EPR and FTIR studies reveal the importance of highly ordered sterol-enriched membrane domains for ostreolysin activity

Biochimica et Biophysica Acta - Biomembranes

Volumn 1798, Issue 5, 2010, Pages 891-902

  Rebolj, Katja ^a   Bakrač, Biserka ^a   Garvas, Maja ^b   Ota, Katja ^a   Šentjurc, Marjeta ^b   Potrich, Cristina ^c,d   Coraiola, Manuela ^c,d   Tomazzolli, Rossella ^c,d   Serra, Mauro Dalla ^c,d   Maček, Peter ^a   Sepčić, Kristina ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

^b JO EF STEFAN INSTITUTE   (Slovenia)

^c CNR   (Italy)

^d FONDAZIONE BRUNO KESSLER   (Italy)

Author keywords

Cholesterol; Electron paramagnetic resonance; Fourier transformed infrared spectroscopy; Lipid raft; Liquid ordered phase; Ostreolysin; Steroid

Indexed keywords

CHOLESTEROL; DIPALMITOYLPHOSPHATIDYLCHOLINE; LIPOSOME; OSTREOLYSIN; PHOSPHOLIPID; SPHINGOMYELIN; STEROID; STEROL; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARTICLE; CHANNEL GATING; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; INFRARED SPECTROSCOPY; LIPID MEMBRANE; MEMBRANE BINDING; MEMBRANE FLUIDITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION;

ANIMALS; CELL MEMBRANE; ELECTRON SPIN RESONANCE SPECTROSCOPY; FUNGAL PROTEINS; HEMOLYSIN PROTEINS; LIPOSOMES; MEMBRANE MICRODOMAINS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SPHINGOMYELINS; STEROLS; SWINE;

OSTREA EDULIS; PLEUROTUS OSTREATUS;

EID: 77649274996     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2010.01.016     Document Type: Article

References (36)

