Functional intersection of the kallikrein-related peptidases (KLKs) and thrombostasis axis

Biological Chemistry

Volumn 391, Issue 4, 2010, Pages 311-320

  Blaber, Michael ^a   Yoon, Hyesook ^a   Juliano, Maria A ^b   Scarisbrick, Isobel A ^c   Blaber, Sachiko I ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c MAYO CLINIC   (United States)

Author keywords

Activation cascade; Kallikrein; Kallikrein related peptidase (KLK); Plasmin; Thrombogenesis; Thrombolysis; Thrombostasis

Indexed keywords

ANGIOSTATIN; KALLIKREIN; PLASMIN; PLASMINOGEN; PREKALLIKREIN; PROTEINASE ACTIVATED RECEPTOR; UROKINASE; UROKINASE RECEPTOR;

BLOOD CLOT LYSIS; CONFERENCE PAPER; ENZYME ACTIVATION; HEMOSTASIS; HUMAN; HYDROLYSIS; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; THROMBOGENESIS; TISSUE INJURY;

ANGIOSTATINS; ANIMALS; ENZYME ACTIVATION; HUMANS; KALLIKREINS; PROTEASE INHIBITORS; RECEPTORS, PROTEINASE-ACTIVATED; THROMBOSIS;

EID: 77951442032     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2010.024     Document Type: Conference Paper

References (100)

1. Angelo, 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 effects. J. Biol. Chem. 281, 3116-3126.
2. Baumann, G. (1991). Growth hormone heterogeneity: genes, isohormones, variants, and binding proteins. Endocr. Rev. 12, 424-449.
3. Bayes, A., Tsetsenis, T., Ventura, S., Vendrell, J., Aviles, F.X., and Sotiropoulou, G. (2004). Human kallikrein 6 activity is regulated via an autoproteolytic mechanism of activation/inactivation. Biol. Chem. 385, 517-524.
4. Beaufort, N., Debela, M., Creutzburg, S., Kellermann, J., Bode, W., Schmitt, M., Pidard, D., and Magdolen, V. (2006). Interplay of human tissue kallikrein 4 (hK4) with the plasminogen activation system: hK4 regulates the structure and functions of the uroki nase-type plasminogen activator receptor (uPAR). Biol. Chem. 387, 217-222.
5. Bhattacharjee, G., Ahamed, J., Pawlinski, R., Liu, C., Mackman, N., Ruf, W., and Edgington, T.S. (2008). Factor Xa binding to annexin 2 mediates signal transduction via protease-activated receptor 1. Circ. Res. 102, 457-464.
6. Bitoun, E., Micheloni, A., Lamant, L., Bonnart, C., Tartaglia-Polcini, A., Cobbold, C., Al Saati, T., Mariotti, F., Mazereeuw-Hautier, J., Boralevi, F., et al. (2003). LEKTI proteolytic processing in human primary keratinocytes, tissue distribution and defective expression in Netherton syndrome. Hum. Mol. Genet. 12, 2417-2430.
7. Blaber, S.I., Yoon, H., Scarisbrick, I.A., Juliano, M.A., and Blaber, M. (2007). The autolytic regulation of human kallikrein-related peptidase 6. Biochemistry 46, 5209-5217.
8. Blanc-Brude, O.P., Archer, F., Leoni, P., Derian, C., Bolsover, S., Laurent, G.J., and Chambers, R.C. (2005). Factor Xa stimulates fibroblast procollagen production, proliferation, and calcium signaling via PAR1 activation. Exp. Cell Res. 304, 16-27.
9. Blasi, F. and Carmeliet, P. (2002). uPAR: a versatile signalling orchestrator. Nat. Rev. Mol. Cell Biol. 3, 932-943.
10. Borgoño, C.A. and Diamandis, E.P. (2004). The emerging roles of human tissue kallikreins in cancer. Nat. Rev. Cancer 4, 876-890.
11. Borgoño, C.A., MIacovos, M.P., and Diamandis, E.P. (2004). Human tissue kallikreins: physiologic roles and applications in cancer. Mol. Cancer Res. 2, 257-280.
