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Home / Equine Research Bank / Vet Rec Open / The anti-inflammatory effects of equine bone marrow stem cel...
Veterinary record open2021; 8(1); e22; doi: 10.1002/vro2.22

The anti-inflammatory effects of equine bone marrow stem cell-derived extracellular vesicles on autologous chondrocytes.

Abstract: Osteoarthritis (OA) in the horse is an economic and welfare issue and there are no current disease modifying drugs available. Stem cells have been suggested as a therapeutic intervention for OA, originally on the basis of their regenerative capacity. However, it is hypothesised that mesenchymal stem cells (MSC) exert their effects via paracrine factors including the production of extracellular vesicles that can themselves recapitulate the MSC effects in the joint. Objective: To isolate extracellular vesicles from bone marrow MSC and investigate their anti-inflammatory effects on chondrocytes. Methods: An in vitro assessment of the effect of direct culturing extracellular vesicles on artificially inflamed chondrocytes. Methods: Extracellular vesicles were isolated from bone marrow MSC using differential sequential ultracentrifugation. Vesicles were characterised using electron microscopy, nanoparticle tracing analysis and protein analysis. Vesicle internalisation was carried out via vesicles being pre-stained and co-cultured with equine chondrocytes before analysis using confocal microscopy. The effects of vesicles on artificially inflamed chondrocytes was examined using quantitative PCR. Results: To the best of the authors' knowledge, this is the first study to isolate and characterise extracellular vesicles from equine bone MSC. Vesicles were taken up by autologous chondrocytes and had anti-inflammatory effects on gene expression following chondrocyte exposure to tumour necrosis factor α and Interleukin 1β. Conclusions: Only three independent biological repeats were performed and the work was done in vitro. Conclusions: Extracellular vesicles can be isolated from equine bone marrow MSC; they may be taken up by chondrocytes and have an anti-inflammatory action.
© 2021 The Authors. Veterinary Record Open published by John Wiley & Sons Ltd on behalf of British Veterinary Association.
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Publication Date: 2021-11-10 PubMed ID: 34795904PubMed Central: PMC8580791DOI: 10.1002/vro2.22Google Scholar: Lookup
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  • 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 study investigates the anti-inflammatory effects of stem cell-derived extracellular vesicles on horse cells in an attempt to find a therapeutic intervention for horse osteoarthritis, a costly and welfare-impacting condition.

Objective of the Research

  • The main objective of this research was to isolate extracellular vesicles from mesenchymal stem cells (MSC) found in bone marrow and observe their potential anti-inflammatory effects on chondrocytes, cells found within joints. The researchers wanted to explore the therapeutic possibilities of these vesicles in mitigating the effects of osteoarthritis (OA) in horses.

Methodology

  • The study began with the extraction of extracellular vesicles from bone marrow MSC via a method known as differential sequential ultracentrifugation.
  • These vesicles were then characterised using different tools such as electron microscopy, nanoparticle tracing analysis, and protein analysis.
  • The researchers went on to introduce these pre-stained vesicles to equine chondrocytes to observe any potential internalisation. This process was visualised and analysed using confocal microscopy.
  • Finally, the impact of these vesicles on artificially inflamed chondrocytes was examined using a procedure called quantitative PCR. This procedure allows researchers to quantify the effects of the vesicles on inflammation markers in the cells.

Results

  • This study, to the best of the researcher’s knowledge, is the first of its kind to isolate and characterise these extracellular vesicles derived from equine bone MSC.
  • Observations suggested that these vesicles were absorbed by autologous chondrocytes (chondrocytes from the same organism) effectively, and showed an anti-inflammatory impact. This result was derived from monitoring changes in gene expression after cells were exposed to inflammation-causing agents, specifically tumour necrosis factor α and Interleukin 1β.

Conclusion

  • The research concluded that extracellular vesicles can indeed be isolated from equine bone marrow-derived mesenchymal stem cells.
  • These vesicles, when introduced to chondrocytes, seemed to have an anti-inflammatory action, indicating a potential therapeutic use for osteoarthritis in horses.
  • However, these results stem from only three independent biological repeats and were conducted entirely in vitro. Hence, additional in vivo studies using a larger sample size are advised for conclusive evidence.

