Sweetened kallikrein-related peptidases (KLKs): Glycan trees as potential regulators of activation and activity

Biological Chemistry

Volumn 395, Issue 9, 2014, Pages 959-976

  Guo, Shihui ^a   Skala, Wolfgang ^a   Magdolen, Viktor ^b   Brandstetter, Hans ^a   Goettig, Peter ^a  

^a UNIVERSITY OF SALZBURG   (Austria)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

turn; N glycosylation; O glycosylation; Posttranslational modification; Protein sector; Surface loops;

Indexed keywords

GLYCAN; GLYCOPROTEIN; GLYCOSYLATED PROTEIN; KALLIKREIN 10; KALLIKREIN 11; KALLIKREIN 12; KALLIKREIN 13; KALLIKREIN 14; KALLIKREIN 15; KALLIKREIN 5; KALLIKREIN 6; NEUROPSIN; PROSTATE SPECIFIC ANTIGEN; STRATUM CORNEUM CHYMOTRYPTIC ENZYME; TISSUE KALLIKREIN; UNCLASSIFIED DRUG; KALLIKREIN; POLYSACCHARIDE;

COMPARATIVE STUDY; CONFERENCE PAPER; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; GLYCOSYLATION; HUMAN; MAMMAL; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE HYPERTROPHY; PROTEIN DEGRADATION; PROTEIN GLYCOSYLATION; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; METABOLISM; MOLECULAR GENETICS;

MAMMALIA;

AMINO ACID SEQUENCE; ANIMALS; GLYCOPROTEINS; GLYCOSYLATION; HUMANS; KALLIKREINS; MOLECULAR SEQUENCE DATA; POLYSACCHARIDES; SUBSTRATE SPECIFICITY;

EID: 84923284996     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/hsz-2014-0140     Document Type: Conference Paper

References (165)

1. Aebi, M. (2013). N-linked protein glycosylation in the ER. BBA-Mol. Cell Res. 1833, 2430-2437.
2. Akopian, D., Shen, K., Zhang, X., and Shan, S.-O. (2013). Signal recognition particle: An essential protein-targeting machine. Annu. Rev. Biochem. 82, 693-721.
3. Aly, A.M., Higuchi, M., Kasper, C.K., Kazazian, H.H., Antonarakis, S.E., and Hoyer, L.W. (1992). Hemophilia a due to mutations that create new n-glycosylation sites. Proc. Natl. Acad. Sci. USA 89, 4933-4937.
4. Andrade, D., Assis, D.M., Lima, A.R., Oliveira, J.R., Araujo, M.S., Blaber, S.I., Blaber, M., Juliano, M.A., and Juliano, L. (2010). Substrate specificity and inhibition of human kallikrein-related peptidase 3 (KLK3 or PSA) activated with sodium citrate and glycosaminoglycans. Arch. Biochem. Biophys. 498, 74-82.
5. Anelli, T. and Sitia, R. (2008). Protein quality control in the early secretory pathway. EMBO J. 27, 315-327.
6. 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 activation effects. J. Biol. Chem. 281, 3116-3126.
7. Angermann, A., Bergmann, C., and Appelhans, H. (1989). Cloning and expression of human salivary-gland kallikrein in Escherichia coli. Biochem. J. 262, 787-793.
8. Appenzeller-Herzog, C. and Hauri, H.-P. (2006). The ER-Golgi intermediate compartment (ergic): in search of its identity and function. J. Cell Sci. 119, 2173-2183.
9. Barak, M., Mecz, Y., Lurie, A., and Gruener, N. (1989). Binding of serum prostate antigen to concanavalin a in patients with cancer or hyperplasia of the prostate. Oncology 46, 375-377.
10. Basu, P.S., Majhi, R., and Batabyal, S.K. (2003). Lectin and serum-PSA interaction as a screening test for prostate cancer. Clin. Biochem. 36, 373-376.
11. Bause, E. (1983). Structural requirements of n-glycosylation of proteins. Studies with proline peptides as conformational probes. Biochem J. 209, 331-336.
12. Bax, B., Blundell, T.L., Murray-Rust, J., and Mcdonald, N.Q. (1997). Structure of mouse 7s NGF: a complex of nerve growth factor with four binding proteins. Structure 5, 1275-1285.
13. Bayani, J. and Diamandis, E.P. (2012). The physiology and pathobiology of human kallikrein-related peptidase 6 (klk6). Clin. Chem. Lab. Med. 50, 211-233.
14. Beaufort, N., Plaza, K., Utzschneider, D., Schwarz, A., Burkhart, J., Creutzburg, S., Debela, M., Schmitt, M., Ries, C., and Magdolen, V. (2010). Interdependence of kallikrein-related peptidases in proteolytic networks. Biol. Chem. 391, 581-587.
15. Behnken, H.N., Ruthenbeck, A., Schulz, J.-M., and Meyer, B. (2014). Glycan analysis of prostate specific antigen (PSA) directly from the intact glycoprotein by HR-ESI/TOF-MS. J. Proteome Res. 13, 997-1001.
16. Beitz, E. (2000). Texshade: shading and labeling of multiple sequence alignments using latex2e. Bioinformatics 16, 135-139.
