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Stem cells international2019; 2019; 4957806; doi: 10.1155/2019/4957806

Equine Adipose-Derived Mesenchymal Stromal Cells Release Extracellular Vesicles Enclosing Different Subsets of Small RNAs.

Abstract: Equine adipose-derived mesenchymal stromal cells (e-AdMSC) exhibit attractive proregenerative properties strongly related to the delivery of extracellular vesicles (EVs) that enclose different kinds of molecules including RNAs. In this study, we investigated small RNA content of EVs produced by e-AdMSC with the aim of speculating on their possible biological role. Methods: EVs were obtained by ultracentrifugation of the conditioned medium of e-AdMSC of 4 subjects. Transmission electron microscopy and scanning electron microscopy were performed to assess their size and nanostructure. RNA was isolated, enriched for small RNAs (<200 nt), and sequenced by Illumina technology. After bioinformatic analysis with state-of-the-art pipelines for short sequences, mapped reads were used to describe EV RNA cargo, reporting classes, and abundances. Enrichment analyses were performed to infer involved pathways and functional categories. Results: Electron microscopy showed the presence of vesicles ranging in size from 30 to 300 nm and expressing typical markers. RNA analysis revealed that ribosomal RNA was the most abundant fraction, followed by small nucleolar RNAs (snoRNAs, 13.67%). Miscellaneous RNA (misc_RNA) reached 4.57% of the total where Y RNA, RNaseP, and vault RNA represented the main categories. miRNAs were sequenced at a lower level (3.51%) as well as protein-coding genes (1.33%). Pathway analyses on the protein-coding fraction revealed a significant enrichment for the "ribosome" pathway followed by "oxidative phosphorylation." Gene Ontology analysis showed enrichment for terms like "extracellular exosome," "organelle envelope," "RNA binding," and "small molecule metabolic process." The miRNA target pathway analysis revealed the presence of "signaling pathways regulating pluripotency of stem cells" coherent with the source of the samples. Conclusions: We herein demonstrated that e-AdMSC release EVs enclosing different subsets of small RNAs that potentially regulate a number of biological processes. These findings shed light on the role of EVs in the context of MSC biology.
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Publication Date: 2019-03-18 PubMed ID: 31011332PubMed Central: PMC6442443DOI: 10.1155/2019/4957806Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research explores the small RNA content of extracellular vesicles (EVs) produced by Equine adipose-derived mesenchymal stromal cells, aiming to understand their possible biological role. The study results show these EVs contain different subsets of small RNAs that could potentially regulate numerous biological processes, providing further insights into the role of EVs in MSC biology.

Research Methodology

  • The researchers applied ultracentrifugation on the conditioned medium of e-AdMSC taken from four different subjects to acquire extracellular vesicles (EVs).
  • Two types of electron microscopy, transmission electron microscopy and scanning electron microscopy, were conducted to assess the size and the nano-structural details of the EVs.
  • The team isolated RNA from the EVs and filtered for small RNAs less than 200 nucleotides, which were then sequenced using Illumina technology.
  • A bioinformatic analysis was then carried out on the sequenced data, specifically focusing on the short sequences.
  • The classes and abundances of the mapped reads were used to describe the RNA cargo of the EVs. Additionally, enrichment analyses were carried out to discern the involved pathways and functional categories.

Research Findings

  • Electron microscopy revealed the presence of vesicles ranging in size from 30 to 300 nanometres, which express typical markers.
  • The researchers found that the most abundant fraction of RNA was ribosomal RNA. Small nucleolar RNAs made up 13.67%, and Miscellaneous RNA constituted 4.57% of the total. Within the misc_RNA section, Y RNA, RNaseP, and vault RNA were the main categories.
  • MicroRNAs were sequenced at a lower level (3.51%), in addition to protein-coding genes (1.33%).

Inferred Pathways and Functional Categories

  • The pathway analyses on the protein-coding fraction revealed significant enrichment for the “ribosome” pathway, which was followed by “oxidative phosphorylation.”
  • The Gene Ontology analysis showed enrichment for several terms, such as “extracellular exosome,” “organelle envelope,” “RNA binding,” and “small molecule metabolic process.”
  • MicroRNA target pathway analysis revealed the presence of “signaling pathways regulating pluripotency of stem cells,” aligning with the source of the samples.
  • These results indicate that e-AdMSC release EVs with different subsets of small RNAs which could potentially regulate a range of biological processes.

Implications and Conclusions

  • This study expands our understanding of the role of EVs in the functionality of MSC biology.
  • Recognizing the broad spectrum of small RNAs present in the extracellular vesicles can help to comprehend their function and involvement in various biological processes better.
  • The results have potential implications on how these small RNAs can be potentially used for therapeutic advancements, particularly in the field of regenerative medicine.

