1932

Abstract

Ceramides are sphingolipids containing a sphingosine or a related base, to which a fatty acid is linked through an amide bond. When incorporated into a lipid bilayer, ceramides exhibit a number of properties not shared by almost any other membrane lipid: Ceramides () are extremely hydrophobic and thus cannot exist in suspension in aqueous media; () increase the molecular order (rigidity) of phospholipids in membranes; () give rise to lateral phase separation and domain formation in phospholipid bilayers; () possess a marked intrinsic negative curvature that facilitates formation of inverted hexagonal phases; () make bilayers and cell membranes permeable to small and large (i.e., protein-size) solutes; and () promote transmembrane (flip-flop) lipid motion. Unfortunately, there is hardly any link between the physical studies reviewed here and the mass of biological and clinical studies on the effects of ceramides in health and disease.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-070317-033309
2018-05-20
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/biophys/47/1/annurev-biophys-070317-033309.html?itemId=/content/journals/10.1146/annurev-biophys-070317-033309&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Al Sazzad MA, Yasuda T, Murata M, Slotte JP 2017. The long-chain sphingoid base of ceramides determines their propensity for lateral segregation. Biophys. J. 112:976–83
    [Google Scholar]
  2. 2.  Alanko SM, Halling KK, Maunula S, Slotte JP, Ramstedt B 2005. Displacement of sterols from sterol/sphingomyelin domains in fluid bilayer membranes by competing molecules. Biochim. Biophys. Acta 1715:111–21
    [Google Scholar]
  3. 3.  Artetxe I, Sergelius C, Kurita M, Yamaguchi S, Katsumura S et al. 2013. Effects of sphingomyelin headgroup size on interactions with ceramide. Biophys. J. 104:604–12
    [Google Scholar]
  4. 4.  Artetxe I, Ugarte-Uribe B, Gil D, Valle M, Alonso A et al. 2017. Does ceramide form channels? The ceramide-induced membrane permeabilization mechanism. Biophys. J. 113:860–68
    [Google Scholar]
  5. 5.  Bai J, Pagano RE 1997. Measurement of spontaneous transfer and transbilayer movement of BODIPY-labeled lipids in lipid vesicles. Biochemistry 36:8840–48
    [Google Scholar]
  6. 6.  Basanez G, Ruiz-Arguello MB, Alonso A, Goñi FM, Karlsson G, Edwards K 1997. Morphological changes induced by phospholipase C and by sphingomyelinase on large unilamellar vesicles: a cryo-transmission electron microscopy study of liposome fusion. Biophys. J. 72:2630–37
    [Google Scholar]
  7. 7.  Boulgaropoulos B, Arsov Z, Laggner P, Pabst G 2011. Stable and unstable lipid domains in ceramide-containing membranes. Biophys. J. 100:2160–68
    [Google Scholar]
  8. 8.  Brockman HL, Momsen MM, Brown RE, He L, Chun J et al. 2004. The 4,5-double bond of ceramide regulates its dipole potential, elastic properties, and packing behavior. Biophys. J. 87:1722–31
    [Google Scholar]
  9. 9.  Busto JV, Fanani ML, De Tullio L, Sot J, Maggio B et al. 2009. Coexistence of immiscible mixtures of palmitoylsphingomyelin and palmitoylceramide in monolayers and bilayers. Biophys. J. 97:2717–26
    [Google Scholar]
  10. 10.  Busto JV, García-Arribas AB, Sot J, Torrecillas A, Gómez-Fernández JC et al. 2014. Lamellar gel (Lß) phases of ternary lipid composition containing ceramide and cholesterol. Biophys. J. 106:621–30
    [Google Scholar]
  11. 11.  Busto JV, Sot J, Requejo-Isidro J, Goñi FM, Alonso A 2010. Cholesterol displaces palmitoylceramide from its tight packing with palmitoylsphingomyelin in the absence of a liquid-disordered phase. Biophys. J. 99:1119–28
    [Google Scholar]