Cite This Article

APA
Hotham WE, Thompson C, Szu-Ting L, Henson FMD. (2021). The anti-inflammatory effects of equine bone marrow stem cell-derived extracellular vesicles on autologous chondrocytes. Vet Rec Open, 8(1), e22. https://doi.org/10.1002/vro2.22

Publication

Veterinary record open
ISSN: 2052-6113
NlmUniqueID: 101653671
Country: United States
Language: English
Volume: 8
Issue: 1
Pages: e22
PII: e22

Researcher Affiliations

Hotham, William Edward
  • Division of Trauma and Orthopaedic Surgery University of Cambridge Cambridge Cambridgeshire UK.
Thompson, Charlotte
  • Cambridge Veterinary School Cambridge Cambridgeshire UK.
Szu-Ting, Lin
  • Cambridge Veterinary School Cambridge Cambridgeshire UK.
Henson, Frances Margaret Daphne
  • Division of Trauma and Orthopaedic Surgery University of Cambridge Cambridge Cambridgeshire UK.

References

This article includes 40 references
  1. Caplan AI. Mesenchymal Stem Cells: Time to Change the Name!. Stem Cells Transl Med 2017 Jun;6(6):1445-1451.
    doi: 10.1002/sctm.17-0051pmc: PMC5689741pubmed: 28452204google scholar: lookup
  2. Smith RK, Werling NJ, Dakin SG, Alam R, Goodship AE, Dudhia J. Beneficial effects of autologous bone marrow-derived mesenchymal stem cells in naturally occurring tendinopathy.. PLoS One 2013;8(9):e75697.
    pmc: PMC3783421pubmed: 24086616doi: 10.1371/journal.pone.0075697google scholar: lookup
  3. Godwin EE, Young NJ, Dudhia J, Beamish IC, Smith RK. Implantation of bone marrow-derived mesenchymal stem cells demonstrates improved outcome in horses with overstrain injury of the superficial digital flexor tendon.. Equine Vet J 2012 Jan;44(1):25-32.
    pubmed: 21615465doi: 10.1111/j.2042-3306.2011.00363.xgoogle scholar: lookup
  4. Broeckx SY, Seys B, Suls M, Vandenberghe A, Mariën T, Adriaensen E, Declercq J, Van Hecke L, Braun G, Hellmann K, Spaas JH. Equine Allogeneic Chondrogenic Induced Mesenchymal Stem Cells Are an Effective Treatment for Degenerative Joint Disease in Horses.. Stem Cells Dev 2019 Mar 15;28(6):410-422.
    pmc: PMC6441287pubmed: 30623737doi: 10.1089/scd.2018.0061google scholar: lookup
  5. McIlwraith CW. Traumatic arthritis and Posttraumatic Osteoarthritis in the Horse. In: McIlwraith CW, Frisbie DD, Kawcak EC, Weeren VR. Joint disease in the horse, 2nd edition. St Louis, MO, USA: Elsevier, 2016, pp 33–48.
  6. Bertoni L, Branly T, Jacquet S, Desancé M, Desquilbet L, Rivory P, Hartmann DJ, Denoix JM, Audigié F, Galéra P, Demoor M. Intra-Articular Injection of 2 Different Dosages of Autologous and Allogeneic Bone Marrow- and Umbilical Cord-Derived Mesenchymal Stem Cells Triggers a Variable Inflammatory Response of the Fetlock Joint on 12 Sound Experimental Horses.. Stem Cells Int 2019;2019:9431894.
    pmc: PMC6525957pubmed: 31191689doi: 10.1155/2019/9431894google scholar: lookup
  7. Drela K, Stanaszek L, Nowakowski A, Kuczynska Z, Lukomska B. Experimental Strategies of Mesenchymal Stem Cell Propagation: Adverse Events and Potential Risk of Functional Changes.. Stem Cells Int 2019;2019:7012692.
