Structural features of distinctin affecting peptide biological and biochemical properties(513 views) Dalla Serra M, Cirioni O, Vitale RM, Renzone G, Coraiola M, Giacometti A, Potrich C, Baroni E, Guella G, Sanseverino M, De Luca S, Scalise G, Amodeo P, Scaloni A
Bruno Kessler Foundation, Institute of Biophysics, National Research Council, 38100 Povo (Trento), Italy
Institute of Infectious Diseases and Public Health, Polytechnic Marche University, 60200 Ancona, Italy
Institute of Biomolecular Chemistry, National Research Council, 80078 Pozzuoli (Naples), Italy
Proteomics and Mass Spectrometry Laboratory, ISPAAM, National Research Council, 80147 Naples, Italy
Laboratory of Bioorganic Chemistry, Department of Physics, University of Trento, 38100 Povo (Trento), Italy
Inbios S.r.l., 80078 Pozzuoli (Naples), Italy
Institute of Biostructures and Bioimages, National Research Council, 80138 Naples, Italy
Inbios S. r. l., 80078 Pozzuoli (Naples), Italy
References: Barra, D., Simmaco, M., Amphibian skin: A promising resource for antimicrobial peptides (1995) Trends Biotechnol, 13, pp. 205-20
Zasloff, M., Antimicrobial peptides of multicellular organisms (2002) Nature, 415, pp. 389-395
Yeaman, M.R., Yount, N.Y., Mechanisms of antimicrobial peptide action and resistence (2003) Pharmacol. Rev, 55, pp. 27-55
Oren, Z., Shai, Y., Mode of action of linear amphipathic α-helical antimicrobial peptides (1999) Biopolymers, 47, pp. 451-463
Lequin, O., Ladram, A., Chabbert, L., Bruston, F., Convert, O., Vanhoye, D., Chassaing, G., Amiche, M., Dermaseptin S9, an α-helical antimicrobial peptide with a hydrophobic core and cationic termini (2006) Biochemistry, 45, pp. 468-480
Vignal, E., Chavanieu, A., Roch, P., Chiche, L., Grassy, G., Calas, B., Aumelas, A., Solution structure of the antimicrobial peptide ranalexin and a study of its interaction with perdeuterated dodecylphosphocholine micelles (1998) Eur. J. Biochem, 253, pp. 221-228
Bechinger, B., Zasloff, M., Opella, S.J., Structure and dynamics of the antibiotic peptide PGLa in membranes by solution and solid-state nuclear magnetic resonance spectroscopy (1998) Biophys. J, 74, pp. 981-987
Park, S.H., Kim, Y.K., Park, J.W., Lee, B., Lee, B.J., Solution structure of the antimicrobial peptide gaegurin 4 by 1H and 15N NMR spectroscopy (2000) Eur. J. Biochem, 267, pp. 2695-2704
Batista, C.V., Scaloni, A., Rigden, D.J., Silva, L.R., Rodrigues Romero, A., Dukor, R., Sebben, A., Bloch, C., A novel heterodimeric antimicrobial peptide from the tree-frog Phyllomedusa distincta (2001) FEBS Lett, 494, pp. 85-89
Lee, I.H., Lee, Y.S., Kim, C.H., Kim, C.R., Hong, T., Menzel, L., Boo, L.M., Lehrer, R.I., Dicynthaurin: An antimicrobial peptide from hemocytes of the solitary tunicate Halocynthia aurantium (2001) Biochim. Biophys. Acta, 1527, pp. 141-148
Jang, W.S., Kim, K.N., Lee, Y.S., Nam, M.H., Lee, I.H., Halocidin: A new antimicrobial peptide from hemocytes of the solitary tunicate Halocynthia aurantium (2002) FEBS Lett, 521, pp. 81-86
Yomogida, S., Nagaoka, I., Yamashita, T., Purification of the 11- and 5-kDa antibacterial polypeptides from guinea pig neutrophils (1996) Arch. Biochem. Biophys, 328, pp. 219-226
Scocchi, M., Zelezetsky, I., Benincasa, M., Gennaro, R., Mazzoli, A., Tossi, A., Structural aspects and biological properties of the cathelicidin PMAP-36 (2005) FEBS J, 272, pp. 4398-4406
Jang, W.S., Kim, C.H., Kim, K.N., Park, S.Y., Lee, J.H., Son, S.M., Lee, I.H., Biological activities of synthetic analogs of halocidin, an antimicrobial peptide from the tunicate Halocynthia aurantium (2003) Antimicrob. Agents Chemother, 47, pp. 2481-2486