  12. 12.  Carrer DC, Maggio B 1999. Phase behavior and molecular interactions in mixtures of ceramide with dipalmitoylphosphatidylcholine. J. Lipid Res. 40:1978–89
    [Google Scholar]
  13. 13.  Castro BM, Silva LC, Fedorov A, de Almeida RF, Prieto M 2009. Cholesterol-rich fluid membranes solubilize ceramide domains: implications for the structure and dynamics of mammalian intracellular and plasma membranes. J. Biol. Chem. 284:22978–87
    [Google Scholar]
  14. 14.  Catapano ER, Lillo MP, García-Rodríguez P, Natale P, Langevin D et al. 2015. Thermomechanical transitions of egg-ceramide monolayers. Langmuir 31:3912–18
    [Google Scholar]
  15. 15.  Catapano ER, Natale P, Monroy F, López-Montero I 2017. The enzymatic sphingomyelin to ceramide conversion increases the shear membrane viscosity at the air-water interface. Adv. Colloid Interface Sci. 247:555–60
    [Google Scholar]
  16. 16.  Chang K-T, Anishkin A, Patwardhan GA, Beverly LJ, Siskind LJ, Colombini M 2015. Ceramide channels: destabilization by Bcl-xL and role in apoptosis. Biochim. Biophys. Acta 1848:2374–84
    [Google Scholar]
  17. 17.  Chiantia S, Kahya N, Ries J, Schwille P 2006. Effects of ceramide on liquid-ordered domains investigated by simultaneous AFM and FCS. Biophys. J. 90:4500–8
    [Google Scholar]
  18. 18.  Chiantia S, Kahya N, Schwille P 2007. Raft domain reorganization driven by short- and long-chain ceramide: a combined AFM and FCS study. Langmuir 23:7659–65
    [Google Scholar]
  19. 19.  Chiantia S, Ries J, Kahya N, Schwille P 2006. Combined AFM and two-focus SFCS study of raft-exhibiting model membranes. Chemphyschem 7:2409–18
    [Google Scholar]
  20. 20.  Colombini M. 2017. Ceramide channels and mitochondrial outer membrane permeability. J. Bioenerg. Biomembr. 49:57–64
    [Google Scholar]
  21. 21.  Contreras FX, Basanez G, Alonso A, Herrmann A, Goñi FM 2005. Asymmetric addition of ceramides but not dihydroceramides promotes transbilayer (flip-flop) lipid motion in membranes. Biophys. J. 88:348–59
    [Google Scholar]
  22. 22.  Contreras FX, Ernst AM, Haberkant P, Bjorkholm P, Lindahl E et al. 2012. Molecular recognition of a single sphingolipid species by a protein's transmembrane domain. Nature 481:525–29
    [Google Scholar]
  23. 23.  Contreras FX, Villar AV, Alonso A, Kolesnick RN, Goñi FM 2003. Sphingomyelinase activity causes transbilayer lipid translocation in model and cell membranes. J. Biol. Chem. 278:37169–74
    [Google Scholar]
  24. 24.  Cremesti AE, Goñi FM, Kolesnick R 2002. Role of sphingomyelinase and ceramide in modulating rafts: Do biophysical properties determine biologic outcome?. FEBS Lett 531:47–53
    [Google Scholar]
  25. 25.  Cui M, Wang Y, Cavaleri J, Kelson T, Teng Y, Han M 2017. Starvation-induced stress response is critically impacted by ceramide levels in Caenorhabditis elegans. Genetics 205:775–85
    [Google Scholar]
  26. 26.  Doroudgar M, Lafleur M 2017. Ceramide-C16 is a versatile modulator of phosphatidylethanolamine polymorphism. Biophys. J. 112:2357–66
    [Google Scholar]
  27. 27.  Dupuy FG, Fernandez Bordin SP, Maggio B, Oliveira RG 2017. Hexagonal phase with ordered acyl chains formed by a short chain asymmetric ceramide. Colloids Surf. B Biointerfaces 149:89–96
    [Google Scholar]
  28. 28.  Dupuy FG, Maggio B 2014. N-acyl chain in ceramide and sphingomyelin determines their mixing behavior, phase state, and surface topography in Langmuir films. J. Phys. Chem. B 118:7475–87
    [Google Scholar]
  29. 29.  Dutagaci B, Becker-Baldus J, Faraldo-Gomez JD, Glaubitz C 2014. Ceramide-lipid interactions studied by MD simulations and solid-state NMR. Biochim. Biophys. Acta 1838:2511–19
    [Google Scholar]
