An active zymogen: Unravelling the mystery of tissue-type plasminogen activator

Biological Chemistry

Volumn 379, Issue 2, 1998, Pages 95-103

  Stubbs, Milton T ^a   Renatus, Martin ^b   Bode, Wolfram ^b  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Activation; Cofactor; Fibrinolysis; Haemostasis; Proteinase; Structure

Indexed keywords

ENZYME PRECURSOR; FIBRIN; PLASMIN; PLASMINOGEN; PROTEINASE; TISSUE PLASMINOGEN ACTIVATOR;

BAT; FIBRINOLYSIS; HEMOSTASIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; REVIEW; SALIVA LEVEL; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CATALYSIS; ENZYME ACTIVATION; ENZYME PRECURSORS; FIBRIN; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN CONFORMATION; TISSUE PLASMINOGEN ACTIVATOR;

DESMODUS ROTUNDUS;

EID: 0031884607     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (63)

1. Bakker, A.H.F., Weening-Verhoeff, E.J.D., and Verheijen, J.H. (1995). The role of the lysyl binding site of tissue-type plasminogen activator in the interaction with a forming fibrin clot. J. Biol. Chem. 270, 12355-12360.
2. Becker, J.W., Marcy, A.I., Rokosz, L.L., Axel, M.G., Burbaum, J.J., Fitzgerald, P.M., Cameron, P.M., Esser, C.K., Hagmann, W.K., Hermes, J.D., and Springer, J.P. (1995). Stromelysin-1: three-dimensional structure of the inhibited catalytic domain and of the C-truncated proenzyme. Protein Sci. 10, 1966-1976.
3. Bennett, W.F., Paoni, N.F., Keyt, B.A., Botstein, D., Jones, A.J.S., Presta, L., Wurm, F.M., and Zoller, M.J. (1991). High resolution analysis of functional determinants on human tissue-type plasminogen activator. J. Biol. Chem. 266, 5191-5201.
4. Bode, W. (1979). The transition of bovine trypsinogen to a trypsin-like state upon strong ligand binding. II. The binding of the pancreatic trypsin inhibitor and of isoleucine-valine and of sequentially related peptides to trypsinogen and to p-guanidino-benzoate-trypsinogen. J. Mol. Biol. 127, 357-374.
5. Bode, W., Fehlhammer, H., and Huber, R. (1976). Crystal structure of bovine trypsinogen at 1.8 Å resolution. I. Data collection, application of Patterson search techniques and preliminary structural interpretation. J. Mol. Biol. 106, 325-335.
6. Brandstetter, H., Kühne, A., Bode, W., Huber, R., von der Saal, W., Wirthensohn, K., and Engh, R. A. (1996). X-ray structure of active site-inhibited clotting factor Xa. Implications for drug design and substrate recognition. J. Biol. Chem. 271, 29988-29992.
7. Bringmann, P., Gruber, D., Liese, A., Toschi, L., Krätzschmar, J., Schleuning, W.-D., and Donner, P. (1995). Structural features mediating fibrin selectivity of vampire bat plasminogen activators. J. Biol. Chem. 270, 25596-25603.
8. Byeon, I.-J.L., and Llinas, M. (1991). Solution structure of the tissue-type plasminogen activator kringle 2 domain complexed to 6-aminohexanoic acid and antifibrinolytic drug. J. Mol. Biol. 222, 1035-1051.
9. Byeon, I.-J.L., Kelley, R.F., Mulkerrin, M.G., An, S.S.A., and Llinas, M. (1995). Ligand binding to the tissue-type plasminogen activator kringle 2 domain: structural characterization by 1H-NMR. Biochemistry 34, 2739-2750.
10. Carmeliet, P., and Collen, D. (1996). Genetic analysis of the plasminogen and coagulation system in mice. Haemostasis 26, 132-153.
11. Coll, M., Guasch, A., Aviles, F.X., and Huber, R. (1991). Three-dimensional structure of porcine procarboxypeptidase B: a structural basis of its inactivity. EMBO J. 10, 1-9.
