Conservation and variability in the structures of serine proteinases of the chymotrypsin family

Journal of Molecular Biology

Volumn 258, Issue 3, 1996, Pages 501-537

  Lesk, Arthur M ^a   Fordham, William D ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b FAIRLEIGH DICKINSON UNIVERSITY   (United States)

Author keywords

Molecular evolution; Serine proteinase; Structural analysis; barrel

Indexed keywords

CHYMOTRYPSIN; SERINE PROTEINASE;

ARTICLE; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME STRUCTURE; PRIORITY JOURNAL; PROTEIN DOMAIN; X RAY CRYSTALLOGRAPHY;

EID: 0029962944     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0264     Document Type: Article

References (91)

1. Alexandrov, N. N., Takahashi, K. & Gō, N. (1992). Common spatial arrangement of backbone fragments in homologous and non-homologous proteins. J. Mol. Biol. 225, 5-9.
2. Allaire, M., Chernaia, M. M., Malcolm, B. A. & James, M. N. G. (1994). Picornaviral 3C cysteine proteinases have a fold similar to the chymotrypsin-like serine proteinases. Nature, 369, 72-76.
3. Baba, T., Watanabe, K., Kashiwabara, S. & Arai, Y. (1989). Primary structure of human proacrosin deduced from its cDNA sequence. FEBS Letters, 27, 296-300.
4. Barrett, A. J. (1977). Editor of Proteinases in Mammalian Cells and Tissues. North-Holland, Amsterdam.
5. Barrett, A. J. (1994). Editor of Proteolytic Enzymes: Serine and Cysteine Peptidases. Methods in Enzymology, vol. 244, Academic Press, New York.
6. Bazan, J. F. & Fletterick, R. J. (1988). Viral cysteine proteinases are homologous to the trypsin-like family of serine proteinases: structural and functional implications. Proc. Natl Acad. Sci. USA, 85, 7872-7876.
7. Bernstein, F. C., Koetzle, T. F., Williams, G. J. B., Meyer, E. F., Jr, Brice, M. D., Rodgers, J. R., Kennard, O., Shimanouchi, T. & Tasumi, M. (1977). The Protein Data Bank: a computer based archival file for macromolecular structures. J. Mol. Biol. 112, 535-542.
8. Blevins, R. A. & 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.
9. Blow, D. M. (1976). Structure and mechanism of chymotrypsin. Accts Chem. Res. 9, 145-152.
10. Bode, W., Chen, Z., Bartels, K., Kutzbach, C., Schmidt-Kastner, G. & Bartunik, H. (1983). Refined 2-Å X-ray crystal structure of porcine pancreatic kallikrein A, a specific trypsin-like serine proteinase. Crystallization, structure determination, crystallographic refinement, structure and its comparison with bovine trypsin. J. Mol. Biol. 164, 237-282.
11. Bode, W., Mayr, I., Baumann, U., Huber, R., Stone, S. R. & Hofsteenge, J. (1989). The refined 1.9-Å crystal structure of human α-thrombin: Interaction with D-Phe-Pro-Arg chloromethylketone and significance of the Tyr-Pro-Pro-Trp insertion segment. EMBO J. 8, 3467-3475.
12. Bode, W., Turk, D. & Karshikov, A. (1992). The refined 1.9-Å X-ray crystal structure of D-Phe-Pro-Arg chloromethylketone-inhibited human α-thrombin: structure analysis, overall structure, electrostatic properties, detailed active-site geometry and structure-function relationships. Protein Sci. 1, 426-471.
13. Bond, J. S. (1991). Plasma-membrane proteases - introductory remarks. Biomed. Biochim. Acta, 50, 775-780.
14. Chambers, J. L. & Stroud, R. M. (1979). The accuracy of refined protein structures, comparison of two independently refined models of bovine trypsin. Acta Crystallog. sect. B, 35, 1861-1874.
15. Chasan, R. & Anderson, K. V. (1989). The role of Easter, an apparent serine protease, in organizing the dorsal-ventral pattern of the Drosophila embryo. Cell, 56, 391-400.
