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Annual Review of Food Science and Technology

Volume 15, 2024

Potential of Milk-Derived Extracellular Vesicles as Carriers for Oral Delivery of Active Phytoconstituents

Abstract

Extracellular vesicles (EVs) play a crucial role in intercellular communication and have the potential to serve as in vivo carriers for delivering active molecules. The biocompatibility advantages of EVs over artificial nanocarriers create new frontiers for delivering modern active molecules. Milk is a favorable source of EVs because of its high bioavailability, low immunogenicity, and commercial producibility. In this review, we analyzed the advantages of milk-derived EVs in the oral delivery of active molecules, discussed their research progress in delivering active phytoconstituents, and summarized the necessary technologies and critical unit operations required for the development of an oral delivery system based on EVs. The review aims to provide innovative ideas and fundamental quality control guidelines for developing the next-generation oral drug delivery system based on milk-derived EVs.

Keyword(s): active phytoconstituents, bioavailability, extracellular vesicles, milk, nanocarriers, oral delivery
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/content/journals/10.1146/annurev-food-072023-034354
2024-06-28
2024-12-05
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Literature Cited

  1. Adriano B, Cotto NM, Chauhan N, Jaggi M, Chauhan SC, Yallapu MM. 2021.. Milk exosomes: nature's abundant nanoplatform for theranostic applications. . Bioact. Mater. 6::2479–90
     [Google Scholar]
  2. Agrawal AK, Aqil F, Jeyabalan J, Spencer WA, Beck J, et al. 2017.. Milk-derived exosomes for oral delivery of paclitaxel. . Nanomed. Nanotechnol. Biol. Med. 13::1627–36
     [Crossref] [Google Scholar]
  3. Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJA. 2011.. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. . Nat. Biotechnol. 29::341–45
     [Crossref] [Google Scholar]
  4. Aqil F, Jeyabalan J, Agrawal AK, Kyakulaga AH, Munagala R, et al. 2017a.. Exosomal delivery of berry anthocyanidins for the management of ovarian cancer. . Food Funct. 8::4100–7
     [Crossref] [Google Scholar]
  5. Aqil F, Kausar H, Agrawal AK, Jeyabalan J, Kyakulaga AH, et al. 2016.. Exosomal formulation enhances therapeutic response of celastrol against lung cancer. . Exp. Mol. Pathol. 101::12–21
     [Crossref] [Google Scholar]
  6. Aqil F, Munagala R, Jeyabalan J, Agrawal AK, Gupta R. 2017b.. Exosomes for the enhanced tissue bioavailability and efficacy of curcumin. . AAPS J. 19::1691–702
     [Crossref] [Google Scholar]
  7. Aqil F, Munagala R, Jeyabalan J, Agrawal AK, Kyakulaga A-H, et al. 2019.. Milk exosomes: natural nanoparticles for siRNA delivery. . Cancer Lett. 449::186–95
     [Crossref] [Google Scholar]
  8. Arntz OJ, Pieters BCH, Oliveira MC, Broeren MGA, Bennink MB, et al. 2015.. Oral administration of bovine milk derived extracellular vesicles attenuates arthritis in two mouse models. . Mol. Nutr. Food Res. 59::1701–12
     [Crossref] [Google Scholar]
  9. Baddela VS, Nayan V, Rani P, Onteru SK, Singh D. 2016.. Physicochemical biomolecular insights into buffalo milk-derived nanovesicles. . Appl. Biochem. Biotechnol. 178::544–57