Cite This Article

APA
Capomaccio S, Cappelli K, Bazzucchi C, Coletti M, Gialletti R, Moriconi F, Passamonti F, Pepe M, Petrini S, Mecocci S, Silvestrelli M, Pascucci L. (2019). Equine Adipose-Derived Mesenchymal Stromal Cells Release Extracellular Vesicles Enclosing Different Subsets of Small RNAs. Stem Cells Int, 2019, 4957806. https://doi.org/10.1155/2019/4957806

Publication

Stem cells international
ISSN: 1687-966X
NlmUniqueID: 101535822
Country: United States
Language: English
Volume: 2019
Pages: 4957806
PII: 4957806

Researcher Affiliations

Capomaccio, Stefano
  • Dipartimento di Medicina Veterinaria, Università degli Studi di Perugia, Via San Costanzo, 4, 06126 Perugia, Italy.
  • Centro di Ricerca sul Cavallo Sportivo (CRCS), Università degli Studi di Perugia, Italy.
Cappelli, Katia
  • Dipartimento di Medicina Veterinaria, Università degli Studi di Perugia, Via San Costanzo, 4, 06126 Perugia, Italy.
  • Centro di Ricerca sul Cavallo Sportivo (CRCS), Università degli Studi di Perugia, Italy.
Bazzucchi, Cinzia
  • Dipartimento di Medicina Veterinaria, Università degli Studi di Perugia, Via San Costanzo, 4, 06126 Perugia, Italy.
Coletti, Mauro
  • Dipartimento di Medicina Veterinaria, Università degli Studi di Perugia, Via San Costanzo, 4, 06126 Perugia, Italy.
  • Centro di Ricerca sul Cavallo Sportivo (CRCS), Università degli Studi di Perugia, Italy.
Gialletti, Rodolfo
  • Dipartimento di Medicina Veterinaria, Università degli Studi di Perugia, Via San Costanzo, 4, 06126 Perugia, Italy.
  • Centro di Ricerca sul Cavallo Sportivo (CRCS), Università degli Studi di Perugia, Italy.
Moriconi, Franco
  • Dipartimento di Medicina Veterinaria, Università degli Studi di Perugia, Via San Costanzo, 4, 06126 Perugia, Italy.
  • Centro di Ricerca sul Cavallo Sportivo (CRCS), Università degli Studi di Perugia, Italy.
Passamonti, Fabrizio
  • Dipartimento di Medicina Veterinaria, Università degli Studi di Perugia, Via San Costanzo, 4, 06126 Perugia, Italy.
  • Centro di Ricerca sul Cavallo Sportivo (CRCS), Università degli Studi di Perugia, Italy.
Pepe, Marco
  • Dipartimento di Medicina Veterinaria, Università degli Studi di Perugia, Via San Costanzo, 4, 06126 Perugia, Italy.
  • Centro di Ricerca sul Cavallo Sportivo (CRCS), Università degli Studi di Perugia, Italy.
Petrini, Stefano
  • Istituto Zooprofilattico Sperimentale dell'Umbria e delle Marche, Italy.
Mecocci, Samanta
  • Dipartimento di Medicina Veterinaria, Università degli Studi di Perugia, Via San Costanzo, 4, 06126 Perugia, Italy.
  • Centro di Ricerca sul Cavallo Sportivo (CRCS), Università degli Studi di Perugia, Italy.
Silvestrelli, Maurizio
  • Dipartimento di Medicina Veterinaria, Università degli Studi di Perugia, Via San Costanzo, 4, 06126 Perugia, Italy.
  • Centro di Ricerca sul Cavallo Sportivo (CRCS), Università degli Studi di Perugia, Italy.
Pascucci, Luisa
  • Dipartimento di Medicina Veterinaria, Università degli Studi di Perugia, Via San Costanzo, 4, 06126 Perugia, Italy.
  • Centro di Ricerca sul Cavallo Sportivo (CRCS), Università degli Studi di Perugia, Italy.

