Structure and stability of the non-covalent swapped dimer of bovine seminal ribonuclease - An enzyme tailored to evade ribonuclease protein inhibitor(443 views) Sica F, Di Fiore A, Merlino A, Mazzarella L
Keywords: Cells, Cytology, Dimerization, Enzyme Inhibition, Proteins, Stability, Cytoxicity, Malignant Cells, Non-Covalent Dimer (ncd), Deoxycytidyl 2, Deoxyadenosine, Cysteine, Protein Inhibitor, Ribonuclease, Unclassified Drug, Amino Terminal Sequence, Article, Cancer Cell, Cattle, Comparative Study, Complex Formation, Crystal Structure, Cytosol, Cytotoxicity, Disulfide Bond, Enzyme Stability, Enzyme Structure, In Vitro Study, In Vivo Study, Isomer, Methylation, Nonhuman, Priority Journal, Sperm, Structure Analysis, Animals, Chromatography, High Pressure Liquid, Circular Dichroism, Crystallography, X-Ray, Endoribonucleases, Heat, Kinetics, Models, Molecular, Protein Binding, Protein Conformation, Protein Folding, Protein Isoforms, Protein Structure, Quaternary, Secondary, Tertiary, Pancreatic, Time Factors, Bos Taurus, Bovinae,
Affiliations: *** IBB - CNR ***
Dipartimento di Chimica, Univ. Studi di Napoli Federico II, Via Cynthia, 80126 Napoli, Italy
Ist. di Biostrutture e Bioimmagini, CNR, Via Mezzocannone 6, 80134 Napoli, Italy
Dipto. di Scienze Farmaceutiche, Universita degli Studi di Salerno, Via ponte don Melillo, 84084, Fisciano (Sa), Italy
References: Schein, C.H., (1997) Nat. Biotechnol., 15, pp. 529-53
Raines, R.T., (1998) Chem. Rev., 98, pp. 1045-1065
Youle, R.J., D'Alessio, G., (1997) Ribonuclease: Structures and Functions, pp. 491-514. , (D'Alessio, G., and Riordan, J. F., eds), Academic Press, San Diego
Leland, P.A., Raines, R.T., (2001) Chem. Biol., 8, pp. 405-413
Makarov, A.A., Ilinskaya, O.N., (2003) FEBS Lett., 540, pp. 15-20
Matousek, J., Soucek, J., Slavik, T., Tomanek, M., Lee, J.E., Raines, R.T., (2003) Comp. Biochem. Physiol. C Toxicol. Pharmacol., 136, pp. 343-356
Kim, J.S., Soucek, J., Matousek, J., Raines, R.T., (1995) J. Biol. Chem., 270, pp. 10525-10530
Antignani, A., Naddeo, M., Cubellis, M.V., Russo, A., D'Alessio, G., (2001) Biochemistry, 40, pp. 3492-3496
Cinatl Jr., J., Cinatl, J., Kotchetkov, R., Matousek, J., Woodcock, B.G., Koehl, U., Vogel, J.U., Schwabe, D., (2000) Anticancer Res., 20, pp. 853-859
Mikulski, S.M., Costanzi, J.J., Vogelzang, N.J., McCachren, S., Taub, R.N., Chun, H., Mittelman, A., Shogen, K., (2002) J. Clin. Oncol., 20, pp. 274-281
Mikulski, S.M., (1995) Int. J. Oncol., 7, pp. 1415-1420
Mikulski, S.M., Viera, A., Shogen, K., (1993) Int. J. Oncol., 2, pp. 807-812
Haigis, M.C., Raines, R.T., (2003) J. Cell Sci., 116, pp. 313-324
D'Alessio, G., Di Donato, A., Mazzarella, L., Piccoli, R., (1997) Ribonuclease: Structures and Functions, pp. 383-423. , (D'Alessio, G., and Riordan, J. F., eds), Academic Press, San Diego
Piccoli, R., Tamburrini, M., Piccialli, G., Di Donato, A., Parente, A., D'Alessio, G., (1992) Proc. Natl. Acad. Sci. U. S. A., 89, pp. 1870-1874
Mazzarella, L., Capasso, S., Demasi, D., Di Lorenzo, G., Mattia, C.A., Zagari, A., (1993) Acta Crystallogr. Sect. D, 49, pp. 389-402
Berisio, R., Sica, F., De Lorenzo, C., Di Fiore, A., Piccoli, R., Zagari, A., Mazzarella, L., (2003) FEBS Lett., 554, pp. 105-110
Merlino, A., Vitagliano, L., Sica, F., Zagari, A., Mazzarella, L., (2004) Biopolymers, 73, pp. 689-695
