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Home / Equine Research Bank / Int J Mol Sci / Effects of Normal Synovial Fluid and Interferon Gamma on Cho...
International journal of molecular sciences2021; 22(12); 6391; doi: 10.3390/ijms22126391

Effects of Normal Synovial Fluid and Interferon Gamma on Chondrogenic Capability and Immunomodulatory Potential Respectively on Equine Mesenchymal Stem Cells.

Abstract: Synovial fluid contains cytokines, growth factors and resident mesenchymal stem cells (MSCs). The present study aimed to (1) determine the effects of autologous and allogeneic synovial fluid on viability, proliferation and chondrogenesis of equine bone marrow MSCs (BMMSCs) and (2) compare the immunomodulatory properties of equine synovial fluid MSCs (SFMSCs) and BMMSCs after stimulation with interferon gamma (INF-γ). To meet the first aim of the study, the proliferation and viability of MSCs were evaluated by MTS and calcein AM staining assays. To induce chondrogenesis, MSCs were cultured in a medium containing TGF-β1 or different concentrations of synovial fluid. To meet the second aim, SFMSCs and BMMSCs were stimulated with IFN-γ. The concentration of indoleamine-2,3-dioxygenase (IDO) and nitric oxide (NO) were examined. Our results show that MSCs cultured in autologous or allogeneic synovial fluid could maintain proliferation and viability activities. Synovial fluid affected chondrocyte differentiation significantly, as indicated by increased glycosaminoglycan contents, compared to the chondrogenic medium containing 5 ng/mL TGF-β1. After culturing with IFN-γ, the conditioned media of both BMMSCs and SFMSCs showed increased concentrations of IDO, but not NO. Stimulating MSCs with synovial fluid or IFN-γ could enhance chondrogenesis and anti-inflammatory activity, respectively, suggesting that the joint environment is suitable for chondrogenesis.
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Publication Date: 2021-06-15 PubMed ID: 34203758PubMed Central: PMC8232615DOI: 10.3390/ijms22126391Google 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 examines the impacts of synovial fluid and Interferon Gamma (INF-γ) on the chondrogenic capability and immunomodulatory potential of horse bone marrow mesenchymal stem cells. The findings show that the stem cells, when cultured in synovial fluid or stimulated with INF-γ, displayed improved chondrogenesis and anti-inflammatory activity respectively.

Objective and Methodology

  • The purpose of the research was two-fold. First, to investigate the impact of autologous (taken from the same individual) and allogeneic (taken from a different individual) synovial fluid on the resilience, multiplication, and chondrogenesis (development into cartilage cells) of horse bone marrow stem cells. Second, to compare the immunomodulatory characteristics of synovial fluid stem cells and bone marrow stem cells when stimulated with INF-γ.
  • The scientists executed the first part of the study by evaluating the stem cells’ proliferation and viability through MTS and calcein AM staining assays. To provoke chondrogenesis, the cells were cultured in a medium containing Transforming Growth Factor Beta 1 (TGF-β1) or varying concentrations of synovial fluid.
  • For the second part of the study, synovial fluid stem cells and bone marrow stem cells were stimulated with INF-γ. Then the concentration of indoleamine-2,3-dioxygenase (IDO) and nitric oxide (NO) in the cells was measured.

Key Findings

  • Results showed that stem cells cultured in autologous or allogeneic synovial fluid could maintain proliferation and viability activities. Interestingly, synovial fluid significantly affected chondrocyte differentiation, which was indicated by an increase in glycosaminoglycan contents, compared to the chondrogenic medium containing 5 ng/mL TGF-β1.
  • It was also found that after the cells were stimulated with INF-γ, both the bone marrow stem cells and the synovial fluid stem cells demonstrated an increase in the concentration of IDO, but not NO. This suggests that stimulation with INF-γ enhances the stem cells’ anti-inflammatory activity.
  • The research concludes that stimulation with either synovial fluid or INF-γ could heighten chondrogenesis and anti-inflammatory activity respectively, which alludes to the fact that the joint environment is potentially suitable for chondrogenesis.

