Analyze Diet
Frontiers in veterinary science2022; 9; 901269; doi: 10.3389/fvets.2022.901269

Small non-coding RNA landscape of extracellular vesicles from a post-traumatic model of equine osteoarthritis.

Abstract: Extracellular vesicles comprise an as yet inadequately investigated intercellular communication pathway in the field of early osteoarthritis. We hypothesised that the small non-coding RNA expression pattern in synovial fluid and plasma would change during progression of experimental osteoarthritis. In this study, we conducted small RNA sequencing to provide a comprehensive overview of the temporal expression profiles of small non-coding transcripts carried by extracellular vesicles derived from plasma and synovial fluid for the first time in a posttraumatic model of equine osteoarthritis. Additionally, we characterised synovial fluid and plasma-derived extracellular vesicles with respect to quantity, size, and surface markers. The different temporal expressions of seven microRNAs in plasma and synovial fluid-derived extracellular vesicles, eca-miR-451, eca-miR-25, eca-miR-215, eca-miR-92a, eca-miR-let-7c, eca-miR-486-5p, and eca-miR-23a, and four snoRNAs, U3, snord15, snord46, and snord58, represent potential biomarkers for early osteoarthritis. Bioinformatics analysis of the differentially expressed microRNAs in synovial fluid highlighted that in early osteoarthritis these related to the inhibition of cell cycle, cell cycle progression, DNA damage and cell proliferation as well as increased cell viability and differentiation of stem cells. Plasma and synovial fluid-derived extracellular vesicle small non-coding signatures have been established for the first time in a temporal model of osteoarthritis. These could serve as novel biomarkers for evaluation of osteoarthritis progression or act as potential therapeutic targets.
Publication Date: 2022-08-08 PubMed ID: 36003409PubMed Central: PMC9393553DOI: 10.3389/fvets.2022.901269Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

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 observes the changes in small non-coding RNA in extracellular vesicles present in synovial fluid and plasma during the progression of experimental osteoarthritis, identifying potential biomarkers that could help detect early osteoarthritis or serve as therapeutic targets.

Role of Extracellular Vesicles and Biomarkers in Osteoarthritis

  • The study revolves around extracellular vesicles, which are a crucial part of intercellular communication, meaning they help cells ‘talk’ to each other. However, their role in early osteoarthritis remains not well understood.
  • The researchers hypothesise that the expression pattern of small non-coding RNA, a type of RNA molecule that does not encode a protein but plays various roles in gene regulation, changes as osteoarthritis progresses.
  • These RNAs are carried by extracellular vesicles in plasma (the liquid part of our blood) and synovial fluid, a substance that reduces friction in the joints.
  • By examining the changes in these RNA patterns, the researchers hope to identify potential biomarkers that can indicate the early onset of osteoarthritis.

Exploring RNA and Discovering Potential Biomarkers

  • The study involved sequencing the small RNA in the extracellular vesicles to understand the expression profiles in a model of equine osteoarthritis.
  • The researchers noticed different expression times for seven microRNAs and four snoRNAs, suggesting these could serve as possible biomarkers for early detection of the disease.
  • These RNAs may also indicate increased cell viability and differentiation of stem cells, which have important roles in tissue repair and regeneration.
  • The study also provided a detailed view of the quantity, size, and surface markers of the vesicles in synovial fluid and plasma.

Impact and Future Opportunities

  • This study is significant because it offers a first glimpse into the small non-coding RNA signatures of extracellular vesicles in plasma and synovial fluid in the case of osteoarthritis.
  • It suggests that these molecular signatures could be further explored as potential biomarkers for diagnosing the early onset of osteoarthritis.
  • It could also pave the way for using these identified biomarkers as therapeutic targets, potentially leading to new treatments for the disease.

Cite This Article

APA
Anderson JR, Jacobsen S, Walters M, Bundgaard L, Diendorfer A, Hackl M, Clarke EJ, James V, Peffers MJ. (2022). Small non-coding RNA landscape of extracellular vesicles from a post-traumatic model of equine osteoarthritis. Front Vet Sci, 9, 901269. https://doi.org/10.3389/fvets.2022.901269

Publication

ISSN: 2297-1769
NlmUniqueID: 101666658
Country: Switzerland
Language: English
Volume: 9
Pages: 901269
PII: 901269

Researcher Affiliations

Anderson, James R
  • Department of Musculoskeletal and Ageing Science, Institute of Life Course and Medical Sciences, University of Liverpool, Liverpool, United Kingdom.
Jacobsen, Stine
  • Department of Veterinary Clinical Sciences, University of Copenhagen, Taastrup, Denmark.
Walters, Marie
  • Department of Veterinary Clinical Sciences, University of Copenhagen, Taastrup, Denmark.
Bundgaard, Louise
  • Department of Veterinary Clinical Sciences, University of Copenhagen, Taastrup, Denmark.
Diendorfer, Andreas
  • TAmiRNA, TAmiRNA GmbH, Vienna, Austria.
Hackl, Matthias
  • TAmiRNA, TAmiRNA GmbH, Vienna, Austria.
Clarke, Emily J
  • Department of Musculoskeletal and Ageing Science, Institute of Life Course and Medical Sciences, University of Liverpool, Liverpool, United Kingdom.
James, Victoria
  • School of Veterinary Medicine and Science, University of Nottingham, Loughborough, United Kingdom.
Peffers, Mandy J
  • Department of Musculoskeletal and Ageing Science, Institute of Life Course and Medical Sciences, University of Liverpool, Liverpool, United Kingdom.