     [Crossref] [Google Scholar]
  10. Ballard O, Morrow AL. 2013.. Human milk composition nutrients and bioactive factors. . Pediatr. Clin. N. Am. 60::49–74
     [Crossref] [Google Scholar]
  11. Barenholz Y. 2012.. Doxil: the first FDA-approved nano-drug: lessons learned. . J. Control. Release 160::117–34
     [Crossref] [Google Scholar]
  12. Barile L, Vassalli G. 2017.. Exosomes: therapy delivery tools and biomarkers of diseases. . Pharmacol. Ther. 174::63–78
     [Crossref] [Google Scholar]
  13. Batrakova EV, Kim MS. 2015.. Using exosomes, naturally-equipped nanocarriers, for drug delivery. . J. Control. Release 219::396–405
     [Crossref] [Google Scholar]
  14. Benmoussa A, Provost P. 2019.. Milk microRNAs in health and disease. . Compr. Rev. Food Sci. Food Saf. 18::703–22
     [Crossref] [Google Scholar]
  15. Betker JL, Angle BM, Graner MW, Anchordoquy TJ. 2019.. The potential of exosomes from cow milk for oral delivery. . J. Pharm. Sci. 108::1496–505
     [Crossref] [Google Scholar]
  16. Blans K, Hansen MS, Sorensen LV, Hvam ML, Howard KA, et al. 2017.. Pellet-free isolation of human and bovine milk extracellular vesicles by size-exclusion chromatography. . J. Extracell. Vesicles 6::1294340
     [Crossref] [Google Scholar]
  17. Boriachek K, Islam MN, Moller A, Salomon C, Nam-Trung N, et al. 2018.. Biological functions and current advances in isolation and detection strategies for exosome nanovesicles. . Small 14::1702153
     [Crossref] [Google Scholar]
  18. Carobolante G, Mantaj J, Ferrari E, Vllasaliu D. 2020.. Cow milk and intestinal epithelial cell-derived extracellular vesicles as systems for enhancing oral drug delivery. . Pharmaceutics 12::226
     [Crossref] [Google Scholar]
  19. Casals E, Pfaller T, Duschl A, Oostingh GJ, Puntes V. 2010.. Time evolution of the nanoparticle protein corona. . ACS Nano 4::3623–32
     [Crossref] [Google Scholar]
  20. Chowdhury P, Roberts AM, Khan S, Hafeez BB, Chauhan SC, et al. 2017.. Magnetic nanoformulations for prostate cancer. . Drug Discov. Today 22::1233–41
     [Crossref] [Google Scholar]
  21. Colombo M, Raposo G, Thery C. 2014.. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. . Annu. Rev. Cell Dev. Biol. 30::255–89
     [Crossref] [Google Scholar]
  22. Contreras-Naranjo JC, Wu HJ, Ugaz VM. 2017.. Microfluidics for exosome isolation and analysis: enabling liquid biopsy for personalized medicine. . Lab Chip 17::3558–77
     [Crossref] [Google Scholar]
  23. de la Torre Gomez C, Goreham RV, Serra JJB, Nann T, Kussmann M. 2018.. “Exosomics”—a review of biophysics, biology and biochemistry of exosomes with a focus on human breast milk. . Front. Genet. 9::92
     [Crossref] [Google Scholar]
  24. Doyle LM, Wang MZ. 2019.. Overview of extracellular vesicles, their origin, composition, purpose, and methods for exosome isolation and analysis. . Cells 8::727
     [Crossref] [Google Scholar]
  25. Feng X, Chen X, Zheng X, Zhu H, Qi Q, et al. 2021.. Latest trend of milk derived exosomes: cargos, functions, and applications. . Front. Nutr. 8::747294
     [Crossref] [Google Scholar]
  26. Ferreira RF, Blees T, Shakeri F, Buness A, Sylvester M, et al. 2021.. Comparative proteome profiling in exosomes derived from porcine colostrum versus mature milk reveals distinct functional proteomes. . J. Proteom. 249::104338