Di Donato, A., Piccoli, R., D'Alessio, G., (1987) Biochem. J., 241, pp. 435-440
Piccoli, R., Di Donato, A., D'Alessio, G., (1988) Biochem. J., 253, pp. 329-336
Cafaro, V., De Lorenzo, C., Piccoli, R., Bracale, A., Mastronicola, M.R., Di Donato, A., D'Alessio, G., (1995) FEBS Lett., 359, pp. 31-34
Murthy, B.S., De Lorenzo, C., Piccoli, R., D'Alessio, G., Sirdeshmukh, R., (1996) Biochemistry, 35, pp. 3880-3885
Sorrentino, S., Barone, R., Bucci, E., Gotte, G., Russo, N., Libonati, M., D'Alessio, G., (2000) FEBS Lett., 466, pp. 35-39
Canals, A., Pous, J., Guasch, A., Benito, A., Ribo, M., Vilanova, M., Coll, M., (2001) Structure, 9, pp. 967-976
Liu, Y., Hart, P.J., Schlunegger, M.P., Eisenberg, D., (1998) Proc. Natl. Acad. Sci. U. S. A., 95, pp. 3437-3442
Liu, Y., Gotte, G., Libonati, M., Eisenberg, D., (2001) Nat. Struct. Biol., 8, pp. 211-214
Matousek, J., Gotte, G., Pouckova, P., Soucek, J., Slavik, T., Vottariello, F., Libonati, M., (2003) J. Biol. Chem., 278, pp. 23817-23822
Kunitz, M., (1946) J. Biol. Chem., 164, pp. 563-568
Otwinowsky, Z., Minor, W., (1997) Methods Enzymol., 276, pp. 307-326
Bailey, S., (1994) Acta Crystallogr. Sect. D, 50, pp. 760-763
Matthews, B.W., (1968) J. Mol. Biol., 33, pp. 491-497
Esnouf, R.M., (1999) Acta Crystallogr. Sect. D, 55, pp. 938-940
Jones, T.A., Bergdoll, M., Kjeldgaard, M., (1990) Crystallography Model Methods Molecular Design, pp. 189-199. , (Bugg, C., and Ealick, S., eds), Springer-Verlag Press, New York
Laskowski, R.A., MacArthur, M.W., Moss, M.D., Thorton, J.M., (1993) J. Appl. Crystallogr., 26, pp. 283-291
Kobe, B., Deisenhofer, J., (1995) Nature, 374, pp. 183-186
Sica, F., Di Fiore, A., Zagari, A., Mazzarella, L., (2003) Proteins, 52, pp. 263-271
Zegers, I., Maes, D., Dao-Thi, M.H., Poortmans, F., Palmer, R., Wyns, L., (1994) Protein Sci., 3, pp. 2322-2339
Gilliland, G., (1997) Ribonuclease: Structures and Functions, pp. 306-341. , (D'Alessio, G., and Riordan, J. F., eds), Academic Press, San Diego
Vitagliano, L., Adinolfi, S., Riccio, A., Sica, F., Zagari, A., Mazzarella, L., (1998) Protein Sci., 7, pp. 1691-1699
Vitagliano, L., Merlino, A., Zagari, A., Mazzarella, L., (2002) Proteins, 46, pp. 97-104
Mazzarella, L., Vitagliano, L., Zagari, A., (1995) Proc. Natl. Acad. Sci. U. S. A., 92, pp. 3799-3803
Avitabile, F., Alfano, C., Spadaccini, R., Crescenzi, O., D'Ursi, A.M., D'Alessio, G., Tancredi, T., Picone, D., (2003) Biochemistry, 42, pp. 8704-8711
Liu, Y., Eisenberg, D., (2002) Protein Sci., 11, pp. 1285-1299
Murthy, B.S., Sirdeshmukh, R., (1992) Biochem. J., 281, pp. 343-348
Schlunegger, M.P., Bennett, M.J., Eisenberg, D., (1997) Adv. Protein Chem., 50, pp. 61-122
D'Alessio, G., (1999) Eur. J. Biochem., 266, pp. 699-708
Kraulis, P.J., (1991) J. Appl. Crystallogr., 24, pp. 946-950
Schein, C. H., (1997) Nat. Biotechnol., 15, pp. 529-53
Raines, R. T., (1998) Chem. Rev., 98, pp. 1045-1065
Youle, R. J., D'Alessio, G., (1997) Ribonuclease: Structures and Functions, pp. 491-514. , (D'Alessio, G., and Riordan, J. F., eds), Academic Press, San Diego
Leland, P. A., Raines, R. T., (2001) Chem. Biol., 8, pp. 405-413
Makarov, A. A., Ilinskaya, O. N., (2003) FEBS Lett., 540, pp. 15-20
Kim, J. S., Soucek, J., Matousek, J., Raines, R. T., (1995) J. Biol. Chem., 270, pp. 10525-10530
Mikulski, S. M., Costanzi, J. J., Vogelzang, N. J., McCachren, S., Taub, R. N., Chun, H., Mittelman, A., Shogen, K., (2002) J. Clin. Oncol., 20, pp. 274-281