  30. 30.  Espinosa G, López-Montero I, Monroy F, Langevin D 2011. Shear rheology of lipid monolayers and insights on membrane fluidity. PNAS 108:6008–13
    [Google Scholar]
  31. 31.  Fabrias G, Munoz-Olaya J, Cingolani F, Signorelli P, Casas J et al. 2012. Dihydroceramide desaturase and dihydrosphingolipids: debutant players in the sphingolipid arena. Prog. Lipid Res. 51:82–94
    [Google Scholar]
  32. 32.  Fanani ML, Maggio B 2010. Phase state and surface topography of palmitoyl-ceramide monolayers. Chem. Phys. Lipids 163:594–600
    [Google Scholar]
  33. 33.  Fyrst H, Herr DR, Harris GL, Saba JD 2004. Characterization of free endogenous C14 and C16 sphingoid bases from Drosophila melanogaster. J. Lipid Res. 45:54–62
    [Google Scholar]
  34. 34.  García-Arribas AB, Ahyayauch H, Sot J, López-González PL, Alonso A, Goñi FM 2016. Ceramide-induced lamellar gel phases in fluid cell lipid extracts. Langmuir 32:9053–63
    [Google Scholar]
  35. 35.  García-Arribas AB, Axpe E, Mujika JI, Merida D, Busto JV et al. 2016. Cholesterol–ceramide interactions in phospholipid and sphingolipid bilayers as observed by positron annihilation lifetime spectroscopy and molecular dynamics simulations. Langmuir 32:5434–44
    [Google Scholar]
  36. 36.  García-Arribas AB, Busto JV, Alonso A, Goñi FM 2015. Atomic force microscopy characterization of palmitoylceramide and cholesterol effects on phospholipid bilayers: a topographic and nanomechanical study. Langmuir 31:3135–45
    [Google Scholar]
  37. 37.  García-Arribas AB, González-Ramírez EJ, Sot J, Areso I, Alonso A, Goñi FM 2017. Complex effects of 24:1 sphingolipids in membranes containing dioleoylphosphatidylcholine and cholesterol. Langmuir 33:5545–54
    [Google Scholar]
  38. 38.  Gillams RJ, Busto JV, Busch S, Goñi FM, Lorenz CD, McLain SE 2015. Solvation and hydration of the ceramide headgroup in a non-polar solution. J. Phys. Chem. B 119:128–39
    [Google Scholar]
  39. 39.  Goñi FM, Alonso A 2006. Biophysics of sphingolipids I. Membrane properties of sphingosine, ceramides and other simple sphingolipids. Biochim. Biophys. Acta 1758:1902–21
    [Google Scholar]
  40. 40.  Goñi FM, Alonso A 2009. Effects of ceramide and other simple sphingolipids on membrane lateral structure. Biochim. Biophys. Acta 1788:169–77
    [Google Scholar]
  41. 41.  Goñi FM, Sot J, Alonso A 2014. Biophysical properties of sphingosine, ceramides and other simple sphingolipids. Biochem. Soc. Trans. 42:1401–8
    [Google Scholar]
  42. 42.  Grösch S, Schiffmann S, Geisslinger G 2012. Chain length-specific properties of ceramides. Prog. Lipid Res. 51:50–62
    [Google Scholar]
  43. 43.  Hernández-Tiedra S, Fabriàs G, Dávila D, Salanueva IJ, Casas J et al. 2016. Dihydroceramide accumulation mediates cytotoxic autophagy of cancer cells via autolysosome destabilization. Autophagy 12:2213–29
    [Google Scholar]
  44. 44.  Holopainen JM, Brockman HL, Brown RE, Kinnunen PK 2001. Interfacial interactions of ceramide with dimyristoylphosphatidylcholine: impact of the N-acyl chain. Biophys. J. 80:765–75
    [Google Scholar]
  45. 45.  Holopainen JM, Lehtonen JY, Kinnunen PK 1997. Lipid microdomains in dimyristoylphos- phatidylcholine–ceramide liposomes. Chem. Phys. Lipids 88:1–13
    [Google Scholar]
  46. 46.  Hsueh Y-W, Giles R, Kitson N, Thewalt J 2002. The effect of ceramide on phosphatidylcholine membranes: a deuterium NMR study. Biophys. J. 82:3089–95
    [Google Scholar]
  47. 47.  Huang H-W, Goldberg EM, Zidovetzki R 1996. Ceramide induces structural defects into phosphatidylcholine bilayers and activates phospholipase A2. Biochem. Biophys. Res. Commun. 220:834–38
    [Google Scholar]