Okuda, D., Yomogida, S., Tamura, H., Nagaoka, I., Determination of the antibacterial and lipopolysaccharide-neutralizing regions of guinea pig neutrophil cathelicidin peptide CAP11 (2006) Antimicrob. Agents Chemother, 50, pp. 2602-2607
Raimondo, D., Andreotti, G., Saint, N., Amodeo, P., Renzone, G., Sanseverino, M., Zocchi, I., Scaloni, A., A folding-dependent mechanism of antimicrobial peptide resistance to degradation unveiled by solution structure of distinctin (2005) Proc. Natl. Acad. Sci. U.S.A, 102, pp. 6309-6314
Mangoni, M.L., Saugar, J.M., Dellisanti, M., Barra, D., Simmaco, M., Rivas, L., Temporins, small antimicrobial peptides with leishmanicidal activity (2005) J. Biol. Chem, 280, pp. 984-990
Brand, G.D., Leite, J.R., Silva, L.P., Albuquerque, S., Prates, M.V., Azevedo, R.B., Carregaro, V., Bloch, C., Dermaseptins from Phyllomedusa oreades and Phyllomedusa distincta: Anti-Trypanosoma cruzi activity without cytotoxicity to mammalian cells (2002) J. Biol. Chem, 277, pp. 49332-49340
Ohsaki, Y., Gazdar, A.F., Chen, H.C., Johnson, B.E., Antitumor activity of magainin analogues against human lung cancer cell lines (1992) Cancer Res, 52, pp. 3534-3538
Cruciani, R.A., Barker, J.L., Zasloff, M., Chen, H.C., Colamonici, O., Antibiotic magainins exert cytolytic activity against transformed cell lines through channel formation (1991) Proc. Natl. Acad. Sci. U.S.A, 88, pp. 3792-3796
Zairi, A., Serres, C., Tangy, F., Jouannet, P., Hani, K., In vitro spermicidal activity of peptides from amphibian skin: Dermaseptin S4 and derivatives (2008) Bioorg. Med. Chem, 16, pp. 266-275
Shai, Y., Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by α-helical antimicrobial and cell non-selective membrane-lytic peptides (1999) Biochim. Biophys. Acta, 1462, pp. 55-70
Matsuzaki, K., Why and how are peptide-lipid interactions utilized for self-defense? Magainins and tachyplesins as archetypes (1999) Biochim. Biophys. Acta, 1462, pp. 1-10
Yang, L., Weiss, T.M., Lehrer, R.I., Huang, H.W., Crystallization of antimicrobial pores in membranes: Magainin and protegrin (2000) Biophys. J, 79, pp. 2002-2009
(2003) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, Approved Standard M7-A6, , Clinical and Laboratory Standards Institute , Villanova, PA
Scaloni, A., Dalla Serra, M., Amodeo, P., Mannina, L., Vitale, R.M., Segre, A.L., Cruciani, O., Fogliano, V., Structure, conformation and biological activity of a novel lipodepsipeptide from Pseudomonas corrugata: Cormycin A (2004) Biochem. J, 384, pp. 25-36
Coraiola, M., Lo Cantore, P., Lazzaroni, S., Evidente, A., Iacobellis, N.S., Dalla Serra, M., WLIP and tolaasin I, lipodepsipeptides from Pseudomonas reactans and Pseudomonas tolaasii, permeabilise model membranes (2006) Biochim. Biophys. Acta, 1758, pp. 1713-1722
Alvarez, C., Dalla Serra, M., Potrich, C., Bernhart, I., Tejuca, M., Martinez, D., Pazos, I.F., Menestrina, G., Effects of lipid composition on membrane permeabilization by Sticholysin I and II, two cytolysins of the sea anemone Stichodactyia helianthus (2001) Biophys. J, 80, pp. 2761-2774
Menestrina, G., Use of Fourier-transformed infrared spectroscopy (FTIR) for secondary structure determination of staphylococcal pore-forming toxins (2000) Bacterial toxins, methods and protocols, pp. 115-132. , Holst, O, Ed, pp, Humana Press, Totowa, NJ
Goormaghtigh, E., Raussens, V., Ruysschaert, J.M., Attenuated total reflection infrared spectroscopy of proteins and lipids in biological membranes (1999) Biochim. Biophys. Acta, 1422, pp. 105-185
