Fetuin-a and cystatin C are endogenous inhibitors of human Meprin metalloproteases

Biochemistry

Volumn 49, Issue 39, 2010, Pages 8599-8607

  Hedrich, Jana ^a   Lottaz, Daniel ^b   Meyer, Katharina ^a   Yiallouros, Irene ^a   Jahnen Dechent, Willi ^c   Stöcker, Walter ^a   Becker Pauly, Christoph ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b UNIVERSITY OF BERN   (Switzerland)

^c RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE PHASE PROTEINS; CYSTATINS; CYTOKINES; ENDOGENOUS INHIBITOR; HUMAN PLASMAS; INFLAMMATORY BOWEL DISEASE; INFLAMMATORY DISEASE; INHIBITION CONSTANTS; INTERLEUKIN-1; INTERLEUKIN-18; KINETIC STUDY; MEPRINS; METALLOPROTEASES; METALLOPROTEINASES; PHYSIOLOGICAL REGULATORS; PROTEASE INHIBITOR; PROTEOLYTIC ENZYME; RESIDUAL ACTIVITY; TUMOR GROWTH;

ZINC;

PROTEINS;

ASTACIN; CHYMOTRYPSIN; CYSTATIN C; FETUIN A; MEPRIN; MEPRIN ALPHA; MEPRIN BETA; PROTEIN; PROTEIN LAST; PROTEIN LAST MAM; RECOMBINANT ENZYME; TRYPSIN; UNCLASSIFIED DRUG;

ADULT; AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; HUMAN; MALE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; BLOOD PROTEINS; CARPS; CATTLE; CYSTATIN C; HUMANS; METALLOENDOPEPTIDASES; MOLECULAR SEQUENCE DATA; PLASMA; SEQUENCE ALIGNMENT;

BOVINAE; CYPRINIDAE;

EID: 77957286829     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi1004238     Document Type: Article

References (59)

