Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Journal of Translational Medicine
Published in: Journal of Translational Medicine 1/2021

Open Access 01-12-2021 | Respiratory Microbiota | Review

Extracellular vesicle-derived miRNA as a novel regulatory system for bi-directional communication in gut-brain-microbiota axis

Authors: Liang Zhao, Yingze Ye, Lijuan Gu, Zhihong Jian, Creed M. Stary, Xiaoxing Xiong

Published in: Journal of Translational Medicine | Issue 1/2021

Login to get access

Abstract

The gut-brain-microbiota axis (GBMAx) coordinates bidirectional communication between the gut and brain, and is increasingly recognized as playing a central role in physiology and disease. MicroRNAs are important intracellular components secreted by extracellular vesicles (EVs), which act as vital mediators of intercellular and interspecies communication. This review will present current advances in EV-derived microRNAs and their potential functional link with GBMAx. We propose that EV-derived microRNAs comprise a novel regulatory system for GBMAx, and a potential novel therapeutic target for modifying GBMAx in clinical therapy.
Literature
1.
Beaumont W. Nutrition classics. Experiments and observations on the gastric juice and the physiology of digestion By william Beaumont. Plattsburgh. Printed by f. P. Allen. 1833. Nutr Rev. 1977;35:144–5.PubMedCrossRef
2.
3.
CANNON. The influence of emotional states on the functions of the alimentary canal. Sciences. 1909;137:480–486
4.
5.
Zhou G, Zhou Y, Chen X. New insight into inter-kingdom communication: horizontal transfer of mobile small RNAs. Front Microbiol. 2017;1(8):768.CrossRef
6.
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.PubMedCrossRef
7.
Liu S, da Cunha AP, Rezende RM, Cialic R, Wei Z, Bry L, et al. The host shapes the gut microbiota via fecal microrna. Cell Host Microbe. 2016;19:32–43.PubMedPubMedCentralCrossRef
8.
Ahmadi Badi S, Moshiri A, Fateh A, Rahimi Jamnani F, Sarshar M, Vaziri F, Siadat SD. Microbiota-derived extracellular vesicles as new systemic regulators. Front Microbiol. 2017;24(8):1610.CrossRef
9.
Maloy KJ, Powrie F. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature. 2011;474(7351):298–306.PubMedCrossRef
10.
11.
Foster JA, McVey Neufeld KA. Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci. 2013;36(5):305–12.PubMedCrossRef
12.
Matteoli G, Boeckxstaens GE. The vagal innervation of the gut and immune homeostasis. Gut. 2013;62(8):1214–22.PubMedCrossRef
13.
14.
Bercik P, Park AJ, Sinclair D, Khoshdel A, Lu J, Huang X, et al. The anxiolytic effect of bifidobacterium longum ncc3001 involves vagal pathways for gut-brain communication. Neurogastroenterol Motil. 2011;23:1132–9.PubMedPubMedCentralCrossRef
15.
16.
17.
18.
Kim VN, Han J, Siomi MC. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol. 2009;10(2):126–39.PubMedCrossRef
19.
20.
21.
22.
23.
Li LC, Okino ST, Zhao H, Pookot D, Place RF, Urakami S, Enokida H, Dahiya R. Small dsRNAs induce transcriptional activation in human cells. Proc Natl Acad Sci USA. 2006;103(46):17337–42.PubMedCrossRefPubMedCentral
24.
Janowski BA, Younger ST, Hardy DB, Ram R, Huffman KE, Corey DR. Activating gene expression in mammalian cells with promoter-targeted duplex RNAs. Nat Chem Biol. 2007;3(3):166–73.PubMedCrossRef
25.
Vasudevan S, Tong Y, Steitz JA. Switching from repression to activation: microRNAs can up-regulate translation. Science. 2007;318(5858):1931–4.PubMedCrossRef
26.
27.
28.
29.
Diaz-Garrido N, Cordero C, Olivo-Martinez Y, Badia J, Baldomà L. Cell-to-cell communication by host-released extracellular vesicles in the gut: implications in health and disease. Int J Mol Sci. 2021;22(4):2213.PubMedPubMedCentralCrossRef
30.
Cui M, Xiao H, Li Y, Dong J, Luo D, Li H, Feng G, Wang H, Fan S. Total abdominal irradiation exposure impairs cognitive function involving miR-34a-5p/BDNF axis. Biochim Biophys Acta Mol Basis Dis. 2017;1863(9):2333–41.PubMedCrossRef
31.
Yuan C, Burns MB, Subramanian S, Blekhman R. Interaction between Host MicroRNAs and the gut microbiota in colorectal cancer. mSystems. 2018;3(3):e00205-17.PubMedPubMedCentralCrossRef
32.
Ji Y, Li X, Zhu Y, Li N, Zhang N, Niu M. Faecal microRNA as a biomarker of the activity and prognosis of inflammatory bowel diseases. Biochem Biophys Res Commun. 2018;503(4):2443–50.PubMedCrossRef
33.
Dalmasso G, Nguyen HT, Yan Y, Laroui H, Charania MA, Ayyadurai S, Sitaraman SV, Merlin D. Microbiota modulate host gene expression via microRNAs. PLoS ONE. 2011;6(4):e19293.PubMedPubMedCentralCrossRef
34.
Viennois E, Chassaing B, Tahsin A, Pujada A, Wang L, Gewirtz AT, et al. Host-derived fecal micrornas can indicate gut microbiota healthiness and ability to induce inflammation. Theranostics. 2019;9:4542–57.PubMedPubMedCentralCrossRef
35.
Peck BC, Mah AT, Pitman WA, Ding S, Lund PK, Sethupathy P. Functional transcriptomics in diverse intestinal epithelial cell types reveals robust microRNA sensitivity in intestinal stem cells to microbial status. J Biol Chem. 2017;292(7):2586–600.PubMedPubMedCentralCrossRef
36.
Moloney GM, Viola MF, Hoban AE, Dinan TG, Cryan JF. Faecal microRNAs: indicators of imbalance at the host-microbe interface? Benef Microbes. 2018;9(2):175–83.PubMedCrossRef