Grant Funding

  • MR/P020941/1 / Medical Research Council

Conflict of Interest Statement

Authors AD and MH were employed by TAmiRNA GmbH. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 100 references
  1. Hunter DJ, Bierma-Zeinstra S. Osteoarthritis.. Lancet 2019 Apr 27;393(10182):1745-1759.
    doi: 10.1016/S0140-6736(19)30417-9pubmed: 31034380google scholar: lookup
  2. Ireland JL, Clegg PD, McGowan CM, McKane SA, Chandler KJ, Pinchbeck GL. Comparison of owner-reported health problems with veterinary assessment of geriatric horses in the United Kingdom.. Equine Vet J 2012 Jan;44(1):94-100.
  3. Todhunter PG, Kincaid SA, Todhunter RJ, Kammermann JR, Johnstone B, Baird AN, Hanson RR, Wright JM, Lin HC, Purohit RC. Immunohistochemical analysis of an equine model of synovitis-induced arthritis.. Am J Vet Res 1996 Jul;57(7):1080-93.
    pubmed: 8807026
  4. Little CB, Ghosh P, Rose R. The effect of strenuous versus moderate exercise on the metabolism of proteoglycans in articular cartilage from different weight-bearing regions of the equine third carpal bone.. Osteoarthritis Cartilage 1997 May;5(3):161-72.
    doi: 10.1016/S1063-4584(97)80011-8pubmed: 9219679google scholar: lookup
  5. Goldring MB. Update on the biology of the chondrocyte and new approaches to treating cartilage diseases.. Best Pract Res Clin Rheumatol 2006 Oct;20(5):1003-25.
    doi: 10.1016/j.berh.2006.06.003pubmed: 16980220google scholar: lookup
  6. Ripmeester EGJ, Caron MMJ, van den Akker GGH, Surtel DAM, Cremers A, Balaskas P, Dyer P, Housmans BAC, Chabronova A, Smagul A, Fang Y, van Rhijn LW, Peffers MJ, Welting TJM. Impaired chondrocyte U3 snoRNA expression in osteoarthritis impacts the chondrocyte protein translation apparatus.. Sci Rep 2020 Aug 10;10(1):13426.
    doi: 10.1038/s41598-020-70453-9pmc: PMC7417995pubmed: 32778764google scholar: lookup
  7. Peffers MJ, Chabronova A, Balaskas P, Fang Y, Dyer P, Cremers A, Emans PJ, Feczko PZ, Caron MM, Welting TJM. SnoRNA signatures in cartilage ageing and osteoarthritis.. Sci Rep 2020 Jun 30;10(1):10641.
    doi: 10.1038/s41598-020-67446-zpmc: PMC7326970pubmed: 32606371google scholar: lookup
  8. Castanheira C, Balaskas P, Falls C, Ashraf-Kharaz Y, Clegg P, Burke K, Fang Y, Dyer P, Welting TJM, Peffers MJ. Equine synovial fluid small non-coding RNA signatures in early osteoarthritis.. BMC Vet Res 2021 Jan 9;17(1):26.
    doi: 10.1186/s12917-020-02707-7pmc: PMC7796526pubmed: 33422071google scholar: lookup
  9. Choudhuri S. Small noncoding RNAs: biogenesis, function, and emerging significance in toxicology.. J Biochem Mol Toxicol 2010 May-Jun;24(3):195-216.
    doi: 10.1002/jbt.20325pubmed: 20143452google scholar: lookup
  10. Tonge DP, Pearson MJ, Jones SW. The hallmarks of osteoarthritis and the potential to develop personalised disease-modifying pharmacological therapeutics.. Osteoarthritis Cartilage 2014 May;22(5):609-21.
    doi: 10.1016/j.joca.2014.03.004pubmed: 24632293google scholar: lookup
  11. Fu H, Hu D, Zhang L, Tang P. Role of extracellular vesicles in rheumatoid arthritis.. Mol Immunol 2018 Jan;93:125-132.
    doi: 10.1016/j.molimm.2017.11.016pubmed: 29175592google scholar: lookup
  12. 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 Jan 1;114(1):19-34.
    doi: 10.1093/cvr/cvx211pmc: PMC5852624pubmed: 29106545google scholar: lookup
  13. Besse B, Charrier M, Lapierre V, Dansin E, Lantz O, Planchard D, Le Chevalier T, Livartoski A, Barlesi F, Laplanche A, Ploix S, Vimond N, Peguillet I, Théry C, Lacroix L, Zoernig I, Dhodapkar K, Dhodapkar M, Viaud S, Soria JC, Reiners KS, Pogge von Strandmann E, Vély F, Rusakiewicz S, Eggermont A, Pitt JM, Zitvogel L, Chaput N. Dendritic cell-derived exosomes as maintenance immunotherapy after first line chemotherapy in NSCLC.. Oncoimmunology 2016 Apr;5(4):e1071008.
  14. Bellavia D, Raimondi L, Costa V, De Luca A, Carina V, Maglio M, Fini M, Alessandro R, Giavaresi G. Engineered exosomes: A new promise for the management of musculoskeletal diseases.. Biochim Biophys Acta Gen Subj 2018 Sep;1862(9):1893-1901.
    doi: 10.1016/j.bbagen.2018.06.003pubmed: 29885361google scholar: lookup
  15. Peffers MJ, Liu X, Clegg PD. Transcriptomic profiling of cartilage ageing.. Genom Data 2014 Dec;2:27-8.
    doi: 10.1016/j.gdata.2014.03.001pmc: PMC4536077pubmed: 26484061google scholar: lookup
  16. Balaskas P, Goljanek-Whysall K, Clegg P, Fang Y, Cremers A, Emans P, Welting T, Peffers M. MicroRNA Profiling in Cartilage Ageing.. Int J Genomics 2017;2017:2713725.
    doi: 10.1155/2017/2713725pmc: PMC5584353pubmed: 28890892google scholar: lookup
  17. Steinbusch MM, Fang Y, Milner PI, Clegg PD, Young DA, Welting TJ, Peffers MJ. Serum snoRNAs as biomarkers for joint ageing and post traumatic osteoarthritis.. Sci Rep 2017 Mar 2;7:43558.
    doi: 10.1038/srep43558pmc: PMC5333149pubmed: 28252005google scholar: lookup
  18. Castanheira CIGD, Anderson JR, Fang Y, Milner PI, Goljanek-Whysall K, House L, Clegg PD, Peffers MJ. Mouse microRNA signatures in joint ageing and post-traumatic osteoarthritis.. Osteoarthr Cartil Open 2021 Dec;3(4):100186.