12. Borgoño, C.A., Gavigan, J.A., Alves, J., Bowles, B., Harris, J.L., Sotiropoulou, G., and Diamandis, E.P. (2007a). Defining the extended substrate specificity of kallikrein 1-related peptidases. Biol. Chem. 388, 1215-1225.
13. Borgoño, C.A., Michael, I.P., Komatsu, N., Jayakumar, A., Kapadia, R., Clayman, G.L., Sotiropoulou, G., and Diamandis, E.P. (2007b). A potential role for multiple tissue kallikrein serine proteases in epidermal desquamation. J. Biol. Chem. 282, 3640-3652.
14. Borgoño, C.A., Michael, I.P., Shaw, J.L.V., Luo, L.Y., Ghosh, M.C., Soosaipilla, A., Grass, L., Katsaros, D., and Diamandis, E.P. (2007c). Expression and functional characterization of the cancer-related serine protease, human tissue kallikrein 14. J. Biol. Chem. 282, 2405-2422.
15. Brattsand, M. and Egelrud, T. (1999). Purification, molecular cloning, and expression of a human stratum corneum trypsin-like serine protease with possible function in desquamation. J. Biol. Chem. 274, 30033-30040.
16. Brattsand, M., Stefansson, K., Lundh, C., Haasum, Y., and Egelrud, T. (2005). A proteolytic cascade of kallikreins in the stratum corneum. J. Invest. Dermatol. 124, 198-203.
17. Brattsand, M., Stefansson, K., Hubiche, T., Nilsson, S.K., and Egelrud, T. (2009). SPINK9: a selective, skin-specific Kazal-type serine protease inhibitor. J. Invest. Dermatol. 129, 1656-1665.
18. Camerer, E., Huang, W., and Coughlin, S.R. (2000). Tissue factorand factor X-dependent activation of protease-activated receptor 2 by factor VIIa. Proc. Natl. Acad. Sci. USA 97, 5255-5260.
19. Catalona, W.J., Smith, D.S., Ratliff, T.L., Dodds, K.M., Coplen, D.E., Yuan, J.J., Petros, J.A., and Andriole, G.L. (1991). Measurement of prostate-specific antigen in serum as a screening test for prostate cancer. N. Engl. J. Med. 324, 1156-1161.
20. Caubet, C., Jonca, N., Brattsand, M., Guerrin, M., Bernard, D., Schmidt, R., Egelrud, T., Simon, M., and Serre, G. (2004). Degradation of corneodesmosome proteins by two serine proteases of the kallikrein family, SCTE/KLK5/hK5 and SCCE/KLK7/ hK7. J. Invest. Dermatol. 122, 1235-1244.
21. Chavanas, S., Bodemer, C., Rochat, A., Hamel-Teillac, D., Ali, M., Irvine, A.D., Bonafé, J.L., Wilkinson, J., Taeb, A., Barrandon, Y., et al. (2000). Mutations in SPINK5, encoding a serine protease inhibitor, cause Netherton syndrome. Nat. Genet. 25, 141-142.
22. Clements, J., Hooper, J., Dong, Y., and Harvey, T. (2001). The expanded human kallikrein (KLK) gene family: genomic organisation, tissue-specific expression and potential functions. Biol. Chem. 382, 5-14.
23. Coughlin, S.R. (2005). Protease-activated receptors in hemostasis, thrombosis and vascular biology. J. Thromb. Haemost. 3, 1800-1814.
24. Debela, M., Magdolen, V., Schechter, N., Valachova, M., Lottspeich, F., Craik, C.S., Choe, Y., Bode, W., and Goettig, P. (2006). Specificity profiling of seven human tissue kallikreins reveals individual subsite preferences. J. Biol. Chem. 281, 25678-25688.
25. Denmeade, S.R., Lovgren, J., Khan, S.R., Lilja, H., and Isaacs, J.T. (2001). Activation of latent protease function of pro-hK2, but not pro-PSA, involves autoprocessing. Prostate 48, 122-126.
26. Diamandis, E.P. and Yousef, G.M. (2001). Human tissue kallikrein gene family: a rich source of novel disease biomarkers. Expert Rev. Mol. Diagn. 1, 182-190.
