Enforcing the positive charge of N-termini enhances membrane interaction and antitumor activity of bovine seminal ribonuclease(478 views) D'Errico G, Ercole C, Lista M, Pizzo E, Falanga A, Galdiero S, Spadaccini R, Picone D
Dipartimento di Chimica Paolo Corradini, Università Degli Studi di Napoli Federico II, Via Cintia, 80126 Napoli, Italy
CSGI, Consorzio Interuniversitario per Lo Sviluppo Dei Sistemi A Grande Interfase, Italy
Dipartimento di Biologia Strutturale e Funzionale, Università Degli Studi di Napoli Federico II, Via Cintia, 80126 Napoli, Italy
Dipartimento di Scienze Biologiche, Università Degli Studi di Napoli Federico II, Via Mezzocannone 16, 80134 Napoli, Italy
Istituto di Biostrutture e Bioimmagini, CNR, Via Mezzocannone 16, 80134 Napoli, Italy
References: Inui, M., Martello, G., Piccolo, S., MicroRNA control of signal transduction (2010) Nat. Rev. Mol. Cell Biol., 11, pp. 252-26
Kim, W.C., Lee, C.H., The role of mammalian ribonucleases (RNases) in cancer (2009) Biochim. Biophys. Acta, 1796, pp. 99-113
Rybak, S.M., Arndt, M.A., Schirrmann, T., Dubel, S., Krauss, J., Ribonucleases and immunoRNases as anticancer drugs (2009) Curr. Pharm. Des., 15, pp. 2665-2675
Los, M., New, exciting developments in experimental therapies in the early 21st century (2009) Eur. J. Pharmacol., 625, pp. 1-5
Leich, F., Stohr, N., Rietz, A., Ulbrich-Hofmann, R., Arnold, U., Endocytotic internalization as a crucial factor for the cytotoxicity of ribonucleases (2007) Journal of Biological Chemistry, 282 (38), pp. 27640-27646. , http://www.jbc.org/cgi/reprint/282/38/27640, DOI 10.1074/jbc.M702240200
Rutkoski, T.J., Raines, R.T., Evasion of ribonuclease inhibitor as a determinant of ribonuclease cytotoxicity (2008) Curr. Pharm. Biotechnol., 9, pp. 185-189
Boix, E., Wu, Y.N., Vasandani, V.M., Saxena, S.K., Ardelt, W., Ladner, J., Youle, R.J., Role of the N terminus in RNase a homologues: Differences in catalytic activity, ribonuclease inhibitor interaction and cytotoxicity (1996) Journal of Molecular Biology, 257 (5), pp. 992-1007. , DOI 10.1006/jmbi.1996.0218
Di Donate, A., Cafaro, V., D'Alessio, G., Ribonuclease A can be transformed into a dimeric ribonuclease with antitumor activity (1994) Journal of Biological Chemistry, 269 (26), pp. 17394-17396
Di Gaetano, S., D'Alessio, G., Piccoli, R., Second generation antitumour human RNase: Significance of its structural and functional features for the mechanism of antitumour action (2001) Biochemical Journal, 358 (1), pp. 241-247. , DOI 10.1042/0264-6021:3580241
Antignani, A., Naddeo, M., Cubellis, M.V., Russo, A., D'Alessio, G., Antitumor action of seminal ribonuclease, its dimeric structure, and its resistance to the cytosolic ribonuclease inhibitor (2001) Biochemistry, 40 (12), pp. 3492-3496. , DOI 10.1021/bi002781m
Laccetti, P., Spalletti-Cernia, D., Portella, G., De Corato, P., D'Alessio, G., Vecchio, G., Seminal ribonuclease inhibits tumor growth and reduces the metastatic potential of Lewis lung carcinoma (1994) Cancer Research, 54 (16), pp. 4253-4256
Piccoli, R., Tamburrini, M., Piccialli, G., Di Donato, A., Parente, A., D'Alessio, G., The dual-mode quaternary structure of seminal RNase (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., Bovine seminal ribonuclease: Structure at 1.9 A resolution (1993) Acta Crystallogr. D Biol. Crystallogr., 49, pp. 389-402