Mikulski, S. M., (1995) Int. J. Oncol., 7, pp. 1415-1420
Mikulski, S. M., Viera, A., Shogen, K., (1993) Int. J. Oncol., 2, pp. 807-812
Wei, C. W., Hu, C. C., Tang, C. H., Lee, M. C., Wang, J. J., (2002) FEBS Lett., 531, pp. 421-426
Haigis, M. C., Kurten, E. L., Raines, R. T., (2003) Nucleic Acids Res., 31, pp. 1024-1032
Haigis, M. C., Raines, R. T., (2003) J. Cell Sci., 116, pp. 313-324
Murthy, B. S., De Lorenzo, C., Piccoli, R., D'Alessio, G., Sirdeshmukh, R., (1996) Biochemistry, 35, pp. 3880-3885
Crestfield, A. M., Stein, W. H., Moore, S., (1962) Arch. Biochem. Biophys., 1, pp. 217-222
Liu, Y., Hart, P. J., Schlunegger, M. P., Eisenberg, D., (1998) Proc. Natl. Acad. Sci. U. S. A., 95, pp. 3437-3442
Matthews, B. W., (1968) J. Mol. Biol., 33, pp. 491-497
Esnouf, R. M., (1999) Acta Crystallogr. Sect. D, 55, pp. 938-940
Jones, T. A., Bergdoll, M., Kjeldgaard, M., (1990) Crystallography Model Methods Molecular Design, pp. 189-199. , (Bugg, C., and Ealick, S., eds), Springer-Verlag Press, New York
Laskowski, R. A., MacArthur, M. W., Moss, M. D., Thorton, J. M., (1993) J. Appl. Crystallogr., 26, pp. 283-291
Murthy, B. S., Sirdeshmukh, R., (1992) Biochem. J., 281, pp. 343-348
Ciglic, M. I., Jackson, P. J., Raillard, S. A., Haugg, M., Jermann, T. M., Opitz, J. G., Trabesinger-Ruf, N., Benner, S. A., (1998) Biochemistry, 37, pp. 4008-4022
Kraulis, P. J., (1991) J. Appl. Crystallogr., 24, pp. 946-950
Structure and stability of the non-covalent swapped dimer of bovine seminal ribonuclease - An enzyme tailored to evade ribonuclease protein inhibitor
A growing number of pancreatic-type ribonucleases (RNases) present cytotoxic activity against malignant cells. The cytoxicity of these enzymes is related to their resistance to the ribonuclease protein inhibitor (RI). In particular, bovine seminal ribonuclease (BS-RNase) is toxic to tumor cells both in vitro and in vivo. BS-RNase is a covalent dimer with two intersubunit disulfide bridges between Cys(31) of one chain and Cys(32) of the second and vice versa. The native enzyme is an equilibrium mixture of two isomers, MxM and M=M. In the former the two subunits swap their N-terminal helices. The cytotoxic action is a peculiar property of MxM. In the reducing environment of cytosol, M=M dissociates into monomers, which are strongly inhibited by RI, whereas MxM remains as a non-covalent dimer (NCD), which evades RI. We have solved the crystal structure of NCD, carboxyamidomethylated at residues Cys(31) and Cys(32) (NCD-CAM), in a complex with 2'-deoxycitidylyl(3'-5')-2'-deoxyadenosine. The molecule reveals a quaternary structural organization much closer to MxM than to other N-terminal-swapped non-covalent dimeric forms of RNases. Model building of the complexes between these non-covalent dimers and RI reveals that NCD-CAM is the only dimer equipped with a quaternary organization capable of interfering seriously with the binding of the inhibitor. Moreover, a detailed comparative structural analysis of the dimers has highlighted the residues, which are mostly important in driving the quaternary structure toward that found in NCD-CAM.
Structure and stability of the non-covalent swapped dimer of bovine seminal ribonuclease - An enzyme tailored to evade ribonuclease protein inhibitor