Structural studies of cysteine proteases and their inhibitors

Acta Biochimica Polonica

Volumn 48, Issue 1, 2001, Pages 1-20

  Grzonka, Zbigniew ^a   Jankowska, Elzbieta ^a   Kasprzykowski, Franciszek ^a   Kasprzykowska, Regina ^a   Łankiewicz, Leszek ^a   Wiczk, Wiesław ^a   Wieczerzak, Ewa ^a   Ciarkowski, Jerzy ^a   Drabik, Piotr ^a   Janowski, Robert ^b   Kozak, Maciej ^b   Jaskólski, Mariusz ^b,c   Grubb, Anders ^d  

^a UNIVERSITY OF GDA SK   (Poland)

^b ADAM MICKIEWICZ UNIVERSITY   (Poland)

^c POLISH ACADEMY OF SCIENCES   (Poland)

^d LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Cystatins; Cysteine proteases; Structure activity relationship; Synthetic inhibitors

Indexed keywords

AMINO ACID; CYSTEINE PROTEINASE; CYSTEINE PROTEINASE INHIBITOR;

AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME ACTIVE SITE; HUMAN; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN MOTIF; PROTEIN TERTIARY STRUCTURE; REVIEW; SEQUENCE HOMOLOGY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACIDS; ANIMALS; CATALYTIC DOMAIN; CONSERVED SEQUENCE; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 0035227644     PISSN: 0001527X     EISSN: None     Source Type: Journal    
DOI: 10.18388/abp.2001_5108     Document Type: Review

References (110)

1. Barrett, A.J. (1994) Classification of peptidases. Methods Enzymol. 244, 1-15.
2. Hartley, B.S. (1960) Proteolytic enzymes. Annu. Rev. Biochem. 9, 45-72.
3. Otto, H.-H. & Schirmeister, T. (1997) Cysteine proteases and their inhibitors. Chem. Rev. 97, 133-171.
4. Rawlings, N.D. & Barrett, A.J. (1999) MEROPS: The peptidase database. Nucleic Acids Res. 27, 325-331.
5. McGrath, M.E. (1999) The lysosomal cysteine proteases. Annu. Rev. Biophys. Biomol. Struct. 28, 181-204.
6. Schechter, I. & Berger, A. (1967) On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27, 157-162.
7. Turk, D., Gunčar, G., Podobnik, M. & Turk, B. (1998) Revised definition of substrate sites of papain-like cysteine proteases. Biol. Chem. 379, 137-147.
8. Berti, P.J. & Storer, A.C. (1995) Alignment/phylogeny of the papain superfamily of cysteine proteases. J. Mol. Biol. 246, 273-283.
9. Turk, B., Turk, V. & Turk, D. (1997) Structural and functional aspects of papain-like cysteine proteinases and their protein inhibitors. Biol. Chem. 378, 141-150.
10. Storer, A.C. & Menard, R. (1994) Catalytic mechanism in papain family of cysteine peptidases. Methods Enzymol. 244, 486-500.
11. Kirschke, H., Barrett, A.J. & Rawlings, N.D. (1995) Proteinases 1: Lysosomal cysteine proteinases; in Proteine Profile 2 (Sheterline, P., ed.) pp. 1587-1643, Oxford University Press.
12. Afonso, S., Romagnano, L. & Babiarz, B. (1997) The expression and function of cystatin C and cathepsin B and cathepsin L during mouse embryo implantation and placentation. Development 124, 3415-3425.
13. Henskens, M.C., Veerman, E.C.I. & Amerongen, A.V.N. (1996) Cystatins in health and disease. Biol. Chem. Hoppe-Seyler 377, 71-86.
14. Grubb, A. (2000) Cystatin C - properties and use as diagnostic marker. Adv. Clin. Chem. 35, 63-99.
15. Warwas, M. & Haczyńska, H. (1998) Rola cystatyn w procesie nowotworowym i jego diagnostyce. Post. Hig. Med. Dośw. 52, 515-526 (in Polish).