17. Bélanger, A., Van Halbeek, H., Graves, H.C., Grandbois, K., Stamey, T.A., Huang, L., Poppe, I., and Labrie, F. (1995). Molecular mass and carbohydrate structure of prostate specific antigen: studies for establishment of an international PSA standard. Prostate 27, 187-197.
18. Bernett, M.J., Blaber, S.I., Scarisbrick, I.A., Dhanarajan, P., Thompson, S.M., and Blaber, M. (2002). Crystal structure and biochemical characterization of human kallikrein 6 reveals that a trypsin-like kallikrein is expressed in the central nervous system. J. Biol. Chem. 277, 24562-24570.
19. Borgoño, C.A., Michael, I.P., Shaw, J.L.V., Luo, L.-Y., Ghosh, M.C., Soosaipillai, A., Grass, L., Katsaros, D., and Diamandis, E.P. (2007). Expression and functional characterization of the cancer-related serine protease, human tissue kallikrein 14. J. Biol. Chem. 282, 2405-2422.
20. 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.
21. 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.
22. 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.
23. Breitling, R., Klingner, S., Callewaert, N., Pietrucha, R., Geyer, A., Ehrlich, G., Hartung, R., Müller, A., Contreras, R., Beverley, S.M., et al. (2002). Non-pathogenic trypanosomatid protozoa as a platform for protein research and production. Protein Expr. Purif. 25, 209-218.
24. Breton, C., Oriol, R., and Imberty, A. (1998). Conserved structural features in eukaryotic and prokaryotic fucosyltransferases. Glycobiology 8, 87-94.
25. 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.
26. Chan, H., Springman, E.B., and Clark, J.M. (1998). Expression and characterization of human tissue kallikrein variants. Protein Expr. Purif. 12, 361-370.
27. Chao, J., Bledsoe, G., Yin, H., and Chao, L. 2006. The tissue kallikrein-kinin system protects against cardiovascular and renal diseases and ischemic stroke independently of blood pressure reduction. Biol. Chem. 387, 665-675.
28. Coombs, G.S., Bergstrom, R.C., Pellequer, J.L., Baker, S.I., Navre, M., Smith, M.M., Tainer, J.A., Madison, E.L., and Corey, D.R. (1998). Substrate specificity of prostate-specific antigen (PSA). Chem. Biol. 5, 475-488.
29. Dalbey, R.E., Lively, M.O., Bron, S., and Dijl, J.M.V. (1997). The chemistry and enzymology of the type i signal peptidases. Protein Sci. 6, 1129-1138.
30. Debela, M., Magdolen, V., Grimminger, V., Sommerhoff, C., Messerschmidt, A., Huber, R., Friedrich, R., Bode, W., and Goettig, P. (2006a). Crystal structures of human tissue kallikrein 4: Activity modulation by a specific zinc binding site. J. Mol. Biol. 362, 1094-1107.
31. Debela, M., Magdolen, V., Schechter, N., Valachova, M., Lottspeich, F., Craik, C.S., Choe, Y., Bode, W., and Goettig, P. (2006b). Specificity profiling of seven human tissue kallikreins reveals individual subsite preferences. J. Biol. Chem. 281, 25678-25688.
32. Debela, M., Goettig, P., Magdolen, V., Huber, R., Schechter, N.M., and Bode, W. (2007a). Structural basis of the zinc inhibition of human tissue kallikrein 5. J. Mol. Biol. 373, 1017-1031.
33. Debela, M., Hess, P., Magdolen, V., Schechter, N.M., Steiner, T., Huber, R., Bode, W., and Goettig, P. (2007b). Chymotryptic specificity determinants in the 1.0 Å structure of the zinc-inhibited human tissue kallikrein 7. Proc. Natl. Acad. Sci. USA 104, 16086-16091.
34. Denmeade, S.R., Lou, W., Lövgren, J., Malm, J., Lilja, H., and Isaacs, J.T. (1997). Specific and efficient peptide substrates for assaying the proteolytic activity of prostate-specific antigen. Cancer Res. 57, 4924-4930.
35. Deraison, C., Bonnart, C., Lopez, F., Besson, C., Robinson, R., Jayakumar, A., Wagberg, F., Brattsand, M., Hachem, J.P., Leonardsson, G., et al. (2007). Lekti fragments specifically inhibit KLK5, KLK7, and KLK14 and control desquamation through a pH-dependent interaction. Mol. Biol. Cell 18, 3607-3619.
36. Deshaies, R.J., Sanders, S.L., Feldheim, D.A., and Schekman, R. (1991). Assembly of yeast sec proteins involved in translocation into the endoplasmic reticulum into a membrane-bound multisubunit complex. Nature 349, 806-808.
37. Dong, Y., Bui, L.T., Odorico, D.M., Tan, O.L., Myers, S.A., Samaratunga, H., Gardiner, R.A., and Clements, J.A. (2005). Compartmentalized expression of kallikrein 4 (KLK4/hk4) isoforms in prostate cancer: Nuclear, cytoplasmic and secreted forms. Endocr. Relat. Cancer 12, 875-889.
38. Dwek, M.V., Jenks, A., and Leathem, A.J.C. (2010). A sensitive assay to measure biomarker glycosylation demonstrates increased fucosylation of prostate specific antigen (PSA) in patients with prostate cancer compared with benign prostatic hyperplasia. Clin. Chim. Acta 411, 1935-1939.