  19. Miyaki S. [Cartilage/chondrocyte research and osteoarthritis. The role of microRNAs and extracellular vesicles in osteoarthritis pathogenesis.].. Clin Calcium 2018;28(6):783-788.
    pubmed: 29848823
  20. Miyaki S, Lotz MK. Extracellular vesicles in cartilage homeostasis and osteoarthritis.. Curr Opin Rheumatol 2018 Jan;30(1):129-135.
  21. Murata K, Yoshitomi H, Tanida S, Ishikawa M, Nishitani K, Ito H, Nakamura T. Plasma and synovial fluid microRNAs as potential biomarkers of rheumatoid arthritis and osteoarthritis.. Arthritis Res Ther 2010;12(3):R86.
    doi: 10.1186/ar3013pmc: PMC2911870pubmed: 20470394google scholar: lookup
  22. Li YH, Tavallaee G, Tokar T, Nakamura A, Sundararajan K, Weston A, Sharma A, Mahomed NN, Gandhi R, Jurisica I, Kapoor M. Identification of synovial fluid microRNA signature in knee osteoarthritis: differentiating early- and late-stage knee osteoarthritis.. Osteoarthritis Cartilage 2016 Sep;24(9):1577-86.
    doi: 10.1016/j.joca.2016.04.019pubmed: 27143365google scholar: lookup
  23. Borgonio Cuadra VM, González-Huerta NC, Romero-Córdoba S, Hidalgo-Miranda A, Miranda-Duarte A. Altered expression of circulating microRNA in plasma of patients with primary osteoarthritis and in silico analysis of their pathways.. PLoS One 2014;9(6):e97690.
  24. Aae TF, Karlsen TA, Haugen IK, Risberg MA, Lian OB, Brinchmann JE. Evaluating plasma extracellular vesicle microRNAs as possible biomarkers for osteoarthritis. Osteoarthritis Cartilage Open (2020) 2019:100018.
  25. Kaur S, Abu-Shahba AG, Paananen RO, Hongisto H, Hiidenmaa H, Skottman H, Seppänen-Kaijansinkko R, Mannerström B. Small non-coding RNA landscape of extracellular vesicles from human stem cells.. Sci Rep 2018 Oct 19;8(1):15503.
    doi: 10.1038/s41598-018-33899-6pmc: PMC6195565pubmed: 30341351google scholar: lookup
  26. Ni Z, Zhou S, Li S, Kuang L, Chen H, Luo X, Ouyang J, He M, Du X, Chen L. Exosomes: roles and therapeutic potential in osteoarthritis.. Bone Res 2020;8:25.
    doi: 10.1038/s41413-020-0100-9pmc: PMC7305215pubmed: 32596023google scholar: lookup
  27. Withrow J, Murphy C, Liu Y, Hunter M, Fulzele S, Hamrick MW. Extracellular vesicles in the pathogenesis of rheumatoid arthritis and osteoarthritis.. Arthritis Res Ther 2016 Dec 1;18(1):286.
    doi: 10.1186/s13075-016-1178-8pmc: PMC5134070pubmed: 27906035google scholar: lookup
  28. Ragni E, Perucca Orfei C, De Luca P, Lugano G, Viganò M, Colombini A, Valli F, Zacchetti D, Bollati V, de Girolamo L. Interaction with hyaluronan matrix and miRNA cargo as contributors for in vitro potential of mesenchymal stem cell-derived extracellular vesicles in a model of human osteoarthritic synoviocytes.. Stem Cell Res Ther 2019 Mar 29;10(1):109.
    doi: 10.1186/s13287-019-1215-zpmc: PMC6440078pubmed: 30922413google scholar: lookup
  29. Cai J, Wu J, Wang J, Li Y, Hu X, Luo S, Xiang D. Extracellular vesicles derived from different sources of mesenchymal stem cells: therapeutic effects and translational potential.. Cell Biosci 2020;10:69.
    doi: 10.1186/s13578-020-00427-xpmc: PMC7245623pubmed: 32483483google scholar: lookup
  30. Cantaluppi V, Gatti S, Medica D, Figliolini F, Bruno S, Deregibus MC, Sordi A, Biancone L, Tetta C, Camussi G. Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells.. Kidney Int 2012 Aug;82(4):412-27.
    doi: 10.1038/ki.2012.105pubmed: 22495296google scholar: lookup
  31. Qiu G, Zheng G, Ge M, Wang J, Huang R, Shu Q, Xu J. Mesenchymal stem cell-derived extracellular vesicles affect disease outcomes via transfer of microRNAs.. Stem Cell Res Ther 2018 Nov 21;9(1):320.
    doi: 10.1186/s13287-018-1069-9pmc: PMC6249826pubmed: 30463593google scholar: lookup
  32. Fathollahi A, Aslani S, Jamshidi A, Mahmoudi M. Epigenetics in osteoarthritis: Novel spotlight.. J Cell Physiol 2019 Aug;234(8):12309-12324.
    doi: 10.1002/jcp.28020pubmed: 30659623google scholar: lookup
  33. Jin Z, Ren J, Qi S. Human bone mesenchymal stem cells-derived exosomes overexpressing microRNA-26a-5p alleviate osteoarthritis via down-regulation of PTGS2.. Int Immunopharmacol 2020 Jan;78:105946.
    doi: 10.1016/j.intimp.2019.105946pubmed: 31784400google scholar: lookup
  34. Teeple E, Jay GD, Elsaid KA, Fleming BC. Animal models of osteoarthritis: challenges of model selection and analysis.. AAPS J 2013 Apr;15(2):438-46.
    doi: 10.1208/s12248-013-9454-xpmc: PMC3675748pubmed: 23329424google scholar: lookup
  35. Frisbie DD, Kawcak CE, Trotter GW, Powers BE, Walton RM, McIlwraith CW. Effects of triamcinolone acetonide on an in vivo equine osteochondral fragment exercise model.. Equine Vet J 1997 Sep;29(5):349-59.
  36. McIlwraith CW, Frisbie DD, Kawcak CE. The horse as a model of naturally occurring osteoarthritis.. Bone Joint Res 2012 Nov;1(11):297-309.
  37. Frisbie DD, Kawcak CE, McIlwraith CW. Evaluation of the effect of extracorporeal shock wave treatment on experimentally induced osteoarthritis in middle carpal joints of horses.. Am J Vet Res 2009 Apr;70(4):449-54.
    doi: 10.2460/ajvr.70.4.449pubmed: 19335099google scholar: lookup
  38. McIlwraith CW, Frisbie DD, Kawcak CE, Fuller CJ, Hurtig M, Cruz A. The OARSI histopathology initiative - recommendations for histological assessments of osteoarthritis in the horse.. Osteoarthritis Cartilage 2010 Oct;18 Suppl 3:S93-105.