27. 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.
28. Dong, Z., Kumar, R., Yang, X., and Fidler, J.J. (1997). Macrophagederived mealloelastase is responsible for the generation of angiostatin in Lewis lung carcinoma. Cell 88, 801-810.
29. Egelrud, T., Brattsand, M., Kreutzmann, P., Walden, M., Vitzithum, K., Marx, U.C., Forssmann, W.G., and Mägert, H.J. (2005). hK5 and hK7, two serine proteinases abundant in human skin, are inhibited by LEKTI domain 6. Br. J. Dermatol. 153, 1200-1203.
30. Ekholm, I.E., Brattsand, M., and Egelrud, T. (2000). Stratum corneum tryptic enzyme in normal epidermis: a missing link in the desquamation process? J. Invest. Dermatol. 114, 56-63.
31. Frenette, G., Tremblay, R.R., Lazure, C., and Dube, J.Y. (1997). Prostatic kallikrein hK2, but not prostate-specific antigen (hK3), activates single-chain urokinase-type plasminogen activator. Int. J. Cancer 71, 897-899.
32. Gan, L., Lee, I., Smith, R., Argonza-Barrett, R., Lei, H., McCuaig, J., Moss, P., Paeper, B., and Wang, K. (2000). Sequencing and expression analysis of the serine protease gene cluster located in chromosome 19q13 region. Gene 257, 119-130.
33. Garcia-Barros, M., Devesa, J., and Arce, V.M. (2000). Proteolytic processing of human growth hormone (GH) by rat tissues in vitro: influence of sex and age. J. Endocrinol. Invest. 23, 748-754.
34. Hansen, K.K., Oikonomopoulou, K., Baruch, A., Ramachandran, R., Beck, P., Diamandis, E.P., and Hollenberg, M.D. (2008). Proteinases as hormones: targets and mechanisms for proteolytic signaling. Biol. Chem. 389, 971-982.
35. 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.
36. Heidtmann, H.-H., Nettelbeck, D.M., Mingels, A., Jager, R.,Welker, H.-G., and Kontermann, R.E. (1999). Generation of angiostatinlike fragments from plasminogen by prostate-specific antigen. Br. J. Cancer 81, 1269-1273.
37. Hollenberg, M.D., Oikonomopoulou, K., Hansen, K.K., Saifeddine, M., Ramachandran, R., and Diamandis, E.P. (2008). Kallikreins and proteinase-mediated signaling: proteinase-activated receptors (PARs) and the pathophysiology of inflammatory diseases and cancer. Biol. Chem. 389, 643-651.
38. Houle, S., Papez, M.D., Ferazzini, M., Hollenberg, M.D., and Ver gnolle, N. (2005). Neutrophils and the kallikrein-kinin system in proteinase-activated receptor 4-mediated inflammation in rodents. Br. J. Pharmacol. 146, 670-678.
39. Janssen, S., Jakobsen, C.M., Rosen, D.M., Ricklis, R.M., Reineke, U., Christensen, S.B., Lilja, H., and Denmeade, S.R. (2004). Screening a combinatorial peptide library to develop a human glandular kallikrein 2-activated prodrug as targeted therapy for prostate cancer. Mol. Cancer Ther. 3, 1439-1450.
40. Kahn, M.L., Zheng, Y.W., Huang, W., Bigornia, V., Zeng, D., Moff, S., Farese, R.V.J., Tam, C., and Coughlin, S.R. (1998). A dual thrombin receptor system for platelet activation. Nature 394, 690-694.
41. Kimura, M., Andersen, T.T., Fenton, J.W. II, Bahou, W.F., and Aviv, A. (1996). Plasmin-platelet interaction involves cleavage of functional thrombin receptor. Am. J. Physiol. 271, C54-C60.
42. Kishi, T., Kato, M., Shimizu, T., Kato, K., Matsumoto, K., Yoshida, S., Shiosaka, S., and Hakoshima, T. (1997). Crystallization and preliminary X-ray analysis of neuropsin, a serine protease expressed in the limbic system of mouse brain. J. Struct. Biol. 118, 248-251.
