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Structure of the Milk Fat Globule Membrane: New Scientific Advances Revealing the Role of Sphingomyelin in Topographical and Mechanical Heterogeneities

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Dairy Fat Products and Functionality

Abstract

 The milk fat globule membrane (MFGM) is a unique interface rich in polar lipids, cholesterol and proteins, bringing specific functions in the gastro-intestinal tract. In this book chapter, new scientific advances about the structure and mechanical properties of the MFGM are reviewed, in relation with the specific composition of this biological membrane and the physical properties of milk polar lipids that are mainly due to the high amount of sphingomyelin (SM). The MFGM is a patchwork of polar lipids with lateral phase separation of high melting temperature Tm saturated polar lipids such as milk-SM (Tm=34.3°C) leading to the formation of ordered microdomains that are higher and more rigid than the surrounding fluid matrix composed of low Tm unsaturated polar lipids in which the proteins are embeded. The microdomains are reactive to thermal kinetics and can diffuse in the plane of the MFGM. Attractive interactions between SM and cholesterol are involved in the formation of complexes in a wide range of temperatures (4 to 60°C). Structural and mechanical heterogeneities in the MFGM and in milk polar lipid assemblies have been evidenced. These recent information will contribute in a better undertanding of MFGM functions and open perspectives in the valorization of milk polar lipids and MFGM-rich ingredients for food and nutritional applications.

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References

  • Bhojoo, U., Chen, M., & Zou, S. (2018). Temperature induced lipid membrane restructuring and changes in nanomechanics. Biochimica et Biophysica Acta (BBA) - Biomembranes, 1860, 700–709.

    Article  CAS  Google Scholar 

  • Cheng, K., Ropers, M.-H., & Lopez, C. (2017). The miscibility of milk sphingomyelin and cholesterol is affected by temperature and surface pressure in mixed Langmuir monolayers. Food Chemistry, 224, 114–123.

    Article  CAS  PubMed  Google Scholar 

  • Deeth, H. C. (1997). The role of phospholipids in the stability of milk fat gobules. Australian Journal of Dairy Technology, 52, 44–46.

    CAS  Google Scholar 

  • Dewettinck, K., Rombaut, R., Thienpont, N., Le, T. T., Messens, K., & Van Camp, J. (2008). Nutritional and technological aspects of milk fat globule membrane material. International Dairy Journal, 18, 436–457.

    Article  CAS  Google Scholar 

  • Douellou, T., Montel, M. C., & Sergentet, D. T. (2017). Anti-adhesive properties of bovine oligosaccharides and bovine milk fat globule membrane-associated glycoconjugates against bacterial food enteropathogens. Journal of Dairy Science, 100, 3348–3359.

    Article  CAS  PubMed  Google Scholar 

  • Et-Thakafy, O., Delorme, N., Guyomarc’h, F., & Lopez, C. (2018). Mechanical properties of milk sphingomyelin bilayer membranes in the gel phase: Effects of naturally complex heterogeneity, saturation and acyl chain length investigated on liposomes using AFM. Chemistry and Physics of Lipids, 210, 47–59.

    Article  CAS  PubMed  Google Scholar 

  • Et-Thakafy, O., Guyomarc’h, F., & Lopez, C. (2017). Lipid domains in the milk fat globule membrane: Dynamics investigated in situ in milk in relation to temperature and time. Food Chemistry, 220, 352–361.

    Article  CAS  PubMed  Google Scholar 

  • Evers, J. M., Haverkamp, R. G., Holroyd, S. E., Jameson, G. B., Mackenzie, D. D. S., & McCarthy, O. J. (2008). Heterogeneity of milk fat globule membrane structure and composition as observed using fluorescence microscopy techniques. International Dairy Journal, 18, 1081–1089.

    Article  CAS  Google Scholar 

  • Gallier, S., Gragson, D., Jiménez-Flores, R., & Everett, D. (2010a). Using confocal laser scanning microscopy to probe the milk fat globule membrane and associated proteins. Journal of Agricultural and Food Chemistry, 58, 4250–4257.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallier, S., Gragson, D., Jiménez-Flores, R., & Everett, D. W. (2010b). Surface characterization of bovine milk phospholipid monolayers by Langmuir isotherms and microscopic techniques. Journal of Agricultural and Food Chemistry, 58, 12275–12285.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallier, S., Gragson, D., Jiménez-Flores, R., & Everett, D. W. (2012). β-Casein–phospholipid monolayers as model systems to understand lipid–protein interactions in the milk fat globule membrane. International Dairy Journal, 22, 58–65.

    Article  CAS  Google Scholar 

  • Gallier, S., Vocking, K., Post, J. A., Van de Heijning, B., Acton, D., Van der Beek, E. M., et al. (2015). A novel infant milk formula concept: Mimicking the human milk fat globule structure. Colloids and Surfaces. B, Biointerfaces, 136, 329–339.