     [Crossref] [Google Scholar]
  27. Forbes-Hernández TY. 2020.. Berries polyphenols: nano-delivery systems to improve their potential in cancer therapy. . J. Berry Res. 10::45–60
     [Crossref] [Google Scholar]
  28. Fu S, Wang Y, Xia X, Zheng JC. 2020.. Exosome engineering: current progress in cargo loading and targeted delivery. . NanoImpact 20::100261
     [Crossref] [Google Scholar]
  29. Galley JD, Besner GE. 2020.. The therapeutic potential of breast milk-derived extracellular vesicles. . Nutrients 12::745
     [Crossref] [Google Scholar]
  30. Gandham S, Su X, Wood J, Nocera AL, Alli SC, et al. 2020.. Technologies and standardization in research on extracellular vesicles. . Trends Biotechnol. 38::1066–98
     [Crossref] [Google Scholar]
  31. Ganju A, Yallapu MM, Khan S, Behrman SW, Chauhan SC, Jaggi M. 2014.. Nanoways to overcome docetaxel resistance in prostate cancer. . Drug Resist. Updates 17::13–23
     [Crossref] [Google Scholar]
  32. Go G, Park HJ, Lee JH, Yun CW, Lee SH. 2022.. Inhibitory effect of oxaliplatin-loaded engineered milk extracellular vesicles on tumor progression. . Anticancer Res. 42::857–66
     [Crossref] [Google Scholar]
  33. Gu Y, Li M, Wang T, Liang Y, Zhong Z, et al. 2012.. Lactation-related microRNA expression profiles of porcine breast milk exosomes. . PLOS ONE 7::e43691
     [Crossref] [Google Scholar]
  34. Gui H, Sun L, Liu R, Si X, Li D, et al. 2022.. Current knowledge of anthocyanin metabolism in the digestive tract: absorption, distribution, degradation, and interconversion. . Crit. Rev. Food Sci. Nutr. 63::5953–66
     [Crossref] [Google Scholar]
  35. Guo SC, Tao SC, Dawn H. 2018.. Microfluidics-based on-a-chip systems for isolating and analysing extracellular vesicles. . J. Extracell. Vesicles 7::1508271
     [Crossref] [Google Scholar]
  36. Haney MJ, Klyachko NL, Zhaoa Y, Gupta R, Plotnikova EG, et al. 2015.. Exosomes as drug delivery vehicles for Parkinson's disease therapy. . J. Control. Release 207::18–30
     [Crossref] [Google Scholar]
  37. Hannafon BN, Ding W-Q. 2013.. Intercellular communication by exosome-derived microRNAs in cancer. . Int. J. Mol. Sci. 14::14240–69
     [Crossref] [Google Scholar]
  38. Hassiotou F, Beltran A, Chetwynd E, Stuebe AM, Twigger AJ, et al. 2012.. Breastmilk is a novel source of stem cells with multilineage differentiation potential. . Stem Cells 30::2164–74
     [Crossref] [Google Scholar]
  39. Hazas MCL, del Pozo-Acebo L, Hansen MS, Gil-Zamorano J, Mantilla-Escalante DC, et al. 2022.. Dietary bovine milk miRNAs transported in extracellular vesicles are partially stable during GI digestion, are bioavailable and reach target tissues but need a minimum dose to impact on gene expression. . Eur. J. Nutr. 61::1043–56
     [Crossref] [Google Scholar]
  40. Hinz K, O'Connor PM, Huppertz T, Ross RP, Kelly AL. 2012.. Comparison of the principal proteins in bovine, caprine, buffalo, equine and camel milk. . J. Dairy Res. 79::185–91
     [Crossref] [Google Scholar]
  41. Iavorovschi AM, Wang A. 2020.. Engineering mesenchymal stromal/stem cell-derived extracellular vesicles with improved targeting and therapeutic efficiency for the treatment of central nervous system disorders. . Neural Regener. Res. 15::2235–36
     [Crossref] [Google Scholar]