16. Machleidt, W., Borchart, U., Fritz, H., Brzin, J., Ritonja, A. & Turk, V. (1983) Protein inhibitors of cysteine proteinases: II. Primary structure of stefin, a cytosolic protein inhibitor of cysteine proteinases from human polymorphonuclear granulocytes. Hoppe-Seyler's Physiol. Chem. 364, 1481-1486.
17. Green, G.D.J., Kembhavi, A.A., Davies, M.E. & Barrett, A.J. (1984) Cystatin-like proteinase inhibitors from human liver. Biochem. J. 218, 939-946.
18. Ritonja, A., Machleidt, W. & Barrett, A.J. (1985) Amino acid sequence of the intracellular cysteine proteinase inhibitor cystatin B from human liver. Biochem. Biophys. Res. Commun. 131, 1187-1192.
19. Takeda, A., Kobayashi, S. & Samejima, T. (1983) Isolation and characterization of two thiol proteinase inhibitors of low molecular weight from newborn rat epidermis. J. Biochem. 94, 811-820.
20. Turk, B., Križaj, I. & Turk, V. (1992) Isolation and characterization of bovine stefin B. Biol. Chem. Hoppe-Seyler 373, 441-446.
21. Turk, B., Ritonja, A., Björk, I., Stoka, V., Dolenc, I. & Turk, V. (1995) Identification of bovine stefin A, a novel inhibitor of cysteine proteinases. FEBS Lett. 360, 101-105.
22. Lenarčič, B., Ritonja, A., Dolenc, I., Stoka, V., Berbic, S., Pungercar, J., Strukelj, P. & Turk, V. (1993) Pig leukocyte cysteine proteinase inhibitor (PLCPI), a new member of stefin family. FEBS Lett. 336, 289-292.
23. Kondo, H., Ijjri, S., Abe, K., Maeda, H. & Arai, S. (1992) Inhibitory effect of oryzacystatins and a truncation mutant on the replication of poliovirus in infected Vero cells. FEBS Lett. 299, 48-50.
24. Lenarčič, B., Križaj, I., Zunec, P. & Turk, V. (1996) Differences in specificity for the interactions of stefins A, B and D with cysteine proteinases. FEBS Lett. 395, 113-118.
25. Rawlings, N.D. & Barrett, A.J. (1990) Evolution of proteins of the cystatin superfamily. J. Mol. Evol. 30, 60-71.
26. Lenarčič, B., Ritonja, A., Sali, A., Kotnik, M., Turk, V. & Machleidt, W. (1986) Properties and structure of human spleen stefin B - a low molecular weight protein inhibitor of cysteine proteinases; in Cysteine Proteinases and their Inhibitors (Turk, V., ed.) pp. 473-487, Walter de Gruyter.
27. Katunuma, N. & Kominami, E. (1986) Distribution and localization of lysosomal cysteine proteinases and cystatins; in Cysteine Proteinases and their Inhibitors (Turk, V., ed.) pp. 219-227, Walter de Gruyter.
28. Abrahamson, M. (1993) Cystatins - protein inhibitors of papain-like cysteine proteinases. Ciencia e Cultura 45, 229-304.
29. Hsieh, W.-T., Fong, D., Sloane, B.F., Golembieski, W. & Smith, D.I. (1991) Mapping of the gene for human cysteine proteinase inhibitor stefin A, STFI, to chromosome 3cen-q21. Genomics 9, 207-209.
30. Pennacchio, L.A., Lahesjoki, A.E., Stone, N.B., Willour, V.L., Virtaneva, K., Miao, J., D'Amato, E., Ramirez, L., Faham, M., Koskiniemi, M., Warrington, J.A., Norio, R., de la Chapelle, A., Cox, D.R. & Myers, R.M. (1996) Mutations in the gene encoding cystatin B in progressive myoclonus epilepsy (EPM1). Science 271, 1731-1734.
31. Fossum, K. & Whitaker, J.R. (1968) Ficin and papain inhibitor from chicken egg white. Arch. Biochem. Biophys. 125, 367-375.
32. Sen, L.C. & Whitaker, J.R. (1973) Some properties of a ficin-papain inhibitor from avian egg white. Arch. Biochem. Biophys. 158, 623-632.