Susi, H., Byler, D.M., Resolution enhanced Fourier transform infrared spectroscopy of enzymes (1986) Methods Enzymol, 130, pp. 290-311
Gordon, L.M., Mobley, P.W., Pilpa, R., Sherman, M.A., Waring, A.J., Conformational mapping of the N-terminal peptide of HIV-1 gp41 in membrane environments using 13C-enhanced Fourier transform IR spectroscopy (2002) Biochim. Biophys. Acta, 1559, pp. 96-120
Fontana, A., Polverino de Laureto, P., De Filippis, V., Scaramella, E., Zambonin, M., (1997) Folding Des, 2, pp. R17-R26
Schwarz, G., Robert, C.H., Pore formation kinetics in membranes, determined from the release of marker molecules out of liposomes or cells (1990) Biophys. J, 58, pp. 577-583
Huang, H.W., Molecular mechanism of antimicrobial peptides: The origin of cooperativity (2006) Biochim. Biophys. Acta, 1758, pp. 1292-1302
Liu, F., Lewis, R.N.A.H., Hodges, R.S., McElhaney, R.N., A differential scanning calorimetric and 31P NMR spectroscopic study of the effect of transmembrane α-helical peptides on the lamellar-reversed hexagonal phase transition of phosphatidylethanolamine model membranes (2001) Biochemistry, 40, pp. 760-768
Hori, Y., Demura, M., Niidome, T., Aoyagi, H., Asakura, T., Orientational behavior of phospholipid membranes with mastoparan studied by 31P solid state NMR (1999) FEBS Lett, 455, pp. 228-232
Dennis, E.A., Plueckthun, A., 31P NMR of phospholipids in micelles (1984) 31P NMR, Principles and Applications, pp. 423-446. , Gorenstein, D. G, Ed, pp, Academic Press, New York
Anderluh, G., Dalla Serra, M., Viero, G., Guella, G., Macek, P., Menestrina, G., Pore formation by equinatoxin II, an eukaryotic protein toxin, occurs by induction of non-lamellar lipid structures (2003) J. Biol. Chem, 278, pp. 45216-45223
Banerjee, U., Zidovetzki, R., Birge, R.R., Chan, S.I., Interaction of alamethicin with lecithin bilayers: A 31P and 2H NMR study (1985) Biochemistry, 24, pp. 7621-7627
Bechinger, B., Skladnev, D.A., Ogrel, A., Li, X., Rogozhkina, E.V., Ovchinnikova, T.V., O'Neil, J.D., Raap, J., 15N and 31P solid-state NMR investigations on the orientation of zervamicin II and alamethicin in phosphatidylcholine membranes (2001) Biochemistry, 40, pp. 9428-9437
Loll, P.J., Miller, R., Weeks, C.M., Axelsen, P.H., A ligand-mediated dimerization mode for vancomycin (1998) Chem. Biol, 5, pp. 293-298
Hornef, M.W., Pütsep, K., Karlsson, J., Refai, E., Andersson, M., Increased diversity of intestinal antimicrobial peptides by covalent dimer formation (2004) Nat. Immunol, 5, pp. 836-843
Oren, Z., Lerman, J.C., Gudmundsson, G.H., Agerberth, B., Shai, Y., Structure and organization of the human antimicrobial peptide LL-37 in phospholipid membranes: Relevance to the molecular basis for its non-cell-selective activity (1999) Biochem. J, 341, pp. 501-513
Schibli, D.J., Hunter, H.N., Aseyev, V., Starner, T.D., Wiencek Jr., J.M., Tack, B.F., Vogel, H.J., The solution structures of the human β-defensins lead to a better understanding of the potent bactericidal activity of HBD3 against Staphylococcus aureus (2002) J. Biol. Chem, 277, pp. 8279-8289
Dempsey, C.E., Ueno, S., Avison, M.B., Enhanced membrane permeabilization and antibacterial activity of a disulfide-dimerized magainin analogue (2003) Biochemistry, 42, pp. 402-409
Tencza, S.B., Creighton, D.J., Yuan, T., Vogel, H.J., Montelaro, R.C., Mietzner, T.A., Lentivirus-derived antimicrobial peptides: Increased potency by sequence engineering and dimerization (1999) J. Antimicrob. Chemother, 44, pp. 33-41