  42. Ishiguro K, Yan IK, Lewis-Tuffin L, Patel T. 2020.. Targeting liver cancer stem cells using engineered biological nanoparticles for the treatment of hepatocellular cancer. . Hepatol. Commun. 4::298–313
     [Crossref] [Google Scholar]
  43. Izumi H, Kosaka N, Shimizu T, Sekine K, Ochiya T, Takase M. 2012.. Bovine milk contains microRNA and messenger RNA that are stable under degradative conditions. . J. Dairy Sci. 95::4831–41
     [Crossref] [Google Scholar]
  44. Izumi H, Tsuda M, Sato Y, Kosaka N, Ochiya T, et al. 2015.. Bovine milk exosomes contain microRNA and mRNA and are taken up by human macrophages. . J. Dairy Sci. 98::2920–33
     [Crossref] [Google Scholar]
  45. Jiang XC, Gao JQ. 2017.. Exosomes as novel bio-carriers for gene and drug delivery. . Int. J. Pharmaceut. 521::167–75
     [Crossref] [Google Scholar]
  46. Kahn S, Liao YL, Du XG, Xu W, Li J, Lonnerdal B. 2018.. Exosomal microRNAs in milk from mothers delivering preterm infants survive in vitro digestion and are taken up by human intestinal cells. . Mol. Nutr. Food Res. 62::1701050
     [Crossref] [Google Scholar]
  47. Kamerkar S, LeBleu VS, Sugimoto H, Yang S, Ruivo CF, et al. 2017.. Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer. . Nature 546::498–503
     [Crossref] [Google Scholar]
  48. Kandimalla R, Aqil F, Alhakeem SS, Jeyabalan J, Tyagi N, et al. 2021a.. Targeted oral delivery of paclitaxel using colostrum-derived exosomes. . Cancers 13::3700
     [Crossref] [Google Scholar]
  49. Kandimalla R, Aqil F, Tyagi N, Gupta R. 2021b.. Milk exosomes: a biogenic nanocarrier for small molecules and macromolecules to combat cancer. . Am. J. Reprod. Immunol. 85::e13349
     [Crossref] [Google Scholar]
  50. Kim MS, Haney MJ, Zhao Y, Mahajan V, Deygen I, et al. 2016.. Development of exosome-encapsulated paclitaxel to overcome MDR in cancer cells. . Nanomed. Nanotechnol. Biol. Med. 12::655–64
     [Crossref] [Google Scholar]
  51. Kleinjan M, van Herwijnen MJC, Libregts S, van Neerven RJJ, Feitsma AL, Wauben MHM. 2021.. Regular industrial processing of bovine milk impacts the integrity and molecular composition of extracellular vesicles. . J. Nutr. 151::1416–25
     [Crossref] [Google Scholar]
  52. Kooijmans SAA, Stremersch S, Braeckmans K, de Smedt SC, Hendrix A, et al. 2013.. Electroporation-induced siRNA precipitation obscures the efficiency of siRNA loading into extracellular vesicles. . J. Control. Release 172::229–38
     [Crossref] [Google Scholar]
  53. Kowal J, Tkach M, Thery C. 2014.. Biogenesis and secretion of exosomes. . Curr. Opin. Cell Biol. 29::116–25
     [Crossref] [Google Scholar]
  54. Kusuma RJ, Manca S, Friemel T, Sukreet S, Nguyen C, Zempleni J. 2016.. Human vascular endothelial cells transport foreign exosomes from cow's milk by endocytosis. . Am. J. Physiol. Cell Physiol. 310::C800–7
     [Crossref] [Google Scholar]
  55. Lee H, Park H, Noh GJ, Lee ES. 2018.. pH-Responsive hyaluronate-anchored extracellular vesicles to promote tumor-targeted drug delivery. . Carbohydr. Polym. 202::323–33
     [Crossref] [Google Scholar]
  56. Leiferman A, Shu J, Upadhyaya B, Cui J, Zempleni J. 2019.. Storage of extracellular vesicles in human milk, and microRNA profiles in human milk exosomes and infant formulas. . J. Pediatr. Gastroenterol. Nutr. 69::235–38