    pmc: PMC6431404pubmed: 30956673doi: 10.1155/2019/7012692google scholar: lookup
  8. Jifcovici A, Solano MA, Fitzpatrick N, Findji L, Blunn G, Sanghani-Kerai A. Comparison of Fat Harvested from Flank and Falciform Regions for Stem Cell Therapy in Dogs.. Vet Sci 2021 Jan 25;8(2).
    pmc: PMC7910945pubmed: 33503997doi: 10.3390/vetsci8020019google scholar: lookup
  9. Lim P, Patel SA, Rameshwar P. Effective tissue repair and immunomodulation by mesenchymal stem cells within a milieu of cytokines. In: Gorodetsky R, Schäfer R, editors. Stem cell‐based tissue repair. Cambridge, UK, Royal Society of Chemistry; 2011. p. 346–365.
  10. Baglio SR, Pegtel DM, Baldini N. Mesenchymal stem cell secreted vesicles provide novel opportunities in (stem) cell-free therapy.. Front Physiol 2012;3:359.
    pmc: PMC3434369pubmed: 22973239doi: 10.3389/fphys.2012.00359google scholar: lookup
  11. 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.
    pmc: PMC6322352pubmed: 30637094doi: 10.1080/20013078.2018.1535750google scholar: lookup
  12. da Silva Meirelles L, Sand TT, Harman RJ, Lennon DP, Caplan AI. MSC frequency correlates with blood vessel density in equine adipose tissue.. Tissue Eng Part A 2009 Feb;15(2):221-9.
    pmc: PMC2810211pubmed: 18847356doi: 10.1089/ten.tea.2008.0103google scholar: lookup
  13. Lai RC, Arslan F, Lee MM, Sze NS, Choo A, Chen TS, Salto-Tellez M, Timmers L, Lee CN, El Oakley RM, Pasterkamp G, de Kleijn DP, Lim SK. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury.. Stem Cell Res 2010 May;4(3):214-22.
    pubmed: 20138817doi: 10.1016/j.scr.2009.12.003google scholar: lookup
  14. Rougerie P, Miskolci V, Cox D. Generation of membrane structures during phagocytosis and chemotaxis of macrophages: role and regulation of the actin cytoskeleton.. Immunol Rev 2013 Nov;256(1):222-39.
    pmc: PMC3806206pubmed: 24117824doi: 10.1111/imr.12118google scholar: lookup
  15. Hartjes TA, Mytnyk S, Jenster GW, van Steijn V, van Royen ME. Extracellular Vesicle Quantification and Characterization: Common Methods and Emerging Approaches.. Bioengineering (Basel) 2019 Jan 16;6(1).
    pmc: PMC6466085pubmed: 30654439doi: 10.3390/bioengineering6010007google scholar: lookup
  16. Lee Y, El Andaloussi S, Wood MJ. Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy.. Hum Mol Genet 2012 Oct 15;21(R1):R125-34.
    pubmed: 22872698doi: 10.1093/hmg/dds317google scholar: lookup
  17. Ge R, Tan E, Sharghi-Namini S, Asada HH. Exosomes in Cancer Microenvironment and Beyond: have we Overlooked these Extracellular Messengers?. Cancer Microenviron 2012 Dec;5(3):323-32.
    pmc: PMC3460057pubmed: 22585423doi: 10.1007/s12307-012-0110-2google scholar: lookup
  18. Mulcahy LA, Pink RC, Carter DR. Routes and mechanisms of extracellular vesicle uptake.. J Extracell Vesicles 2014;3.
    pmc: PMC4122821pubmed: 25143819doi: 10.3402/jev.v3.24641google scholar: lookup
  19. 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.
    pmc: PMC3142546pubmed: 21560073doi: 10.1007/s00018-011-0689-3google scholar: lookup
