Abstract
The binding of cationic polyamines to negatively charged lipid membranes is driven by electrostatic interactions and additional hydrophobic contributions. We investigated the effect of polyamines with different number of charges and charge separation on the phase transition behavior of vesicles of phosphatidylglycerols (dipalmitoylphosphatidylglycerol and dimyristoylphosphatidylglycerol) to differentiate between effects caused by the number of charges, the charge distance, and the hydrophobicity of the methylene spacer. Using differential scanning calorimetry and Fourier transform infrared spectroscopy complemented with monolayer experiments, we found that the binding constant of polyamines to negatively charged lipid vesicles depends as expected on the number of charges. However, for diamines, the effect of binding on the main phase transition of phosphatidylglycerols (PGs) is also strongly influenced by the charge distance between the ammonium groups in the backbone. Oligoamines with charges separated by two or three methylene groups bind more strongly and have larger stabilizing effects on the lipid gel phase of PGs. With multivalent polyamines, the appearance of several transition peaks points to effects of molecular crowding on the surface, i.e., binding of only two or three charges to the surface in the case of spermine, and possible concomitant domain formation.
Acknowledgments
We thank Bettina Fölting for her help in performing the calorimetric experiments. This work was supported by the Deutsche Forschungsgemeinschaft (GRK 1026 Conformational Transitions in Macromolecular Interactions, Project A1).
References
Arouri, A., Dathe, M., and Blume, A. (2009). Peptide induced demixing in PG/PE lipid mixtures: a mechanism for the specificity of antimicrobial peptides towards bacterial membranes? Biochim. Biophys. Acta 1788, 650–659.10.1016/j.bbamem.2008.11.022Search in Google Scholar
Babin, Y., D’Amour, J., Pigeon, M., and Pézolet, M. (1987). A study of the structure of polymyxin B-dipalmitoylphosphatidylglycerol complexes by vibrational spectroscopy. Biochim. Biophys. Acta 903, 78–88.10.1016/0005-2736(87)90157-XSearch in Google Scholar
Ben-Tal, N., Honig, B., Peitzsch, R., Denisov, G., and McLaughlin, S. (1996). Binding of small basic peptides to membranes containing acidic lipids: theoretical models and experimental results. Biophys. J. 71, 561–575.10.1016/S0006-3495(96)79280-9Search in Google Scholar
Berdysheva-Désert, O., Desbat, B., and Saint-Pierre-Chazalet, M. (2005). Competition of natural polyamines with dimethylsilyl analogues and monovalent cations in presence of a charged dipalmitoylphosphatidylglycerol monolayer. Colloids Surf. B 42, 227–234.10.1016/j.colsurfb.2005.02.008Search in Google Scholar
Bertoluzza, A., Bonora, S., Fini, G., and Morelli, M.A. (1988). Spectroscopic and calorimetric studies of phospholipid polyamine molecular-interactions. J. Raman Spectrosc. 19, 369–373.10.1002/jrs.1250190512Search in Google Scholar
Bloomfield, V. (1996). DNA condensation. Curr. Opin. Struct. Biol. 6, 334–341.10.1016/S0959-440X(96)80052-2Search in Google Scholar
Blume, A. (1979). A comparative study of the phase transitions of phospholipid bilayers and monolayers. Biochim. Biophys. Acta 557, 32–44.10.1016/0005-2736(79)90087-7Search in Google Scholar
Blume, A., Hübner, W., and Messner, G. (1988). Fourier transform infrared spectroscopy of 13C=O-labeled phospholipids hydrogen bonding to carbonyl groups. Biochemistry 27, 8239–8249.10.1021/bi00421a038Search in Google Scholar PubMed