43. Komatsu, N., Takata, M., Otsuki, N., Ohka, R., Amano, O., Takehara, K., and Saijoh, K. (2002). Elevated stratum corneum hydrolytic activity in Netherton syndrome suggests an inhibitory regulation of desquamation by SPINK5-derived peptides. J. Invest. Dermatol. 118, 436-443.
44. Komatsu, N., Takata, M., Otsuki, N., Toyama, T., Ohka, R., Takehara, K., and Saijoh, K. (2003). Expression and localization of tissue kallikrein mRNAs in human epidermis and appendages. J. Invest. Dermatol. 121, 542-549.
45. Komatsu, N., Saijoh, K., Otsuki, N., Kishi, T., Michael, I.P., Obiezu, C.V., Borgono, C.A., Takehara, K., Jayakumar, A., Wu, H.K., et al. (2007). Proteolytic processing of human growth hormone by multiple tissue kallikreins and regulation by the serine protease inhibitor Kazal-Type5 (SPINK5) protein. Clin. Chim. Acta 377, 228-236.
46. Komatsu, N., Saijoh, K., Jayakumar, A., Clayman, G.L., Tohyama, M., Suga, Y., Mizuno, Y., Tsukamoto, K., Taniuchi, K., Takehara, K., et al. (2008). Correlation between SPINK5 gene mutations and clinical manifestations in Netherton syndrome patients. J. Invest. Dermatol. 128, 1148-1159.
47. Kuliopulos, A., Covic, L., Seeley, S.K., Sheridan, P.J., Helin, J., and Costello, C.E. (1999). Plasmin desensitization of the PAR1 thrombin receptor: kinetics, sites of truncation, and implications for thrombolytic therapy. Biochemistry 38, 4572-4585.
48. Lafleur, M.A., Hollenberg, M.D., Atkinson, S.J., Knäuper, V., Murphy, G., and Edwards, D.R. (2001). Activation of pro-(matrix metalloproteinase-2) (pro-MMP-2) by thrombin is membranetype-MMP-dependent in human umbilical vein endothelial cells and generates a distinct 63 kDa active species. Biochem. J. 357, 107-115.
49. Li, H.-X., Hwang, B.-Y., Laxmikanthan, G., Blaber, S.I., Blaber, M., Golubkov, P.A., Ren, P., Iverson, B.L., and Georgiou, G. (2008). The substrate specificity of human kallikrein 1 and 6 determined by phage display. Protein Sci. 17, 664-672.
50. Lilja, H. (1985). A kallikrein-like serine protease in prostatic fluid cleaves the predominant seminal vesicle protein. J. Clin. Invest. 76, 1899-1903.
51. Lilja, H., Ulmert, D., and Vickers, A.J. (2008). Prostate-specific antigen and prostate cancer: prediction, detection and monitoring. Nat. Rev. Cancer 8, 268-278.
52. List, K., Jensen, O.N., Bugge, T.H., Lund, L.R., Ploug, M., Danø, K., and Behrendt, N. (2000). Plasminogen-independent initiation of the pro-urokinase activation cascade in vivo. Activation of pro-urokinase by glandular kallikrein (mGK-6) in plasminogendeficient mice. Biochemistry 39, 508-515.
53. Little, S.P., Dixon, E.P., Norris, F., Buckley, W., Becker, G.W., Johnson, M., Dobbins, J.R., Wyrick, T., Miller, J.R., MacKellar, W., et al. (1997). Zyme, a novel and potentially amyloidogenic enzyme cDNA isolated from Alzheimer's disease brain. J. Biol. Chem. 272, 25135-25142.
54. Lovgren, J., Rajakoski, K., Karp, M., Lundwall, A., and Lilja, H. (1997). Activation of the zymogen form of prostate-specific antigen by human glandular kallikrein 2. Biochem. Biophys. Res. Commun. 238, 549-555. (Pubitemid 27464425)
55. Lovgren, J., Airas, K., and Lilja, H. (1999). Enzymatic action of human glandular kallikrein 2 (hK2). Substrate specificity and regulation by Zn2q and extracellular protease inhibitors. Eur. J. Biochem. 262, 781-789.