37.
Xue X, Feng T, Yao S, Wolf KJ, Liu CG, Liu X, Elson CO, Cong Y. Microbiota downregulates dendritic cell expression of miR-10a, which targets IL-12/IL-23p40. J Immunol. 2011;187(11):5879–86.PubMedCrossRef
38.
Nakata K, Sugi Y, Narabayashi H, Kobayakawa T, Nakanishi Y, Tsuda M, Hosono A, Kaminogawa S, Hanazawa S, Takahashi K. Commensal microbiota-induced microRNA modulates intestinal epithelial permeability through the small GTPase ARF4. J Biol Chem. 2017;292(37):15426–33.PubMedPubMedCentralCrossRef
39.
Dalmasso G, Nguyen HTT, Faïs T, Massier S, Barnich N, Delmas J, Bonnet R. Crohn’s disease-associated adherent-invasive Escherichia coli manipulate host autophagy by impairing SUMOylation. Cells. 2019;8(1):35.PubMedCentralCrossRef
40.
Veltman K, Hummel S, Cichon C, Sonnenborn U, Schmidt MA. Identification of specific miRNAs targeting proteins of the apical junctional complex that simulate the probiotic effect of E. coli Nissle 1917 on T84 epithelial cells. Int J Biochem Cell Biol. 2012;44(2):341–9.PubMedCrossRef
41.
Sabharwal H, Cichon C, Ölschläger TA, Sonnenborn U, Schmidt MA. Interleukin-8, CXCL1, and MicroRNA miR-146a Responses to Probiotic Escherichia coli Nissle 1917 and Enteropathogenic E. coli in Human Intestinal Epithelial T84 and Monocytic THP-1 Cells after Apical or Basolateral Infection. Infect Immun. 2016;84(9):2482–92.PubMedPubMedCentralCrossRef
42.
Kreuzer-Redmer S, Bekurtz JC, Arends D, Bortfeldt R, Kutz-Lohroff B, Sharbati S, et al. Feeding of enterococcus faecium ncimb 10415 leads to intestinal mirna-423-5p-induced regulation of immune-relevant genes. Appl Environ Microbiol. 2016;82:2263–9.PubMedPubMedCentralCrossRef
43.
Rodriguez-Nogales A, Algieri F, Garrido-Mesa J, Vezza T, Utrilla MP, Chueca N, et al. Differential intestinal anti-inflammatory effects of lactobacillus fermentum and lactobacillus salivarius in dss mouse colitis: Impact on micrornas expression and microbiota composition. Mol Nutr Food Res. 2017;61:1.CrossRef
44.
Hoban AE, Stilling RM, Moloney RD, Shanahan F, Dinan TG, et al. Microbial regulation of microrna expression in the amygdala and prefrontal cortex. Microbiome. 2017;5:102.PubMedPubMedCentralCrossRef
45.
Moloney GM, O’Leary OF, Salvo-Romero E, Desbonnet L, Shanahan F, Dinan TG, et al. Microbial regulation of hippocampal mirna expression: Implications for transcription of kynurenine pathway enzymes. Behav Brain Res. 2017;334:50–4.PubMedCrossRef
46.
Chen JJ, Zeng BH, Li WW, Zhou CJ, Fan SH, Cheng K, et al. Effects of gut microbiota on the microrna and mrna expression in the hippocampus of mice. Behav Brain Res. 2017;322:34–41.PubMedCrossRef
47.
Hoban AE, Stilling RM, Moloney G, Moloney RD, Shanahan F, Dinan TG, Cryan JF, Clarke G. Microbial regulation of microRNA expression in the amygdala and prefrontal cortex. Microbiome. 2017;5(1):102.PubMedPubMedCentralCrossRef
48.
Kumar M, Singh P, Murugesan S, Vetizou M, McCulloch J, Badger JH, et al. Microbiome as an immunological modifier. In: Thurin M, Cesano A, Marincola FM, editors., et al., Biomarkers for immunotherapy of cancer: Methods and protocols. New York: Springer; 2020. p. 595–638.
49.
50.
Akers JC, Gonda D, Kim R, Carter BS, Chen CC. Biogenesis of extracellular vesicles (ev): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J Neurooncol. 2013;113:1–11.PubMedPubMedCentralCrossRef
51.
Taylor DD, Zacharias W, Gercel-Taylor C. Exosome isolation for proteomic analyses and RNA profiling. Methods Mol Biol. 2011;728:235–46.PubMedCrossRef
52.
Matsuo H, Chevallier J, Mayran N, Le Blanc I, Ferguson C, Fauré J, Blanc NS, Matile S, Dubochet J, Sadoul R, Parton RG, Vilbois F, Gruenberg J. Role of LBPA and Alix in multivesicular liposome formation and endosome organization. Science. 2004;303(5657):531–4.PubMedCrossRef
53.
Pant S, Hilton H, Burczynski ME. The multifaceted exosome: biogenesis, role in normal and aberrant cellular function, and frontiers for pharmacological and biomarker opportunities. Biochem Pharmacol. 2012;83(11):1484–94.PubMedCrossRef
54.
Colombo M, Raposo G, Théry C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014;30:255–89.PubMedCrossRef
55.
Abels ER, Breakefield XO. Introduction to extracellular vesicles: biogenesis, RNA cargo selection, content, release, and uptake. Cell Mol Neurobiol. 2016;36(3):301–12.PubMedPubMedCentralCrossRef
56.
57.
Zomer A, Maynard C, Verweij FJ, Kamermans A, Schäfer R, Beerling E, Schiffelers RM, de Wit E, Berenguer J, Ellenbroek SIJ, Wurdinger T, Pegtel DM, van Rheenen J. In Vivo imaging reveals extracellular vesicle-mediated phenocopying of metastatic behavior. Cell. 2015;161(5):1046–57.PubMedPubMedCentralCrossRef
58.
Keerthikumar S, Chisanga D, Ariyaratne D, Al Saffar H, Anand S, Zhao K, Samuel M, Pathan M, Jois M, Chilamkurti N, Gangoda L, Mathivanan S. ExoCarta: a web-based compendium of exosomal cargo. J Mol Biol. 2016;428(4):688–92.PubMedCrossRef
59.
Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic Mark M, Molina H, Kohsaka S, Di Giannatale A, Ceder S, Singh S, Williams C, Soplop N, Uryu K, Pharmer L, King T, Bojmar L, Davies AE, Ararso Y, Zhang T, Zhang H, Hernandez J, Weiss JM, Dumont-Cole VD, Kramer K, Wexler LH, Narendran A, Schwartz GK, Healey JH, Sandstrom P, Labori KJ, Kure EH, Grandgenett PM, Hollingsworth MA, de Sousa M, Kaur S, Jain M, Mallya K, Batra SK, Jarnagin WR, Brady MS, Fodstad O, Muller V, Pantel K, Minn AJ, Bissell MJ, Garcia BA, Kang Y, Rajasekhar VK, Ghajar CM, Matei I, Peinado H, Bromberg J, Lyden D. Tumour exosome integrins determine organotropic metastasis. Nature. 2015;527(7578):329–35.PubMedPubMedCentralCrossRef
60.
Sastre B, Cañas JA, Rodrigo-Muñoz JM, Del Pozo V. Novel Modulators of Asthma and Allergy: Exosomes and MicroRNAs. Front Immunol. 2017;21(8):826.CrossRef
61.
Blandford SN, Galloway DA, Moore CS. The roles of extracellular vesicle microRNAs in the central nervous system. Glia. 2018;66(11):2267–78.PubMedCrossRef
62.
Chen JJ, Zhao B, Zhao J, Li S. Potential roles of exosomal MicroRNAs as diagnostic biomarkers and therapeutic application in Alzheimer’s disease. Neural Plast. 2017;2017:7027380.PubMedPubMedCentralCrossRef
63.
Liang X, Zhang L, Wang S, Han Q, Zhao RC. Exosomes secreted by mesenchymal stem cells promote endothelial cell angiogenesis by transferring miR-125a. J Cell Sci. 2016;129(11):2182–9.PubMedCrossRef
64.
Maemura T, Fukuyama S, Sugita Y, Lopes TJS, Nakao T, Noda T, Kawaoka Y. Lung-derived exosomal miR-483-3p regulates the innate immune response to influenza virus infection. J Infect Dis. 2018;217(9):1372–82.PubMedCrossRef
65.
Salehi M, Sharifi M. Exosomal miRNAs as novel cancer biomarkers: challenges and opportunities. J Cell Physiol. 2018;233(9):6370–80.PubMedCrossRef
66.
Wang S, Wang JQ, Lv XW. Exosomal miRNAs as biomarkers in the diagnosis of liver disease. Biomark Med. 2017;11(6):491–501.PubMedCrossRef
67.
Qiu G, Zheng G, Ge M, Wang J, Huang R, Shu Q. Mesenchymal stem cell-derived extracellular vesicles affect disease outcomes via transfer of micrornas. Stem Cell Res Ther. 2018;9:320.PubMedPubMedCentralCrossRef
68.
Wang M, Yu F, Ding H, Wang Y, Li P, Wang K. Emerging function and clinical values of exosomal micrornas in cancer. Mol Ther Nucleic Acids. 2019;16:791–804.PubMedPubMedCentralCrossRef
69.
Yoshikawa FSY, Teixeira FME, Sato MN, Oliveira L. Delivery of micrornas by extracellular vesicles in viral infections: could the news be packaged? Cells. 2019;8:1.CrossRef
70.
Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mrnas and micrornas is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9:654–9.PubMedCrossRef
71.
Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol. 2009;11(9):1143–9.PubMedCrossRef
72.
Koppers-Lalic D, Hackenberg M, Bijnsdorp IV, van Eijndhoven MAJ, Sadek P, Sie D, Zini N, Middeldorp JM, Ylstra B, de Menezes RX, Würdinger T, Meijer GA, Pegtel DM. Nontemplated nucleotide additions distinguish the small RNA composition in cells from exosomes. Cell Rep. 2014;8(6):1649–58.PubMedCrossRef
73.
Kosaka N, Iguchi H, Hagiwara K, Yoshioka Y, Takeshita F, Ochiya T. Neutral sphingomyelinase 2 (nSMase2)-dependent exosomal transfer of angiogenic microRNAs regulate cancer cell metastasis. J Biol Chem. 2013;288(15):10849–59.PubMedPubMedCentralCrossRef
74.
Lee YS, Pressman S, Andress AP, Kim K, White JL, Cassidy JJ, Li X, Lubell K, Lim DH, Cho IS, Nakahara K, Preall JB, Bellare P, Sontheimer EJ, Carthew RW. Silencing by small RNAs is linked to endosomal trafficking. Nat Cell Biol. 2009;11(9):1150–6.PubMedPubMedCentralCrossRef
75.
Villarroya-Beltri C, Gutiérrez-Vázquez C, Sánchez-Cabo F, Pérez-Hernández D, Vázquez J, Martin-Cofreces N, Martinez-Herrera DJ, Pascual-Montano A, Mittelbrunn M, Sánchez-Madrid F. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun. 2013;4:2980.PubMedCrossRef
76.
Zhang J, Li S, Li L, Li M, Guo C, Yao J, Mi S. Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinform. 2015;13(1):17–24.CrossRef
77.
Sluijter JPG, Davidson SM, Boulanger CM, Buzás EI, de Kleijn DPV, Engel FB, Giricz Z, Hausenloy DJ, Kishore R, Lecour S, Leor J, Madonna R, Perrino C, Prunier F, Sahoo S, Schiffelers RM, Schulz R, Van Laake LW, Ytrehus K, Ferdinandy P. Extracellular vesicles in diagnostics and therapy of the ischaemic heart: Position Paper from the Working Group on Cellular Biology of the Heart of the European Society of Cardiology. Cardiovasc Res. 2018;114(1):19–34.PubMedCrossRef
78.
Coumans FAW, Brisson AR, Buzas EI, Dignat-George F, Drees EEE, El-Andaloussi S, Emanueli C, Gasecka A, Hendrix A, Hill AF, Lacroix R, Lee Y, van Leeuwen TG, Mackman N, Mäger I, Nolan JP, van der Pol E, Pegtel DM, Sahoo S, Siljander PRM, Sturk G, de Wever O, Nieuwland R. Methodological guidelines to study extracellular vesicles. Circ Res. 2017;120(10):1632–48.PubMedCrossRef
79.
Ridger VC, Boulanger CM, Angelillo-Scherrer A, Badimon L, Blanc-Brude O, Bochaton-Piallat ML, Boilard E, Buzas EI, Caporali A, Dignat-George F, Evans PC, Lacroix R, Lutgens E, Ketelhuth DFJ, Nieuwland R, Toti F, Tunon J, Weber C, Hoefer IE. Microvesicles in vascular homeostasis and diseases Position Paper of the European Society of Cardiology (ESC) Working Group on Atherosclerosis and Vascular Biology. Thromb Haemost. 2017;117(7):1296–316.PubMedCrossRef
80.