References

This article includes 60 references
  1. Rani S, Ritter T. The Exosome - A Naturally Secreted Nanoparticle and its Application to Wound Healing.. Adv Mater 2016 Jul;28(27):5542-52.
    doi: 10.1002/adma.201504009pubmed: 26678528google scholar: lookup
  2. György B, Szabó TG, Pásztói M, Pál Z, Misják P, Aradi B, László V, Pállinger E, Pap E, Kittel A, Nagy G, Falus A, Buzás EI. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles.. Cell Mol Life Sci 2011 Aug;68(16):2667-88.
    doi: 10.1007/s00018-011-0689-3pmc: PMC3142546pubmed: 21560073google scholar: lookup
  3. Abels ER, Breakefield XO. Introduction to Extracellular Vesicles: Biogenesis, RNA Cargo Selection, Content, Release, and Uptake.. Cell Mol Neurobiol 2016 Apr;36(3):301-12.
    doi: 10.1007/s10571-016-0366-zpmc: PMC5546313pubmed: 27053351google scholar: lookup
  4. Tan CY, Lai RC, Wong W, Dan YY, Lim SK, Ho HK. Mesenchymal stem cell-derived exosomes promote hepatic regeneration in drug-induced liver injury models.. Stem Cell Res Ther 2014 Jun 10;5(3):76.
    doi: 10.1186/scrt465pmc: PMC4229780pubmed: 24915963google scholar: lookup
  5. Zhou Y, Xu H, Xu W, Wang B, Wu H, Tao Y, Zhang B, Wang M, Mao F, Yan Y, Gao S, Gu H, Zhu W, Qian H. Exosomes released by human umbilical cord mesenchymal stem cells protect against cisplatin-induced renal oxidative stress and apoptosis in vivo and in vitro.. Stem Cell Res Ther 2013 Apr 25;4(2):34.
    doi: 10.1186/scrt194pmc: PMC3707035pubmed: 23618405google scholar: lookup
  6. Blazquez R, Sanchez-Margallo FM, de la Rosa O, Dalemans W, Alvarez V, Tarazona R, Casado JG. Immunomodulatory Potential of Human Adipose Mesenchymal Stem Cells Derived Exosomes on in vitro Stimulated T Cells.. Front Immunol 2014;5:556.
    doi: 10.3389/fimmu.2014.00556pmc: PMC4220146pubmed: 25414703google scholar: lookup
  7. Zhang B, Yin Y, Lai RC, Tan SS, Choo AB, Lim SK. Mesenchymal stem cells secrete immunologically active exosomes.. Stem Cells Dev 2014 Jun 1;23(11):1233-44.
    doi: 10.1089/scd.2013.0479pubmed: 24367916google scholar: lookup
  8. Katsuda T, Ochiya T. Molecular signatures of mesenchymal stem cell-derived extracellular vesicle-mediated tissue repair.. Stem Cell Res Ther 2015 Nov 11;6:212.
    doi: 10.1186/s13287-015-0214-ypmc: PMC4642616pubmed: 26560482google scholar: lookup
  9. Pascucci L, Alessandri G, Dall'Aglio C, Mercati F, Coliolo P, Bazzucchi C, Dante S, Petrini S, Curina G, Ceccarelli P. Membrane vesicles mediate pro-angiogenic activity of equine adipose-derived mesenchymal stromal cells.. Vet J 2014 Nov;202(2):361-6.
    doi: 10.1016/j.tvjl.2014.08.021pubmed: 25241947google scholar: lookup
  10. Zhang HC, Liu XB, Huang S, Bi XY, Wang HX, Xie LX, Wang YQ, Cao XF, Lv J, Xiao FJ, Yang Y, Guo ZK. Microvesicles derived from human umbilical cord mesenchymal stem cells stimulated by hypoxia promote angiogenesis both in vitro and in vivo.. Stem Cells Dev 2012 Dec 10;21(18):3289-97.
    doi: 10.1089/scd.2012.0095pmc: PMC3516422pubmed: 22839741google scholar: lookup
  11. Huang X, Yuan T, Tschannen M, Sun Z, Jacob H, Du M, Liang M, Dittmar RL, Liu Y, Liang M, Kohli M, Thibodeau SN, Boardman L, Wang L. Characterization of human plasma-derived exosomal RNAs by deep sequencing.. BMC Genomics 2013 May 10;14:319.
    doi: 10.1186/1471-2164-14-319pmc: PMC3653748pubmed: 23663360google scholar: lookup
  12. El-Mogy M, Lam B, Haj-Ahmad TA, McGowan S, Yu D, Nosal L, Rghei N, Roberts P, Haj-Ahmad Y. Diversity and signature of small RNA in different bodily fluids using next generation sequencing.. BMC Genomics 2018 May 29;19(1):408.
    doi: 10.1186/s12864-018-4785-8pmc: PMC5975555pubmed: 29843592google scholar: lookup