56. Lu, Y., Papagerakis, P., Yamakoshi, Y., Hu, J.C., Bartlett, J.D., and Simmer, J.P. (2008). Functions of KLK4 and MMP-20 in dental enamel formation. Biol. Chem. 389, 695-700.
57. Ludeman, M.J., Kataoka, H., Srinivasan, Y., Esmon, N.L., Esmon, C.T., and Coughlin, S.R. (2005). PAR1 cleavage and signaling in response to activated protein C and thrombin. J. Biol. Chem. 280, 13122-13128.
58. Lundstrom, A. and Egelrud, T. (1991). Stratum corneum chymotryptic enzyme: a proteinase which may be generally present in the stratum corneum and with a possible involvement in desquamation. Acta Derm. Venereol. 71, 471-474.
59. Lundwall, A., Band, V., Blaber, M., Clements, J.A., Courty, Y., Diamandis, E.P., Fritz, H., Lilja, H., Malm, J., Maltais, L.J., et al. (2006). A comprehensive nomenclature for serine proteases with homology to tissue kallikreins. Biol. Chem. 387, 637-641.
60. Luo, L.Y., Shan, S.J.C., Elliott, M.B., Soosaipilla, A., and Diamandis, E.P. (2006). Purification and characterization of human kallikrein 11, a candidate prostate and ovarian cancer biomarker, from seminal plasma. Hum. Cancer Biol. 12, 742-750.
61. Mägert, H.J., Ständker, L., Kreutzmann, P., Zucht, H.D., Reinecke, M., Sommerhoff, C.P., Fritz, H., and Forssmann, W.G. (1999). LEKTI, a novel 15-domain type of human serine proteinase inhibitor. J. Biol. Chem. 274, 21499-21502.
62. Meyer-Hoffert, U., Wu, Z., and Schröder, J.M. (2009). Identification of lympho-epithelial Kazal-type inhibitor 2 in human skin as a kallikrein-related peptidase 5-specific protease inhibitor. PLoS One 4, e4372.
63. Michael, I.P., Sotiropoulou, G., Pampalakis, G., Magklara, A., Ghosh, M., Wasney, G.A., and Diamandis, E.P. (2005). Biochemical and enzymatic characterization of human kallikrein 5 (hK5), a novel serine protease potentially involved in cancer progression. J. Biol. Chem. 280, 14628-14635.
64. Michael, I.P., Pampalakis, G., Mikolajczyk, S.D., Malm, J., Sotiropoulou, G., and Diamandis, E.P. (2006). Human tissue kallikrein 5 (hK5) is a member of a proteolytic cascade pathway involved in seminal clot liquefaction and potentially in prostate cancer progression. J. Biol. Chem. 281, 12743-12750.
65. Mikolajczyk, S.D., Millar, L.S., Kumar, A., and Saedi, M.S. (1999). Prostatic human kallikrein 2 inactivates and complexes with plasminogen activator inhibitor-1. Int. J. Cancer 81, 438-442.
66. Mitsudo, K., Jayakumar, A., Henderson, Y., Frederick, M.J., Kang, Y., Wang, M., El-Naggar, A.K., and Clayman, G.L. (2003). Inhibition of serine proteinases plasmin, trypsin, subtilisin A, cathepsin G, and elastase by LEKTI: a kinetic analysis. Biochemistry 42, 3874-3881.
67. Nelson, P.S., Gan, L., Ferguson, C., Moss, P., Gelinas, R., Hood, L., and Wang, K. (1999). Molecular cloning and characterization of prostase, an androgen-regulated serine protease with prostate restricted expression. Proc. Natl. Acad. Sci. USA 96, 3114-3119.
68. O'Reilly, M.S., Holmgren, L., Shing, Y., Chen, C., Rosenthal, R.A., Moses, M., Lane, W.S., Cao, Y., Sage, E.H., and Folkman, J. (1994). Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by Lewis lung carcinoma. Cell 79, 315-328.