  48. 48.  Jiménez-Rojo N, García-Arribas AB, Sot J, Alonso A, Goñi FM 2014. Lipid bilayers containing sphingomyelins and ceramides of varying N-acyl lengths: a glimpse into sphingolipid complexity. Biochim. Biophys. Acta 1838:456–64
    [Google Scholar]
  49. 49.  Jiménez-Rojo N, Sot J, Busto JV, Shaw WA, Duan J et al. 2014. Biophysical properties of novel 1-deoxy-(dihydro)ceramides occurring in mammalian cells. Biophys. J. 107:2850–59
    [Google Scholar]
  50. 50.  Kolesnick RN, Goñi FM, Alonso A 2000. Compartmentalization of ceramide signaling: physical foundations and biological effects. J. Cell. Physiol. 184:285–300
    [Google Scholar]
  51. 51.  Leung SSW, Busto JV, Keyvanloo A, Goñi FM, Thewalt J 2012. Insights into sphingolipid miscibility: separate observation of sphingomyelin and ceramide N-acyl chain melting. Biophys. J. 103:2465–74
    [Google Scholar]
  52. 52.  Levy M, Futerman AH 2010. Mammalian ceramide synthases. IUBMB Life 62:347–56
    [Google Scholar]
  53. 53.  Li X-M, Momsen MM, Brockman HL, Brown RE 2002. Lactosylceramide: effect of acyl chain structure on phase behavior and molecular packing. Biophys. J. 83:1535–46
    [Google Scholar]
  54. 54.  López-Montero I, Catapano ER, Espinosa G, Arriaga LR, Langevin D, Monroy F 2013. Shear and compression rheology of Langmuir monolayers of natural ceramides: solid character and plasticity. Langmuir 29:6634–44
    [Google Scholar]
  55. 55.  López-Montero I, Rodriguez N, Cribier S, Pohl A, Vélez M, Devaux PF 2005. Rapid transbilayer movement of ceramides in phospholipid vesicles and in human erythrocytes. J. Biol. Chem. 280:25811–19
    [Google Scholar]
  56. 56.  López-Montero I, Vélez M, Devaux PF 2007. Surface tension induced by sphingomyelin to ceramide conversion in lipid membranes. Biochim. Biophys. Acta 1768:553–61
    [Google Scholar]
  57. 57.  Maté S, Busto JV, García-Arribas AB, Sot J, Vazquez R et al. 2014. N-nervonoylsphingomyelin (C24:1) prevents lateral heterogeneity in cholesterol-containing membranes. Biophys. J. 106:2606–16
    [Google Scholar]
  58. 58.  Maula T, Al Sazzad MA, Slotte JP 2015. Influence of hydroxylation, chain length, and chain unsaturation on bilayer properties of ceramides. Biophys. J. 109:1639–51
    [Google Scholar]
  59. 59.  Maula T, Artetxe I, Grandell PM, Slotte JP 2012. Importance of the sphingoid base length for the membrane properties of ceramides. Biophys. J. 103:1870–79
    [Google Scholar]
  60. 60. Megha, Bakht O, London E 2006. Cholesterol precursors stabilize ordinary and ceramide-rich ordered lipid domains (lipid rafts) to different degrees. Implications for the Bloch hypothesis and sterol biosynthesis disorders. J. Biol. Chem. 281:21903–13
    [Google Scholar]
  61. 61.  Montes LR, Alonso A, Goñi FM, Bagatolli LA 2007. Giant unilamellar vesicles electroformed from native membranes and organic lipid mixtures under physiological conditions. Biophys. J. 93:3548–54
    [Google Scholar]
  62. 62.  Montes LR, Ruiz-Arguello MB, Goñi FM, Alonso A 2002. Membrane restructuring via ceramide results in enhanced solute efflux. J. Biol. Chem. 277:11788–94
    [Google Scholar]
  63. 63.  Papahadjopoulos D, Nir S, Oki S 1972. Permeability properties of phospholipid membranes: effect of cholesterol and temperature. Biochim. Biophys. Acta 266:561–83
    [Google Scholar]
  64. 64.  Pascher I. 1976. Molecular arrangements in sphingolipids: conformation and hydrogen bonding of ceramide and their implication on membrane stability and permeability. Biochim. Biophys. Acta 455:433–51
    [Google Scholar]
  65. 65.  Patel H, Tscheka C, Heerklotz H 2009. Characterizing vesicle leakage by fluorescence lifetime measurements. Soft Matter 5:2849–51
    [Google Scholar]