33. Saitoh, E., Sabatini, L., Eddy, R.L., Shows, T.B., Azen, S., Isemura, S. & Sanada, K. (1989) The human cystatin C gene (CST3) is a member of the cystatin gene family which is localized on chromosome 20. Biochem. Biophys. Res. Commun. 162, 1324-1331.
34. Freije, J.P., Pendas, A.M., Velasco, G., Roca, A., Abrahamson, M. & Lopez-Otin, C. (1993) Localization of the human cystatin D gene (CST5) to human chromosome 20p11.21 by in situ hybridization. Cytogen. Cell. Genet. 62, 29-31.
35. Isemura, S., Saitoh, E., Sanada, K. & Minekata, K. (1991) Identification of full-sized forms of salivary (S-type) cystatins (cystatin SN, cystatin SA, cystatin S, and two phosphorylated forms of cystatin S) in human whole saliva and determination of phosphorylation sites of cystatin S. J. Biochem. (Tokyo) 110, 648-654.
36. Balbin, B., Freije, J.P., Abrahamson, M., Velasco, G., Grubb, A. & Lopez-Otin, C. (1993) A sequence variation in the human cystatin D gene resulting in an amino acid (Cys/Arg) polymorphism at the protein level. Hum. Genet. 90, 668-669.
37. Freije, J.P., Balbin, M., Abrahamson, M., Velasco, G., Dalbøge, M., Grubb, A. & Lopez-Otin, C. (1993) Human cystatin D. cDNA cloning, characterization of the Escherichia coli expressed inhibitor, and identification of the native protein in saliva. J. Biol. Chem. 268, 15737-15744.
38. Ni, J., Abrahamson, M., Zhang, M., Alvarez-Fernandez, M., Grubb, A., Su, J., Yu, G.-L., Li, Y., Parmelee, D., Xing, L., Coleman, T.A., Gentz, S., Thotakura, R., Nguyen, N., Hesselberg, M. & Gentz, R. (1997) Cystatin E is a novel human cysteine proteinase inhibitor with structural resemblance to family 2 cystatins. J. Biol. Chem. 272, 10853-10858.
39. Sotiropoulou, G., Anisonowicz, A. & Sager, R. (1997) Identification, cloning, and characterization of cystatin M, a novel cysteine proteinase inhibitor, down-regulated in breast cancer. J. Biol. Chem. 272, 903-910.
40. Ni, J., Fernandez, M.A., Danielsson, L., Chillakuru, R.A., Zhong, J., Grubb, A., Su, J., Gentz, R. & Abrahamson, M. (1998) Cystatin F is a glycosylated human low molecular weight cysteine proteinase inhibitor. J. Biol. Chem. 273, 24797-24804.
41. Halfon, S., Ford, J., Foster, J., Dowling, L., Lucian, L., Sterling, M., Xu, Y., Weiss, M., Ikeda, M., Liggett, D., Helm, A., Caux, C., Lebecques, S., Hannum, C., Menon, S., Mc Clanahan, T., Gorman, D. & Zurawski, G. (1998) Leukocystatin, a new class II cystatin expressed selectively by hematopoietic cells. J. Biol. Chem. 273, 16400-16408.
42. Grubb, A. & Lofberg, H. (1982) Human γ-trace, a basic microprotein: Amino acid sequence and presence in the adenophysis. Proc. Natl. Acad. Sci. U.S.A. 79, 3024-3027.
43. Abrahamson, M., Grubb, A., Olafsson, I. & Lundwall, A. (1987) Molecular cloning and sequence analysis of cDNA coding for the precursor of the human cysteine proteinase inhibitor cystatin C. FEBS Lett. 216, 229-233.
44. Abrahamson, M., Ritonja, A., Brown, M.A., Grubb, A., Machleidt, W. & Barrett, A.J. (1987) Identification of the probable inhibitory reactive sites of the cysteine proteinase inhibitors human cystatin C and chicken cystatin. J. Biol. Chem. 262, 9688-9694.
45. Abrahamson, M., Barrett, A.J., Salvessen, G. & 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.
46. DeLa Cadena, R.A. & Colman, R.N. (1991) Structure and functions of human kininogens. Trends Pharmacol. Sci. 12, 272-275.
