Ordered-disordered domain coexistence in ternary lipid monolayers activates sphingomyelinase by clearing ceramide from the active phase

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 11, 2012, Pages 2767-2776

  Ale, Elisa Carmen ^a   Maggio, Bruno ^a   Fanani, Maria Laura ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

Brewster angle microscopy; Lipid domain border; Liquid expanded phase; Liquid ordered domain; Sphingomyelin; Tie line

Indexed keywords

CERAMIDE; CHOLESTANOL; PHOSPHATIDYLCHOLINE; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE;

ADSORPTION KINETICS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME SUBSTRATE; HYDROLYSIS; LIPID COMPOSITION; LIPID MONOLAYER; MEMBRANE FORMATION; MEMBRANE STRUCTURE; PRIORITY JOURNAL; SURFACE PROPERTY;

CERAMIDES; ENZYME ACTIVATION; FLUORESCENT DYES; LIPIDS; SPHINGOMYELIN PHOSPHODIESTERASE;

EID: 84865271182     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.06.017     Document Type: Article

References (50)

1. H. Grassme, J. Riethmuller, and E. Gulbins Biological aspects of ceramide-enriched membrane domains Prog. Lipid Res. 46 2007 161 170 (Pubitemid 46962121)
2. C.R. Bollinger, V. Teichgraber, and E. Gulbins Ceramide-enriched membrane domains Biochim. Biophys. Acta 1746 2005 284 294 (Pubitemid 41815022)
3. Y. Zhang, X. Li, K.A. Becker, and E. Gulbins Ceramide-enriched membrane domains-structure and function Biochim. Biophys. Acta 1788 2009 178 183
4. F.X. Contreras, J. Sot, M.B. Ruiz-Arguello, A. Alonso, and F.M. Goni Cholesterol modulation of sphingomyelinase activity at physiological temperatures Chem. Phys. Lipids 130 2004 127 134 (Pubitemid 38681197)
5. L.C. Silva, A.H. Futerman, and M. Prieto Lipid raft composition modulates sphingomyelinase activity and ceramide-induced membrane physical alterations Biophys. J. 96 2009 3210 3222
6. L. De Tullio, B. Maggio, and M.L. Fanani Sphingomyelinase acts by an area-activated mechanism on the liquid-expanded phase of sphingomyelin monolayers J. Lipid Res. 49 2008 2347 2355
7. R.F. de Almeida, A. Fedorov, and M. Prieto Sphingomyelin/ phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts Biophys. J. 85 2003 2406 2416 (Pubitemid 37210789)
8. M.L. Fanani, and B. Maggio Liquid-liquid domain miscibility driven by composition and domain thickness mismatch in ternary lipid monolayers J. Phys. Chem. B 115 2011 41 49
9. L. Chao, A.P. Gast, T.A. Hatton, and K.F. Jensen Sphingomyelinase-induced phase transformations: causing morphology switches and multiple-time-domain ceramide generation in model raft membranes Langmuir 26 2010 344 356
10. Ira, S. Zou, D.M. Ramirez, S. Vanderlip, W. Ogilvie, Z.J. Jakubek, and L.J. Johnston Enzymatic generation of ceramide induces membrane restructuring: correlated AFM and fluorescence imaging of supported bilayers J. Struct. Biol. 168 2009 78 89
11. Ira, and L.J. Johnston Sphingomyelinase generation of ceramide promotes clustering of nanoscale domains in supported bilayer membranes Biochim. Biophys. Acta 1778 2008 185 197
12. S. Chiantia, N. Kahya, J. Ries, and P. Schwille Effects of ceramide on liquid-ordered domains investigated by simultaneous AFM and FCS Biophys. J. 90 2006 4500 4508 (Pubitemid 43830895)
13. B.M. Castro, L.C. Silva, A. Fedorov, R.F. de Almeida, and M. Prieto Cholesterol-rich fluid membranes solubilize ceramide domains: implications for the structure and dynamics of mammalian intracellular and plasma membranes J. Biol. Chem. 284 2009 22978 22987
14. D.J. Benvegnu, and H.M. McConnell Surface dipole densities in lipid monolayers J. Phys. Chem. 97 1993 6686 6691
