kouzuma Y., Suetake M., Kimura M., Yamasaki N. Isolation and primary structure of proteinase inhibitors from Erythrina variegata (Linn.) var. Orientalis seeds. Biosci. Biotechnol. Biochem. 1992, 56:1819-1824.
65. Macedo M.L., de Matos D.G., Machado O.L., Marangoni S., Novello J.C. Trypsin inhibitor from Dimorphandra mollis seeds: purification and properties. Phytochemistry 2000, 54:553-558.
66. Heussen-Schemmer C., Merrifield E.H., Dowdle E.B. The Erythrina protease inhibitor: interactions with tissue plasminogen activator. Thromb. Haemost. 1991, 66:226-231.
67. Neuhof C., Oliva M.L., Maybauer D., Maybauer M., de Oliveira C., Sampaio M.U., Sampaio C.A., Neuhof H. Effect of plant Kunitz inhibitors from Bauhinia bauhinioides and Bauhinia rufa on pulmonary edema caused by activated neutrophils. Biol. Chem. 2003, 384:939-944.
68. Gianotti A., Rios W.M., Soares-Costa A., Nogaroto V., Carmona A.K., Oliva M.L., Andrade S.S., Henrique-Silva F. Recombinant expression, purification, and functional analysis of two novel cystatins from sugarcane (Saccharum officinarum). Protein Expr. Purif. 2006, 47:483-489.
69. Otto H.H., Schirmeister T. Cysteine proteases and their inhibitors. Chem. Rev. 1997, 97:133-171.
70. Chye M., Sin S., Xu Z., Yeung E. Serine proteinase inhibitor proteins: exogenous and endogenous functions. In Vitro Cell. Dev. Biol. Plant 2006, 42:100-108.
71. Bhattacharyya A., Mazumdar Leighton S., Babu C.R. Bioinsecticidal activity of Archidendron ellipticum trypsin inhibitor on growth and serine digestive enzymes during larval development of Spodoptera litura. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2007, 145:669-677.
72. Giri A.P., Harsulkar A.M., Ku M.S., Gupta V.S., Deshpande V.V., Ranjekar P.K., Franceschi V.R. Identification of potent inhibitors of Helicoverpa armigera gut proteinases from winged bean seeds. Phytochemistry 2003, 63:523-532.
73. Inanaga H., Kobayasi D., Kouzuma Y., Aoki-Yasunaga C., Iiyama K., Kimura M. Protein engineering of novel proteinase inhibitors and their effects on the growth of Spodoptera exigua larvae. Biosci. Biotechnol. Biochem. 2001, 65:2259-2264.
74. Soares-Costa A., Beltramini L.M., Thiemann O.H., Henrique-Silva F. A sugarcane cystatin: recombinant expression, purification, and antifungal activity. Biochem. Biophys. Res. Commun. 2002, 296:1194-1199.
75. Garcia V.A., Freire M.G., Novello J.C., Marangoni S., Macedo M.L. Trypsin inhibitor from Poecilanthe parviflora seeds: purification, characterization, and activity against pest proteases. Protein J. 2004, 23:343-350.
76. Koiwa H., Shade R.E., Zhu-Salzman K., D'Urzo M.P., Murdock L.L., Bressan R.A., Hasegawa P.M. A plant defensive cystatin (soyacystatin) targets cathepsin L-like digestive cysteine proteinases (DvCALs) in the larval midgut of western corn rootworm (Diabrotica virgifera virgifera). FEBS Lett. 2000, 471:67-70.
77. Ramos V.S., Silva G.S., Freire M.G.M., Machado O.L., Parra J.R., Macedo M.L. Purification and characterization of a trypsin inhibitor from Plathymenia foliolosa seeds. J. Agric. Food Chem. 2008, 56:11348-11355.
78. Oppert B., Morgan T.D., Culbertson C., Kramer K.J. Dietary mixtures of cysteine and serine proteinase inhibitors exhibit synergistic toxicity toward the red flour beetle, Tribolium castaneum. Comp. Biochem. Physiol. 1993, 105C:379-385.
