Ceramide: From lateral segregation to mechanical stress

Biochimica et Biophysica Acta - Biomembranes

Volumn 1798, Issue 7, 2010, Pages 1348-1356

  López Montero, Iván ^a   Monroy, Francisco ^a   Vélez, Marisela ^b,c   Devaux, Philippe F ^d  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b INSTITUTO DE CATÁLISIS Y PETROLEOQUÍMICA   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^d INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

Author keywords

Ceramide; Lipid domains; Mechanical stress; Sphingomyelinase

Indexed keywords

CERAMIDE; SPHINGOLIPID; SPHINGOMYELIN; SPHINGOMYELIN PHOSPHODIESTERASE;

ARTIFICIAL MEMBRANE; EFFUSION; ENZYME ACTIVITY; ENZYME DEGRADATION; EUKARYOTIC CELL; IMAGE ANALYSIS; LIPID ANALYSIS; LIPID MEMBRANE; MECHANICAL STRESS; MEMBRANE LEAFLET; MOLECULAR MECHANICS; NONHUMAN; PHASE SEPARATION; PHASE TRANSITION; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN TARGETING; REVIEW; SHEAR STRESS; SURFACE TENSION; VISCOELASTICITY;

ANIMALS; CELL MEMBRANE; CERAMIDES; EUKARYOTIC CELLS; MODELS, BIOLOGICAL; SPHINGOMYELINS; SURFACE TENSION; VISCOSITY;

EUKARYOTA;

EID: 77954809178     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamem.2009.12.007     Document Type: Review

References (87)