  13. Hayashi T, Hoffman MP. Exosomal microRNA communication between tissues during organogenesis.. RNA Biol 2017 Dec 2;14(12):1683-1689.
    doi: 10.1080/15476286.2017.1361098pmc: PMC5731799pubmed: 28816640google scholar: lookup
  14. Zomer A, Vendrig T, Hopmans ES, van Eijndhoven M, Middeldorp JM, Pegtel DM. Exosomes: Fit to deliver small RNA.. Commun Integr Biol 2010 Sep;3(5):447-50.
    doi: 10.4161/cib.3.5.12339pmc: PMC2974077pubmed: 21057637google scholar: lookup
  15. Otsuru S, Desbourdes L, Guess AJ, Hofmann TJ, Relation T, Kaito T, Dominici M, Iwamoto M, Horwitz EM. Extracellular vesicles released from mesenchymal stromal cells stimulate bone growth in osteogenesis imperfecta.. Cytotherapy 2018 Jan;20(1):62-73.
    doi: 10.1016/j.jcyt.2017.09.012pubmed: 29107738google scholar: lookup
  16. Moon GJ, Sung JH, Kim DH, Kim EH, Cho YH, Son JP, Cha JM, Bang OY. Application of Mesenchymal Stem Cell-Derived Extracellular Vesicles for Stroke: Biodistribution and MicroRNA Study.. Transl Stroke Res 2019 Oct;10(5):509-521.
    doi: 10.1007/s12975-018-0668-1pubmed: 30341718google scholar: lookup
  17. La Greca A, Solari C, Furmento V, Lombardi A, Biani MC, Aban C, Moro L, García M, Guberman AS, Sevlever GE, Miriuka SG, Luzzani C. Extracellular vesicles from pluripotent stem cell-derived mesenchymal stem cells acquire a stromal modulatory proteomic pattern during differentiation.. Exp Mol Med 2018 Sep 10;50(9):1-12.
    doi: 10.1038/s12276-018-0142-xpmc: PMC6131549pubmed: 30201949google scholar: lookup
  18. Baglio SR, Rooijers K, Koppers-Lalic D, Verweij FJ, Pérez Lanzón M, Zini N, Naaijkens B, Perut F, Niessen HW, Baldini N, Pegtel DM. Human bone marrow- and adipose-mesenchymal stem cells secrete exosomes enriched in distinctive miRNA and tRNA species.. Stem Cell Res Ther 2015 Jul 1;6(1):127.
    doi: 10.1186/s13287-015-0116-zpmc: PMC4529699pubmed: 26129847google scholar: lookup
  19. Eirin A, Riester SM, Zhu XY, Tang H, Evans JM, O'Brien D, van Wijnen AJ, Lerman LO. MicroRNA and mRNA cargo of extracellular vesicles from porcine adipose tissue-derived mesenchymal stem cells.. Gene 2014 Nov 1;551(1):55-64.
    doi: 10.1016/j.gene.2014.08.041pmc: PMC4174680pubmed: 25158130google scholar: lookup
  20. Pascucci L, Dall'Aglio C, Bazzucchi C, Mercati F, Mancini MG, Pessina A, Alessandri G, Giammarioli M, Dante S, Brunati G, Ceccarelli P. Horse adipose-derived mesenchymal stromal cells constitutively produce membrane vesicles: a morphological study.. Histol Histopathol 2015 May;30(5):549-57.
    doi: 10.14670/HH-30.549pubmed: 25418078google scholar: lookup
  21. Perrini C, Strillacci MG, Bagnato A, Esposti P, Marini MG, Corradetti B, Bizzaro D, Idda A, Ledda S, Capra E, Pizzi F, Lange-Consiglio A, Cremonesi F. Microvesicles secreted from equine amniotic-derived cells and their potential role in reducing inflammation in endometrial cells in an in-vitro model.. Stem Cell Res Ther 2016 Nov 18;7(1):169.
    doi: 10.1186/s13287-016-0429-6pmc: PMC5114748pubmed: 27863532google scholar: lookup
  22. Lange-Consiglio A, Perrini C, Tasquier R, Deregibus MC, Camussi G, Pascucci L, Marini MG, Corradetti B, Bizzaro D, De Vita B, Romele P, Parolini O, Cremonesi F. Equine Amniotic Microvesicles and Their Anti-Inflammatory Potential in a Tenocyte Model In Vitro.. Stem Cells Dev 2016 Apr 15;25(8):610-21.
    doi: 10.1089/scd.2015.0348pubmed: 26914245google scholar: lookup
  23. Pascucci L, Curina G, Mercati F, Marini C, Dall'Aglio C, Paternesi B, Ceccarelli P. Flow cytometric characterization of culture expanded multipotent mesenchymal stromal cells (MSCs) from horse adipose tissue: towards the definition of minimal stemness criteria.. Vet Immunol Immunopathol 2011 Dec 15;144(3-4):499-506.
    doi: 10.1016/j.vetimm.2011.07.017pubmed: 21839521google scholar: lookup