69. Obiezu, C.V., Michael, I.P., Levesque, M.A., and Diamandis, E.P. (2006). Human kallikrein 4: enzymatic activity, inhibition, and degradation of extracellular matrix proteins. Biol. Chem. 387, 749-759.
70. Oikonomopoulou, K., Hansen, K.K., Saifeddine, M., Tea, I., Blaber, M., Blaber, S.I., Scarisbrick, I., Andrade-Gordon, P., Cottrell, G.S., Bunnett, N.W., et al. (2006a). Proteinase-activated receptors, targets for kallikrein signaling. J. Biol. Chem. 281, 32095-32112.
71. Oikonomopoulou, K., Hansen, K.K., Saifeddine, M., Vergnolle, N., Tea, I., Blaber, M., Blaber, S.I., Scarisbrick, I., Diamandis, E.P., and Hollenberg, M.D. (2006b). Kallikrein-mediated cell signalling: targeting proteinase-activated receptors (PARs). Biol. Chem. 387, 817-824.
72. Oikonomopoulou, K., Hansen, K.K., Baruch, A., Hollenberg, M.D., and Diamandis, E.P. (2008). Immunofluormetric activity-based probe analysis of active KLK6 in biological fluids. Biol. Chem. 389, 747-756.
73. Pettus, J.R., Johnson, J.J., Shi, Z., Davis, J.W., Koblinski, J., Ghosh, S., Liu, Y., Ravosa, M.J., Frazier, S., and Stack, M.S. (2009). Multiple kallikrein (KLK 5, 7, 8, and 10) expression in squamous cell carcinoma of the oral cavity. Histol. Histophathol. 24, 197-207.
74. Ploug, M. (2003). Structure-function relationships in the interaction between the urokinase-type plasminogen activator and its receptor. Curr. Pharm. Des. 9, 1499-1528.
75. Quinton, T.M., Kim, S., Derian, C.K., Jin, J., and Kunapuli, S.P. (2004). Plasmin-mediated activation of platelets occurs by cleavage of protease-activated receptor 4. J. Biol. Chem. 279, 18434-18439.
76. Rajapakse, S., Ogiwara, K., Takano, N., Moriyama, A., and Takahashi, T. (2005). Biochemical characterization of human kallikrein 8 and its possible involvement in the degradation of extracellular matrix proteins. FEBS Lett. 579, 6879-6884.
77. Rajapakse, S., Yamano, N., Ogiwara, K., Hirata, K., Takahashi, S., and Takahashi, T. (2007). Estrogen-dependent expression of the tissue kallikrein gene (Klk1) in the mouse uterus and its implications for endometrial tissue growth. Mol. Reprod. Dev. 74, 1053-1063.
78. Ramsay, A.J., Dong, Y., Hunt, M.L., Linn, M., Samaratunga, H., Clements, J.A., and Hooper, J.D. (2008a). Kallikrein-related peptidase 4 (KLK4) initiates intracellular signaling via proteaseactivated receptors (PARs). KLK4 and PAR-2 are co-expressed during prostate cancer progression. J. Biol. Chem. 283, 12293-12304.
79. Ramsay, A.J., Reid, J.C., Adams, M.N., Samaratunga, H., Dong, Y., Clements, J.A., and Hooper, J.D. (2008b). Prostatic trypsin-like kallikrein-related peptidases (KLKs) and other prostateexpressed tryptic proteinases as regulators of signalling via proteinase-activated receptors (PARs). Biol. Chem. 389, 653-668.
80. Ruf, W. and Mueller, B.M. (2006). Thrombin generation and the pathogenesis of cancer. Semin. Thromb. Hemost. 32 (Suppl. 1), 61-68.
81. Ruf, W., Dorfleutner, A., and Riewald, M. (2003). Specificity of coagulation factor signaling. J. Thromb. Haemost. 1, 1495-1503.
82. Ryu, O., Hu, J.C., Yamakoshi, Y., Villemain, J.L., Cao, X., Zhang, C., Bartlett, J.D., and Simmer, J.P. (2002). Porcine kallikrein-4 activation, glycosylation, activity, and expression in prokaryotic and eukaryotic hosts. Eur. J. Oral Sci. 110, 358-365.
