Micrometric segregation of fluorescent membrane lipids: Relevance for endogenous lipids and biogenesis in erythrocytes

Journal of Lipid Research

Volumn 54, Issue 4, 2013, Pages 1066-1076

  D'Auria, Ludovic ^a   Fenaux, Marisa ^a   Aleksandrowicz, Paulina ^a   Van Der Smissen, Patrick ^a   Chantrain, Christophe ^b   Vermylen, Christiane ^b   Vikkula, Miikka ^c   Courtoy, Pierre J ^a   Tyteca, Donatienne ^a  

^a CLINIQUES UNIVERSITAIRES SAINT LUC   (Belgium)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^c DE DUVE INSTITUTE   (Belgium)

Author keywords

Cholesterol; Compartmentation; Confocal imaging; Lipid domains; Membrane tension; Membrane:spectrin anchorage complexes; Plasma membrane; Spherocytosis

Indexed keywords

ANKYRIN; CHOLESTEROL; MEMBRANE LIPID; MONOSIALOTETRAHEXOSYLGANGLIOSIDE; PHOSPHATIDYLCHOLINE; PROTEIN KINASE C; SPECTRIN; SPHINGOMYELIN; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CASE REPORT; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; CYTOSKELETON; ERYTHROCYTE; ERYTHROCYTE DEFORMABILITY; ERYTHROCYTE FRAGILITY; ERYTHROCYTE MEMBRANE; HUMAN; HUMAN CELL; LIPID ANALYSIS; LIPID BILAYER; LIPID MEMBRANE; MEMBRANE FLUIDITY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; SPHEROCYTOSIS;

BETA-CYCLODEXTRINS; BLOTTING, WESTERN; BORON COMPOUNDS; CELL MEMBRANE; CELLS, CULTURED; CHOLESTEROL; CHROMATOGRAPHY, THIN LAYER; ERYTHROCYTES; GLYCOSPHINGOLIPIDS; HETEROCYCLIC COMPOUNDS, 3-RING; HUMANS; MEMBRANE LIPIDS; MICROSCOPY, ELECTRON, SCANNING; PHOSPHATIDYLCHOLINES; SPHINGOMYELINS;

EID: 84875862847     PISSN: 00222275     EISSN: 15397262     Source Type: Journal    
DOI: 10.1194/jlr.M034314     Document Type: Article

References (63)