  24. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H, Alfonso ZC, Fraser JK, Benhaim P, Hedrick MH. Human adipose tissue is a source of multipotent stem cells.. Mol Biol Cell 2002 Dec;13(12):4279-95.
    doi: 10.1091/mbc.e02-02-0105pmc: PMC138633pubmed: 12475952google scholar: lookup
  25. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data.. Bioinformatics 2014 Aug 1;30(15):2114-20.
    doi: 10.1093/bioinformatics/btu170pmc: PMC4103590pubmed: 24695404google scholar: lookup
  26. Aken BL, Ayling S, Barrell D, Clarke L, Curwen V, Fairley S, Fernandez Banet J, Billis K, García Girón C, Hourlier T, Howe K, Kähäri A, Kokocinski F, Martin FJ, Murphy DN, Nag R, Ruffier M, Schuster M, Tang YA, Vogel JH, White S, Zadissa A, Flicek P, Searle SM. The Ensembl gene annotation system.. Database (Oxford) 2016;2016.
    doi: 10.1093/database/baw093pmc: PMC4919035pubmed: 27337980google scholar: lookup
  27. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data.. Bioinformatics 2010 Jan 1;26(1):139-40.
    doi: 10.1093/bioinformatics/btp616pmc: PMC2796818pubmed: 19910308google scholar: lookup
  28. Haunsberger SJ, Connolly NM, Prehn JH. miRNAmeConverter: an R/bioconductor package for translating mature miRNA names to different miRBase versions.. Bioinformatics 2017 Feb 15;33(4):592-593.
    doi: 10.1093/bioinformatics/btw660pubmed: 27797767google scholar: lookup
  29. Li M, Zeringer E, Barta T, Schageman J, Cheng A, Vlassov AV. Analysis of the RNA content of the exosomes derived from blood serum and urine and its potential as biomarkers.. Philos Trans R Soc Lond B Biol Sci 2014 Sep 26;369(1652).
    doi: 10.1098/rstb.2013.0502pmc: PMC4142023pubmed: 25135963google scholar: lookup
  30. Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M, Bork P, Jensen LJ, von Mering C. STRING v10: protein-protein interaction networks, integrated over the tree of life.. Nucleic Acids Res 2015 Jan;43(Database issue):D447-52.
    doi: 10.1093/nar/gkဃpmc: PMC4383874pubmed: 25352553google scholar: lookup
  31. Ferris DJ, Frisbie DD, Kisiday JD, McIlwraith CW, Hague BA, Major MD, Schneider RK, Zubrod CJ, Kawcak CE, Goodrich LR. Clinical outcome after intra-articular administration of bone marrow derived mesenchymal stem cells in 33 horses with stifle injury.. Vet Surg 2014 Mar;43(3):255-65.
    doi: 10.1111/j.1532-950X.2014.12100.xpubmed: 24433318google scholar: lookup
  32. Ricco S, Renzi S, Del Bue M, Conti V, Merli E, Ramoni R, Lucarelli E, Gnudi G, Ferrari M, Grolli S. Allogeneic adipose tissue-derived mesenchymal stem cells in combination with platelet rich plasma are safe and effective in the therapy of superficial digital flexor tendonitis in the horse.. Int J Immunopathol Pharmacol 2013 Jan-Mar;26(1 Suppl):61-8.
    doi: 10.1177/03946320130260S108pubmed: 24046950google scholar: lookup
  33. Textor JA, Clark KC, Walker NJ, Aristizobal FA, Kol A, LeJeune SS, Bledsoe A, Davidyan A, Gray SN, Bohannon-Worsley LK, Woolard KD, Borjesson DL. Allogeneic Stem Cells Alter Gene Expression and Improve Healing of Distal Limb Wounds in Horses.. Stem Cells Transl Med 2018 Jan;7(1):98-108.
    doi: 10.1002/sctm.17-0071pmc: PMC5746157pubmed: 29063737google scholar: lookup
  34. Smith RK, Garvican ER, Fortier LA. The current 'state of play' of regenerative medicine in horses: what the horse can tell the human.. Regen Med 2014;9(5):673-85.
    doi: 10.2217/rme.14.42pubmed: 25372081google scholar: lookup
  35. Burk J, Ribitsch I, Gittel C, Juelke H, Kasper C, Staszyk C, Brehm W. Growth and differentiation characteristics of equine mesenchymal stromal cells derived from different sources.. Vet J 2013 Jan;195(1):98-106.
    doi: 10.1016/j.tvjl.2012.06.004pubmed: 22841420google scholar: lookup
