Login Register Cart 0
Mini-Review Article

Instead of Calories, Should We Be Counting our Consumption of Exosomes and MicroRNAs?

Author(s): Kendal Dee Hirschi*, Vignesh Nalliah and Hormat Shadgou Rhein

Volume 12, Issue 3, 2023

Published on: 12 May, 2023

Page: [165 - 170] Pages: 6

DOI: 10.2174/2211536612666230331083455

Price: $65

Abstract

The specific foods to eat for optimal nutrition remain ill-defined. Studies using plantbased diets or milk suggest that vesicles, termed exosomes, and small RNAs termed microRNAs (miRNAs) are health promoting components in foods. However, numerous studies refute the potential of dietary cross-kingdom communication of exosomes and miRNAs. While research reinforces that plant-based diets and milk are healthy components of a well-rounded diet, the bioavailability and bioactivity of the exosomes and miRNAs present in plant-based diets and milk remain unclear. Further investigations of plant-based diet and milk exosome like particles may open a new era in application of food for overall health enhancement. In addition, the potential biotechnological plantbased diet and milk exosome like particles can aid in cancer treatment.

Keywords: Exosomes, miRNAs, morphology, PDEVs, extracellular vesicles, nucleic acids, microvesicles.

Next »
Graphical Abstract

[1]
McNeill EM, Hirschi KD. Roles of regulatory RNAs in nutritional control. Annu Rev Nutr 2020; 40(1): 77-104.
[http://dx.doi.org/10.1146/annurev-nutr-122319-035633] [PMID: 32966184]
[2]
Li D, Yao X, Yue J, et al. Advances in bioactivity of micrornas of plant-derived exosome-like nanoparticles and milk-derived extracellular vesicles. J Agric Food Chem 2022; 70(21): 6285-99.
[http://dx.doi.org/10.1021/acs.jafc.2c00631] [PMID: 35583385]
[3]
van Niel G, Carter DRF, Clayton A, Lambert DW, Raposo G, Vader P. Challenges and directions in studying cell–cell communication by extracellular vesicles. Nat Rev Mol Cell Biol 2022; 23(5): 369-82.
[http://dx.doi.org/10.1038/s41580-022-00460-3] [PMID: 35260831]
[4]
van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol 2018; 19(4): 213-28.
[http://dx.doi.org/10.1038/nrm.2017.125] [PMID: 29339798]
[5]
Urzì O, Raimondo S, Alessandro R. Extracellular vesicles from plants: Current knowledge and open questions. Int J Mol Sci 2021; 22(10): 5366.
[http://dx.doi.org/10.3390/ijms22105366] [PMID: 34065193]
[6]
Varga Z, Fehér B, Kitka D, et al. Size measurement of extracellular vesicles and synthetic liposomes: The impact of the hydration shell and the protein corona. Colloids Surf B Biointerfaces 2020; 192: 111053.
[http://dx.doi.org/10.1016/j.colsurfb.2020.111053] [PMID: 32361376]
[7]
Kameli N, Dragojlovic-Kerkache A, Savelkoul P, Stassen FR. Plant-derived extracellular vesicles: current findings, challenges, and future applications. Membranes 2021; 11(6): 411.
[http://dx.doi.org/10.3390/membranes11060411] [PMID: 34072600]
[8]
Garaeva L, Kamyshinsky R, Kil Y, et al. Delivery of functional exogenous proteins by plant-derived vesicles to human cells in vitro. Sci Rep 2021; 11(1): 6489.
[http://dx.doi.org/10.1038/s41598-021-85833-y] [PMID: 33753795]
[9]
Teng Y, Ren Y, Sayed M, et al. Plant-derived exosomal microRNAs shape the gut microbiota. Cell Host Microbe 2018; 24(5): 637-652.e8.