12. Cygler, M., Sivaraman, J., Grochulski, P., Coulombe, R., Storer, A.C., and Mort, J.S. (1996). Structure of rat procathepsin B: model for inhibition of cysteine protease activity by the proregion. Structure 4, 405-416.
13. Davidson, S. (1997). New clot busters threaten Genentech's PA. Nature Biotech. 15, 405.
14. De Vos, A.M., Ultsch, M.H., Kelley, R.F., Padmanabhan, K., Tulinsky, A., Westbrook, M.L., and Kossiakoff, A.A. (1992). Crystal structure of the kringle 2 domain of tissue plasminogen activator at 2.4 Å resolution. Biochemistry 31, 270-279.
15. Downing, A.K., Driscoll, P.C., Harvey, T.S., Dudgeon, T.J., Smith, B.O., Baron, M., and Campbell, I.D. (1992). Solution structure of the fibrin binding finger domain of tissue-type plasminogen activator determined by 1H nuclear magnetic resonance. J. Mol. Biol. 225, 821-833.
16. Fehlhammer, H., Bode, W., and Huber, R. (1977). Crystal structure of bovine trypsinogen at 1.8 Å resolution. II. Crystallographic refinement, refined crystal structure and comparison with bovine trypsin. J. Mol. Biol. 111, 415-438.
17. Freer, S.T., Kraut, J., Robertus, J.D., Wright, H.T., and Xuong, N.H. (1970). Chymotrypsinogen, 2.5 Å crystal structure, comparison with α-chymotrypsin and implications for zymogen activation. Biochemistry 9, 1997-2009.
18. Gallagher, T., Gilliland, G., Wang, L., and Bryan, P. (1995). The prosegment-subtilisin BPN' complex: crystal structure of a specific 'foldase'. Structures, 3, 907-914.
19. Gardell, S.J., Duong, L.T., Diehel, R.E., York, J.D., Hare, T.R., Register, R.B., Jacobs, J.W., Dixon, R.A.F., and Friedman, P.A. (1989). Isolation, characterization, and cDNA cloning of a vampire bat salivary plasminogen activator. J. Biol. Chem. 264, 17947-17952.
20. Grailhe, P., Nieuwenhuizen, W., and Angles-Cano, E. (1994). Study of tissue-type plasminogen activator binding sites on fibrin using distinct fragments of fibrinogen. Eur. J. Biochem. 219, 961-967.
21. Higgins, D.L., Lamb, M.C., Young, S.L., Powers, D.B., and Anderson, S. (1990). The effect of the one-chain to two-chain conversion in tissue plasminogen activator: characterization of mutations at position 275. Thromb. Res. 57, 527-539.
22. Horrevoets, A.J.G., Smilde, A., DeVries, C., and Pannekoek, H. (1994). Mutants of tissue-type plasminogen activator during in vitro fibrinolysis. J. Biol. Chem. 269, 12639-12644.
23. Hoylaerts, M., Rijken, D.C., Lijnen, H.R., and Collen, D. (1982). Kinetics of the activation of plasminogen by human tissue plasminogen activator. Role of fibrin. J. Biol. Chem. 257, 2912-2919.
24. Hu, C.-K., Kohnert, U., Stürzebecher, J., Fischer, S., and Linas, M. (1996). Complexation of the tissue plasminogen activator protease with benzamidine-type inhibitors: interference by the kringle 2 module. Biochem. 35, 3270-3276.
25. Huber, R., and Bode, W. (1978). Structural basis of the activation and action of trypsin. Accounts Chem. Res. 11, 114-122.
26. James, M.N., and Sielecki, A.R. (1986). Molecular structure of an aspartic proteinase zymogen, porcine pepsinogen, at 1.8 Aα resolution. Nature 319, 33-38.
27. Keyt, B.A., Paoni, N.F., Refino, C.J., Berleau, L., Nguyen, H., Chow, A., Lai, J., Peña, L., Pater, C., Ogez, J., Etcheverry, T., Botstein, D., and Bennett, W.F. (1994). A faster-acting and more potent form of tissue plasminogen activator. Proc. Natl. Acad. Sci. USA 91, 3670-3674.
28. Kohnert, U., Hellerbrand, K., Martin, U., Stern, A., Popp, F., and Fischer, S. (1996). The recombinant Escherichia coli-derived protease domain of tissue-type plasminogen activator is a potent and fibrin specific fibrinolytic agent. Fibrinolysis 10, 93-102.
