Substrate specificity of kallikrein-related peptidase 13 activated by salts or glycosaminoglycans and a search for natural substrate candidates

Biochimie

Volumn 93, Issue 10, 2011, Pages 1701-1709

  Andrade, Douglas ^a   Assis, Diego M ^a   Santos, Jorge A N ^a   Alves, Fabiana M ^a   Hirata, Izaura Y ^a   Araujo, Mariana S ^a   Blaber, Sachiko I ^b   Blaber, Michael ^b   Juliano, Maria A ^a   Juliano, Luiz ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

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

Author keywords

Histatins; Kinin; Kosmotropic salts; Myelin basic protein; Protease

Indexed keywords

GLYCOSAMINOGLYCAN; HISTATIN; HISTATIN 3; KALLIKREIN 13; MYELIN BASIC PROTEIN; SODIUM CHLORIDE; UNCLASSIFIED DRUG;

ALKALINITY; AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME SUBSTRATE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HYDROLYSIS; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN LOCALIZATION; SALIVARY GLAND; TESTIS;

CITRATES; ENZYME ACTIVATION; FEMALE; GLYCOSAMINOGLYCANS; HUMANS; KALLIKREINS; MALE; SALIVARY GLANDS; SALTS; SUBSTRATE SPECIFICITY;

PRIMATES;

EID: 80052079878     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2011.05.037     Document Type: Article

References (61)