Borkovec, M., Cakara, D., and Koper, G.J.M. (2012). Resolution of microscopic protonation enthalpies of polyprotic molecules by means of cluster expansions. J. Phys. Chem. B 116, 4300–4309.10.1021/jp301164fSearch in Google Scholar PubMed
Chung, L., Kaloyanides, G., McDaniel, R., McLaughlin, A., and McLaughlin, S. (1985). Interaction of gentamicin and spermine with bilayer membranes containing negatively charged phospholipids. Biochemistry 24, 442–452.10.1021/bi00323a030Search in Google Scholar PubMed
Cohen, S.S. (1998). A Guide to the Polyamines (New York: Oxford University Press).Search in Google Scholar
de Kruijff, B., Rietveld, A., Telders, N., and Vaandrager, B. (1985). Molecular aspects of the bilayer stabilization induced by poly(L-lysines) of varying size in cardiolipin liposomes. Biochim. Biophys. Acta 820, 295–304.10.1016/0005-2736(85)90124-5Search in Google Scholar
Eklund, K. and Kinnunen, P. (1986). Effects of polyamines on the thermotropic behaviour of dipalmitoylphosphatidylglycerol. Chem. Phys. Lipids 39, 109.Search in Google Scholar
Fair, W.R. and Wehner, N. (1971). Antibacterial action of spermine: effect on urinary tract pathogens. Appl. Microbiol. 21, 6–8.10.1128/am.21.1.6-8.1971Search in Google Scholar
Garidel, P. and Blume, A. (1999). Interaction of alkaline earth cations with the negatively charged phospholipid 1,2-dimyristoyl-sn-glycero-3-phosphoglycerol: a differential scanning and isothermal titration calorimetric study. Langmuir 15, 5526–5534.10.1021/la990217aSearch in Google Scholar
Garidel, P. and Blume, A. (2005). 1,2-Dimyristoyl-sn-glycero-3-phosphoglycerol (DMPG) monolayers: influence of temperature, pH, ionic strength and binding of alkaline earth cations. Chem. Phys. Lipids 138, 50–59.10.1016/j.chemphyslip.2005.08.001Search in Google Scholar
Hamana, K., Tanaka, T., Hosoya, R., Niitsu, M., and Itoh, T. (2003). Cellular polyamines of the acidophilic, thermophilic and thermoacidophilic archaebacteria, Acidilobus, Ferroplasma, Pyrobaculum, Pyrococcus, Staphylothermus, Thermococcus, Thermodiscus and Vulcanisaeta. J. Gen. Appl. Microbiol. 49, 287–293.10.2323/jgam.49.287Search in Google Scholar
Heimburg, T. (1998). Mechanical aspects of membrane thermodynamics. Estimation of the mechanical properties of lipid membranes close to the chain melting transition from calorimetry. Biochim. Biophys. Acta 1415, 147–162.10.1016/S0005-2736(98)00189-8Search in Google Scholar
Hoernke, M., Schwieger, C., Kerth, A., and Blume, A. (2012). Binding of cationic pentapeptides with modified side chain lengths to negatively charged lipid membranes: complex interplay of electrostatic and hydrophobic interactions. Biochim. Biophys. Acta 1818, 1663–1672.10.1016/j.bbamem.2012.03.001Search in Google Scholar
Khan, M., Mel’Nikov, S., and Jönsson, B. (1999). Anomalous salt effects on DNA conformation: experiment and theory. Macromolecules 32, 8836–8840.10.1021/ma9905627Search in Google Scholar
Kim, J., Mosior, M., Chung, L., Wu, H., and McLaughlin, S. (1991). Binding of peptides with basic residues to membranes containing acidic phospholipids. Biophys. J. 60, 135–148.10.1016/S0006-3495(91)82037-9Search in Google Scholar
Kwon, D.H. and Lu, C.-D. (2006). Polyamines induce resistance to cationic peptide, aminoglycoside, and quinolone antibiotics in Pseudomonas aeruginosa PAO1. Antimicrob. Agents Chemother. 50, 1615–1622.10.1128/AAC.50.5.1615-1622.2006Search in Google Scholar PubMed PubMed Central