    doi: 10.1016/j.joca.2010.05.031pubmed: 20864027google scholar: lookup
  39. Filipe V, Hawe A, Jiskoot W. Critical evaluation of Nanoparticle Tracking Analysis (NTA) by NanoSight for the measurement of nanoparticles and protein aggregates.. Pharm Res 2010 May;27(5):796-810.
    doi: 10.1007/s11095-010-0073-2pmc: PMC2852530pubmed: 20204471google scholar: lookup
  40. Diendorfer A, Khamina K, Pultar M, Hackl M. miND (miRNA NGS Discovery pipeline): a small RNA-seq analysis pipeline and report generator for microRNA biomarker discovery studies. F1000 Res (2022) 2022:94159.1.
  41. Andrews S. FastQC: A Quality Control Tool for High Throughput Sequence Data. .
  42. Ewels P, Magnusson M, Lundin S, Käller M. MultiQC: summarize analysis results for multiple tools and samples in a single report.. Bioinformatics 2016 Oct 1;32(19):3047-8.
  43. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnetjournal (2011) 17:10.
    doi: 10.14806/ej.17.1.200google scholar: lookup
  44. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.. Genome Biol 2009;10(3):R25.
    doi: 10.1186/gb-2009-10-3-r25pmc: PMC2690996pubmed: 19261174google scholar: lookup
  45. Friedländer MR, Mackowiak SD, Li N, Chen W, Rajewsky N. miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades.. Nucleic Acids Res 2012 Jan;40(1):37-52.
    doi: 10.1093/nar/gkr688pmc: PMC3245920pubmed: 21911355google scholar: lookup
  46. Zerbino DR, Achuthan P, Akanni W, Amode MR, Barrell D, Bhai J, Billis K, Cummins C, Gall A, Girón CG, Gil L, Gordon L, Haggerty L, Haskell E, Hourlier T, Izuogu OG, Janacek SH, Juettemann T, To JK, Laird MR, Lavidas I, Liu Z, Loveland JE, Maurel T, McLaren W, Moore B, Mudge J, Murphy DN, Newman V, Nuhn M, Ogeh D, Ong CK, Parker A, Patricio M, Riat HS, Schuilenburg H, Sheppard D, Sparrow H, Taylor K, Thormann A, Vullo A, Walts B, Zadissa A, Frankish A, Hunt SE, Kostadima M, Langridge N, Martin FJ, Muffato M, Perry E, Ruffier M, Staines DM, Trevanion SJ, Aken BL, Cunningham F, Yates A, Flicek P. Ensembl 2018.. Nucleic Acids Res 2018 Jan 4;46(D1):D754-D761.
    doi: 10.1093/nar/gkx1098pmc: PMC5753206pubmed: 29155950google scholar: lookup
  47. Griffiths-Jones S. The microRNA Registry.. Nucleic Acids Res 2004 Jan 1;32(Database issue):D109-11.
    doi: 10.1093/nar/gkh023pmc: PMC308757pubmed: 14681370google scholar: lookup
  48. . RNAcentral: a hub of information for non-coding RNA sequences.. Nucleic Acids Res 2019 Jan 8;47(D1):D221-D229.
    doi: 10.1093/nar/gky1034pmc: PMC6324050pubmed: 30395267google scholar: lookup
  49. 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.
  50. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.. Genome Biol 2014;15(12):550.
    doi: 10.1186/s13059-014-0550-8pmc: PMC4302049pubmed: 25516281google scholar: lookup
  51. Chen J, Bardes EE, Aronow BJ, Jegga AG. ToppGene Suite for gene list enrichment analysis and candidate gene prioritization.. Nucleic Acids Res 2009 Jul;37(Web Server issue):W305-11.
    doi: 10.1093/nar/gkp427pmc: PMC2703978pubmed: 19465376google scholar: lookup
  52. Supek F, Bošnjak M, Škunca N, Šmuc T. REVIGO summarizes and visualizes long lists of gene ontology terms.. PLoS One 2011;6(7):e21800.
  53. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. Cytoscape: a software environment for integrated models of biomolecular interaction networks.. Genome Res 2003 Nov;13(11):2498-504.
    doi: 10.1101/gr.1239303pmc: PMC403769pubmed: 14597658google scholar: lookup
  54. Walters M, Skovgaard K, Heegaard P, Peffers MJ, Fang Y, Bundgaard L. Changes in small non-coding RNA expression in synovial fluid during disease progression in an equine model of experimental osteoarthritis. Osteoarthritis Cartilage (2021) 29:SS155.
  55. Théry C, Witwer KW, Aikawa E, Alcaraz MJ, Anderson JD, Andriantsitohaina R, Antoniou A, Arab T, Archer F, Atkin-Smith GK, Ayre DC, Bach JM, Bachurski D, Baharvand H, Balaj L, Baldacchino S, Bauer NN, Baxter AA, Bebawy M, Beckham C, Bedina Zavec A, Benmoussa A, Berardi AC, Bergese P, Bielska E, Blenkiron C, Bobis-Wozowicz S, Boilard E, Boireau W, Bongiovanni A, Borràs FE, Bosch S, Boulanger CM, Breakefield X, Breglio AM, Brennan MÁ, Brigstock DR, Brisson A, Broekman ML, Bromberg JF, Bryl-Górecka P, Buch S, Buck AH, Burger D, Busatto S, Buschmann D, Bussolati B, Buzás EI, Byrd JB, Camussi G, Carter DR, Caruso S, Chamley LW, Chang YT, Chen C, Chen S, Cheng L, Chin AR, Clayton A, Clerici SP, Cocks A, Cocucci E, Coffey RJ, Cordeiro-da-Silva A, Couch Y, Coumans FA, Coyle B, Crescitelli R, Criado MF, D'Souza-Schorey C, Das S, Datta Chaudhuri A, de Candia P, De Santana EF, De Wever O, Del Portillo HA, Demaret T, Deville S, Devitt A, Dhondt B, Di Vizio D, Dieterich LC, Dolo V, Dominguez Rubio AP, Dominici M, Dourado MR, Driedonks TA, Duarte FV, Duncan HM, Eichenberger RM, Ekström K, El Andaloussi S, Elie-Caille C, Erdbrügger U, Falcón-Pérez JM, Fatima F, Fish JE, Flores-Bellver M, Försönits A, Frelet-Barrand A, Fricke F, Fuhrmann G, Gabrielsson S, Gámez-Valero A, Gardiner C, Gärtner K, Gaudin R, Gho YS, Giebel B, Gilbert C, Gimona M, Giusti I, Goberdhan DC, Görgens