Cite This Article

APA
Zayed M, Adair S, Dhar M. (2021). Effects of Normal Synovial Fluid and Interferon Gamma on Chondrogenic Capability and Immunomodulatory Potential Respectively on Equine Mesenchymal Stem Cells. Int J Mol Sci, 22(12), 6391. https://doi.org/10.3390/ijms22126391

Publication

International journal of molecular sciences
ISSN: 1422-0067
NlmUniqueID: 101092791
Country: Switzerland
Language: English
Volume: 22
Issue: 12
PII: 6391

Researcher Affiliations

Zayed, Mohammed
  • Department of Large Animal Clinical Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, TN 37996, USA.
  • Department of Surgery, College of Veterinary Medicine, South Valley University, Qena 83523, Egypt.
Adair, Steve
  • Department of Large Animal Clinical Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, TN 37996, USA.
Dhar, Madhu
  • Department of Large Animal Clinical Sciences, College of Veterinary Medicine, University of Tennessee, Knoxville, TN 37996, USA.

MeSH Terms

  • Animals
  • Bone Marrow Cells / cytology
  • Cell Differentiation / drug effects
  • Cell Proliferation / drug effects
  • Cell Shape / drug effects
  • Cell Survival / drug effects
  • Chondrogenesis / drug effects
  • Colony-Forming Units Assay
  • Horses
  • Immunomodulation / drug effects
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / metabolism
  • Interferon-gamma / pharmacology
  • Mesenchymal Stem Cells / cytology
  • Mesenchymal Stem Cells / drug effects
  • Mesenchymal Stem Cells / enzymology
  • Mesenchymal Stem Cells / immunology
  • Nitric Oxide / metabolism
  • Synovial Fluid / metabolism

Grant Funding

  • Grant number R181710145 / Center of Excellence in Livestock Diseases and Human Health, University of Tennessee