79. Oliveira A.S., Migliolo L., Aquino R.O., Ribeiro J.K., Macedo L.L., Andrade L.B., Bemquerer M.P., Santos E.A., Kiyota S., de Sales M.P. Purification and characterization of a trypsin-papain inhibitor from Pithecelobium dumosum seeds and its in vitro effects towards digestive enzymes from insect pests. Plant Physiol. Biochem. 2007, 45:858-865.
80. Valueva T.A., Revina T.A., Kladnitskaya G.V., Mosolov V.V. Kunitz-type proteinase inhibitors from intact and Phytophthora-infected potato tubers. FEBS Lett. 1998, 426:131-134.
81. De Leo F., Gallerani R. The mustard trypsin inhibitor 2 affects the fertility of Spodoptera littoralis larvae fed on transgenic plants. Insect Biochem. Mol. Biol. 2002, 32:489-496.
82. Gatehouse A.M., Norton E., Davison G.M., Babbe S.M., Newell C.A., Gatehouse J.A. Digestive proteolytic activity in larvae of tomato moth, Lacanobia oleracea; effects of plant protease inhibitors in vitro and in vivo. J. Insect Physiol. 1999, 45:545-558.
83. Haq S.K., Atif S.M., Khan R.H. Protein proteinase inhibitor genes in combat against insects, pests, and pathogens: natural and engineered phytoprotection. Arch. Biochem. Biophys. 2004, 431:145-159.
84. Huang B., Ng T.B., Fong W.P., Wan C.C., Yeung H.W. Isolation of a trypsin inhibitor with deletion of N-terminal pentapeptide from the seeds of Momordica cochinchinensis, the Chinese drug mubiezhi. Int. J. Biochem. Cell Biol. 1999, 31:707-715.
85. Khalf M., Goulet C., Vorster J., Brunelle F., Anguenot R., Fliss I., Michaud D. Tubers from potato lines expressing a tomato Kunitz protease inhibitor are substantially equivalent to parental and transgenic controls. Plant Biotechnol. J. 2009, 8:155-169.
86. Telang M., Srinivasan A., Patankar A., Harsulkar A., Joshi V., Damle A., Deshpande V., Sainani M., Ranjekar P., Gupta G., Birah A., Rani S., Kachole M., Giri A., Gupta V. Bitter gourd proteinase inhibitors: potential growth inhibitors of Helicoverpa armigera and Spodoptera litura. Phytochemistry 2003, 63:643-652.
87. Telang M.A., Giri A.P., Pyati P.S., Gupta V.S., Tegeder M., Franceschi V.R. Winged bean chymotrypsin inhibitors retard growth of Helicoverpa armigera. Gene 2009, 431:80-85.
88. Zavala J.A., Patankar A.G., Gase K., Hui D., Baldwin I.T. Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiol. 2004, 134:1181-1190.
89. Batista I.F., Nonato M.C., Bonfadini M.R., Beltramini L.M., Oliva M.L., Sampaio M.U., Sampaio C.A., Garratt R.C. Preliminary crystallographic studies of EcTI, a serine proteinase inhibitor from Enterolobium contortisiliquum seeds. Acta Crystallogr. D Biol. Crystallogr. 2001, 57:602-604.
90. De Meester P., Brick P., Lloyd L.F., Blow D.M., Onesti S. Structure of the Kunitz-type soybean trypsin inhibitor (STI): implication for the interactions between members of the STI family and tissue-plasminogen activator. Acta Crystallogr. D Biol. Crystallogr. 1998, 54:589-597.
91. McCoy A.J., Kortt A.A. The 1.8 A crystal structure of winged bean albumin 1, the major albumin from Psophocarpus tetragonolobus (L.) DC. J. Mol. Biol. 1997, 269:881-891.
92. Polikarpov I., Golubev A.M., Perles L.A., Pando S.C., Novello J.C., Marangoni S. Purification, crystallization and preliminary crystallographic study of a Kunitz-type trypsin inhibitor from Delonix regia seeds. Acta Crystallogr. D Biol. Crystallogr. 1999, 55:1611-1613.