A, Gorski SM, Greening DW, Gross JC, Gualerzi A, Gupta GN, Gustafson D, Handberg A, Haraszti RA, Harrison P, Hegyesi H, Hendrix A, Hill AF, Hochberg FH, Hoffmann KF, Holder B, Holthofer H, Hosseinkhani B, Hu G, Huang Y, Huber V, Hunt S, Ibrahim AG, Ikezu T, Inal JM, Isin M, Ivanova A, Jackson HK, Jacobsen S, Jay SM, Jayachandran M, Jenster G, Jiang L, Johnson SM, Jones JC, Jong A, Jovanovic-Talisman T, Jung S, Kalluri R, Kano SI, Kaur S, Kawamura Y, Keller ET, Khamari D, Khomyakova E, Khvorova A, Kierulf P, Kim KP, Kislinger T, Klingeborn M, Klinke DJ 2nd, Kornek M, Kosanović MM, Kovács ÁF, Krämer-Albers EM, Krasemann S, Krause M, Kurochkin IV, Kusuma GD, Kuypers S, Laitinen S, Langevin SM, Languino LR, Lannigan J, Lässer C, Laurent LC, Lavieu G, Lázaro-Ibáñez E, Le Lay S, Lee MS, Lee YXF, Lemos DS, Lenassi M, Leszczynska A, Li IT, Liao K, Libregts SF, Ligeti E, Lim R, Lim SK, Linē A, Linnemannstöns K, Llorente A, Lombard CA, Lorenowicz MJ, Lörincz ÁM, Lötvall J, Lovett J, Lowry MC, Loyer X, Lu Q, Lukomska B, Lunavat TR, Maas SL, Malhi H, Marcilla A, Mariani J, Mariscal J, Martens-Uzunova ES, Martin-Jaular L, Martinez MC, Martins VR, Mathieu M, Mathivanan S, Maugeri M, McGinnis LK, McVey MJ, Meckes DG Jr, Meehan KL, Mertens I, Minciacchi VR, Möller A, Møller Jørgensen M, Morales-Kastresana A, Morhayim J, Mullier F, Muraca M, Musante L, Mussack V, Muth DC, Myburgh KH, Najrana T, Nawaz M, Nazarenko I, Nejsum P, Neri C, Neri T, Nieuwland R, Nimrichter L, Nolan JP, Nolte-'t Hoen EN, Noren Hooten N, O'Driscoll L, O'Grady T, O'Loghlen A, Ochiya T, Olivier M, Ortiz A, Ortiz LA, Osteikoetxea X, Østergaard O, Ostrowski M, Park J, Pegtel DM, Peinado H, Perut F, Pfaffl MW, Phinney DG, Pieters BC, Pink RC, Pisetsky DS, Pogge von Strandmann E, Polakovicova I, Poon IK, Powell BH, Prada I, Pulliam L, Quesenberry P, Radeghieri A, Raffai RL, Raimondo S, Rak J, Ramirez MI, Raposo G, Rayyan MS, Regev-Rudzki N, Ricklefs FL, Robbins PD, Roberts DD, Rodrigues SC, Rohde E, Rome S, Rouschop KM, Rughetti A, Russell AE, Saá P, Sahoo S, Salas-Huenuleo E, Sánchez C, Saugstad JA, Saul MJ, Schiffelers RM, Schneider R, Schøyen TH, Scott A, Shahaj E, Sharma S, Shatnyeva O, Shekari F, Shelke GV, Shetty AK, Shiba K, Siljander PR, Silva AM, Skowronek A, Snyder OL 2nd, Soares RP, Sódar BW, Soekmadji C, Sotillo J, Stahl PD, Stoorvogel W, Stott SL, Strasser EF, Swift S, Tahara H, Tewari M, Timms K, Tiwari S, Tixeira R, Tkach M, Toh WS, Tomasini R, Torrecilhas AC, Tosar JP, Toxavidis V, Urbanelli L, Vader P, van Balkom BW, van der Grein SG, Van Deun J, van Herwijnen MJ, Van Keuren-Jensen K, van Niel G, van Royen ME, van Wijnen AJ, Vasconcelos MH, Vechetti IJ Jr, Veit TD, Vella LJ, Velot É, Verweij FJ, Vestad B, Viñas JL, Visnovitz T, Vukman KV, Wahlgren J, Watson DC, Wauben MH, Weaver A, Webber JP, Weber V, Wehman AM, Weiss DJ, Welsh JA, Wendt S, Wheelock AM, Wiener Z, Witte L, Wolfram J, Xagorari A, Xander P, Xu J, Yan X, Yáñez-Mó M, Yin H, Yuana Y, Zappulli V, Zarubova J, Žėkas V, Zhang JY, Zhao Z, Zheng L, Zheutlin AR, Zickler AM, Zimmermann P, Zivkovic AM, Zocco D, Zuba-Surma EK. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines.. J Extracell Vesicles 2018;7(1):1535750.
  56. Harding CV, Heuser JE, Stahl PD. Exosomes: looking back three decades and into the future.. J Cell Biol 2013 Feb 18;200(4):367-71.
    doi: 10.1083/jcb.201212113pmc: PMC3575527pubmed: 23420870google scholar: lookup
  57. Ale Ebrahim S, Ashtari A, Zamani Pedram M, Ale Ebrahim N, Sanati-Nezhad A. Publication Trends in Exosomes Nanoparticles for Cancer Detection.. Int J Nanomedicine 2020;15:4453-4470.
    doi: 10.2147/IJN.S247210pmc: PMC7326184pubmed: 32617003google scholar: lookup
  58. Tzaridis T, Bachurski D, Liu S, Surmann K, Babatz F, Gesell Salazar M, Völker U, Hallek M, Herrlinger U, Vorberg I, Coch C, Reiners KS, Hartmann G. Extracellular Vesicle Separation Techniques Impact Results from Human Blood Samples: Considerations for Diagnostic Applications.. Int J Mol Sci 2021 Aug 26;22(17).
    doi: 10.3390/ijms22179211pmc: PMC8431127pubmed: 34502122google scholar: lookup
  59. Brennan K, Martin K, FitzGerald SP, O'Sullivan J, Wu Y, Blanco A, Richardson C, Mc Gee MM. A comparison of methods for the isolation and separation of extracellular vesicles from protein and lipid particles in human serum.. Sci Rep 2020 Jan 23;10(1):1039.
    doi: 10.1038/s41598-020-57497-7pmc: PMC6978318pubmed: 31974468google scholar: lookup
  60. Raposo G, Stahl PD. Extracellular vesicles: a new communication paradigm?. Nat Rev Mol Cell Biol 2019 Sep;20(9):509-510.
    doi: 10.1038/s41580-019-0158-7pubmed: 31324871google scholar: lookup
  61. Foers AD, Chatfield S, Dagley LF, Scicluna BJ, Webb AI, Cheng L, Hill AF, Wicks IP, Pang KC. Enrichment of extracellular vesicles from human synovial fluid using size exclusion chromatography.. J Extracell Vesicles 2018;7(1):1490145.
  62. Esa A, Connolly KD, Williams R, Archer CW. Extracellular Vesicles in the Synovial Joint: Is there a Role in the Pathophysiology of Osteoarthritis?. Malays Orthop J 2019 Mar;13(1):1-7.
    doi: 10.5704/MOJ.1903.012pmc: PMC6459045pubmed: 31001376google scholar: lookup