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 56 references
  1. Camarero-Espinosa S, Rothen-Rutishauser B, Foster EJ, Weder C. Articular cartilage: from formation to tissue engineering.. Biomater Sci 2016 May 26;4(5):734-67.
    doi: 10.1039/C6BM00068Apubmed: 26923076google scholar: lookup
  2. Nöth U, Steinert AF, Tuan RS. Technology insight: adult mesenchymal stem cells for osteoarthritis therapy.. Nat Clin Pract Rheumatol 2008 Jul;4(7):371-80.
    doi: 10.1038/ncprheum0816pubmed: 18477997google scholar: lookup
  3. Nouri Barkestani M, Naserian S, Uzan G, Shamdani S. Post-decellularization techniques ameliorate cartilage decellularization process for tissue engineering applications.. J Tissue Eng 2021 Jan-Dec;12:2041731420983562.
    doi: 10.1177/2041731420983562pmc: PMC7934046pubmed: 33738088google scholar: lookup
  4. Kalamegam G, Memic A, Budd E, Abbas M, Mobasheri A. A Comprehensive Review of Stem Cells for Cartilage Regeneration in Osteoarthritis.. Adv Exp Med Biol 2018;1089:23-36.
    doi: 10.1007/5584_2018_205pubmed: 29725971google scholar: lookup
  5. Nam Y, Rim YA, Lee J, Ju JH. Current Therapeutic Strategies for Stem Cell-Based Cartilage Regeneration.. Stem Cells Int 2018;2018:8490489.
    doi: 10.1155/2018/8490489pmc: PMC5889878pubmed: 29765426google scholar: lookup
  6. Buckwalter JA. Articular cartilage injuries.. Clin Orthop Relat Res 2002 Sep;(402):21-37.
    doi: 10.1097/00003086-200209000-00004pubmed: 12218470google scholar: lookup
  7. Cokelaere S, Malda J, van Weeren R. Cartilage defect repair in horses: Current strategies and recent developments in regenerative medicine of the equine joint with emphasis on the surgical approach.. Vet J 2016 Aug;214:61-71.
    doi: 10.1016/j.tvjl.2016.02.005pubmed: 27387728google scholar: lookup
  8. Ude CC, Sulaiman SB, Min-Hwei N, Hui-Cheng C, Ahmad J, Yahaya NM, Saim AB, Idrus RB. Cartilage regeneration by chondrogenic induced adult stem cells in osteoarthritic sheep model.. PLoS One 2014;9(6):e98770.
    doi: 10.1371/journal.pone.0098770pmc: PMC4049590pubmed: 24911365google scholar: lookup
  9. Broeckx SY, Martens AM, Bertone AL, Van Brantegem L, Duchateau L, Van Hecke L, Dumoulin M, Oosterlinck M, Chiers K, Hussein H, Pille F, Spaas JH. The use of equine chondrogenic-induced mesenchymal stem cells as a treatment for osteoarthritis: A randomised, double-blinded, placebo-controlled proof-of-concept study.. Equine Vet J 2019 Nov;51(6):787-794.
    doi: 10.1111/evj.13089pmc: PMC6850029pubmed: 30815897google scholar: lookup
  10. 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.
    doi: 10.1089/scd.2018.0061pmc: PMC6441287pubmed: 30623737google scholar: lookup
  11. Kafienah W, Mistry S, Dickinson SC, Sims TJ, Learmonth I, Hollander AP. Three-dimensional cartilage tissue engineering using adult stem cells from osteoarthritis patients.. Arthritis Rheum 2007 Jan;56(1):177-87.
    doi: 10.1002/art.22285pubmed: 17195220google scholar: lookup
  12. Steinert AF, Ghivizzani SC, Rethwilm A, Tuan RS, Evans CH, Nöth U. Major biological obstacles for persistent cell-based regeneration of articular cartilage.. Arthritis Res Ther 2007;9(3):213.
    doi: 10.1186/ar2195pmc: PMC2206353pubmed: 17561986google scholar: lookup
  13. Okazaki R, Sakai A, Uezono Y, Ootsuyama A, Kunugita N, Nakamura T, Norimura T. Sequential changes in transforming growth factor (TGF)-beta1 concentration in synovial fluid and mRNA expression of TGF-beta1 receptors in chondrocytes after immobilization of rabbit knees.. J Bone Miner Metab 2001;19(4):228-35.
    doi: 10.1007/s007740170025pubmed: 11448015google scholar: lookup
  14. Chen J, Wang C, Lü S, Wu J, Guo X, Duan C, Dong L, Song Y, Zhang J, Jing D, Wu L, Ding J, Li D. In vivo chondrogenesis of adult bone-marrow-derived autologous mesenchymal stem cells.. Cell Tissue Res 2005 Mar;319(3):429-38.
    doi: 10.1007/s00441-004-1025-0pubmed: 15672263google scholar: lookup
  15. Rodrigo JJ, Steadman JR, Syftestad G, Benton H, Silliman J. Effects of human knee synovial fluid on chondrogenesis in vitro.. Am J Knee Surg 1995 Fall;8(4):124-9.
    pubmed: 8590122