    Article  CAS  PubMed  Google Scholar 

  • Garcia, C., Lutz, N. W., Confort-Gouny, S., Cozzone, P. J., Armand, M., & Bernard, M. (2012). Phospholipid fingerprints of milk from different mammalians determined by 31P NMR: Towards specific interest in human health. Food Chemistry, 135, 1777–1783.

    Article  CAS  PubMed  Google Scholar 

  • Giuffrida, F., Cruz-Hernandez, C., Flück, B., Tavazzi, I., Thakkar, S. K., Destaillats, F., et al. (2013). Quantification of phospholipids classes in human milk. Lipids, 48, 1051–1058.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guyomarc’h, F., Chen, M., Et-Thakafy, O., Zou, S., & Lopez, C. (2017). Gel-gel phase separation within milk sphingomyelin domains revealed at the nanoscale using atomic force microscopy. Biochimica et Biophysica Acta, Biomembranes, 1859, 949–958.

    Article  PubMed  CAS  Google Scholar 

  • Guyomarc’h, F., Zou, S., Chen, M., Milhiet, P.-E., Godefroy, C., Vie, V., et al. (2014). Milk sphingomyelin domains in biomimetic membranes and the role of cholesterol: Morphology and nanomechanical properties investigated using AFM and force spectroscopy. Langmuir, 30, 6516–6524.

    Article  PubMed  CAS  Google Scholar 

  • Heid, H. W., & Keenan, T. W. (2005). Intracellular origin and secretion of milk fat globules. European Journal of Cell Biology, 84, 245–258.

    Article  CAS  PubMed  Google Scholar 

  • Jiménez-Flores, R., & Brisson, G. (2008). The milk fat globule membrane as an ingredient: why, how, when? Dairy Science & Technology, 88, 5–18.

    Article  CAS  Google Scholar 

  • Liao, Y., Alvarado, R., Phinney, B., & Lönnerdal, B. (2011). Proteomic characterization of human milk fat globule membrane proteins during a 12 month lactation period. Journal of Proteome Research, 10, 3530–3541.

    Article  CAS  PubMed  Google Scholar 

  • Lopez, C. (2011). Milk fat globules enveloped by their biological membrane: Unique colloidal assemblies with a specific composition and structure. Current Opinion in Colloid & Interface Science, 16, 391–404.

    Article  CAS  Google Scholar 

  • Lopez, C., Briard-Bion, V., Beaucher, E., & Ollivon, M. (2008). Multiscale characterization of the organization of triglycerides and phospholipids in emmental cheese: From the microscopic to the molecular level. Journal of Agricultural and Food Chemistry, 56, 2406–2414.

    Article  CAS  PubMed  Google Scholar 

  • Lopez, C., Briard-Bion, V., & Ménard, O. (2014). Polar lipids, sphingomyelin and long-chain unsaturated fatty acids from the milk fat globule membrane are increased in milks produced by cows fed fresh pasture based diet during spring. Food Research International, 58, 59–68.

    Article  CAS  Google Scholar 

  • Lopez, C., Briard-Bion, V., Ménard, O., Beaucher, E., Rousseau, F., Fauquant, J., et al. (2011). Fat globules selected from whole milk according to their size: Different compositions and structure of the biomembrane, revealing sphingomyelin-rich domains. Food Chemistry, 125, 355–368.

    Article  CAS  Google Scholar 

  • Lopez, C., Briard-Bion, V., Menard, O., Rousseau, F., Pradel, P., & Besle, J.-M. (2008). Phospholipid, sphingolipid, and fatty acid compositions of the milk fat globule membrane are modified by diet. Journal of Agricultural and Food Chemistry, 56, 5226–5236.

    Article  CAS  PubMed  Google Scholar 

  • Lopez, C., Cauty, C., & Guyomarc’h, F. (2015). Organization of lipids in milks, infant milk formulas and various dairy products: Role of technological processes and potential impacts. Dairy Science & Technology, 95, 863–893.

    Article  CAS  Google Scholar 

  • Lopez, C., Cauty, C., & Guyomarc’h, F. (2019). Unraveling the complexity of milk fat globules to tailor bioinspired emulsions providing health benefits: The key role played by the biological membrane. European Journal of Lipid Science and Technology, 121, 1800201.

    Google Scholar 

  • Lopez, C., Cauty, C., Rousseau, F., Blot, M., Margolis, A., & Famelart, M.-H. (2017). Lipid droplets coated with milk fat globule membrane fragments: Microstructure and functional properties as a function of pH. Food Research International, 91, 26–37.