     [Crossref] [Google Scholar]
  57. Li B, Cheng Z, Sun X, Si X, Gong E, et al. 2020.. Lonicera caerulea L. polyphenols alleviate oxidative stress-induced intestinal environment imbalance and lipopolysaccharide-induced liver injury in HFD-fed rats by regulating the Nrf2/HO-1/NQO1 and MAPK pathways. . Mol. Nutr. Food Res. 64::1901315
     [Crossref] [Google Scholar]
  58. Li D, Yao SR, Zhou ZF, Shi J, Huang ZH, Wu ZM. 2020.. Hyaluronan decoration of milk exosomes directs tumor-specific delivery of doxorubicin. . Carbohydr. Res. 493::108032
     [Crossref] [Google Scholar]
  59. Li J, He X, Deng Y, Yang C. 2019.. An update on isolation methods for proteomic studies of extracellular vesicles in biofluids. . Molecules 24::3516
     [Crossref] [Google Scholar]
  60. Li P, Kaslan M, Lee SH, Yao J, Gao Z. 2017.. Progress in exosome isolation techniques. . Theranostics 7::789–804
     [Crossref] [Google Scholar]
  61. Li S, Tang Y, Dou Y. 2021.. The potential of milk-derived exosomes for drug delivery. . Curr. Drug Deliv. 18::688–99
     [Crossref] [Google Scholar]
  62. Li Y, Zhang X, Zhang C, Yang JJ, Chi HY, et al. 2022.. Comparative study on the immunomodulatory function of extracellular vesicles from different dairy products. . Food Funct. 13::2504–14
     [Crossref] [Google Scholar]
  63. Liao YL, Du XG, Li J, Lonnerdal B. 2017.. Human milk exosomes and their microRNAs survive digestion in vitro and are taken up by human intestinal cells. . Mol. Nutr. Food Res. 61::1700082
     [Crossref] [Google Scholar]
  64. Link J, Thon C, Schanze D, Steponaitiene R, Kupcinskas J, et al. 2019.. Food-derived xeno-microRNAs: influence of diet and detectability in gastrointestinal tract-proof-of-principle study. . Mol. Nutr. Food Res. 63::1800076
     [Crossref] [Google Scholar]
  65. Luan X, Sansanaphongpricha K, Myers I, Chen H, Yuan H, Sun D. 2017.. Engineering exosomes as refined biological nanoplatforms for drug delivery. . Acta Pharmacol. Sin. 38::754–63
     [Crossref] [Google Scholar]
  66. Luo SQ, Sun XL, Huang M, Ma QH, Du LB, Cui Y. 2021.. Enhanced neuroprotective effects of epicatechin gallate encapsulated by bovine milk-derived exosomes against Parkinson's disease through antiapoptosis and antimitophagy. . J. Agric. Food Chem. 69::5134–43
     [Crossref] [Google Scholar]
  67. Maiorano G, Sabella S, Sorce B, Brunetti V, Malvindi MA, et al. 2010.. Effects of cell culture media on the dynamic formation of protein-nanoparticle complexes and influence on the cellular response. . ACS Nano 4::7481–91
     [Crossref] [Google Scholar]
  68. McClements DJ, Li F, Xiao H. 2015.. The nutraceutical bioavailability classification scheme: classifying nutraceuticals according to factors limiting their oral bioavailability. . Annu. Rev. Food Sci. Technol. 6::299–327
     [Crossref] [Google Scholar]
  69. Melnik BC, Kakulas F, Geddes DT, Hartmann PE, John SM, et al. 2016.. Milk miRNAs: simple nutrients or systemic functional regulators?. Nutr. Metab. 13::42
     [Crossref] [Google Scholar]
  70. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan MLG, et al. 2012.. Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. . Blood 119::756–66
     [Crossref] [Google Scholar]