29. Kraulis, P.J. (1991). MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24, 946-950.
30. Krätzschmar, J., Haendler, B., Langer, G., Boidol, W., Bringmann, P., Alagon, A., Donner, P., and Schleuning, W.-D. (1991). The plasminogen activator family from the salivary gland of the vampire bat Desmodus rotundus: cloning and expression. Gene 105, 229-237.
31. Lamba, D., Bauer, M., Huber, R., Fischer, S., Rudolph, R., Kohnert, U., and Bode, W. (1996). The 2.3 Å crystal structure of the catalytic domain of recombinant two-chain human tissue-type plasminogen activator. J. Mol. Biol. 258, 117-135.
32. Lijnen, H.R., Bachmann, F., Collen, D., Ellis, V., Pannekoek, H., Rijken, D.C., and Thorsen, S. (1994). Mechanisms of plasminogen activation. J. Intern. Med. 236, 415-424.
33. Madison, E.L. (1994). Probing structure-function relationships of tissue-type plasminogen activator by site-specific mutagenesis. Fibrinolysis 8, 221-236.
34. Madison, E.L., Goldsmith, E.J., Gerard, R.D., Gething, M.-J.H., and Sambrook, J.F. (1989). Serpin-resistant mutants of human tissue-type plasminogen activator. Nature 339, 721-724.
35. Madison, E.L., Goldsmith, E.J., Gerard, R.D., Gething, M.-J.H., Sambrook, J.F., and Bassel-Duby, R.S. (1990). Amino acid residues that affect interaction of tissue-type plasminogen activator with plasminogen activator inhibitor 1. Proc. Natl. Acad. Sci. USA 87, 3530-3533.
36. Madison, E.L., Kobe, A., Gething, M.-J., Sambrook, J.F., and Goldsmith, E.J. (1993). Converting tissue plasminogen activator to a zymogen: A regulatory triad of Asp-His-Ser. Science 262, 419-421.
37. Margossian, S.S., Slayter, H.S., Kaczmarek, E., and McDonagh, J. (1993). Physical characterization of recombinant tissue plasminogen activator. Biochim. Biophys Acta 1163, 250-256.
38. Merritt, E.A., and Murphy, M.E.P. (1994). Raster3D Version 2.0: A Program for Photorealistic Molecular Graphics. Acta Cryst. D50, 869-873.
39. Neurath, H. (1989). Proteolytic processing and physiological regulation. Trends Biochem. Sci. 14, 268-271.
40. Nienaber, V.L., Young, S.L., Birktoft, J.J., Higgins, D.L., and Berliner, L.J. (1992). Conformational similarities between one-chain and two-chain tissue plasminogen activator (tPA): Implications to the activation mechanism on one-chain tPA. Biochemistry 31, 3852-3861.
41. Nieuwenhuizen, W. (1994). Sites in fibrin involved in the acceleration of plasminogen activation by t-PA. Possible role of fibrin polymerisation. Thromb. Res. 75, 343-347.
42. Novokhatny, V.V., Ingham, K.C., and Medved, L.V. (1991). Domain structure and domain-domain interactions of recombinant tissue plasminogen activator. J. Biol. Chem. 266, 12944-13002.
43. Ny, T., Elgh, F., and Lund, B. (1984). The structure of the human tissue-type plasminogen activator gene: correlation of intron and exon structures to functional and structural domains. Proc. Natl. Acad. Sci. USA 81, 5355-5359.
44. Paoni, N.F., Keyt, B.A., Refino, C.J., Chow, A.M., Nguyen, H.V., Bereleau, L.T., Badillo, J., Peña, L.C., Brady, K., Wurm, F.M., Ogez, J., and Bennett, W.F. (1993). A slow clearing, fibrin-specific. PAI-1 resistant variant of tPA (T103N, KHRR 296-299 AAAA). Thromb. Haemostas. 70, 307-312.
45. Pennica, D., Holmes, W.E., Kohr, W.J., Harkins, R.N., Vehar, G.A., Ward, C.A., Bennett, W.F., Yelverton, E., Seeburg, P.H., Heyneker, H.L., Goeddel, D.V., and Collen, D. (1983). Cloning and expression of human tissue-type plasminogen activator cDNA in E.coli. Nature 301, 214-221.