  16. Yang KG, Saris DB, Verbout AJ, Creemers LB, Dhert WJ. The effect of synovial fluid from injured knee joints on in vitro chondrogenesis.. Tissue Eng 2006 Oct;12(10):2957-64.
    doi: 10.1089/ten.2006.12.2957pubmed: 17518663google scholar: lookup
  17. Colbath AC, Dow SW, Hopkins LS, Phillips JN, McIlwraith CW, Goodrich LR. Allogeneic vs. autologous intra-articular mesenchymal stem cell injection within normal horses: Clinical and cytological comparisons suggest safety.. Equine Vet J 2020 Jan;52(1):144-151.
    doi: 10.1111/evj.13136pubmed: 31120574google scholar: lookup
  18. Colbath AC, Dow SW, Phillips JN, McIlwraith CW, Goodrich LR. Autologous and Allogeneic Equine Mesenchymal Stem Cells Exhibit Equivalent Immunomodulatory Properties In Vitro.. Stem Cells Dev 2017 Apr 1;26(7):503-511.
    doi: 10.1089/scd.2016.0266pubmed: 27958776google scholar: lookup
  19. Colbath AC, Dow SW, McIlwraith CW, Goodrich LR. Mesenchymal stem cells for treatment of musculoskeletal disease in horses: Relative merits of allogeneic versus autologous stem cells.. Equine Vet J 2020 Sep;52(5):654-663.
    doi: 10.1111/evj.13233pubmed: 31971273google scholar: lookup
  20. Zayed M, Caniglia C, Misk N, Dhar MS. Donor-Matched Comparison of Chondrogenic Potential of Equine Bone Marrow- and Synovial Fluid-Derived Mesenchymal Stem Cells: Implications for Cartilage Tissue Regeneration.. Front Vet Sci 2016;3:121.
    doi: 10.3389/fvets.2016.00121pmc: PMC5241318pubmed: 28149840google scholar: lookup
  21. Murata D, Miyakoshi D, Hatazoe T, Miura N, Tokunaga S, Fujiki M, Nakayama K, Misumi K. Multipotency of equine mesenchymal stem cells derived from synovial fluid.. Vet J 2014 Oct;202(1):53-61.
    doi: 10.1016/j.tvjl.2014.07.029pubmed: 25151209google scholar: lookup
  22. Prado AA, Favaron PO, da Silva LC, Baccarin RY, Miglino MA, Maria DA. Characterization of mesenchymal stem cells derived from the equine synovial fluid and membrane.. BMC Vet Res 2015 Nov 10;11:281.
    doi: 10.1186/s12917-015-0531-5pmc: PMC4640348pubmed: 26555093google scholar: lookup
  23. Bernardo ME, Fibbe WE. Mesenchymal stromal cells: sensors and switchers of inflammation.. Cell Stem Cell 2013 Oct 3;13(4):392-402.
    doi: 10.1016/j.stem.2013.09.006pubmed: 24094322google scholar: lookup
  24. Krampera M, Cosmi L, Angeli R, Pasini A, Liotta F, Andreini A, Santarlasci V, Mazzinghi B, Pizzolo G, Vinante F, Romagnani P, Maggi E, Romagnani S, Annunziato F. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells.. Stem Cells 2006 Feb;24(2):386-98.
    doi: 10.1634/stemcells.2005-0008pubmed: 16123384google scholar: lookup
  25. Szabó E, Fajka-Boja R, Kriston-Pál É, Hornung Á, Makra I, Kudlik G, Uher F, Katona RL, Monostori É, Czibula Á. Licensing by Inflammatory Cytokines Abolishes Heterogeneity of Immunosuppressive Function of Mesenchymal Stem Cell Population.. Stem Cells Dev 2015 Sep 15;24(18):2171-80.
    doi: 10.1089/scd.2014.0581pubmed: 26153898google scholar: lookup
  26. Alsaleh G, Sparsa L, Chatelus E, Ehlinger M, Gottenberg JE, Wachsmann D, Sibilia J. Innate immunity triggers IL-32 expression by fibroblast-like synoviocytes in rheumatoid arthritis.. Arthritis Res Ther 2010;12(4):R135.
    doi: 10.1186/ar3073pmc: PMC2945025pubmed: 20615213google scholar: lookup
  27. Li YS, Luo W, Zhu SA, Lei GH. T Cells in Osteoarthritis: Alterations and Beyond.. Front Immunol 2017;8:356.
    doi: 10.3389/fimmu.2017.00356pmc: PMC5371609pubmed: 28424692google scholar: lookup
  28. Schroder K, Hertzog PJ, Ravasi T, Hume DA. Interferon-gamma: an overview of signals, mechanisms and functions.. J Leukoc Biol 2004 Feb;75(2):163-89.
    doi: 10.1189/jlb.0603252pubmed: 14525967google scholar: lookup
  29. Carrade DD, Borjesson DL. Immunomodulation by mesenchymal stem cells in veterinary species.. Comp Med 2013 Jun;63(3):207-17.
    pmc: PMC3690426pubmed: 23759523
  30. King NJ, Thomas SR. Molecules in focus: indoleamine 2,3-dioxygenase.. Int J Biochem Cell Biol 2007;39(12):2167-72.
    doi: 10.1016/j.biocel.2007.01.004pubmed: 17320464google scholar: lookup
