Cholesterol Decreases the Size and the Mechanical Resistance to Rupture of Sphingomyelin Rich Domains, in Lipid Bilayers Studied as a Model of the Milk Fat Globule Membrane

Langmuir

Volumn 32, Issue 26, 2016, Pages 6757-6765

  Murthy, Appala Venkata Ramana ^a   Guyomarc'H, Fanny ^a   Lopez, Christelle ^a  

^a AGROCAMPUS OUEST   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMIC FORCE MICROSCOPY; BIOLOGICAL MEMBRANES; CHOLESTEROL; CYTOLOGY; OILS AND FATS; PHOSPHOLIPIDS; X RAY DIFFRACTION;

FOOD EMULSIONS; FORCE SPECTROSCOPY; FUNCTIONAL RELEVANCE; MECHANICAL RESISTANCE; MICRO-DOMAINS; MILK FAT GLOBULES; ORDERED DOMAINS; SPHINGOMYELIN;

LIPID BILAYERS;

CHOLESTEROL; GLYCOLIPID; GLYCOPROTEIN; MILK FAT GLOBULE; SPHINGOMYELIN;

CHEMISTRY; LIPID BILAYER; MEMBRANE MICRODOMAIN;

CHOLESTEROL; GLYCOLIPIDS; GLYCOPROTEINS; LIPID BILAYERS; MEMBRANE MICRODOMAINS; SPHINGOMYELINS;

EID: 84978174459     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/acs.langmuir.6b01040     Document Type: Article

References (64)