    Article  CAS  PubMed  Google Scholar 

  • Lopez, C., Cheng, K., & Perez, J. (2018). Thermotropic phase behavior of milk sphingomyelin and role of cholesterol in the formation of the liquid ordered phase examined using SR-XRD and DSC. Chemistry and Physics of Lipids, 215, 46–55.

    Article  CAS  PubMed  Google Scholar 

  • Lopez, C., Madec, M.-N., & Jimenez-Flores, R. (2010). Lipid rafts in the bovine milk fat globule membrane revealed by the lateral segregation of phospholipids and heterogeneous distribution of glycoproteins. Food Chemistry, 120, 22–33.

    Article  CAS  Google Scholar 

  • Lopez, C., & Ménard, O. (2011). 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 and Surfaces B: Biointerfaces, 83, 29–41.

    Article  CAS  PubMed  Google Scholar 

  • Luo, J., Huang, Z., Liu, H., Zhang, Y., & Ren, F. (2018). Yak milk fat globules from the Qinghai-Tibetan Plateau: Membrane lipid composition and morphological properties. Food Chemistry, 245, 731–737.

    Article  CAS  PubMed  Google Scholar 

  • Malmsten, M., Bergenståhl, B., Nyberg, L., & Odham, G. (1994). Sphingomyelin from milk-characterization of liquid crystalline, liposome and emulsion properties. Journal of the American Oil Chemists’ Society, 71, 1021–1026.

    Article  CAS  Google Scholar 

  • Mather, I. H. (2000). A review and proposed nomenclature for major proteins of the milk-fat globule membrane1,2. Journal of Dairy Science, 83, 203–247.

    Article  CAS  PubMed  Google Scholar 

  • Ménard, O., Ahmad, S., Rousseau, F., Briard-Bion, V., Gaucheron, F., & Lopez, C. (2010). Buffalo vs. cow milk fat globules: Size distribution, zeta-potential compositions in total fatty acids and in polar lipids from the milk fat globule membrane. Food Chemistry, 120, 544–551.

    Article  CAS  Google Scholar 

  • Mesilati-Stahy, R., & Argov-Argaman, N. (2014). The relationship between size and lipid composition of the bovine milk fat globule is modulated by lactation stage. Food Chemistry, 145, 562–570.

    Article  CAS  PubMed  Google Scholar 

  • Murthy, A. V. R., Guyomarc’h, F., & Lopez, C. (2016a). 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, 32, 6757–6765.

    Article  CAS  PubMed  Google Scholar 

  • Murthy, A. V. R., Guyomarc’h, F., & Lopez, C. (2016b). The temperature-dependent physical state of polar lipids and their miscibility impact the topography and mechanical properties of bilayer models of the milk fat globule membrane. Biochimica et Biophysica Acta - Biomembranes, 1858, 2181–2190.

    Article  CAS  Google Scholar 

  • Murthy, A. V. R., Guyomarc’h, F., & Lopez, C. (2018). Palmitoyl ceramide promotes milk sphingomyelin gel phase domains formation and affects the mechanical properties of the fluid phase in milk-SM/DOPC supported membranes. Biochimica et Biophysica Acta (BBA) - Biomembranes, 1860, 635–644.

    Article  CAS  Google Scholar 

  • Murthy, A. V. R., Guyomarc’h, F., Paboeuf, G., Vié, V., & Lopez, C. (2015). Cholesterol strongly affects the organization of lipid monolayers studied as models of the milk fat globule membrane: Condensing effect and change in the lipid domain morphology. Biochimica et Biophysica Acta (BBA) - Biomembranes, 1848, 2308–2316.

    Article  CAS  Google Scholar 

  • Nguyen, H. T. H., Madec, M.-N., Ong, L., Kentish, S. E., Gras, S. L., & Lopez, C. (2016). The dynamics of the biological membrane surrounding the buffalo milk fat globule investigated as a function of temperature. Food Chemistry, 204, 343–351.

    Article  CAS  PubMed  Google Scholar 

  • Nguyen, H. T. H., Ong, L., Beaucher, E., Madec, M.-N., Kentish, S. E., Gras, S. L., et al. (2015). Buffalo milk fat globules and their biological membrane: In situ structural investigations. Food Research International, 67, 35–43.

    Article  CAS  Google Scholar 

  • Nilsson, A. (2016). Role of sphingolipids in infant gut health and immunity. The Journal of Pediatrics, 173, S53–S59.

    Article  CAS  PubMed  Google Scholar 

  • Noh, S. K., & Koo, S. I. (2004). Milk sphingomyelin is more effective than egg sphingomyelin in inhibiting intestinal absorption of cholesterol and fat in rats. The Journal of Nutrition, 134, 2611–2616.