  71. Mueller J, Prozeller D, Ghazaryan A, Kokkinopoulou M, Mailaender V, et al. 2018.. Beyond the protein corona—lipids matter for biological response of nanocarriers. . Acta Biomater. 71::420–31
     [Crossref] [Google Scholar]
  72. Munagala R, Aqil F, Jeyabalan J, Agrawal AK, Mudd AM, et al. 2017.. Exosomal formulation of anthocyanidins against multiple cancer types. . Cancer Lett. 393::94–102
     [Crossref] [Google Scholar]
  73. Munagala R, Aqil F, Jeyabalan J, Gupta RC. 2016.. Bovine milk-derived exosomes for drug delivery. . Cancer Lett. 371::48–61
     [Crossref] [Google Scholar]
  74. Oliveira MC, Arntz OJ, Davidson ENB, van Lent P, Koenders MI, et al. 2016.. Milk extracellular vesicles accelerate osteoblastogenesis but impair bone matrix formation. . J. Nutr. Biochem. 30::74–84
     [Crossref] [Google Scholar]
  75. Ong SL, Blenkiron C, Haines S, Acevedo-Fani A, Leite JAS, et al. 2021.. Ruminant milk-derived extracellular vesicles: a nutritional and therapeutic opportunity?. Nutrients 13::2505
     [Crossref] [Google Scholar]
  76. Pan BT, Johnstone RM. 1983.. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. . Cell 33::967–78
     [Crossref] [Google Scholar]
  77. Pieters BCH, Arntz OJ, Bennink MB, Broeren MGA, van Caam APM, et al. 2015.. Commercial cow milk contains physically stable extracellular vesicles expressing immunoregulatory TGF-β. . PLOS ONE 10::e0121123
     [Crossref] [Google Scholar]
  78. Qi J, Zhou YL, Jiao ZY, Wang X, Zhao Y, et al. 2017.. Exosomes derived from human bone marrow mesenchymal stem cells promote tumor growth through hedgehog signaling pathway. . Cell. Physiol. Biochem. 42::2242–54
     [Crossref] [Google Scholar]
  79. Rahman MJ, Regn D, Bashratyan R, Yang DD. 2013.. Exosomes released by islet-derived mesenchymal stem cells trigger autoimmune responses in NOD mice. . Diabetes 63::1008–20
     [Crossref] [Google Scholar]
  80. Rahman MM, Shimizu K, Yamauchi M, Takase H, Ugawa S, et al. 2019.. Acidification effects on isolation of extracellular vesicles from bovine milk. . PLOS ONE 14::e0222613
     [Crossref] [Google Scholar]
  81. Rahman MM, Takashima S, Kamatari YO, Badr Y, Kitamura Y, et al. 2021a.. Proteomic profiling of milk small extracellular vesicles from bovine leukemia virus-infected cattle. . Sci. Rep. 11::2951
     [Crossref] [Google Scholar]
  82. Rahman MM, Takashima S, Kamatari YO, Shimizu K, Okada A, Inoshima Y. 2021b.. Comprehensive proteomic analysis revealed a large number of newly identified proteins in the small extracellular vesicles of milk from late-stage lactating cows. . Animals 11::2506
     [Crossref] [Google Scholar]
  83. Rani P, Vashisht M, Golla N, Shandilya S, Onteru SK, Singh D. 2017.. Milk miRNAs encapsulated in exosomes are stable to human digestion and permeable to intestinal barrier in vitro. . J. Funct. Foods 34::431–39
     [Crossref] [Google Scholar]
  84. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, et al. 1996.. B lymphocytes secrete antigen-presenting vesicles. . J. Exp. Med. 183::1161–72
     [Crossref] [Google Scholar]
  85. Reinhardt TA, Sacco RE, Nonnecke BJ, Lippolis JD. 2013.. Bovine milk proteome: quantitative changes in normal milk exosomes, milk fat globule membranes and whey proteomes resulting from Staphylococcus aureus mastitis. . J. Proteom. 82::141–54
     [Crossref] [Google Scholar]
