Targeting the autolysis loop of urokinase-type plasminogen activator with conformation-specific monoclonal antibodies

Biochemical Journal

Volumn 438, Issue 1, 2011, Pages 39-51

  Botkjaer, Kenneth A ^a   Fogh, Sarah ^a   Bekes, Erin C ^b   Chen, Zhuo ^a,c   Blouse, Grant E ^a   Jensen, Janni M ^a   Mortensen, Kim K ^a   Huang, Mingdong ^a,c   Deryugina, Elena ^b   Quigley, James P ^b   Declerck, Paul J ^d   Andreasen, Peter A ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

^c FUJIAN INSTITUTE OF RESEARCH ON THE STRUCTURE OF MATTER   (China)

^d UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Antibody; Cancer; Conformation; Immunofluorescence; Urokinase type plasminogen activator (uPA); Zymogen

Indexed keywords

APROTININ; ENZYME PRECURSOR; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 101; MONOCLONAL ANTIBODY 112; MONOCLONAL ANTIBODY 12E6B10; PLASMINOGEN; UNCLASSIFIED DRUG; UROKINASE;

ANTIBODY SPECIFICITY; ARTICLE; AUTOLYSIS; BINDING AFFINITY; CANCER INHIBITION; CANCER INVASION; CATALYSIS; CELL CULTURE; CELL STRAIN HEK293; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; FEASIBILITY STUDY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; PLASMINOGEN ACTIVATION; PRIORITY JOURNAL; PROTEIN TARGETING;

ANIMALS; ANTIBODIES, MONOCLONAL; AUTOLYSIS; CELL MOVEMENT; CHICK EMBRYO; ENZYME ACTIVATION; ENZYME PRECURSORS; FIBRINOLYTIC AGENTS; HUMANS; HYDROLYSIS; KINETICS; MICE; MICE, INBRED BALB C; PLASMINOGEN; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; SURFACE PLASMON RESONANCE; UROKINASE-TYPE PLASMINOGEN ACTIVATOR;

EID: 79960721542     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110129     Document Type: Article

References (46)