1. Pascher I. Molecular arrangements in sphingolipids. Conformation and hydrogen bonding of ceramide and their implication on membrane stability and permeability. Biochim. Biophys. Acta (BBA) - Biomembr. 1976, 455:433-451.
2. Löfgren H., Pascher I. Molecular arrangements of sphingolipids. The monolayer behaviour of ceramides. Chem. Phys. Lipids 1977, 20:273-284.
3. Shah J., Atienza J.M., Rawlings A.V., Shipley G.G. Physical properties of ceramides: effect of fatty acid hydroxylation. J. Lipid Res. 1995, 36:1945-1955.
4. Singer S.J., Nicolson G.L. The fluid mosaic model of the structure of cell membranes. Science 1972, 175:720-731.
5. Simons K., Ikonen E. Functional rafts in cell membranes. Nature 1997, 387:569-572.
6. Engelman D.M. Membranes are more mosaic than fluid. Nature 2005, 438:578-580.
7. Pike L.J. Rafts defined: a report on the Keystone symposium on lipid rafts and cell function. J. Lipid Res. 2006, 47:1597-1598.
8. Munro S. Lipid rafts: elusive or illusive?. Cell 2003, 115:377-388.
9. Parrott D.T., Turner J.E. Mesophase formation by ceramides and cholesterol: a model for stratum corneum lipid packing?. Biochim. Biophys. Acta (BBA) - Biomembr. 1993, 1147:273-276.
10. Kolesnick R., Hannun Y.A. Ceramide and apoptosis. Trends Biochem. Sci. 1999, 24:224-225.
11. Hannun Y.A., Luberto C. Ceramide in the eukaryotic stress response. Trends Cell Biol. 2000, 10:73-80.
12. Futerman A.H., Hannun Y.A. The complex life of simple sphingolipids. EMBO Rep. 2004, 5:777-782.
13. Huang H.-W., Goldberg E.M., Zidovetzki R. Ceramide induces structural defects into phosphatidylcholine bilayers and activates phospholipase A2. Biochem. Biophys. Res. Commun. 1996, 220:834-838.
14. Holopainen J.M., Lehtonen J.Y.A., Kinnunen P.K.J. Lipid microdomains in dimyristoylphosphatidylcholine-ceramide liposomes. Chem. Phys. Lipids 1997, 88:1-13.
15. Venkataraman K., Futerman A.H. Ceramide as a second messenger: sticky solutions to sticky problems. Trends Cell Biol. 2000, 10:408-412.
16. van Blitterswijk W.J., van der Luit A.H., Veldman R.J., Verheij M., Borst J. Ceramide: second messenger or modulator of membrane structure and dynamics?. Biochem. J. 2003, 369:199-211.
17. Goñi F.M., Alonso A. Biophysics of sphingolipids I. Membrane properties of sphingosine, ceramides and other simple sphingolipids. Biochim. Biophys. Acta (BBA) - Biomembr. 2006, 1758:1902-1921.
18. Grassmé H., Riethmüller J., Gulbins E. Biological aspects of ceramide-enriched membrane domains. Prog. Lipid Res. 2007, 46:161-170.
19. Zhang Y., Li X., Becker K.A., Gulbins E. Ceramide-enriched membrane domains-structure and function. Biochim. Biophys. Acta (BBA) - Biomembr. 2009, 1788:178-183.
20. Goñi F.M., Alonso A. Effects of ceramide and other simple sphingolipids on membrane lateral structure. Biochim. Biophys. Acta (BBA) - Biomembr. 2009, 1788:169-177.
21. Holopainen J.M., Brockman H.L., Brown R.E., Kinnunen P.K.J. Interfacial interactions of ceramide with dimyristoylphosphatidylcholine: impact of the N-acyl chain. Biophys. J. 2001, 80:765-775.
22. Silva L.C., de Almeida R.F.M., Fedorov A., Matos A.P., Prieto M. Ceramide-platform formation and -induced biophysical changes in a fluid phospholipid membrane. Mol. Membr. Biol. 2006, 23:137-148.
23. Karttunen M., Haataja M.P., Saily M., Vattulainen I., Holopainen J.M. Lipid domain morphologies in phosphatidylcholine-ceramide monolayers. Langmuir 2009, 25:4595-4600.
24. Fidorra M., Duelund L., Leidy C., Simonsen A.C., Bagatolli L.A. Absence of fluid-ordered/fluid-disordered phase coexistence in ceramide/POPC mixtures containing cholesterol. Biophys. J. 2006, 90:4437-4451.
25. Staneva G., Momchilova A., Wolf C., Quinn P.J., Koumanov K. Membrane microdomains: role of ceramides in the maintenance of their structure and functions. Biochim. Biophys. Acta (BBA) - Biomembr. 2009, 1788:666-675.