  63. Zaborowski MP, Balaj L, Breakefield XO, Lai CP. Extracellular Vesicles: Composition, Biological Relevance, and Methods of Study.. Bioscience 2015 Aug 1;65(8):783-797.
    doi: 10.1093/biosci/biv084pmc: PMC4776721pubmed: 26955082google scholar: lookup
  64. Vestad B, Llorente A, Neurauter A, Phuyal S, Kierulf B, Kierulf P, Skotland T, Sandvig K, Haug KBF, Øvstebø R. Size and concentration analyses of extracellular vesicles by nanoparticle tracking analysis: a variation study.. J Extracell Vesicles 2017;6(1):1344087.
  65. Holcar M, Ferdin J, Sitar S, Tušek-Žnidarič M, Dolžan V, Plemenitaš A, Žagar E, Lenassi M. Enrichment of plasma extracellular vesicles for reliable quantification of their size and concentration for biomarker discovery.. Sci Rep 2020 Dec 7;10(1):21346.
    doi: 10.1038/s41598-020-78422-ypmc: PMC7721811pubmed: 33288809google scholar: lookup
  66. Kolhe R, Hunter M, Liu S, Jadeja RN, Pundkar C, Mondal AK, Mendhe B, Drewry M, Rojiani MV, Liu Y, Isales CM, Guldberg RE, Hamrick MW, Fulzele S. Gender-specific differential expression of exosomal miRNA in synovial fluid of patients with osteoarthritis.. Sci Rep 2017 May 17;7(1):2029.
    doi: 10.1038/s41598-017-01905-ypmc: PMC5435729pubmed: 28515465google scholar: lookup
  67. Gao K, Zhu W, Li H, Ma D, Liu W, Yu W, Wang L, Cao Y, Jiang Y. Association between cytokines and exosomes in synovial fluid of individuals with knee osteoarthritis.. Mod Rheumatol 2020 Jul;30(4):758-764.
    doi: 10.1080/14397595.2019.1651445pubmed: 31370732google scholar: lookup
  68. Zhao Y, Xu J. Synovial fluid-derived exosomal lncRNA PCGEM1 as biomarker for the different stages of osteoarthritis.. Int Orthop 2018 Dec;42(12):2865-2872.
    doi: 10.1007/s00264-018-4093-6pubmed: 30128669google scholar: lookup
  69. Avci O, Ünlü NL, Özkumur AY, Ünlü MS. Interferometric Reflectance Imaging Sensor (IRIS)--A Platform Technology for Multiplexed Diagnostics and Digital Detection.. Sensors (Basel) 2015 Jul 20;15(7):17649-65.
    doi: 10.3390/s150717649pmc: PMC4541952pubmed: 26205273google scholar: lookup
  70. Kowal J, Arras G, Colombo M, Jouve M, Morath JP, Primdal-Bengtson B, Dingli F, Loew D, Tkach M, Théry C. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes.. Proc Natl Acad Sci U S A 2016 Feb 23;113(8):E968-77.
    doi: 10.1073/pnas.1521230113pmc: PMC4776515pubmed: 26858453google scholar: lookup
  71. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends.. J Cell Biol 2013 Feb 18;200(4):373-83.
    doi: 10.1083/jcb.201211138pmc: PMC3575529pubmed: 23420871google scholar: lookup
  72. Andreu Z, Yáñez-Mó M. Tetraspanins in extracellular vesicle formation and function.. Front Immunol 2014;5:442.
    doi: 10.3389/fimmu.2014.00442pmc: PMC4165315pubmed: 25278937google scholar: lookup
  73. Caballero JN, Frenette G, Belleannée C, Sullivan R. CD9-positive microvesicles mediate the transfer of molecules to Bovine Spermatozoa during epididymal maturation.. PLoS One 2013;8(6):e65364.
  74. Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells.. Nat Cell Biol 2007 Jun;9(6):654-9.
    doi: 10.1038/ncb1596pubmed: 17486113google scholar: lookup
  75. Shao H, Im H, Castro CM, Breakefield X, Weissleder R, Lee H. New Technologies for Analysis of Extracellular Vesicles.. Chem Rev 2018 Feb 28;118(4):1917-1950.
    doi: 10.1021/acs.chemrev.7b00534pmc: PMC6029891pubmed: 29384376google scholar: lookup
  76. Turchinovich A, Weiz L, Langheinz A, Burwinkel B. Characterization of extracellular circulating microRNA.. Nucleic Acids Res 2011 Sep 1;39(16):7223-33.
    doi: 10.1093/nar/gkr254pmc: PMC3167594pubmed: 21609964google scholar: lookup
  77. Ali SA, Gandhi R, Potla P, Keshavarzi S, Espin-Garcia O, Shestopaloff K, Pastrello C, Bethune-Waddell D, Lively S, Perruccio AV, Rampersaud YR, Veillette C, Rockel JS, Jurisica I, Appleton CT, Kapoor M. Sequencing identifies a distinct signature of circulating microRNAs in early radiographic knee osteoarthritis.. Osteoarthritis Cartilage 2020 Nov;28(11):1471-1481.
    doi: 10.1016/j.joca.2020.07.003pubmed: 32738291google scholar: lookup
  78. Beyer C, Zampetaki A, Lin NY, Kleyer A, Perricone C, Iagnocco A, Distler A, Langley SR, Gelse K, Sesselmann S, Lorenzini R, Niemeier A, Swoboda B, Distler JH, Santer P, Egger G, Willeit J, Mayr M, Schett G, Kiechl S. Signature of circulating microRNAs in osteoarthritis.. Ann Rheum Dis 2015 Mar;74(3):e18.
  79. Ntoumou E, Tzetis M, Braoudaki M, Lambrou G, Poulou M, Malizos K, Stefanou N, Anastasopoulou L, Tsezou A. Serum microRNA array analysis identifies miR-140-3p, miR-33b-3p and miR-671-3p as potential osteoarthritis biomarkers involved in metabolic processes.. Clin Epigenetics 2017;9:127.
    doi: 10.1186/s13148-017-0428-1pmc: PMC5728069pubmed: 29255496google scholar: lookup
  80. Clayton A, Boilard E, Buzas EI, Cheng L, Falcón-Perez JM, Gardiner C, Gustafson D, Gualerzi A, Hendrix A, Hoffman A, Jones J, Lässer C, Lawson C, Lenassi M, Nazarenko I, O'Driscoll L, Pink R, Siljander PR, Soekmadji C, Wauben M, Welsh JA, Witwer K, Zheng L, Nieuwland R. Considerations towards a roadmap for collection, handling and storage of blood extracellular vesicles.. J Extracell Vesicles 2019;8(1):1647027.