  31. Carrade DD, Lame MW, Kent MS, Clark KC, Walker NJ, Borjesson DL. Comparative Analysis of the Immunomodulatory Properties of Equine Adult-Derived Mesenchymal Stem Cells().. Cell Med 2012;4(1):1-11.
    doi: 10.3727/215517912X647217pmc: PMC3495591pubmed: 23152950google scholar: lookup
  32. Zayed MN, Schumacher J, Misk N, Dhar MS. Effects of pro-inflammatory cytokines on chondrogenesis of equine mesenchymal stromal cells derived from bone marrow or synovial fluid.. Vet J 2016 Nov;217:26-32.
    doi: 10.1016/j.tvjl.2016.05.014pubmed: 27810206google scholar: lookup
  33. 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
  34. Zayed M, Adair S, Ursini T, Schumacher J, Misk N, Dhar M. Concepts and challenges in the use of mesenchymal stem cells as a treatment for cartilage damage in the horse.. Res Vet Sci 2018 Jun;118:317-323.
    doi: 10.1016/j.rvsc.2018.03.011pubmed: 29601969google scholar: lookup
  35. McIlwraith CW, Frisbie DD, Rodkey WG, Kisiday JD, Werpy NM, Kawcak CE, Steadman JR. Evaluation of intra-articular mesenchymal stem cells to augment healing of microfractured chondral defects.. Arthroscopy 2011 Nov;27(11):1552-61.
    doi: 10.1016/j.arthro.2011.06.002pubmed: 21862278google scholar: lookup
  36. Sayegh S, El Atat O, Diallo K, Rauwel B, Degboé Y, Cavaignac E, Constantin A, Cantagrel A, Trak-Smayra V, Alaaeddine N, Davignon JL. Rheumatoid Synovial Fluids Regulate the Immunomodulatory Potential of Adipose-Derived Mesenchymal Stem Cells Through a TNF/NF-κB-Dependent Mechanism.. Front Immunol 2019;10:1482.
    doi: 10.3389/fimmu.2019.01482pmc: PMC6611153pubmed: 31316519google scholar: lookup
  37. Mauck RL, Yuan X, Tuan RS. Chondrogenic differentiation and functional maturation of bovine mesenchymal stem cells in long-term agarose culture.. Osteoarthritis Cartilage 2006 Feb;14(2):179-89.
    doi: 10.1016/j.joca.2005.09.002pubmed: 16257243google scholar: lookup
  38. Pavelka K, Uebelhart D. Efficacy evaluation of highly purified intra-articular hyaluronic acid (Sinovial(®)) vs hylan G-F20 (Synvisc(®)) in the treatment of symptomatic knee osteoarthritis. A double-blind, controlled, randomized, parallel-group non-inferiority study.. Osteoarthritis Cartilage 2011 Nov;19(11):1294-300.
    doi: 10.1016/j.joca.2011.07.016pubmed: 21875678google scholar: lookup
  39. Kawasaki K, Ochi M, Uchio Y, Adachi N, Matsusaki M. Hyaluronic acid enhances proliferation and chondroitin sulfate synthesis in cultured chondrocytes embedded in collagen gels.. J Cell Physiol 1999 May;179(2):142-8.
    doi: 10.1002/(SICI)1097-4652(199905)179:2<142::AID-JCP4>3.0.CO;2-Qpubmed: 10199553google scholar: lookup
  40. Grishko V, Xu M, Ho R, Mates A, Watson S, Kim JT, Wilson GL, Pearsall AW 4th. Effects of hyaluronic acid on mitochondrial function and mitochondria-driven apoptosis following oxidative stress in human chondrocytes.. J Biol Chem 2009 Apr 3;284(14):9132-9.
    doi: 10.1074/jbc.M804178200pmc: PMC2666563pubmed: 19193642google scholar: lookup
  41. Hashizume M, Mihara M. High molecular weight hyaluronic acid inhibits IL-6-induced MMP production from human chondrocytes by up-regulating the ERK inhibitor, MKP-1.. Biochem Biophys Res Commun 2010 Dec 10;403(2):184-9.
    doi: 10.1016/j.bbrc.2010.10.135pubmed: 21059338google scholar: lookup
  42. Ogueta S, Muñoz J, Obregon E, Delgado-Baeza E, García-Ruiz JP. Prolactin is a component of the human synovial liquid and modulates the growth and chondrogenic differentiation of bone marrow-derived mesenchymal stem cells.. Mol Cell Endocrinol 2002 Apr 25;190(1-2):51-63.
    doi: 10.1016/S0303-7207(02)00013-8pubmed: 11997178google scholar: lookup
  43. Gupta RC, Lall R, Srivastava A, Sinha A. Hyaluronic Acid: Molecular Mechanisms and Therapeutic Trajectory.. Front Vet Sci 2019;6:192.
    doi: 10.3389/fvets.2019.00192pmc: PMC6603175pubmed: 31294035google scholar: lookup
  44. Álvarez V, Sánchez-Margallo FM, Blázquez R, Tarazona R, Casado JG. Comparison of mesenchymal stem cells and leukocytes from Large White and Göttingen Minipigs: Clues for stem cell-based immunomodulatory therapies.. Vet Immunol Immunopathol 2016 Oct 15;179:63-9.