Yang, L., Harroun, T.A., Weiss, T.M., Ding, L., Huang, H.W., Barrel-stave model or toroidal model? A case study on melittin pores (2001) Biophys. J, 81, pp. 1475-1485
Lee, M.T., Chen, F.Y., Huang, H.W., Energetics of pore formation induced by membrane active peptides (2004) Biochemistry, 43, pp. 3590-3599
Glaser, R.W., Sachse, C., Dürr, U.H., Wadhwani, P., Ulrich, A.S., Orientation of the antimicrobial peptide PGLa in lipid membranes determined from 19F-NMR dipolar couplings of 4-CF3-phenylglycine labels (2004) J. Magn. Reson, 168, pp. 153-163
Tremouilhac, P., Strandberg, E., Wadhwani, P., Ulrich, A.S., Conditions affecting the re-alignment of the antimicrobial peptide PGLa in membranes as monitored by solid state 2H-NMR (2006) Biochim. Biophys. Acta, 1758, pp. 1330-1342
Giacometti, A., Cirioni, O., Ghiselli, R., Orlando, F., Silvestri, C., Renzone, G., Testa, I., Scalise, G., Distinctin improves the efficacies of glycopeptides and betalactams against staphylococcal Biofilm in an experimental model of central venous catheter infection (2007) J. Biomed. Mater. Res., Part A, 81, pp. 233-239
Yeaman, M. R., Yount, N. Y., Mechanisms of antimicrobial peptide action and resistence (2003) Pharmacol. Rev, 55, pp. 27-55
Park, S. H., Kim, Y. K., Park, J. W., Lee, B., Lee, B. J., Solution structure of the antimicrobial peptide gaegurin 4 by 1H and 15N NMR spectroscopy (2000) Eur. J. Biochem, 267, pp. 2695-2704
Batista, C. V., Scaloni, A., Rigden, D. J., Silva, L. R., Rodrigues Romero, A., Dukor, R., Sebben, A., Bloch, C., A novel heterodimeric antimicrobial peptide from the tree-frog Phyllomedusa distincta (2001) FEBS Lett, 494, pp. 85-89
Lee, I. H., Lee, Y. S., Kim, C. H., Kim, C. R., Hong, T., Menzel, L., Boo, L. M., Lehrer, R. I., Dicynthaurin: An antimicrobial peptide from hemocytes of the solitary tunicate Halocynthia aurantium (2001) Biochim. Biophys. Acta, 1527, pp. 141-148
Jang, W. S., Kim, K. N., Lee, Y. S., Nam, M. H., Lee, I. H., Halocidin: A new antimicrobial peptide from hemocytes of the solitary tunicate Halocynthia aurantium (2002) FEBS Lett, 521, pp. 81-86
Jang, W. S., Kim, C. H., Kim, K. N., Park, S. Y., Lee, J. H., Son, S. M., Lee, I. H., Biological activities of synthetic analogs of halocidin, an antimicrobial peptide from the tunicate Halocynthia aurantium (2003) Antimicrob. Agents Chemother, 47, pp. 2481-2486
Mangoni, M. L., Saugar, J. M., Dellisanti, M., Barra, D., Simmaco, M., Rivas, L., Temporins, small antimicrobial peptides with leishmanicidal activity (2005) J. Biol. Chem, 280, pp. 984-990
Brand, G. D., Leite, J. R., Silva, L. P., Albuquerque, S., Prates, M. V., Azevedo, R. B., Carregaro, V., Bloch, C., Dermaseptins from Phyllomedusa oreades and Phyllomedusa distincta: Anti-Trypanosoma cruzi activity without cytotoxicity to mammalian cells (2002) J. Biol. Chem, 277, pp. 49332-49340
Cruciani, R. A., Barker, J. L., Zasloff, M., Chen, H. C., Colamonici, O., Antibiotic magainins exert cytolytic activity against transformed cell lines through channel formation (1991) Proc. Natl. Acad. Sci. U. S. A, 88, pp. 3792-3796
(2003) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, Approved Standard M7-A6, , Clinical and Laboratory Standards Institute, Villanova, PA
Gordon, L. M., Mobley, P. W., Pilpa, R., Sherman, M. A., Waring, A. J., Conformational mapping of the N-terminal peptide of HIV-1 gp41 in membrane environments using 13C-enhanced Fourier transform IR spectroscopy (2002) Biochim. Biophys. Acta, 1559, pp. 96-120
Huang, H. W., Molecular mechanism of antimicrobial peptides: The origin of cooperativity (2006) Biochim. Biophys. Acta, 1758, pp. 1292-1302
