Differences in substrate and inhibitor sequence specificity of human, mouse and rat tissue kallikreins

Biochemical Journal

Volumn 380, Issue 3, 2004, Pages 775-781

  Fogaça, Sandro E ^a   Melo, Robson L ^a   Pimenta, Daniel C ^a   Hosoi, Kazuo ^b   Juliano, Luiz ^a   Juliano, Maria A ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

Bradykinin; Fluorescent peptide; Inflammation; Inhibitor; Kallikrein; Protease

Indexed keywords

BIOSYNTHESIS; ENZYME INHIBITION; FLUORESCENCE; HYDROLYSIS; PARAMETER ESTIMATION; POLYPEPTIDES; REACTION KINETICS;

PREFERENTIAL HYDROLYSIS; SYNTHETIC PEPTIDES;

BIOCHEMISTRY;

2 AMINOBENZOYLMETHIONYLTHREONYLGLUTAMYLMETHIONYLALANYLARGINYLARGINYLPROLYLPROLYLGL YCYLPHENYLALANYLSERYLPROLYLPHENYLALANYLARGINYLSERYLVALYLTHREONYLVALYLGLUTAMINAMI DE; 2 AMINOBENZOYLMETHIONYLTHREONYLSERYLVALYLISOLEUCYLARGINYLARGINYLPROLYLPROLYLGLYCYL PHENYLALANYLSERYLPROLYLPHENYLALANYLARGINYLALANYLPROLYLARGINYLVALINAMIDE; ALANINE; ARGININE; BRADYKININ; BRADYKININ DERIVATIVE; BRADYKININ[1-8]; GLUTAMINE; KALLIKREIN; KALLIKREIN INHIBITOR; METHIONINE; PEPTIDE; PHENYLALANINE; RECEPTOR; SERINE; UNCLASSIFIED DRUG; VALINE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CHEMICAL BOND; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME BINDING; ENZYME SPECIFICITY; ENZYME SUBSTRATE; FEMALE; FLUORESCENCE; HUMAN; HYDROLYSIS; KINETICS; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PARAMETER; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPECIES COMPARISON; TISSUE;

AMINO ACID SEQUENCE; ANIMALS; BRADYKININ; ENZYME INHIBITORS; FEMALE; FLUORESCENT DYES; HUMANS; HYDROLYSIS; KININS; MICE; MICE, INBRED ICR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PEPTIDES; RATS; SUBSTRATE SPECIFICITY; TISSUE KALLIKREINS;

ANIMALIA;

EID: 3042742025     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20031047     Document Type: Article

References (50)