26. ten Grotenhuis E., Demel R.A., Ponec M., Boer D.R., van Miltenburg J.C., Bouwstra J.A. Phase behavior of stratum corneum lipids in mixed Langmuir-Blodgett monolayers. Biophys. J. 1996, 71:1389-1399.
27. Ekelund K., Eriksson L., Sparr E. Rectangular solid domains in ceramide-cholesterol monolayers - 2D crystals. Biochim. Biophys. Acta (BBA) - Biomembr. 2000, 1464:1-6.
28. Sparr E., Eriksson L., Bouwstra J.A., Ekelund K. AFM study of lipid monolayers: III. Phase behavior of ceramides, cholesterol and fatty acids. Langmuir 2000, 17:164-172.
29. Sot J., Bagatolli L.A., Goñi F.M., Alonso A. Detergent-resistant, ceramide-enriched domains in sphingomyelin/ceramide bilayers. Biophys. J. 2006, 90:903-914.
30. Castro B.M., Silva L.C., Fedorov A., de Almeida R.F.M., Prieto M. Cholesterol-rich fluid membranes solubilize ceramide domains: implications for the structure and dynamics of mammalian intracellular and plasma membranes. J. Biol. Chem. 2009, 284:22978-22987.
31. Chiantia S., Kahya N., Ries J., Schwille P. Effects of ceramide on liquid-ordered domains investigated by simultaneous AFM and FCS. Biophys. J. 2006, 90:4500-4508.
32. Megha E.London Ceramide selectively displaces cholesterol from ordered lipid domains (rafts): implications for lipid raft structure and function. J. Biol. Chem. 2004, 279:9997-10004.
33. Chiantia S., Kahya N., Schwille P. Raft domain reorganization driven by short- and long-chain ceramide: a combined AFM and FCS study. Langmuir 2007, 23:7659-7665.
34. Popov J., Vobornik D., Coban O., Keating E., Miller D., Francis J., Petersen N.O., Johnston L.J. Chemical mapping of ceramide distribution in sphingomyelin-rich domains in monolayers. Langmuir 2008, 24:13502-13508.
35. Chiantia S., Ries J., Chwastek G., Carrer D., Li Z., Bittman R., Schwille P. Role of ceramide in membrane protein organization investigated by combined AFM and FCS. Biochim. Biophys. Acta (BBA) - Biomembr. 2008, 1778:1356-1364.
36. Bacia K., Schwille P., Kurzchalia T. Sterol structure determines the separation of phases and the curvature of the liquid-ordered phase in model membranes. Proc. Natl Acad. Sci. USA 2005, 102:3272-3277.
37. Lopez-Montero I., Rodriguez N., Cribier S., Pohl A., Velez M., Devaux P.F. Rapid transbilayer movement of ceramides in phospholipid vesicles and in human erythrocytes. J. Biol. Chem. 2005, 280:25811-25819.
38. Pohl A., López-Montero I.n., Rouvière F., Giusti F., Devaux P.F. Rapid transmembrane diffusion of ceramide and dihydroceramide spin-labelled analogues in the liquid ordered phase. Mol. Membr. Biol. 2009, 26:194-204.
39. Sullan R.M.A., Li J.K., Zou S. Direct correlation of structures and nanomechanical properties of multicomponent lipid bilayers. Langmuir 2009, 25:7471-7477.
40. Fanani M.L., Härtel S., Oliveira R.G., Maggio B. Bidirectional control of sphingomyelinase activity and surface topography in lipid monolayers. Biophys. J. 2002, 83:3416-3424.
41. Härtel S., Laura Fanani M., Maggio B. Shape transitions and lattice structuring of ceramide-enriched domains generated by sphingomyelinase in lipid monolayers. Biophys. J. 2005, 88:287-304.
42. Holopainen J.M., Angelova M.I., Kinnunen P.K.J. Vectorial budding of vesicles by asymmetrical enzymatic formation of ceramide in giant liposomes. Biophys. J. 2000, 78:830-838.
43. Taniguchi Y., Ohba T., Miyata H., Ohki K. Rapid phase change of lipid microdomains in giant vesicles induced by conversion of sphingomyelin to ceramide. Biochim. Biophys. Acta (BBA) - Biomembr. 2006, 1758:145-153.
44. López-Montero I., Vélez M., Devaux P.F. Surface tension induced by sphingomyelin to ceramide conversion in lipid membranes. Biochim. Biophys. Acta (BBA) - Biomembr. 2007, 1768:553-561.