16. Chasan, R., Jin, Y. & Anderson, K. V. (1992). Activation of the Easter zymogen is regulated by five other genes to define dorsal-ventral polarity in the Drosophila embryo. Development, 115, 607-616.
17. Chothia, C. & Janin, J. (1982). Orthogonal packing of β-pleated sheets in proteins. Biochemistry, 21, 3955-3965.
18. Chothia, C. & Lesk, A. M. (1982). The evolution of proteins formed by β-sheets. I. Plastocyanin and azurin. J. Mol. Biol. 160, 309-323.
19. Chothia, C. & Lesk, A. M. (1985). Helix movements and the reconstruction of the haem pocket during the evolution of the cytochrome c family. J. Mol. Biol. 182, 151-158.
20. Chothia, C. & Lesk, A. M. (1986). Relationship between the divergence of sequence and structure in proteins. EMBO J. 5, 823-826.
21. Cook, W. J., Jeffrey, L. C., Carson, M., Chen, Z. & Pickart, C. M. (1992). Structure of a diubiquitin conjugate and a model for interaction with ubiquitin conjugating enzyme (E2). J. Biol. Chem. 267, 16467-16471.
22. Davie, E. W., Fujikawa, K. & Kisiel, W. (1991). The coagulation cascade: initiation, maintenance and regulation. Biochemistry, 20, 10363-10370.
23. Diamond, R. (1992). On the multiple simultaneous superposition of molecular structures by rigid body transformations. Protein Sci. 1, 1279-1287.
24. Dodson, G. G., Lawson, D. M. & Winkler, F. K. (1992). Structural and evolutionary relationships in lipase mechanism and activation. Faraday Discuss. 93, 95-105.
25. Donate, L. E., Gherardi, E., Srinivasan, N., Sowdhamini, R., Aparicio, S. & Blundell, T. L. (1994). Molecular evolution and domain structure of plasminogen-related growth factors (HGF/S and HGF1/MSP). Protein Sci. 3, 2378-2394.
26. Erhan, S. & Greller, L. D. (1974). Do immunoglobulins have proteolytic activity? Nature, 251, 353-355.
27. Fersht, A. (1984). Enzyme Structure and Mechanism, 2nd edit., W. H. Freeman, San Francisco, CA.
28. Froelich, C. J., Zhang X., Turbov, J., Hudig, D., Winkler, U. & Hanna, W. L. (1993). Human granzyme B degrades aggrecan proteoglycan in matrix synthesized by chondrocytes. J. Immunol. 151, 7161-7171.
29. Fujinaga, M. & James, M. N. G. (1987). Rat submaxillary gland serine protease, tonin. Structure solution and refinement at 1.8 Ångstroms resolution. J. Mol. Biol. 195, 373-396.
30. Fujinaga, M., Delbaere, L. T. J., Brayer, G. D. & James, M. N. G. (1985). Refined structure of α-lytic proteinase at 1.7 Å resolution. Analysis of hydrogen bonding and solvent structure. J. Mol. Biol. 184, 479-502.
31. Gay, N. J. & Keith, F. J. (1992). Regulation of translation and proteolysis during the development of embryonic dorso-ventral polarity in Drosophila. Homology of Easter proteinase with Limulus proclotting enzyme and translational activation of Toll receptor synthesis. Biochim. Biophys. Acta, 1132, 290-296.
32. Gerstein, M., Anderson, B. F., Norris, G. E., Baker, E. N., Lesk, A. M. & Chothia, C. (1993). Domain closure in Lactoferrin: two hinges produce a see-saw motion between alternative close-packed interfaces. J. Mol. Biol. 234, 357-372.
33. Goldberger, G., Bruns, G. A. P., Rits, M., Edge, M. D. & Kwiatkowski, D. J. (1987). Human complement factor I: analysis of cDNA-derived primary structure and assignment of its gene to chromosome 4. J. Biol. Chem. 262, 10065-10071.