1. Singer, S. J., and G. L. Nicolson. 1972. The fl uid mosaic model of the structure of cell membranes. Science. 175 : 720-731.
2. Lingwood, D., and K. Simons. 2010. Lipid rafts as a membraneorganizing principle. Science. 327 : 46-50.
3. Lingwood, D., J. Ries, P. Schwille, and K. Simons. 2008. Plasma membranes are poised for activation of raft phase coalescence at physiological temperature. Proc. Natl. Acad. Sci. USA. 105 : 10005-10010.
4. Pike, L. J. 2006. Rafts defi ned: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J. Lipid Res. 47 : 1597-1598.
5. Fujita, A., J. Cheng, M. Hirakawa, K. Furukawa, S. Kusunoki, and T. Fujimoto. 2007. Gangliosides GM1 and GM3 in the living cell membrane form clusters susceptible to cholesterol depletion and chilling. Mol. Biol. Cell. 18 : 2112-2122.
6. Mizuno, H., M. Abe, P. Dedecker, A. Makino, S. Rocha, Y. Ohno-Iwashita, J. Hofkens, T. Kobayashi, and A. Miyawaki. 2011. Fluorescent probes for superresolution imaging of lipid domains on the plasma membrane. Chem Sci. 2 : 1548-1553.
7. Bagatolli, L. A., J. H. Ipsen, A. C. Simonsen, and O. G. Mouritsen. 2010. An outlook on organization of lipids in membranes: searching for a realistic connection with the organization of biological membranes. Prog. Lipid Res. 49 : 378-389.
8. Kahya, N., D. Scherfeld, K. Bacia, B. Poolman, and P. Schwille. 2003. Probing lipid mobility of raft-exhibiting model membranes by fl uorescence correlation spectroscopy. J. Biol. Chem. 278 : 28109-28115.
9. Baumgart, T., S. T. Hess, and W. W. Webb. 2003. Imaging coexisting fl uid domains in biomembrane models coupling curvature and line tension. Nature. 425 : 821-824.
10. Goñi, F. M., and A. Alonso. 2009. Effects of ceramide and other simple sphingolipids on membrane lateral structure. Biochim. Biophys. Acta. 1788 : 169-177.
11. Busto, J. V., J. Sot, J. Requejo-Isidro, F. M. Goni, and A. Alonso. 2010. Cholesterol displaces palmitoylceramide from its tight packing with palmitoylsphingomyelin in the absence of a liquid-disordered phase. Biophys. J. 99 : 1119-1128.
12. Kusumi, A., K. G. Suzuki, R. S. Kasai, K. Ritchie, and T. K. Fujiwara. 2011. Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem. Sci. 36 : 604-615.
13. Yechiel, E., and M. Edidin. 1987. Micrometer-scale domains in fi-broblast plasma membranes. J. Cell Biol. 105 : 755-760.
14. Fujiwara, T., K. Ritchie, H. Murakoshi, K. Jacobson, and A. Kusumi. 2002. Phospholipids undergo hop diffusion in compartmentalized cell membrane. J. Cell Biol. 157 : 1071-1081.
15. Singh, R. D., Y. Liu, C. L. Wheatley, E. L. Holicky, A. Makino, D. L. Marks, T. Kobayashi, G. Subramaniam, R. Bittman, and R. E. Pagano. 2006. Caveolar endocytosis and microdomain association of a glycosphingolipid analog is dependent on its sphingosine stereochemistry. J. Biol. Chem. 281 : 30660-30668.
16. Gousset, K., W. F. Wolkers, N. M. Tsvetkova, A. E. Oliver, C. L. Field, N. J. Walker, J. H. Crowe, and F. Tablin. 2002. Evidence for a physiological role for membrane rafts in human platelets. J. Cell. Physiol. 190 : 117-128.
17. Hao, M., S. Mukherjee, and F. R. Maxfi eld. 2001. Cholesterol depletion induces large scale domain segregation in living cell membranes. Proc. Natl. Acad. Sci. USA. 98 : 13072-13077.
18. Gaus, K., E. Gratton, E. P. Kable, A. S. Jones, I. Gelissen, L. Kritharides, and W. Jessup. 2003. Visualizing lipid structure and raft domains in living cells with two-photon microscopy. Proc. Natl. Acad. Sci. USA. 100 : 15554-15559.
19. Tyteca, D., L. D'Auria, P. V. Der Smissen, T. Medts, S. Carpentier, J. C. Monbaliu, P. de Diesbach, and P. J. Courtoy. 2010. Three unrelated sphingomyelin analogs spontaneously cluster into plasma membrane micrometric domains. Biochim. Biophys. Acta. 1798 : 909-927.
20. D'Auria, L., P. Van der Smissen, F. Bruyneel, P. J. Courtoy, and D. Tyteca. 2011. Segregation of fl uorescent membrane lipids into distinct micrometric domains: evidence for phase compartmentation of natural lipids? PLoS ONE. 6 : e17021.