47. Brown, W.M. & Dziegielewska, K.M. (1997) Friends and relations of the cystatin superfamily - New members and their evolution. Protein Sci. 6, 5-12.
48. Murzin, A. (1993) Sweet-tasting protein monellin is related to the cystatin family of thiol proteinase inhibitors. J. Mol. Biol. 230, 680-694.
49. Somoza, J.R., Jiang, F., Tong, L., Kang, C.-H., Cho, J.M. & Kim, S.-H. (1993) The crystal structures of a potently sweet protein. Natural monellin at 2.75 Å resolution and a single-chain monellin at 1.7 Å resolution. J. Mol. Biol. 234, 390-404.
50. Bode, W., Engh, R., Musil, D., Laber, B., Stubbs, M., Huber, R. & Turk, V. (1990) Mechanism of interaction of cysteine proteinases and their protein inhibitors as compared to the serine proteinase-inhibitor interaction. Biol. Chem. Hoppe-Seyler 371, 111-118.
51. Björk, I. & Ylinenjärvi, K. (1989) Interaction of chicken cystatin with inactivated papains. Biochem. J. 260, 61-68.
52. Abrahamson, M. (1994) Cystatins. Methods Enzymol. 244, 685-700.
53. Lindahl, P., Abrahamson, M. & Björk, I. (1992) Interaction of recombinant human cystatin C with cysteine proteinases papain and actinidin. Biochem. J. 28, 49-55.
54. Müller-Esterl, W., Fritz, H., Machleidt, W., Ritonja, A., Brzin, J., Kotnik, M., Turk, V., Kellermann, J. & Lottspeich, F. (1985) Human plasma kininogens are identical with α-cysteine proteinase inhibitors. FEBS Lett. 182, 310-314.
55. Barrett, A.J., Rawlings, N.D., Davies, M.E., Machleidt, W., Salvesen, G. & Turk, V. (1986) Cysteine proteinase inhibitors of the cystatin superfamily; in Proteinase Inhibitors (Barrett, A.J. & Salvesen, G., eds.) pp. 515-569, Springer-Verlag.
56. Grubb, A., Abrahamson, M., Olafsson, I., Trojnar, J., Kasprzykowska, R., Kasprzykowski, F. & Grzonka, Z. (1990) Synthesis of cysteine proteinase inhibitors structurally based on the proteinase interacting N-terminal region of human cystatin C. Biol. Chem. Hoppe-Seyler 371 (Suppl.), 137-144.
57. Bode, W., Engh, R., Musil, D., Thiele, U., Huber, R., Karshnikov, A., Brzin, J., Kos, J. & Turk, V. (1988) The 2.0 Å X-ray crystal structure of chicken egg white cystatin and its possible mode of interaction with cysteine proteinases. EMBO J. 7, 2593-2599.
58. Stubbs, M.T., Laber, B., Bode, W., Huber, R., Jerala, R., Lenarčič, B. & Turk, V. (1990) The refined 2.4 Å X-ray crystal structure of the recombinant human stefin B in complex with the cysteine proteinase papain: A novel type of proteinase inhibitor interaction. EMBO J. 9, 1939-1947.
59. Martin, J.R., Jerala, R., Kroon-Zitko, L., Žerovnik, E., Turk, V. & Waltho, J.P. (1994) Structural characterization of human stefin A in solution and implications for binding to cysteine proteinases. Eur. J. Biochem. 225, 1181-1194.
60. Martin, J.R., Craven, C.J., Jerala, R., Kroon-Zitko, L., Žerovnik, E., Turk, V. & Waltho, J.P. (1995) The three-dimensional solution structure of human stefin A. J. Mol. Biol. 246, 331-343.
61. Abrahamson, M., Olafsson, I., Palsdottir, A. Ulvsbäck, M., Lundwall, Å., Jensson, O. & Grubb, A. (1990) Structure and expression of the human cystatin C gene. Biochem. J. 268, 287-294.
62. Schnittger, S., Gopal Rao, V.V.N., Abrahamson, M. & Hansmann, L. (1993) Cystatin C (CST3), the candidate gene for hereditary cystatin C amyloid angiopathy (HCCAA), and other members of the cystatin gene family are clustered on chromosome 20p11.2. Genomics, 16, 50-55.