    Article  CAS  PubMed  Google Scholar 

  • Nyberg, L., Duan, R.-D., & Nilsson, Å. (2000). A mutual inhibitory effect on absorption of sphingomyelin and cholesterol. The Journal of Nutritional Biochemistry, 11, 244–249.

    Article  CAS  PubMed  Google Scholar 

  • Rasmussen, J. T. (2009). Bioactivity of milk fat globule membrane proteins. Australian Journal of Dairy Technology, 64, 63–67.

    CAS  Google Scholar 

  • Reinhardt, T. A., & Lippolis, J. D. (2006). Bovine milk fat globule membrane proteome. Journal of Dairy Research, 73, 406–416.

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Juanes, F., Alonso, J. M., Zancada, L., & Hueso, P. (2009). Distribution and fatty acid content of phospholipids from bovine milk and bovine milk fat globule membranes. International Dairy Journal, 19, 273–278.

    Article  CAS  Google Scholar 

  • Simons, K., & Ikonen, E. (1997). Functional rafts in cell membranes. Nature, 387, 569–572.

    Article  CAS  PubMed  Google Scholar 

  • Singh, H. (2006). The milk fat globule membrane—A biophysical system for food applications. Current Opinion in Colloid & Interface Science, 11, 154–163.

    Article  CAS  Google Scholar 

  • Sprong, R. C., Hulstein, M. F. E., Lambers, T. T., & van der Meer, R. (2012). Sweet buttermilk intake reduces colonisation and translocation of Listeria monocytogenes in rats by inhibiting mucosal pathogen adherence. British Journal of Nutrition, 108, 2026–2033.

    Article  CAS  PubMed  Google Scholar 

  • Wooding, F. B. P. (1971). The structure of the milk fat globule membrane. Journal of Ultrastructure Research, 37, 388–400.

    Article  CAS  PubMed  Google Scholar 

  • Wooding, F. B. P., & Mather, I. H. (2017). Ultrastructural and immunocytochemical evidence for the reorganisation of the milk fat globule membrane after secretion. Cell and Tissue Research, 367, 283–295.

    Article  CAS  PubMed  Google Scholar 

  • Wooding, F. B. P., & Sargeant, T. J. (2015). Immunocytochemical evidence for golgi vesicle involvement in milk fat globule secretion. The Journal of Histochemistry and Cytochemistry, 63, 943–951.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao, Y., Zhao, G., Xiang, J., Zou, X., Jin, Q., & Wang, X. (2016). Lipid composition and structural characteristics of bovine, caprine and human milk fat globules. International Dairy Journal, 56, 64–73.

    Article  CAS  Google Scholar 

  • Zheng, H., Jimenez-Flores, R., & Everett, D. W. (2014). Lateral lipid organization of the bovine milk fat globule membrane is revealed by washing processes. Journal of Dairy Science, 97, 5964–5974.

    Article  CAS  PubMed  Google Scholar 

  • Zou, X., Guo, Z., Jin, Q., Huang, J., Cheong, L., Xu, X., et al. (2015). Composition and microstructure of colostrum and mature bovine milk fat globule membrane. Food Chemistry, 185, 362–370.

    Article  CAS  PubMed  Google Scholar 

  • Zou, X.-Q., Guo, Z., Huang, J.-H., Jin, Q.-Z., Cheong, L.-Z., Wang, X.-G., et al. (2012). Human milk fat globules from different stages of lactation: A lipid composition analysis and microstructure characterization. Journal of Agricultural and Food Chemistry, 60, 7158–7167.

    Article  CAS  PubMed  Google Scholar 

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Author information

Authors and Affiliations

  1. INRAE, UMR STLO, Rennes, France

    Christelle Lopez

  2. INRAE, UR BIA, Nantes, France

    Christelle Lopez

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  1. Christelle Lopez
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Correspondence to Christelle Lopez .

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Editors and Affiliations

  1. School of Science, College of Science Engineering and Health, RMIT University, Melbourne, VIC, Australia

    Tuyen Truong

  2. INRAE, French National Research Institute for Agriculture, Food & Environment, Research Unit BIA, Nantes, France

    Christelle Lopez

  3. ARC Dairy Innovation Hub, School of Agriculture and Food Sciences, The University of Queensland, St Lucia, QLD, Australia

    Bhesh Bhandari

  4. School of Agriculture and Food Sciences, The University of Queensland, St Lucia, QLD, Australia

    Sangeeta Prakash

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Lopez, C. (2020). Structure of the Milk Fat Globule Membrane: New Scientific Advances Revealing the Role of Sphingomyelin in Topographical and Mechanical Heterogeneities. In: Truong, T., Lopez, C., Bhandari, B., Prakash, S. (eds) Dairy Fat Products and Functionality. Springer, Cham. https://doi.org/10.1007/978-3-030-41661-4_3

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