Martell, A.E.S. and Motekaitis, R.J. (2004). Critically Selected Stability Constants of Metal Complexes Database, version 8.0. (Gaithersburg, MD: National Institute of Standards and Technology).Search in Google Scholar
Momo, F., Fabris, S., and Stevanato, R. (2000). Interaction of linear mono- and diamines with dimyristoylphosphatidylcholine and dimyristoylphosphatidylglycerol multilamellar liposomes. Arch. Biochem. Biophys. 382, 224–231.10.1006/abbi.2000.2014Search in Google Scholar
Pegg, A.E. and Michael, A.J. (2010). Spermine synthase. Cell Mol. Life Sci. 67, 113–121.10.1007/s00018-009-0165-5Search in Google Scholar
Raspaud, E., Olvera De La Cruz, M., Sikorav, J.-L., and Livolant, F. (1998). Precipitation of DNA by polyamines: a polyelectrolyte behavior. Biophys. J. 74, 381–393.10.1016/S0006-3495(98)77795-1Search in Google Scholar
Rozansky, R., Bachrach, U., and Grossowicz, N. (1954). Studies on the antibacterial action of spermine. J. Gen. Microbiol. 10, 11–16.10.1099/00221287-10-1-11Search in Google Scholar
Schneider, M., Marsh, D., Jahn, W., Kloesgen, B., and Heimburg, T. (1999). Network formation of lipid membranes: triggering structural transitions by chain melting. Proc. Natl. Acad. Sci. USA 96, 14312–14317.10.1073/pnas.96.25.14312Search in Google Scholar
Schuster, I. and Bernhardt, R. (2011). Interactions of natural polyamines with mammalian proteins. BioMol. Concepts 2, 79–94.10.1515/bmc.2011.007Search in Google Scholar
Schwarz, G. and Stankowski, S. (1979). Linear cooperative binding of large ligands involving mutual exclusion of different binding modes. Biophys. Chem. 10, 173–181.10.1016/0301-4622(79)85037-1Search in Google Scholar
Schwieger, C. and Blume, A. (2007). Interaction of poly(l-lysines) with negatively charged membranes: an FT-IR and DSC study. Eur. Biophys. J. 36, 437–450.10.1007/s00249-006-0080-8Search in Google Scholar
Schwieger, C. and Blume, A. (2009). Interaction of poly(L-arginine) with negatively charged DPPG membranes: calorimetric and monolayer studies. Biomacromolecules 10, 2152–2161.10.1021/bm9003207Search in Google Scholar
Stankowski, S. (1983). Large-ligand adsorption to membranes. 1. Linear ligands as a limiting case. Biochim. Biophys. Acta 735, 341–351.10.1016/0005-2736(83)90148-7Search in Google Scholar
Stankowski, S. (1984). Large-ligand adsorption to membranes. 3. Cooperativity and general ligand shapes. Biochim. Biophys. Acta 777, 167–182.10.1016/0005-2736(84)90418-8Search in Google Scholar
Tabor, H. and Tabor, C. (1964). Spermidine, spermine and related amines. Pharmacol. Rev. 16, 245–300.Search in Google Scholar
Träuble, H., Teubner, M., Woolley, P., and Eibl, H. (1976). Electrostatic interactions at charged lipid membranes: I. Effects of pH and univalent cations on membrane structure. Biophys. Chem. 4, 319–342.10.1016/0301-4622(76)80013-0Search in Google Scholar
Wallace, H.M. (2000). The physiological role of the polyamines. Eur. J. Clin. Invest. 30, 1–3.10.1046/j.1365-2362.2000.00585.xSearch in Google Scholar PubMed
Wilson, R. and Bloomfield, V. (1979). Counterion-induced condensation of deoxyribonucleic acid. A light-scattering study. Biochemistry 18, 2192–2196.10.1021/bi00578a009Search in Google Scholar PubMed
Yao, X. and Lu, C.-D. (2012). A PBP 2 mutant devoid of the transpeptidase domain abolishes spermine-β-lactam synergy in Staphylococcus aureus Mu50. Antimicrob. Agents Chemother. 56, 83–91.10.1128/AAC.05415-11Search in Google Scholar PubMed PubMed Central
©2014 by Walter de Gruyter Berlin/Boston
