Cholesterol segregates into submicrometric domains at the living erythrocyte membrane: Evidence and regulation

Cellular and Molecular Life Sciences

Volumn 72, Issue 23, 2015, Pages 4633-4651

  Carquin, Mélanie ^a   Conrard, Louise ^a   Pollet, Hélène ^a   Van Der Smissen, Patrick ^a   Cominelli, Antoine ^a   Veiga Da Cunha, Maria ^a   Courtoy, Pierre J ^a   Tyteca, Donatienne ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

125I toxin; BODIPY sphingomyelin; C2C12 myoblasts; His mCherry theta D4; Lateral membrane heterogeneity; Membrane tension; Temperature; Vital confocal imaging

Indexed keywords

CHOLESTEROL; CLOSTRIDIUM TOXIN; SPHINGOMYELIN; 4,4-DIFLUORO-4-BORA-3A,4A-DIAZA-S-INDACENE; BACTERIAL TOXIN; BORON DERIVATIVE; CLOSTRIDIUM PERFRINGENS THETA-TOXIN; HEMOLYSIN;

ARTICLE; ARTIFICIAL LIPID MEMBRANE; BINDING AFFINITY; CELL ANCHORAGE; CELL LABELING; CELLULAR DISTRIBUTION; CHOLESTEROL TRANSPORT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; ERYTHROCYTE DEFORMABILITY; ERYTHROCYTE LEVEL; ERYTHROCYTE MEMBRANE; ERYTHROPHAGOCYTOSIS; HUMAN; HUMAN CELL; LIPID ANALYSIS; LIPID MEMBRANE; MEMBRANE FLUIDITY; SUBMICROMETRIC DOMAIN; TEMPERATURE DEPENDENCE; ANIMAL; CELL LINE; CELL MEMBRANE; CHEMISTRY; GENETICS; METABOLISM; MOUSE; MYOBLAST; TEMPERATURE;

ANIMALS; BACTERIAL TOXINS; BORON COMPOUNDS; CELL LINE; CHOLESTEROL; ERYTHROCYTE MEMBRANE; HEMOLYSIN PROTEINS; HUMANS; MEMBRANE MICRODOMAINS; MICE; MYOBLASTS; SPHINGOMYELINS; TEMPERATURE;

EID: 84946480970     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-015-1951-x     Document Type: Article

References (66)