Wang T, Turko IV. Proteomic toolbox to standardize the separation of extracellular vesicles and lipoprotein particles. J Proteome Res. 2018;17(9):3104–13.PubMedPubMedCentralCrossRef
81.
Simonsen JB. What are we looking at? Extracellular vesicles, lipoproteins, or both? Circ Res. 2017;121(8):920–2.PubMedCrossRef
82.
Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG. Caveolin, a protein component of caveolae membrane coats. Cell. 1992;68:673–82.PubMedCrossRef
83.
Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, et al. Syndecan-syntenin-alix regulates the biogenesis of exosomes. Nat Cell Biol. 2012;14:677–85.PubMedCrossRef
84.
Li B, Antonyak MA, Zhang J, Cerione RA. Rhoa triggers a specific signaling pathway that generates transforming microvesicles in cancer cells. Oncogene. 2012;31:4740–9.PubMedPubMedCentralCrossRef
85.
Verderio C, Gabrielli M, Giussani P. Role of sphingolipids in the biogenesis and biological activity of extracellular vesicles. J Lipid Res. 2018;59:1325–40.PubMedPubMedCentralCrossRef
86.
Russell AE, Sneider A, Witwer KW, Bergese P, Bhattacharyya SN, Cocks A, et al. Biological membranes in ev biogenesis, stability, uptake, and cargo transfer: An isev position paper arising from the isev membranes and evs workshop. J Extracell Vesicles. 2019;8:1684862.PubMedPubMedCentralCrossRef
87.
Taylor J, Azimi I, Monteith G, Bebawy M. Ca(2+) mediates extracellular vesicle biogenesis through alternate pathways in malignancy. J Extracell Vesic. 2020;9:1734326–1734326.CrossRef
88.
David G, Zimmermann P. Heparanase involvement in exosome formation. Adv Exp Med Biol. 2020;1221:285–307.PubMedCrossRef
89.
Groot M, Lee H. Sorting mechanisms for micrornas into extracellular vesicles and their associated diseases. Cells. 2020;9:1.CrossRef
90.
McNamara RP, Costantini LM, Myers TA, Schouest B, Maness NJ, Griffith JD, et al. Nef secretion into extracellular vesicles or exosomes is conserved across human and simian immunodeficiency viruses. mBio. 2018;9:1.CrossRef
91.
Jones LB, Kumar S, Curry AJ, Price JS, Krendelchtchikov A, Crenshaw BJ, et al. Alcohol exposure impacts the composition of hela-derived extracellular vesicles. Biomedicines. 2019;7:1.CrossRef
92.
Jabbari N, Karimipour M, Khaksar M, Akbariazar E, Heidarzadeh M, Mojarad B, et al. Tumor-derived extracellular vesicles: Insights into bystander effects of exosomes after irradiation. Lasers Med Sci. 2020;35:531–45.PubMedCrossRef
93.
Kumar A, Deep G. Hypoxia in tumor microenvironment regulates exosome biogenesis: molecular mechanisms and translational opportunities. Cancer Lett. 2020;479:23–30.PubMedCrossRef
94.
Gallart-Palau X, Guo X, Serra A, Sze SK. Alzheimer’s disease progression characterized by alterations in the molecular profiles and biogenesis of brain extracellular vesicles. Alzheimers Res Ther. 2020;12:54.PubMedPubMedCentralCrossRef
95.
Nakamura Y, Kita S, Tanaka Y, Fukuda S, Obata Y, Okita T, et al. Adiponectin stimulates exosome release to enhance mesenchymal stem-cell-driven therapy of heart failure in mice. Mol Ther. 2020;28(10):2203–19.PubMedPubMedCentralCrossRef
96.
Creemers EE, Tijsen AJ, Pinto YM. Circulating microRNAs: novel biomarkers and extracellular communicators in cardiovascular disease? Circ Res. 2012;110(3):483–95.PubMedCrossRef
97.
Williams MR, Stedtfeld RD, Tiedje JM, Hashsham SA. MicroRNAs-based inter-domain communication between the host and members of the gut microbiome. Front Microbiol. 2017;27(8):1896.CrossRef
98.
Pegtel DM, Peferoen L, Amor S. Extracellular vesicles as modulators of cell-to-cell communication in the healthy and diseased brain. Philos Trans R Soc Lond B Biol Sci. 2014;369(1652):20130516.PubMedPubMedCentralCrossRef
99.
Antonucci F, Turola E, Riganti L, Caleo M, Gabrielli M, Perrotta C, Novellino L, Clementi E, Giussani P, Viani P, Matteoli M, Verderio C. Microvesicles released from microglia stimulate synaptic activity via enhanced sphingolipid metabolism. EMBO J. 2012;31(5):1231–40.PubMedPubMedCentralCrossRef
100.
Fröhlich D, Kuo WP, Frühbeis C, Sun JJ, Zehendner CM, Luhmann HJ, Pinto S, Toedling J, Trotter J, Krämer-Albers EM. Multifaceted effects of oligodendroglial exosomes on neurons: impact on neuronal firing rate, signal transduction and gene regulation. Philos Trans R Soc Lond B Biol Sci. 2014;369(1652):20130510.PubMedPubMedCentralCrossRef
101.
Luarte A, Cisternas P, Caviedes A, Batiz LF, Lafourcade C, Wyneken U, Henzi R. Astrocytes at the hub of the stress response: potential modulation of neurogenesis by miRNAs in astrocyte-derived exosomes. Stem Cells Int. 2017;2017:1719050.PubMedPubMedCentralCrossRef
102.
103.
Balusu S, Van Wonterghem E, De Rycke R, Raemdonck K, Stremersch S, Gevaert K, Brkic M, Demeestere D, Vanhooren V, Hendrix A, Libert C, Vandenbroucke RE. Identification of a novel mechanism of blood-brain communication during peripheral inflammation via choroid plexus-derived extracellular vesicles. EMBO Mol Med. 2016;8(10):1162–83.PubMedPubMedCentralCrossRef
104.
Park S, Ahn ES, Kim Y. Neuroblastoma SH-SY5Y cell-derived exosomes stimulate dendrite-like outgrowths and modify the differentiation of A375 melanoma cells. Cell Biol Int. 2015;39(4):379–87.PubMedCrossRef
105.