  20. Uder C, Brückner S, Winkler S, Tautenhahn HM, Christ B. Mammalian MSC from selected species: Features and applications.. Cytometry A 2018 Jan;93(1):32-49.
    pubmed: 28906582doi: 10.1002/cyto.a.23239google scholar: lookup
  21. Cosenza S, Ruiz M, Toupet K, Jorgensen C, Noël D. Mesenchymal stem cells derived exosomes and microparticles protect cartilage and bone from degradation in osteoarthritis.. Sci Rep 2017 Nov 24;7(1):16214.
    pmc: PMC5701135pubmed: 29176667doi: 10.1038/s41598-017-15376-8google scholar: lookup
  22. Carpenter RS, Goodrich LR, Frisbie DD, Kisiday JD, Carbone B, McIlwraith CW, Centeno CJ, Hidaka C. Osteoblastic differentiation of human and equine adult bone marrow-derived mesenchymal stem cells when BMP-2 or BMP-7 homodimer genetic modification is compared to BMP-2/7 heterodimer genetic modification in the presence and absence of dexamethasone.. J Orthop Res 2010 Oct;28(10):1330-7.
    pmc: PMC3200399pubmed: 20309952doi: 10.1002/jor.21126google scholar: lookup
  23. Lombana KG, Goodrich LR, Phillips JN, Kisiday JD, Ruple-Czerniak A, McIlwraith CW. An Investigation of Equine Mesenchymal Stem Cell Characteristics from Different Harvest Sites: More Similar Than Not.. Front Vet Sci 2015;2:67.
    pmc: PMC4672231pubmed: 26664993doi: 10.3389/fvets.2015.00067google scholar: lookup
  24. Subedi P, Schneider M, Philipp J, Azimzadeh O, Metzger F, Moertl S, Atkinson MJ, Tapio S. Comparison of methods to isolate proteins from extracellular vesicles for mass spectrometry-based proteomic analyses.. Anal Biochem 2019 Nov 1;584:113390.
    pubmed: 31401005doi: 10.1016/j.ab.2019.113390google scholar: lookup
  25. 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.
    pubmed: 26914245doi: 10.1089/scd.2015.0348google scholar: lookup
  26. 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.
    pubmed: 25418078doi: 10.14670/hh-30.549google scholar: lookup
  27. 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.
    pubmed: 25241947doi: 10.1016/j.tvjl.2014.08.021google scholar: lookup
  28. Klymiuk MC, Balz N, Elashry MI, Heimann M, Wenisch S, Arnhold S. Exosomes isolation and identification from equine mesenchymal stem cells.. BMC Vet Res 2019 Jan 28;15(1):42.
    pmc: PMC6348641pubmed: 30691449doi: 10.1186/s12917-019-1789-9google scholar: lookup
  29. Capomaccio S, Cappelli K, Bazzucchi C, Coletti M, Gialletti R, Moriconi F, Passamonti F, Pepe M, Petrini S, Mecocci S, Silvestrelli M, Pascucci L. Equine Adipose-Derived Mesenchymal Stromal Cells Release Extracellular Vesicles Enclosing Different Subsets of Small RNAs.. Stem Cells Int 2019;2019:4957806.
    pmc: PMC6442443pubmed: 31011332doi: 10.1155/2019/4957806google scholar: lookup
  30. 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.
    pmc: PMC5114748pubmed: 27863532doi: 10.1186/s13287-016-0429-6google scholar: lookup
  31. Dabrowska S, Del Fattore A, Karnas E, Frontczak-Baniewicz M, Kozlowska H, Muraca M, Janowski M, Lukomska B. Imaging of extracellular vesicles derived from human bone marrow mesenchymal stem cells using fluorescent and magnetic labels.. Int J Nanomedicine 2018;13:1653-1664.
    pmc: PMC5865569pubmed: 29593411doi: 10.2147/ijn.s159404google scholar: lookup
  32. Rajendran RL, Gangadaran P, Bak SS, Oh JM, Kalimuthu S, Lee HW, Baek SH, Zhu L, Sung YK, Jeong SY, Lee SW, Lee J, Ahn BC. Extracellular vesicles derived from MSCs activates dermal papilla cell in vitro and promotes hair follicle conversion from telogen to anagen in mice.. Sci Rep 2017 Nov 14;7(1):15560.
    pmc: PMC5686117pubmed: 29138430doi: 10.1038/s41598-017-15505-3google scholar: lookup
  33. Haga H, Yan IK, Takahashi K, Matsuda A, Patel T. Extracellular Vesicles from Bone Marrow-Derived Mesenchymal Stem Cells Improve Survival from Lethal Hepatic Failure in Mice.. Stem Cells Transl Med 2017 Apr;6(4):1262-1272.
    pmc: PMC5442843pubmed: 28213967doi: 10.1002/sctm.16-0226google scholar: lookup
  34. Wen S, Dooner M, Papa E, Del Tatto M, Pereira M, Borgovan T, Cheng Y, Goldberg L, Liang O, Camussi G, Quesenberry P. Biodistribution of Mesenchymal Stem Cell-Derived Extracellular Vesicles in a Radiation Injury Bone Marrow Murine Model.. Int J Mol Sci 2019 Nov 2;20(21).
    pmc: PMC6861905pubmed: 31684046doi: 10.3390/ijms20215468google scholar: lookup
  35. Vonk LA, van Dooremalen SFJ, Liv N, Klumperman J, Coffer PJ, Saris DBF, Lorenowicz MJ. Mesenchymal Stromal/stem Cell-derived Extracellular Vesicles Promote Human Cartilage Regeneration In Vitro.. Theranostics 2018;8(4):906-920.
    pmc: PMC5817101pubmed: 29463990doi: 10.7150/thno.20746google scholar: lookup
  36. Richardson DW, Dodge GR. Effects of interleukin-1beta and tumor necrosis factor-alpha on expression of matrix-related genes by cultured equine articular chondrocytes.. Am J Vet Res 2000 Jun;61(6):624-30.
    pubmed: 10850836doi: 10.2460/ajvr.2000.61.624google scholar: lookup
  37. Caron JP, Gandy JC, Schmidt M, Hauptman JG, Sordillo LM. Influence of corticosteroids on interleukin-1β-stimulated equine chondrocyte gene expression.. Vet Surg 2013 Apr;42(3):231-7.
    pubmed: 23278565doi: 10.1111/j.1532-950x.2012.01025.xgoogle scholar: lookup
  38. Barrachina L, Remacha AR, Romero A, Vitoria A, Albareda J, Prades M, Roca M, Zaragoza P, Vázquez FJ, Rodellar C. Assessment of effectiveness and safety of repeat administration of proinflammatory primed allogeneic mesenchymal stem cells in an equine model of chemically induced osteoarthritis.. BMC Vet Res 2018 Aug 17;14(1):241.
    pmc: PMC6098603pubmed: 30119668doi: 10.1186/s12917-018-1556-3google scholar: lookup
  39. Broeckx S, Suls M, Beerts C, Vandenberghe A, Seys B, Wuertz-Kozak K, Duchateau L, Spaas JH. Allogenic mesenchymal stem cells as a treatment for equine degenerative joint disease: a pilot study.. Curr Stem Cell Res Ther 2014;9(6):497-503.
    pubmed: 25175766doi: 10.2174/1574888x09666140826110601google scholar: lookup
  40. Boere J, Malda J, van de Lest CHA, van Weeren PR, Wauben MHM. Extracellular Vesicles in Joint Disease and Therapy.. Front Immunol 2018;9:2575.
    pmc: PMC6240615pubmed: 30483255doi: 10.3389/fimmu.2018.02575google scholar: lookup