1. Lange Y, Swaisgood MH, Ramos BV, Steck TL (1989) Plasma membranes contain half the phospholipid and 90% of the cholesterol and sphingomyelin in cultured human fibroblasts. J Biol Chem 264:3786-3793
2. Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327:46-50
3. Pike LJ (2006) Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function. J Lipid Res 47:1597-1598
4. Parton RG, Way M, Zorzi N, Stang E (1997) Caveolin-3 associates with developing T-tubules during muscle differentiation. J Cell Biol 136:137-154
5. Schroeder F, Nemecz G, Wood WG, Joiner C, Morrot G, Ayraut-Jarrier M, Devaux PF (1991) Transmembrane distribution of sterol in the human erythrocyte. Biochim Biophys Acta 1066:183-192
6. Lange Y, Slayton JM (1982) Interaction of cholesterol and lysophosphatidylcholine in determining red cell shape. J Lipid Res 23:1121-1127
7. Sun M, Northup N, Marga F, Huber T, Byfield FJ, Levitan I, Forgacs G (2007) The effect of cellular cholesterol on membrane-cytoskeleton adhesion. J Cell Sci 120:2223-2231
8. Laurenzana A, Fibbi G, Chilla A, Margheri G, Del Rosso T, Rovida E, Del Rosso M, Margheri F (2015) Lipid rafts: integrated platforms for vascular organization offering therapeutic opportunities. Cell Mol Life Sci 72:1537-1557
9. Baumann P, Thiele W, Cremers N, Muppala S, Krachulec J, Diefenbacher M, Kassel O, Mudduluru G, Allgayer H, Frame M, Sleeman JP (2012) CD24 interacts with and promotes the activity of c-src within lipid rafts in breast cancer cells, thereby increasing integrin-dependent adhesion. Cell Mol Life Sci 69:435-448
10. Chichili GR, Rodgers W (2009) Cytoskeleton-membrane interactions in membrane raft structure. Cell Mol Life Sci 66:2319-2328
11. Veiga MP, Arrondo JL, Goni 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 40:2614-2622
12. Fidorra M, Heimburg T, Bagatolli LA (2009) Direct visualization of the lateral structure of porcine brain cerebrosides/POPC mixtures in presence and absence of cholesterol. Biophys J 97:142-154
13. Bali R, Savino L, Ramirez DA, Tsvetkova NM, Bagatolli L, Tablin F, Crowe JH, Leidy C (2009) Macroscopic domain formation during cooling in the platelet plasma membrane: an issue of low cholesterol content. Biochim Biophys Acta 1788:1229-1237
14. Grossmann G, Opekarova M, Malinsky J, Weig-Meckl I, Tanner W (2007) Membrane potential governs lateral segregation of plasma membrane proteins and lipids in yeast. EMBO J 26:1-8
15. Malinsky J, Opekarova M, Grossmann G, Tanner W (2013) Membrane microdomains, rafts, and detergent-resistant membranes in plants and fungi. Annu Rev Plant Biol 64:501-529
16. Hamilton-Miller JM (1973) Chemistry and biology of the polyene macrolide antibiotics. Bacteriol Rev 37:166-196
17. Gimpl G, Gehrig-Burger K (2011) Probes for studying cholesterol binding and cell biology. Steroids 76:216-231
18. Waheed AA, Shimada Y, Heijnen HF, Nakamura M, Inomata M, Hayashi M, Iwashita S, Slot JW, Ohno-Iwashita Y (2001) Selective binding of perfringolysin O derivative to cholesterol-rich membrane microdomains (rafts). Proc Natl Acad Sci USA 98:4926-4931
19. Shimada Y, Maruya M, Iwashita S, Ohno-Iwashita Y (2002) The C-terminal domain of perfringolysin O is an essential cholesterol-binding unit targeting to cholesterol-rich microdomains. Eur J Biochem 269:6195-6203
20. Bavdek A, Gekara NO, Priselac D, Gutierrez Aguirre I, Darji A, Chakraborty T, Macek P, Lakey JH, Weiss S, Anderluh G (2007) Sterol and pH interdependence in the binding, oligomerization, and pore formation of Listeriolysin O. Biochemistry 46:4425-4437
21. Farrand AJ, LaChapelle S, Hotze EM, Johnson AE, Tweten RK (2010) Only two amino acids are essential for cytolytic toxin recognition of cholesterol at the membrane surface. Proc Natl Acad Sci USA 107:4341-4346
22. Nelson LD, Johnson AE, London E (2008) 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 283:4632-4642
23. Rossjohn J, Feil SC, McKinstry WJ, Tweten RK, Parker MW (1997) Structure of a cholesterol-binding, thiol-activated cytolysin and a model of its membrane form. Cell 89:685-692