45. Ira L.J. Johnston, ceramide promotes restructuring of model raft membranes. Langmuir 2006, 22:11284-11289.
46. De Tullio L., Maggio B., Fanani M.L. Sphingomyelinase acts by an area-activated mechanism on the liquid-expanded phase of sphingomyelin monolayers. J. Lipid Res. 2008, 49:2347-2355.
47. Fanani M.L., De Tullio L., Hartel S., Jara J., Maggio B. Sphingomyelinase-induced domain shape relaxation driven by out-of-equilibrium changes of composition. Biophys. J. 2009, 96:67-76.
48. Jungner M., Ohvo H., Slotte J.P. Interfacial regulation of bacterial sphingomyelinase activity. Biochim. Biophys. Acta (BBA) - Lipids Lipid Metab. 1997, 1344:230-240.
49. Contreras F.X., Sot J., Ruiz-Argüello M.B., Alonso A., Goñi F.M. Cholesterol modulation of sphingomyelinase activity at physiological temperatures. Chem. Phys. Lipids 2004, 130:127-134.
50. Silva L.C., Futerman A.H., Prieto M. Lipid raft composition modulates sphingomyelinase activity and ceramide-induced membrane physical alterations. Biophys. J. 2009, 96:3210-3222.
51. Veatch S.L., Keller S.L. Miscibility phase diagrams of giant vesicles containing sphingomyelin. Phys. Rev. Lett. 2005, 94:148101.
52. de Almeida R.F.M., Fedorov A., Prieto M. Sphingomyelin/phosphatidylcholine/cholesterol phase diagram: boundaries and composition of lipid rafts. Biophys. J. 2003, 85:2406-2416.
53. Ira L.J.Johnston Sphingomyelinase generation of ceramide promotes clustering of nanoscale domains in supported bilayer membranes. Biochim. Biophys. Acta (BBA) - Biomembr. 2008, 1778:185-197.
54. Silva L.C., de Almeida R.F.M., Castro B.M., Fedorov A., Prieto M. Ceramide-domain formation and collapse in lipid rafts: membrane reorganization by an apoptotic lipid. Biophys. J. 2007, 92:502-516.
55. Basáñez G., Ruiz-Argüello M.B., Alonso A., Goñi F.M., Karlsson G., Edwards K. Morphological changes induced by phospholipase C and by sphingomyelinase on large unilamellar vesicles: a cryo-transmission electron microscopy study of liposome fusion. Biophys. J. 1997, 72:2630-2637.
56. Ruiz-Arguello M.B., Basanez G., Goni F., Alonso A. Different effects of enzyme-generated ceramides and diacylglycerols in phospholipid membrane fusion and leakage. J. Biol. Chem. 1996, 271:26616-26621.
57. Montes L.R., Ruiz-Arguello M.B., Goni F.M., Alonso A. Membrane restructuring via ceramide results in enhanced solute efflux. J. Biol. Chem. 2002, 277:11788-11794.
58. Sot J., Goñi F.M., Alonso A. Molecular associations and surface-active properties of short- and long-N-acyl chain ceramides. Biochim. Biophys. Acta (BBA) - Biomembr. 2005, 1711:12-19.
59. Simon C.G., Holloway P.W., Gear A.R.L. Exchange of C16-ceramide between phospholipid vesicles. Biochemistry 1999, 38:14676-14682.
60. Carrer D.C., Maggio B. Phase behavior and molecular interactions in mixtures of ceramide with dipalmitoylphosphatidylcholine. J. Lipid Res. 1999, 40:1978-1989.
61. Carrer D.C., Maggio B. Transduction to self-assembly of molecular geometry and local interactions in mixtures of ceramides and ganglioside GM1. Biochim. Biophys. Acta (BBA) - Biomembr. 2001, 1514:87-99.
62. Maggio B. Favorable and unfavorable lateral interactions of ceramide, neutral glycosphingolipids and gangliosides in mixed monolayers. Chem. Phys. Lipids 2004, 132:209-224.
63. Li X.-M., Momsen M.M., Smaby J.M., Brockman H.L., Brown R.E. Cholesterol decreases the interfacial elasticity and detergent solubility of sphingomyelins. Biochemistry 2001, 40:5954-5963.
64. Lopez-Montero I., Arriaga L.R., Monroy F., Rivas G., Tarazona P., Velez M. High fluidity and soft elasticity of the inner membrane of Escherichia coli revealed by the surface rheology of model Langmuir monolayers. Langmuir 2008, 24:4065-4076.
65. Unpublished results. PhD thesis of G. Espinosa, Paris 2009.