  66. 66.  Peñalva DA, Oresti GM, Dupuy F, Antollini SS, Maggio B et al. 2014. Atypical surface behavior of ceramides with nonhydroxy and 2-hydroxy very long-chain (C28–C32) PUFAs. Biochim. Biophys. Acta 1838:731–38
    [Google Scholar]
  67. 67.  Peñalva DA, Wilke N, Maggio B, Aveldano MI, Fanani ML 2014. Surface behavior of sphingomyelins with very long chain polyunsaturated fatty acids and effects of their conversion to ceramides. Langmuir 30:4385–95
    [Google Scholar]
  68. 68.  Perera MN, Ganesan V, Siskind LJ, Szulc ZM, Bielawska A et al. 2016. Ceramide channel: structural basis for selective membrane targeting. Chem. Phys. Lipids 194:110–16
    [Google Scholar]
  69. 69.  Pinto SN, Fernandes F, Fedorov A, Futerman AH, Silva LC, Prieto M 2013. A combined fluorescence spectroscopy, confocal and 2-photon microscopy approach to re-evaluate the properties of sphingolipid domains. Biochim. Biophys. Acta 1828:2099–110
    [Google Scholar]
  70. 70.  Pinto SN, Laviad EL, Stiban J, Kelly SL, Merrill AH Jr et al. 2014. Changes in membrane biophysical properties induced by sphingomyelinase depend on the sphingolipid N-acyl chain. J. Lipid Res. 55:53–61
    [Google Scholar]
  71. 71.  Pinto SN, Silva LC, Futerman AH, Prieto M 2011. Effect of ceramide structure on membrane biophysical properties: the role of acyl chain length and unsaturation. Biochim. Biophys. Acta 1808:2753–60
    [Google Scholar]
  72. 72.  Pohl A, López-Montero I, Rouvière F, Giusti F, Devaux PF 2009. Rapid transmembrane diffusion of ceramide and dihydroceramide spin-labelled analogues in the liquid ordered phase. Mol. Membr. Biol. 26:194–204
    [Google Scholar]
  73. 73.  Rerek ME, Van Wyck D, Mendelsohn R, Moore DJ 2005. FTIR spectroscopic studies of lipid dynamics in phytosphingosine ceramide models of the stratum corneum lipid matrix. Chem. Phys. Lipids 134:51–58
    [Google Scholar]
  74. 74.  Rodriguez-Cuenca S, Pellegrinelli V, Campbell M, Oresic M, Vidal-Puig A 2017. Sphingolipids and glycerophospholipids—the “ying and yang” of lipotoxicity in metabolic diseases. Prog. Lipid Res. 66:14–29
    [Google Scholar]
  75. 75.  Ruiz-Arguello MB, Basanez G, Goñi FM, Alonso A 1996. Different effects of enzyme-generated ceramides and diacylglycerols in phospholipid membrane fusion and leakage. J. Biol. Chem. 271:26616–21
    [Google Scholar]
  76. 76.  Ruiz-Arguello MB, Goñi FM, Alonso A 1998. Vesicle membrane fusion induced by the concerted activities of sphingomyelinase and phospholipase C. J. Biol. Chem. 273:22977–82
    [Google Scholar]
  77. 77.  Samanta S, Stiban J, Maugel TK, Colombini M 2011. Visualization of ceramide channels by transmission electron microscopy. Biochim. Biophys. Acta 1808:1196–201
    [Google Scholar]
  78. 78.  Senkal CE, Salama MF, Snider AJ, Allopenna JJ, Rana NA et al. 2017. Ceramide is metabolized to acylceramide and stored in lipid droplets. Cell. Metab. 25:686–97
    [Google Scholar]
  79. 79.  Siddique MM, Li Y, Chaurasia B, Kaddai VA, Summers SA 2015. Dihydroceramides: from bit players to lead actors. J. Biol. Chem. 290:15371–79
    [Google Scholar]
  80. 80.  Silva LC, Ben David O, Pewzner-Jung Y, Laviad EL, Stiban J et al. 2012. Ablation of ceramide synthase 2 strongly affects biophysical properties of membranes. J. Lipid Res. 53:430–36
    [Google Scholar]
  81. 81.  Silva LC, de Almeida RF, Castro BM, Fedorov A, Prieto M 2007. Ceramide-domain formation and collapse in lipid rafts: membrane reorganization by an apoptotic lipid. Biophys. J. 92:502–16
    [Google Scholar]
  82. 82.  Silva LC, de Almeida RF, Fedorov A, Matos AP, Prieto M 2006. Ceramide-platform formation and -induced biophysical changes in a fluid phospholipid membrane. Mol. Membr. Biol. 23:137–48