34. Gorbalenya, A. E., Donchenko, A. P., Blinov, V. M. & Koonin, E. V. (1986). Cysteine proteinases of positive strand RNA viruses and chymotrypsin-like serine proteinases. A distinct protein superfamily with a common structural fold. FEBS Letters, 243, 103-114.
35. Greer, J. (1990). Comparative modeling methods: application to the family of the mammalian serine proteinases. Proteins: Struct. Funct. Genet. 7, 317-334.
36. Grütter, M. G., Priestle, J. P., Rahuel, J., Grossenbacher, H., Bode, W., Hofsteenge, J. & Stone, S. R. (1990). Crystal structure of the thrombin-hirudin complex: a novel mode of serine proteinase inhibition. EMBO J. 9, 2361-2365.
37. Harel, M., Su, C.-T., Frolow, F., Silman, I. & Sussman, J. L. (1991). γ-Chymotrypsin is a complex of α-Chymotrypsin with its own autolysis products. Biochemistry, 30, 5217-5225.
38. Hartley, B. S. (1970). Homologies in serine proteinases. Phil. Trans. Roy. Soc. ser. B, 257, 77-87.
39. Henderson, B. R., Tansey, W. P., Phillips, S. M., Ramshaw, I. A. & Kefford, R. F. (1992). Transcriptional and posttranscriptional activation of urokinase plasminogen activator gene expression in metastatic tumor cells. Cancer Res. 52, 2489-2496.
40. Hörl, W. H. (1989). Proteinases: potential role in health and disease. In Design of Enzyme Inhibitors as Drugs (Sandler, M. & Smith, H. J., eds), pp. 573-581, Oxford University Press, Oxford.
41. Hubbard, S. J., Campbell, S. F. & Thornton, J. M. (1991). Molecular recognition. Conformational analysis of limited proteolysis sites and serine proteinase protein inhibitors. J. Mol. Biol. 220, 507-530.
42. Huber, R. & Bode, W. (1978). Structural basis of the activation and action of trypsin. Accts Chem. Res. 11, 114-122.
43. James, M. N. G., Delbaere, L. T. J. & Brayer, G. D. (1978). Amino acid sequence alignment of bacterial and mammalian pancreatic serine proteinases based on topological equivalences. Can. J. Biochem. 56, 396-402.
44. Keil, B. (1992). Specificity of Proteolysis. Springer Verlag, Berlin, New York and Heidelberg.
45. Kraut, J. (1971). Subtilisin: X-ray structure. In The Enzymes (Boyer, P. D., ed.), vol. 3, pp. 547-560, Academic Press, New York and London.
46. Lee, B. & Richards, F. M. (1971). The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55, 379-400.
47. Lesk, A. M. (1981). Introduction to Physical Chemistry, sections 18-10, Prentice-Hall, Inc., Englewood Cliffs, NJ.
48. Lesk, A. M. (1986a). Integrated access to sequence and structural data. In Biosequences: Perspectives and User Services in Europe (Saccone, C., ed.), pp. 23-28, EEC, Bruxelles.
49. Lesk, A. M. (1986b). Molecular speleology: the exploration of crevices in proteins for prediction of binding sites, design of drugs and analysis of surface recognition. Acta Crystallog. sect A, 42, 83-85.
50. Lesk, A. M. & Chothia, C. (1980). How different amino acid sequences determine similar protein structures: the structure and evolutionary dynamics of the globins. J. Mol. Biol. 136, 225-270.
51. Lesk, A. M. & Chothia, C. (1982). The evolution of proteins formed by β-sheets. II. The core of the immunoglobulin domains. J. Mol. Biol. 160, 325-342.
52. Lesk, A. M. & Chothia, C. (1986). The response of protein structures to amino acid sequence changes. Phil. Trans. Roy. Soc. London, 317, 345-356.
53. Lesk, A. M., Brändén, C.-I. & Chothia, C. (1989). Structural principles of α-β barrel proteins: the packing of the interior of the sheet. Proteins: Struct. Funct. Genet. 5, 139-148.
54. Liao, D., Breddam, K., Sweet, R. M., Bullock, T. & Remington, S. J. (1992). Refined atomic model of wheat serine carboxypeptidase II at 2.2-Å resolution. A new class of serine proteinase. Biochemistry, 31, 9796-9812.
