The 1.8 Å crystal structure of human cathepsin G in complex with Suc-Val-Pro-Phe(P)-(OPh)2: A Janus-faced proteinase with two opposite specificities

EMBO Journal

Volumn 15, Issue 20, 1996, Pages 5481-5491

  Hof, Peter ^a   Mayr, Irmgard ^a   Huber, Robert ^a   Korzus, Edward ^b,c   Potempa, Jan ^b,d   Travis, James ^b   Powers, James C ^e   Bode, Wolfram ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b UNIVERSITY OF GEORGIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d JAGIELLONIAN UNIVERSITY   (Poland)

^e GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Crystal structure; Inflammation; Inhibitor; Serine proteinase; Specificity

Indexed keywords

CARBOXYLIC ACID DERIVATIVE; CATHEPSIN G; GLUTAMINE; LYSINE; PHENYLALANINE; PROTEINASE; SERINE PROTEINASE; AUR PROTEIN, STAPHYLOCOCCUS AUREUS; CATHEPSIN; LEUKOCYTE ELASTASE; METALLOPROTEINASE; OLIGOPEPTIDE; SOMATOMEDIN B RECEPTOR; SUCCINYL VALYL PROLYL PHENYLALANYL DIPHENYLPHOSPHONATE; SUCCINYL-VALYL-PROLYL-PHENYLALANYL-DIPHENYLPHOSPHONATE;

ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; ELECTRICITY; ENZYME ACTIVE SITE; MAST CELL; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; STEREOCHEMISTRY; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; HUMAN; METABOLISM; MOLECULAR GENETICS; NEUTROPHIL; PROTEIN CONFORMATION; RAT; STEREOISOMERISM; X RAY CRYSTALLOGRAPHY;

JANUS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CATHEPSINS; CRYSTALLOGRAPHY, X-RAY; HUMANS; LEUKOCYTE ELASTASE; METALLOENDOPEPTIDASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEUTROPHILS; OLIGOPEPTIDES; PROTEIN CONFORMATION; RATS; RECEPTOR, IGF TYPE 2; SERINE ENDOPEPTIDASES; STEREOISOMERISM;

EID: 0029853820     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00933.x     Document Type: Article

References (71)