15. H.M. McConnell, and A. Radhakrishnan Condensed complexes of cholesterol and phospholipids Biochim. Biophys. Acta 1610 2003 159 173 (Pubitemid 36324461)
16. E. Lancelot, and C. Grauby-Heywang Comparison of the interaction of dihydrocholesterol and cholesterol with sphingolipid or phospholipid Langmuir monolayers Colloids Surf. B Biointerfaces 59 2007 81 86 (Pubitemid 47016927)
17. I.D. Bianco, and B. Maggio Interactions of neutral and anionic glycosphingolipids with dilauroylphosphatidylcholine and dilauroylphosphatidic acid in mixed monolayers Colloids Surf. 40 1989 249 260 (Pubitemid 20610732)
18. M.L. Fanani, and B. Maggio Mutual modulation of sphingomyelinase and phospholipase A2 activities against mixed lipid monolayers by their lipid intermediates and glycosphingolipids Mol. Membr. Biol. 14 1997 25 29 (Pubitemid 27219904)
19. C. Lheveder, J. Meunier, and S. Henon Brewster angle microscopy A. Baszkin, W. Norde, Physical Chemistry of Biological Interfaces 2000 Marcel Dekker, Inc. NY
20. S. Hartel, M.L. Fanani, and B. Maggio Shape transitions and lattice structuring of ceramide-enriched domains generated by sphingomyelinase in lipid monolayers Biophys. J. 88 2005 287 304 (Pubitemid 40070677)
21. M.L. Fanani, S. Hartel, B. Maggio, T.L. De, J. Jara, F. Olmos, and R.G. Oliveira The action of sphingomyelinase in lipid monolayers as revealed by microscopic image analysis Biochim. Biophys. Acta 1798 2010 1309 1323
22. M.L. Fanani, and B. Maggio Kinetic steps for the hydrolysis of sphingomyelin by Bacillus cereus sphingomyelinase in lipid monolayers J. Lipid Res. 41 2000 1832 1840
23. J.V. Busto, M.L. Fanani, T.L. De, J. Sot, B. Maggio, F.M. Goni, and A. Alonso Coexistence of immiscible mixtures of palmitoylsphingomyelin and palmitoylceramide in monolayers and bilayers Biophys. J. 97 2009 2717 2726
24. M.B. Ruiz-Arguello, M.P. Veiga, J.L. Arrondo, F.M. Goni, and A. Alonso Sphingomyelinase cleavage of sphingomyelin in pure and mixed lipid membranes. Influence of the physical state of the sphingolipid Chem. Phys. Lipids 114 2002 11 20 (Pubitemid 34158763)
25. G. Roberts Langmuir-Blodgett Films 1990 Plenum Press NY
26. M.L. Fanani, S. Hartel, R.G. Oliveira, and B. Maggio Bidirectional control of sphingomyelinase activity and surface topography in lipid monolayers Biophys. J. 83 2002 3416 3424 (Pubitemid 36041958)
27. A. Cruz, L. Vazquez, M. Velez, and J. Perez-Gil Influence of a fluorescent probe on the nanostructure of phospholipid membranes: dipalmitoylphosphatidylcholine interfacial monolayers Langmuir 21 2005 5349 5355 (Pubitemid 40850618)
28. J.M. Holopainen, M. Subramanian, and P.K. Kinnunen Sphingomyelinase induces lipid microdomain formation in a fluid phosphatidylcholine/sphingomyelin membrane Biochemistry 37 1998 17562 17570 (Pubitemid 29013758)
29. M.L. Fanani, T.L. De, S. Hartel, J. Jara, and B. Maggio Sphingomyelinase-induced domain shape relaxation driven by out-of-equilibrium changes of composition Biophys. J. 96 2009 67 76
30. Ira, and L.J. Johnston Ceramide promotes restructuring of model raft membranes Langmuir 22 2006 11284 11289 (Pubitemid 46129674)
31. D.F. Evans, and H. Wennerstrom The Colloidal Domain 1999 Wiley-VCH New York
32. G. Staneva, A. Momchilova, C. Wolf, P.J. Quinn, and K. Koumanov Membrane microdomains: role of ceramides in the maintenance of their structure and functions Biochim. Biophys. Acta 1788 2009 666 675
33. F.M. Goni, and A. Alonso Effects of ceramide and other simple sphingolipids on membrane lateral structure Biochim. Biophys. Acta 1788 2009 169 177
34. B. Boulgaropoulos, H. Amenitsch, P. Laggner, and G. Pabst Implication of sphingomyelin/ceramide molar ratio on the biological activity of sphingomyelinase Biophys. J. 99 2010 499 506