Berisio, R., Sica, F., De Lorenzo, C., Di Fiore, A., Piccoli, R., Zagari, A., Mazzarella, L., Crystal structure of the dimeric unswapped form of bovine seminal ribonuclease (2003) FEBS Letters, 554 (1-2), pp. 105-110. , DOI 10.1016/S0014-5793(03)01114-1
Sica, F., Di Fiore, A., Merlino, A., Mazzarella, L., Structure and stability of the non-covalent swapped dimer of bovine seminal ribonuclease: An enzyme tailored to evade ribonuclease protein inhibitor (2004) Journal of Biological Chemistry, 279 (35), pp. 36753-36760. , DOI 10.1074/jbc.M405655200
Giancola, C., Ercole, C., Fotticchia, I., Spadaccini, R., Pizzo, E., D'Alessio, G., Picone, D., Structure-cytotoxicity relationships in bovine seminal ribonuclease: New insights from heat and chemical denaturation studies on variants (2011) FEBS J., 278, pp. 111-122
Saxena, S.K., Rybak, S.M., Winkler, G., Meade, H.M., McGray, P., Youle, R.J., Ackerman, E.J., Comparison of RNases and toxins upon injection into Xenopus oocytes (1991) Journal of Biological Chemistry, 266 (31), pp. 21208-21214
Turcotte, R.F., Lavis, L.D., Raines, R.T., Onconase cytotoxicity relies on the distribution of its positive charge (2009) FEBS J., 276, pp. 3846-3857
Matousek, J., Gotte, G., Pouckova, P., Soucek, J., Slavik, T., Vottariello, F., Libonati, M., Antitumor activity and other biological actions of oligomers of ribonuclease A (2003) Journal of Biological Chemistry, 278 (26), pp. 23817-23822. , DOI 10.1074/jbc.M302711200
Notomista, E., Mancheno, J.M., Crescenzi, O., Di Donato, A., Gavilanes, J., D'Alessio, G., The role of electrostatic interactions in the antitumor activity of dimeric RNases (2006) FEBS Journal, 273 (16), pp. 3687-3697. , DOI 10.1111/j.1742-4658.2006.05373.x
Mancheno, J.M., Gasset, M., Onaderra, M., Gavilanes, J.G., D'Alessio, G., Bovine seminal ribonuclease destabilizes negatively charged membranes (1994) Biochemical and Biophysical Research Communications, 199 (1), pp. 119-124. , DOI 10.1006/bbrc.1994.1202
Eswar, N., Webb, B., Marti-Renom, M.A., Madhusudhan, M.S., Eramian, D., Shen, M.Y., Pieper, U., Sali, A., Comparative protein structure modeling using modeller (2006) Curr. Protoc. Bioinformatics, , Chapter 5 Unit 5 6
Fiser, A., Do, R.K., Sali, A., Modeling of loops in protein structures (2000) Protein Sci., 9, pp. 1753-1773
Koradi, R., Billeter, M., Wuthrich, K., MOLMOL: A program for display and analysis of macromolecular structures (1996) Journal of Molecular Graphics, 14 (1), pp. 51-55. , DOI 10.1016/0263-7855(96)00009-4
Delano, W.L., (2002) The PyMOL Molecular Graphics System, , DeLano Scientific Palo Alto, CA, USA
Rocchia, W., Alexov, E., Honig, B., Extending the applicability of the nonlinear Poisson-Boltzmann equation: Multiple dielectric constants and multivalent ions (2001) Journal of Physical Chemistry B, 105 (28), pp. 6507-6514. , DOI 10.1021/jp010454y
Di Donato, A., D'Alessio, G., Heterogeneity of bovine seminal ribonuclease (1981) Biochemistry, 20, pp. 7232-7237
Di Donato, A., Galletti, P., D'Alessio, G., Selective deamidation and enzymatic methylation of seminal ribonuclease (1986) Biochemistry, 25 (26), pp. 8361-8368. , DOI 10.1021/bi00374a005
