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Original Research Article

Pellet-free isolation of human and bovine milk extracellular vesicles by size-exclusion chromatography

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Article: 1294340 | Received 08 Jul 2016, Accepted 06 Feb 2017, Published online: 15 Mar 2017

References

  • Lönnerdal B. Bioactive proteins in human milk: mechanisms of action. J Pediatr. 2010;156:1–16.
  • Chatterton DEW, Nguyen DN, Bering SB, et al. Anti-inflammatory mechanisms of bioactive milk proteins in the intestine of newborns. Int J Biochem Cell Biol. 2013;45:1730–1747.
  • Civardi E, Garofoli F, Mazzucchelli I, et al. Enteral nutrition and infections: the role of human milk. Early Hum Dev. 2014;90:57–59.
  • Raikos V, Dassios T. Health-promoting properties of bioactive peptides derived from milk proteins in infant food: a review. Dairy Sci Technol. 2014;94:91–101.
  • Walker WA, Iyengar RS. Breast milk, microbiota, and intestinal immune homeostasis. Pediatr Res. 2015;77:220–228.
  • Stewart P, Puppione D, Patton S. The presence of microvilli and other membrane fragments in the non-fat phase of bovine milk. Cell Tissue Res. 1971;123:161–167.
  • Admyre C, Johansson SM, Qazi KR, et al. Exosomes with immune modulatory features are present in human breast milk. J Immunol Baltim Md 1950. 2007;179:1969–1978.
  • Reinhardt TA, Lippolis JD, Nonnecke BJ, et al. Bovine milk exosome proteome. J Proteomics. 2012;75:1486–1492.
  • Lässer C, Alikhani VS, Ekström K, et al. Human saliva, plasma and breast milk exosomes contain RNA: uptake by macrophages. J Transl Med. 2011;9:9.
  • Hata T, Murakami K, Nakatani H, et al. Isolation of bovine milk-derived microvesicles carrying mRNAs and microRNAs. Biochem Biophys Res Commun. 2010;396:528–533.
  • Benmoussa A, Lee CHC, Laffont B, et al. Commercial dairy cow milk microRNAs resist digestion under simulated gastrointestinal tract conditions. J Nutr. 2016;146:2206–2215.
  • Izumi H, Kosaka N, Shimizu T, et al. Bovine milk contains microRNA and messenger RNA that are stable under degradative conditions. J Dairy Sci. 2012;95:4831–4841.
  • Izumi H, Tsuda M, Sato Y, et al. Bovine milk exosomes contain microRNA and mRNA and are taken up by human macrophages. J Dairy Sci. 2015;98:2920–2933.
  • Torregrosa Paredes P, Gutzeit C, Johansson S, et al. Differences in exosome populations in human breast milk in relation to allergic sensitization and lifestyle. Allergy. 2014;69:463–471.
  • Zonneveld MI, Brisson AR, van Herwijnen MJC, et al. Recovery of extracellular vesicles from human breast milk is influenced by sample collection and vesicle isolation procedures. J Extracell Vesicles. 2014;3:24215.
  • van Herwijnen MJC, Zonneveld MI, Goerdayal S, et al. Comprehensive proteomic analysis of human milk-derived extracellular vesicles unveils a novel functional proteome distinct from other milk components. Mol Cell Proteomics MCP. 2016;15:3412–3423.
  • Field CJ. The immunological components of human milk and their effect on immune development in infants. J Nutr. 2005;135:1–4.
  • Melnik BC, John SM, Schmitz G. Milk: an exosomal microRNA transmitter promoting thymic regulatory T cell maturation preventing the development of atopy? J Transl Med. 2014;12:43.
  • Nakatani H, Aoki N, Nakagawa Y, et al. Weaning-induced expression of a milk-fat globule protein, MFG-E8, in mouse mammary glands, as demonstrated by the analyses of its mRNA, protein and phosphatidylserine-binding activity. Biochem J. 2006;395:21–30.
  • Sun Q, Chen X, Yu J, et al. Immune modulatory function of abundant immune-related microRNAs in microvesicles from bovine colostrum. Protein Cell. 2013;4:197–210.
  • Baier SR, Nguyen C, Xie F, et al. MicroRNAs are absorbed in biologically meaningful amounts from nutritionally relevant doses of cow milk and affect gene expression in peripheral blood mononuclear cells, HEK-293 kidney cell cultures, and mouse livers. J Nutr. 2014;144:1495–1500.
  • Auerbach A, Vyas G, Li A, et al. Uptake of dietary milk miRNAs by adult humans: a validation study. F1000Research. 2016;5:721.
  • Mather IH, Keenan TW. Origin and secretion of milk lipids. J Mammary Gland Biol Neoplasia. 1998;3:259–273.
  • McMahon DJ, Oommen BS. Supramolecular structure of the casein micelle. J Dairy Sci. 2008;91:1709–1721.
  • Patton S, Keenan TW. The relationship of milk phospholipids to membranes of the secretory cell. Lipids. 1971;6:58–61.
  • Hernell O. Human milk vs. cow’s milk and the evolution of infant formulas. Nestlé Nutr Workshop Ser Paediatr Programme. 2011;67:17–28.
  • Fox PF, McSweeney PLH. Dairy chemistry and biochemistry. London: Thomson Science; 1998. p. 181.
  • Yamada T, Inoshima Y, Matsuda T, et al. Comparison of methods for isolating exosomes from bovine milk. J Vet Med Sci. 2012;74:1523–1525.
