S1′ and S2′ subsite specificities of human plasma kallikrein and tissue kallikrein 1 for the hydrolysis of peptides derived from the bradykinin domain of human kininogen

Biological Chemistry

Volumn 389, Issue 12, 2008, Pages 1487-1494

  Lima, Aurelio Resende ^a   Alves, Fabiana M ^a   Ângelo, Pedro Francisco ^a   Andrade, Douglas ^a   Blaber, Sachiko I ^b   Blaber, Michael ^b   Juliano, Luiz ^a   Juliano, Maria Aparecida ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b FLORIDA STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Bradykinin; Kinin; Peptidase; Peptides; Phosphorylation; Protease

Indexed keywords

ARGININE; BETA 1 ADRENERGIC RECEPTOR; BRADYKININ; KININOGEN; LYSINE; METHIONINE; PHENYLALANINE; PLASMA KALLIKREIN; SERINE; TISSUE KALLIKREIN; TISSUE KALLIKREIN 1; UNCLASSIFIED DRUG; ANTHRANILIC ACID DERIVATIVE; KININ; PEPTIDE; RECOMBINANT PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL BOND; ENZYME SPECIFICITY; HUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN PHOSPHORYLATION; CHEMISTRY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HYDROLYSIS; KINETICS; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION;

AMINO ACID SEQUENCE; ANTHRANILIC ACIDS; BRADYKININ; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; HYDROLYSIS; KINETICS; KININOGENS; KININS; MOLECULAR SEQUENCE DATA; PEPTIDES; PHOSPHORYLATION; PLASMA KALLIKREIN; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY; TISSUE KALLIKREINS;

EID: 57649128315     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2008.166     Document Type: Article

References (55)

