Equilibrium-fluctuation-analysis of single liposome binding events reveals how cholesterol and Ca2+ modulate glycosphingolipid trans-interactions

Scientific Reports

Volumn 3, Issue , 2013, Pages

  Kunze, Angelika ^a   Bally, Marta ^b   Höök, Fredrik ^b   Larson, Göran ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CHOLESTEROL; FLUORESCENT DYE; GLYCOSPHINGOLIPID; LIPOSOME;

ARTICLE; CARBOHYDRATE ANALYSIS; CHEMISTRY; KINETICS; LIPID BILAYER; METABOLISM;

CALCIUM; CARBOHYDRATE SEQUENCE; CHOLESTEROL; FLUORESCENT DYES; GLYCOSPHINGOLIPIDS; KINETICS; LIPID BILAYERS; LIPOSOMES;

EID: 84875188554     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep01452     Document Type: Article

References (52)

1. Bovin, N. V. Carbohydrate-carbohydrate interaction: A review. Biochemistry (Moscow) 61, 694-704 (1996).
2. Rojo, J., Morales, J. C. & Penade, J. Carbohydrate-carbohydrate interactions in biological and model systems. Host-Guest Chemistry 218, 45-92 (2002).
3. Bucior, I. & Burger, M. M. Carbohydrate-carbohydrate interactions in cell recognition. Curr. Opin. Struct. Biol. 14, 631-637 (2004). (Pubitemid 39328091)
4. Handa, K. & Hakomori, S.-I. Carbohydrate to carbohydrate interaction in development process and cancer progression. Glycoconj. J. 29, 627-637 (2012).
5. Pincet, F. et al. Ultraweak sugar-sugar interactions for trancient cell adhesion. Biophys. J. 80, 1354-1358 (2001). (Pubitemid 32182159)
6. Eggens, I. et al. Specific interaction between Lex and Lex determinants. J. Biol. Chem. 264, 9476-9484 (1989).
7. Fenderson, B. A., Zehavi, U. & Hakomori, S.-I. A multivalent lacto-Nfucopentaose III-lysyllysine conjugate decompacts preimplantation mouse embryos, while the free oligosaccharide is ineffective. J. Exp. Med. 160, 1591-1596 (1984). (Pubitemid 15220786)
8. Todeschini, A. G. & Hakomori, S.-I. Functional role of glycosphingolipids and gangliosides in control of cell adhesion, motility, and growth, through glycosynaptic microdomains. Biochim. Biophys. Acta 1780, 421-433 (2008).
9. Kojima, N. et al. Cell adhesion in a dynamic flow system as compared to static system. J. Biol. Chem. 267, 17261-17270 (1992).
10. Kojima, N. et al. Further studies on cell adhesion based on Lex-Lex interaction, with new approaches: embryoglycan aggregation of F9 teratocarcinoma cells, and adhesion of various tumour cells based on Lex expression. Glycoconj. J. 11, 238-248 (1994). (Pubitemid 24300506)
11. Gege, C., Geyer, A. & Schmidt, R. R. Carbohydrate-carbohydrate recognition between Lewis X blood broup antigens, bediated by calcium ions. Eur. J. Org. Chem. 2475-2485 (2002).
12. Geyer, A., Gege, C. & Schmidt, R. R. Carbohydrate-carbohydrate recognition between Lewisx glycoconjugates. Angew. Chem. Int. Ed. 38, 1466-1468 (1999).
13. Geyer, A., Gege, C. & Schmidt, R. R. Calcium dependent carbohydratecarbohydrate recognition between Lewisx blood group antigens. Angew. Chem. Int. Ed. 39, 3245-3249 (2000).
14. Gourier, C. et al. Specific and non specific interactions involving Lex determinant quantified by lipid vesicles micromanipulation. Glycoconj. J. 21, 165-174 (2004). (Pubitemid 39382661)
15. Gourier, C. et al. The natural Lewisx-beraing lipids promote membrane adhesion: influence of ceramide on carbohydrate-carbohydrate recognition. Angew. Chem. Int. Ed. 44, 1683-1687 (2005).
16. Siuzdak, G. et al. Evidence of Ca21-dependent carbohydrate associations through ion spray mass spectrometry. J. Am. Chem. Soc. 115, 2877-2881 (1993).
17. Tromas, C. et al. Adhesion forces between Lewisx determinant antigens as measured by atomic force microscopy. Angew. Chem. Int. Ed. 40, 3052-3055 (2001). (Pubitemid 32802949)
18. de la Fuente, J. M. & Penade, J. Understanding carbohydrate- carbohydrate interactions by means of glyconanotechnology. Glycoconj. J. 21, 149-163 (2004). (Pubitemid 39382660)
19. Hernaz, M. J., de la Fuente, J. M., Barrientos, A. G. & Penade, J. A model system mimicking glycosphingolipid clusters to quantify carbohydrate self-interactions by surface plasmon resonance. Angew. Chem. Int. Ed. 41, 1554-1557 (2002). (Pubitemid 34534398)
20. McKibbin, J.M. et al. Lewis blood group fucolipids and their isomers from human and canine intestine. J. Biol. Chem. 257, 755-760 (1982). (Pubitemid 12110208)
21. Karlsson, K. A. & Larson, G. Molecular characterization of cell surface antigens of fetal tissue. Detailed analysis of glycosphingolipids of meconium of a human O Le(a-b1) secretor. J. Biol. Chem. 256, 3512-3524 (1981). (Pubitemid 11082519)
22. Briand, E., Zah, M., Svedhem, S., Kasemo, B. & Petronis, S. Combined QCM-D and EIS study of supported lipid bilayer formation and interaction with poreforming peptides. Analyst 135, 343-350 (2010).
23. Janshoff, A. & Steinem, C. Transport across artificial membranes-an analytical perspective. Anal. Bioanal. Chem. 385, 433-451 (2006). (Pubitemid 43791931)
24. Janshoff, A., Steinem, C., Sieber, M. & Galla, H.-J. Specific binding of peanut agglutinin to GM1-doped solid supported lipid bilayers investigated by shear wave resonator measurements. Eur. Biophys. J. 25, 105-113 (1996).
25. Glasmatar, K., Larsson, C., Ho, F. & Kasemo, B. Protein adsorption on supported phospholipid bilayers. J. Colloid Interface Sci. 246, 40-47 (2002). (Pubitemid 34969224)
26. Rydell, G. E., Dahlin, A. B., Ho, F. & Larson, G. QCM-D studies of human norovirus VLPs binding to glycosphingolipids in supported lipid bilayers reveal strain-specific characteristics. Glycobiology 19, 1176-1184 (2009).
27. Bally, M. et al. Interaction of single viruslike particles with vesicles containing glycosphingolipids. Phys. Rev. Letters 107, 188103 (2011).
28. Wikstro, A., Svedhem, S., Sivignon, M. & Kasemo, B. Real-time QCM-D monitoring of electrostatically driven lipid transfer between two lipid bilayer membranes. J. Phys. Chem. B 112, 14069-14074 (2008).
29. Kunze, A., Svedhem, S. & Kasemo, B. Lipid transfer between charged supported lipid bilayers and oppositely charged vesicles. Langmuir 25, 5146-5158 (2009).
30. Andersson, A.-S., Glasmatar, K., Sutherland, D., Lidberg, U. & Kasemo, B. Cell adhesion on supported lipid bilayers. J. Biomed. Mater. Res., Part A 64, 622-629 (2003). (Pubitemid 37517297)
31. Svedhem, S. et al. In situ peptide-modified supported lipid bilayers for controlled cell attachment. Langmuir 19, 6730-6736 (2003).
32. Lorenz, B. et al. Model system for cell adhesion mediated by weak carbohydrate2carbohydrate interactions. J. Am. Chem. Soc. 134, 3326-3329 (2012).
33. Gunnarsson, A. et al. Kinetics of ligand binding to membrane receptors from equilibrium fluctuation analysis of single binding events. J. Am. Chem. Soc. 133, 14852-14855 (2011).
34. Gunnarsson, A., Josson, P., Marie, R., Tegenfeldt, J. O. & Ho, F. Singlemolecule detection and mismatch discrimination of unlabled DNA targets. Nano Lett. 8, 183-188 (2007).