21. Grossmann, G., J. Malinsky, W. Stahlschmidt, M. Loibl, I. Weig-Meckl, W. B. Frommer, M. Opekarova, and W. Tanner. 2008. Plasma membrane microdomains regulate turnover of transport proteins in yeast. J. Cell Biol. 183 : 1075-1088.
22. Klose, C., C. S. Ejsing, A. J. Garcia-Saez, H. J. Kaiser, J. L. Sampaio, M. A. Surma, A. Shevchenko, P. Schwille, and K. Simons. 2010. Yeast lipids can phase-separate into micrometer-scale membrane domains. J. Biol. Chem. 285 : 30224-30232.
23. Kusumi, A., T. K. Fujiwara, R. Chadda, M. Xie, T. A. Tsunoyama, Z. Kalay, R. S. Kasai, and K. G. Suzuki. 2012. Dynamic organizing principles of the plasma membrane that regulate signal transduction: commemorating the fortieth anniversary of Singer and Nicolson's fl uid-mosaic model. Annu. Rev. Cell Dev. Biol. 28 : 215-250.
24. van Meer, G., D. R. Voelker, and G. W. Feigenson. 2008. Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9 : 112-124.
25. Ramstedt, B., and J. P. Slotte. 2002. Membrane properties of sphingomyelins. FEBS Lett. 531 : 33-37.
26. Edidin, M. 2003. The state of lipid rafts: from model membranes to cells. Annu. Rev. Biophys. Biomol. Struct. 32 : 257-283.
27. Bali, R., L. Savino, D. A. Ramirez, N. M. Tsvetkova, L. Bagatolli, F. Tablin, J. H. Crowe, and C. Leidy. 2009. Macroscopic domain formation during cooling in the platelet plasma membrane: an issue of low cholesterol content. Biochim. Biophys. Acta. 1788 : 1229-1237.
28. Sun, M., N. Northup, F. Marga, T. Huber, F. J. Byfi eld, I. Levitan, and G. Forgacs. 2007. The effect of cellular cholesterol on membrane-cytoskeleton adhesion. J. Cell Sci. 120 : 2223-2231.
29. Salomao, M., X. Zhang, Y. Yang, S. Lee, J. H. Hartwig, J. A. Chasis, N. Mohandas, and X. An. 2008. Protein 4.1R-dependent multiprotein complex: new insights into the structural organization of the red blood cell membrane. Proc. Natl. Acad. Sci. USA. 105 : 8026-8031.
30. Baines, A. J. 2010. The spectrin-Ankyrin-4.1-Adducin membrane skeleton: adapting eukaryotic cells to the demands of animal life. Protoplasma. 244 : 99-131.
31. Sheetz, M. P., J. E. Sable, and H. G. Dobereiner. 2006. Continuous membrane-cytoskeleton adhesion requires continuous accommodation to lipid and cytoskeleton dynamics. Annu. Rev. Biophys. Biomol. Struct. 35 : 417-434.
32. Zachowski, A. 1993. Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. Biochem. J. 294 : 1-14.
33. Svoboda, K., C. F. Schmidt, D. Branton, and S. M. Block. 1992. Conformation and elasticity of the isolated red blood cell membrane skeleton. Biophys. J. 63 : 784-793.
34. Bennett, V., and J. Healy. 2008. Organizing the fl uid membrane bilayer: diseases linked to spectrin and ankyrin. Trends Mol. Med. 14 : 28-36.
35. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purifi cation. Can. J. Biochem. Physiol. 37 : 911-917.
36. Marinetti, G. V., R. Baumgarten, D. Sheeley, and S. Gordesky. 1973. Cross-linking of phospholipids to proteins in the erythrocyte membrane. Biochem. Biophys. Res. Commun. 53 : 302-308.
37. Prausnitz, M. R., B. S. Lau, C. D. Milano, S. Conner, R. Langer, and J. C. Weaver. 1993. A quantitative study of electroporation showing a plateau in net molecular transport. Biophys. J. 65 : 414-422.
38. Cheng, Z. J., R. D. Singh, D. K. Sharma, E. L. Holicky, K. Hanada, D. L. Marks, and R. E. Pagano. 2006. Distinct mechanisms of clathrin-independent endocytosis have unique sphingolipid requirements. Mol. Biol. Cell. 17 : 3197-3210.
39. Marsh, J. B., and D. B. Weinstein. 1966. Simple charring method for determination of lipids. J. Lipid Res. 7 : 574-576.
40. Mikhalyov, I., and A. Samsonov. 2011. Lipid raft detecting in membranes of live erythrocytes. Biochim. Biophys. Acta. 1808 : 1930-1939.
41. Byfi eld, F. J., H. Aranda-Espinoza, V. G. Romanenko, G. H. Rothblat, and I. Levitan. 2004. Cholesterol depletion increases membrane stiffness of aortic endothelial cells. Biophys. J. 87 : 3336-3343.
42. Ferru, E., K. Giger, A. Pantaleo, E. Campanella, J. Grey, K. Ritchie, R. Vono, F. Turrini, and P. S. Low. 2011. Regulation of membranecytoskeletal interactions by tyrosine phosphorylation of erythrocyte band 3. Blood. 117 : 5998-6006.