24. Das A, Brown MS, Anderson DD, Goldstein JL, Radhakrishnan A (2014) Three pools of plasma membrane cholesterol and their relation to cholesterol homeostasis. Elife 3:e02882
25. Das A, Goldstein JL, Anderson DD, Brown MS, Radhakrishnan A (2013) Use of mutant 125I-perfringolysin O to probe transport and organization of cholesterol in membranes of animal cells. Proc Natl Acad Sci USA 110:10580-10585
26. Ohno-Iwashita Y, Shimada Y, Waheed AA, Hayashi M, Inomata M, Nakamura M, Maruya M, Iwashita S (2004) Perfringolysin O, a cholesterol-binding cytolysin, as a probe for lipid rafts. Anaerobe 10:125-134
27. Mizuno H, Abe M, Dedecker P, Makino A, Rocha S, Ohno-Iwashita Y, Hofkens J, Kobayashi T, Miyawaki A (2011) Fluorescent probes for superresolution imaging of lipid domains on the plasma membrane. Chem Sci 2:1548-1553
28. Frisz JF, Klitzing HA, Lou K, Hutcheon ID, Weber PK, Zimmerberg J, Kraft ML (2013) Sphingolipid domains in the plasma membranes of fibroblasts are not enriched with cholesterol. J Biol Chem 288:16855-16861
29. Frisz JF, Lou K, Klitzing HA, Hanafin WP, Lizunov V, Wilson RL, Carpenter KJ, Kim R, Hutcheon ID, Zimmerberg J, Weber PK, Kraft ML (2013) Direct chemical evidence for sphingolipid domains in the plasma membranes of fibroblasts. Proc Natl Acad Sci USA 110:E613-E622
30. Ziomek CA, Schulman S, Edidin M (1980) Redistribution of membrane proteins in isolated mouse intestinal epithelial cells. J Cell Biol 86:849-857
31. Grimmer S, van Deurs B, Sandvig K (2002) Membrane ruffling and macropinocytosis in A431 cells require cholesterol. J Cell Sci 115:2953-2962
32. Carquin M, Pollet H, Veiga-da-Cunha M, Cominelli A, Van Der Smissen P, N'Kuli F, Emonard H, Henriet P, Mizuno H, Courtoy PJ, Tyteca D (2014) Endogenous sphingomyelin segregates into submicrometric domains in the living erythrocyte membrane. J Lipid Res 55:1331-1342
33. D'Auria L, Fenaux M, Aleksandrowicz P, Van Der Smissen P, Chantrain C, Vermylen C, Vikkula M, Courtoy PJ, Tyteca D (2013) Micrometric segregation of fluorescent membrane lipids: relevance for endogenous lipids and biogenesis in erythrocytes. J Lipid Res 54:1066-1076
34. D'Auria L, Van Der Smissen P, Bruyneel F, Courtoy PJ, Tyteca D (2011) Segregation of fluorescent membrane lipids into distinct micrometric domains: evidence for phase compartmentation of natural lipids? PLoS One 6:e17021
35. Tyteca D, D'Auria L, Van Der Smissen P, Medts T, Carpentier S, Monbaliu JC, de Diesbach P, Courtoy PJ (2010) Three unrelated sphingomyelin analogs spontaneously cluster into plasma membrane micrometric domains. Biochim Biophys Acta 1798:909-927
36. Zachowski A (1993) Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement. Biochem J 294(Pt 1):1-14
37. Goodman SR, Kurdia A, Ammann L, Kakhniashvili D, Daescu O (2007) The human red blood cell proteome and interactome. Exp Biol Med (Maywood) 232:1391-1408
38. Salomao M, Zhang X, Yang Y, Lee S, Hartwig JH, Chasis JA, Mohandas N, An X (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
39. Cooper RA (1978) Influence of increased membrane cholesterol on membrane fluidity and cell function in human red blood cells. J Supramol Struct 8:413-430
40. Cornwell DG, Heikkila RE, Bar RS, Biagi GL (1967) Red blood cell lipids and the plasma membrane. JAOCS 45:297-304
41. Ohno-Iwashita Y, Iwamoto M, Mitsui K, Ando S, Nagai Y (1988) Protease-nicked theta-toxin of Clostridium perfringens, a new membrane probe with no cytolytic effect, reveals two classes of cholesterol as toxin-binding sites on sheep erythrocytes. Eur J Biochem 176:95-101
42. Betz T, Lenz M, Joanny JF, Sykes C (2009) ATP-dependent mechanics of red blood cells. Proc Natl Acad Sci USA 106:15320-15325
43. Wustner D (2007) Plasma membrane sterol distribution resembles the surface topography of living cells. Mol Biol Cell 18:211-228
44. Maekawa M, Fairn GD (2015) Complementary probes reveal that phosphatidylserine is required for the proper transbilayer distribution of cholesterol. J Cell Sci 128:1422-1433