39. Eissa, A., Amodeo, V., Smith, C.R., and Diamandis, E.P. (2011). Kal-likrein- 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, 687-706.
40. Ekholm, I.E., Brattsand, M., and Egelrud, T. (2000). Stratum corneum tryptic enzyme in normal epidermis: a missing link in the desquamation process. J. Investig. Dermatol. 114, 56-63.
41. Frenette, G., Deperthes, D., Tremblay, R.R., Lazure, C., and Dubé, J.Y. (1997). Purification of enzymatically active kallikrein hk2 from human seminal plasma. BBA-Gen. Subjects 1334, 109-115.
42. Frey, E.K. and Kraut, H. (1928). Ein neues kreislaufhormon und seine wirkung. Iii. Mitteilung. Naunyn-Schmiedeberg's Arch. Exp. Pathol. Pharmakol. 133, 1-56.
43. Fujinaga, M. and James, M.N. (1987). Rat submaxillary gland serine protease, tonin. Structure solution and refinement at 1.8 Åresolution. J. Mol. Biol. 195, 373-396.
44. Gidalevitz, T., Stevens, F., and Argon, Y. (2013). Orchestration of secretory protein folding by er chaperones. BBA-Mol. Cell Res. 1833, 2410-2424.
45. Gilgunn, S., Conroy, P.J., Saldova, R., Rudd, P.M., and O'kennedy, R.J. (2013). Aberrant PSA glycosylation-a sweet predictor of prostate cancer. Nat. Rev. Urol. 10, 99-107.
46. Gille, C. and Frömmel, C. (2001). Strap: Editor for structural alignments of proteins. Bioinformatics 17, 377-378.
47. Goettig, P. and Magdolen, V. (2012). Kallikrein-related peptidase 5. In: Handbook of proteolytic enzymes, Rawlings, N.D. and Salvesen, G., eds. (Oxford: Academic Press, Elsevier), pp. 2772-2778.
48. Goettig, P., Magdolen, V., and Brandstetter, H. (2010). Natural and synthetic inhibitors of kallikrein-related peptidases (KLKs). Biochimie 92, 1546-1567.
49. Grabenhorst, E., Nimtz, M., Costa, J., and Conradt, H.S. (1998). In vivo specificity of human α1,3/4-fucosyltransferases III-VII in the biosynthesis of lewisX and sialyl lewisX motifs on complex-type N-glycans: coexpression studies from bhk-21 cells together with human β-trace protein. J. Biol. Chem. 273, 30985-30994.
50. Habeck, L.L., Belagaje, R.M., Becker, G.W., Hale, J.E., Churgay, L.M., Ulmer, M., Yang, X.Y., Shackelford, K.A., Richardson, J.M., Johnson, M.G., et al. (2001). Expression, purification, and characterization of active recombinant prostate-specific antigen in Pichia pastoris (yeast). Prostate 46, 298-306.
51. Haguenauer-Tsapis, R. (1992). Protein-specific features of the general secretion pathway in yeast: the secretion of acid phosphatase. Mol. Microbiol. 6, 573-579.
52. Halabi, N., Rivoire, O., Leibler, S., and Ranganathan, R. (2009). Protein sectors: evolutionary units of three-dimensional structure. Cell 138, 774-786.
53. Hamilton, S.R. and Gerngross, T.U. (2007). Glycosylation engineering in yeast: the advent of fully humanized yeast. Curr. Opin. Biotech. 18, 387-392.
54. Hansen, J.E., Lund, O., Nielsen, J.O., Hansen, J.-E.S., and Brunak, S. (1996). O-glycbase: a revised database of O-glycosylated proteins. Nucleic Acids Res. 24, 248-252.
55. Hansson, L., Stromqvist, M., Backman, A., Wallbrandt, P., Carlstein, A., and Egelrud, T. (1994). Cloning, expression, and characterization of stratum corneum chymotryptic enzyme. A skin-specific human serine proteinase. J. Biol. Chem. 269, 19420-19426.
56. Hart, P.S., Hart, T.C., Michalec, M.D., Ryu, O.H., Simmons, D., Hong, S., and Wright, J.T. (2004). Mutation in kallikrein 4 causes autosomal recessive hypomaturation amelogenesis imperfecta. J. Med. Genet. 41, 545-549.
57. Hsieh, M.-C. and Cooperman, B.S. (2000). The preparation and catalytic properties of recombinant human prostate-specific antigen (rPSA). BBA-Protein Struct. M. 1481, 75-87.
58. Hu, Y., Hu, J.C.C., Smith, C.E., Bartlett, J.D., and Simmer, J.P. (2011). Kallikrein-related peptidase 4, matrix metalloproteinase 20, and the maturation of murine and porcine enamel. Eur. J. Oral Sci. 119, 217-225.
59. Hubbard, S.C. and Ivatt, R.J. (1981). Synthesis and processing of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 50, 555-583.
60. Ishida-Yamamoto, A., Simon, M., Kishibe, M., Miyauchi, Y., Takahashi, H., Yoshida, S., O'brien, T.J., Serre, G., and Iizuka, H. (2004). Epidermal lamellar granules transport different cargoes as distinct aggregates. J. Investig. Dermatol. 122, 1137-1144.