Liu, F., Lewis, R. N. A. H., Hodges, R. S., McElhaney, R. N., A differential scanning calorimetric and 31P NMR spectroscopic study of the effect of transmembrane -helical peptides on the lamellar-reversed hexagonal phase transition of phosphatidylethanolamine model membranes (2001) Biochemistry, 40, pp. 760-768
Dennis, E. A., Plueckthun, A., 31P NMR of phospholipids in micelles (1984) 31P NMR, Principles and Applications, pp. 423-446. , Gorenstein, D. G, Ed, pp, Academic Press, New York
Loll, P. J., Miller, R., Weeks, C. M., Axelsen, P. H., A ligand-mediated dimerization mode for vancomycin (1998) Chem. Biol, 5, pp. 293-298
Hornef, M. W., P tsep, K., Karlsson, J., Refai, E., Andersson, M., Increased diversity of intestinal antimicrobial peptides by covalent dimer formation (2004) Nat. Immunol, 5, pp. 836-843
Schibli, D. J., Hunter, H. N., Aseyev, V., Starner, T. D., Wiencek Jr., J. M., Tack, B. F., Vogel, H. J., The solution structures of the human -defensins lead to a better understanding of the potent bactericidal activity of HBD3 against Staphylococcus aureus (2002) J. Biol. Chem, 277, pp. 8279-8289
Dempsey, C. E., Ueno, S., Avison, M. B., Enhanced membrane permeabilization and antibacterial activity of a disulfide-dimerized magainin analogue (2003) Biochemistry, 42, pp. 402-409
Tencza, S. B., Creighton, D. J., Yuan, T., Vogel, H. J., Montelaro, R. C., Mietzner, T. A., Lentivirus-derived antimicrobial peptides: Increased potency by sequence engineering and dimerization (1999) J. Antimicrob. Chemother, 44, pp. 33-41
Lee, M. T., Chen, F. Y., Huang, H. W., Energetics of pore formation induced by membrane active peptides (2004) Biochemistry, 43, pp. 3590-3599
Glaser, R. W., Sachse, C., D rr, U. H., Wadhwani, P., Ulrich, A. S., Orientation of the antimicrobial peptide PGLa in lipid membranes determined from 19F-NMR dipolar couplings of 4-CF3-phenylglycine labels (2004) J. Magn. Reson, 168, pp. 153-163
Structural features of distinctin affecting peptide biological and biochemical properties
The antimicrobial peptide distinctin consists of two peptide chains linked by a disulfide bridge; it presents a peculiar fold in water resulting from noncovalent dimerization of two heterodimeric molecules. To investigate the contribution of each peptide chain and the S-S bond to distinctin biochemical properties, different monomeric and homodimeric peptide analogues were synthesized and comparatively evaluated with respect to the native molecule. Our experiments demonstrate that the simultaneous occurrence of both peptide chains and the disulfide bond is essential for the formation of the quaternary structure of distinctin in aqueous media, able to resist protease action. In contrast, distinctin and monomeric and homodimeric analogues exhibited comparable antimicrobial activities, suggesting only a partial contribution of the S-S bond to peptide killing effectiveness. Relative bactericidal properties paralleled liposome permeabilization results, definitively demonstrating that microbial membranes are the main target of distinctin activity. Various biophysical experiments performed in membrane-mimicking media, before and after peptide addition, provided information about peptide secondary structure, lipid bilayer organization, and lipid-peptide orientation with respect to membrane surface. These data were instrumental in the generation of putative models of peptide-lipid supramolecular pore complexes.
Structural features of distinctin affecting peptide biological and biochemical properties