  36. Mateescu B, Kowal EJ, van Balkom BW, Bartel S, Bhattacharyya SN, Buzás EI, Buck AH, de Candia P, Chow FW, Das S, Driedonks TA, Fernández-Messina L, Haderk F, Hill AF, Jones JC, Van Keuren-Jensen KR, Lai CP, Lässer C, Liegro ID, Lunavat TR, Lorenowicz MJ, Maas SL, Mäger I, Mittelbrunn M, Momma S, Mukherjee K, Nawaz M, Pegtel DM, Pfaffl MW, Schiffelers RM, Tahara H, Théry C, Tosar JP, Wauben MH, Witwer KW, Nolte-'t Hoen EN. Obstacles and opportunities in the functional analysis of extracellular vesicle RNA - an ISEV position paper.. J Extracell Vesicles 2017;6(1):1286095.
    doi: 10.1080/20013078.2017.1286095pmc: PMC5345583pubmed: 28326170google scholar: lookup
  37. van Balkom BW, Eisele AS, Pegtel DM, Bervoets S, Verhaar MC. Quantitative and qualitative analysis of small RNAs in human endothelial cells and exosomes provides insights into localized RNA processing, degradation and sorting.. J Extracell Vesicles 2015;4:26760.
    doi: 10.3402/jev.v4.26760pmc: PMC4450249pubmed: 26027894google scholar: lookup
  38. Chen L, Han L, Wei J, Zhang K, Shi Z, Duan R, Li S, Zhou X, Pu P, Zhang J, Kang C. SNORD76, a box C/D snoRNA, acts as a tumor suppressor in glioblastoma.. Sci Rep 2015 Feb 26;5:8588.
    doi: 10.1158/1538-7445.am2015-235pmc: PMC5390076pubmed: 25715874google scholar: lookup
  39. Falaleeva M, Stamm S. Processing of snoRNAs as a new source of regulatory non-coding RNAs: snoRNA fragments form a new class of functional RNAs.. Bioessays 2013 Jan;35(1):46-54.
    doi: 10.1002/bies.201200117pmc: PMC3732821pubmed: 23180440google scholar: lookup
  40. Kaur D, Gupta AK, Kumari V, Sharma R, Bhattacharya A, Bhattacharya S. Computational prediction and validation of C/D, H/ACA and Eh_U3 snoRNAs of Entamoeba histolytica.. BMC Genomics 2012 Aug 14;13:390.
    doi: 10.1186/1471-2164-13-390pmc: PMC3542256pubmed: 22892049google scholar: lookup
  41. Labialle S, Cavaillé J. Do repeated arrays of regulatory small-RNA genes elicit genomic imprinting?: Concurrent emergence of large clusters of small non-coding RNAs and genomic imprinting at four evolutionarily distinct eutherian chromosomal loci.. Bioessays 2011 Aug;33(8):565-73.
    doi: 10.1002/bies.201100032pubmed: 21618561google scholar: lookup
  42. Valleron W, Laprevotte E, Gautier EF, Quelen C, Demur C, Delabesse E, Agirre X, Prósper F, Kiss T, Brousset P. Specific small nucleolar RNA expression profiles in acute leukemia.. Leukemia 2012 Sep;26(9):2052-60.
    doi: 10.1038/leu.2012.111pubmed: 22522792google scholar: lookup
  43. Falaleeva M, Pages A, Matuszek Z, Hidmi S, Agranat-Tamir L, Korotkov K, Nevo Y, Eyras E, Sperling R, Stamm S. Dual function of C/D box small nucleolar RNAs in rRNA modification and alternative pre-mRNA splicing.. Proc Natl Acad Sci U S A 2016 Mar 22;113(12):E1625-34.
    doi: 10.1073/pnas.1519292113pmc: PMC4812717pubmed: 26957605google scholar: lookup
  44. Scott MS, Ono M. From snoRNA to miRNA: Dual function regulatory non-coding RNAs.. Biochimie 2011 Nov;93(11):1987-92.
    doi: 10.1016/j.biochi.2011.05.026pmc: PMC3476530pubmed: 21664409google scholar: lookup
  45. Bachellerie JP, Cavaillé J, Hüttenhofer A. The expanding snoRNA world.. Biochimie 2002 Aug;84(8):775-90.
    doi: 10.1016/S0300-9084(02)01402-5pubmed: 12457565google scholar: lookup
  46. Kishore S, Stamm S. Regulation of alternative splicing by snoRNAs.. Cold Spring Harb Symp Quant Biol 2006;71:329-34.
    doi: 10.1101/sqb.2006.71.024pubmed: 17381313google scholar: lookup
  47. Gong M, Yu B, Wang J, Wang Y, Liu M, Paul C, Millard RW, Xiao DS, Ashraf M, Xu M. Mesenchymal stem cells release exosomes that transfer miRNAs to endothelial cells and promote angiogenesis.. Oncotarget 2017 Jul 11;8(28):45200-45212.