1. Allen, D.H. and Tracy, P.B. (1995) Human coagulation factor V is activated to the functional cofactor by elastase and cathepsin G expressed at the monocyte surface. J. Biol. Chem., 270, 1408-1415.
2. Avril, L.E., di Martino-Ferrer, M., Pignede, G., Seman, M. and Gauthier, F. (1994) Identification of the U-937 membrane-associated proteinase interacting with the V3 loop of HIV-1 gp120 as cathepsin G. FEBS Lett., 345, 81-86.
3. Avril, L.E., di Martino-Ferrer, M., Brillard-Bourdet, M. and Gauthier, F. (1995) Inhibition of U-937 membrane-associated cathepsin G by GP120 (IIIB) and V3 loop-derived peptides from several strains of HIV-1. FEBS Lett., 367, 251-256.
4. Baggiolini, M., Schnyder, J., Bretz, U., Dewald, B. and Ruch, W. (1979) Cellular mechanisms of proteinase release from inflammatory cells and the degradation of extracellular proteins. Ciba Foundation Symposium, 75, 105-121.
5. Bangalore, N. and Travis, J. (1994) Comparison of properties of membrane bound versus soluble forms of human leukocytic elastase and cathepsin G. Biol. Chem. Hoppe-Seyler, 375, 659-666.
6. Bangalore, N., Travis, J., Onunka, V.C., Pohl, J. and Shafer, W.M. (1990) Identification of the primary antimicrobial domains in human neutrophil cathepsin G. J. Biol. Chem., 265, 13584-13588.
7. Barton, G.J. (1993) ALSCRIPT: a tool to format multiple sequence alignments. Prot. Engng, 6, 37-40.
8. Baugh, R.J. and Travis, J. (1976) Human leukocyte granule elastase: rapid isolation and characterization. Biochemistry, 15, 836-841.
9. Beatty, K., Bieth, J. and Travis, J. (1980) Kinetics of association of serine proteinases with native and oxidized alpha-1-proteinase inhibitor and alpha-1-antichymotrypsin. J. Biol. Chem., 255, 3931-3934.
10. Bertrand, J.A., Oleksyszyn, J. Kam, C.-M., Boduszek, B., Presnell, S., Plaskon, R.R., Suddath, F.L., Powers, J.C. and Williams, L.D. (1996) Inhibition of trypsin and thrombin by amino (4-amidinophenyl) methanephosphonate diphenyl ester derivatives: X-ray structures and molecular models. Biochemistry, 35, 3147-3155.
11. Blevins, R.A. and Tulinsky, A. (1985) The refinement and the structure of the dimer of α-chymotrypsin at 1.67 Å resolution. J. Biol. Chem., 260, 4264-4275.
12. Bode, W. (1996) The three-dimensional structure of human neutrophil elastase. In Crystal, R.G. (ed.), Lung Biology in Health and Disease. Marcel Dekker, Inc., New York, Vol. 88, pp. 97-117.
13. Bode, W. and Huber, R. (1986) Crystal structures of pancreatic serine endopeptidases. In Desnuelle, P. (ed.), Molecular and Cellular Basis of Digestion. Elsevier, Amsterdam, pp. 213-234.
14. Bode, W. and Schwager, P. (1975) The refined crystal structure of bovine β-trypsin at 1.8 Å resolution. II. Crystallographic refinement, calcium binding site, benzamidine binding site and active site at pH 7.0. J. Mol. Biol., 98, 693-717.
15. Bode, W., Wei, A.Z., Huber, R., Meyer, E., Travis, J. and Neumann, S. (1986) X-ray crystal structure of the complex of human leukocyte elastase (PMN elastase) and the third domain of the turkey ovomucoid inhibitor. EMBO J., 5, 2453-2458.
16. Brandstetter, H., Bauer, M., Huber, R., Lollar, P. and Bode, W. (1995) X-ray structure of clotting factor IXa: active site and module structure related to Xase activity and hemophilia B. Proc. Natl Acad. Sci. USA. 92, 9796-9800.
17. Brinkmann, T., Schnierer, S. and Tschesche, H. (1991) Recombinant aprotinin homologue with new inhibitory specificity for cathepsin G. Eur. J. Biochem., 202, 95-99.
18. Brünger, A. (1992) X-PLOR Version 3.1, A System for X-ray Crystallography and NMR. Yale University Press, New Haven, CT.
19. Campbell, E.J., Silverman, E.K. and Campbell, M.A. (1989) Elastase and cathepsin G of human monocytes. Quantification of cellular content, release in response to stimuli, and heterogeneity in elastase-mediated proteolytic activity. J. Immunol., 143, 2961-2968.
20. Caputo, A., James, M.N.G., Powers, J.C., Hudig, D. and Bleakley, R.C. (1994) Conversion of the substrate specificity of mouse proteinase granzyme B. Nature Struct. Biol., 1, 364-367.
21. Caughey, G.H. (1994) Serine proteinases of mast cell and leukocyte granules. A league of their own. Am. J. Respir. Crit. Care Med., 150, S138-S142.
22. Chandrasekharan, U.M., Sanker, S., Glynias, M.J., Karnik, S.S. and Husain, A. (1996) Angiotensin II-forming activity in a reconstructed ancestral chymase. Science, 271, 502-505.
23. Collaborative Computational Project (1994) The CCP4 Suite: programs for protein crystallography. Acta Crystallogr., D50, 760-763.
24. Engh, R.A. and Huber, R. (1991) Accurate bond and angle parameters for X-ray protein structure and refinement. Acta Crystallogr., A47, 392-400.