1. Bond, J. S. and Beynon, R. J. (1995) The astacin family of metalloendopeptidases Protein Sci. 4, 1247-1261
2. Stocker, W., Grams, F., Baumann, U., Reinemer, P., Gomis-Ruth, F. X., McKay, D. B., and Bode, W. (1995) The metzincins: Topological and sequential relations between the astacins, adamalysins, serralysins, and matrixins (collagenases) define a superfamily of zinc peptidases Protein Sci. 4, 823-840
3. Sterchi, E. E., Stocker, W., and Bond, J. S. (2008) Meprins, membrane-bound and secreted astacin metalloproteinases Mol. Aspects Med. 29, 309-328
4. Bertenshaw, G. P., Norcum, M. T., and Bond, J. S. (2003) Structure of homo- and hetero-oligomeric meprin metalloproteases. Dimers, tetramers, and high molecular mass multimers J. Biol. Chem. 278, 2522-2532
5. Becker, C., Kruse, M. N., Slotty, K. A., Kohler, D., Harris, J. R., Rosmann, S., Sterchi, E. E., and Stocker, W. (2003) Differences in the activation mechanism between the α and β subunits of human meprin Biol. Chem. 384, 825-831
6. Hahn, D., Pischitzis, A., Roesmann, S., Hansen, M. K., Leuenberger, B., Luginbuehl, U., and Sterchi, E. E. (2003) Phorbol 12-myristate 13-acetate-induced ectodomain shedding and phosphorylation of the human meprin β metalloprotease J. Biol. Chem. 278, 42829-42839
7. Banerjee, S. and Bond, J. S. (2008) Prointerleukin-18 is activated by meprin β in vitro and in vivo in intestinal inflammation J. Biol. Chem. 283, 31371-31377
8. Oneda, B., Lods, N., Lottaz, D., Becker-Pauly, C., Stocker, W., Pippin, J., Huguenin, M., Ambort, D., Marti, H. P., and Sterchi, E. E. (2008) Metalloprotease meprin β in rat kidney: Glomerular localization and differential expression in glomerulonephritis PLoS One 3, e2278
9. Becker-Pauly, C., Howel, M., Walker, T., Vlad, A., Aufenvenne, K., Oji, V., Lottaz, D., Sterchi, E. E., Debela, M., Magdolen, V., Traupe, H., and Stocker, W. (2007) The α and β subunits of the metalloprotease meprin are expressed in separate layers of human epidermis, revealing different functions in keratinocyte proliferation and differentiation J. Invest. Dermatol. 127, 1115-1125
10. Lottaz, D., Hahn, D., Muller, S., Muller, C., and Sterchi, E. E. (1999) Secretion of human meprin from intestinal epithelial cells depends on differential expression of the α and β subunits Eur. J. Biochem. 259, 496-504
11. Crisman, J. M., Zhang, B., Norman, L. P., and Bond, J. S. (2004) Deletion of the mouse meprin β metalloprotease gene diminishes the ability of leukocytes to disseminate through extracellular matrix J. Immunol. 172, 4510-4519
12. Huguenin, M., Muller, E. J., Trachsel-Rosmann, S., Oneda, B., Ambort, D., Sterchi, E. E., and Lottaz, D. (2008) The metalloprotease meprinbeta processes E-cadherin and weakens intercellular adhesion PLoS One 3, e2153
13. Bergin, D. A., Greene, C. M., Sterchi, E. E., Kenna, C., Geraghty, P., Belaaouaj, A., Taggart, C. C., O'Neill, S. J., and McElvaney, N. G. (2008) Activation of the epidermal growth factor receptor (EGFR) by a novel metalloprotease pathway J. Biol. Chem. 283, 31736-31744
14. Herzog, C., Haun, R. S., Kaushal, V., Mayeux, P. R., Shah, S. V., and Kaushal, G. P. (2009) Meprin A and meprin α generate biologically functional IL-1β from pro-IL-1β Biochem. Biophys. Res. Commun. 379, 904-908
15. Schütte, A., Hedrich, J., Stöcker, W., and Becker-Pauly, C. (2010) Let It Flow: Morpholino Knockdown in Zebrafish Embryos Reveals a Pro-Angiogenic Effect of the Metalloprotease Meprin α2 PLoS One 5 e8835
16. Banerjee, S., Oneda, B., Yap, L. M., Jewell, D. P., Matters, G. L., Fitzpatrick, L. R., Seibold, F., Sterchi, E. E., Ahmad, T., Lottaz, D., and Bond, J. S. (2009) MEP1A allele for meprin A metalloprotease is a susceptibility gene for inflammatory bowel disease Mucosal Immunol. 2, 220-231
17. Lottaz, D., Maurer, C. A., Hahn, D., Buchler, M. W., and Sterchi, E. E. (1999) Nonpolarized secretion of human meprin α in colorectal cancer generates an increased proteolytic potential in the stroma Cancer Res. 59, 1127-1133
18. Villa, J. P., Bertenshaw, G. P., and Bond, J. S. (2003) Critical amino acids in the active site of meprin metalloproteinases for substrate and peptide bond specificity J. Biol. Chem. 278, 42545-42550
19. Kruse, M. N., Becker, C., Lottaz, D., Kohler, D., Yiallouros, I., Krell, H. W., Sterchi, E. E., and Stocker, W. (2004) Human meprin α and β homo-oligomers: Cleavage of basement membrane proteins and sensitivity to metalloprotease inhibitors Biochem. J. 378, 383-389