63. Grubb, A., Weiber, H. & Löfberg, H. (1983) The γ-trace concentration of normal human seminal plasma is thirty-six times that of normal human blood plasma. Scand. J. Clin. Lab. 43, 421-425.
64. Grubb, A. (1992) Diagnostic value of analysis of cystatin C and protein HC in biological fluids. Clin. Nephrol. 38 (Suppl. 1), S20-S27.
65. Randers, E. & Erlandsen, E.J. (1999) Serum cystatin C as an endogenous marker of the renal function - a review. Clin. Chem. Lab. Med. 37, 389-395.
66. Hall, A., Håkansson, K., Mason, R. W., Grubb, A. & Abrahamson, M. (1995) Structural basis for the biological specificity of cystatin C. Identification of leucine 9 in the N-terminal binding region as a selectivity-conferring residue in the inhibition of mammalian cysteine peptidases. J. Biol. Chem. 270, 5115-5121.
67. Mason, R.W., Sol-Church, K. & Abrahamson, M. (1998) Amino acid substitutions in the N-terminal segment of cystatin C create selective protein inhibitors of lysosomal cysteine proteinases. Biochem. J. 330, 833-838.
68. Hall, A., Dalbøge, H., Grubb, A. & Abrahamson, M. (1993) Importance of the evolutionary conserved glycine residue in the N-terminal region of human cystatin C. Biochem. J. 291, 123-129.
69. Ekiel, I., Abrahamson, M., Fulton, D.B., Lindahl, P., Storer, A.C., Levadoux, W., Lafrance, M., Labelle, S., Pomerleau, Y., Groleau, D., LeSauteur, L. & Gehring, K. (1997) NMR structural studies of human cystatin C dimers and monomers. J. Mol. Biol. 271, 266-277.
70. Hall, A., Ekiel, I., Mason, R.W., Kasprzykowski, F., Grubb, A. & Abrahamson, M. (1998) Structural basis for different inhibitory specificities of human cystatins C and D. Biochemistry 37, 4071-4079.
71. Gudmundsson, G., Hallgrimsson, J., Jonasson, T.A. & Bjarnason, O. (1972) Hereditary cerebral hemorrhage with amyloidosis. Brain 95, 387-404.
72. Löfberg, H., Grubb, A., Nilsson, E.K., Jensson, O., Gudmundsson, G., Blondal, H., Arnason, A. & Thorsteinsson, L. (1987) Immunohistochemical characterization of the amyloid deposits and quantification of pertinent cerebrospinal proteins in hereditary cerebral hemorrhage with amyloidosis. Stroke 18, 431-440.
73. Abrahamson, M. & Grubb, A. (1994) Increased body temperature accelerates aggregation of the Leu→Gln mutant cystatin C, the amyloid-forming protein in hereditary cystatin C amyloid angiopathy. Proc. Natl. Acad. Sci. U.S.A. 91, 1416-1420.
74. Olafsson, I. & Grubb, A. (2000) Hereditary cystatin C amyloid angiopathy. J. Exp. Clin. Invest. 7, 70-79.
75. Gerhartz, B., Ekiel, I. & Abrahamson, M. (1998) Two stable unfolding intermediates of the disease-causing L68Q variant of human cystatin C. Biochemistry 37, 17309-17317.
76. Žerovnik, E., Cimerman, N., Kos, J., Turk, V. & Lohner, K. (1997) Thermal denaturation of human cystatin C and two of its variants; comparison to chicken cystatin. Biol. Chem. Hoppe-Seyler 378, 1199-1203.
77. Ekiel, I. & Abrahamson, M. (1996) Folding-related dimerization of human cystatin C. J. Biol. Chem. 271, 1314-1321.
78. Jankowska, E., Banecki, B., Wiczk, W. & Grzonka, Z. (1999) Self-association of cystatin; in Peptide Science - Present and Future (Shomonishi, Y., ed.), pp. 654-656, Kluwer Academic Publishers, Dordrecht.
79. Oberg, K.A. & Fink, A.L. (1998) A new attenuated total reflectance Fourrier transform infrared spectroscopy method for the study of protein in solution. Anal. Biochem. 256, 92-106.