1. G.M. Yousef, L.Y. Luo, S.W. Scherer, G. Sotiropoulou, and E.P. Diamandis Molecular characterization of Zyme/Protease M/Neurosin (PRSS9), a hormonally regulated kallikrein-like serine protease Genomics 62 1999 251 259 (Pubitemid 30053941)
2. C.A. Borgoño, and E.P. Diamandis The emerging roles of human tissue kallikreins in cancer Nat. Rev. Cancer 4 2004 876 890 (Pubitemid 39472954)
3. T.J. Harvey, J.D. Hooper, S.A. Myers, S.A. Stephenson, L.K. Ashworth, and J.A. Clements Tissue-specific expression patterns and fine mapping of the human kallikrein (KLK) locus on proximal 19q13.4 J. Biol. Chem. 275 2000 35397 35406
4. G.M. Yousef, and E.P. Diamandis The new human tissue kallikrein gene family: structure, function and association to disease Endocr. Rev. 22 2001 184 204 (Pubitemid 32458158)
5. C.A. Borgoño, I.P. Michael, and E.P. Diamandis Human tissue kallikreins: physiologic roles and applications in cancer Mol. Cancer Res. 2 2004 257 280 (Pubitemid 39031076)
6. K. Oikonomopoulou, E.P. Diamandis, and M.D. Hollenberg Kallikrein-related peptidases: proteolysis and signaling in cancer, the new frontier Biol. Chem. 391 2010 299 310
7. A. Lundwall, and M. Brattsand Kallikrein-related peptidases Cell Mol. Life Sci. 65 2008 2019 2038
8. C.D. Petraki, V.N. Karavana, and E.P. Diamandis Human kallikrein 13 expression in normal tissues: an immunohistochemical study J. Histochem. Cytochem. 51 2003 493 501 (Pubitemid 36418045)
9. C.D. Petraki, P.A. Papanastasiou, V.N. Karavana, and E.P. Diamandis Cellular distribution of human tissue kallikreins: immunohistochemical localization Biol. Chem. 387 2006 653 663 (Pubitemid 43964787)
10. J.L.V. Shaw, and E.P. Diamandis Distribution of 15 human kallikreins in tissues and biological fluids Clin. Chem. 53 2007 1423 1432 (Pubitemid 47206338)
11. K.D. Bhoola, C.D. Figueroa, and K. Worthy Bioregulation of kinins-kallikreins, kininogens, and kininases Pharmcol. Rev. 44 1922 1 80
12. H. Lilja A kallikrein-like serine protease in prostatic fluid cleaves the predominant seminal vesicle protein J. Clin. Invest. 76 1985 1899 1903 (Pubitemid 16196061)
13. (2+), a tight-binding inhibitor Prostate 45 2000 132 139
14. T.K. Takayama, B.A. McMullen, P.S. Nelson, M. Matsumura, and K. Fujikawa Characterization of hK4 (Prostase), a prostate-specific serine protease: activation of the precursor of prostate specific antigen (pro-PSA) and single-chain urokinase-type plasminogen activator and degradation of prostatic acid phosphatase Biochemistry 40 2001 15341 15348 (Pubitemid 33151949)
15. M. Matsumura, A.S. Bhatt, D. Andress, N. Clegg, T.K. Takayama, C.S. Craik, and P.S. Nelson Substrates of the prostate-specific serine protease Prostase/KLK4 defined by positional-scanning peptide libraries Prostate 62 2005 1 13 (Pubitemid 39614288)
16. M. Debela, V. Magdolen, V. Grimminger, C. Sommerhoff, A. Messerschimidt, R. Huber, R. Friedrich, W. Bode, and P. Goettig Crystal structures of human tissue kallikrein 4: activity modulation by a specific zinc binding site J. Mol. Biol. 362 2006 1094 1107 (Pubitemid 44382693)
17. Y. Lu, P. Papagerakis, Y. Yamakoshi, J.C.-C. Hu, J.D. Bartlett, and J.P. Simmer Functions of KLK4 and MMP-20 in dental enamel formation Biol. Chem. 389 2008 695 700 (Pubitemid 352009413)
18. P.F. Ângelo, A.R. Lima, F.M. Alves, S.I. Blaber, I.A. Scarisbrick, M. Blaber, L. Juliano, and M.A. Juliano Substrate specificity of human kallikrein 6: salt and glycosaminoglycan activation effects J. Biol. Chem. 281 2006 3116 3126 (Pubitemid 43845921)
19. I.A. Scarisbrick, S.I. Blaber, J.T. Tingling, M. Rodriguez, M. Blaber, and G.P. Christophi Potential scope of action of tissue kallikreins in CNS immune-mediated disease J. Neuroimmunol. 178 2006 67 176
20. A.G. Vandell, N. Larson, G. Laxmikanthan, M. Panos, S.I. Blaber, M. Blaber, and I.A. Scarisbrick Protease-activated receptor dependent and independent signaling by kallikreins 1 and 6 in CNS neuron and astroglial cell lines J. Neurochem. 107 2008 855 870
21. K. Oikonomopoulou, K.K. Hansen, M. Saifeddine, I. Tea, M. Blaber, S.I. Blaber, I. Scarisbrick, P. Andrade-Gordon, G.S. Cottrell, N.W. Bunnett, E.P. Diamandis, and M.D. Hollenberg Proteinase-activated receptors, targets for kallikrein signaling J. Biol. Chem. 281 2006 32095 32112 (Pubitemid 46036764)
22. M.J. Bernett, S.I. Blaber, I.A. Scarisbrick, P. Dhanarajan, S.M. Thompson, and M. Blaber Crystal structure and biochemical characterization of human kallirein 6 reveals that a trypsin-like kallikrein is expressed in the central nervous system J. Biol. Chem. 277 2002 24562 24570 (Pubitemid 34951983)