  • Keenan TW, Morré DJ, Olson DE, et al. Biochemical and morphological comparison of plasma membrane and milk fat globule membrane from bovine mammary gland. J Cell Biol. 1970;44:80–93.
  • Kobylka D, Carraway KL. Proteins and glycoproteins of the milk fat globule membrane. Biochim Biophys Acta. 1972;288:282–295.
  • Lozano-Ramos I, Bancu I, Oliveira-Tercero A, et al. Size-exclusion chromatography-based enrichment of extracellular vesicles from urine samples. J Extracell Vesicles. 2015;4:27369.
  • Böing AN, van der Pol E, Grootemaat AE, et al. Single-step isolation of extracellular vesicles by size-exclusion chromatography. J Extracell Vesicles. 2014;3:23430.
  • Welton JL, Webber JP, Botos L-A, et al. Ready-made chromatography columns for extracellular vesicle isolation from plasma. J Extracell Vesicles. 2015;4:27269.
  • Taylor DD, Shah S. Methods of isolating extracellular vesicles impact down-stream analyses of their cargoes. Methods San Diego Calif. 2015;87:3–10.
  • Witwer KW, Buzás EI, Bemis LT, et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles. 2013;2:20360.
  • Huston GE, Patton S. Membrane distribution in human milks throughout lactation as revealed by phospholipid and cholesterol analyses. J Pediatr Gastroenterol Nutr. 1986;5:602–607.
  • Hvarregaard J, Andersen MH, Berglund L, et al. Characterization of glycoprotein PAS-6/7 from membranes of bovine milk fat globules. Eur J Biochem FEBS. 1996;240:628–636.
  • Kvistgaard AS, Pallesen LT, Arias CF, et al. Inhibitory effects of human and bovine milk constituents on rotavirus infections. J Dairy Sci. 2004;87:4088–4096.
  • Schacterle GR, Pollack RL. A simplified method for the quantitative assay of small amounts of protein in biologic material. Anal Biochem. 1973;51:654–655.
  • Dragovic RA, Gardiner C, Brooks AS, et al. Sizing and phenotyping of cellular vesicles using nanoparticle tracking analysis. Nanomedicine Nanotechnol Biol Med. 2011;7:780–788.
  • Tao H, Lee SC, Moeller A, et al. Engineered nanostructured β-sheet peptides protect membrane proteins. Nat Methods. 2013;10:759–761.
  • Suloway C, Pulokas J, Fellmann D, et al. Automated molecular microscopy: the new leginon system. J Struct Biol. 2005;151:41–60.
  • Kishimoto K, Urade R, Ogawa T, et al. Nondestructive quantification of neutral lipids by thin-layer chromatography and laser-fluorescent scanning: suitable methods for “lipidome” analysis. Biochem Biophys Res Commun. 2001;281:657–662.
  • Lässer C. Identification and analysis of circulating exosomal microRNA in human body fluids. Methods Mol Biol Clifton NJ. 2013;1024:109–128.
  • Jeppesen DK, Hvam ML, Primdahl-Bengtson B, et al. Comparative analysis of discrete exosome fractions obtained by differential centrifugation. J Extracell Vesicles. 2014;3:25011.
  • Fox PF, McSweeney PLH. Dairy chemistry and biochemistry. London: Thomson Science; 1998. p. 180–182.
  • Bezkorovainy A. Human milk and colostrum proteins: a review. J Dairy Sci. 1977;60:1023–1037.
  • Fox PF, McSweeney PLH. Dairy chemistry and biochemistry. London: Thomson Science; 1998. p. 149.
  • Contarini G, Povolo M. Phospholipids in milk fat: composition, biological and technological significance, and analytical strategies. Int J Mol Sci. 2013;14:2808–2831.
  • Munagala R, Aqil F, Jeyabalan J, et al. Bovine milk-derived exosomes for drug delivery. Cancer Lett. 2016;371:48–61.
  • Lötvall J, Hill AF, Hochberg F, et al. Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles. J Extracell Vesicles. 2014;3:26913.
  • Yang Y, Zheng N, Zhao X, et al. Proteomic characterization and comparison of mammalian milk fat globule proteomes by iTRAQ analysis. J Proteomics. 2015;116C:34–43.
  • Yuana Y, Levels J, Grootemaat A, et al. Co-isolation of extracellular vesicles and high-density lipoproteins using density gradient ultracentrifugation. J Extracell Vesicles. 2014;3:23262.
  • Subra C, Laulagnier K, Perret B, et al. Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies. Biochimie. 2007;89:205–212.
  • Llorente A, Skotland T, Sylvänne T, et al. Molecular lipidomics of exosomes released by PC-3 prostate cancer cells. Biochim Biophys Acta. 2013;1831:1302–1309.
  • Fong BY, Norris CS, MacGibbon AKH. Protein and lipid composition of bovine milk-fat-globule membrane. Int Dairy J. 2007;17:275–288.
  • Laulagnier K, Motta C, Hamdi S, et al. Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem J. 2004;380:161–171.
  • Llorente A, van Deurs B, Sandvig K. Cholesterol regulates prostasome release from secretory lysosomes in PC-3 human prostate cancer cells. Eur J Cell Biol. 2007;86:405–415.
  • Huston GE, Patton S. Factors related to the formation of cytoplasmic crescents on milk fat globules. J Dairy Sci. 1990;73:2061–2066.