  86. Samuel M, Fonseka P, Sanwlani R, Gangoda L, Chee SH, et al. 2021.. Oral administration of bovine milk-derived extracellular vesicles induces senescence in the primary tumor but accelerates cancer metastasis. . Nat. Commun. 12::3950
     [Crossref] [Google Scholar]
  87. Sato YT, Umezaki K, Sawada S, Mukai S-A, Sasaki Y, et al. 2016.. Engineering hybrid exosomes by membrane fusion with liposomes. . Sci. Rep. 6::21933
     [Crossref] [Google Scholar]
  88. Sedykh S, Kuleshova A, Nevinsky G. 2020.. Milk exosomes: perspective agents for anticancer drug delivery. . Int. J. Mol. Sci. 21::6646
     [Crossref] [Google Scholar]
  89. Shandilya S, Rani P, Onteru SK, Singh D. 2017.. Small interfering RNA in milk exosomes is resistant to digestion and crosses the intestinal barrier in vitro. . J. Agric. Food Chem. 65::9506–13
     [Crossref] [Google Scholar]
  90. Sheng HM, Hassanali S, Nugent C, Wen L, Hamilton-Williams E, et al. 2011.. Insulinoma-released exosomes or microparticles are immunostimulatory and can activate autoreactive T cells spontaneously developed in nonobese diabetic mice. . J. Immunol. 187::1591–600
     [Crossref] [Google Scholar]
  91. Si X, Bi J, Chen Q, Cui H, Bao Y, et al. 2021.. Effect of blueberry anthocyanin-rich extracts on peripheral and hippocampal antioxidant defensiveness: the analysis of the serum fatty acid species and gut microbiota profile. . J. Agric. Food Chem. 69::3658–66
     [Crossref] [Google Scholar]
  92. Somiya M, Yoshioka Y, Ochiya T. 2018.. Biocompatibility of highly purified bovine milk-derived extracellular vesicles. . J. Extracell. Vesicles 7::1440132
     [Crossref] [Google Scholar]
  93. Thery C, Boussac M, Veron P, Ricciardi-Castagnoli P, Raposo G, et al. 2001.. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. . J. Immunol. 166::7309–18
     [Crossref] [Google Scholar]
  94. Thery C, Witwer KW, Aikawa E, Alcaraz MJ, Anderson JD, et al. 2018.. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. . J. Extracell. Vesicles 1::7
     [Google Scholar]
  95. Tian J-L, Si X, Shu C, Wang Y-H, Tan H, et al. 2022.. Synergistic effects of combined anthocyanin and metformin treatment for hyperglycemia in vitro and in vivo. . J. Agric. Food Chem. 70::1182–95
     [Crossref] [Google Scholar]
  96. Tong L, Hao H, Zhang Z, Lv Y, Liang X, et al. 2021.. Milk-derived extracellular vesicles alleviate ulcerative colitis by regulating the gut immunity and reshaping the microbiota. . Theranostics 11::8570–86
     [Crossref] [Google Scholar]
  97. Vashisht M, Rani P, Onteru SK, Singh D. 2017.. Curcumin encapsulated in milk exosomes resists human digestion and possesses enhanced intestinal permeability in vitro. . Appl. Biochem. Biotechnol. 183::993–1007
     [Crossref] [Google Scholar]
  98. Vogel R, Coumans FAW, Maltesen RG, Boing AN, Bonnington KE, et al. 2016.. A standardized method to determine the concentration of extracellular vesicles using tunable resistive pulse sensing. . J. Extracell. Vesicles 5::31242
     [Crossref] [Google Scholar]
  99. Wahlgren J, Karlson TDL, Brisslert M, Sani FV, Telemo E, et al. 2012.. Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes. . Nucleic Acids Res. 40::e130
     [Crossref] [Google Scholar]
  100. Walker S, Busatto S, Pham A, Tian M, Suh A, et al. 2019.. Extracellular vesicle-based drug delivery systems for cancer treatment. . Theranostics 9::8001–17