23. G. Sotiropoulou, G. Pampalakis, and E.P. Diamandis Functional roles of human kallikrein-related peptidases J. Biol. Chem. 284 2009 32989 32994
24. A. Eissa, V. Amodeo, C.R. Smith, and E.P. Diamandis Kallikrein-related peptidase-8 (KLK8) is an active serine protease in human epidermis and sweat and is involved in a skin barrier proteolytic cascade J. Biol. Chem. 286 2011 687 706
25. N. Komatsu, K. Saijoh, T. Toyama, R. Ohka, N. Otsuki, G. Hussack, K. Takehara, and E.P. Diamandis Multiple tissue kallikrein mRNA and protein expression in normal skin and skin diseases Br. J. Dermatol. 153 2005 274 281 (Pubitemid 41228422)
26. A. Scolaris, C.A. Borgoño, N. Harbeck, J. Dorn, B. Schmalfelt, M. Schimitt, and E.P. Diamandis Human kallikrein 13 protein in ovarian cancer cytosols: a new favorable prognostic marker J. Clin. Oncol. 22 2004 678 685 (Pubitemid 41095071)
27. M.R. Darling, L. Jakson-Boeters, T.D. Daley, and E.P. Diamandis Human kallikrein 13 expresssion in salivary gland tumors Int. J. Biol. Markers 21 2006 106 110 (Pubitemid 44210039)
28. A. Chang, G.M. Yousef, K. Jung, E. Rajpert-De Meyts, and E.P. Diamandis Identification and molecular characterization of five novel kallikrein gene 13 (KLK13; KLK-L4) splice variants: differential expression in testicular cancer Anticancer Res. 21 2001 3147 3152 (Pubitemid 34224211)
29. L.-Y. Luo, G. Yousef, and E.P. Diamandis Human tissue kallikreins and testicular cancer Acta Pathol. Microbiol. Immunol. Scand. 111 2003 225 233 (Pubitemid 36566692)
30. C. Kapadia, M.C. Ghosh, L. Grass, and E.P. Diamandis Human kallikrein 13 involvement in extracellular matrix degradation Biochem. Biophys. Res. Comm. 323 2004 1084 1090 (Pubitemid 39243429)
31. C.A. Borgoño, J.A. Gavigan, J. Alves, B. Bowles, J.L. Harris, G. Sotiropoulou, and E.P. Diamandis Defining the extended substrate specificity of kallikrein 1-related peptidases Biol. Chem. 388 2007 1215 1225 (Pubitemid 350059617)
32. I. Schecheter, and A. Berger On the size of the active site in proteases. I. Papain Biochem. Biophys. Res. Comm. 27 1967 157 162
33. J.L. Harris, B.J. Backes, F. Leonetti, S. Mahrus, J.A. Ellman, and C.S. Craik Rapid and general profiling of protease specificity by using combinatorial fluorogenic substrate libraries Proc. Natl. Acad. Sci. U S A 97 2000 7754 7759 (Pubitemid 30460720)
34. B.J. Backes, J.L. Harris, F. Leonetti, C.S. Craik, and J.A. Ellman Synthesis of positional-scanning libraries of fluorogenic peptide substrates to define the extended substrate specificity of plasmin and thrombin Nat. Biotechnol. 18 2000 187 193 (Pubitemid 30091180)
35. X. Huang, C.T. Knoell, G. Frey, M. Hazegh-Azam, A.H. Tashjian, L. Hedstrom, R.H. Abeles, and S.N. Timasheff Modulation of recombinant human prostate-specific antigen: activation by Hofmeister salts and inhibition by azapeptides. Appendix: thermodynamic interpretation of the activation by concentrated salts Biochemistry 40 2001 11734 11741 (Pubitemid 32906035)
36. D. Andrade, D.M. Assis, A.R. Lima, J.R. Oliveira, M.S. Araujo, S.I. Blaber, M. Blaber, M.,A. Juliano, and L. Juliano Substrate specificity and inhibition of human kallikrein-related peptidase 3 (KLK3 or PSA) activated with sodium citrate and glycosaminoglycans Arch. Biochem. Biophys. 498 2010 74 82
37. E. Del Nery, J.R. Chagas, M.A. Juliano, E.S. Prado, and L. Juliano Evaluation of the extent of the binding site in human tissue kallikrein by synthetic substrates with sequences of human kininogen fragments Biochem. J. 312 1995 233 238
38. L.M. Sabatini, T. Ota, and E.A. Azen Nucleotide sequence analysis of the human salivary protein genes HIS1 and HIS2, and evolution of the STATH/HIS gene family Mol. Biol. Evol. 10 1993 497 511 (Pubitemid 23157235)
39. H. Tsai, and L.A. Bobek Human salivary histatins: promising anti-fungal therapeutic agents Crit. Rev. Oral Biol. Med. 9 1998 480 497 (Pubitemid 29402012)
40. E.J. Helmerhorst, R.F. Troxler, and F.G. Oppenheim The human salivary peptide histatin 5 exerts its antifungal activity through the formation of reactive oxygen species Proc. Natl. Acad. Sci. U S A 98 2001 14637 14642 (Pubitemid 33121444)
41. A.L. Ruissen, J. Groenink, E.J. Helmerhorst, E. Walgreen-Weterings, W. Van't Hof, E.C. Veerman, and A.V. Nieuw Amerongen Effects of histatin 5 and derived peptides on Candida albicans Biochem. J. 356 2001 361 368 (Pubitemid 32532346)