1. Almeida, P.C., Chagas, J.R., Cezari, M.H.S., Juliano, M.A., and Juliano, L. (2000). Hydrolysis by plasma kallikrein of fluorogenic peptides derived from prorenin processing site. Biochem. Biophys. Acta 1479, 83-90.
2. Ângelo, P.F., Lima, A.R., Alves, F.M., Blaber, S.I., Scarisbrick, I.A., Blaber, M., Juliano, L., and Juliano, M.A. (2006). Substrate specificity of human kallikrein 6: salt and glycosaminoglycan activation effects. J. Biol. Chem. 281, 3116-3126.
3. Babiker, A.A., Ronquist, G., Nilsson, B., and Ekdahl, K.N. (2006). Overexpression of ecto-protein kinases in prostasomes of metastatic cell origin. Prostate 66, 675-686.
4. Bhoola, K.D., Figueroa, C.D., and Worthy, K. (1992). Bioregulation of kinins: kallikreins, kininogens, and kininases. Pharmacol. Rev. 44, 1-80.
5. Blom, N., Gammeltoft, S., and Brunak, S. (1999). Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J. Mol. Biol. 294, 1351-1362.
6. Bourgeois, L., Brillard-Bourdet, M., Deperthes, D., Juliano, M.A., Juliano, L., Tremblay, R.R., Dubé, J.Y., and Gauthier, F. (1997). Serpin-derived peptide substrates for investigating the substrate specificity of human tissue kallikreins hK1 and hK2. J. Biol. Chem. 272, 29590-29595.
7. Chagas, J.R., Juliano, L., and Prado, E.S. (1991). Intramolecularly quenched fluorogenic tetrapeptide substrates for tissue and plasma kallikreins. Anal. Biochem. 192, 419-425.
8. Chagas, J.R., Portaro, F.C.V., 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.
9. 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.
10. 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.
11. Diamandis, E.P., Yousef, G.M., Clements, J., Ashworth, L.K., Yoshida, S., Egelrud, T., Nelson, P.S., Shiosaka, S., Little, S., Lilja, H., et al. (2000). New nomenclature for the human tissue kallikrein gene family. Clin. Chem. 46, 1855-1858.
12. Diamandis, E.P., Yousef, G.M., and Olsson, Y. (2004). An update on human and mouse glandular kallikreins. Clin. Chem. 37, 258-260.
13. Ekdahl, K.N. and Nilsson, B. (1999). Phosphorylation of plasma proteins with emphasis on complement component C3. Mol. Immunol. 36, 233-239.
14. Fiedler, F. and Hinz, H. (1992). Kinetics of bond cleavages at kallidin release by tissue kallikrein: cleavage of two peptide bonds in a single enzyme-substrate complex? Agents Actions 38 (Suppl. 1), 82-88.
15. Fiedler, F., Hinz, H., and Lottspeich, F. (1986). Individual reaction steps in the release of kallidin from kininogen by tissue kallikrein. Adv. Exp. Med. Biol. 198 (Part A), 283-289.
16. Fogaça, S.E., Melo, R.L., Pimenta, D.C., Hosoi, K., Juliano, L., and Juliano, M.A. (2004). Differences in substrate and inhibitor sequence specificity of human, mouse and rat tissue kallikreins. Biochem. J. 380, 775-781.
17. Gosalia, D.N., Salisbury, C.M., Ellman, J.A., and Diamond, S.L. (2005). High throughput substrate specificity profiling of serine and cysteine proteases using solution-phase fluorogenic peptide microarrays. Mol. Cell. Proteomics 4, 626-636.
18. Hirata, I., Cezari, M.H.C., Nakaie, C.R., Boshcov, P., Ito, A.S., Juliano, M.A., and Juliano, L. (1994). Internally quenched fluorogenic protease substrates: solid-phase synthesis and fluorescence spectroscopy of peptides containing ortho-aminobenzoyl/dinitrophenyl groups as donor-acceptor pairs. Lett. Peptide Sci. 1, 299-308.
19. Hjerrild, M. and Gammeltoft, S. (2006). Phosphoproteomics toolbox: computational biology, protein chemistry and mass spectrometry. FEBS Lett. 580, 4764-4770.
20. Iakoucheva, L.M., Radivojac, P., Brown, C.J., O'Connor, T.R., Sikes, J.G., Obradovic, Z., and Dunker, A.K. (2004). The importance of intrinsic disorder for protein phosphorylation. Nucleic Acids Res. 32, 1037-1049.
21. Jameson, G.W., Roberts, D.V., Adams, R.W., Kyle, W.S.A., and Elmore, D.T. (1973). Determination of the operational molarity of solutions of bovine α-chymotrypsin, trypsin, thrombin and factor Xa by spectrofluorimetric titration. Biochem. J. 131, 107-117.
22. Kaplan, A.P., Joseph, K., and Silverberg, M. (2002). Pathways for bradykinin formation and inflammatory disease. J. Allergy Clin. Immunol. 109, 195-209.
23. Katz, B.A., Liu, B., Barnes, M., and Springman, E.B. (1998). Crystal structure of recombinant human tissue kallikrein at 2.0 Å resolution. Protein Sci. 7, 875-885.
24. Kitamura, N., Kitagawa, H., Fukushima, D., Takagaki, Y., Miyata, T., and Nakanishi, S. (1985). Structural organization of the human kininogen gene and a model for its evolution. J. Biol. Chem. 260, 8610-8617.
25. Kobe, B., Kampmann, T., Forwood, J.K., Listwan, P., and Brinkworth, R.I. (2005). Substrate specificity of protein kinases and computational prediction of substrates. Biochim. Biophys. Acta 1754, 200-209.
26. Laxmikanthan, G., Blaber, S.I., Bernett, M.J., Scarisbrick, I.A., Juliano, M.A., and Blaber, M. (2005). 1.70 Å X-ray structure of human apo kallikrein 1: structural changes upon peptide inhibitor/substrate binding. Proteins Struct. Funct. Bioinformatics 58, 802-814.