25. Ermolieff, J., Boudier, C., Laine, A., Meyer, B. and Bieth, J.G. (1994) Heparin protects cathepsin G against inhibition by protein proteinase inhibitors. J. Biol. Chem., 269, 29502-29508.
26. Faber, J.P., Poller, W., Olek, K., Baumann, U., Carlson, J., Lindmark, B. and Eriksson, S. (1993) The molecular basis of alpha 1-antichymotrypsin deficiency in a heterozygote with liver and lung disease. J. Hepatol., 18, 313-321.
27. Fioretti, E., Angeletti, M., Coletta, M., Ascenzi, P., Bolognesi, M., Menegatti, E., Rizzi, M. and Ascoli, F. (1993) Binding of bovine basic pancreatic trypsin inhibitor (Kunitz) as well as bovine and porcine pancreatic secretory trypsin inhibitor (Kazal) to human cathepsin G: a kinetic and thermodynamic study. J. Enzyme Inhibition, 7, 57-64.
28. Frommherz, K.J., Faller, B. and Bieth, J.G. (1991) Heparin strongly decreases the rate of inhibition of neutrophil elastase by alpha 1-proteinase inhibitor. J Biol. Chem., 266, 15356-15362.
29. Gabay, J.E. (1994) Antimicrobial proteins with homology to serine proteases. Ciba Foundation Symposium, 186, 237-247, 247-249.
30. Garwicz, D., Lindmark, A. and Gullberg, U. (1995) Human cathepsin G lacking functional glycosylation site is proteolytically processed and targeted for storage in granules after transfection to the ral basophilic/ mast cell line RBL or the murine myeloid cell line 32D. J. Biol. Chem., 270, 28413-28418.
31. Griffiths, G.M. and Isaaz, S. (1993) Granzymes A and B are targeted to the lytic granules of lymphocytes by the mannose-6-phosphate receptor. J. Cell Biol., 120, 885-896.
32. Gullberg, U., Lindmark, A., Nilsson, E., Persson, A.M. and Olsson, I. (1994) Processing of human cathepsin G after transfection to the rat basophilic/ mast cell tumor line RBL. J. Biol. Chem., 269, 25219-25225.
33. Haddad, P., Jenne, D., Tschopp, J., Clement, M.V., Mathieu-Mahul, D. and Sasportes, M. (1991) Structure and evolutionary origin of the human granzyme H gene. Int. Immunol., 3, 57-66.
34. Hartley, B.S. and Shotton, D.M. (1971) Pancreatic elastase. In Boyer, P.D. (ed.), The Enzymes. Academic Press, New York, Vol. III, pp. 323-373.
35. Hase-Yamazaki, T. and Aoki, Y. (1995) Stimulation of human lymphocytes by cathepsin G. Cell. Immunol., 160, 24-32.
36. Jenne, D.E., Masson, D., Zimmer, M., Haefliger, J.-A., Li, W.-H. and Tschopp, J. (1989) Isolation and complete structure of the lymphocyte serine protease granzyme G, a novel member of the granzyme multigene family in murine cytolytic T lymphocytes. Evolutionary origin of lymphocyte proteases. Biochemistry, 28, 7953-7961.
37. Kraulis, P.J. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr., 24, 946-950.
38. Leslie, A.G.W. (1991) Recent Changes to the MOSFLM Package for Processing Film and Image Plate Data. SERC Laboratory, Daresbury, Warrington WA4 4AD, UK.
39. Maison, C.M., Villiers, C.L. and Colomb, M.G. (1991) Proteolysis of C3 on U937 cell plasma membranes. Purification of cathepsin G. J. Immunol., 147, 921-926.
40. McGuire, M.J., Lipsky, P.E. and Thiele, D.L. (1993) Generation of active myeloid and lymphoid granule serine proteases requires processing by the granule thiol protease dipeptidyl peptidase I. J. Biol. Chem., 268, 2458-2467.
41. Merritt, E.A. and Murphy, M.E.P. (1994) Raster3D version 2.0. A program for photorealistic molecular graphics. Acta Crystallogr., D50, 869-873.
42. Mikes, O., Holeysovsky, V., Tomasek, V. and Sorm, F. (1966) Covalent structure of bovine trypsinogen. The position of the remaining amides. Biochem. Biophys. Res. Commun., 24, 346-352.
43. Molino, M, Blanchard, N., Belmonte, E., Tarver, A.P., Abrams, C., Hoxie, J.A., Cerletti, C. and Brass, L.F. (1995) Proteolysis of the human platelet and endothelial cell thrombin receptor by neutrophil-derived cathepsin G. J. Biol. Chem., 270, 11168-11175.
44. Murphy, M.E.P., Moult, J., Bleackley, R.C., Gershenfeld, H., Weissman, I.L. and James, M.N.G. (1988) Comparative molecular model building of two serine proteinases from cytotoxic T lymphocytes. Proteins, 4, 190-204.
45. Navaza, J. (1994) Amore - an automated package for molecular replacement. Acta Crystallogr., A50, 157-163.
46. Navia, M.A., McKeever, B.M., Springer, J.P., Lin, T.-Y., Wiliams, H.R., Fluder, E.M., Dorn, C.P. and Hoogsten, K. (1989) Structure of human neutrophil elastase in complex with a peptide chloromethyl ketone inhibitor at 1.84-Å resolution. Proc. Natl Acad. Sci. USA, 86, 7-11.
47. Nicholls, A., Bharadwaj, R. and Honig, B. (1993) Grasp - graphical representation and analysis of surface properties. Biophys. J., 64, A166.
48. Oleksyszyn, J. and Powers, J.C. (1994) Amino acid and peptide phosphonate derivatives as specific inhibitors of serine peptidases. Methods Enzymol., 244, 442-457.