[http://dx.doi.org/10.1016/j.chom.2018.10.001] [PMID: 30449315]
[10]
Gao L, Jiang F. MicroRNA (miRNA) Profiling. Methods Mol Biol 2016; 1381: 151-61.
[http://dx.doi.org/10.1007/978-1-4939-3204-7_8] [PMID: 26667459]
[11]
Garcia-Martin R, Wang G, Brandão BB, et al. MicroRNA sequence codes for small extracellular vesicle release and cellular retention. Nature 2022; 601(7893): 446-51.
[http://dx.doi.org/10.1038/s41586-021-04234-3] [PMID: 34937935]
[12]
Meyerowitz EM. Plants compared to animals: The broadest comparative study of development. Science 2002; 295(5559): 1482-5.
[http://dx.doi.org/10.1126/science.1066609] [PMID: 11859185]
[13]
Zhang L, Hou D, Chen X, et al. Exogenous plant MIR168a specifically targets mammalian LDLRAP1: Evidence of cross-kingdom regulation by microRNA. Cell Res 2012; 22(1): 107-26.
[http://dx.doi.org/10.1038/cr.2011.158] [PMID: 21931358]
[14]
Bartel DP. MicroRNAs: Genomics, biogenesis, mechanism, and function. cell 2004; 116(2): 281-97.
[15]
Lewis BP, Shih I, Jones-Rhoades MW, Bartel DP, Burge CB. Prediction of mammalian microRNA targets. Cell 2003; 115(7): 787-98.
[http://dx.doi.org/10.1016/S0092-8674(03)01018-3] [PMID: 14697198]
[16]
Enright AJ, John B, Gaul U, et al. MicroRNA targets in Drosophila. Genome Biol 2003; 5(1): R1.
[http://dx.doi.org/10.1186/gb-2003-5-1-r1] [PMID: 14709173]
[17]
Stark A, Brennecke J, Russell RB, Cohen SM. Identification of Drosophila microRNA targets. PLoS Biol 2003; 1(3): e60.
[http://dx.doi.org/10.1371/journal.pbio.0000060] [PMID: 14691535]
[18]
Xie Z, Kasschau KD, Carrington JC. Negative feedback regulation of Dicer-Like1 in Arabidopsis by microRNA-guided mRNA degradation. Curr Biol 2003; 13(9): 784-9.
[http://dx.doi.org/10.1016/S0960-9822(03)00281-1] [PMID: 12725739]
[19]
Ueguchi-Tanaka M, Hirano K, Hasegawa Y, Kitano H, Matsuoka M. Release of the repressive activity of rice DELLA protein SLR1 by gibberellin does not require SLR1 degradation in the gid2 mutant. Plant Cell 2008; 20(9): 2437-46.
[http://dx.doi.org/10.1105/tpc.108.061648] [PMID: 18827181]
[20]
Millar AA, Waterhouse PM. Plant and animal microRNAs: Similarities and differences. Funct Integr Genomics 2005; 5(3): 129-35.
[http://dx.doi.org/10.1007/s10142-005-0145-2] [PMID: 15875226]
[21]
Cui C, Wang Y, Liu J, Zhao J, Sun P, Wang S. A fungal pathogen deploys a small silencing RNA that attenuates mosquito immunity and facilitates infection. Nat Commun 2019; 10(1): 4298.
[http://dx.doi.org/10.1038/s41467-019-12323-1] [PMID: 31541102]
[22]
Sattar S, Song Y, Anstead JA, Sunkar R, Thompson GA. Cucumis melo microRNA expression profile during aphid herbivory in a resistant and susceptible interaction. Mol Plant Microbe Interact 2012; 25(6): 839-48.
[http://dx.doi.org/10.1094/MPMI-09-11-0252] [PMID: 22375710]
[23]
Duguet TB, Soichot J, Kuzyakiv R, Malmström L, Tritten L. Extracellular vesicle-contained microRNA of C. elegans as a tool to decipher the molecular basis of nematode parasitism. Front Cell Infect Microbiol 2020; 10: 217.
[http://dx.doi.org/10.3389/fcimb.2020.00217] [PMID: 32523895]
[24]
Ma J, Wang C, Long K, et al. Exosomal microRNAs in giant panda (Ailuropoda melanoleuca) breast milk: potential maternal regulators for the development of newborn cubs. Sci Rep 2017; 7(1): 3507.