Avitabile, F., Alfano, C., Spadaccini, R., Crescenzi, O., D'Ursi, A.M., D'Alessio, G., Tancredi, T., Picone, D., The swapping of terminal arms in ribonucleases: Comparison of the solution structure of monomeric bovine seminal and pancreatic ribonucleases (2003) Biochemistry, 42 (29), pp. 8704-8711. , DOI 10.1021/bi0342517
Ercole, C., Spadaccini, R., Alfano, C., Tancredi, T., Picone, D., A new mutant of bovine seminal ribonuclease with a reversed swapping propensity (2007) Biochemistry, 46 (8), pp. 2227-2232. , DOI 10.1021/bi0613630
Kunitz, M., A spectrophotometric method for the measurement of ribonuclease activity (1946) J. Biol. Chem., 164, pp. 563-568
Ercole, C., Avitabile, F., Del Vecchio, P., Crescenzi, O., Tancredi, T., Picone, D., Role of the hinge peptide and the intersubunit interface in the swapping of N-termini in dimeric bovine seminal RNase (2003) European Journal of Biochemistry, 270 (23), pp. 4729-4735. , DOI 10.1046/j.1432-1033.2003.03872.x
Adinolfi, B.S., Cafaro, V., D'Alessio, G., Di Donato, A., Full antitumor action of recombinant seminal ribonuclease depends on the removal of its N-terminal methionine (1995) Biochem. Biophys. Res. Commun., 213, pp. 525-532
Abe, K., Kimura, H., Amyloid β toxicity consists of a Ca 2+-independent early phase and a Ca 2+-dependent late phase (1996) Journal of Neurochemistry, 67 (5), pp. 2074-2078
Gazit, E., Lee, W.-J., Brey, P.T., Shai, Y., Mode of action of the antibacterial cecropin B2: A spectrofluorometric study (1994) Biochemistry, 33 (35), pp. 10681-10692
Mozsolits, H., Thomas, W.G., Aguilar, M.-I., Surface plasmon resonance spectroscopy in the study of membrane-mediated cell signalling (2003) Journal of Peptide Science, 9 (2), pp. 77-89. , DOI 10.1002/psc.439
Morton, T.A., Myszka, D.G., Chaiken, I.M., Interpreting complex binding kinetics from optical biosensors: A comparison of linear analysis, the integrated rate equation and numerical integration (1995) Anal. Biochem., 227, pp. 176-185
D'Errico, G., D'Ursi, A.M., Marsh, D., Interaction of a peptide derived from glycoprotein gp36 of feline immunodeficiency virus and its lipoylated analogue with phospholipid membranes (2008) Biochemistry, 47 (19), pp. 5317-5327. , DOI 10.1021/bi7025062
Gordon, L.M., Curtain, C.C., Electron spin resonance analysis of model and biological membranes (1988) Advances in Membrane Fluidity: Methods for Studying Membrane Fluidity, 1, pp. 25-89. , R.C. Aloia, C.C. Curtain, L.M. Gordon, Alan R. Liss New York
D'Errico, G., Vitiello, G., Ortona, O., Tedeschi, A., Ramunno, A., D'Ursi, A.M., Interaction between Alzheimer's Abeta(25-35) peptide and phospholipid bilayers: The role of cholesterol (2008) Biochim. Biophys. Acta, 1778, pp. 2710-2716
Lee, J.E., Raines, R.T., Cytotoxicity of bovine seminal ribonuclease: Monomer versus dimer (2005) Biochemistry, 44 (48), pp. 15760-15767. , DOI 10.1021/bi051668z
Kobe, B., Deisenhofer, J., Mechanism of ribonuclease inhibition by ribonuclease inhibitor protein based on the crystal structure of its complex with ribonuclease A (1996) Journal of Molecular Biology, 264 (5), pp. 1028-1043. , DOI 10.1006/jmbi.1996.0694