49. Owen, C.A. and Campbell, E.J. (1995) Neutrophil proteinases and matrix degradation. The cell biology of pericellular proteolysis. Cell Biol., 6, 367-376.
50. Padmanabhan, K., Padmanabhan, K.R. Tulinsky, A., Park, C.H., Bode, W., Huber, R., Blankenship, D.T., Cardin, A.D. and Kisiel, W. (1993) Structure of human des(1-45) factor Xa at 2.2 Å resolution. J. Mol. Biol., 232, 947-966.
51. Padrines, M., Wolf, M, Walz, A. and Baggiolini, M. (1994) Interleukin-8 processing by neutrophil elastase, cathepsin G and proteinase-3. FEBS Lett., 352, 231-235.
52. Powers, J.C. and Harper, J.W. (1986) Inhibitors of metalloproteases. In Barrett, A.J. and Salvesen, G. (eds), Research Monographs in Cell and Tissue Physiology. Elsevier, Amsterdam, Vol. 12, pp. 219-298.
53. Powers, J.C. et al. (1985) Mammalian chymotrypsin-like enzymes. Comparative reactivities of rat mast cell proteases, human and dog skin chymases, and human cathepsin G with peptide 4-nitroanilide substrates and with peptide chloromethyl ketone and sulfonyl fluoride inhibitors. Biochemistry, 24, 2048-2058.
54. Powers, J.C., Kam, C.-M., Narasimhan, L., Oleksyszyn, J., Hernandez, M.A. and Ueda, T. (1989) Mechanism-based isocoumarin inhibitors for serine proteases: use of active site structure and substrate specificity in inhibitor design. J. Cell. Biochem., 39, 33-46.
55. Reilly, C.F., Tewsksbury, D.A., Schechter, N.M. and Travis, J. (1982). Rapid conversion of angiotensin I to angiotensin II by neutrophil and mast cell proteinases. J. Biol. Chem., 257, 8619-8622.
56. Remington, S.J., Woodbury, R.G., Reynolds, R.A., Matthews, B.W. and Neurath, H. (1988) The structure of rat mast cell protease II at 1.9 Å resolution. Biochemistry, 27, 8097-8105.
57. Salvesen, G. and Enghild, J.J. (1990) An unusual specificity in the activation of neutrophil serine proteinase zymogens. Biochemistry, 29, 5304-5308.
58. Salvesen, G., Farley, D., Shuman, J., Przybyla, A., Reilly, C. and Travis, J. (1987) Molecular cloning of human cathepsin G: structural similarity to mast cell and cytotoxic T lymphocyte proteinases. Biochemistry, 26, 2289-2293.
59. Savage, M.J., Iqbal, M., Loh, T., Trusko, S.P, Scott, R. and Siman, R. (1994) Cathepsin G: localization in human cerebral cortex and generation of amyloidogenic fragments from the beta-amyloid precursor protein. Neuroscience, 60, 607-619.
60. Schechter, N.M, Wang, Z.M., Blacher, R.W., Lessin, S.R., Lazarus, G.S. and Rubin, H. (1994) Determination of the primary structures of human skin chymase and cathepsin G from cutaneous mast cells of urticaria pigmentosa lesions. J. Immunol., 152, 4062-4069.
61. Schiessler, H., Arnhold, M., Ohlsson, K. and Fritz, H. (1976) Inhibitors of acrosin and granulocyte proteinases from human genital tract secretions. Hoppe-Seylers Z. Physiol. Chem., 357, 1251-1260.
62. Selak, M.A. (1994) Cathepsin G and thrombin: evidence for two different platelet receptors. Biochem. J., 297, 269-275.
63. Shafer, W.M., Pohl, J., Onunka, V.C., Bangalore, N. and Travis, J. (1991) Human lysosomal cathepsin G and granzyme B share a functionally conserved broad spectrum antibacterial peptide. J. Biol. Chem., 266, 112-116.
64. Sinha, S., Watorek, W., Karr, S., Giles, J., Bode, W. and Travis, J. (1987) Primary structure of human neutrophil elastase. Proc. Natl Acad. Sci. USA, 84, 2228-2232.
65. Snyder, R.A., Kaempfer, C.E. and Wintroub, B.U. (1985) Chemistry of a human monocyte-derived cell line (U937): identification of the angiotensin I-converting activity as leukocyte cathepsin G. Blood, 65, 176-182.
66. Tanaka, T., Minematsu, Y., Reilly, C.F., Travis, J. and Powers, J.C. (1985) Human leukocyte cathepsin G. Subsite mapping with 4-nitroanilides, chemical modification, and effect of possible cofactors. Biochemistry, 24, 2040-2047.
67. Travis, J. (1988) Structure, function, and control of neutrophil proteinases. Am. J. Med., 84, 37-42.
68. Travis, J., Garner, D. and Bowen, J. (1978) Human alpha-1-antichymotrypsin: purification and properties. Biochemistry, 17, 5647-5651.
69. Turk, D. (1992) Weitereentwicklung eines Programmes für Molekülgrafik und Elektronendichte-Manipulation und seine Anwendung auf verschiendene Protein-Strukturaufklärungen. Technische Universität München, München.
70. Wei, A.Z., Mayr, I. and Bode, W. (1988) The refined 2.3 Å crystal structure of human leukocyte elastase in a complex with a valine chloromethyl ketone inhibitor. FEBS Lett., 234, 367-373.
71. Woodbury, R.G., Katunuma, N., Kobayashi, K., Titani, K. and Neurath, H. (1978) Covalent structure of a group-specific protease from rat small intestine. Biochemistry, 17, 811-819.