20. Ohler, A., Debela, M., Wagner, S., Magdolen, V., and Becker-Pauly, C. (2010) Analyzing the protease web in skin: Meprin metalloproteases are activated specifically by KLK4, 5 and 8 vice versa leading to processing of proKLK7 thereby triggering its activation Biol. Chem. 391, 455-460
21. Rosmann, S., Hahn, D., Lottaz, D., Kruse, M. N., Stocker, W., and Sterchi, E. E. (2002) Activation of human meprin-α in a cell culture model of colorectal cancer is triggered by the plasminogen-activating system J. Biol. Chem. 277, 40650-40658
22. Hirano, M., Ma, B. Y., Kawasaki, N., Okimura, K., Baba, M., Nakagawa, T., Miwa, K., Kawasaki, N., Oka, S., and Kawasaki, T. (2005) Mannan-binding protein blocks the activation of metalloproteases meprin α and β J. Immunol. 175, 3177-3185
23. Abrahamson, M., Alvarez-Fernandez, M., and Nathanson, C. M. (2003) Cystatins Biochem. Soc. Symp., 179-199
24. Brzin, J., Popovic, T., Turk, V., Borchart, U., and Machleidt, W. (1984) Human cystatin, a new protein inhibitor of cysteine proteinases Biochem. Biophys. Res. Commun. 118, 103-109
25. Barrett, A. J., Davies, M. E., and Grubb, A. (1984) The place of human κ-trace (cystatin C) amongst the cysteine proteinase inhibitors Biochem. Biophys. Res. Commun. 120, 631-636
26. Abrahamson, M., Olafsson, I., Palsdottir, A., Ulvsback, M., Lundwall, A., Jensson, O., and Grubb, A. (1990) Structure and expression of the human cystatin C gene Biochem. J. 268, 287-294
27. Abrahamson, M., Barrett, A. J., Salvesen, G., and Grubb, A. (1986) Isolation of six cysteine proteinase inhibitors from human urine. Their physicochemical and enzyme kinetic properties and concentrations in biological fluids J. Biol. Chem. 261, 11282-11289
28. Tsai, P. L., Chen, C. H., Huang, C. J., Chou, C. M., and Chang, G. D. (2004) Purification and cloning of an endogenous protein inhibitor of carp nephrosin, an astacin metalloproteinase J. Biol. Chem. 279, 11146-11155
29. Lee, C., Bongcam-Rudloff, E., Sollner, C., Jahnen-Dechent, W., and Claesson-Welsh, L. (2009) Type 3 cystatins; fetuins, kininogen and histidine-rich glycoprotein Front. Biosci. 14, 2911-2922
30. Nawratil, P., Lenzen, S., Kellermann, J., Haupt, H., Schinke, T., Muller-Esterl, W., and Jahnen-Dechent, W. (1996) Limited proteolysis of human α2-HS glycoprotein/fetuin. Evidence that a chymotryptic activity can release the connecting peptide J. Biol. Chem. 271, 31735-31741
31. Terkelsen, O. B., Jahnen-Dechent, W., Nielsen, H., Moos, T., Fink, E., Nawratil, P., Muller-Esterl, W., and Mollgard, K. (1998) Rat fetuin: Distribution of protein and mRNA in embryonic and neonatal rat tissues Anat. Embryol. 197, 125-133
32. Dziegielewska, K. M., Andersen, N. A., Lovell, D., Nicol, S. C., Muller-Esterl, W., and Saunders, N. R. (1992) Fetuin: A new acute phase protein in the adult and in the fetus Folia Histochem. Cytobiol. 30, 187-189
33. Lebreton, J. P., Joisel, F., Raoult, J. P., Lannuzel, B., Rogez, J. P., and Humbert, G. (1979) Serum concentration of human α2 HS glycoprotein during the inflammatory process: Evidence that α2 HS glycoprotein is a negative acute-phase reactant J. Clin. Invest. 64, 1118-1129
34. Wang, X. Q., Hayes, M. T., Kempf, M., Fraser, J. F., Liu, P. Y., Cuttle, L., Friend, L. R., Rothnagel, J. A., Saunders, N. A., and Kimble, R. M. (2008) Fetuin-A: A major fetal serum protein that promotes "wound closure" and scarless healing J. Invest. Dermatol. 128, 753-757
35. Schafer, C., Heiss, A., Schwarz, A., Westenfeld, R., Ketteler, M., Floege, J., Muller-Esterl, W., Schinke, T., and Jahnen-Dechent, W. (2003) The serum protein α2-Heremans-Schmid glycoprotein/fetuin-A is a systemically acting inhibitor of ectopic calcification J. Clin. Invest. 112, 357-366
36. Dziegielewska, K. M., Andersen, N. A., and Saunders, N. R. (1998) Modification of macrophage response to lipopolysaccharide by fetuin Immunol. Lett. 60, 31-35
37. Wang, H., Zhang, M., Bianchi, M., Sherry, B., Sama, A., and Tracey, K. J. (1998) Fetuin (α2-HS-glycoprotein) opsonizes cationic macrophage-deactivating molecules Proc. Natl. Acad. Sci. U.S.A. 95, 14429-14434
38. Srinivas, P. R., Wagner, A. S., Reddy, L. V., Deutsch, D. D., Leon, M. A., Goustin, A. S., and Grunberger, G. (1993) Serum α2-HS-glycoprotein is an inhibitor of the human insulin receptor at the tyrosine kinase level Mol. Endocrinol. 7, 1445-1455
39. Galembeck, F. and Cann, J. R. (1974) Fetuin as a trypsin inhibitor Arch. Biochem. Biophys. 164, 326-331
40. Ashida, H., Yamamoto, K., and Kumagai, H. (2000) Trypsin inhibitory activity of bovine fetuin de-O-glycosylated by endo-α-N- acetylgalactosaminidase Biosci., Biotechnol., Biochem. 64, 2266-2268