Papo, N., Shai, Y., Exploring peptide membrane interaction using surface plasmon resonance: Differentiation between pore formation versus membrane disruption by lytic peptides (2003) Biochemistry, 42 (2), pp. 458-466. , DOI 10.1021/bi0267846
Shai, Y., Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides (1999) Biochim. Biophys. Acta, 1462, pp. 55-70
Galdiero, S., Falanga, A., Vitiello, G., Vitiello, M., Pedone, C., D'Errico, G., Galdiero, M., Role of membranotropic sequences from herpes simplex virus type i glycoproteins B and H in the fusion process (2010) Biochim. Biophys. Acta, 1798, pp. 579-591
Marsh, D., Electron spin resonance in membrane research: Protein-lipid interactions (2008) Methods, 46, pp. 83-96
Sankaram, M.B., Brophy, P.J., Marsh, D., Spin-label ESR studies on the interaction of bovine spinal cord myelin basic protein with dimyristoylphosphatidylglycerol dispersions (1989) Biochemistry, 28 (25), pp. 9685-9691. , DOI 10.1021/bi00451a022
Haigis, M.C., Raines, R.T., Secretory ribonucleases are internalized by a dynamin-independent endocytic pathway (2003) Journal of Cell Science, 116 (2), pp. 313-324. , DOI 10.1242/jcs.00214
Kim, W. C., Lee, C. H., The role of mammalian ribonucleases (RNases) in cancer (2009) Biochim. Biophys. Acta, 1796, pp. 99-113
Rybak, S. M., Arndt, M. A., Schirrmann, T., Dubel, S., Krauss, J., Ribonucleases and immunoRNases as anticancer drugs (2009) Curr. Pharm. Des., 15, pp. 2665-2675
Rutkoski, T. J., Raines, R. T., Evasion of ribonuclease inhibitor as a determinant of ribonuclease cytotoxicity (2008) Curr. Pharm. Biotechnol., 9, pp. 185-189
Youle, R. J., D'Alessio, G., (1997) Ribonucleases: Structures and Functions, , Academic Press NewYork
Boix, E., Wu, Y. N., Vasandani, V. M., Saxena, S. K., Ardelt, W., Ladner, J., Youle, R. J., Role of the N terminus in RNase a homologues: Differences in catalytic activity, ribonuclease inhibitor interaction and cytotoxicity (1996) Journal of Molecular Biology, 257 (5), pp. 992-1007. , DOI 10. 1006/jmbi. 1996. 0218
Saxena, S. K., Rybak, S. M., Winkler, G., Meade, H. M., McGray, P., Youle, R. J., Ackerman, E. J., Comparison of RNases and toxins upon injection into Xenopus oocytes (1991) Journal of Biological Chemistry, 266 (31), pp. 21208-21214
Turcotte, R. F., Lavis, L. D., Raines, R. T., Onconase cytotoxicity relies on the distribution of its positive charge (2009) FEBS J., 276, pp. 3846-3857
Mancheno, J. M., Gasset, M., Onaderra, M., Gavilanes, J. G., D'Alessio, G., Bovine seminal ribonuclease destabilizes negatively charged membranes (1994) Biochemical and Biophysical Research Communications, 199 (1), pp. 119-124. , DOI 10. 1006/bbrc. 1994. 1202
Fiser, A., Do, R. K., Sali, A., Modeling of loops in protein structures (2000) Protein Sci., 9, pp. 1753-1773
Delano, W. L., (2002) The PyMOL Molecular Graphics System, , DeLano Scientific Palo Alto, CA, USA
Adinolfi, B. S., Cafaro, V., D'Alessio, G., Di Donato, A., Full antitumor action of recombinant seminal ribonuclease depends on the removal of its N-terminal methionine (1995) Biochem. Biophys. Res. Commun., 213, pp. 525-532
Gazit, E., Lee, W. -J., Brey, P. T., Shai, Y., Mode of action of the antibacterial cecropin B2: A spectrofluorometric study (1994) Biochemistry, 33 (35), pp. 10681-10692
Morton, T. A., Myszka, D. G., Chaiken, I. M., Interpreting complex binding kinetics from optical biosensors: A comparison of linear analysis, the integrated rate equation and numerical integration (1995) Anal. Biochem., 227, pp. 176-185
Gordon, L. M., Curtain, C. C., Electron spin resonance analysis of model and biological membranes (1988) Advances in Membrane Fluidity: Methods for Studying Membrane Fluidity, 1, pp. 25-89. , R. C. Aloia, C. C. Curtain, L. M. Gordon, Alan R. Liss New York
Lee, J. E., Raines, R. T., Cytotoxicity of bovine seminal ribonuclease: Monomer versus dimer (2005) Biochemistry, 44 (48), pp. 15760-15767. , DOI 10. 1021/bi051668z
Sankaram, M. B., Brophy, P. J., Marsh, D., Spin-label ESR studies on the interaction of bovine spinal cord myelin basic protein with dimyristoylphosphatidylglycerol dispersions (1989) Biochemistry, 28 (25), pp. 9685-9691. , DOI 10. 1021/bi00451a022
Haigis, M. C., Raines, R. T., Secretory ribonucleases are internalized by a dynamin-independent endocytic pathway (2003) Journal of Cell Science, 116 (2), pp. 313-324. , DOI 10. 1242/jcs. 00214
Enforcing the positive charge of N-termini enhances membrane interaction and antitumor activity of bovine seminal ribonuclease
Binding to cell membrane, followed by translocation into the cytosol and RNA degradation, is a necessary requirement to convert a ribonuclease into a cytotoxin for malignant tumor cells. In this paper, we investigate the membrane binding attitude of bovine seminal ribonuclease (BS-RNase) and its variant G38K-BS-RNase, bearing an enforced cluster of positive charges at the N-termini surface. By using a combination of biophysical techniques, including CD. SPR and ESR, we find for the two proteins a common, two-step mechanism of interaction with synthetic liposomes, an initial binding to the bilayer surface, driven by electrostatic interactions, followed by a shallow penetration in the lipid core. Protein binding effectively perturbs lipid packing and dynamics. Remarkably, the higher G38K-BS-RNase membrane interacting capability well correlates with its increased cytotoxicity for tumor cells. Overall, these studies shed light on the mechanism of membrane binding and perturbation, proving definitely the importance of electrostatic interactions in the cytotoxic activity of BS-RNase, and provide a rational basis to design proteins with anticancer potential. (C) 2011 Elsevier B.V. All rights reserved.
Enforcing the positive charge of N-termini enhances membrane interaction and antitumor activity of bovine seminal ribonuclease
No results.
Enforcing the positive charge of N-termini enhances membrane interaction and antitumor activity of bovine seminal ribonuclease
Petraglia F, Singh AA, Carafa V, Nebbioso A, Conte M, Scisciola L, Valente S, Baldi A, Mandoli A, Petrizzi VB, Ingenito C, De Falco S, Cicatiello V, Apicella I, Janssen-megens EM, Kim B, Yi G, Logie C, Heath S, Ruvo M, Wierenga ATJ, Flicek P, Yaspo ML, Della Valle V, Bernard O, Tomassi S, Novellino E, Feoli A, Sbardella G, Gut I, Vellenga E, Stunnenberg HG, Mai A, Martens JHA, Altucci L * Combined HAT/EZH2 modulation leads to cancer-selective cell death(284 views) Oncotarget (ISSN: 1949-2553electronic, 1949-2553linking), 2018 May 22; 9(39): 25630-25646. Impact Factor:5.008 ViewExport to BibTeXExport to EndNote