Abstract
Sporidesmin, a mycotoxin fromPithomyces chartarum is a hydrophobic molecule. It can therefore be easily incorporated in the cell membrane, where it is likely to cause changes in the bilayer organization and the properties of membrane proteins. In order to understand the redox behaviour of sporidesmin in a hydrophobic environment, we have investigated the effects of oxidized and reduced sporidesmin on the phase transition properties of bilayers and on the susceptibility of bilayers to pancreatic phospholipase A2 (PLA2). The changes induced by sporidesmin in the thermotropic phase transition profiles of dimyristoyl-sn-3-phosphatidyl choline (DMPC) bilayers were similar to those caused by solutes known to localize in the glycerol-backbone region of the lipid bilayer, suggesting a similar localization for oxidized and reduced sporidesmin. Neither form of toxin disrupt the bilayer or membrane organization even at relatively high mole fractions. At concentrations <10 mole% both forms partitioned equally well in the gel and liquid-crystalline phases, whereas at higher concentrations (≈30 mole%) reduced sporidesmin is preferentially localized in the liquid-crystalline phase. These effects of sporidesmin on the phase properties of DMPC vesicles were also reported by the fluorescence behavior of 10-pyrenedecanoic acid (PDA). The effects of oxidized and reduced sporidesmins on PLA2 kinetics are consistent with their ability to perturb bilayer organisation.
References
Apitz-Castro, R., Jain, M. K. and De Haas, G. H. (1982) Origin of the latency phase during the action of phospholipase A2 on unmodified phosphatidylcholine vesicles.Biochim Biophys Acta 64:349–356.
Bashford, C. L., Alder, G. M., Menestrina, G., Micklem, K. J., Murphy, J. J. and Pasternak, C. A. (1986). Membrane damage by hemolytic viruses, toxins, complement and other cytotoxic agents.J. Biol. Chem 261:9300–9308.
Brasitus, T. A. and Schachter, D. (1980) Lipid dynamics and lipid-protein interactions in rate enterocyte basolteral and microvillus membranes.Biochemistry 19:2763–2769.
Campbell, A. G., Meyer, H. H., Henderson, H. V. and Wesselink, K. (1981) Breeding for facial eczema resistance—a progress report.Proceedings of NZ Society of Animal production 41:273–278.
Hill, M. W. (1974) The effect of anaesthetic-like molecules on the phase transition in smectic mesophases of dipalmitoyllecthin I. The normal alcohol up to C=9 and three inhalation anaesthetics.Biochim. Biophys. Acta 356:117–124.
Impraim, C. C., Foster, K. A., Micklem, K. J., and Pasternak, C. A. (1980) Nature of virally-mediated changes in membrane permeability to small molecules.Biochem. J. 186:847–860.
Jain, M. K. (1983) Non-random lateral organization in bilayers and biomembranes.Membrane Fluidity in Biology 1:1–37.
Jain, M. K. (1988) Order and dynamics in bilayers. In:Introduction to biological Membranes. Wiley-Interscience Publications, New York pp 122–146.
Jain, M. K. and Berg, O. G. (1989) The kinetics of interfacial catalysis by phospholipase A2 and regulation of interfacial activation: hopping versus scooting.Biochim. Biophys. Acta 1002:127–156.
Jain, M. K. and Wu, N. M. (1977) Effect of small molecules on the dipalmitoyl lecithin lipsomal bilayer.: III. Phase transition in lipid bilayer.J. Membrane Biol. 34:157–201.
Jain, M. K., Egmond, M. R., Verheij, H. M., Apitz-Castro, R., Dijkman, R. and De Haas, G. H. (1982) Interaction of phospholipase A2 and phospholipid bilayers.Biochim. Biophys. Acta 688:341–348.
Jain, M. K., Yu, B. Z. and Kozubek, A. (1989) Binding of phospholipase A2 to zwitterionic bilayers is promoted by lateral segregation of anionic amphiphiles.Biochim. Biophys. Acta 980:23–32.