42. M. Castagnola, R. Inzitari, D.V. Rossetti, C. Olmi, T. Cabras, V. Piras, P. Nicolussi, M.T. Sanna, M. Pellegrini, B. Giardina, and I. Messana A cascade of 24 histatins (histatin 3 fragments) in human saliva J. Biol. Chem. 279 2004 41436 41443
43. E. Del Nery, M.A. Juliano, M. Meldal, I. Svendsen, J. Sharfstein, and A.R. Walmsley Characterization of the substrate specificity of the major cysteine protease (cruzipain) from Trypanosoma cruzi using a portion-mixing combinatorial library and Fuorogenic peptide, L. Juliano Biochem. J. 323 1997 427 433 (Pubitemid 27183126)
44. P.M. St Hilaire, M. Willert, M.A. Juliano, L. Juliano, and M. Meldal Fluorescence-quenched solid phase combinatorial libraries in the characterization of cysteine protease substrate specificity J. Comb. Chem. 1 1999 509 523
45. P.M. St Hilaire, L.C. Alves, S.J. Sanderson, J.C. Mottram, M.A. Juliano, L. Juliano, G.H. Coombs, and M. Meldal The substrate specificity of a recombinant cysteine protease from Leishmania mexicana: application of a combinatorial peptide library approach Chembiochem 1 2000 115 122
46. F.M. Alves, I.Y. Hirata, I.E. Gouvea, M.F. Alves, M. Meldal, D. Brömme, L. Juliano, and M.A. Juliano Controlled peptide salvation in portion-mixing libraries of FRET peptides: inproved specificity determination for dengue 2 virus NS2B-NS3 protease and human cathepsin S J. Comb. Chem. 9 2007 627 634
47. G.W. Jameson, D.V. Roberts, R.W. Adams, W.S.A. Kyle, and D.T. Elmore Determination of the operational molarity of solutions of bovine alpha-chymotrypsin, trypsin, thrombin and factor Xa by spectrofluorimetric titration Biochem. J. 131 1973 107 117
48. I. Hirata, M.H.C. Cezari, C.R. Nakaie, P. Boshcov, A.S. Ito, M.A. Juliano, and L. Juliano Internally quenched fluorogenic protease substrates: solid-phase synthesis and fluorescence spectroscopy of peptides containing ortho-aminobenzoyl/dinitrophenyl groups as donor-acceptor pairs Lett. Pept. Sci. 1 1994 299 308
49. B. Korkmaz, S. Attucci, M.A. Juliano, T. Kalupov, M.L. Jourdan, L. Juliano, and F. Gauthier Measuring elastase, proteinase 3, and cathepsin G activities at the surface of human neutrophils with fluorescence energy transfersubstrates Nat. Protoc. 3 2008 991 1000 (Pubitemid 351818687)
50. M. Roice, I. Johannsen, and M. Meldal High capacity poly(ethylene glycol) based amino polymers for peptide and organic synthesis QSAR Comb. Chem. 23 2004 662 673 (Pubitemid 39531953)
51. C.P. Dietrich, I.L.S. Tersariol, L. Toma, C.T. Moraes, M.A. Porcionatto, F.W. Oliveira, and H.B. Nader Structure of heparin sulfate: identification of variable and Constant oligosaccharide domains in eight heparan sulfates of different origins Cell Mol. Biol. 44 1998 417 429
52. K. Shimamoto, T. Ando, S. Tanaka, Y. Nakahashi, T. Nishitani, S. Hosoda, H. Ishida, and O. Iimura Na improved method for the determination of human blood kinin levels by sensitive kinin radioimmunoassay Endocrinol. Jpn. 29 1982 487 494 (Pubitemid 13144906)
53. R.J. Ellis Macromolecular crowding: obvious but underappreciated Trends Biochem. Sci. 26 2001 597 604 (Pubitemid 32925190)
54. K.K. Singh, M.M. Desouki, R.B. Franklin, and L.C. Costello Mitochondrial aconitase and citrte metabolism in malignant and nonmalignant human prostate tissues Mol. Cancer 5 2006 14 21
55. L.C. Costello, R.B. Franklin, and P. Narayan Citrate in the diagnosis of prostate cancer The Prostate 38 1999 237 245 (Pubitemid 29054940)
56. M.E. Mycielska, A. Patel, N. Rizaner, M.P. Mazurek, H.Keun, A. Patel, V. Ganapathy, and M.B.A. Djamgoz Citrate transport and metabolism in mammalian cells BioEssays 31 2009 10 20
57. H. Yoon, G. Laxmikanthan, J. Lee, S.I. Blaber, A. Rodrigues, J.M. Kogot, I.A. Scarisbrick, and M. Blaber Activation profiles and regulatory cascades of the human kallikrein-related peptidases J. Biol. Chem. 282 2007 31852 31864 (Pubitemid 350106429)
58. I.E. Triantaphyllidou, N.S. Mastronikolis, Th.A. Papadas, and D.H. Vynios HPLC identification of oversulphated chondroitin as the major glycosaminoglycan of human tonsils Biomed. Chromatogr. 2004 694 699 (Pubitemid 39591844)
59. L.M. Loeb, M.G. Naffah-Mazzacoratti, M.A. Porcionatto, J.M.R. Martins, M. Kouyoumdjian, L.M. Weckx, and H.B. Nader Chondroitin sulfate and kallikrein in saliva: markers for glossodynia Int. Immunopharmacol. 8 2008 1056 1058
60. C.E. Bandtlow, and D.R. Zimmermann Proteoglycans in the developing brain: new conceptual insights for old proteins Physiol. Rev. 80 2000 1267 1290
61. U. Rauch Extracellular matrix components associated with remodeling processes in brain Cell Mol. Life Sci. 61 2004 2031 2045 (Pubitemid 39149893)