1. Berne S., Križaj I., Pohleven F., Turk T., Maček P., and Sepčić K. Pleurotus and Agrocybe hemolysins, new proteins hypothetically involved in fungal fruiting. Biochim. Biophys. Acta 1570 (2002) 153-159
2. Sepčić K., Berne S., Rebolj K., Batista U., Plemenitaš A., Šentjurc M., and Maček P. Ostreolysin, a pore-forming protein from the oyster mushroom, interacts specifically with membrane cholesterol-rich lipid domains. FEBS Lett. 575 (2004) 81-85
3. Rebolj K., Poklar Ulrih N., Maček P., and Sepčić K. Steroid structural requirements for interaction of ostreolysin, a lipid-raft binding cytolysin, with lipid monolayers and bilayers. Biochem. Biophys. Acta 1758 (2006) 1662-1670
4. Sepčić K., Berne S., Potrich C., Turk T., Maček P., and Menestrina G. Interaction of ostreolysin, a cytolytic protein from the edible mushroom Pleurotus ostreatus, with lipid membranes and modulation by lysophospholipids. Eur. J. Biochem. 270 (2003) 1199-1210
5. Chowdhury H.H., Rebolj K., Kreft M., Zorec R., Maček P., and Sepčić K. Lysophospholipids prevent binding of a cytolytic protein ostreolysin to cholesterol-enriched membrane domains. Toxicon 51 (2008) 1345-1356
6. Lingwood D., and Simons K. Lipid rafts as a membrane-organizing principle. Science 327 (2010) 46-50
7. Maličev E., Chowdhury H.H., Maček P., and Sepčić K. Effect of ostreolysin, an Asp-hemolysin isoform, on human chondrocytes and osteoblasts, and possible role of Asp-hemolysin in pathogenesis. Med. Mycol. 45 (2007) 123-130
8. Crowe J.H., Tablin F., Tsvetkova N., Oliver A.E., Walker N., and Crowe L.M. Are lipid phase transitions responsible for chilling damage in human platelets?. Cryobiology 38 (1999) 180-191
9. Štrancar J., Šentjurc M., and Schara M. Fast and accurate characterization of biological membranes by EPR spectral simulations of nitroxides. J. Magn. Reson. 142 (2000) 254-265
10. Štrancar J., Koklič T., and Arsov Z. Soft picture of lateral heterogeneity in biomembranes. J. Membr. Biol. 196 (2003) 135-146
11. Štrancar J., Koklič T., Arsov Z., Filipič B., Stopar D., and Hemminga M.A. Spin label EPR-based characterization of biosystem complexity. J. Chem. Inf. Comput. Sci. 45 (2005) 394-406
12. Vrhovnik K., Kristl J., Šentjurc M., and Šmid-Korbar J. Influence of liposome bilayer fluidity on the transport of encapsulated substance into the skin as evaluated by EPR. Pharm. Res. 15 (1998) 523-529
13. Hung W.C., Lee M.T., Chen F.Y., and Huang H.W. The condensing effect of cholesterol in lipid bilayers. Biophys. J. 92 (2007) 3960-3967
14. Aittoniemi J., Niemelä P.S., Hyvönen M.T., Karttunen M., and Vattulainen I. Insight into the putative specific interactions between cholesterol, sphingomyelin, and palmitoyl-oleoyl phosphatidylcholine. Biophys. J. 92 (2007) 1125-1137
15. de Almeida R.F., Fedorov A., and Prieto M. Sphingomyelin/phosphatidylcholine/ cholesterol phase diagram: boundaries and composition of lipid rafts. Biophys. J. 85 (2003) 2406-2416
16. Arsov Z., and Quaroni L. Detection of lipid phase coexistence and lipid interactions in sphingomyelin/cholesterol membranes by ATR-FTIR spectroscopy. Biochim. Biophys. Acta 1778 (2008) 880-889
17. Xu X., Bittman R., Duportail G., Heissler D., Vilcheze C., and London E. Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide. J. Biol. Chem. 276 (2001) 33540-33546
18. Halling K.K., and Slotte J.P. Membrane properties of plant sterols in phospholipid bilayers as determined by differential scanning calorimetry, resonance energy transfer and detergent-induced solubilization. Biochim. Biophys. Acta 1664 (2004) 161-171
19. Xu X., and London E. Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide. Biochemistry 39 (2000) 844-849
20. Yeagle P.L., Martin R.B., Lala A.K., Lin H.K., and Bloch K. Differential effects of cholesterol and lanosterol on artificial membranes. Proc. Natl. Acad. Sci. U.S.A. 74 (1977) 4924-4926
21. Urbina J.A., Pekerar S., Le H.B., Patterson J., Montez B., and Oldfield E. Molecular order and dynamics of phosphatidylcholine bilayer membranes in the presence of cholesterol, ergosterol and lanosterol: a comparative study using 2H-, 13C- and 31P-NMR spectroscopy. Biochim. Biophys. Acta 1238 (1995) 163-176
22. Ben-Yashar V., and Barenholz Y. The interaction of cholesterol and cholest-4-en-3-one with dipalmitoylphosphatidylcholine. Comparison based on the use of three fluorophores. Biochim. Biophys. Acta 985 (1989) 271-278
23. Slotte J.P. Effect of sterol structure on molecular interactions and lateral domain formation in monolayers containing dipalmitoyl phosphatidylcholine. Biochim. Biophys. Acta 1237 (1995) 127-134
24. Li X.M., Momsen M.M., Brockman H.L., and Brown R.E. Sterol structure and sphingomyelin acyl chain length modulate lateral packing elasticity and detergent solubility in model membranes. Biophys. J. 85 (2003) 3788-3801
25. Marsh D. Electron spin resonance: spin labels. In: Grell E. (Ed). Membrane Spectroscopy (1981), Springer Verlag, Berlin 52-141
26. Berne S., Sepčić K., Anderluh G., Turk T., Maček P., and Poklar Ulrih N. Effect of pH on the pore forming activity and conformational stability of ostreolysin, a lipid raft-binding protein from the edible mushroom Pleurotus ostreatus. Biochemistry 44 (2005) 11137-11147
27. Palmer M. Cholesterol and the activity of bacterial toxins. FEMS Microbiol. Lett. 238 (2004) 281-289
28. Nelson L.D., Johnson A.E., and London E. How interaction of perfringolysin O with membranes is controlled by sterol structure, lipid structure, and physiological low pH: insights into the origin of perfringolysin O-lipid raft interaction. J. Biol. Chem. 283 (2008) 4632-4642
29. Pike L.J. Lipid rafts: heterogeneity on the high seas. Biochem. J. 378 (2004) 281-292
30. de Almeida R.F., Loura L.M., Fedorov A., and Prieto M. Lipid rafts have different sizes depending on membrane composition: a time-resolved fluorescence resonance energy transfer study. J. Mol. Biol. 346 (2005) 1109-1120
31. Hancock J.F. Lipid rafts: contentious only from simplistic standpoints. Nat. Rev. Mol. Cell. Biol. 7 (2006) 456-462
32. Roper K., Corbeil D., and Huttner W.B. Retention of prominin in microvilli reveals distinct cholesterol-based lipid micro-domains in the apical plasma membrane. Nat. Cell Biol. 2 (2000) 582-592
33. Mishra S., and Joshi P.G. Lipid raft heterogeneity: an enigma. J. Neurochem. 103 (2007) 135-142
34. Chen Y., Qin J., Cai J., and Chen Z.W. Cold induces micro- and nano-scale reorganization of lipid raft markers at mounds of T-cell membrane fluctuations. PLoS ONE 4 (2009) 1-12
35. Zidar J., Merzel F., Hodošček M., Rebolj K., Sepčić K., Maček P., and Janežič D. Liquid-ordered phase formation in cholesterol/sphingomyelin bilayers: all-atom molecular dynamics simulations. J. Phys. Chem. B 113 (2009) 15795-15802
36. Flanagan J.J., Tweten R.K., Johnson A.E., and Heuck A.P. Cholesterol exposure at the membrane surface is necessary and sufficient to trigger perfringolysin O binding. Biochemistry 28 (2009) 3977-3987