    doi: 10.1016/j.vetimm.2016.08.002pubmed: 27590427google scholar: lookup
  45. MacDonald ES, Barrett JG. The Potential of Mesenchymal Stem Cells to Treat Systemic Inflammation in Horses.. Front Vet Sci 2019;6:507.
    doi: 10.3389/fvets.2019.00507pmc: PMC6985200pubmed: 32039250google scholar: lookup
  46. Zayed M, Newby S, Misk N, Donnell R, Dhar M. Xenogenic Implantation of Equine Synovial Fluid-Derived Mesenchymal Stem Cells Leads to Articular Cartilage Regeneration.. Stem Cells Int 2018;2018:1073705.
    doi: 10.1155/2018/1073705pmc: PMC6011062pubmed: 29977305google scholar: lookup
  47. Barrachina L, Remacha AR, Romero A, Vázquez FJ, Albareda J, Prades M, Gosálvez J, Roy R, Zaragoza P, Martín-Burriel I, Rodellar C. Priming Equine Bone Marrow-Derived Mesenchymal Stem Cells with Proinflammatory Cytokines: Implications in Immunomodulation-Immunogenicity Balance, Cell Viability, and Differentiation Potential.. Stem Cells Dev 2017 Jan 1;26(1):15-24.
    doi: 10.1089/scd.2016.0209pubmed: 27712399google scholar: lookup
  48. Gao F, Chiu SM, Motan DA, Zhang Z, Chen L, Ji HL, Tse HF, Fu QL, Lian Q. Mesenchymal stem cells and immunomodulation: current status and future prospects.. Cell Death Dis 2016 Jan 21;7(1):e2062.
    doi: 10.1038/cddis.2015.327pmc: PMC4816164pubmed: 26794657google scholar: lookup
  49. Mancheño-Corvo P, Menta R, del Río B, Franquesa M, Ramírez C, Hoogduijn MJ, DelaRosa O, Dalemans W, Lombardo E. T Lymphocyte Prestimulation Impairs in a Time-Dependent Manner the Capacity of Adipose Mesenchymal Stem Cells to Inhibit Proliferation: Role of Interferon γ, Poly I:C, and Tryptophan Metabolism in Restoring Adipose Mesenchymal Stem Cell Inhibitory Effect.. Stem Cells Dev 2015 Sep 15;24(18):2158-70.
    doi: 10.1089/scd.2014.0508pubmed: 26058889google scholar: lookup
  50. Sato K, Ozaki K, Oh I, Meguro A, Hatanaka K, Nagai T, Muroi K, Ozawa K. Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells.. Blood 2007 Jan 1;109(1):228-34.
    doi: 10.1182/blood-2006-02-002246pubmed: 16985180google scholar: lookup
  51. Han Z, Tian Z, Lv G, Zhang L, Jiang G, Sun K, Wang C, Bu X, Li R, Shi Y, Wu M, Wei L. Immunosuppressive effect of bone marrow-derived mesenchymal stem cells in inflammatory microenvironment favours the growth of B16 melanoma cells.. J Cell Mol Med 2011 Nov;15(11):2343-52.
    doi: 10.1111/j.1582-4934.2010.01215.xpmc: PMC3822946pubmed: 21091630google scholar: lookup
  52. Ren G, Zhang L, Zhao X, Xu G, Zhang Y, Roberts AI, Zhao RC, Shi Y. Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide.. Cell Stem Cell 2008 Feb 7;2(2):141-50.
    doi: 10.1016/j.stem.2007.11.014pubmed: 18371435google scholar: lookup
  53. Williams LB, Koenig JB, Black B, Gibson TW, Sharif S, Koch TG. Equine allogeneic umbilical cord blood derived mesenchymal stromal cells reduce synovial fluid nucleated cell count and induce mild self-limiting inflammation when evaluated in an lipopolysaccharide induced synovitis model.. Equine Vet J 2016 Sep;48(5):619-25.
    doi: 10.1111/evj.12477pubmed: 26114736google scholar: lookup
  54. Carter-Arnold JL, Neilsen NL, Amelse LL, Odoi A, Dhar MS. In vitro analysis of equine, bone marrow-derived mesenchymal stem cells demonstrates differences within age- and gender-matched horses.. Equine Vet J 2014 Sep;46(5):589-95.
    doi: 10.1111/evj.12142pubmed: 23855680google scholar: lookup
  55. Schnabel LV, Pezzanite LM, Antczak DF, Felippe MJ, Fortier LA. Equine bone marrow-derived mesenchymal stromal cells are heterogeneous in MHC class II expression and capable of inciting an immune response in vitro.. Stem Cell Res Ther 2014 Jan 24;5(1):13.
    doi: 10.1186/scrt402pmc: PMC4055004pubmed: 24461709google scholar: lookup
  56. Takeshita K, Motoike S, Kajiya M, Komatsu N, Takewaki M, Ouhara K, Iwata T, Takeda K, Mizuno N, Fujita T, Kurihara H. Xenotransplantation of interferon-gamma-pretreated clumps of a human mesenchymal stem cell/extracellular matrix complex induces mouse calvarial bone regeneration.. Stem Cell Res Ther 2017 Apr 26;8(1):101.
    doi: 10.1186/s13287-017-0550-1pmc: PMC5406942pubmed: 28446226google scholar: lookup