Citations

This article has been cited 22 times.
  1. Ossendorff R, Grad S, Tertel T, Wirtz DC, Giebel B, Börger V, Schildberg FA. Immunomodulatory potential of mesenchymal stromal cell-derived extracellular vesicles in chondrocyte inflammation. Front Immunol 2023;14:1198198.
    doi: 10.3389/fimmu.2023.1198198pubmed: 37564645google scholar: lookup
  2. Mustonen AM, Lehmonen N, Paakkonen T, Raekallio M, Käkelä R, Niemelä T, Mykkänen A, Sihvo SP, Nieminen P. Equine osteoarthritis modifies fatty acid signatures in synovial fluid and its extracellular vesicles. Arthritis Res Ther 2023 Mar 9;25(1):39.
    doi: 10.1186/s13075-023-02998-9pubmed: 36895037google scholar: lookup
  3. 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
  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. Höglund N, Koho N, Rossi H, Karttunen J, Mustonen AM, Nieminen P, Rilla K, Oikari S, Mykkänen A. Isolation of Extracellular Vesicles From the Bronchoalveolar Lavage Fluid of Healthy and Asthmatic Horses. Front Vet Sci 2022;9:894189.
    doi: 10.3389/fvets.2022.894189pubmed: 35799843google scholar: lookup
  7. Uberti B, Plaza A, Henríquez C. Pre-conditioning Strategies for Mesenchymal Stromal/Stem Cells in Inflammatory Conditions of Livestock Species. Front Vet Sci 2022;9:806069.
    doi: 10.3389/fvets.2022.806069pubmed: 35372550google scholar: lookup
  8. Beaumont RE, Flood C, Guest DJ. Inhibition of interleukin-1 receptor-associated kinase (IRAK)-4 provides partial rescue of interleukin-1 beta induced functional and gene expression changes in equine tenocytes. Mol Biol Rep 2025 Nov 6;53(1):54.
    doi: 10.1007/s11033-025-11219-2pubmed: 41196436google scholar: lookup
  9. Tarasova K, Arteaga MB, Kidtiwong A, Nivarthi H, Gamauf J, Corso G, Gültekin S, Bileck A, Rothbauer M, Toegel S, Hackl M, Kau-Strebinger S, Gerner C, Grillari R, Gerner I, Jenner F. Ontogenetic stage and type of donor cells shape extracellular vesicles' therapeutic potential for osteoarthritis. Stem Cell Res Ther 2025 Sep 1;16(1):478.
    doi: 10.1186/s13287-025-04585-ypubmed: 40890860google scholar: lookup
  10. Banu SA, Sharun K, Emmanuel RS, Mamachan M, Manjusha KM, Muthu S, El-Husseiny HM, Kumar R, Pawde AM, Dhama K, Amarpal. Stem Cell Exosomes for Osteoarthritis in Veterinary Medicine. Stem Cells Int 2025;2025:4888569.
    doi: 10.1155/sci/4888569pubmed: 40704321google scholar: lookup
  11. González-Rodríguez A, De Toro FJ, Jorge-Mora A, Fernandez-Pernas P, Rivadulla CP, Fraga M, Fafián-Labora JA, Arufe MC. Targeting osteoarthritis with small extracellular vesicle therapy: potential and perspectives. Front Bioeng Biotechnol 2025;13:1570526.
    doi: 10.3389/fbioe.2025.1570526pubmed: 40621210google scholar: lookup
  12. 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
  13. Reynolds DE, Vallapureddy P, Morales RT, Oh D, Pan M, Chintapula U, Linardi RL, Gaesser AM, Ortved K, Ko J. Equine mesenchymal stem cell derived extracellular vesicle immunopathology biomarker discovery. J Extracell Biol 2023 Jun;2(6):e89.
    doi: 10.1002/jex2.89pubmed: 38938916google scholar: lookup
  14. Quam VG, Belacic ZA, Long S, Rice HC, Dhar MS, Durgam S. Equine bone marrow MSC-derived extracellular vesicles mitigate the inflammatory effects of interleukin-1β on navicular tissues in vitro. Equine Vet J 2025 Jan;57(1):232-242.
    doi: 10.1111/evj.14090pubmed: 38587145google scholar: lookup
  15. Gaesser AM, Usimaki AIJ, Barot DA, Linardi RL, Molugu S, Musante L, Ortved KF. Equine mesenchymal stem cell-derived extracellular vesicle productivity but not overall yield is improved via 3-D culture with chemically defined media. J Am Vet Med Assoc 2024 Jun 1;262(S1):S97-S108.
    doi: 10.2460/javma.24.01.0001pubmed: 38547591google scholar: lookup
  16. Ivanova Z, Petrova V, Grigorova N, Vachkova E. Identification of the Reference Genes for Relative qRT-PCR Assay in Two Experimental Models of Rabbit and Horse Subcutaneous ASCs. Int J Mol Sci 2024 Feb 14;25(4).
    doi: 10.3390/ijms25042292pubmed: 38396967google scholar: lookup
  17. 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
  18. Roberts EL, Abraham BD, Dang T, Gysel E, Mehrpouyan S, Alizadeh AH, Koch TG, Kallos MS. Computer controlled expansion of equine cord blood mesenchymal stromal cells on microcarriers in 3 L vertical-wheel(®) bioreactors. Front Bioeng Biotechnol 2023;11:1250077.
    doi: 10.3389/fbioe.2023.1250077pubmed: 37929186google scholar: lookup
  19. 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
  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. Tamura N, Heidari N, Faragher RGA, Smith RKW, Dudhia J. Effects of resveratrol and its analogues on the cell cycle of equine mesenchymal stem/stromal cells. J Equine Sci 2023 Sep;34(3):67-72.
    doi: 10.1294/jes.34.67pubmed: 37781569google scholar: lookup
  22. Koprivec S, Majdič G. Extracellular Vesicles in Domestic Animals: Cellular Communication in Health and Disease. Adv Exp Med Biol 2024;1450:39-57.
    doi: 10.1007/5584_2023_779pubmed: 37421538google scholar: lookup
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