  81. Tao SC, Guo SC, Zhang CQ. Platelet-derived Extracellular Vesicles: An Emerging Therapeutic Approach.. Int J Biol Sci 2017;13(7):828-834.
    doi: 10.7150/ijbs.19776pmc: PMC5555101pubmed: 28808416google scholar: lookup
  82. Palviainen M, Saraswat M, Varga Z, Kitka D, Neuvonen M, Puhka M, Joenväärä S, Renkonen R, Nieuwland R, Takatalo M, Siljander PRM. Extracellular vesicles from human plasma and serum are carriers of extravesicular cargo-Implications for biomarker discovery.. PLoS One 2020;15(8):e0236439.
  83. Rousseau JC, Millet M, Croset M, Sornay-Rendu E, Borel O, Chapurlat R. Association of circulating microRNAs with prevalent and incident knee osteoarthritis in women: the OFELY study.. Arthritis Res Ther 2020 Jan 2;22(1):2.
    doi: 10.1186/s13075-019-2086-5pmc: PMC6941326pubmed: 31898522google scholar: lookup
  84. Zhang X, Wang C, Zhao J, Xu J, Geng Y, Dai L, Huang Y, Fu SC, Dai K, Zhang X. miR-146a facilitates osteoarthritis by regulating cartilage homeostasis via targeting Camk2d and Ppp3r2.. Cell Death Dis 2017 Apr 6;8(4):e2734.
    doi: 10.1038/cddis.2017.146pmc: PMC5477577pubmed: 28383548google scholar: lookup
  85. Yamasaki K, Nakasa T, Miyaki S, Ishikawa M, Deie M, Adachi N, Yasunaga Y, Asahara H, Ochi M. Expression of MicroRNA-146a in osteoarthritis cartilage.. Arthritis Rheum 2009 Apr;60(4):1035-41.
    doi: 10.1002/art.24404pmc: PMC2670476pubmed: 19333945google scholar: lookup
  86. Kang L, Yang C, Song Y, Liu W, Wang K, Li S, Zhang Y. MicroRNA-23a-3p promotes the development of osteoarthritis by directly targeting SMAD3 in chondrocytes.. Biochem Biophys Res Commun 2016 Sep 9;478(1):467-473.
    doi: 10.1016/j.bbrc.2016.06.071pubmed: 27318087google scholar: lookup
  87. Seol D, McCabe DJ, Choe H, Zheng H, Yu Y, Jang K, Walter MW, Lehman AD, Ding L, Buckwalter JA, Martin JA. Chondrogenic progenitor cells respond to cartilage injury.. Arthritis Rheum 2012 Nov;64(11):3626-3637.
    doi: 10.1002/art.34613pmc: PMC4950521pubmed: 22777600google scholar: lookup
  88. Li Z, Huang Z, Bai L. Cell Interplay in Osteoarthritis.. Front Cell Dev Biol 2021;9:720477.
    doi: 10.3389/fcell.2021.720477pmc: PMC8369508pubmed: 34414194google scholar: lookup
  89. Müller M, Fazi F, Ciaudo C. Argonaute Proteins: From Structure to Function in Development and Pathological Cell Fate Determination.. Front Cell Dev Biol 2019;7:360.
    doi: 10.3389/fcell.2019.00360pmc: PMC6987405pubmed: 32039195google scholar: lookup
  90. Liu P, Zhang X, Li Z, Wei L, Peng Q, Liu C, Wu Y, Yan Q, Ma J. A significant role of transcription factors E2F in inflammation and tumorigenesis of nasopharyngeal carcinoma.. Biochem Biophys Res Commun 2020 Apr 16;524(4):816-824.
    doi: 10.1016/j.bbrc.2020.01.158pubmed: 32044038google scholar: lookup
  91. Pellicelli M, Picard C, Wang D, Lavigne P, Moreau A. E2F1 and TFDP1 Regulate PITX1 Expression in Normal and Osteoarthritic Articular Chondrocytes.. PLoS One 2016;11(11):e0165951.
  92. Liu Y, Zou R, Wang Z, Wen C, Zhang F, Lin F. Exosomal KLF3-AS1 from hMSCs promoted cartilage repair and chondrocyte proliferation in osteoarthritis.. Biochem J 2018 Nov 28;475(22):3629-3638.
    doi: 10.1042/BCJ20180675pubmed: 30341166google scholar: lookup
  93. van den Akker GGH, Caron MMJ, Peffers MJ, Welting TJM. Ribosome dysfunction in osteoarthritis.. Curr Opin Rheumatol 2022 Jan 1;34(1):61-67.
  94. Chabronova A, van den Akker GGH, Meekels-Steinbusch MMF, Friedrich F, Cremers A, Surtel DAM, Peffers MJ, van Rhijn LW, Lausch E, Zabel B, Caron MMJ, Welting TJM. Uncovering pathways regulating chondrogenic differentiation of CHH fibroblasts.. Noncoding RNA Res 2021 Dec;6(4):211-224.
    doi: 10.1016/j.ncrna.2021.12.003pmc: PMC8688813pubmed: 34988338google scholar: lookup
  95. Balaskas P, Green JA, Haqqi TM, Dyer P, Kharaz YA, Fang Y, Liu X, Welting TJM, Peffers MJ. Small Non-Coding RNAome of Ageing Chondrocytes.. Int J Mol Sci 2020 Aug 7;21(16).
    doi: 10.3390/ijms21165675pmc: PMC7461137pubmed: 32784773google scholar: lookup
  96. Peffers M, Liu X, Clegg P. Transcriptomic signatures in cartilage ageing.. Arthritis Res Ther 2013 Aug 23;15(4):R98.
    doi: 10.1186/ar4278pmc: PMC3978620pubmed: 23971731google scholar: lookup
  97. Pimlott Z, Hontoir F, Ashraf Kharaz Y, Anderson J, Dyer P, Collins J. Small nucleolar RNAs as mediators of oxidative stress in cross species cartilage and osteoarthritis. Osteoarthritis Cartilage (2020) 28:S342.
  98. Langhendries JL, Nicolas E, Doumont G, Goldman S, Lafontaine DL. The human box C/D snoRNAs U3 and U8 are required for pre-rRNA processing and tumorigenesis.. Oncotarget 2016 Sep 13;7(37):59519-59534.
    doi: 10.18632/oncotarget.11148pmc: PMC5312328pubmed: 27517747google scholar: lookup
  99. Peffers MJ, Fang Y, Welting TM, Haldenby S, Liu X, James V. Small RNA Sequencing Reveals Small Non-coding RNA Communication Between Synoviocytes and Chondrocytes. London: United Kingdom Extracellular Vesicle Society; (2019).
  100. Addis A, Clarke EJ, Peffers MJ. Characterisation of equine synovial fluid derived extracellular vesicles from young and old horses. Insider Imprint (2022) 5:25–9.
    doi: 10.17638/03150605google scholar: lookup