1. Clements, J., Hooper, J., Dong, Y. and Harvey, T. (2001) The expanded human kallikrein (KLK) gene family: genomic organization, tissue-specific expression and potential functions. Biol. Chem. 382, 5-14
2. Bhoola, K. D., Figueroa, C. D. and Worthy, K. (1992) Bioregulation of kinins: kallikreins, kininogens, and kininases. Pharmacol. Rev. 44, 1-80
3. Evans, B. A., Drinkwater, C. C. and Richards, R. I. (1987) Mouse glandular kallikrein genes. Structure and partial sequence analysis of the kallikrein gene locus. J. Biol. Chem. 262, 8027-8034
4. Southard-Smith, M., Pierce, J. C. and MacDonald, R. J. (1994) Physical mapping of the rat tissue kallikrein family in two gene clusters by analysis of P1 bacteriophage clones. Genomics 22, 404-417
5. Harvey, T. J., Hooper, J. D., Myers, S. A., Stephenson, S. A., Ashworth, L. K. and Clements, J. A. (2000) Tissue-specific expression patterns and fine mapping of the human kallikrein (KLK) locus on proximal 19q13.4. J. Biol. Chem. 275, 37397-37406
6. Yousef, G. M., Chang, A., Scorilas, A. and Diamandis, E. P. (2000) Genomic organization of the human kallikrein gene family on chromosome 19q13.3-q13.4. Biochem. Biophys. Res. Commun. 276, 125-133
7. Rittenhouse, H. G., Finlay, J. A., Mikolajczyk, S. D. and Partin, A. W. (1998) Human Kallikrein 2 (hK2) and prostate-specific antigen (PSA): two closely related, but distinct, kallikreins in the prostate. Crit. Rev. Clin. Lab. Sci. 35, 275-368
8. Diamandis, E. P., Yousef, G. M., Luo, L. Y., Magklara, A. and Obiezu, C. V. (2000) The new human kallikrein gene family: implications in carcinogenesis. Trends Endocrinol. Metab. 11, 54-60
9. Olsson, A. Y. and Lundwall, A. (2002) Organization and evolution of the glandular kallikrein locus in Mus musculus. Biochem. Biophys. Res. Commun. 299, 305-311
10. Evans, B. A., Drinkwater, C. C. and Richards, R. I. (1987) Mouse glandular kallikrein genes. Structure and partial sequence analysis of the kallikrein gene locus. J. Biol. Chem. 262, 8027-8034
11. van Leeuwen, B. H., Evans, B. A., Tregear, G. W. and Richards, R. I. (1986) Mouse glandular kallikrein genes. Identification, structure, and expression of the renal kallikrein gene. J. Biol. Chem. 261, 5529-5535
12. Christiansen, S. C., Proud, D. and Cochrane, C. G. (1987) Detection of tissue kallikrein in the bronchoalveolar lavage fluid of asthmatic subjects. J. Clin. Invest. 79, 188-197
13. Proud, D., Togias, A., Naclerio, R. M., Crush, S. A., Norman, P. S. and Linchtenstein, L. M. (1983) Kinins are generated in vivo following nasal airway challenge of allergic individuals with allergen. J. Clin. Invest. 72, 1678-1685
14. Braumgarten, C. R., Nichols, R. C., Naclerio, R. M. and Proud, D. (1986) Concentrations of glandular kallikrein in human nasal secretions increase during experimentally induced allergic rhinitis. J. Immunol. 137, 1323-1328
15. MacDonald, R. J., Margolius, H. S. and Erdös, E. G. (1988) Molecular biology of tissue kallikrein. Biochem. J. 253, 313-321
16. Axen, R., Gross, E., Witkop, B., Pierce, J. V. and Webster, M. E. (1966) Release of kinin activity from human kininogens and fresh plasma by cyanogen bromide. Biochem. Biophys. Res. Commun. 5, 353-357
17. Alhenc-Gelas, F., Marchetti, J., Alegrini, J., Carod, P. and Menard, J. (1981) Measurement of urinary kallikrein activity. Species differences in kinin production. Biochim. Biophys. Acta 677, 477-488
18. Kato, H., Enjyoji, K., Miyata, T., Hayashi, I., Oh-ishi, S. and Iwagaga, S. (1985) Demonstration of arginyl-bradykinin moiety in rat HMW kininogen: direct evidence for liberation of bradykinin by rat glandular kallikreins. Biochem. Biophys. Res. Commun. 127, 289-295
19. Hosoi, K., Tsunasawa, S., Kurihara, K., Aoyama, H., Ueha, T., Murai, T. and Sakiyama, F. (1994) Identification of mK1, a true tissue (glandular) kallikrein of mouse submandibular gland: tissue distribution and a comparison of kinin-releasing activity with other submandibular kallikreins. J. Biochem. (Tokyo) 115, 137-143
20. 2- and COOH-terminal sequences and susceptibility to various glandular kallikreins. J. Biol. Chem. 265, 10030-10035
21. Emim, J. A. S., Souccar, C. A., Castro, M. S., Godinho, R. O., Cezari, M. H. S., Juliano, L. and Lapa, A. J. (2000) Evidence for activation of the tissue kallikrein-kinin system in nociceptive transmission and inflammatory responses of mice using a specific enzyme inhibitor. Br. J. Pharmacol. 130, 1099-1107
22. Meneton, P., Bloch-Faure, M., Hagege, A. A., Ruetten, H., Huang, W., Bergaya, S., Ceiler, D., Gehring, D., Martins, I., Salmon, G. et al. (2001) Cardiovascular abnormalities with normal blood pressure in tissue kallikrein-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 98, 2634-2639
23. Chao, J. and Chao, L. (1997) Experimental kallikrein gene therapy in hypertension, cardiovascular and renal diseases. Pharmacol. Res. 35, 517-522
24. Agata, J., Chao, L. and Chao, J. (2002) Kallikrein gene delivery improves cardiac reserve and attenuates remodeling after myocardial infarction. Hypertension 40, 653-659
25. Silva, Jr, J. A., Araújo, R. C., Baltatu, O., Oliveira, S. M., Tschope, C., Fink, E., Hoffmann, S., Plehm, R., Chai, K. X., Chao, L. et al. (2000) Reduced cardiac hypertrophy and altered blood pressure control in transgenic rats with the human tissue kallikrein gene. FASEB J. 14, 1858-1860
26. Reference deleted
27. Furuto-Kato, S., Matsumoto, A., Kitamura, N. and Nakanishi, S. (1985) Primary structures of the mRNAs encoding the rat precursors for bradykinin and T-kinin. Structural relationship of kininogens with major acute phase protein and α1-cysteine proteinase inhibitor. J. Biol. Chem. 260, 12054-12059
28. Melo, R. L., Alves, L. C., Del Nery, E., Juliano, L. and Juliano, M. A. (2001) Synthesis and hydrolysis by cysteine and serine proteases of short internally quenched fluorogenic peptides. Anal. Biochem. 293, 71-77
29. Pimenta, D. C., Juliano, M. A. and Juliano, L. (1997) Hydrolysis of somatostatin by human tissue kallikrein after the amino acid pair Phe-Phe. Biochem. J. 327, 27-30
30. Pimenta, D. C., Fogaça, S. E., Melo, R. L., Juliano, L. and Juliano, M. A. (2003) Specificity of S′1 and S′2 subsites of human tissue kallikrein using the reactive-centre loop of kallistatin: the importance of P′1 and P′2 positions in design of inhibitors. Biochem. J. 371, 1021-1025
31. Portaro, F. C., Cezari, M. H. S., Juliano, M. A., Juliano, L., Walmsley, A. R. and Prado, E. S. (1997) Design of kallidin-releasing tissue kallikrein inhibitors based on the specificities of the enzyme's binding subsites. Biochem. J. 323, 67-71
32. Hirata, I. Y., Cezari, M. H. S., Nakaie, C., Boschcov, P., Ito, A. S., Juliano, M. and Juliano, L. (1994) Internally quenched fluorogenic protease substrates: solid-phase synthesis and fluorescence spectroscopy of peptides containing orthoaminobenzoyl/dinitrophenyl groups as donor-acceptor pairs. Lett. Peptide Sci. 1, 299-308
33. Hosoi, K., Tanaka, I., Ishii, Y. and Ueha, T. (1983) A new esteroproteinase (proteinase F) from the submandibular gland of female mice. Biochim. Biophys. Acta 756, 163-170
34. Shimamoto, K., Chao, J. and Margolius, H. S. (1980) The radioimmunoassay of human urinary kallikrein and comparisons with kallikrein activity measurements. J. Endocrinol. Metab. 51, 840-848
35. El Moujahed, A., Brillard-Bourdet, M., Juliano, M. A., Moreau, T., Chagas, J. R., Gutman, N., Prado, E. S. and Gauthier, F. (1997) Kininogen-derived fluorogenic substrates for investigating the vasoactive properties of rat tissue kallikreins - identification of a T-kinin-releasing rat kallikrein. Eur. J. Biochem. 247, 652-658
36. Sampaio, C. A. M., Sampaio, M. U. and Prado, E. S. (1984) Active-site titration of horse urinary kallikrein. Hoppe Seyler's Z. Physiol. Chem. 365, 297-302
37. Wilkinson, G. N. (1961) Statistical estimations in enzyme kinetics. Biochem. J. 80, 324-332
38. Pimenta, D. C., Chao, J., Chao, L., Juliano, M. A. and Juliano, L. (1999) Specificity of human tissue kallikrein towards substrates containing Phe-Phe pair of amino acids. Biochem. J. 339, 473-479
39. Chen, Z. and Bode, W. (1983) Refined 2.5 Å X-ray crystal structure of the complex formed by porcine kallikrein A and the bovine pancreatic trypsin inhibitor. Crystallization, Patterson search, structure determination, refinement, structure and comparison with its components and with the bovine trypsin-pancreatic trypsin inhibitor complex. J. Mol. Biol. 164, 283-311
40. Araujo-Viel, M. S., Juliano, M. A., Oliveira, L. and Prado, E. S. (1988) Horse urinary kallikrein, II. Effect of subsite interactions on its catalytic activity. Biol. Chem. Hoppe Seyler 369, 397-401
41. Chagas, J. R., Portaro, F. C., Hirata, I. Y., Almeida, P. C., Juliano, M. A., Juliano, L. and Prado, E. S. (1995) Determinants of the unusual cleavage specificity of lysyl-bradykinin-releasing kallikreins. Biochem. J. 306, 63-69
42. Del Nery, E., Chagas, J. R., Juliano, M. A., Prado, E. S. and Juliano, L. (1995) Evaluation of the extent of the binding site in human tissue kallikrein by synthetic substrates with sequences of human kininogen fragments. Biochem. J. 312, 233-238
43. Del Nery, E., Chagas, J. R., Juliano, M. A., Juliano, L. and Prado, E. S. (1999) Comparison of human and porcine tissue kallikrein substrate specificities. Immunopharmacology 45, 151-157
44. Bourgeois, L., Brillard-Bourdet, M., Deperthes, D., Juliano, M. A., Juliano, L., Tremblay, R. R., Dube, J. Y. and Gauthier, F. (1977) Serpin-derived peptide substrates for investigating the substrate specificity of human tissue kallikreins hK1 and hK2. J. Biol. Chem. 272, 29590-29595
45. Del Nery, E., Juliano, M. A., Lima, A. P., Scharfstein, J. and Juliano, L. (1997) Kininogenase activity by the major cysteinyl proteinase (cruzipain) from Trypanosoma cruzi. J. Biol. Chem. 272, 25713-25718
46. Cordova, M., Jara, J., Del Nery, E., Hirata, I. Y., Araujo, M. S., Carmona, A. K., Juliano, M. A. and Juliano, L. (2001) Characterization of two cysteine prateinases secreted by Fasciola hepatica and demonstration of their kininogenase activity. Mol. Biochem. Parasitol. 116, 109-115
47. Chagas, J. R., Hirata, I. Y., Juliano, M. A., Xiong, W., Wang, C., Chao, J., Juliano, L. and Prado, E. S. (1992) Substrate specificities of tissue kallikrein and T-kininogenase: their possible role in kininogen processing. Biochemistry 31, 4969-4974
48. Fiedler, F. (1987) Effects of secondary interactions on the kinetics of peptide and peptide ester hydrolysis by tissue kallikrein and trypsin. Eur. J. Biochem. 163, 303-312
49. Melo, R. L., Barbosa-Pozzo, R. C., Pimenta, D. C., Perissutti, E., Caliendo, G., Santagada, V., Juliano, L. and Juliano, M. A. (2001) Human tissue kallikrein S1 subsite recognition of non-natural basic amino acids. Biochemistry 40, 5226-5232
50. Okada, Y., Tsuda, Y., Tada, M., Wanaka, K., Hijikata-Okunomiya, A., Okamoto, U. and Okamoto, S. (1999) Development of plasma kallikrein selective inhibitors. Biopolymers 51, 41-50