1. Maxfield, F. R.; van Meer, G. Cholesterol, the central lipid of mammalian cells Curr. Opin. Cell Biol. 2010, 22, 422-429 10.1016/j.ceb.2010.05.004
2. Silvius, J. R. Role of cholesterol in lipid raft formation: lessons from lipid model systems Biochim. Biophys. Acta, Biomembr. 2003, 1610, 174-183 10.1016/S0005-2736(03)00016-6
3. Simons, K.; Ikonen, E. How cells handle cholesterol Science 2000, 290, 1721-1726 10.1126/science.290.5497.1721
4. Simons, K.; Ikonen, E. Functional rafts in cell membranes Nature 1997, 387, 569-572 10.1038/42408
5. Yeagle, P. L. Cholesterol and the cell membrane Biochim. Biophys. Acta, Rev. Biomembr. 1985, 822, 267-287 10.1016/0304-4157(85)90011-5
6. Mather, I. H.; Keenan, T. W. Origin and secretion of milk lipids Journal of Mammary Gland Biology and Neoplasia 1998, 3, 259-273 10.1023/A:1018711410270
7. Keenan, T. W.; Morré, D. J.; Olson, D. E.; Yunghans, W. N.; Stuart, P. Biochemical and morphological comparison of plasma membrane and milk fat globule membrane from bovine mammary gland J. Cell Biol. 1970, 44, 80-93 10.1083/jcb.44.1.80
8. Dewettinck, K.; Rombaut, R.; Thienpont, N.; Le, T. T.; Messens, K.; van Camp, J. Nutritional and technological aspects of milk fat globule membrane material Int. Dairy J. 2008, 18, 436-457 10.1016/j.idairyj.2007.10.014
9. Lopez, C. Milk fat globules enveloped by their biological membrane: Unique colloidal assemblies with a specific composition and structure Curr. Opin. Colloid Interface Sci. 2011, 16, 391-404 10.1016/j.cocis.2011.05.007
10. Murthy, A. V. R.; Guyomarc'h, F.; Paboeuf, G.; Vié, V.; Lopez, C. Cholesterol strongly affects the organization of lipid layers studied as models of the milk fat globule membrane: condensing effect and change in the lipid domain morphology Biochim. Biophys. Acta, Biomembr. 2015, 1848, 2308-2316 10.1016/j.bbamem.2015.06.014
11. Deeth, H. C. The role of phospholipids in the stability of milk fat globules Aust. J. Dairy Technol. 1997, 52, 44-46
12. Jensen, R. G.; Newburg, D. S. Bovine milk lipids. In Handbook of Milk Composition; Jensen, R. G., Ed.; Academic Press: New York, 1995; 543-575.
13. Evers, J. M.; Haverkamp, R. G.; Holroyd, S. E.; Jameson, G. B.; Mackenzie, D. D. S.; McCarthy, O. J. Heterogeneity of milk fat globule membrane structure and composition as observed using fluorescence microscopy techniques Int. Dairy J. 2008, 18, 1081-1089 10.1016/j.idairyj.2008.06.001
14. Gallier, S.; Gragson, D.; Jiménez-Flores, R.; Everett, D. W. Surface characterization of bovine milk phospholipid monolayers by Langmuir isotherms and microscopic techniques J. Agric. Food Chem. 2010, 58, 12275-12285 10.1021/jf102185a
15. Lopez, C.; Madec, M.-N.; Jiménez-Flores, R. Lipid rafts in the bovine milk fat globule membrane revealed by the lateral segregation of phospholipids and heterogeneous distribution of glycoproteins Food Chem. 2010, 120, 22-33 10.1016/j.foodchem.2009.09.065
16. Lopez, C.; Ménard, O. Human milk fat globules: Polar lipid composition and in situ structural investigations revealing the heterogeneous distribution of proteins and the lateral segregation of sphingomyelin in the biological membrane Colloids Surf., B 2011, 83, 29-41 10.1016/j.colsurfb.2010.10.039
17. Nguyen, H. T. H.; Ong, L.; Beaucher, E.; Madec, M.-N.; Kentish, S.; Gras, S. L.; Lopez, C. Buffalo milk fat globules and their biological membrane: in situ structural investigations Food Res. Int. 2015, 67, 35-43 10.1016/j.foodres.2014.10.022
18. Zou, X.-Q.; Guo, Z.; Huang, J.-H.; Jin, Q.-Z.; Cheong, L.-Z.; Wang, X.-G.; Xu, X.-B. Human milk fat globules from different stages of lactation: a lipid composition analysis and microstructure characterization J. Agric. Food Chem. 2012, 60, 7158-7167 10.1021/jf3013597
19. Zou, X.-Q.; Guo, Z.; Jin, Q.-Z.; Huang, J.-H.; Cheong, L.-Z.; Xu, X.-B.; Wang, X.-G. Composition and microstructure of colostrum and mature bovine milk fat globule membrane Food Chem. 2015, 185, 362-370 10.1016/j.foodchem.2015.03.145
20. Nguyen, H. T. H.; Madec, M.-N.; Ong, L.; Kentish, S. E.; Gras, S. L.; Lopez, C. The dynamics of the biological membrane surrounding the buffalo milk fat globule investigated as a function of temperature Food Chem. 2016, 204, 343-351 10.1016/j.foodchem.2016.02.141
21. Alessandrini, A.; Seeger, H. M.; Di Cerbo, A.; Caramaschi, T.; Facci, P. What do we really measure in AFM punch-through experiments on supported lipid bilayers? Soft Matter 2011, 7, 7054-7064 10.1039/c1sm05453h