80. Grzonka, Z., Kasprzykowski, F., Oldziej, S., Wiczk, W. & Grubb, A. (1993) Recent developments in the chemistry and biology of cystatins; in Peptide Chemistry 1992 (Yanaihara, N., ed.) pp. 243-246, ESCOM, Leiden.
81. Dieckmann, T., Mitschang, L., Hofmann, M., Kos, J., Turk, V., Auerswald, E.A., Jaenicke, R. & Oschkinat, H. (1993) The structures of native phosphorylated chicken cystatin and of recombinant unphosphorylated variant in solution. J. Mol. Biol. 234, 1048-1059.
82. Engh, R.A., Dieckmann, T., Bode, W., Auerswald, E.A., Turk, V., Huber, R. & Oschkinat, H. (1993) Conformational variability of chicken cystatin. Comparison of structures determined by X-ray diffraction and NMR spectroscopy. J. Mol. Biol. 234, 1060-1069.
83. Alvarez-Fernadez, M., Abrahamson, M. & Su, X.-D. (2000) Crystal structure of cystatin D, an inhibitor of papain-like cysteine proteinases; in Max-lab Activity Report 1999 (Andersen, J.N., Nyholm, S.L. & Sorensen, H., eds.) pp. 224-225.
84. Abrahamson, M., Mason, R.W., Hansson, H., Buttle, D.J., Grubb, A. & Ohlsson, K. (1991) Human cystatin C. Role of the N-terminal segment in the inhibition of human cysteine proteinases and in its inactivation by leucocyte elastase. Biochem. J. 273, 621-626.
85. Grubb, A., Löfberg, H. & Barrett, A.J. (1984) The disuphide bridges of human cystatin C (γ-trace) and chicken cystatin. FEBS Lett. 170, 370-374.
86. Barret, A.J. (1987) The cystatins: A new class of peptidase inhibitors. Trends Biochem. Sci. 12, 193-196.
87. Kozak, M., Jankowska, E., Janowski, R., Grzonka, Z., Grubb, A., Alvarez-Fernadez, M., Abrahamson, M. & Jaskólski, M. (1999) Expression of a selonomethionyl derivative and preliminary crystallographic studies of human cystatin C. Acta Crystallogr. D55, 1939-1942.
88. Abrahamson, M., Dalbøge, H., Olafsson, I., Carlsen, S. & Grubb, A. (1988) Efficient production of native, biologically active human cystatin C by Escherichia coli. FEBS Lett. 236, 14-18.
89. Matthews, B.W. (1968) Solvent content in protein crystals. J. Mol. Biol. 33, 491-497.
90. Björck, L., Åkesson, P., Bohus, M., Trojnar, J., Abrahamson, M., Olafsson, I. & Grubb, A. (1989) Bacterial growth blocked by a synthetic peptide based on the structure of a human proteinase inhibitor. Nature 337, 385-386.
91. Hall, A., Abrahamson, M., Grubb, A., Trojnar, J., Kania, P., Kasprzykowska, R. & Kasprzykowski, F. (1992) Cystatin C based peptidyl diazomethanes as cysteine proteinase inhibitors: Influence of the peptidyl chain length. J. Enzyme. Inhib. 6, 113-123.
92. Kasprzykowski, F., Kasprzykowska, R., Plucińska, K., Kania, P., Grubb, A., Abrahamson, M. & Schalen, C. (2001) Peptidyl diazomethylketones as cysteine protease inhibitors structurally based upon the inhibitory centers of cystatins. Pol. J. Chem. (in press).
93. Leary, R., Larsen, D., Watanabe, H. & Shaw, E. (1977) Diazomethyl ketone substrate derivatives as active-site-directed inhibitors of thiol proteases. Papain. Biochemistry 16, 5857-5861.
94. Tarnowska, M., Ołdziej, S., Liwo, A., Kania, P., Kasprzykowski, F. & Grzonka, Z. (1992) MNDO study of the mechanism of the inhibition of cysteine proteinases by diazomethyl ketones. Eur. Biophys. J. 21, 217-222.