Citations

This article has been cited 23 times.
  1. Donnenfield JI, Karamchedu NP, Proffen BL, Molino J, Fleming BC, Murray MM. Transcriptomic changes in porcine articular cartilage one year following disruption of the anterior cruciate ligament. PLoS One 2023;18(5):e0284777.
    doi: 10.1371/journal.pone.0284777pubmed: 37134114google scholar: lookup
  2. Jammes M, Contentin R, Cassé F, Galéra P. Equine osteoarthritis: Strategies to enhance mesenchymal stromal cell-based acellular therapies. Front Vet Sci 2023;10:1115774.
    doi: 10.3389/fvets.2023.1115774pubmed: 36846261google scholar: lookup
  3. Baker ME, Lee S, Clinton M, Hackl M, Castanheira C, Peffers MJ, Taylor SE. Investigation of MicroRNA Biomarkers in Equine Distal Interphalangeal Joint Osteoarthritis. Int J Mol Sci 2022 Dec 8;23(24).
    doi: 10.3390/ijms232415526pubmed: 36555166google scholar: lookup
  4. Clarke EJ, Johnson E, Caamaño Gutierrez E, Andersen C, Berg LC, Jenkins RE, Lindegaard C, Uvebrant K, Lundgren-Åkerlund E, Turlo A, James V, Jacobsen S, Peffers MJ. Temporal extracellular vesicle protein changes following intraarticular treatment with integrin α10β1-selected mesenchymal stem cells in equine osteoarthritis. Front Vet Sci 2022;9:1057667.
    doi: 10.3389/fvets.2022.1057667pubmed: 36504839google scholar: lookup
  5. Mustonen AM, Lehmonen N, Oikari S, Capra J, Raekallio M, Mykkänen A, Paakkonen T, Rilla K, Niemelä T, Nieminen P. Counts of hyaluronic acid-containing extracellular vesicles decrease in naturally occurring equine osteoarthritis. Sci Rep 2022 Oct 20;12(1):17550.
    doi: 10.1038/s41598-022-21398-8pubmed: 36266410google scholar: lookup
  6. Clarke EJ, Lima C, Anderson JR, Castanheira C, Beckett A, James V, Hyett J, Goodacre R, Peffers MJ. Optical photothermal infrared spectroscopy can differentiate equine osteoarthritic plasma extracellular vesicles from healthy controls. Anal Methods 2022 Sep 29;14(37):3661-3670.
    doi: 10.1039/d2ay00779gpubmed: 36066093google scholar: lookup
  7. Zou Y, Lu Y, Lu S, Wei Z, Li L, Liao S, Zeng T, Zhang Y, Miao R. CGSDA: inferring snoRNA-disease associations via ChebNetII and GatedGCN. Front Genet 2025;16:1684484.
    doi: 10.3389/fgene.2025.1684484pubmed: 41170197google scholar: lookup
  8. Cullen JN, Cieslak J, Petersen JL, Bellone RR, Finno CJ, Kalbfleisch TS, Calloe K, Capomaccio S, Cappelli K, Coleman SJ, Distl O, Durward-Akhurst SA, Giulotto E, Hamilton NA, Hill EW, Katz LM, Klaerke DA, Lindgren G, MacHugh DE, Mackowski M, MacLeod JN, Metzger J, Murphy BA, Orlando L, Raudsepp T, Silvestrelli M, Strand E, Tozaki T, Trachsel DS, Valderrama Figueroa LS, Velie BD, Wade CM, Waud B, Mickelson JR, McCue ME. Charting the equine miRNA landscape: An integrated pipeline and browser for annotating, quantifying, and visualizing expression. PLoS Genet 2025 Sep;21(9):e1011835.
    doi: 10.1371/journal.pgen.1011835pubmed: 40911641google scholar: lookup
  9. Wang T, Ng CY, Ng BZJ, Toh WS, Hui JHP. Multi-omics analysis of small extracellular vesicles in osteoarthritis: bridging the gap between molecular insights and clinical applications. Burns Trauma 2025;13:tkaf023.
    doi: 10.1093/burnst/tkaf023pubmed: 40740687google scholar: lookup
  10. Chabronova A, Walters M, Regårdh S, Jacobsen S, Bundgaard L, Anderson JR, Peffers MJ. Exploring the roles of snoRNA-induced ribosome heterogeneity in equine osteoarthritis. Front Vet Sci 2025;12:1562508.
    doi: 10.3389/fvets.2025.1562508pubmed: 40709001google scholar: lookup
  11. Castanheira CIGD, Anderson JR, Clarke EJ, Hackl M, James V, Clegg PD, Peffers MJ. Extracellular Vesicle-Derived microRNA Crosstalk Between Equine Chondrocytes and Synoviocytes-An In Vitro Approach. Int J Mol Sci 2025 Apr 3;26(7).
    doi: 10.3390/ijms26073353pubmed: 40244190google scholar: lookup
  12. Klymiuk MC, Speer J, Marco I, Elashry MI, Heimann M, Wenisch S, Arnhold S. Determination of the miRNA profile of extracellular vesicles from equine mesenchymal stem cells after different treatments. Stem Cell Res Ther 2025 Apr 5;16(1):162.
    doi: 10.1186/s13287-025-04287-5pubmed: 40188160google scholar: lookup
  13. Atasoy-Zeybek A, Showel KK, Nagelli CV, Westendorf JJ, Evans CH. The intersection of aging and estrogen in osteoarthritis. NPJ Womens Health 2025;3(1):15.
    doi: 10.1038/s44294-025-00063-1pubmed: 40017990google scholar: lookup
  14. Walters M, Skovgaard K, Heegaard PMH, Fang Y, Kharaz YA, Bundgaard L, Skovgaard LT, Jensen HE, Andersen PH, Peffers MJ, Jacobsen S. Identification and characterisation of temporal abundance of microRNAs in synovial fluid from an experimental equine model of osteoarthritis. Equine Vet J 2025 Jul;57(4):1138-1150.
    doi: 10.1111/evj.14456pubmed: 39775906google scholar: lookup
  15. Alimoradi N, Ramezani A, Tahami M, Firouzabadi N. Metformin Exhibits Anti-Inflammatory Effects by Regulating microRNA-451/CXCL16 and B Cell Leukemia/Lymphoma 2 in Patients With Osteoarthritis. ACR Open Rheumatol 2025 Jan;7(1):e11755.
    doi: 10.1002/acr2.11755pubmed: 39435687google scholar: lookup
  16. Bundgaard L, Årman F, Åhrman E, Walters M, Auf dem Keller U, Malmström J, Jacobsen S. An Equine Protein Atlas Highlights Synovial Fluid Proteome Dynamics during Experimentally LPS-Induced Arthritis. J Proteome Res 2024 Nov 1;23(11):4849-4863.
    doi: 10.1021/acs.jproteome.4c00125pubmed: 39395021google scholar: lookup
  17. Dellar ER, Hill C, Carter DRF, Baena-Lopez LA. Oxidative stress-induced changes in the transcriptomic profile of extracellular vesicles. J Extracell Biol 2024 Apr;3(4):e150.
    doi: 10.1002/jex2.150pubmed: 38938847google scholar: lookup
  18. Andersen C, Walters M, Bundgaard L, Berg LC, Vonk LA, Lundgren-Åkerlund E, Henriksen BL, Lindegaard C, Skovgaard K, Jacobsen S. Intraarticular treatment with integrin α10β1-selected mesenchymal stem cells affects microRNA expression in experimental post-traumatic osteoarthritis in horses. Front Vet Sci 2024;11:1374681.
    doi: 10.3389/fvets.2024.1374681pubmed: 38596460google scholar: lookup
  19. Connard SS, Gaesser AM, Clarke EJ, Linardi RL, Even KM, Engiles JB, Koch DW, Peffers MJ, Ortved KF. Plasma and synovial fluid extracellular vesicles display altered microRNA profiles in horses with naturally occurring post-traumatic osteoarthritis: an exploratory study. J Am Vet Med Assoc 2024 Jun 1;262(S1):S83-S96.
    doi: 10.2460/javma.24.02.0102pubmed: 38593834google scholar: lookup
  20. Clarke E, Varela L, Jenkins RE, Lozano-Andrés E, Cywińska A, Przewozny M, van Weeren PR, van de Lest CHA, Peffers M, Wauben MHM. Proteome and phospholipidome interrelationship of synovial fluid-derived extracellular vesicles in equine osteoarthritis: An exploratory 'multi-omics' study to identify composite biomarkers. Biochem Biophys Rep 2024 Mar;37:101635.
    doi: 10.1016/j.bbrep.2023.101635pubmed: 38298208google scholar: lookup
  21. Velot É, Balmayor ER, Bertoni L, Chubinskaya S, Cicuttini F, de Girolamo L, Demoor M, Grigolo B, Jones E, Kon E, Lisignoli G, Murphy M, Noël D, Vinatier C, van Osch GJVM, Cucchiarini M. Women's contribution to stem cell research for osteoarthritis: an opinion paper. Front Cell Dev Biol 2023;11:1209047.
    doi: 10.3389/fcell.2023.1209047pubmed: 38174070google scholar: lookup
  22. Anderson JR, Johnson E, Jenkins R, Jacobsen S, Green D, Walters M, Bundgaard L, Hausmans BAC, van den Akker G, Welting TJM, Chabronova A, Kharaz YA, Clarke EJ, James V, Peffers MJ. Multi-Omic Temporal Landscape of Plasma and Synovial Fluid-Derived Extracellular Vesicles Using an Experimental Model of Equine Osteoarthritis. Int J Mol Sci 2023 Oct 4;24(19).
    doi: 10.3390/ijms241914888pubmed: 37834337google scholar: lookup
  23. Zhang H, Yang S, Zhu W, Niu T, Wang J, Yang M, Liu E, Wang J, Li S, Zhang H. Exosomal miR-let-7c-5p is involved in the cognitive function of type 2 diabetes mellitus patients by interleukin 10: A cross-sectional study. J Diabetes 2023 Nov;15(11):978-986.
    doi: 10.1111/1753-0407.13450pubmed: 37532673google scholar: lookup