[http://dx.doi.org/10.1038/s41598-017-03707-8] [PMID: 28615713]
[25]
Liang H, Zhang S, Fu Z, et al. Effective detection and quantification of dietetically absorbed plant microRNAs in human plasma. J Nutr Biochem 2015; 26(5): 505-12.
[http://dx.doi.org/10.1016/j.jnutbio.2014.12.002] [PMID: 25704478]
[26]
Chin AR, Fong MY, Somlo G, et al. Cross-kingdom inhibition of breast cancer growth by plant miR159. Cell Res 2016; 26(2): 217-28.
[http://dx.doi.org/10.1038/cr.2016.13] [PMID: 26794868]
[27]
Cavalieri D, Rizzetto L, Tocci N, et al. Plant microRNAs as novel immunomodulatory agents. Sci Rep 2016; 6(1): 25761.
[http://dx.doi.org/10.1038/srep25761] [PMID: 27167363]
[28]
Wang W, Hang C, Zhang Y, et al. Dietary miR-451 protects erythroid cells from oxidative stress via increasing the activity of Foxo3 pathway. Oncotarget 2017; 8(63): 107109-24.
[http://dx.doi.org/10.18632/oncotarget.22346] [PMID: 29291015]
[29]
Yang J, Elbaz-Younes I, Primo C, Murungi D, Hirschi KD. Intestinal permeability, digestive stability and oral bioavailability of dietary small RNAs. Sci Rep 2018; 8(1): 10253.
[http://dx.doi.org/10.1038/s41598-018-28207-1] [PMID: 29980707]
[30]
Yang J, Kongchan N, Primo Planta C, Neilson JR, Hirschi KD. The atypical genesis and bioavailability of the plant-based small RNA MIR2911: Bulking up while breaking down. Mol Nutr Food Res 2017; 61(9): 1600974.
[http://dx.doi.org/10.1002/mnfr.201600974] [PMID: 28319645]
[31]
Yang J, Hotz T, Broadnax L, Yarmarkovich M, Elbaz-Younes I, Hirschi KD. Anomalous uptake and circulatory characteristics of the plant-based small RNA MIR2911. Sci Rep 2016; 6(1): 26834.
[http://dx.doi.org/10.1038/srep26834] [PMID: 27251858]
[32]
Zhou Z, Li X, Liu J, et al. Honeysuckle-encoded atypical microRNA2911 directly targets influenza A viruses. Cell Res 2015; 25(1): 39-49.
[http://dx.doi.org/10.1038/cr.2014.130] [PMID: 25287280]
[33]
Liu S, da Cunha AP, Rezende RM, et al. The host shapes the gut microbiota via fecal microRNA. Cell Host Microbe 2016; 19(1): 32-43.
[http://dx.doi.org/10.1016/j.chom.2015.12.005] [PMID: 26764595]
[34]
Xiao J, Feng S, Wang X, et al. Identification of exosome-like nanoparticle-derived microRNAs from 11 edible fruits and vegetables. PeerJ 2018; 6: e5186.
[http://dx.doi.org/10.7717/peerj.5186] [PMID: 30083436]
[35]
Ionescu RF, Enache RM, Cretoiu SM, Cretoiu D. The Interplay Between Gut Microbiota and miRNAs in Cardiovascular Diseases. Front Cardiovasc Med 2022; 9: 856901.
[http://dx.doi.org/10.3389/fcvm.2022.856901] [PMID: 35369298]
[36]
Spinler JK, Oezguen N, Runge JK, et al. Dietary impact of a plant-derived microRNA on the gut microbiome. ExRNA 2020; 2(1): 11.
[http://dx.doi.org/10.1186/s41544-020-00053-2] [PMID: 33542959]
[37]
Díez-Sainz E, Lorente-Cebrián S, Aranaz P, Riezu-Boj JI, Martínez JA, Milagro FI. Potential mechanisms linking food-derived microRNAs, gut microbiota and intestinal barrier functions in the context of nutrition and human health. Front Nutr 2021; 8: 586564.
[http://dx.doi.org/10.3389/fnut.2021.586564] [PMID: 33768107]
[38]
Depommier C, Everard A, Druart C, et al. Supplementation with Akkermansia muciniphila in overweight and obese human volunteers: A proof-of-concept exploratory study. Nat Med 2019; 25(7): 1096-103.
[http://dx.doi.org/10.1038/s41591-019-0495-2] [PMID: 31263284]