55. Liebman, M. (1986). Structural organization in the serine proteinases. I. Macromolecular specificity in limited proteolysis. Enzyme, 36, 115-140.
56. Mann, K. G., Nesheim, M. E., Church, W. R., Haley, P. & Krishnaswamy, S. (1990). Surface dependent reactions of the vitamin K-dependent enzyme complexes. Blood, 76, 1-16.
57. Matthews, B. W., Sigler, P. B., Henderson, R. & Blow, D. M. (1967). Three-dimensional structure of tosyl-α-chymotrypsin. Nature, 214, 652-656.
58. Matthews, D. A., Smith, W. W., Ferre, R. A., Condon, B., Budahazi, G., Sisson, W., Villafranca, J. E., Janson, C. A., McElroy, H. E., Gribskov, C. L. & Worland, S. (1994). Structure of human rhinovirus 3C proteinase reveals a trypsin-like polypeptide fold, RNA-binding site, and means for cleaving precurson polyprotein. Cell, 77, 1-20.
59. McLachlan, A. D. (1979). Gene duplications in the structural evolution of chymotrypsin. J. Mol. Biol. 128, 49-79.
60. Meyer, E., Cole, G., Radhakrishnan, R. & Epp, O. (1988). Structure of native porcine pancreatic elastase at 1.65 Å resolution. Acta Crystallog. sect. B, 44, 26-38.
61. Moult, J., Sussman, F. & James, M. N. G. (1985). Electron density calculations as an extension of protein structure refinement. Streptomyces griseus proteinase A at 1.5 Å resolution. J. Mol. Biol. 182, 555-566.
62. Murzin, A. G., Lesk, A. M. & Chothia, C. (1992). β-Trefoil fold. Patterns of structure and sequence in the Kunitz inhibitors, interleukins-1β and 1α and fibroblast growth factors J. Mol. Biol. 223, 531-543.
63. Murzin, A. G., Lesk, A. M. & Chothia, C. (1994a). Principles determining the structure of β-sheet barrels in proteins: I. A theoretical analysis. J. Mol. Biol. 236, 1369-1381.
64. Murzin, A. G., Lesk, A. M. & Chothia, C. (1994b). Principles determining the structure of β-sheet barrels in proteins: II. The observed structures. J. Mol. Biol. 236, 1382-1400.
65. Neurath, H. (1984). Evolution of proteolytic enzymes. Science, 224, 350-357.
66. Neurath, H. (1985). Proteolytic enzymes, past and present. Fed. Proc. Fed. Am. Soc. Expt. Biol. 44, 2907-2913.
67. Pastore, A. & Lesk, A. M. (1990). Comparison of the structures of globins and phycocyanins: evidence for evolutionary relationship. Proteins: Struct. Funct. Genet. 8, 133-155.
68. Paul, S., Volle, D. J., Beach, C. M., Johnson, D. R., Powell, M. J. & Massey, R. J. (1989). Catalytic hydrolysis of vasoactive intestinal peptide by human autoantibody Science, 244, 1158-1162.
69. Paul, S., Sun, M., Mody, R., Tewary, H. K., Stemmer, P., Massey, R. J., Gianferrara, T., Mehrotra, S., Dreyer, T., Meldal, M. & Tramontano, A. (1992). Peptidolytic monoclonal antibody elicited by a neuropeptide. J. Biol. Chem. 267, 13142-13145.
70. Perona, J. J. & Craik, C. S. (1995). Structural basis of substrate specificity in the serine proteinases. Protein Sci. 4, 337-360.
71. Perona, J. J., Hedstrom, L., Rutter, W. J. & Fletterick, R. J. (1995). Structural origins of substrate discrimination in trypsin and chymotrypsin. Biochemistry, 34, 1489-1499.
72. Polgàr, L. (1989). Mechanisms of Proteinase Action. CRC Press, Boca Raton, FA.
73. Powers, J. C., Tanaka, T., Harper, J. W., Minematsu, Y., Barker, L., Lincoln, D., Crumley, K. V., Fraki, J. E., Schechter, N. M., Lazarus, G. G., Nakajima, K., Nakashino, K., Neurath, H. & Woodbury, R. G. (1985). Mammalian chymotrypsin-like enzymes. Comparative reactivities of rat mast cell proteinases, 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.