35. J. Sot, M. Ibarguren, J.V. Busto, L.R. Montes, F.M. Goni, and A. Alonso Cholesterol displacement by ceramide in sphingomyelin-containing liquid-ordered domains, and generation of gel regions in giant lipidic vesicles FEBS Lett. 582 2008 3230 3236
36. G. Staneva, C. Chachaty, C. Wolf, K. Koumanov, and P.J. Quinn The role of sphingomyelin in regulating phase coexistence in complex lipid model membranes: competition between ceramide and cholesterol Biochim. Biophys. Acta 1778 2008 2727 2739
37. T.K. Nyholm, P.M. Grandell, B. Westerlund, and J.P. Slotte Sterol affinity for bilayer membranes is affected by their ceramide content and the ceramide chain length Biochim. Biophys. Acta 1798 2010 1008 1013
38. B. Boulgaropoulos, Z. Arsov, P. Laggner, and G. Pabst Stable and unstable lipid domains in ceramide-containing membranes Biophys. J. 100 2011 2160 2168
39. J.V. Busto, J. Sot, J. Requejo-Isidro, F.M. Goni, and A. Alonso Cholesterol displaces palmitoylceramide from its tight packing with palmitoylsphingomyelin in the absence of a liquid-disordered phase Biophys. J. 99 2010 1119 1128
40. Megha, and E. London Ceramide selectively displaces cholesterol from ordered lipid domains (rafts): implications for lipid raft structure and function J. Biol. Chem. 279 2004 9997 10004 (Pubitemid 38372602)
41. S. Nybond, Y.J. Bjorkqvist, B. Ramstedt, and J.P. Slotte Acyl chain length affects ceramide action on sterol/sphingomyelin-rich domains Biochim. Biophys. Acta 1718 2005 61 66 (Pubitemid 41698896)
42. E. London How principles of domain formation in model membranes may explain ambiguities concerning lipid raft formation in cells Biochim. Biophys. Acta 1746 2005 203 220 (Pubitemid 41815017)
43. S.L. Souza, M.J. Capitan, J. Alvarez, S.S. Funari, M.H. Lameiro, and E. Melo Phase behavior of aqueous dispersions of mixtures of N-palmitoyl ceramide and cholesterol: a lipid system with ceramide-cholesterol crystalline lamellar phases J. Phys. Chem. B 113 2009 1367 1375
44. L. Chao, F. Chen, K.F. Jensen, and T.A. Hatton Two-dimensional solvent-mediated phase transformation in lipid membranes induced by sphingomyelinase Langmuir 27 2011 10050 10060
45. F. Lang, E. Gulbins, I. Szabo, A. Lepple-Wienhues, S.M. Huber, C. Duranton, P.A. Lang, and T. Wieder Cell volume and the regulation of apoptotic cell death J. Mol. Recognit. 17 2004 473 480 (Pubitemid 39218991)
46. L. De Tullio, B. Maggio, S. Hartel, J. Jara, and M.L. Fanani The initial surface composition and topography modulate sphingomyelinase-driven sphingomyelin to ceramide conversion in lipid monolayers Cell Biochem. Biophys. 47 2007 169 177 (Pubitemid 47338359)
47. L.C. Silva, R.F. de Almeida, B.M. Castro, A. Fedorov, and M. Prieto Ceramide-domain formation and collapse in lipid rafts: membrane reorganization by an apoptotic lipid Biophys. J. 92 2007 502 516 (Pubitemid 46145783)
48. Megha, P. Sawatzki, T. Kolter, R. Bittman, and E. London Effect of ceramide N-acyl chain and polar headgroup structure on the properties of ordered lipid domains (lipid rafts) Biochim. Biophys. Acta 1768 2007 2205 2212 (Pubitemid 47379609)
49. M.R. Ali, K.H. Chen, and J. Huang Ceramide drives cholesterol out of the ordered lipid bilayer phase into the crystal phase in 1-palmitoyl-2-oleoyl-sn- glycero-3-phosphocholine/cholesterol/ceramide ternary mixtures Biochemistry 45 2006 12629 12638 (Pubitemid 44583704)
50. J.P. Slotte, G. Hedstrom, S. Rannstrom, and S. Ekman Effects of sphingomyelin degradation on cell cholesterol oxidizability and steady-state distribution between the cell surface and the cell interior Biochim. Biophys. Acta 985 1989 90 96 (Pubitemid 19240340)