     [Crossref] [Google Scholar]
  101. Wang X. 2017.. Isolation of extracellular vesicles from breast milk. . Methods Mol. Biol. 1660::351–53
     [Crossref] [Google Scholar]
  102. Wang XY, Yan XY, Zhang L, Cai JY, Zhou YH, et al. 2019.. Identification and peptidomic profiling of exosomes in preterm human milk: insights into necrotizing enterocolitis prevention. . Mol. Nutr. Food Res. 63::1801247
     [Crossref] [Google Scholar]
  103. Wijenayake S, Eisha S, Tawhidi Z, Pitino MA, Steele MA, et al. 2021.. Comparison of methods for pre-processing, exosome isolation, and RNA extraction in unpasteurized bovine and human milk. . PLOS ONE 16::e0257633
     [Crossref] [Google Scholar]
  104. Yallapu MM, Jaggi M, Chauhan SC. 2012.. Curcumin nanoformulations: a future nanomedicine for cancer. . Drug Discov. Today 17::71–80
     [Crossref] [Google Scholar]
  105. Yamauchi M, Shimizu K, Rahman M, Ishikawa H, Takase H, et al. 2019.. Efficient method for isolation of exosomes from raw bovine milk. . Drug Dev. Ind. Pharm. 45::359–64
     [Crossref] [Google Scholar]
  106. Yassin AM, Hamid MIA, Farid OA, Amer H, Warda M. 2016.. Dromedary milk exosomes as mammary transcriptome nano-vehicle: their isolation, vesicular and phospholipidomic characterizations. . J. Adv. Res. 7::749–56
     [Crossref] [Google Scholar]
  107. Yong T, Zhang X, Bie N, Zhang H, Zhang X, et al. 2019.. Tumor exosome-based nanoparticles are efficient drug carriers for chemotherapy. . Nat. Commun. 10::3838
     [Crossref] [Google Scholar]
  108. Yu SR, Zhao ZH, Sun LM, Li P. 2017.. Fermentation results in quantitative changes in milk-derived exosomes and different effects on cell growth and survival. . J. Agric. Food Chem. 65::1220–28
     [Crossref] [Google Scholar]
  109. Zeng B, Chen T, Xie MY, Luo JY, He JJ, et al. 2019.. Exploration of long noncoding RNA in bovine milk exosomes and their stability during digestion in vitro. . J. Dairy Sci. 102::6726–37
     [Crossref] [Google Scholar]
  110. Zhang M, Jin K, Gao L, Zhang Z, Li F, et al. 2018.. Methods and technologies for exosome isolation and characterization. . Small Methods 2::1800021
     [Crossref] [Google Scholar]
  111. Zhao X, Wu D, Ma X, Wang J, Hou W, Zhang W. 2020.. Exosomes as drug carriers for cancer therapy and challenges regarding exosome uptake. . Biomed. Pharmacother. 128::110273
     [Crossref] [Google Scholar]
  112. Zhong J, Xia B, Shan S, Zheng A, Zhang S, et al. 2021.. High-quality milk exosomes as oral drug delivery system. . Biomaterials 277::121126
     [Crossref] [Google Scholar]
  113. Zhou Q, Li M, Wang X, Li Q, Wang T, et al. 2012.. Immune-related microRNAs are abundant in breast milk exosomes. . Int. J. Biol. Sci. 8::118–23
     [Crossref] [Google Scholar]
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Potential of Milk-Derived Extracellular Vesicles as Carriers for Oral Delivery of Active Phytoconstituents
Annual Review of Food Science and Technology 15, 431 (2024); https://doi.org/10.1146/annurev-food-072023-034354
/content/journals/10.1146/annurev-food-072023-034354
/content/journals/10.1146/annurev-food-072023-034354
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  • Article Type: Review Article

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