61. Izumi, A., Iijima, Y., Noguchi, H., Numakawa, T., Okada, T., Hori, H., Kato, T., Tatsumi, M., Kosuga, A., Kamijima, K., et al. (2008). Genetic variations of human neuropsin gene and psychiatric disorders: polymorphism screening and possible association with bipolar disorder and cognitive functions. Neuropsychopharmacology 33, 3237-3245.
62. Izutani, W., Fujita, M., Nishizawa, K., and Koga, J. (2001). The trimannosyl cores of n-glycans are important for the procoagulant protease-inhibitory activity of urinary protein C inhibitor. Thromb. Res. 104, 65-74.
63. Kalies, K.-U., Rapoport, T.A., and Hartmann, E. (1998). The β subunit of the sec61 complex facilitates cotranslational protein transport and interacts with the signal peptidase during translocation. J. Cell. Biol. 141, 887-894.
64. Kapadia, C., Chang, A., Sotiropoulou, G., Yousef, G.M., Grass, L., Soosaipillai, A., Xing, X., Howarth, D.H.C., and Diamandis, E.P. (2003). Human kallikrein 13: production and purification of recombinant protein and monoclonal and polyclonal antibodies, and development of a sensitive and specific immunofluorometric assay. Clin. Chem. 49, 77-86.
65. Karla, A., Lively, M.O., Paetzel, M., and Dalbey, R. (2005). The identification of residues that control signal peptidase cleavage fidelity and substrate specificity. J. Biol. Chem. 280, 6731-6741.
66. 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.
67. Kelleher, D.J., Karaoglu, D., Mandon, E.C., and Gilmore, R. (2003). Oligosaccharyltransferase isoforms that contain different catalytic stt3 subunits have distinct enzymatic properties. Mol. Cell 12, 101-111.
68. Kellermann, J., Lottspeich, F., Geiger, R., and Deutzmann, R. (1988). Human urinary kallikrein-amino acid sequence and carbohydrate attachment sites. Protein Seq. Data Anal. 1, 177-182.
69. Kim, J.H., Johannes, L., Goud, B., Antony, C., Lingwood, C.A., Daneman, R., and Grinstein, S. (1998). Noninvasive measurement of the ph of the endoplasmic reticulum at rest and during calcium release. Proc. Natl. Acad. Sci. USA 95, 2997-3002.
70. Kishi, T., Kato, M., Shimizu, T., Kato, K., Matsumoto, K., Yoshida, S., Shiosaka, S., and Hakoshima, T. (1999). Crystal structure of neuropsin, a hippocampal protease involved in kindling epileptogenesis. J. Biol. Chem. 274, 4220-4224.
71. Krainer, F.W., Gmeiner, C., Neutsch, L., Windwarder, M., Pletzenauer, R., Herwig, C., Altmann, F., Glieder, A., and Spadiut, O. (2013). Knockout of an endogenous mannosyltransferase increases the homogeneity of glycoproteins produced in pichia pastoris. Sci. Rep. 3, 3279.
72. Kraut, H., Frey, E.K., and Werle, E. (1930). Der nachweis eines kreislaufhormones in der pankreasdrüse. Z. Physiol. Chem. 189, 97.
73. Kumar, V., Yadav, V.K., Hassan, M.I., Singh, A.K., Dey, S., Singh, S., Singh, T.P., and Yadav, S. (2012). Kinetic and structural studies on the interactions of heparin and proteins of human seminal plasma using surface plasmon resonance. Protein Pept. Lett. 19, 795-803.
74. Kuzmanov, U., Jiang, N.X., Smith, C.R., Soosaipillai, A., and Diamandis, E.P. (2009). Differential N-glycosylation of kallikrein 6 derived from ovarian cancer cells or the central nervous system. Mol. Cell. Proteomics 8, 791-798.
75. Kuzmanov, U., Smith, C.R., Batruch, I., Soosaipillai, A., Diamandis, A., and Diamandis, E.P. (2012). Separation of kallikrein 6 glycoprotein subpopulations in biological fluids by anion-exchange chromatography coupled to elisa and identification by mass spectrometry. Proteomics 12, 799-809.
76. Kuzmanov, U., Kosanam, H., and Diamandis, E.P. (2013). The sweet and sour of serological glycoprotein tumor biomarker quantification. BMC Med. 11, 1-14.
77. Lam, P.V.N., Goldman, R., Karagiannis, K., Narsule, T., Simonyan, V., Soika, V., and Mazumder, R. (2013). Structure-based comparative analysis and prediction of N-linked glycosylation sites in evolutionarily distant eukaryotes. Genomics, Proteomics, Bioinformatics 11, 96-104.
78. Laxmikanthan, G., Blaber, S.I., Bernett, M.J., Scarisbrick, I.A., Juliano, M.A., and Blaber, M. (2005). 1.70 angstrom X-ray structure of human apo kallikrein 1: structural changes upon peptide inhibitor/substrate binding. Proteins: Struct. Funct. Bioinf. 58, 802-814.
79. Lenting, P.J., Pegon, J.N., Christophe, O.D., and Denis, C.V. (2010). Factor VIII and von Willebrand factor - too sweet for their own good. Haemophilia 16, 194-199.
80. Li, W., Johnson, D.J.D., Esmon, C.T., and Huntington, J.A. (2004). Structure of the antithrombin-thrombin-heparin ternary complex reveals the antithrombotic mechanism of heparin. Nat. Struct. Mol. Biol. 11, 857-862.