[39]
Qin J, Li Y, Cai Z, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 2012; 490(7418): 55-60.
[http://dx.doi.org/10.1038/nature11450] [PMID: 23023125]
[40]
de Vos WM, Tilg H, Van Hul M, Cani PD. Gut microbiome and health: Mechanistic insights. Gut 2022; 71(5): 1020-32.
[http://dx.doi.org/10.1136/gutjnl-2021-326789] [PMID: 35105664]
[41]
Alfieri M, Leone A, Ambrosone A. Plant-derived nano and microvesicles for human health and therapeutic potential in nanomedicine. Pharmaceutics 2021; 13(4): 498.
[http://dx.doi.org/10.3390/pharmaceutics13040498] [PMID: 33917448]
[42]
Rutter BD, Innes RW. Growing pains: Addressing the pitfalls of plant extracellular vesicle research. New Phytol 2020; 228(5): 1505-10.
[http://dx.doi.org/10.1111/nph.16725] [PMID: 32506490]
[43]
Witwer KW, Zhang CY. Diet-derived microRNAs: Unicorn or silver bullet? Genes Nutr 2017; 12(1): 15.
[http://dx.doi.org/10.1186/s12263-017-0564-4] [PMID: 28694875]
[44]
Dickinson B, Zhang Y, Petrick JS, Heck G, Ivashuta S, Marshall WS. Lack of detectable oral bioavailability of plant microRNAs after feeding in mice. Nat Biotechnol 2013; 31(11): 965-7.
[http://dx.doi.org/10.1038/nbt.2737] [PMID: 24213763]
[45]
Huang H, Davis C, Wang T. Extensive degradation and low bioavailability of orally consumed corn miRNAs in mice. Nutrients 2018; 10(2): 215.
[http://dx.doi.org/10.3390/nu10020215] [PMID: 29462875]
[46]
Witwer KW, McAlexander MA, Queen SE, Adams RJ. Real-time quantitative PCR and droplet digital PCR for plant miRNAs in mammalian blood provide little evidence for general uptake of dietary miRNAs. RNA Biol 2013; 10(7): 1080-6.
[http://dx.doi.org/10.4161/rna.25246] [PMID: 23770773]
[47]
Snow JW, Hale AE, Isaacs SK, Baggish AL, Chan SY. Ineffective delivery of diet-derived microRNAs to recipient animal organisms. RNA Biol 2013; 10(7): 1107-16.
[http://dx.doi.org/10.4161/rna.24909] [PMID: 23669076]
[48]
Chan SY, Snow JW. Formidable challenges to the notion of biologically important roles for dietary small RNAs in ingesting mammals. Genes Nutr 2017; 12(1): 13.
[http://dx.doi.org/10.1186/s12263-017-0561-7] [PMID: 29308096]
[49]
Urzì O, Gasparro R, Ganji NR, Alessandro R, Raimondo S. Plant-RNA in extracellular vesicles: The secret of cross-kingdom communication. Membranes 2022; 12(4): 352.
[http://dx.doi.org/10.3390/membranes12040352] [PMID: 35448322]
[50]
Zempleni J, Sukreet S, Zhou F, Wu D, Mutai E. Milk-derived exosomes and metabolic regulation. Annu Rev Anim Biosci 2019; 7: 245-62.
[http://dx.doi.org/10.1146/annurev-animal-020518-115300]
[51]
Zhou F, Ebea P, Mutai E, et al. Small extracellular vesicles in milk cross the blood-brain barrier in murine cerebral cortex endothelial cells and promote dendritic complexity in the hippocampus and brain function in C57BL/6J mice. Front Nutr 2022; 9: 838543.
[http://dx.doi.org/10.3389/fnut.2022.838543] [PMID: 35600828]
[52]
Zhou F, Paz HA, Sadri M, et al. Dietary bovine milk exosomes elicit changes in bacterial communities in C57BL/6 mice. Am J Physiol Gastrointest Liver Physiol 2019; 317(5): G618-24.
[http://dx.doi.org/10.1152/ajpgi.00160.2019] [PMID: 31509432]
[53]
Oliveira MC, Arntz OJ, Blaney Davidson EN, et al. Milk extracellular vesicles accelerate osteoblastogenesis but impair bone matrix formation. J Nutr Biochem 2016; 30: 74-84.