45. Iwamoto M, Ohno-Iwashita Y, Ando S (1990) Effect of isolated C-terminal fragment of theta-toxin (perfringolysin O) on toxin assembly and membrane lysis. Eur J Biochem 194:25-31
46. Sokolov A, Radhakrishnan A (2010) Accessibility of cholesterol in endoplasmic reticulum membranes and activation of SREBP-2 switch abruptly at a common cholesterol threshold. J Biol Chem 285:29480-29490
47. McKanna JA, Haigler HT, Cohen S (1979) Hormone receptor topology and dynamics: morphological analysis using ferritin-labeled epidermal growth factor. Proc Natl Acad Sci USA 76:5689-5693
48. De Roe C, Courtoy PJ, Baudhuin P (1987) A model of protein-colloidal gold interactions. J Histochem Cytochem 35:1191-1198
49. Cai M, Zhao W, Shang X, Jiang J, Ji H, Tang Z, Wang H (2012) Direct evidence of lipid rafts by in situ atomic force microscopy. Small 8:1243-1250
50. Bosmann HB, Hagopian A, Eylar EH (1968) Cellular membranes: the isolation and characterization of the plasma and smooth membranes of HeLa cells. Arch Biochem Biophys 128:51-69
51. Perkins RG, Scott RE (1978) Plasma membrane phospholipid, cholesterol and fatty acyl composition of differentiated and undifferentiated L6 myoblasts. Lipids 13:334-337
52. Bezrukov L, Blank PS, Polozov IV, Zimmerberg J (2009) An adhesion-based method for plasma membrane isolation: evaluating cholesterol extraction from cells and their membranes. Anal Biochem 394:171-176
53. Oglecka K, Rangamani P, Liedberg B, Kraut RS, Parikh AN (2014) Oscillatory phase separation in giant lipid vesicles induced by transmembrane osmotic differentials. Elife 3:e03695
54. Kusumi A, Suzuki KG, Kasai RS, Ritchie K, Fujiwara TK (2011) Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem Sci 36:604-615
55. Fujiwara T, Ritchie K, Murakoshi H, Jacobson K, Kusumi A (2002) Phospholipids undergo hop diffusion in compartmentalized cell membrane. J Cell Biol 157:1071-1081
56. Kusumi A, Fujiwara TK, Chadda R, Xie M, Tsunoyama TA, Kalay Z, Kasai RS, Suzuki KG (2012) Dynamic organizing principles of the plasma membrane that regulate signal transduction: commemorating the fortieth anniversary of Singer and Nicolson's fluid-mosaic model. Annu Rev Cell Dev Biol 28:215-250
57. Ehrig J, Petrov EP, Schwille P (2011) Near-critical fluctuations and cytoskeleton-assisted phase separation lead to subdiffusion in cell membranes. Biophys J 100:80-89
58. Honigmann A, Sadeghi S, Keller J, Hell SW, Eggeling C, Vink R (2014) A lipid bound actin meshwork organizes liquid phase separation in model membranes. Elife 3:e01671
59. Sinha B, Koster D, Ruez R, Gonnord P, Bastiani M, Abankwa D, Stan RV, Butler-Browne G, Vedie B, Johannes L, Morone N, Parton RG, Raposo G, Sens P, Lamaze C, Nassoy P (2011) Cells respond to mechanical stress by rapid disassembly of caveolae. Cell 144:402-413
60. Guo Q, Park S, Ma H (2012) Microfluidic micropipette aspiration for measuring the deformability of single cells. Lab Chip 12:2687-2695
61. Bassereau P, Sorre B, Levy A (2014) Bending lipid membranes: experiments after W. Helfrich's model. Adv Colloid Interface Sci 208:47-57
62. Willekens FL, Werre JM, Groenen-Dopp YA, Roerdinkholder-Stoelwinder B, de Pauw B, Bosman GJ (2008) Erythrocyte vesiculation: a self-protective mechanism? Br J Haematol 141:549-556
63. Salzer U, Zhu R, Luten M, Isobe H, Pastushenko V, Perkmann T, Hinterdorfer P, Bosman GJ (2008) Vesicles generated during storage of red cells are rich in the lipid raft marker stomatin. Transfusion 48:451-462
64. Bosman GJ, Lasonder E, Groenen-Dopp YA, Willekens FL, Werre JM (2012) The proteome of erythrocyte-derived microparticles from plasma: new clues for erythrocyte aging and vesiculation. J Proteomics 76:203-210
65. van Galen J, Campelo F, Martinez-Alonso E, Scarpa M, Martinez-Menarguez JA, Malhotra V (2014) Sphingomyelin homeostasis is required to form functional enzymatic domains at the trans-Golgi network. J Cell Biol 206:609-618
66. van den Bogaart G, Meyenberg K, Risselada HJ, Amin H, Willig KI, Hubrich BE, Dier M, Hell SW, Grubmuller H, Diederichsen U, Jahn R (2011) Membrane protein sequestering by ionic protein-lipid interactions. Nature 479:552-555