    [Google Scholar]
  83. 83.  Silva LC, Futerman AH, Prieto M 2009. Lipid raft composition modulates sphingomyelinase activity and ceramide-induced membrane physical alterations. Biophys. J. 96:3210–22
    [Google Scholar]
  84. 84.  Siskind LJ, Colombini M 2000. The lipids C2- and C16-ceramide form large stable channels. Implications for apoptosis. J. Biol. Chem. 275:38640–44
    [Google Scholar]
  85. 85.  Slotte JP, Bierman EL 1988. Depletion of plasma-membrane sphingomyelin rapidly alters the distribution of cholesterol between plasma membranes and intracellular cholesterol pools in cultured fibroblasts. Biochem. J. 250:653–58
    [Google Scholar]
  86. 86.  Slotte JP, Yasuda T, Engberg O, Al Sazzad MA, Hautala V et al. 2017. Bilayer interactions among unsaturated phospholipids, sterols, and ceramide. Biophys. J. 112:1673–81
    [Google Scholar]
  87. 87.  Sot J, Aranda FJ, Collado M-I, Goñi FM, Alonso A 2005. Different effects of long- and short-chain ceramides on the gel-fluid and lamellar-hexagonal transitions of phospholipids: a calorimetric, NMR, and x-ray diffraction study. Biophys. J. 88:3368–80
    [Google Scholar]
  88. 88.  Sot J, Bagatolli LA, Goñi FM, Alonso A 2006. Detergent-resistant, ceramide-enriched domains in sphingomyelin/ceramide bilayers. Biophys. J. 90:903–14
    [Google Scholar]
  89. 89.  Sot J, Goñi FM, Alonso A 2005. Molecular associations and surface-active properties of short- and long-N-acyl chain ceramides. Biochim. Biophys. Acta 1711:12–19
    [Google Scholar]
  90. 90.  Sot J, Ibarguren M, Busto JV, Montes LR, Goñi FM, Alonso A 2008. Cholesterol displacement by ceramide in sphingomyelin-containing liquid-ordered domains, and generation of gel regions in giant lipidic vesicles. FEBS Lett 582:3230–36
    [Google Scholar]
  91. 91.  Sullan RM, Li JK, Hao C, Walker GC, Zou S 2010. Cholesterol-dependent nanomechanical stability of phase-segregated multicomponent lipid bilayers. Biophys. J. 99:507–16
    [Google Scholar]
  92. 92.  Sullan RM, Li JK, Zou S 2009. Direct correlation of structures and nanomechanical properties of multicomponent lipid bilayers. Langmuir 25:7471–77
    [Google Scholar]
  93. 93.  Sullan RM, Li JK, Zou S 2009. Quantification of the nanomechanical stability of ceramide-enriched domains. Langmuir 25:12874–77
    [Google Scholar]
  94. 94.  Taniguchi Y, Ohba T, Miyata H, Ohki K 2006. Rapid phase change of lipid microdomains in giant vesicles induced by conversion of sphingomyelin to ceramide. Biochim. Biophys. Acta 1758:145–53
    [Google Scholar]
  95. 95.  Veiga MP, Arrondo JL, Goñi FM, Alonso A 1999. Ceramides in phospholipid membranes: effects on bilayer stability and transition to nonlamellar phases. Biophys. J. 76:342–50
    [Google Scholar]
  96. 96.  Veiga MP, Arrondo JL, Goñi FM, Alonso A, Marsh D 2001. Interaction of cholesterol with sphingomyelin in mixed membranes containing phosphatidylcholine, studied by spin-label ESR and IR spectroscopies. A possible stabilization of gel-phase sphingolipid domains by cholesterol. Biochemistry 40:2614–22
    [Google Scholar]
  97. 97.  Vieira CR, Munoz-Olaya JM, Sot J, Jiménez-Baranda S, Izquierdo-Useros N et al. 2010. Dihydrosphingomyelin impairs HIV-1 infection by rigidifying liquid-ordered membrane domains. Chem. Biol. 17:766–75
    [Google Scholar]
  98. 98.  Zha X, Pierini LM, Leopold PL, Skiba PJ, Tabas I, Maxfield FR 1998. Sphingomyelinase treatment induces ATP-independent endocytosis. J. Cell Biol. 140:39–47
    [Google Scholar]
/content/journals/10.1146/annurev-biophys-070317-033309
Loading
/content/journals/10.1146/annurev-biophys-070317-033309
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error