Menestrina, G., Bashford, C. L. and Pasternak, C. A. (1990) Pore-forming toxins: experiments withS. aureus α-toxin,C. perfrigrgens θ toxin, and E. coli hemolysin in lipid bilayers, liposomes, and intact cells.Toxicon 28:477–491
Morris, C. A., Jordan, T. W., Loong, P. C., Lewis, M. H. and Towers, N. R. (1988) Associations between transferrin type and facial eczema susceptibility and some production traits in sheep.NZ Journal of Agricultural Research 31:301–305.
Mortimer, P. H. and Ronaldson, J. W. (1983) Fungal-toxin-induced photosensitization. In:Handbook of Natural Toxins: Plant and Fungal Toxins (Keeler, R. F. and Tu, A. U., eds) Vol 1: Marcel Dekker Inc, NY, 361–419.
Munday, R. (1982) Studies on the mechanism of toxicity of the mycotoxin, sporidesmin I. Generation of superoxide radical by sporidesmin.Chem-Biol Interactions 412:361–374.
Munday, R. (1984) Studies on the mechanism of toxicity of the mycotoxin sporidesmin. 3-Inhibition by metals of the generation of superoxide radical by sporidesmin.Journal of Applied Toxicology 4:182–186.
Munday R. (1987) Studies on the mechanism of toxicity of the mycotoxin, sporidesmin V. Generation of hydroxyl radical by sporidesmin.Journal of Applied Toxicology 7:17–22.
Nieuwenhuizen, W., Kunze, H. and De Haas, G. H. (1974) Phospholipase A2 (Phosphatide Acylhydrolase EC 3.1.1.4) from porcine pancreas.Methods Enzymol. 32B:147–154.
Pasternak, C. A., Alder, G. M., Bashford, C. L., Korchev, Y. E., Pederzolli, C. and Rostovtseva, T. K. (1992) Membrane damage: common mechanisms of induction and prevention. FEMS Microbiol. Immunol.105:83–92.
Pringle, M. J. and Miller, K. W. (1979) Differential effects on phospholipid phase transitions produced by structurally related long chain alcohols.Biochemistry 15:3314–3320.
Ronaldson, J. W. (1982) Purification of sporidesmin by preparative high-pressure liquid chromatogranhy.J. Chem. Tech. Biotechnol. 32:556–558.
Towers, N. R. and Stratton, G. C. (1978) Serum gamma-glutamyltransferase as a measure of sporidesmin-induced liver damage in sheep.NZ Veterinary Journal 26:109–112.
Upreti, G. C. and Jain, M. K. (1978) Effect of the state of phosphatidylcholine on the rate of its hydrolysis by phospholipase A2 (bee venom).Arch. Biochem. Biophys. 188:364–375.
Upreti, G. C. and Jain, M. K. (1980) Action of phospholipase A2 on unmodified phosphatiolycholine bilayers: Organizational defects are preferred sites of action.J. Membrane biol. 55:113–121.
Upreti, G. C., Rainer, S. and Jain, M. K. (1980) Intrinsic differences in the perturbing ability of alkanols in bilayer. Action of phospholipase A2 on the alkanol-modified phospholipid bilayer.J. Membrane Biol. 55:97–112.
Upreti, G. C., Riches, P. C., Morris, C. A. and Gravett, I. M. (1991) Prediction of resistance/susceptibility to facial eczema, A hepatotoxic disease of sheep by studies on erythrocyte membranes. In:Biomembranes in Health and Disease, Proceedings of International Conference on Biomembranes in Health and Disease. (Kidwai, A. M., Upreti, R. K. and Ray, P. K. (eds) Vol 1: Today and Tomorrows Printers and Publishers, New Delhi, India 53–60
Zimmer, G. (1984) Fluidity of cell membranes in the presence of some drugs and inhibitors. In:Biomembranes; Membrane Fluidity. (Kates, M. and Mason, L. A. eds) Vol 12: Plenum Press, NY 169–198.
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Upreti, G.C., Jain, M.K. Interaction of sporidesmin, a mycotoxin fromPithomyces chartarum, with lipid bilayers. Biosci Rep 13, 233–243 (1993). https://doi.org/10.1007/BF01123505
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DOI: https://doi.org/10.1007/BF01123505