74. Qiu, X., Padmanabhan, K. P., Carperos, V. E., Tulinsky, A., Kline, T., Maraganore, J. M. & Fenton, J. W., II (1992). Structure of the hirulog 3-thrombin complex and nature of the S′ subsites of substrates and inhibitors. Biochemistry, 31, 11689-11697.
75. Read, R. J. & James, M. N. G. (1988). Refined crystal structure of Streptomyces griseus trypsin at 1.7 Å resolution. J. Mol. Biol. 200, 523-551.
76. Read, R. J., Fujinaga, M., Sielecki, A. R. & James, M. N. G. (1983). Structure of the complex of Streptomyces griseus proteinase B and the third domain of the turkey ovomucoid inhibitor at 1.8 Å resolution. Biochemistry, 22, 4420-4433.
77. Reid, K. B. M., Bentley, D. R., Campbell, R. D., Chung, L. D., Sim, R. B., Kristensen, T. & Tack, B. F. (1986). Complement system proteins which interact with C3B or C4B. Immunol. Today, 7, 230-234.
78. Remington, S. J., Woodbury, R. G., Reynolds, R. A., Matthews, B. W. & Neurath, H. (1988). The structure of rat mast cell proteinase II at 1.9 Å resolution. Biochemistry, 27, 8097-8105.
79. Rosing, J. & Tans, C. (1988). Meizothrombin, a major product of Factor Xa-catalyzed prothrombin activation. Thromb. Haemostasis, 60, 355-360.
80. Rydel, T. J., Ravichandran, K. G., Tulinsky, A., Bode, W., Huber, R., Roitsch, C. & Fenton, J. W., II (1990). The structure of a complex of recombinant hirudin and human α-thrombin. Science, 249, 277-280.
81. Schechter, I. & Berger, A. (1967). On the size of the active site in proteinases. I. Papain. Biochem. Biophys. Res. Commun. 27, 157-162.
82. Smith, C. L. & DeLotto, R. (1992). A common domain within the proenzyme regions of the Drosophila snake and Easter proteins and Tachypleus proclotting enzyme defines a new subfamily of serine proteases. Protein Sci. 1, 1225-1226.
83. Stroud, R. (1974). A family of protein-cutting proteins. Sci. Am. 231(1), 74-88.
84. Stubbs, M., Oschkinat, H., Mayr, I., Huber, R., Angliker, H., Stone, S. R. & Bode, W. (1992). The interaction of thrombin with fibrinogen. A structural basis for its specificity Eur. J. Biochem. 206, 187-195.
85. Tong, L., Wengler, G. & Rossman, M. G. (1993). Refined structure of Sindbis virus core protein and comparison with other chymotrypsin-like serine proteinase structures. J. Mol. Biol. 230, 228-247.
86. Tsunasawa, S., Masaki, T., Hirose, M., Soejima, M. & Sakiyama, F. (1989). The primary structure and structural characteristics of Achromobacter lyticus proteinase I, a lysine-specific serine proteinase. J. Biol. Chem. 264, 3832-3839.
87. Twining, S. S. (1994). Regulation of proteolytic activity in tissues. Crit. Revs. Biochem. Mol. Biol. 29, 315-383.
88. Vriend, G. & Sander, C. (1991). Detection of common three-dimensional substructures in proteins. Proteins: Struct. Funct. Genet. 11, 52-58.
89. Watorek, W., Farley, D., Salvesen, G. & Travis, J. (1988). Neutrophil elastase and cathepsin G: structure, function, and biological control. Advan. Expt. Med. Biol. 240, 23-31.
90. Wibley, K. S. & Barlow, D. J. (1992). The conformational analysis of serine proteinase inhibitors and its applications for drug design. J. Enzyme Inhib. 5, 331-338.
91. Yoshida, N., Everitt, M. T., Neurath, H., Woodbury, R. G. & Powers, J. C. (1980). Substrate specificity of two chymotrypsin-like proteinases from rat mast cells. Studies with peptide 4-nitroanilides and comparison with cathepsin G. Biochemistry, 19, 5799-5804.