41. Song, H. D., Sun, X. J., Deng, M., Zhang, G. W., Zhou, Y., Wu, X. Y., Sheng, Y., Chen, Y., Ruan, Z., Jiang, C. L., Fan, H. Y., Zon, L. I., Kanki, J. P., Liu, T. X., Look, A. T., and Chen, Z. (2004) Hematopoietic gene expression profile in zebrafish kidney marrow Proc. Natl. Acad. Sci. U.S.A. 101, 16240-16245
42. Becker-Pauly, C., Bruns, B. C., Damm, O., Schutte, A., Hammouti, K., Burmester, T., and Stocker, W. (2009) News from an ancient world: Two novel astacin metalloproteases from the horseshoe crab J. Mol. Biol. 385, 236-248
43. Stocker, W., Sauer, B., and Zwilling, R. (1991) Kinetics of nitroanilide cleavage by astacin Biol. Chem. 372, 385-392
44. Ketteler, M., Wanner, C., Metzger, T., Bongartz, P., Westenfeld, R., Gladziwa, U., Schurgers, L. J., Vermeer, C., Jahnen-Dechent, W., and Floege, J. (2003) Deficiencies of calcium-regulatory proteins in dialysis patients: A novel concept of cardiovascular calcification in uremia Kidney Int., Suppl., S84-S87
45. Bieth, J. G. (1984) In vivo significance of kinetic constants of protein proteinase inhibitors Biochem. Med. 32, 387-397
46. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., and Higgins, D. G. (1997) The CLUSTAL-X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools Nucleic Acids Res. 25, 4876-4882
47. Meier, U. C., Boetzel, J., Kellermann, J., Mann, K., Billich, A., Stocker, W., and Schramm, H. J. (1994) The cleavage of the bait region of α2-macroglobulin by human immunodeficiency virus proteinases and by astacin Ann. N.Y. Acad. Sci. 737, 431-433
48. Chau, P., Fielding, P. E., and Fielding, C. J. (2007) Bone morphogenetic protein-1 (BMP-1) cleaves human proapolipoprotein A1 and regulates its activation for lipid binding Biochemistry 46, 8445-8450
49. Zhang, Y., Ge, G., and Greenspan, D. S. (2006) Inhibition of bone morphogenetic protein 1 by native and altered forms of α2-macroglobulin J. Biol. Chem. 281, 39096-39104
50. Bond, J. S., Matters, G. L., Banerjee, S., and Dusheck, R. E. (2005) Meprin metalloprotease expression and regulation in kidney, intestine, urinary tract infections and cancer FEBS Lett. 579, 3317-3322
51. Swallow, C. J., Partridge, E. A., Macmillan, J. C., Tajirian, T., DiGuglielmo, G. M., Hay, K., Szweras, M., Jahnen-Dechent, W., Wrana, J. L., Redston, M., Gallinger, S., and Dennis, J. W. (2004) α2HS-glycoprotein, an antagonist of transforming growth factor beta in vivo, inhibits intestinal tumor progression Cancer Res. 64, 6402-6409
52. Kundranda, M. N., Henderson, M., Carter, K. J., Gorden, L., Binhazim, A., Ray, S., Baptiste, T., Shokrani, M., Leite-Browning, M. L., Jahnen-Dechent, W., Matrisian, L. M., and Ochieng, J. (2005) The serum glycoprotein fetuin-A promotes Lewis lung carcinoma tumorigenesis via adhesive-dependent and adhesive-independent mechanisms Cancer Res. 65, 499-506
53. Turk, V., Stoka, V., and Turk, D. (2008) Cystatins: Biochemical and structural properties, and medical relevance Front. Biosci. 13, 5406-5420
54. Galteau, M. M., Guyon, M., Gueguen, R., and Siest, G. (2001) Determination of serum cystatin C: Biological variation and reference values Clin. Chem. Lab. Med. 39, 850-857
55. Janowski, R., Kozak, M., Jankowska, E., Grzonka, Z., Grubb, A., Abrahamson, M., and Jaskolski, M. (2001) Human cystatin C, an amyloidogenic protein, dimerizes through three-dimensional domain swapping Nat. Struct. Biol. 8, 316-320
56. Pallares, I., Bonet, R., Garcia-Castellanos, R., Ventura, S., Aviles, F. X., Vendrell, J., and Gomis-Ruth, F. X. (2005) Structure of human carboxypeptidase A4 with its endogenous protein inhibitor, latexin Proc. Natl. Acad. Sci. U.S.A. 102, 3978-3983
57. Nycander, M., Estrada, S., Mort, J. S., Abrahamson, M., and Bjork, I. (1998) Two-step mechanism of inhibition of cathepsin B by cystatin C due to displacement of the proteinase occluding loop FEBS Lett. 422, 61-64
58. Bjork, I., Pol, E., Raub-Segall, E., Abrahamson, M., Rowan, A. D., and Mort, J. S. (1994) Differential changes in the association and dissociation rate constants for binding of cystatins to target proteinases occurring on N-terminal truncation of the inhibitors indicate that the interaction mechanism varies with different enzymes Biochem. J. 299 (Part 1) 219-225
59. Bode, W., Engh, R., Musil, D., Laber, B., Stubbs, M., Huber, R., and Turk, V. (1990) Mechanism of interaction of cysteine proteinases and their protein inhibitors as compared to the serine proteinase-inhibitor interaction Biol. Chem. 371 (Suppl.) 111-118