Trotta T, Panaro MA, Cianciulli A, Mori G, Di Benedetto A, Porro C. Microglia-derived extracellular vesicles in alzheimer’s disease: A double-edged sword. Biochem Pharmacol. 2018;148:184–92.PubMedCrossRef
106.
Welton JL, Loveless S, Stone T, von Ruhland C, Robertson NP, Clayton A. Cerebrospinal fluid extracellular vesicle enrichment for protein biomarker discovery in neurological disease; multiple sclerosis. J Extracell Vesicles. 2017;6(1):1369805.PubMedPubMedCentralCrossRef
107.
Figueroa JM, Skog J, Akers J, Li H, Komotar R, Jensen R, Ringel F, Yang I, Kalkanis S, Thompson R, LoGuidice L, Berghoff E, Parsa A, Liau L, Curry W, Cahill D, Bettegowda C, Lang FF, Chiocca EA, Henson J, Kim R, Breakefield X, Chen C, Messer K, Hochberg F, Carter BS. Detection of wild-type EGFR amplification and EGFRvIII mutation in CSF-derived extracellular vesicles of glioblastoma patients. Neuro Oncol. 2017;19(11):1494–502.PubMedPubMedCentralCrossRef
108.
Kawikova I, Askenase PW. Diagnostic and therapeutic potentials of exosomes in CNS diseases. Brain Res. 2015;18(1617):63–71.CrossRef
109.
Osier N, Motamedi V, Edwards K, Puccio A, Diaz-Arrastia R, Kenney K, Gill J. Exosomes in acquired neurological disorders: new insights into pathophysiology and treatment. Mol Neurobiol. 2018;55(12):9280–93.PubMedCrossRef
110.
Ciregia F, Urbani A, Palmisano G. Extracellular vesicles in brain tumors and neurodegenerative diseases. Front Mol Neurosci. 2017;31(10):276.CrossRef
111.
Lee Y, Park JY, Lee EH, Yang J, Jeong BR, Kim YK, Seoh JY, Lee S, Han PL, Kim EJ. Rapid assessment of microbiota changes in individuals with autism spectrum disorder using bacteria-derived membrane vesicles in urine. Exp Neurobiol. 2017;26(5):307–17.PubMedPubMedCentralCrossRef
112.
Rufino-Ramos D, Albuquerque PR, Carmona V, Perfeito R, Nobre RJ, Almeida L. Extracellular vesicles: Novel promising delivery systems for therapy of brain diseases. J Control Release. 2017;262:247–58.PubMedCrossRef
113.
Yuan D, Zhao Y, Banks WA, Bullock KM, Haney M, Batrakova E, Kabanov AV. Macrophage exosomes as natural nanocarriers for protein delivery to inflamed brain. Biomaterials. 2017;142:1–12.PubMedPubMedCentralCrossRef
114.
Murgoci AN, Cizkova D, Majerova P, Petrovova E, Medvecky L, Fournier I, Salzet M. Brain-cortex microglia-derived exosomes: nanoparticles for glioma therapy. ChemPhysChem. 2018;19(10):1205–14.PubMedCrossRef
115.
Venkat P, Chen J, Chopp M. Exosome-mediated amplification of endogenous brain repair mechanisms and brain and systemic organ interaction in modulating neurological outcome after stroke. J Cereb Blood Flow Metab. 2018;38(12):2165–78.PubMedPubMedCentralCrossRef
116.
Otero-Ortega L, de Frutos MC, Laso-García F, Rodríguez-Frutos B, Medina-Gutiérrez E, López JA, Vázquez J, Díez-Tejedor E, Gutiérrez-Fernández M. Exosomes promote restoration after an experimental animal model of intracerebral hemorrhage. J Cereb Blood Flow Metab. 2018;38(5):767–79.PubMedCrossRef
117.
Yelamanchili SV, Lamberty BG, Rennard DA, Morsey BM, Hochfelder CG, Meays BM, Levy E, Fox HS. Correction: MiR-21 in extracellular vesicles leads to neurotoxicity via TLR7 signaling in SIV neurological Disease. PLoS Pathog. 2018;14(5):e1007068.PubMedPubMedCentralCrossRef
118.
Banigan MG, Kao PF, Kozubek JA, Winslow AR, Medina J, Costa J, Schmitt A, Schneider A, Cabral H, Cagsal-Getkin O, Vanderburg CR, Delalle I. Differential expression of exosomal microRNAs in prefrontal cortices of schizophrenia and bipolar disorder patients. PLoS ONE. 2013;8(1):e48814.PubMedPubMedCentralCrossRef
119.
Yang JK, Yang JP, Tong J, Jing SY, Fan B, Wang F, Sun GZ, Jiao BH. Exosomal miR-221 targets DNM3 to induce tumor progression and temozolomide resistance in glioma. J Neurooncol. 2017;131(2):255–65.PubMedCrossRef
120.
Zhang L, Zhang S, Yao J, Lowery FJ, Zhang Q, Huang WC, Li P, Li M, Wang X, Zhang C, Wang H, Ellis K, Cheerathodi M, McCarty JH, Palmieri D, Saunus J, Lakhani S, Huang S, Sahin AA, Aldape KD, Steeg PS, Yu D. Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth. Nature. 2015;527(7576):100–4.PubMedPubMedCentralCrossRef
121.
Picciolini S, Gualerzi A, Vanna R, Sguassero A, Gramatica F, Bedoni M, Masserini M, Morasso C. Detection and characterization of different brain-derived subpopulations of plasma exosomes by surface plasmon resonance imaging. Anal Chem. 2018;90(15):8873–80.PubMedCrossRef
122.
Patterson SA, Deep G, Brinkley TE. Detection of the receptor for advanced glycation endproducts in neuronally-derived exosomes in plasma. Biochem Biophys Res Commun. 2018;500(4):892–6.PubMedPubMedCentralCrossRef
123.
Gamez-Valero A, Campdelacreu J, Vilas D, Ispierto L, Rene R, Alvarez R, et al. Exploratory study on microrna profiles from plasma-derived extracellular vesicles in alzheimer’s disease and dementia with lewy bodies. Transl Neurodegener. 2019;8:31.PubMedPubMedCentralCrossRef
124.
Cha DJ, Mengel D, Mustapic M, Liu W, Selkoe DJ, Kapogiannis D, et al. Mir-212 and mir-132 are downregulated in neurally derived plasma exosomes of alzheimer’s patients. Front Neurosci. 2019;13:1208.PubMedPubMedCentralCrossRef
125.