1. Bode, W., Schwager, P. and Huber, R. (1978) The transition of bovine trypsinogen to a trypsin-like state upon strong ligand binding. The refined crystal structures of the bovine trypsinogen-pancreatic trypsin inhibitor complex and of its ternary complex with Ile-Val at 1.9 A resolution. J. Mol. Biol. 118, 99-112
2. Hedstrom, L. (2002) Serine protease mechanism and specificity. Chem. Rev. 102, 4501-4524
3. Ye, S. and Goldsmith, E. J. (2001) Serpins and other covalent protease inhibitors. Curr. Opin. Struct. Biol. 11, 740-745
4. Huntington, J. A. (2006) Shape-shifting serpins-advantages of a mobile mechanism. Trends Biochem. Sci. 31, 427-435
5. Dupont, D. M., Madsen, J. B., Kristensen, T., Bodker, J. S., Blouse, G. E., Wind, T. and Andreasen, P. A. (2009) Biochemical properties of plasminogen activator inhibitor-1. Front. Biosci. 14, 1337-1361
6. Dano, K., Andreasen, P. A., Grondahl-Hansen, J., Kristensen, P., Nielsen, L. S. and Skriver, L. (1985) Plasminogen activators, tissue degradation, and cancer. Adv. Cancer Res. 44, 139-266
7. Andreasen, P. A., Kjoller, L., Christensen, L. and Duffy, M. J. (1997) The urokinase-type plasminogen activator system in cancer metastasis: a review. Int. J. Cancer. 72, 1-22
8. Andreasen, P. A., Egelund, R. and Petersen, H. H. (2000) The plasminogen activation system in tumor growth, invasion, and metastasis. Cell. Mol. Life Sci. 57, 25-40
9. List, K., Jensen, O. N., Bugge, T. H., Lund, L. R., Ploug, M., Dano, 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 plasminogen-deficient mice. Biochemistry 39, 508-515
10. Kilpatrick, L. M., Harris, R. L., Owen, K. A., Bass, R., Ghorayeb, C., Bar-Or, A. and Ellis, V. (2006) Initiation of plasminogen activation on the surface of monocytes expressing the type II transmembrane serine protease matriptase. Blood 108, 2616-2623
11. Moran, P., Li, W., Fan, B., Vij, R., Eigenbrot, C. and Kirchhofer, D. (2006) Pro-urokinase-type plasminogen activator is a substrate for hepsin. J. Biol. Chem. 281, 30439-30446
12. Dickinson, C. D., Shobe, J. and Ruf, W. (1998) Influence of cofactor binding and active site occupancy on the conformation of the macromolecular substrate exosite of factor VIIa. J. Mol. Biol. 277, 959-971
13. Shobe, J., Dickinson, C. D. and Ruf, W. (1999) Regulation of the catalytic function of coagulation factor VIIa by a conformational linkage of surface residue Glu 154 to the active site. Biochemistry 38, 2745-2751
14. Ganesan, R., Eigenbrot, C., Wu, Y., Liang, W. C., Shia, S., Lipari, M. T. and Kirchhofer, D. (2009) Unraveling the allosteric mechanism of serine protease inhibition by an antibody. Structure 17, 1614-1624
15. Blouse, G. E., Botkjaer, K. A., Deryugina, E., Byszuk, A. A., Jensen, J. M., Mortensen, K. K., Quigley, J. P. and Andreasen, P. A. (2009) A novel mode of intervention with serine protease activity: targeting zymogen activation. J. Biol. Chem. 284, 4647-4657
16. Egelund, R., Petersen, T. E. and Andreasen, P. A. (2001) A serpin-induced extensive proteolytic susceptibility of urokinase-type plasminogen activator implicates distortion of the proteinase substrate-binding pocket and oxyanion hole in the serpin inhibitory mechanism. Eur. J. Biochem. 268, 673-685
17. Botkjaer, K. A., Byszuk, A. A., Andersen, L. M., Christensen, A., Andreasen, P. A. and Blouse, G. E. (2009) Nonproteolytic induction of catalytic activity into the single-chain form of urokinase-type plasminogen activator by dipeptides. Biochemistry 48, 9606-9617
18. Petersen, H. H., Hansen, M., Schousboe, S. L. and Andreasen, P. A. (2001) Localization of epitopes for monoclonal antibodies to urokinase-type plasminogen activator: relationship between epitope localization and effects of antibodies on molecular interactions of the enzyme. Eur. J. Biochem. 268, 4430-4439
19. Dupont, D. M., Blouse, G. E., Hansen, M., Mathiasen, L., Kjelgaard, S., Jensen, J. K., Christensen, A., Gils, A., Declerck, P. J., Andreasen, P. A. and Wind, T. (2006) Evidence for a pre-latent form of the serpin plasminogen activator inhibitor-1 with a detached β-strand 1C. J. Biol. Chem. 281, 36071-36081
20. Wind, T., Jensen, J. K., Dupont, D. M., Kulig, P. and Andreasen, P. A. (2003) Mutational analysis of plasminogen activator inhibitor-1. Eur. J. Biochem. 270, 1680-1688
21. Declerck, P. J., Lijnen, H. R., Verstreken, M., Moreau, H. and Collen, D. (1990) A monoclonal antibody specific for two-chain urokinase-type plasminogen activator. Application to the study of the mechanism of clot lysis with single-chain urokinase-type plasminogen activator in plasma. Blood 75, 1794-1800
22. Jespersen, M. H., Jensen, J., Rasmussen, L. H., Ejlersen, E., Moller-Petersen, J. and Sperling-Petersen, H. U. (1993) The reference range for complexed α2-macroglobulin human plasma: development of a new enzyme linked in immunosorbent assay (ELISA) for quantitation of complexed α2-macroglobulin. Scand. J. Clin. Lab. Invest 53, 639-648
23. Knoop, A., Andreasen, P. A., Andersen, J. A., Hansen, S., Laenkholm, A. V., Simonsen, A. C., Andersen, J., Overgaard, J. and Rose, C. (1998) Prognostic significance of urokinase-type plasminogen activator and plasminogen activator inhibitor-1 in primary breast cancer. Br. J. Cancer. 77, 932-940
24. Nielsen, L. S., Andreasen, P. A., Grondahl-Hansen, J., Huang, J. Y., Kristensen, P. and Dano, K. (1986) Monoclonal antibodies to human 54,000 molecular weight plasminogen activator inhibitor from fibrosarcoma cells-inhibitor neutralization and one-step affinity purification. Thromb. Haemost. 55, 206-212
25. Gils, A., Pedersen, K. E., Skottrup, P., Christensen, A., Naessens, D., Deinum, J., Enghild, J. J., Declerck, P. J. and Andreasen, P. A. (2003) Biochemical importance of glycosylation of plasminogen activator inhibitor-1. Thromb. Haemost. 90, 206-217
26. Conn, E. M., Botkjaer, K. A., Kupriyanova, T. A., Andreasen, P. A., Deryugina, E. I. and Quigley, J. P. (2009) Comparative analysis of metastasis variants derived from human prostate carcinoma cells: roles in intravasation of VEGF-mediated angiogenesis and uPA-mediated invasion. Am. J. Pathol. 175, 1638-1652
27. Lund, L. R., Georg, B., Nielsen, L. S., Mayer, M., Dano, K. and Andreasen, P. A. (1988) Plasminogen activator inhibitor type 1: cell-specific and differentiation-induced expression and regulation in human cell lines, as determined by enzyme-linked immunosorbent assay. Mol. Cell. Endocrinol. 60, 43-53
28. Reference deleted
29. Skriver, L., Nielsen, L. S., Stephens, R. and Dano, K. (1982) Plasminogen activator released as inactive proenzyme from murine cells transformed by sarcoma virus. Eur. J. Biochem. 124, 409-414
30. Nielsen, L. S., Hansen, J. G., Skriver, L., Wilson, E. L., Kaltoft, K., Zeuthen, J. and Dano, K. (1982) Purification of zymogen to plasminogen activator from human glioblastoma cells by affinity chromatography with monoclonal antibody. Biochemistry 21, 6410-6415 (Pubitemid 13141147)
31. Behrendt, N., List, K., Andreasen, P. A. and Dano, K. (2003) The pro-urokinase plasminogen-activation system in the presence of serpin-type inhibitors and the urokinase receptor: rescue of activity through reciprocal pro-enzyme activation. Biochem. J. 371, 277-287 (Pubitemid 36547610)
32. Ellis, V. and Dano, K. (1993) Potentiation of plasminogen activation by an anti-urokinase monoclonal antibody due to ternary complex formation. A mechanistic model for receptor-mediated plasminogen activation. J. Biol. Chem. 268, 4806-4813
33. Mathiasen, L., Dupont, D. M., Christensen, A., Blouse, G. E., Jensen, J. K., Gils, A., Declerck, P. J., Wind, T. and Andreasen, P. A. (2008) A peptide accelerating the conversion of plasminogen activator inhibitor-1 to an inactive latent state. Mol. Pharmacol. 74, 641-653
34. Kaltoft, K., Nielsen, L. S., Zeuthen, J. and Dano, K. (1982) Monoclonal antibody that specifically inhibits a human Mr 52,000 plasminogen-activating enzyme. Proc. Natl. Acad. Sci. U.S.A. 79, 3720-3723
35. Lund, I. K., Jogi, A., Rono, B., Rasch, M. G., Lund, L. R., Almholt, K., Gardsvoll, H., Behrendt, N., Romer, J. and Hoyer-Hansen, G. (2008) Antibody-mediated targeting of the urokinase-type plasminogen activator proteolytic function neutralizes fibrinolysis in vivo. J. Biol. Chem. 283, 32506-32515
36. Jogi, A., Rono, B., Lund, I. K., Nielsen, B. S., Ploug, M., Hoyer-Hansen, G., Romer, J. and Lund, L. R. (2010) Neutralisation of uPA with a monoclonal antibody reduces plasmin formation and delays skin wound healing in tPA-deficient mice. PLoS One 5, e12746
37. Scheuerlein, J. G., Kalies, I., Gluth, W. P. and Kalden, J. R. (1991) Monoclonal antibodies monospecific to single-chain urokinase-type plasminogen activator (scu-PA). Hybridoma 10, 395-399
38. Ke, S. H., Tachias, K., Lamba, D., Bode, W. and Madison, E. L. (1997) Identification of a hydrophobic exosite on tissue type plasminogen activator that modulates specificity for plasminogen. J. Biol. Chem. 272, 1811-1816
39. Lin, Z., Jiang, L., Yuan, C., Jensen, J. K., Zhang, X., Luo, Z., Furie, B. C., Furie, B., Andreasen, P. A. and Huang, M. (2011) Structural basis for recognition of urokinase-type plasminogen activator by plasminogen activator inhibitor-1. J Biol Chem. 286, 7027-7032
40. Reference deleted
41. Zhao, G., Yuan, C., Wind, T., Huang, Z., Andreasen, P. A. and Huang, M. (2007) Structural basis of specificity of a peptidyl urokinase inhibitor, upain-1. J. Struct. Biol. 160, 1-10
42. Bolognesi, M., Gatti, G., Menagatti, E., Guarneri, M., Marquart, M., Papamokos, E. and Huber, R. (1982) Three-dimensional structure of the complex between pancreatic secretory trypsin inhibitor (Kazal type) and trypsinogen at 1.8 A resolution. Structure solution, crystallographic refinement and preliminary structural interpretation. J. Mol. Biol. 162, 839-868
43. Arnold, K., Bordoli, L., Kopp, J. and Schwede, T. (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201 (Pubitemid 43205406)
44. Huntington, J. A., Read, R. J. and Carrell, R. W. (2000) Structure of a serpin-protease complex shows inhibition by deformation. Nature 407, 923-926
45. Jensen, J. K. and Gettins, P. G. (2008) High-resolution structure of the stable plasminogen activator inhibitor type-1 variant 14-1B in its proteinase-cleaved form: a new tool for detailed interaction studies and modeling. Protein Sci. 17, 1844-1849
46. Spraggon, G., Phillips, C., Nowak, U. K., Ponting, C. P., Saunders, D., Dobson, C. M., Stuart, D. I. and Jones, E. Y. (1995) The crystal structure of the catalytic domain of human urokinase-type plasminogen activator. Structure 3, 681-691