27. Leatherbarrow, R.J. (1992). Grafit Version 3.0 (Staines, UK: Erithacus Software).
28. Li, T., Li, F., and Zhang, X. (2008). Prediction of kinase-specific phosphorylation sites with sequence features by a log-odds ratio approach. Proteins Struct. Funct. Bioinformatics 70, 404-414.
29. Marcondes, S. and Antunes, E. (2005). The plasma and tissue kininogen-kallikrein-kinin system: role in the cardiovascular system. Curr. Med. Chem. Cardiovasc. Hematol. Agents 3, 33-44.
30. Melo, R.L., Alves, L.C., Del Nery, E., Juliano, L., and Juliano, M.A. (2001a). Synthesis and hydrolysis by cysteine and serine proteases of short internally quenched fluorogenic peptides. Anal. Biochem. 293, 71-77.
31. Melo, R.L., Barbosa-Pozzo, R.C., Pimenta, D.C., Perissutti, E., Caliendo, G., Santagada, V., Juliano, L., and Juliano, M.A. (2001b). Human tissue kallikrein S1 subsite recognition of non-natural basic amino acids. Biochemistry 40, 5226-5232.
32. Mueller-Esterl, W., Rauth, G., Lottspeich, F., Kellermann, J., and Henschen, A. (1985). Limited proteolysis of human low-molecular-mass kininogen by tissue kallikrein. Isolation and characterization of the heavy and the light chains. Eur. J. Biochem. 149, 15-22.
33. Obenauer, J.C., Cantley, L.C., and Yaffe, M.B. (2003). Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs. Nucleic Acids Res. 31, 3635-3641.
34. Oliva, M.L.V., Grisolia, D., and Sampaio, M.U. (1982). Properties of highly purified human plasma kallikrein. Agents Actions 9 (Suppl.), 52-57.
35. Oliva, M.L., Sampaio, M.U., and Sampaio, C.A. (1987). Serine and SH-proteinase inhibitors from Enterolobium contortisiliquum beans. Braz. J. Med. Biol. Res. 20, 767-770.
36. Oliveira, E.B., Souza, L.L., Sivieri, D.O. Jr., Bispo-da-Silva, L.B., Pereira, H.J., Costa-Neto, C.M., Sousa, M.V., and Salgado, M.C. (2007). Carboxypeptidase B and other kininases of the rat coronary and mesenteric arterial bed perfusates. Am. J. Physiol. Heart Circ. Physiol. 293, H3550-H3557.
37. 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.
38. 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.
39. 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.
40. 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.
41. Qin, H., Kemp, J., Yip, M., Lam-Po-Tang, P.R.L., and Morris, B.J. (1991). Localization of human glandular kallikrein-1 gene to chromosome 19q13.3-13.4 by in situ hybridization. Hum. Hered. 41, 222-226.
42. Redegeld, F.A., Caldwell, C.C., and Sitkovsky, M.V. (1999). Ectoprotein kinases: ecto-domain phosphorylation as a novel target for pharmacological manipulation? Trends Pharmacol. Sci. 20, 453-459.
43. Riegman, P.H., Vlietstra, R.J., Suurmeijer, L., Cleutjens, C.B., and Trapman, J. (1992). Characterization of the human kallikrein locus. Genomics 14, 6-11.
44. Sainz, I.M., Pixley, R.A., and Colman, R.W. (2007). Fifty years of research on the plasma kallikrein-kinin system: from protein structure and function to cell biology and in-vivo pathophysiology. Thromb. Haemost. 98, 77-83.
45. Schechter, I. and Berger, A. (1967). On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27, 157-162.
46. Schmaier, A.H. (2008). Assembly, activation, and physiologic influence of the plasma kallikrein/kinin system. Int. Immunopharmacol. 8, 161-165.
47. Schmaier, A.H. and McCrae, K.R. (2007). The plasma kallikreinkinin system: its evolution from contact activation. J. Thromb. Haemost. 5, 2323-2329.
48. Takagaki, Y., Kitamura, N., and Nakanishi, S. (1985). Cloning and sequence analysis of cDNAs for human high molecular weight and low molecular weight prekininogens. Primary structures of two human prekininogens. J. Biol. Chem. 260, 8601-8609.
49. Tang, J., Yu, C.L., Williams, S.R., Springman, E., Jeffery, D., Sprengeler, P.A., Estevez, A., Sampang, J., Shrader, W., Spencer, J., et al. (2005). Expression, crystallization, and three-dimensional structure of the catalytic domain of human plasma kallikrein. J. Biol. Chem. 280, 41077-41089.
50. Ubersax, J.A. and Ferrel, J.E. Jr. (2007). Mechanisms of specificity in protein phosphorylation. Nat. Rev. Mol. Cell Biol. 8, 530-541.
51. Xue, Y., Fengfeng, F., Zhu, M., Chen, G., and Yao, X. (2005). GPS: a comprehensive www server for phosphorylation sites prediction. Nucleic Acids Res. 33, W184-W187.
52. Yousef, G.M. and Diamandis, E.P. (2001). The new human tissue kallikrein gene family: structure, function, and association to disease. Endocr. Rev. 22, 184-204.
53. Zhang, J., Krishnan, R., Arnold, C.S., Mattsson, E., Kilpatrick, J.M., Bantia, S., Dehghani, A., Boudreaux, B., Gupta, S.N., Kotian, P.L., et al. (2006). Discovery of highly potent small molecule kallikrein inhibitors. Med. Chem. 2, 545-553.
54. Zhou, F.F., Xue, Y., Chen, G.L., and Yao, X. (2004). GPS: a novel group-based phosphorylation predicting and scoring method. Biochem. Biophys. Res. Commun. 325, 1443-1448.
55. Zhou, L., Li-Ling, J., Huang, H., Ma, F., and Li, Q. (2008). Phylogenetic analysis of vertebrate kininogen genes. Genomics 91, 129-141.