    doi: 10.18632/oncotarget.16778pmc: PMC5542178pubmed: 28423355google scholar: lookup
  48. Urbich C, Kuehbacher A, Dimmeler S. Role of microRNAs in vascular diseases, inflammation, and angiogenesis.. Cardiovasc Res 2008 Sep 1;79(4):581-8.
    doi: 10.1093/cvr/cvn156pubmed: 18550634google scholar: lookup
  49. Sen CK, Gordillo GM, Khanna S, Roy S. Micromanaging vascular biology: tiny microRNAs play big band.. J Vasc Res 2009;46(6):527-40.
    doi: 10.1159/000226221pmc: PMC2803349pubmed: 19571573google scholar: lookup
  50. Pakravan K, Babashah S, Sadeghizadeh M, Mowla SJ, Mossahebi-Mohammadi M, Ataei F, Dana N, Javan M. MicroRNA-100 shuttled by mesenchymal stem cell-derived exosomes suppresses in vitro angiogenesis through modulating the mTOR/HIF-1α/VEGF signaling axis in breast cancer cells.. Cell Oncol (Dordr) 2017 Oct;40(5):457-470.
    doi: 10.1007/s13402-017-0335-7pubmed: 28741069google scholar: lookup
  51. 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 Jun 1;129(11):2182-9.
    doi: 10.1242/jcs.170373pubmed: 27252357google scholar: lookup
  52. Fang L, Deng Z, Shatseva T, Yang J, Peng C, Du WW, Yee AJ, Ang LC, He C, Shan SW, Yang BB. MicroRNA miR-93 promotes tumor growth and angiogenesis by targeting integrin-β8.. Oncogene 2011 Feb 17;30(7):806-21.
    doi: 10.1038/onc.2010.465pubmed: 20956944google scholar: lookup
  53. Liang H, Wang F, Chu D, Zhang W, Liao Z, Fu Z, Yan X, Zhu H, Guo W, Zhang Y, Guan W, Chen X. miR-93 functions as an oncomiR for the downregulation of PDCD4 in gastric carcinoma.. Sci Rep 2016 Mar 29;6:23772.
    doi: 10.1038/srep23772pmc: PMC4810498pubmed: 27021515google scholar: lookup
  54. Liu LJ, Yu JJ, Xu XL. MicroRNA-93 inhibits apoptosis and promotes proliferation, invasion and migration of renal cell carcinoma ACHN cells via the TGF-β/Smad signaling pathway by targeting RUNX3.. Am J Transl Res 2017;9(7):3499-3513.
    pmc: PMC5527264pubmed: 28804566
  55. Kane NM, Howard L, Descamps B, Meloni M, McClure J, Lu R, McCahill A, Breen C, Mackenzie RM, Delles C, Mountford JC, Milligan G, Emanueli C, Baker AH. Role of microRNAs 99b, 181a, and 181b in the differentiation of human embryonic stem cells to vascular endothelial cells.. Stem Cells 2012 Apr;30(4):643-54.
    doi: 10.1002/stem.1026pmc: PMC3490385pubmed: 22232059google scholar: lookup
  56. Deng C, Liu G. The PI3K/Akt signalling pathway plays essential roles in mesenchymal stem cells.. British Biomedical Bulletin 2017;5(2):p. 301.
  57. Phinney DG, Di Giuseppe M, Njah J, Sala E, Shiva S, St Croix CM, Stolz DB, Watkins SC, Di YP, Leikauf GD, Kolls J, Riches DW, Deiuliis G, Kaminski N, Boregowda SV, McKenna DH, Ortiz LA. Mesenchymal stem cells use extracellular vesicles to outsource mitophagy and shuttle microRNAs.. Nat Commun 2015 Oct 7;6:8472.
    doi: 10.1038/ncomms9472pmc: PMC4598952pubmed: 26442449google scholar: lookup
  58. Jang SC, Crescitelli R, Cvjetkovic A. A subgroup of mitochondrial extracellular vesicles discovered in human melanoma tissues are detectable in patient blood.. bioRxiv 2017.
    doi: 10.1101/174193google scholar: lookup
  59. Soubannier V, McLelland GL, Zunino R, Braschi E, Rippstein P, Fon EA, McBride HM. A vesicular transport pathway shuttles cargo from mitochondria to lysosomes.. Curr Biol 2012 Jan 24;22(2):135-41.
    doi: 10.1016/j.cub.2011.11.057pubmed: 22226745google scholar: lookup
  60. Willms E, Johansson HJ, Mäger I, Lee Y, Blomberg KE, Sadik M, Alaarg A, Smith CI, Lehtiö J, El Andaloussi S, Wood MJ, Vader P. Cells release subpopulations of exosomes with distinct molecular and biological properties.. Sci Rep 2016 Mar 2;6:22519.
    doi: 10.1038/srep22519pmc: PMC4773763pubmed: 26931825google scholar: lookup