22. Alessandrini, A.; Seeger, H. M.; Caramaschi, T.; Facci, P. Dynamic force spectroscopy on supported lipid bilayers: effect of temperature and sample preparation Biophys. J. 2012, 103, 38-47 10.1016/j.bpj.2012.05.039
23. Dufrêne, Y. F.; Barger, W. R.; Green, J.-B. D.; Lee, G. U. Nanometer-scale surface properties of mixed phospholipid monolayers and bilayers Langmuir 1997, 13, 4779-4784 10.1021/la970221r
24. Garcia-Manyes, S.; Sanz, F. Nanomechanics of lipid bilayers by force spectroscopy with AFM: A perspective Biochim. Biophys. Acta, Biomembr. 2010, 1798, 741-749 10.1016/j.bbamem.2009.12.019
25. Li, J. K.; Sullan, R. M. A.; Zou, S. Atomic force microscopy force mapping in the study of supported lipid bilayers Langmuir 2011, 27, 1308-1313 10.1021/la103927a
26. Guyomarc'h, F.; Zou, S.; Chen, M.; Milhiet, P.-E.; Godefroy, C.; Vié, V.; Lopez, C. Milk sphingomyelin domains in biomimetic membranes and the role of cholesterol: morphology and nanomechanical properties investigated using AFM and force spectroscopy Langmuir 2014, 30, 6516-6524 10.1021/la501640y
27. Sanchez-Juanes, F.; Alonso, J. M.; Zancada, L.; Hueso, P. Distribution and fatty acid content of phospholipids from bovine milk and bovine milk fat globule membranes Int. Dairy J. 2009, 19, 273-278 10.1016/j.idairyj.2008.11.006
28. Blanton, T. N.; Barnes, C. N.; Lelental, M. Preparation of silver behenate coatings to provide low- to mid-angle diffraction calibration J. Appl. Crystallogr. 2000, 33, 172-173 10.1107/S0021889899012388
29. Alessandrini, A.; Facci, P. Phase transition in supported lipid bilayers studied by AFM Soft Matter 2014, 10, 7145-7164 10.1039/C4SM01104J
30. Chemin, C.; Bourgaux, C.; Pean, J.-M.; Pabst, G.; Wuthrich, P.; Couvreur, P.; Ollivon, M. Consequences of ions and pH on the supramolecular organization of sphingomyelin and sphingomyelin/cholesterol bilayers Chem. Phys. Lipids 2008, 153, 119-129 10.1016/j.chemphyslip.2008.03.002
31. Maulik, P. R.; Shipley, G. G. Interactions of N-stearoyl sphingomyelin with cholesterol and dipalmitoylphosphatidylcholine in bilayer membranes Biophys. J. 1996, 70, 2256-2265 10.1016/S0006-3495(96)79791-6
32. McMullen, T. P. W.; Lewis, R. N. A. H.; McElhaney, R. N. Cholesterol-phospholipid interactions, the liquid-ordered phase and lipid rafts in model and biological membranes Curr. Opin. Colloid Interface Sci. 2004, 8, 459-468 10.1016/j.cocis.2004.01.007
33. Butt, H.-J.; Cappella, B.; Kappl, M. Force measurements with the atomic force microscope: technique, interpretation and applications Surf. Sci. Rep. 2005, 59, 1-152 10.1016/j.surfrep.2005.08.003
34. Lopez, C.; Cauty, C.; Guyomarc'h, F. Organization of lipids in milk, infant formulas and various dairy products: role of technological processes and potential impacts Dairy Sci. Technol. 2015, 95, 863-895 10.1007/s13594-015-0263-0
35. Redondo-Morata, L.; Giannotti, M. I.; Sanz, F. Structural impact of cations on lipid bilayer models: nanomechanical properties by AFM-force spectroscopy Mol. Membr. Biol. 2014, 31, 17-28 10.3109/09687688.2013.868940
36. 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 10.1016/S0006-3495(03)74664-5
37. Feigenson, G. W. Phase diagrams and lipid domains in multicomponents lipid bilayer mixtures Biochim. Biophys. Acta, Biomembr. 2009, 1788, 47-52 10.1016/j.bbamem.2008.08.014
38. Filippov, A.; Öradd, G.; Lindblom, G. Sphingomyelin structure influences the lateral diffusion and raft formation in lipid bilayers Biophys. J. 2006, 90, 2086-2092 10.1529/biophysj.105.075150
39. Veatch, S. L.; Keller, S. L. Seeing spots: complex phase behavior in simple membranes Biochim. Biophys. Acta, Mol. Cell Res. 2005, 1746, 172-185 10.1016/j.bbamcr.2005.06.010
40. Veatch, S. L.; Soubias, O.; Keller, S. L.; Gawrisch, K. Critical fluctuation in domain-forming mixtures Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 17650-17655 10.1073/pnas.0703513104
41. 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 10.1021/la900395w
42. Reyes Mateo, C.; Ulises Acuna, A.; Brochon, J. C. Liquid-crystalline phases of cholesterol lipid bilayers as revealed by the fluorescence of trans-parinaric acid Biophys. J. 1995, 68, 978-987 10.1016/S0006-3495(95)80273-0
43. Blanchette, C. D.; Lin, W.-C.; Orme, C. A.; Ratto, T. V.; Longo, M. L. Domain nucleation rates and interfacial line tensions in supported bilayers of ternary mixtures containing galactosylceramide Biophys. J. 2008, 94, 2691-2697 10.1529/biophysj.107.122572
44. García-Sáez, A. J.; Chiantia, S.; Schwille, P. Effect of line tension on the lateral organization of lipid membranes J. Biol. Chem. 2007, 282, 33537-33544 10.1074/jbc.M706162200
45. Tokumasu, F.; Jin, A. J.; Feigenson, G. W.; Dvorak, J. A. Nanoscopic lipid domains dynamics revealed by atomic force microscopy Biophys. J. 2003, 84, 2609-2618 10.1016/S0006-3495(03)75066-8
46. Frolov, V. A. J.; Chizmadzhev, Y. A.; Cohen, F. S.; Zimmerberg, J. "Entropic traps" in the kinetics of phase separation in multicomponent membranes stabilize nanodomains Biophys. J. 2006, 91, 189-205 10.1529/biophysj.105.068502
47. Simons, K.; Vaz, W. L. C. Model systems, lipid rafts, and cell membranes Annu. Rev. Biophys. Biomol. Struct. 2004, 33, 269-295 10.1146/annurev.biophys.32.110601.141803
48. Rinia, H. A.; Snel, M. M. E.; van der Eerden, J. P. J. M.; de Kruijff, B. Visualizing detergent resistant domains in model membranes with atomic force microscopy FEBS Lett. 2001, 501, 92-96 10.1016/S0014-5793(01)02636-9
49. Sullan, R. M. A.; Li, J. K.; Hao, C.; Walker, G. C.; Zou, S. Cholesterol-dependent nanomechanical stability of phase-segregated multicomponent lipid bilayers Biophys. J. 2010, 99, 507-516 10.1016/j.bpj.2010.04.044
50. Milhiet, P.-E.; Domec, C.; Giocondi, M.-C.; van Mau, N.; Heitz, F.; Le Grimellec, C. Domain formation in models of the renal brush border membrane outer leaflet Biophys. J. 2001, 81, 547-555 10.1016/S0006-3495(01)75721-9
51. Dols-Perez, A.; Fumagalli, L.; Gomila, G. Structural and nanomechanical effects of cholesterol in binary and ternary spin-coated single lipid bilayers in dry conditions Colloids Surf., B 2014, 116, 295-302 10.1016/j.colsurfb.2013.12.049
52. Redondo-Morata, L.; Giannotti, M. I.; Sanz, F. Influence of cholesterol on the phase transition of lipid bilayers: A temperature-controlled force spectroscopy study Langmuir 2012, 28, 12851-12860 10.1021/la302620t
53. An, H.; Nussio, M. R.; Huson, M. G.; Voelcker, N. H.; Shapter, J. G. Material properties of lipid microdomains: force-volume imaging study of the effect of cholesterol on lipid microdomain rigidity Biophys. J. 2010, 99, 834-844 10.1016/j.bpj.2010.04.072
54. Gumí-Audenis, B.; Sanz, F.; Giannotti, M. I. Impact of galactosylceramides on the nanomechanical properties of lipid bilayer models: an AFM-force spectroscopy study Soft Matter 2015, 11, 5447-5454 10.1039/C5SM01252J
55. Redondo-Morata, L.; Giannotti, M. I.; Sanz, F. Influence of cholesterol on the phase transition of lipid bilayers: A temperature-controlled force spectroscopy study Langmuir 2012, 28, 12851-12860 10.1021/la302620t
56. Shaikh, S. R.; Dumaual, A. C.; Jenski, L. J.; Stillwell, W. Lipid phase separation in phospholipid bilayers and monolayers modeling the plasma membrane Biochim. Biophys. Acta, Biomembr. 2001, 1512, 317-328 10.1016/S0005-2736(01)00335-2
57. Smaby, J. M.; Brockman, H. L.; Brown, R. E. Cholesterol's interfacial interactions with sphingomyelins and phosphatodylcholines: hydrocarbon chain structure determines the magnitude of condensation Biochemistry 1994, 33, 9135-9142 10.1021/bi00197a016
58. Brown, D. A.; London, E. Structure of detergent-resistant membrane domains: does phase separation occur in biological membranes? Biochem. Biophys. Res. Commun. 1997, 240, 1-7 10.1006/bbrc.1997.7575
59. Smaby, J. M.; Momsen, M. M.; Brockman, H. L.; Brown, R. E. Phosphatidylcholine acyl unsaturation modulates the decrease in interfacial elasticity induced by cholesterol Biophys. J. 1997, 73, 1492-1505 10.1016/S0006-3495(97)78181-5
60. McElhaney, R. N. The use of differential scanning calorimetry and differential thermal analysis in studies of model and biological membranes Chem. Phys. Lipids 1982, 30, 229-259 10.1016/0009-3084(82)90053-6
61. Chatterton, D. E. W.; Nguyen, D. N.; Bering, S. B.; Sangild, P. T. Anti-inflammatory mechanisms of bioactive milk proteins in the intestine of newborns Int. J. Biochem. Cell Biol. 2013, 45, 1730-1747 10.1016/j.biocel.2013.04.028
62. Garcia-Manyes, S.; Redondo-Morata, L.; Oncins, G.; Sanz, F. Nanomechanics of lipid bilayers: heads or tails? J. Am. Chem. Soc. 2010, 132, 12874-12886 10.1021/ja1002185
63. García-Arribas, A. B.; Busto, J. V.; Alonso, A.; Goni, F. M. Atomic force microscopy characterization of palmitoylceramide and cholesterol effects on phospholipid bilayers: a topographic and nanomechanical study Langmuir 2015, 31, 3135-3145 10.1021/la504047n
64. Shamitko-Klingensmith, N.; Molchanoff, K. M.; Burke, K. A.; Magnone, G. J.; Legleiter, J. Mapping the mechanical properties of cholesterol-containing supported lipid bilayers with nanoscale spatial resolution Langmuir 2012, 28, 13411-13422 10.1021/la302705f