95. Johansson, L., Grubb, A., Abrahamson, M., Kasprzykowski, F., Kasprzykowska, R., Grzonka, Z. & Lerner, U.H. (2000) A peptidyl derivative structurally based on the inhibitory center of cystatin C inhibits bone resorption in vitro. Bone 26, 451-459.
96. Barrett, A.J., Kembhavi, A., Brown, M.A., Kirschke, H., Knight, C.G., Tamai, M. & Hanada, K. (1982) L-trans-epoxysuccinyl-leucylamido(4-guanidino)butane (E-64) and its analogues as inhibitors of cysteine proteinases including cathepsins B, H and L. Biochem. J. 201, 189-198.
97. Matsumoto, K., Mizoue, K., Kitamura, K., Tse, W.C., Huber, C.P. & Ishida, T. (1999) Structural basis of inhibition of cysteine proteases by E-64 and its derivatives. Biopolymers 51, 99-107.
98. Kasprzykowski, F., Schalen, C., Kasprzykowska, R., Jastrzçbska, B. & Grubb, A. (2000) Synthesis and antibacterial properties of peptidyl derivatives and cyclopeptides structurally based upon the inhibitory center of human cystatin C. APMIS 108, 471-481.
99. Yamamoto, D., Matsumoto, K., Ohishi, H., Inoue, M., Kitamura, K. & Mizuno, H. (1991) Refined X-ray structure of papain E-64 complex at 2.1 Å resolution. J. Biol. Chem. 266, 14771-14777.
100. Kozak, M., Kozian, E., Grzonka, Z. & Jaskólski, M. (1997) Crystalization and preliminary crystallographic studies of a covalent complex between papain an oxirane-based inhibitor; in Peptides 1996 (Ramage, R. & Epton, E., eds.) pp. 551-552, European Peptide Society.
101. Drenth, J. & Jansonius, J.N. (1959) The unit cell of mercuripapain crystals. Nature 28, 1718-1719.
102. Czaplewski, C., Grzonka, Z., Jaskólski, M., Kasprzykowski, F., Kozak, M., Politowska, E. & Ciarkowski, J. (1999) Binding modes of a new epoxysuccinyl-peptide inhibitor of cysteine proteases. Where and how do cysteine proteases express their selectivity? Biochim. Biophys. Acta 1431, 290-305.
103. Drenth, J., Kalk, K.H. & Swen, H.M. (1976) Binding of chloromethyl ketone substrate analogues to crystalline papain. Biochemistry 15, 3731-3738.
104. Pickersgill, R.W., Harris, G.W. & Garman, E. (1992) Structure of monoclinic papain at 1.6 Å resolution. Acta Crystallogr. B48, 59-67.
105. SYBFL 6.1. (1994) Tripos Inc., 1699 S. Manley Rd., St. Louis, MO 63144, U.S.A.
106. Bernstein, F.C., Koetzle, T.F., Williams, G.J.B., Meyer, E.F., Jr., Brice, M.D., Rodgers, J.R., Kennard, O., Shimanouchi, T. & Tasami, M. (1977) The protein data bank: A computer-based archive file for macromolecular structures. J. Mol. Biol. 112, 535-542.
107. Case, D.A., Pearlman, D.A., Caldwell, J.W., Cheatham III, T.E., Ross, W.S., Darden, T., Merz, K.M., Stanton, R.V., Cheng, A., Vincent, J.J., Crowley, M., Ferguson, D.M., Radmer, R., Seibel, G.L., Singh, U.C., Wiener, P. & Kollman, P.A. (1997) Amber 5.0, University of California, San Francisco.
108. Bayly, C.I., Cieplak, P., Cornell, W.D. & Kollman, P.A. (1993) A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges: The RESP model. J. Phys. Chem. 97, 10269-10280.
109. Schroder, E., Phillips, C., Garman, E., Harlos, K. & Crawford, C. (1993) X-Ray crystallographic structure of a papain-leupeptin complex. FEBS Lett. 315, 38-42.
110. Varughese, K.I., Ahmed, F.R., Carey, P.R., Hasnain, S., Huber, C.P. & Storer, A.C. (1989) Crystal structure of a papain-E-64 complex. Biochemistry 28, 1330-1332.