93. Ravichandran S., Sen U., Chakrabarti C., Dattagupta J.K. Cryocrystallography of a Kunitz-type serine protease inhibitor: the 90 K structure of winged bean chymotrypsin inhibitor (WCI) at 2.13 A resolution. Acta Crystallogr. D Biol. Crystallogr. 1999, 55:1814-1821.
94. Iwanaga S., Yamasaki N., Kimura M., Kouzuma Y. Contribution of conserved Asn residues to the inhibitory activities of Kunitz-type protease inhibitors from plants. Biosci. Biotechnol. Biochem. 2005, 69:220-223.
95. Speransky A.S., Cimaglia F., Krinitsina A.A., Poltronieri P., Fasano P., Bogacheva A.M., Valueva T.A., Halterman D., Shevelev A.B., Santino A. Kunitz-type protease inhibitors group B from Solanum palustre. Biotechnol. J. 2007, 2:1417-1424.
96. Das S., Mukhopadhyay P. Protease inhibitors in chemoprevention of cancer. An overview. Acta Oncol. 1994, 33:859-865.
97. Ohba H., Nishikawa M., Kimura M., Yamasaki N., Moriwaki S., Itoh K. Cytotoxicity induced by Erythrina variegata serine proteinase inhibitors in tumor hematopoietic stem cell lines. Biosci. Biotechnol. Biochem. 1998, 62:1166-1170.
98. Troncoso M.F., Biron V.A., Longhi S.A., Retegui L.A., Wolfenstein-Todel C. Peltophorum dubium and soybean Kunitz-type trypsin inhibitors induce human Jurkat cell apoptosis. Int. Immunopharmacol 2007, 7:625-636.
99. Ye X., Ng T.B. A trypsin-chymotrypsin inhibitor with antiproliferative activity from small glossy black soybeans. Planta Med. 2009, 75:550-556.
100. Mello G.C., Desouza I.A., Mariano N.S., Ferreira T., Macedo M.L., Antunes E. Mechanisms involved in the rat peritoneal leukocyte migration induced by a Kunitz-type inhibitor isolated from Dimorphandra mollis seeds. Toxicon 2009, 53:323-329.
101. Asztalos B.F., Schaefer E.J., Horvath K.V., Cox C.E., Skinner S., Gerrior J., Gorbach S.L., Wanke C. Protease inhibitor-based HAART, HDL, and CHD-risk in HIV-infected patients. Atherosclerosis 2006, 184:72-77.
102. Cheung A.H., Wong J.H., Ng T.B. Trypsin-chymotrypsin inhibitors from Vigna mungo seeds. Protein Pept. Lett. 2009, 16:277-284.
103. Fanga E.F., Wong J.H., Ng T.B. Thermostable Kunitz trypsin inhibitor with cytokine inducing, antitumor and HIV-1 reverse transcriptase inhibitory activities from Korean large black soybeans. J. Biosci. Bioeng. 2010, 109:211-217.
104. Yeni P. Update on HAART in HIV. J. Hepatol. 2006, 44:S100-S103.
105. Wang H.X., Ng T.B. Concurrent isolation of a Kunitz-type trypsin inhibitor with antifungal activity and a novel lectin from Pseudostellaria heterophylla roots. Biochem. Biophys. Res. Commun. 2006, 342:349-353.
106. Liener I.E. Implications of antinutritional components in soybean foods. Crit. Rev. Food Sci. Nutr. 1994, 34:31-67.
107. Silva M.R., Silva M.A.A.P. Fatores antinutricionais: inibidores de proteases electinas. Rev. Nutr. 2000, 13:3-9.
108. Falco M.C., Silva-Filho M.C. Expression of soybean proteinase inhibitors in transgenic sugarcane plants: effects on natural defense against Diatraea saccharalis. Plant Physiol. Biochem. 2003, 41:761-766.
109. Habib H., Fazili K.M. Plant protease inhibitors: a defense strategy in plants. Biotech. Mol. Biol. Rev. 2007, 2:68-85.