Serpente M, Fenoglio C, D’Anca M, Arcaro M, Sorrentino F, Visconte C, et al. Mirna profiling in plasma neural-derived small extracellular vesicles from patients with alzheimer’s disease. Cells. 2020;9:1.CrossRef
126.
Chatterjee SN, Das J. Electron microscopic observations on the excretion of cell-wall material by Vibrio cholerae. J Gen Microbiol. 1967;49(1):1–11.PubMedCrossRef
127.
Zhou L, Srisatjaluk R, Justus DE, Doyle RJ. On the origin of membrane vesicles in gram-negative bacteria. FEMS Microbiol Lett. 1998;163(2):223–8.PubMedCrossRef
128.
Yu YJ, Wang XH, Fan GC. Versatile effects of bacterium-released membrane vesicles on mammalian cells and infectious/inflammatory diseases. Acta Pharmacol Sin. 2018;39:514–33.PubMedCrossRef
129.
Yoon H. Bacterial outer membrane vesicles as a delivery system for virulence regulation. J Microbiol Biotechnol. 2016;26(8):1343–7.PubMedCrossRef
130.
Pathirana RD, Kaparakis-Liaskos M. Bacterial membrane vesicles: biogenesis, immune regulation and pathogenesis. Cell Microbiol. 2016;18:1518–24.PubMedCrossRef
131.
Gao XJ, Li T, Wei B, Yan ZX, Hu N, Huang YJ, et al. Bacterial outer membrane vesicles from dextran sulfate sodium-induced colitis differentially regulate intestinal udp-glucuronosyltransferase 1a1 partially through toll-like receptor 4/mitogen-activated protein kinase/phosphatidylinositol 3-kinase pathway. Drug Metab Dispos. 2018;46:292–302.PubMedCrossRef
132.
Vanaja SK, Russo AJ, Behl B, Banerjee I, Yankova M, Deshmukh SD, Rathinam VAK. Bacterial outer membrane vesicles mediate cytosolic localization of LPS and caspase-11 activation. Cell. 2016;165(5):1106–19.PubMedPubMedCentralCrossRef
133.
Shah B, Sullivan CJ, Lonergan NE, Stanley S, Soult MC, Britt LD. Circulating bacterial membrane vesicles cause sepsis in rats. Shock. 2012;37(6):621–8.PubMedCrossRef
134.
Kaparakis-Liaskos M, Ferrero RL. Immune modulation by bacterial outer membrane vesicles. Nat Rev Immunol. 2015;15(6):375–87.PubMedCrossRef
135.
Crowley JT, Toledo AM, LaRocca TJ, Coleman JL, London E, Benach JL. Lipid exchange between Borrelia burgdorferi and host cells. PLoS Pathog. 2013;9(1):e1003109.PubMedPubMedCentralCrossRef
136.
Soult MC, Dobrydneva Y, Wahab KH, Britt LD, Sullivan CJ. Outer membrane vesicles alter inflammation and coagulation mediators. J Surg Res. 2014;192(1):134–42.PubMedCrossRef
137.
Kim JH, Yoon YJ, Lee J, Choi EJ, Yi N, Park KS, Park J, Lötvall J, Kim YK, Gho YS. Outer membrane vesicles derived from Escherichia coli up-regulate expression of endothelial cell adhesion molecules in vitro and in vivo. PLoS ONE. 2013;8(3):e59276.PubMedPubMedCentralCrossRef
138.
Jung AL, Stoiber C, Herkt CE, Schulz C, Bertrams W, Schmeck B. Legionella pneumophila-derived outer membrane vesicles promote bacterial replication in macrophages. PLoS Pathog. 2016;12(4):e1005592.PubMedPubMedCentralCrossRef
139.
Jager J, Keese S, Roessle M, Steinert M, Schromm AB. Fusion of legionella pneumophila outer membrane vesicles with eukaryotic membrane systems is a mechanism to deliver pathogen factors to host cell membranes. Cell Microbiol. 2015;17:607–20.PubMedCrossRef
140.
Roberts R, Moreno G, Bottero D, Gaillard ME, Fingermann M, Graieb A, Rumbo M, Hozbor D. Outer membrane vesicles as acellular vaccine against pertussis. Vaccine. 2008;26(36):4639–46.PubMedCrossRef
141.
Wang S, Gao J, Wang Z. Outer membrane vesicles for vaccination and targeted drug delivery. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2019;11(2):e1523.PubMedCrossRef
142.
Sierra GV, Campa HC, Varcacel NM, Garcia IL, Izquierdo PL, Sotolongo PF, Casanueva GV, Rico CO, Rodriguez CR, Terry MH. Vaccine against group B Neisseria meningitidis: protection trial and mass vaccination results in Cuba. NIPH Ann. 1991;14(2):195–207 (discussion 208–10).
143.
Fábrega MJ, Aguilera L, Giménez R, Varela E, Alexandra Cañas M, Antolín M, Badía J, Baldomà L. Activation of immune and defense responses in the intestinal mucosa by outer membrane vesicles of commensal and probiotic Escherichia coli strains. Front Microbiol. 2016;11(7):705.
144.
Chelakkot C, Choi Y, Kim DK, Park HT, Ghim J, Kwon Y, Jeon J, Kim MS, Jee YK, Gho YS, Park HS, Kim YK, Ryu SH. Akkermansia muciniphila-derived extracellular vesicles influence gut permeability through the regulation of tight junctions. Exp Mol Med. 2018;50(2):e450.PubMedPubMedCentralCrossRef
145.
Kang CS, Ban M, Choi EJ, Moon HG, Jeon JS, Kim DK, Park SK, Jeon SG, Roh TY, Myung SJ, Gho YS, Kim JG, Kim YK. Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis. PLoS ONE. 2013;8(10):e76520.PubMedPubMedCentralCrossRef
146.
Alvarez CS, Badia J, Bosch M, Giménez R, Baldomà L. Outer membrane vesicles and soluble factors released by probiotic Escherichia coli Nissle 1917 and commensal ECOR63 enhance barrier function by regulating expression of tight junction proteins in intestinal epithelial cells. Front Microbiol. 2016;15(7):1981.
147.
Cañas MA, Fábrega MJ, Giménez R, Badia J, Baldomà L. Outer membrane vesicles from probiotic and commensal Escherichia coli activate NOD1-mediated immune responses in intestinal epithelial cells. Front Microbiol. 2018;20(9):498.CrossRef
148.
Gao XJ, Li T, Wei B, Yan ZX, Yan R. Regulatory mechanisms of gut microbiota on intestinal CYP3A and P-glycoprotein in rats with dextran sulfate sodium-induced colitis. Yao Xue Xue Bao. 2017;52(1):34–43.PubMed