Citations

This article has been cited 21 times.
  1. De Ciucis CG, Fruscione F, De Paolis L, Mecocci S, Zinellu S, Guardone L, Franzoni G, Cappelli K, Razzuoli E. Toll-like Receptors and Cytokine Modulation by Goat Milk Extracellular Vesicles in a Model of Intestinal Inflammation. Int J Mol Sci 2023 Jul 4;24(13).
    doi: 10.3390/ijms241311096pubmed: 37446274google scholar: lookup
  2. Adelipour M, Lubman DM, Kim J. Potential applications of mesenchymal stem cells and their derived exosomes in regenerative medicine. Expert Opin Biol Ther 2023 Jan-Jun;23(6):491-507.
    doi: 10.1080/14712598.2023.2211203pubmed: 37147781google scholar: lookup
  3. Mecocci S, Trabalza-Marinucci M, Cappelli K. Extracellular Vesicles from Animal Milk: Great Potentialities and Critical Issues. Animals (Basel) 2022 Nov 22;12(23).
    doi: 10.3390/ani12233231pubmed: 36496752google scholar: lookup
  4. Jia L, Li B, Fang C, Liang X, Xie Y, Sun X, Wang W, Zheng L, Wang D. Extracellular Vesicles of Mesenchymal Stem Cells Are More Effectively Accessed through Polyethylene Glycol-Based Precipitation than by Ultracentrifugation. Stem Cells Int 2022;2022:3577015.
    doi: 10.1155/2022/3577015pubmed: 36110890google scholar: lookup
  5. Hart DA. One of the Primary Functions of Tissue-Resident Pluripotent Pericytes Cells May Be to Regulate Normal Organ Growth and Maturation: Implications for Attempts to Repair Tissues Later in Life. Int J Mol Sci 2022 May 14;23(10).
    doi: 10.3390/ijms23105496pubmed: 35628309google scholar: lookup
  6. Mecocci S, Ottaviani A, Razzuoli E, Fiorani P, Pietrucci D, De Ciucis CG, Dei Giudici S, Franzoni G, Chillemi G, Cappelli K. Cow Milk Extracellular Vesicle Effects on an In Vitro Model of Intestinal Inflammation. Biomedicines 2022 Feb 28;10(3).
    doi: 10.3390/biomedicines10030570pubmed: 35327370google scholar: lookup
  7. Mecocci S, Pietrucci D, Milanesi M, Pascucci L, Filippi S, Rosato V, Chillemi G, Capomaccio S, Cappelli K. Transcriptomic Characterization of Cow, Donkey and Goat Milk Extracellular Vesicles Reveals Their Anti-Inflammatory and Immunomodulatory Potential. Int J Mol Sci 2021 Nov 25;22(23).
    doi: 10.3390/ijms222312759pubmed: 34884564google scholar: lookup
  8. Hotham WE, Thompson C, Szu-Ting L, Henson FMD. The anti-inflammatory effects of equine bone marrow stem cell-derived extracellular vesicles on autologous chondrocytes. Vet Rec Open 2021 Dec;8(1):e22.
    doi: 10.1002/vro2.22pubmed: 34795904google scholar: lookup
  9. Hart DA. What Molecular Recognition Systems Do Mesenchymal Stem Cells/Medicinal Signaling Cells (MSC) Use to Facilitate Cell-Cell and Cell Matrix Interactions? A Review of Evidence and Options. Int J Mol Sci 2021 Aug 11;22(16).
    doi: 10.3390/ijms22168637pubmed: 34445341google scholar: lookup
  10. Harman RM, Marx C, Van de Walle GR. Translational Animal Models Provide Insight Into Mesenchymal Stromal Cell (MSC) Secretome Therapy. Front Cell Dev Biol 2021;9:654885.
    doi: 10.3389/fcell.2021.654885pubmed: 33869217google scholar: lookup
  11. Zakirova EY, Aimaletdinov AM, Malanyeva AG, Rutland CS, Rizvanov AA. Extracellular Vesicles: New Perspectives of Regenerative and Reproductive Veterinary Medicine. Front Vet Sci 2020;7:594044.
    doi: 10.3389/fvets.2020.594044pubmed: 33330719google scholar: lookup
  12. Mecocci S, Gevi F, Pietrucci D, Cavinato L, Luly FR, Pascucci L, Petrini S, Ascenzioni F, Zolla L, Chillemi G, Cappelli K. Anti-Inflammatory Potential of Cow, Donkey and Goat Milk Extracellular Vesicles as Revealed by Metabolomic Profile. Nutrients 2020 Sep 23;12(10).
    doi: 10.3390/nሐ2908pubmed: 32977543google scholar: lookup
  13. Kim KH, Park TS, Cho BW, Kim TM. Nanoparticles from Equine Fetal Bone Marrow-Derived Cells Enhance the Survival of Injured Chondrocytes. Animals (Basel) 2020 Sep 23;10(10).
    doi: 10.3390/ani10101723pubmed: 32977476google scholar: lookup
  14. Mocchi M, Dotti S, Bue MD, Villa R, Bari E, Perteghella S, Torre ML, Grolli S. Veterinary Regenerative Medicine for Musculoskeletal Disorders: Can Mesenchymal Stem/Stromal Cells and Their Secretome Be the New Frontier?. Cells 2020 Jun 11;9(6).
    doi: 10.3390/cells9061453pubmed: 32545382google scholar: lookup
  15. Zappaterra M, Gioiosa S, Chillemi G, Zambonelli P, Davoli R. Muscle transcriptome analysis identifies genes involved in ciliogenesis and the molecular cascade associated with intramuscular fat content in Large White heavy pigs. PLoS One 2020;15(5):e0233372.
    doi: 10.1371/journal.pone.0233372pubmed: 32428048google scholar: lookup
  16. Zhang J, Liu Y, Yin W, Hu X. Adipose-derived stromal cells in regulation of hematopoiesis. Cell Mol Biol Lett 2020;25:16.
    doi: 10.1186/s11658-020-00209-wpubmed: 32161623google scholar: lookup
  17. Liu J, Gao F, Wang D, Zhou R, Huang C. Effects and mechanisms of exosomes in microenvironment angiogenesis in breast cancer: An updated review. Oncol Res 2025;33(6):1323-1334.
    doi: 10.32604/or.2024.059113pubmed: 40486870google scholar: lookup
  18. Lanci A, Iacono E, Merlo B. Therapeutic Application of Extracellular Vesicles Derived from Mesenchymal Stem Cells in Domestic Animals. Animals (Basel) 2024 Jul 24;14(15).
    doi: 10.3390/ani14152147pubmed: 39123673google scholar: lookup
  19. Mecocci S, Pietrucci D, Milanesi M, Capomaccio S, Pascucci L, Evangelista C, Basiricò L, Bernabucci U, Chillemi G, Cappelli K. Comparison of colostrum and milk extracellular vesicles small RNA cargo in water buffalo. Sci Rep 2024 Aug 3;14(1):17991.
    doi: 10.1038/s41598-024-67249-6pubmed: 39097641google scholar: lookup
  20. O'Brien TJ, Hollinshead F, Goodrich LR. Extracellular vesicles in the treatment and prevention of osteoarthritis: can horses help us translate this therapy to humans?. Extracell Vesicles Circ Nucl Acids 2023 Jun;4(2):151-169.
    doi: 10.20517/evcna.2023.11pubmed: 37829144google scholar: lookup
  21. Ju YK, Fang BR. [Research advances on the mechanism of extracellular vesicles of adipose-derived mesenchymal stem cells in promoting wound angiogenesis]. Zhonghua Shao Shang Yu Chuang Mian Xiu Fu Za Zhi 2023 Jan 20;39(1):85-90.
    doi: 10.3760/cma.j.cn501225-20220322-00080pubmed: 36740432google scholar: lookup
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