81. Li, Y., Tao, S.-C., Bova, G.S., Liu, A.Y., Chan, D.W., Zhu, H., and Zhang, H. (2011). Detection and verification of glycosylation patterns of glycoproteins from clinical specimens using lectin microarrays and lectin-based immunosorbent assays. Anal. Chem. 83, 8509-8516.
82. Liang, H., Vanvalkenburgh, C., Chen, X., Mullins, C., Van Kaer, L., Green, N., and Fang, H. (2003). Genetic complementation in yeast reveals functional similarities between the catalytic subunits of mammalian signal peptidase complex. J. Biol. Chem. 278, 50932-50939.
83. Lommel, M. and Strahl, S. (2009). Protein O-mannosylation: conserved from bacteria to humans. Glycobiology 19, 816-828.
84. 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.
85. Lovgren, J., Airas, K., and Lilja, H. (1999). Enzymatic action of human glandular kallikrein 2 (hK2). Substrate specificity and regulation by Zn2+ and extracellular protease inhibitors. Eur. J. Biochem. 262, 781-789.
86. Lu, H.S., Hsu, Y.-R., Lu, L.I., Ruff, D., Lyons, D., and Lin, F.-K. (1996a). Isolation and characterization of human tissue kallikrein produced in Escherichia coli: biochemical comparison to the enzymatically inactive prokallikrein and methionyl kallikrein. Protein Expression Purif. 8, 215-226.
87. Lu, H.S., Hsu, Y.-R., Narhi, L.O., Karkare, S., and Lin, F.-K. (1996b). Purification and characterization of human tissue prokallikrein and kallikrein isoforms expressed in chinese hamster ovary cells. Protein Expression Purif. 8, 227-237.
88. Lu, Y., Papagerakis, P., Yamakoshi, Y., Hu, J.C.C., Bartlett, J.D., and Simmer, J.P. (2008). Functions of KLK4 and MMP-20 in dental enamel formation. Biol. Chem. 389, 695-700.
89. Luo, L.Y. and Diamandis, E.P. (2012). Human tissue kallikrein 10. In: Handbook of proteolytic enzymes, Rawlings, N.D. and Salvesen, G., eds. (Oxford: Academic Press, Elsevier), pp. 2798-2801.
90. Malm, J., Hellman, J., Hogg, P., and Lilja, H. (2000). Enzymatic action of prostate-specific antigen (PSA or hK3): Substrate specificity and regulation by Zn2+, a tight-binding inhibitor. Prostate 45, 132-139.
91. Mattsson, J.M., Valmu, L., Laakkonen, P., Stenman, U.-H., and Koistinen, H. (2008). Structural characterization and anti-angiogenic properties of prostate-specific antigen isoforms in seminal fluid. Prostate 68, 945-954.
92. Mccoy, A.J., Pei, X.Y., Skinner, R., Abrahams, J.P., and Carrell, R.W. (2003). Structure of β-antithrombin and the effect of glycosylation on antithrombin's heparin affinity and activity. J. Mol. Biol. 326, 823-833.
93. Memari, N., Grass, L., Nakamura, T., Karakucuk, I., and Diamandis, E.P. (2006). Human tissue kallikrein 9: production of recombinant proteins and specific antibodies. Biol. Chem. 387, 733-740.
94. Memari, N., Jiang, W., Diamandis, E.P., and Luo, L.-Y. (2007). Enzymatic properties of human kallikrein-related peptidase 12 (KLK12). Biol. Chem. 388, 427-435.
95. Menez, R., Michel, S., Muller, B.H., Bossus, M., Ducancel, F., Jolivet-Reynaud, C., and Stura, E.A. (2008). Crystal structure of a ternary complex between human prostate-specific antigen, its substrate acyl intermediate and an activating antibody. J. Mol. Biol. 376, 1021-1033.
96. Michael, I.P., Sotiropoulou, G., Pampalakis, G., Magklara, A., Ghosh, M., Wasney, G., 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.
97. Mikolajczyk, S.D., Millar, L.S., Marker, K.M., Grauer, L.S., Goel, A., Cass, M.M.J., Kumar, A., and Saedi, M.S. (1997). Ala217 is important for the catalytic function and autoactivation of prostate-specific human kallikrein 2. Eur. J. Biochem. 246, 440-446.
98. Mikolajczyk, S.D., Millar, L.S., Kumar, A., and Saedi, M.S. (1998). Human glandular kallikrein, hK2, shows arginine-restricted specificity and forms complexes with plasma protease inhibitors. Prostate 34, 44-50.
99. Mitsui, S., Tsuruoka, N., Yamashiro, K., Nakazato, H., and Yamaguchi, N. (1999). A novel form of human neuropsin, a brain-related serine protease, is generated by alternative splicing and is expressed preferentially in human adult brain. Eur. J. Biochem. 260, 627-634.
100. Nagae, M. and Yamaguchi, Y. (2012). Function and 3D structure of the N-glycans on glycoproteins. Int. J. Mol. Sci. 13, 8398-8429.
101. Negrier, C., Knobe, K., Tiede, A., Giangrande, P., and Møss, J. (2011). Enhanced pharmacokinetic properties of a glycopegylated recombinant factor IX: a first human dose trial in patients with hemophilia B. Blood 118, 2695-2701.
102. Nyathi, Y., Wilkinson, B.M., and Pool, M.R. (2013). Co-translational targeting and translocation of proteins to the endoplasmic reticulum. BBA-Mol. Cell Res. 1833, 2392-2402.
103. 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.
104. Ohyama, C., Hosono, M., Nitta, K., Oh-Eda, M., Yoshikawa, K., Habuchi, T., Arai, Y., and Fukuda, M. (2004). Carbohydrate structure and differential binding of prostate specific antigen to maackia amurensis lectin between prostate cancer and benign prostate hypertrophy. Glycobiology 14, 671-679.
105. Oka, O.B.V. and Bulleid, N.J. (2013). Forming disulfides in the endoplasmic reticulum. BBA-Mol. Cell Res. 1833, 2425-2429.
106. Oka, T., Hakoshima, T., Itakura, M., Yamamori, S., Takahashi, M., Hashimoto, Y., Shiosaka, S., and Kato, K. (2002). Role of loop structures of neuropsin in the activity of serine protease and regulated secretion. J. Biol. Chem. 277, 14724-14730.
107. Okada, T., Sato, Y., Kobayashi, N., Sumida, K., Satomura, S., Matsuura, S., Takasaki, M., and Endo, T. (2001). Structural characteristics of the N-glycans of two isoforms of prostate-specific antigens purified from human seminal fluid. BBA-Gen. Subjects 1525, 149-160.
108. Paetzel, M., Karla, A., Strynadka, N.C.J., and Dalbey, R.E. (2002). Signal peptidases. Chem. Rev. 102, 4549-4580.
109. Parodi, A.J. (2000). Role of n-oligosaccharide endoplasmic reticulum processing reactions in glycoprotein folding and degradation. Biochem J. 348, 1-13.
110. Peracaula, R., Tabares, G., Royle, L., Harvey, D.J., Dwek, R.A., Rudd, P.M., and De Llorens, R. (2003). Altered glycosylation pattern allows the distinction between prostate-specific antigen (PSA) from normal and tumor origins. Glycobiology 13, 457-470.
111. Pless, D.D. and Lennarz, W.J. (1977). Enzymatic conversion of proteins to glycoproteins. Proc. Natl. Acad. Sci. USA 74, 134-138.
112. Prakash, S. and Robbins, P.W. (2000). Glycotyping of prostate specific antigen. Glycobiology 10, 173-176.
113. Radulovic, M., Yoon, H., Larson, N., Wu, J., Linbo, R., Burda, J.E., Diamandis, E.P., Blaber, S.I., Blaber, M., Fehlings, M.G., et al. (2013). Kallikrein cascades in traumatic spinal cord injury: in vitro evidence for roles in axonopathy and neuron degeneration. J. Neuropathol. Exp. Neurol. 72, 1072-1089 1010.1097/NEN.0000000000000007.
114. Rajapakse, S. and Takahashi, T. (2007). Expression and enzymatic characterization of recombinant human kallikrein 14. Zoolog. Sci. 24, 774-780.
115. Roth, J. (2002). Protein N-glycosylation along the secretory pathway: relationship to organelle topography and function, protein quality control, and cell interactions. Chem. Rev. 102, 285-304.
116. Ruiz-Canada, C., Kelleher, D.J., and Gilmore, R. (2009). Cotranslational and posttranslational N-glycosylation of polypeptides by distinct mammalian ost isoforms. Cell 136, 272-283.
117. Ryu, O., Hu, J., C. 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.
118. Saedi, M.S., Zhu, Z., Marker, K., Liu, R.-S., Carpenter, P.M., Rittenhouse, H., and Mikolajczyk, S.D. (2001). Human kallikrein 2 (hK2), but not prostate-specific antigen (PSA), rapidly complexes with protease inhibitor 6 (PI-6) released from prostate carcinoma cells. Int. J. Cancer 94, 558-563.
119. Sarrats, A., Saldova, R., Comet, J., O'donoghue, N., De Llorens, R., Rudd, P.M., and Peracaula, R. (2010). Glycan characterization of PSA 2-de subforms from serum and seminal plasma. OMICS 14, 465-474.
120. Sastry, M., Bewley, C., and Kwong, P. (2012). Mammalian expression of isotopically labeled proteins for nmr spectroscopy. In: Isotope labeling in biomolecular nmr, ed. Atreya, H.S., ed. (The Netherlands: Springer), pp. 197-211.
121. Satomi, Y., Shimonishi, Y., and Takao, T. (2004). N-glycosylation at Asn491 in the Asn-Xaa-Cys motif of human transferrin. FEBS Lett. 576, 51-56.
122. Scarisbrick, I.A., Sabharwal, P., Cruz, H., Larsen, N., Vandell, A.G., Blaber, S.I., Ameenuddin, S., Papke, L.M., Fehlings, M.G., Reeves, R.K., et al. (2006). Dynamic role of kallikrein 6 in traumatic spinal cord injury. Eur. J. Neurosci. 24, 1457-1469.
123. 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.
124. Schjoldager, K.T.B.G. and Clausen, H. (2012). Site-specific protein o-glycosylation modulates proprotein processing - deciphering specific functions of the large polypeptide GalNac-transferase gene family. BBA-Gen. Subjects 1820, 2079-2094.
125. Scully, J.L., Bartlett, J.D., Chaparian, M.G., Fukae, M., Uchida, T., Xue, J., Hu, C.C., and Simmer, J.P. (1998). Enamel matrix serine proteinase 1: stage-specific expression and molecular modeling. Connect. Tissue Res. 39, 111-122, discussion 141-149.
126. Seiz, L., Kotzsch, M., Grebenchtchikov, N.I., Geurts-Moespot, A.J., Fuessel, S., Goettig, P., Gkazepis, A., Wirth, M.P., Schmitt, M., Lossnitzer, A., et al. (2010). Polyclonal antibodies against kallikrein-related peptidase 4 (KLK4): immunohistochemical assessment of KLK4 expression in healthy tissues and prostate cancer. Biol. Chem. 391, 391-401.
127. Seiz, L., Dorn, J., Kotzsch, M., Walch, A., Grebenchtchikov, N.I., Gkazepis, A., Schmalfeldt, B., Kiechle, M., Bayani, J., Diamandis, E.P., et al. (2012). Stromal cell-associated expression of kallikrein-related peptidase 6 (KLK6) indicates poor prognosis of ovarian cancer patients. Biol. Chem. 393, 391-401.
128. Shaw, J.L.V. and Diamandis, E.P. (2007). Distribution of 15 human kallikreins in tissues and biological fluids. Clin. Chem. 53, 1423-1432.
129. Shaw, J.L.V., Grass, L., Sotiropoulou, G., and Diamandis, E.P. (2007). Development of an immunofluorometric assay for human kallikrein 15 (KLK15) and identification of klk15 in tissues and biological fluids. Clin. Biochem. 40, 104-110.
130. Shibata, K., Kajihara, J.-I., Kato, K., and Hirano, K. (1997). Purification and characterization of prostate specific antigen from human urine. BBA-Gen. Subjects 1336, 425-433.
131. Shimizu, C., Yoshida, S., Shibata, M., Kato, K., Momota, Y., Matsumoto, K., Shiosaka, T., Midorikawa, R., Kamachi, T., Kawabe, A., et al. (1998). Characterization of recombinant and brain neuropsin, a plasticity-related serine protease. J. Biol. Chem. 273, 11189-11196.
132. Simmer, J.P., Hu, Y., Lertlam, R., Yamakoshi, Y., and Hu, J.C.C. (2009). Hypomaturation enamel defects in KLK4 knockout/lacz knockin mice. J. Biol. Chem. 284, 19110-19121.
133. Sinha, U. and Wolf, D.L. (1993). Carbohydrate residues modulate the activation of coagulation factor X. J. Biol. Chem. 268, 3048-3051.
134. 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.
135. Steen, P.V.D., Rudd, P.M., Dwek, R.A., and Opdenakker, G. (1998). Concepts and principles of O-linked glycosylation. Crit. Rev. Biochem. Mol. Biol. 33, 151-208.
136. Stura, E.A., Muller, B.H., Bossus, M., Michel, S., Jolivet-Reynaud, C., and Ducancel, F. (2011). Crystal structure of human prostate-specific antigen in a sandwich antibody complex. J. Mol. Biol. 414, 530-544.
137. Sun, W., Parry, S., Panico, M., Morris, H.R., Kjellberg, M., Engstrom, A., Dell, A., and Schedin-Weiss, S. (2008). N-glycans and the N-terminus of protein C inhibitor affect the cofactor-enhanced rates of thrombin inhibition. J. Biol. Chem. 283, 18601-18611.
138. Tabares, G., Radcliffe, C.M., Barrabes, S., Ramirez, M., Aleixandre, R.N., Hoesel, W., Dwek, R.A., Rudd, P.M., Peracaula, R., and De Llorens, R. (2006). Different glycan structures in prostate-specific antigen from prostate cancer sera in relation to seminal plasma psa. Glycobiology 16, 132-145.
139. Tabares, G., Jung, K., Reiche, J., Stephan, C., Lein, M., Peracaula, R., De Llorens, R., and Hoesel, W. (2007). Free PSA forms in prostatic tissue and sera of prostate cancer patients: analysis by 2-D and Western blotting of immunopurified samples. Clin. Biochem. 40, 343-350.
140. Tajiri, M., Ohyama, C., and Wada, Y. (2008). Oligosaccharide profiles of the prostate specific antigen in free and complexed forms from the prostate cancer patient serum and in seminal plasma: a glycopeptide approach. Glycobiology 18, 2-8.
141. Takahashi, N., Tsukamoto, Y., Shiosaka, S., Kishi, T., Hakoshima, T., Arata, Y., Yamaguchi, Y., Kato, K., and Shimada, I. (1999). N-glycan structures of murine hippocampus serine protease, neuropsin, produced in trichoplusia ni cells. Glycoconjugate J. 16, 405-414.
142. Takayama, T.K., Fujikawa, K., and Davie, E.W. (1997). Characterization of the precursor of prostate-specific antigen-activation by trypsin and by human glandular kallikrein. J. Biol. Chem. 272, 21582-21588.
143. Takayama, T.K., Carter, C.A., and Deng, T. (2001a). Activation of prostate-specific antigen precursor (pro-PSA) by prostin, a novel human prostatic serine protease identified by degenerate PCR. Biochemistry 40, 1679-1687.
144. Takayama, T.K., McMullen, B.A., Nelson, P.S., Matsumura, M., and Fujikawa, K. (2001b). 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.
145. Tamura, H., Ishikawa, Y., Hino, N., Maeda, M., Yoshida, S., Kaku, S., and Shiosaka, S. (2006). Neuropsin is essential for early processes of memory acquisition and schaffer collateral long-term potentiation in adult mouse hippocampus in vivo. J. Physiol. 570, 541-551.
146. Thanka Christlet, T.H. and Veluraja, K. (2001). Database analysis of O-glycosylation sites in proteins. Biophys J. 80, 952-960.
147. Timm, D.E. (1997). The crystal structure of the mouse glandular kallikrein-13 (prorenin converting enzyme). Protein Sci 6, 1418-1425.
148. Varki, A., Freeze, H.H., and Gagneux, P. (2009). Evolution of glycan diversity. In: Essentials of glycobiology, Varki, A., Cummings, R.D., Esko, J.D., Freeze, H.H., Stanley, P., Bertozzi, C.R., Hart, G.W. and Etzler, M.E., eds. (Cold Spring Harbour: Cold Spring Harbour Laboratory Press), pp. 281-292.
149. Vermassen, T., Speeckaert, M.M., Lumen, N., Rottey, S., and Delanghe, J.R. (2012). Glycosylation of prostate specific antigen and its potential diagnostic applications. Clinica Chimica Acta 413, 1500-1505.
150. Wang, J., Chao, J., and Chao, L. (1991). Purification and characterization of recombinant tissue kallikrein from Escherichia coli and yeast. Biochem. J. 276 (Pt 1), 63-71.
151. Wang, L. and Dobberstein, B. (1999). Oligomeric complexes involved in translocation of proteins across the membrane of the endoplasmic reticulum. FEBS Letters 457, 316-322.
152. Wang, S.-K., Hu, Y., Simmer, J.P., Seymen, F., Estrella, N.M.R.P., Pal, S., Reid, B.M., Yildirim, M., Bayram, M., Bartlett, J.D., et al. (2013). Novel KLK4 and MMP20 mutations discovered by whole-exome sequencing. J. Dent. Res. 92, 266-271.
153. Watson, E., Shah, B., Leiderman, L., Hsu, Y.-R., Karkare, S., Lu, H.S., and Lin, F.-K. (1994). Comparison of n-linked oligosaccharides of recombinant human tissue kallikrein produced by chinese hamster ovary cells on microcarrier beads and in serum-free suspension culture. Biotechnol. Progr. 10, 39-44.
154. Wendorf, P., Geyer, R., Sziegoleit, A., and Linder, D. (1989). Localization and characterization of the glycosylation site of human pancreatic elastase 1. FEBS Lett. 249, 275-278.
155. White, K.Y., Rodemich, L., Nyalwidhe, J.O., Comunale, M.A., Clements, M.A., Lance, R.S., Schellhammer, P.F., Mehta, A.S., Semmes, O.J., and Drake, R.R. (2009). Glycomic characterization of prostate-specific antigen and prostatic acid phosphatase in prostate cancer and benign disease seminal plasma fluids. J. Prot. Res. 8, 620-630.
156. Wopereis, S., Lefeber, D.J., Morava, É., and Wevers, R.A. (2006). Mechanisms in protein O-glycan biosynthesis and clinical and molecular aspects of protein O-glycan biosynthesis defects: a review. Clin. Chem. 52, 574-600.
157. Yahiro, J. and Nagato, T. (2002). Distribution of kallikrein in striated duct cells of monkey submandibular glands. Arch. Oral Biol. 47, 631-635.
158. Yamakoshi, Y., Yamakoshi, F., Hu, J.C.C., and Simmer, J.P. (2011). Characterization of kallikrein-related peptidase 4 glycosylations. Eur. J. Oral Sci. 119, 234-240.
159. Yang, L., Manithody, C., and Rezaie, A.R. (2009). Functional role of o-linked and n-linked glycosylation sites present on the activation peptide of factor X. J. Thromb. Haemostas. 7, 1696-1702.
160. 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.
161. Yoshimasu, M.A., Tanaka, T., Ahn, J.-K., and Yada, R.Y. (2004). Effect of N-linked glycosylation on the aspartic proteinase porcine pepsin expressed from Pichia pastoris. Glycobiology 14, 417-429.
162. Yousef, G.M., Kapadia, C., Polymeris, M.E., Borgono, C., Hutchinson, S., Wasney, G.A., Soosaipillai, A., and Diamandis, E.P. (2003). The human kallikrein protein 5 (hK5) is enzymatically active, glycosylated and forms complexes with two protease inhibitors in ovarian cancer fluids. Biochim. Biophys. Acta. 1628, 88-96.
163. Zheng, X., Lu, D., and Sadler, J.E. (1999). Apical sorting of bovine enteropeptidase does not involve detergent-resistant association with sphingolipid-cholesterol rafts. J. Biol. Chem. 274, 1596-1605.
164. Zielinska, D.F., Gnad, F., Wiśniewski, J.R., and Mann, M. (2010). Precision mapping of an in vivo N-glycoproteome reveals rigid topological and sequence constraints. Cell 141, 897-907.
165. Zielinska, D.F., Gnad, F., Schropp, K., Wiśniewski, J., and Mann, M. (2012). Mapping N-glycosylation sites across seven evolutionarily distant species reveals a divergent substrate proteome despite a common core machinery. Mol. Cell 46, 542-548.