83. Schechter, N.M., Choi, E.J., Wang, Z.M., Hanakawa, Y., Stanley, J.R., Kang, Y., Clayman, G.L., and Jayakumar, A. (2005). Inhibition of human kallikreins 5 and 7 by the serine protease inhibitor lympho-epithelial Kazal-type inhibitor (LEKTI). Biol. Chem. 386, 1173-1184.
84. Sotiropoulou, G., Rogakos, V., Tsetsenis, T., Pampalakis, G., Zafiropoulos, N., Simillides, G., Yiotakis, A., and Diamandis, E.P. (2003). Emerging interest in the kallikrein gene family for understanding and diagnosing cancer. Oncol. Res. 13, 381-391.
85. Sotiropoulou, G., Pampalakis, G., and Diamandis, E.P. (2009). Functional roles of human kallikrein-related peptidases. J. Biol. Chem. 284, 32989-32994.
86. Stamey, T.A., Yang, N., Hay, A.R., McNal, J.E., Freiha, F.S., and Redwine, E. (1987). Prostate-specific antigen as a serum marker for adenocarcinoma of the prostate. N. Engl. J. Med. 15, 909-916.
87. Stubbs, M.T., Renatus, M., and Bode, W. (1998). An active zymogen: unravelling the mystery of tissue-type plasminogen activator. Biol. Chem. 379, 95-103.
88. Takayama, T.K., McMullen, B.A., Nelson, P.S., Matsumura, M., and Fujikawa, K. (2001). 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, 15341-15348.
89. Traynelis, S.F. and Trejo, J. (2007). Protease-activated receptor signaling: new roles and regulatory mechanisms. Curr. Opin. Hematol. 14, 230-235.
90. Tsurupa, G. and Medved, L. (2001). Identification and characterization of novel tPA-and plasminogen-binding sites within fibrin(ogen) aC-domains. Biochemistry 40, 801-808.
91. Vandell, A.G., Larson, N., Laxmikanthan, G., Panos, M., Blaber, S.I., Blaber, M., and Scarisbrick, I.A. (2008). Protease-activated receptor dependent and independent signaling by kallikreins 1 and 6 in CNS neuron and astroglial cell lines. J. Neurochem. 107, 855-870.
92. Versteeg, H.H. and Ruf, W. (2006). Emerging insights in tissue factor-dependent signaling events. Semin. Thromb. Hemost. 32, 24-32.
93. Watt, K.W.K., Lee, P.-J., M'Timkulu, T., Chan, W.-P., and Loor, R. (1986). Human prostate-specific antigen: structural and functional similarity with serine proteases. Proc. Natl. Acad. Sci. USA 83, 3166-3170.
94. Xu, W.F., Andersen, H., Whitmore, T.E., Presnell, S.R., Yee, D.P., Ching, A., Gilbert, T., Davie, E.W., and Foster, D.C. (1998). Cloning and characterization of human protease-activated receptor 4. Proc. Natl. Acad. Sci. USA 95, 6642-6646.
95. Yoon, H., Laxmikanthan, G., Lee, J., Blaber, S.I., Rodriguez, A., Kogot, J.M., Scarisbrick, I.A., and Blaber, M. (2007). Activation profiles and regulatory cascades of the human kallikrein-related proteases. J. Biol. Chem. 282, 31852-31864.
96. Yoon, H., Blaber, S.I., Evans, D.M., Trim, J., Juliano, M.A., Scarisbrick, I.A., and Blaber, M. (2008). Activation profiles of human kallikrein-related peptidases by proteases of the thrombostasis axis. Protein Sci. 17, 1998-2007.
97. Yoon, H., Blaber, S.I., Debela, M., Goettig, P., Scarisbrick, I.A., and Blaber, M. (2009). A completed KLK activome profile: investigation of activation profiles of KLK9, 10 and 15. Biol. Chem. 390, 373-377.
98. 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.
99. Yousef, G.M. and Diamandis, E.P. (2003). An overview of the kallikrein gene families in humans and other species: emerging candidate tumour markers. Clin. Biochem. 36, 443-452.
100. 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.