46. Petersen, L. C., Boel, E., Johannessen, M., and Foster, D. (1990). Quenching of the amidolytic activity of one-chain tissue-type plasminogen activator by mutation of lysine-416. Biochemistry 23, 3451-3457.
47. Retry, E. (1912). In: Real-Enzyklopädie der Gesamten Pharmazie, 2. Aufl. XIII, Moeller and Thoms, eds. (Berlin/Wien: Urban und Schwarzenberg), pp. 129-130.
48. Rånby, M., Bergsdorf, N., and Nilsson, T. (1982). Enzymatic properties of the one- and two-chain form of tissue plasminogen activator. Thromb. Res. 27, 175-183.
49. Renatus, M., Bode, W., Huber, R., Stürzebecher, J., Prasa, D., Fischer, S., Kohnert, U., and Stubbs, M.T. (1997a). Structural mapping of the active site specificity determinants of human tissue-type plasminogen activator. J. Biol. Chem. 272, 21713-21719.
50. Renatus, M., Engh, R.A., Stubbs, M.T., Huber, R., Fischer, S., Kohnert, U., and Bode, W. (1997b). Lysine 156 promotes the anomalous proenzyme activity of tPA: X-ray crystal structure of single-chain human tPA. EMBO J. 16, 4797-4805.
51. Renatus, M., Stubbs, M.T., Huber, R., Bringmann, P., Donner, P., Schleuning, W.-D., and Bode, W. (1997c). Catalytic domain structure of vampire bat plasminogen activator: A molecular paradigm for proteolysis without activation cleavage. Biochemistry 36, 13483-13493.
52. Smalling, R.W. (1996). Molecular biology of plasminogen activators: what are the clinical implications of drug design? Am. J. Cardiol. 78, 2-7.
53. Smith, B.O., Downing, A.K., Driscoll, P.C., Dudgeon, T.J., and Campbell, I.D. (1995). The solution structure and backbone dynamics of the fibronectin type I and epidermal growth factor-like pair of modules of tissue-type plasminogen activator. Structure 3, 823-833.
54. 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.
55. Spraggon, G., Everse, S.J., and Doolittle, R.F. (1997). Crystal structures of fragment D from human fibrinogen and its cross-linked counterpart from fibrin. Nature 389, 455-462.
56. Strandberg, L., and Madison, E.L. (1995). Variants of tissue-type plasminogen activator with substantially enhanced response and selectivity toward fibrin co-factors. J. Biol. Chem. 270, 23444-23449.
57. Tachias, K., and Madison, E.L. (1995). Variants of tissue-type plasminogen activator which display substantially enhanced stimulation by fibrin. J. Biol. Chem. 270, 18319-18322.
58. Tachias, K., and Madison, E.L. (1996). Converting tissue-type plasminogen activator into a zymogen. J. Biol. Chem. 277, 28749-28752.
59. Tachias, K., and Madison, E.L. (1997). Converting tissue-type plasminogen activator into a zymogen. Important role of Lys156. J. Biol. Chem. 272, 28-31.
60. Tate, K.M., Higgins, D.L., Holmes, W.E., Winkler, M.E., Heyneker, H.L., and Vehar, G.A. (1987). Functional role of proteolytic cleavage at Arginine-275 of human tissue plasminogen activator as assessed by site-directed mutagenesis. Biochemistry 26, 338-343.
61. Turk, D., Podobnik, M., Kuhelj, R., Dolinar, M., and Turk, V. (1996). Crystal structures of human procathepsin B at 3.2 and 3.3 A resolution reveal an interaction motif between a papain-like cysteine protease and its propeptide. FEBS Lett. 384, 211-214.
62. Wallén, P., Pohl, G., Bersdorf, N., Rånby, M., Ny, M., and Jörnvall, H. (1983). Purification and characterization of melanoma cell plasminogen activator. Eur. J. Biochem. 132, 681-686.
63. Wang, D., Bode, W., and Huber, R. (1985). Bovine chymotrypsinogen. A X-ray crystal structure analysis and refinement of a new crystal form at 1.8 Å resolution. J. Mol. Biol. 185, 595-624.