35. Gunnarsson, A., Josson, P., Zhdanov, V. P. & Ho, F. Kinetic and thermodaynamic characterization of single-mismatch discrimination using single-molecule imaging. Nucleic Acids Res. 37, e99 (2009).
36. Alberts, B. et al. In Molecular Biology of the Cell Ch. 10, Garland Science, (2002).
37. Lingwood, D. et al. Cholesterol modulates glycolipid conformation and receptor activity. Nat. Chem. Biol. 7, 260-262 (2011).
38. Filippov, A., Orad, G. & Lindblom, G. Influence of cholesterol and water content on phospholipid lateral diffusion in bilayers. Langmuir 19, 6397-6400 (2003).
39. Lin, W.-C., Blanchette, C. D. & Longo, M. L. Fluid-phase chain unsaturation controlling domain microstructure and phase in ternary lipid bilayers containing GalCer and cholesterol. Biophys. J. 92, 2831-2841 (2007). (Pubitemid 46557857)
40. Stroberg, N., Nyholm, P. G., Pascher, I. & Normark, S. Saccharide orientation at the cell surface affects glycolipid receptor function. Proc. Natl. Acad. Sci. USA 88, 9340-9344 (1991). (Pubitemid 21915627)
41. Smith, A.-S., Vesicles as a model for controlled (de-)adhesion of cells: a thermodynamic approach. Softmatter 3, 275-289 (2007).
42. Fenz, S. F. et al. Switching from Ultraweak to Strong Adhesion. Adv. Mater. 23, 2622-2626 (2011).
43. Almeida, P. F. F. Thermodynamics of lipid interactions in complex bilayers. Biochim. Biophys. Acta 1788, 72-85 (2009).
44. J, R., S. Role of cholesterol in lipid raft formation: lessons from lipid model systems. Biochim. Biophys. Acta 1610, 174-183 (2003).
45. Mashaghi, A., Swann, M., Popplewell, J., Textor, M. & Reimhult, E. Optical anisotropy of supported lipid structures probed by waveguide spectroscopy and its application to study of supported lipid bilayer formation kinetics. Anal. Chem. 80, 3666-3676 (2008). (Pubitemid 351705866)
46. Kunze, A., Zhao, F., Marel, A.-K., Svedhem, S. & Kasemo, B. Ion-mediated changes of supported lipid bilayers and their coupling to the substrate. A case of bilayer slip? Softmatter 7, 8582-8591 (2011).
47. Garcia-Manyes, S., Oncins, G. & Sanz, F. Effect of pH and ionic strength on phospholipid nanomechanics and on deposition process onto hydrophilic surfaces measured by AFM. Electrochim. Acta 51, 5029-5036 (2006). (Pubitemid 43927714)
48. Binder, H. & Zschonig, O. The effect of metal cations on the phase behavior and hydration characteristics of phospholipid membranes. Chem. Phys. Lipids 115, 39-61 (2002). (Pubitemid 34621168)
49. Nieh, M. P., Harroun, T. A., Raghunathan, V. A., Glinka, C. J. & Katsaras, J. Spontaneously formed monodisperse biomimetic unilamellar vesicles: The effect of charge, dilution, and time. Biophys. J. 86, 2615-2629 (2004). (Pubitemid 38524447)
50. Tamura-Lis, W., Reber, E. J., Cunningham, B. A., Collins, J. M. & Lis, L. J. Ca21 induced phase separations in phospholipid mixtures. Chem. Phys. Lipids 39, 119-124 (1986). (Pubitemid 16170285)
51. Hope, M. J., Bally, M. B.,Webb, G. & Cullis, P. R. Production of large unilamellar vesicles by a rapid extrusion procedure. Characterization of size distribution, trapped volume and ability to maintain a membrane potential. Biochim. Biophys. Acta 812, 55-65 (1985). (Pubitemid 15159822)
52. Potanin, A. A., Verkhusha, V. V., Belokoneva, O. S. & Wiegel, F. W. Kinetics of ligand binding to a cluster of membrane-associated receptors. Eur. Biophys. J. 23, 197-205 (1994). (Pubitemid 24275237)