149.
Kelly JR, Kennedy PJ, Cryan JF, Dinan TG, Clarke G, Hyland NP. Breaking down the barriers: the gut microbiome, intestinal permeability and stress-related psychiatric disorders. Front Cell Neurosci. 2015;14(9):392.
150.
Muraca M, Putignani L, Fierabracci A, Teti A, Perilongo G. Gut microbiota-derived outer membrane vesicles: under-recognized major players in health and disease? Discov Med. 2015;19(106):343–8.PubMed
151.
Choi SJ, Kim MH, Jeon J, Kim OY, Choi Y, Seo J, Hong SW, Lee WH, Jeon SG, Gho YS, Jee YK, Kim YK. Active immunization with extracellular vesicles derived from Staphylococcus aureus effectively protects against staphylococcal lung infections, mainly via Th1 cell-mediated immunity. PLoS ONE. 2015;10(9):e0136021.PubMedPubMedCentralCrossRef
152.
Choi HI, Choi JP, Seo J, Kim BJ, Rho M, Han JK, Kim JG. Helicobacter pylori-derived extracellular vesicles increased in the gastric juices of gastric adenocarcinoma patients and induced inflammation mainly via specific targeting of gastric epithelial cells. Exp Mol Med. 2017;49(5):e330.PubMedPubMedCentralCrossRef
153.
Singhrao SK, Olsen I. Are porphyromonas gingivalis outer membrane vesicles microbullets for sporadic alzheimer’s disease manifestation? J Alzheimers Dis Rep. 2018;2:219–28.PubMedPubMedCentralCrossRef
154.
Choi J, Kim YK, Han PL. Extracellular vesicles derived from lactobacillus plantarum increase bdnf expression in cultured hippocampal neurons and produce antidepressant-like effects in mice. Exp Neurobiol. 2019;28:158–71.PubMedPubMedCentralCrossRef
155.
Koeppen K, Hampton TH, Jarek M, Scharfe M, Gerber SA, Mielcarz DW, et al. A novel mechanism of host-pathogen interaction through srna in bacterial outer membrane vesicles. PLoS Pathog. 2016;12:e1005672–e1005672.PubMedPubMedCentralCrossRef
156.
Choi JW, Kim SC, Hong SH, Lee HJ. Secretable small rnas via outer membrane vesicles in periodontal pathogens. J Dent Res. 2017;96:458–66.PubMedCrossRef
157.
Buck AH, Coakley G, Simbari F, McSorley HJ, Quintana JF, Le Bihan T, et al. Erratum: Exosomes secreted by nematode parasites transfer small rnas to mammalian cells and modulate innate immunity. Nat Commun. 2015;6:8772.PubMedCrossRef
158.
Drexler SK, Foxwell BM. The role of toll-like receptors in chronic inflammation. Int J Biochem Cell Biol. 2010;42:506–18.PubMedCrossRef
159.
160.
Sun MF, Shen YQ. Dysbiosis of gut microbiota and microbial metabolites in parkinson’s disease. Ageing Res Rev. 2018;45:53–61.PubMedCrossRef
161.
Han EC, Choi SY, Lee Y, Park JW, Hong SH, Lee HJ. Extracellular rnas in periodontopathogenic outer membrane vesicles promote tnf-α production in human macrophages and cross the blood-brain barrier in mice. Faseb J. 2019;33:13412–22.PubMedPubMedCentralCrossRef
162.
Wei SC, Wei W, Peng WJ, Liu Z, Cai ZY, Zhao B. Metabolic alterations in the outer membrane vesicles of patients with Alzheimer’s disease: an lc-ms/ms-based metabolomics analysis. Curr Alzheimer Res. 2019;16:1183–95.PubMedCrossRef
163.
Leclair-Visonneau L, Neunlist M, Derkinderen P, Lebouvier T. The gut in parkinson’s disease: bottom-up, top-down, or neither? Neurogastroenterol Motil. 2020;32:e13777.PubMedCrossRef
164.
Wei S, Peng W, Mai Y, Li K, Wei W, Hu L, et al. Outer membrane vesicles enhance tau phosphorylation and contribute to cognitive impairment. J Cell Physiol. 2020;235:4843–55.PubMedCrossRef
165.
Łuc M, Misiak B, Pawłowski M, Stańczykiewicz B, Zabłocka A, Szcześniak D, et al. Gut microbiota in dementia Critical review of novel findings and their potential application. Progr Neuro-Psychopharmacol Biol Psychiatry. 2021;104:110039.CrossRef
166.
Figliolini F, Cantaluppi V, De Lena M, Beltramo S, Romagnoli R, Salizzoni M, et al. Isolation, characterization and potential role in beta cell-endothelium cross-talk of extracellular vesicles released from human pancreatic islets. PLoS ONE. 2014;9:e102521.PubMedPubMedCentralCrossRef
167.
Fleetwood AJ, Lee MKS, Singleton W, Achuthan A, Lee MC, O’Brien-Simpson NM, et al. Metabolic remodeling, inflammasome activation, and pyroptosis in macrophages stimulated by porphyromonas gingivalis and its outer membrane vesicles. Front Cell Infect Microbiol. 2017;7:351.PubMedPubMedCentralCrossRef
168.
Li X, Ballantyne LL, Yu Y, Funk CD. Perivascular adipose tissue-derived extracellular vesicle mir-221-3p mediates vascular remodeling. FASEB J. 2019;33:12704–22.PubMedPubMedCentralCrossRef
169.
Seyama M, Yoshida K, Yoshida K, Fujiwara N, Ono K, Eguchi T, et al. Outer membrane vesicles of porphyromonas gingivalis attenuate insulin sensitivity by delivering gingipains to the liver. Biochim Biophys Acta Mol Basis Dis. 2020;1866:165731.PubMedCrossRef
170.
Jiang F, Chen Q, Wang W, Ling Y, Yan Y, Xia P. Hepatocyte-derived extracellular vesicles promote endothelial inflammation and atherogenesis via microrna-1. J Hepatol. 2020;72:156–66.PubMedCrossRef
171.
Li Y, Meng Y, Zhu X, Saadiq IM, Jordan KL, Eirin A, et al. Metabolic syndrome increases senescence-associated micro-rnas in extracellular vesicles derived from swine and human mesenchymal stem/stromal cells. Cell Commun Signal. 2020;18:124.PubMedPubMedCentralCrossRef