43. Betz, T., M. Lenz, J. F. Joanny, and C. Sykes. 2009. ATP-dependent mechanics of red blood cells. Proc. Natl. Acad. Sci. USA. 106 : 15320-15325.
44. Manno, S., Y. Takakuwa, and N. Mohandas. 2005. Modulation of erythrocyte membrane mechanical function by protein 4.1 phosphorylation. J. Biol. Chem. 280 : 7581-7587.
45. Gallagher, P. G. 2005. Hematologically important mutations: ankyrin variants in hereditary spherocytosis. Blood Cells Mol. Dis. 35 : 345-347.
46. Ipsaro, J. J., L. Huang, and A. Mondragon. 2009. Structures of the spectrin-Ankyrin interaction binding domains. Blood. 113 : 5385-5393.
47. Dahl, K. N., C. M. Westhoff, and D. E. Discher. 2003. Fractional attachment of CD47 (IAP) to the erythrocyte cytoskeleton and visual colocalization with Rh protein complexes. Blood. 101 : 1194-1199.
48. King, M. J., M. A. Jepson, A. Guest, and R. Mushens. 2011. Detection of hereditary pyropoikilocytosis by the eosin-5-maleimide (EMA)-binding test is attributable to a marked reduction in EMA-reactive transmembrane proteins. Int. J. Lab. Hematol. 33 : 205-211.
49. Ziólkowska, N. E., R. Christiano, and T. C. Walther. 2012. Organized living: formation mechanisms and functions of plasma membrane domains in yeast. Trends Cell Biol. 22 : 151-158.
50. Kuerschner, L., C. S. Ejsing, K. Ekroos, A. Shevchenko, K. I. Anderson, and C. Thiele. 2005. Polyene-lipids: a new tool to image lipids. Nat. Methods. 2 : 39-45.
51. Fidorra, M., T. Heimburg, and L. A. Bagatolli. 2009. Direct visualization of the lateral structure of porcine brain cerebrosides/POPC mixtures in presence and absence of cholesterol. Biophys. J. 97 : 142-154.
52. Malínská, K., J. Malinsky, M. Opekarova, and W. Tanner. 2003. Visualization of protein compartmentation within the plasma membrane of living yeast cells. Mol. Biol. Cell. 14 : 4427-4436.
53. Malinsky, J., M. Opekarova, and W. Tanner. 2010. The lateral compartmentation of the yeast plasma membrane. Yeast. 27 : 473-478.
54. Reed, C. F., and S. N. Swisher. 1966. Erythrocyte lipid loss in hereditary spherocytosis. J. Clin. Invest. 45 : 777-781.
55. Klappauf, E., and D. Schubert. 1977. Band 3-protein from human erythrocyte membranes strongly interacts with cholesterol. FEBS Lett. 80 : 423-425.
56. Schubert, D., and K. Boss. 1982. Band 3 protein-cholesterol interactions in erythrocyte membranes. Possible role in anion transport and dependency on membrane phospholipid. FEBS Lett. 150 : 4-8.
57. Diakowski, W., L. Ozimek, E. Bielska, S. Bem, M. Langner, and A. F. Sikorski. 2006. Cholesterol affects spectrin-phospholipid interactions in a manner different from changes resulting from alterations in membrane fl uidity due to fatty acyl chain composition. Biochim. Biophys. Acta. 1758 : 4-12.
58. Kwik, J., S. Boyle, D. Fooksman, L. Margolis, M. P. Sheetz, and M. Edidin. 2003. Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4,5-bisphosphate-dependent organization of cell actin. Proc. Natl. Acad. Sci. USA. 100 : 13964-13969.
59. Pike, L. J., and J. M. Miller. 1998. Cholesterol depletion delocalizes phosphatidylinositol bisphosphate and inhibits hormone-stimulated phosphatidylinositol turnover. J. Biol. Chem. 273 : 22298-22304.
60. An, X., X. Zhang, G. Debnath, A. J. Baines, and N. Mohandas. 2006. Phosphatidylinositol-4,5-biphosphate (PIP2) differentially regulates the interaction of human erythrocyte protein 4.1 (4.1R) with membrane proteins. Biochemistry. 45 : 5725-5732.
61. Sinha, B., D. Koster, R. Ruez, P. Gonnord, M. Bastiani, D. Abankwa, R. V. Stan, G. Butler-Browne, B. Vedie, L. Johannes, et al. 2011. Cells respond to mechanical stress by rapid disassembly of caveolae. Cell. 144 : 402-413.
62. Gauthier, N. C., T. A. Masters, and M. P. Sheetz. 2012. Mechanical feedback between membrane tension and dynamics. Trends Cell Biol. 22 : 527-535.
63. Muralidharan-Chari, V., J. W. Clancy, A. Sedgwick, and C. D'Souza-Schorey. 2010. Microvesicles: mediators of extracellular communication during cancer progression. J. Cell Sci. 123 : 1603-1611.