66. Wilke N., Maggio B. The influence of domain crowding on the lateral diffusion of ceramide-enriched domains in a sphingomyelin monolayer. J. Phys. Chem. B 2009, 113:12844-12851.
67. Intermolecular and Surface Forces 1985, Academic Press, London. 2 ed. J.N. Israelachvili (Ed.).
68. Carrer D.C., Härtel S., Mónaco H.L., Maggio B. Ceramide modulates the lipid membrane organization at molecular and supramolecular levels. Chem. Phys. Lipids 2003, 122:147-152.
69. Carrer D.C., Schreier S., Patrito M., Maggio B. Effects of a short-chain ceramide on bilayer domain formation, thickness, and chain mobililty: DMPC and asymmetric ceramide mixtures. Biophys. J. 2006, 90:2394-2403.
70. Veiga M.P., Arrondo J.L.R., Goñi F.M., Alonso A. Ceramides in phospholipid membranes: effects on bilayer stability and transition to nonlamellar phases. Biophys. J. 1999, 76:342-350.
71. Contreras F.X., Villar A.-V., Alonso A., Kolesnick R.N., Goni F.M. Sphingomyelinase activity causes transbilayer lipid translocation in model and cell membranes. J. Biol. Chem. 2003, 278:37169-37174.
72. Contreras F.X., Basañez G., Alonso A., Herrmann A., Goñi F.M. Asymmetric addition of ceramides but not dihydroceramides promotes transbilayer (flip-flop) lipid motion in membranes. Biophys. J. 2005, 88:348-359.
73. Traïkia M., Warschawski D.E., Lambert O., Rigaud J.-L., Devaux P.F. Asymmetrical Membranes and Surface Tension 2002, vol. 83:1443-1454.
74. Raphael R.M., Waugh R.E., Svetina S.a., Zeks B.t. Fractional occurrence of defects in membranes and mechanically driven interleaflet phospholipid transport. Physical Review E 2001, 64:051913.
75. van Meer G., Voelker D.R., Feigenson G.W. Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 2008, 9:112-124.
76. Seigneuret M. P.F. devaux, ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes. Proc. Natl. Acad. Sci. USA 1984, 81:3751-3755.
77. Steck T.L., Ye J., Lange Y. Probing red cell membrane cholesterol movement with cyclodextrin. Biophys. J. 2002, 83:2118-2125.
78. Grassme H., Jekle A., Riehle A., Schwarz H., Berger J., Sandhoff K., Kolesnick R., Gulbins E. CD95 signaling via ceramide-rich membrane rafts. J. Biol. Chem. 2001, 276:20589-20596.
79. Grassme H., Jendrossek V., Bock J., Riehle A., Gulbins E. Ceramide-rich membrane rafts mediate CD40 clustering. J. Immunol. 2002, 168:298-307.
80. Grassme H., Jendrossek V., Riehle A., von Kurthy G., Berger J., Schwarz H., Weller M., Kolesnick R., Gulbins E. Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts. Nat. Med. 2003, 9:322-330.
81. Cremesti A.E., Goni F.M., Kolesnick R. Role of sphingomyelinase and ceramide in modulating rafts: do biophysical properties determine biologic outcome?. FEBS Lett. 2002, 531:47-53.
82. Gulbins E., Dreschers S., Wilker B., Grassmé H. Ceramide, membrane rafts and infections. J. Mol. Med. 2004, 82:357-363.
83. Bollinger C.R., Teichgräber V., Gulbins E. Ceramide-enriched membrane domains. Biochim. Biophys. Acta (BBA) - Mol. Cell Res. 2005, 1746:284-294.
84. Tepper A.D., Ruurs P., Wiedmer T., Sims P.J., Borst J., van Blitterswijk W.J. Sphingomyelin hydrolysis to ceramide during the execution phase of apoptosis results from phospholipid scrambling and alters cell-surface morphology. J. Cell Biol. 2000, 150:155-164.
85. Green D.R. Apoptosis and sphingomyelin hydrolysis: the flip side. J. Cell Biol. 2000, 150:5F-8F.
86. Herz J., Pardo J., Kashkar H., Schramm M., Kuzmenkina E., Bos E., Wiegmann K., Wallich R., Peters P.J., Herzig S., Schmelzer E., Krönke M., Simon M.M., U.O. Acid sphingomyelinase is a key regulator of cytotoxic granule secretion by primary T lymphocytes. Nat. Immunol. 2009, 10:761-768.
87. Trajkovic K., Hsu C., Chiantia S., Rajendran L., Wenzel D., Wieland F., Schwille P., Brugger B., Simons M. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008, 319:1244-1247.