172.
Kowal J, Arras G, Colombo M, Jouve M, Morath J, Primdal-Bengtson B, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci USA. 2016;113:1.CrossRef
173.
Zhang H, Freitas D, Kim HS, Fabijanic K, Li Z, Chen H, et al. Identification of distinct nanoparticles and subsets of extracellular vesicles by asymmetric flow field-flow fractionation. Nat Cell Biol. 2018;20:332–43.PubMedPubMedCentralCrossRef
174.
Choi D, Lee TH, Spinelli C, Chennakrishnaiah S, D’Asti E, Rak J. Extracellular vesicle communication pathways as regulatory targets of oncogenic transformation. Semin Cell Dev Biol. 2017;67:11–22.PubMedCrossRef
175.
Zocco D, Zarovni N. Extraction and analysis of extracellular vesicle-associated mirnas following antibody-based extracellular vesicle capture from plasma samples. Methods Mol Biol. 2017;1660:269–85.PubMedCrossRef
176.
Kaur S, Abu-Shahba AG, Paananen RO, Hongisto H, Hiidenmaa H, Skottman H, et al. Small non-coding rna landscape of extracellular vesicles from human stem cells. Sci Rep. 2018;8:15503.PubMedPubMedCentralCrossRef
177.
Lin CW, Jan MS, Kuo JS. The microrna expression profiles in extracellular vesicles from hela cancer cells in response to cationic lipid- or polyethylenimine-mediated gene delivery. J Drug Target. 2019;27:94–102.PubMedCrossRef
178.
179.
Rothschild D, Weissbrod O, Barkan E, Kurilshikov A, Korem T, Zeevi D, et al. Environment dominates over host genetics in shaping human gut microbiota. Nature. 2018;555:210–5.PubMedCrossRef
180.
181.
Teodori L, Petrignani I, Giuliani A, Prattichizzo F, Gurău F, Matacchione G, et al. Inflamm-aging micrornas may integrate signals from food and gut microbiota by modulating common signalling pathways. Mech Ageing Devel. 2019;182:111127.CrossRef
182.
Cuevas-Sierra A, Ramos-Lopez O, Riezu-Boj JI, Milagro FI, Martinez JA. Diet, gut microbiota, and obesity: Links with host genetics and epigenetics and potential applications. Adv Nutr. 2019;10:S17–30.PubMedPubMedCentralCrossRef
183.
Xing SC, Huang CB, Mi JD, Wu YB, Liao XD. Bacillus coagulans r11 maintained intestinal villus health and decreased intestinal injury in lead-exposed mice by regulating the intestinal microbiota and influenced the function of faecal micrornas. Environ Pollut. 2019;255:113139.PubMedCrossRef
184.
Neu J. Gut microbiota, host gene expression, and cell traffic via milk. Nestle Nutr Inst Workshop Ser. 2020;94:94–102.PubMedCrossRef
185.
Yuan C, Burns MB, Subramanian S, Blekhman R. Interaction between host micrornas and the gut microbiota in colorectal cancer. mSystems. 2018;3:1.CrossRef
186.
187.
Chevillet JR, Kang Q, Ruf IK, Briggs HA, Vojtech LN, Hughes SM, et al. Quantitative and stoichiometric analysis of the microrna content of exosomes. Proc Natl Acad Sci USA. 2014;111:14888–93.PubMedCrossRefPubMedCentral
188.
Lefebvre FA, Benoit Bouvrette LP, Perras L, Blanchet-Cohen A, Garnier D, Rak J, et al. Comparative transcriptomic analysis of human and drosophila extracellular vesicles. Sci Rep. 2016;6:27680.PubMedPubMedCentralCrossRef
189.
Wei Z, Batagov AO, Schinelli S, Wang J, Wang Y, El Fatimy R, et al. Coding and noncoding landscape of extracellular rna released by human glioma stem cells. Nat Commun. 2017;8:1145.PubMedPubMedCentralCrossRef
190.
Bryniarski K, Ptak W, Martin E, Nazimek K, Szczepanik M, Sanak M, et al. Free extracellular mirna functionally targets cells by transfecting exosomes from their companion cells. PLoS ONE. 2015;10:e0122991–e0122991.PubMedPubMedCentralCrossRef
191.
Stremersch S, Brans T, Braeckmans K, De Smedt S, Raemdonck K. Nucleic acid loading and fluorescent labeling of isolated extracellular vesicles requires adequate purification. Int J Pharm. 2018;548:783–92.PubMedCrossRef
Metadata
Title
Extracellular vesicle-derived miRNA as a novel regulatory system for bi-directional communication in gut-brain-microbiota axis
Authors
Liang Zhao
Yingze Ye
Lijuan Gu
Zhihong Jian
Creed M. Stary
Xiaoxing Xiong
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2021
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-021-02861-y

Other articles of this Issue 1/2021

Journal of Translational Medicine 1/2021 Go to the issue

Research

Trajectories of cardiovascular disease risk and their association with the incidence of cardiovascular events over 18 years of follow-up: The Tehran Lipid and Glucose study

Research

Collaborative relationships in translational medical research among Chinese clinicians: an internet-based cross-sectional survey

Review

Hypoxia and the phenomenon of immune exclusion

Research

KPNA2 interaction with CBX8 contributes to the development and progression of bladder cancer by mediating the PRDM1/c-FOS pathway

Research

The fecal microbiota of patients with pancreatic ductal adenocarcinoma and autoimmune pancreatitis characterized by metagenomic sequencing

Correction

Correction to: Nerve growth factor improves functional recovery by inhibiting endoplasmic reticulum stress-induced neuronal apoptosis in rats with spinal cord injury
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.

Watch now

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits