Milk sphingomyelin domains in biomimetic membranes and the role of cholesterol: Morphology and nanomechanical properties investigated using AFM and force spectroscopy

Langmuir

Volumn 30, Issue 22, 2014, Pages 6516-6524

  Guyomarc'H, Fanny ^a   Zou, Shan ^b   Chen, Maohui ^b   Milhiet, Pierre Emmanuel ^c   Godefroy, Cédric ^c   Vié, Véronique ^d   Lopez, Christelle ^a  

^a UMR1253   (France)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c CENTRE DE BIOCHIMIE STRUCTURALE   (France)

^d UNIVERSITÉ DE RENNES 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMIC FORCE MICROSCOPY; BIOMIMETICS; LIPID BILAYERS; MECHANICAL PROPERTIES; MORPHOLOGY; OILS AND FATS; PHOSPHOLIPIDS;

BIOMIMETIC MEMBRANE; BIOPHYSICAL PROPERTIES; DIOLEOYLPHOSPHATIDYLCHOLINE; FUNCTIONAL PROPERTIES; MORPHOLOGY AND MECHANICAL PROPERTIES; NANOMECHANICAL PROPERTY; STRUCTURAL AND MECHANICAL PROPERTIES; SUPPORTED LIPID BILAYERS;

CHOLESTEROL;

1,2-OLEOYLPHOSPHATIDYLCHOLINE; ARTIFICIAL MEMBRANE; CHOLESTEROL; PHOSPHATIDYLCHOLINE; SPHINGOMYELIN;

ANIMAL; ARTIFICIAL MEMBRANE; ATOMIC FORCE MICROSCOPY; BIOMIMETICS; CHEMISTRY; PROCEDURES;

ANIMALS; BIOMIMETICS; CHOLESTEROL; MEMBRANES, ARTIFICIAL; MICROSCOPY, ATOMIC FORCE; PHOSPHATIDYLCHOLINES; SPHINGOMYELINS;

EID: 84902182054     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la501640y     Document Type: Article

References (49)

1. Dewettinck, K.; Rombaut, R.; Thienpont, N.; Trung Le, T.; Messens, K.; van Camp, J. Nutritional and technological aspects of milk fat globule membrane material Int. Dairy J. 2008, 18, 436-457
2. 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
3. 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
4. Gallier, S.; Gragson, D.; Jiménez-Flores, R.; Everett, D. W. Using Confocal Laser Scanning Microscopy To Probe the Milk Fat Globule Membrane and Associated Proteins J. Agric. Food Chem. 2010, 58, 4250-4257
5. 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
6. Lopez, C.; Briard-Bion, V.; Ménard, O.; Beaucher, E.; Rousseau, F.; Fauquant, J.; Leconte, N.; Robert, B. Fat globules selected from whole milk according to their size: different compositions and structure of the biomembrane, revealing sphingomyelin-rich domains Food Chem. 2011, 125, 355-368
7. 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
8. 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
9. Simons, K.; Ikonen, E. Functional rafts in cell membranes Nature 1997, 5, 569-572
10. Simons, K.; Ikonen, E. How cells handle cholesterol Science 2000, 290, 1721-1726
11. van Meer, G. Caveolin, Cholesterol, and Lipid Droplets? J. Cell Biol. 2001, 152, F29-F34
12. Mather, I. H.; Keenan, T. W. Origin and secretion of milk lipids J. Mammary Gland Biol. Neoplasia 1998, 3, 259-273
13. Halling, K. K.; Ramstedt, B.; Nyström, J. H.; Slotte, J. P.; Nyholm, T. K. M. Cholesterol interactions with fluid-phase phospholipids: Effect on the lateral organization of the bilayer Biophys. J. 2008, 95, 3861-3871
14. Simons, K.; Vaz, W. L. C. Model systems, lipid rafts, and cell membranes Annu. Rev. Biophys. Biomol. Struct. 2004, 33, 269-295
15. Mesilati-Stahy, R.; Argov-Argaman, N. The relationship between size and lipid composition of the bovine milk fat globule is modulated by lactation stage Food Chem. 2014, 145, 562-570
16. Quinn, P. J. Plasma membrane phospholipid asymmetry Subcell. Biochem. 2002, 36, 39-60
17. Zachowski, A. Phospholipids in animal eukaryotic membranes: Transverse asymmetry and movement Biochem. J. 1993, 294, 1-14
18. Shaw, K. P.; Brooks, N. J.; Clarke, J. A.; Ces, O.; Seddon, J. M.; Law, R. V. Pressure-temperature phase behaviour of natural sphingomyelin extracts Soft Matter 2012, 8, 1070-1078
19. Filippov, A.; Munavirov, B.; Gröbner, G.; Rudakova, M. Lateral diffusion in equimolar mixtures of natural sphingomyelins with dioleoylphosphatidylcholine Magn. Reson. Imaging 2012, 30, 413-421
20. Weeraman, C.; Chen, M.; Moffatt, D. J.; Lausten, R.; Stolow, A.; Johnston, L. J. A combined vibrational sum frequency generation spectroscopy and atomic force microscopy study of sphingomyelin-cholesterol monolayers Langmuir 2012, 28, 12999-13007
21. Dufrêne, Y. F.; Pelling, A. E. Force nanoscopy of cell mechanics and cell adhesion Nanoscale 2013, 5, 4094-4104
22. Balasuriya, T. S.; Ong, L.; Gras, S. L.; Dagastine, R. R. Changes in morphological and nano-mechanical properties of the milk fat globule membrane during processing R. Soc. Chem. Adv. 2012, 2, 2384-2394
23. 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
24. Gallier, S.; Gragson, D.; Jiménez-Flores, R.; Everett, D. W. β-Casein-phospholipid monolayers as model systems to understand lipid-protein interactions in the milk fat globule membrane Int. Dairy J. 2012, 22, 58-65
25. Jiménez-Flores, R.; Brisson, G. The milk fat globule membrane as an ingredient: Why, how, when? Dairy Sci. Technol. 2008, 88, 5-18
26. Czolkos, I.; Jesorka, A.; Orwar, O. Molecular phospholipid films on solid supports Soft Matter 2011, 7, 4562-4576
27. Garcia-Manyes, S.; Sanz, F. Nanomechanics of lipid bilayers by force spectroscopy with AFM: A perspective Biochim. Biophys. Acta 2010, 1798, 741-749
28. Giocondi, M.-C.; Yamamoto, D.; Lesniewska, E.; Milhiet, P.-E.; Ando, T.; Le Grimellec, C. Surface topography of membrane domains Biochim. Biophys. Acta 2010, 1798, 703-718
29. Zou, S.; Johnston, L. J. Ceramide-enriched microdomains in planar membranes Curr. Opin. Colloid Interface Sci. 2010, 15, 489-498
30. 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
31. 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
32. Malmsten, M.; Bergenståhl, B.; Nyberg, L.; Odham, G. Sphingomyelin from milk-characterization of liquid crystalline, liposome, and emulsion properties J. Am. Oil Chem. Soc. 1994, 71, 1021-1026
33. Fritzsching, K. J.; Kim, J.; Holland, G. P. Probing lipid-cholesterol interactions in DOPC/eSM/Chol and DOPC/DPPC/Chol model lipid rafts with DSC and 13C solid-state NMR Biochim. Biophys. Acta 2013, 1828, 1889-1898
34. 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
35. Seeger, H. M.; Di Cerbo, A.; Alessandrini, A.; Facci, P. Supported lipid bilayers on mica and silicon oxide: comparison of the main phase transition behavior J. Phys. Chem. B 2010, 114, 8926-8933
36. Lawrence, J. C.; Saslowski, D. E.; Edwardson, J. M.; Henderson, R. M. Real-time analysis of the effects of cholesterol on lipid raft behavior using atomic force microscopy Biophys. J. 2003, 84, 1827-1832
37. Rinia, H. A.; Snelb, M. M. E.; van der Eerdenb, J. P. J. M.; de Kruijff, B. Visualizing detergent resistant domains in model membranes with atomic force microscopy FEBS Lett. 2001, 501, 92-96
38. 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
39. 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
40. Milhiet, P.-E.; Giocondi, M.-C.; Le Grimellec, C. Cholesterol is not crucial for the existence of microdomains in kidney brush-border membrane models J. Biol. Chem. 2002, 277, 875-878
41. Goksu, E. I.; Vanegas, J. M.; Blanchette, C. D.; Lin, W.-C.; Longo, M. L. AFM for structure and dynamics of biomembranes Biochim. Biophys. Acta 2009, 1788, 254-266
42. Giocondi, M.-C.; Boichot, S.; Plénat, T.; Le Grimellec, C. Structural diversity of sphingomyelin microdomains Ultramicroscopy 2004, 100, 135-143
43. Milhiet, P.-E.; Vié, V.; Giocondi, M.-C.; Le Grimellec, C. AFM characterization of model rafts in supported bilayers Single Mol. 2001, 2, 119-121
44. Zhong, J.; Yang, C.; Zheng, W.; Huang, L.; Hong, Y.; Wang, L.; Sha, Y. Effect of lipid composition and phase on membrane interaction of the prion peptide 106-126 amide Biophys. J. 2009, 96, 4610-4621
45. Popov, J.; Vobornik, D.; Coban, O.; Keating, E.; Miller, D.; Francis, J.; Petersen, N. O.; Johnston, L. J. Chemical mapping of ceramide distribution in sphingomyelin-rich domains in monolayers Langmuir 2008, 24, 13502-13508
46. Chiantia, S.; Ries, J.; Kahya, N.; Schwille, P. Combined AFM and two-focus SFCS study of raft-exhibiting model membranes ChemPhysChem 2006, 7, 2409-2418
47. Li, X.-M.; Momsen, M. M.; Smaby, J. M.; Brockman, H. L.; Brown, R. E. Cholesterol decreases the interfacial elasticity and detergent solubility of sphingomyelins Biochemistry 2001, 40, 5954-5963
48. Wang, T.; Shogomori, H.; Hara, M.; Yamada, T.; Kobayashi, T. Nanomechanical recognition of sphingomyelin-rich membrane domains by atomic force microscopy Biochemistry 2012, 51, 74-82
49. Li, X.-M.; Momsen, M. M.; Brockman, H. L.; Brown, R. E. Sterol structure and sphingomyelin acyl chain length modulate lateral packing elasticity and detergent solubility in model membranes Biophys. J. 2003, 85, 3788-3801