Citations

This article has been cited 8 times.
  1. Leal Reis I, Lopes B, Sousa P, Sousa AC, Branquinho M, Caseiro AR, Pedrosa SS, Rêma A, Oliveira C, Porto B, Atayde L, Amorim I, Alvites R, Santos JM, Maurício AC. Allogenic Synovia-Derived Mesenchymal Stem Cells for Treatment of Equine Tendinopathies and Desmopathies-Proof of Concept. Animals (Basel) 2023 Apr 11;13(8).
    doi: 10.3390/ani13081312pubmed: 37106875google scholar: lookup
  2. Brachtl G, Poupardin R, Hochmann S, Raninger A, Jürchott K, Streitz M, Schlickeiser S, Oeller M, Wolf M, Schallmoser K, Volk HD, Geissler S, Strunk D. Batch Effects during Human Bone Marrow Stromal Cell Propagation Prevail Donor Variation and Culture Duration: Impact on Genotype, Phenotype and Function. Cells 2022 Mar 10;11(6).
    doi: 10.3390/cells11060946pubmed: 35326396google scholar: lookup
  3. Lu V, Tennyson M, Zhang J, Khan W. Mesenchymal Stem Cell-Derived Extracellular Vesicles in Tendon and Ligament Repair-A Systematic Review of In Vivo Studies. Cells 2021 Sep 27;10(10).
    doi: 10.3390/cells10102553pubmed: 34685532google scholar: lookup
  4. Khaled H, Zayed M, Kim B, Jeong BH, Oh SI. Enhanced tenogenic potential of tendon-derived mesenchymal stem cells: transcriptomic profiling and in vivo validation. Front Cell Dev Biol 2025;13:1687816.
    doi: 10.3389/fcell.2025.1687816pubmed: 41181702google scholar: lookup
  5. Zayed M, Elwakeel E, Ezzat P, Jeong BH. Mesenchymal stem cell-derived exosomes as a potential therapeutic strategy for ferroptosis. Stem Cell Res Ther 2025 Jul 15;16(1):368.
    doi: 10.1186/s13287-025-04511-2pubmed: 40660292google scholar: lookup
  6. Zayed M, Jeong BH. Mesenchymal Stem Cell Secretome Attenuates PrP(106-126)-Induced Neurotoxicity by Suppressing Neuroinflammation and Apoptosis and Enhances Cell Migration. Cells 2025 Jun 5;14(11).
    doi: 10.3390/cells14110851pubmed: 40498027google scholar: lookup
  7. Lee MJ, Park K, Yeon Lee S, Jang KH, Won S, Hyunchul Jo C. Effects of Conditioned Media From Human Umbilical Cord-Derived Mesenchymal Stem Cells on Tenocytes From Degenerative Rotator Cuff Tears in an Interleukin 1β-Induced Tendinopathic Condition. Orthop J Sports Med 2024 Nov;12(11):23259671241286412.
    doi: 10.1177/23259671241286412pubmed: 39534392google scholar: lookup
  8. Paudel S, Feltham T, Manandhar L, Guo Y, Schon L, Zhang Z. Mild Synovitis Impairs Chondrogenic Joint Environment. Cells Tissues Organs 2024;213(3):245-254.
    doi: 10.1159/000532008pubmed: 37524055google scholar: lookup
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