[http://dx.doi.org/10.1016/j.jnutbio.2015.11.017] [PMID: 27012623]
[54]
Sedykh S, Kuleshova A, Nevinsky G. Milk exosomes: Perspective agents for anticancer drug delivery. Int J Mol Sci 2020; 21(18): 6646.
[http://dx.doi.org/10.3390/ijms21186646] [PMID: 32932782]
[55]
Kamerkar S, LeBleu VS, Sugimoto H, et al. Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer. Nature 2017; 546(7659): 498-503.
[http://dx.doi.org/10.1038/nature22341] [PMID: 28607485]
[56]
Baier SR, Nguyen C, Xie F, Wood JR, Zempleni J. 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(10): 1495-500.
[http://dx.doi.org/10.3945/jn.114.196436] [PMID: 25122645]
[57]
Hirschi KD. Uptake of dietary milk microRNAs by adult humans: rules for the game of hide and seek. J Nutr 2018; 148(1): 5-6.
[http://dx.doi.org/10.1093/jn/nxx065] [PMID: 29378059]
[58]
Melnik BC, Kakulas F, Geddes DT, et al. Milk miRNAs: simple nutrients or systemic functional regulators? Nutr Metab 2016; 13(1): 42.
[http://dx.doi.org/10.1186/s12986-016-0101-2] [PMID: 27330539]
[59]
Le Doare K, Holder B, Bassett A, Pannaraj PS. Mother’s milk: a purposeful contribution to the development of the infant microbiota and immunity. Front Immunol 2018; 9: 361.
[http://dx.doi.org/10.3389/fimmu.2018.00361] [PMID: 29599768]
[60]
Ogunnaike M, Wang H, Zempleni J. Bovine mammary alveolar MAC-T cells afford a tool for studies of bovine milk exosomes in drug delivery. Int J Pharm 2021; 610: 121263.
[http://dx.doi.org/10.1016/j.ijpharm.2021.121263] [PMID: 34742829]
[61]
Sidhom K, Obi PO, Saleem A. A review of exosomal isolation methods: Is size exclusion chromatography the best option? Int J Mol Sci 2020; 21(18): 6466.
[http://dx.doi.org/10.3390/ijms21186466] [PMID: 32899828]
[62]
Nguyen T. Unravelling the mysteries of microRNA in breast milk. Nature 2020; 582(7812): S12-3.
[http://dx.doi.org/10.1038/d41586-020-01768-w]
[63]
Manca S, Upadhyaya B, Mutai E, et al. Milk exosomes are bioavailable and distinct microRNA cargos have unique tissue distribution patterns. Sci Rep 2018; 8(1): 11321.
[http://dx.doi.org/10.1038/s41598-018-29780-1] [PMID: 30054561]
[64]
Aguilar-Lozano A, Baier S, Grove R, et al. Concentrations of purine metabolites are elevated in fluids from adults and infants and in livers from mice fed diets depleted of bovine milk exosomes and their RNA cargos. J Nutr 2018; 148(12): 1886-94.
[http://dx.doi.org/10.1093/jn/nxy223] [PMID: 30517726]
[65]
Mutai E, Ngu AKH, Zempleni J. Preliminary evidence that lectins in infant soy formula apparently bind bovine milk exosomes and prevent their absorption in healthy adults. BMC Nutr 2022; 8(1): 7.
[http://dx.doi.org/10.1186/s40795-022-00503-0] [PMID: 35063038]
[66]
Title AC, Denzler R, Stoffel M. Uptake and function studies of maternal milk-derived microRNAs. J Biol Chem 2015; 290(39): 23680-91.
[http://dx.doi.org/10.1074/jbc.M115.676734] [PMID: 26240150]
[67]
Mutai E, Ramer-Tait AE, Zempleni J. MicroRNAs in bovine milk exosomes are bioavailable in humans but do not elicit a robust pro-inflammatory cytokine response. ExRNA 2020; 2(1): 2.
[http://dx.doi.org/10.1186/s41544-019-0041-x]

Rights & Permissions Print Cite
Article Metrics
18
1
Wayfinder Image
© 2024 Bentham Science Publishers | Privacy Policy