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Stem cell research & therapy2014; 5(1); 25; doi: 10.1186/scrt414

Equine mesenchymal stem cells from bone marrow, adipose tissue and umbilical cord: immunophenotypic characterization and differentiation potential.

Abstract: Studies with mesenchymal stem cells (MSCs) are increasing due to their immunomodulatory, anti-inflammatory and tissue regenerative properties. However, there is still no agreement about the best source of equine MSCs for a bank for allogeneic therapy. The aim of this study was to evaluate the cell culture and immunophenotypic characteristics and differentiation potential of equine MSCs from bone marrow (BM-MSCs), adipose tissue (AT-MSCs) and umbilical cord (UC-MSCs) under identical in vitro conditions, to compare these sources for research or an allogeneic therapy cell bank. Methods: The BM-MSCs, AT-MSCs and UC-MSCs were cultured and evaluated in vitro for their osteogenic, adipogenic and chondrogenic differentiation potential. Additionally, MSCs were assessed for CD105, CD44, CD34, CD90 and MHC-II markers by flow cytometry, and MHC-II was also assessed by immunocytochemistry. To interpret the flow cytometry results, statistical analysis was performed using ANOVA. Results: The harvesting and culturing procedures of BM-MSCs, AT-MSCs and UC-MSCs were feasible, with an average cell growth until the third passage of 25 days for BM-MSCs, 15 days for AT-MSCs and 26 days for UC-MSCs. MSCs from all sources were able to differentiate into osteogenic (after 10 days for BM-MSCs and AT-MSCs and 15 days for UC-MSCs), adipogenic (after 8 days for BM-MSCs and AT-MSCs and 15 days for UC-MSCs) and chondrogenic (after 21 days for BM-MSCs, AT-MSCs and UC-MSCs) lineages. MSCs showed high expression of CD105, CD44 and CD90 and low or negative expression of CD34 and MHC-II. The MHC-II was not detected by immunocytochemistry techniques in any of the MSCs studied. Conclusions: The BM, AT and UC are feasible sources for harvesting equine MSCs, and their immunophenotypic and multipotency characteristics attained minimal criteria for defining MSCs. Due to the low expression of MHC-II by MSCs, all of the sources could be used in clinical trials involving allogeneic therapy in horses. However, the BM-MSCs and AT-MSCs showed fastest ''in vitro'' differentiation and AT-MSCs showed highest cell growth until third passage. These findings suggest that BM and AT may be preferable for cell banking purposes.
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Publication Date: 2014-02-21 PubMed ID: 24559797PubMed Central: PMC4055040DOI: 10.1186/scrt414Google Scholar: Lookup
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Summary

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

The research explores the potential of three different sources of equine mesenchymal stem cells (BM-MSCs, AT-MSCs, and UC-MSCs) for use in allogeneic stem cell therapies. It found that all sources could be feasibly used and had minimal criteria for defining MSCs, with the BM-MSCs and AT-MSCs showing the most promising results for cell banking.

Research Objective

  • The primary goal of this study was to find out the best potential source of equine mesenchymal stem cells (MSCs) for an allogeneic therapy cell bank. In simple terms, allogeneic therapy is a procedure in which cells, tissues, or organs are transferred from one individual to another of the same species. The sources assessed were bone marrow (BM-MSCs), adipose tissue (AT-MSCs), and umbilical cord (UC-MSCs).

Research Methodology

  • Mesenchymal stem cells from all three sources were cultured under identical in vitro conditions.
  • These were then evaluated for their capacity to differentiate into osteogenic, adipogenic, and chondrogenic lineages.
  • The MSCs were also tested for immunophenotypic markers (CD105, CD44, CD34, CD90, and MHC-II) using flow cytometry and immunocytochemistry techniques.
  • Statistical analysis, using ANOVA, was conducted to interpret the flow cytometry results.

Key Findings

  • The harvesting procedures for MSCs from all three sources were viable. The average cell growth until the third passage was 25 days for BM-MSCs, 15 days for AT-MSCs, and 26 days for UC-MSCs.
  • All the sourced MSCs could differentiate into osteogenic, adipogenic, and chondrogenic cells.
  • The cells showed high expression of CD105, CD44, and CD90 markers and low or no expression of CD34 and MHC-II. MHC-II was not detected in any of the MSCs through immunocytochemistry techniques.
  • All the sources can be potentially used for allogeneic therapy due to the low expression of MHC-II.

Conclusions

  • The study concluded that all sources (BM, AT, and UC) meet the minimal criteria for defining MSCs and can be used for stem-cell therapies in horses.
  • However, the most conducive for in vitro differentiation were BM-MSCs and AT-MSCs, and AT-MSCs showed the highest cell growth until the third passage, making them more preferable for cell banking purposes.

Cite This Article

APA
Barberini DJ, Freitas NP, Magnoni MS, Maia L, Listoni AJ, Heckler MC, Sudano MJ, Golim MA, da Cruz Landim-Alvarenga F, Amorim RM. (2014). Equine mesenchymal stem cells from bone marrow, adipose tissue and umbilical cord: immunophenotypic characterization and differentiation potential. Stem Cell Res Ther, 5(1), 25. https://doi.org/10.1186/scrt414

Publication

Stem cell research & therapy
ISSN: 1757-6512
NlmUniqueID: 101527581
Country: England
Language: English
Volume: 5
Issue: 1
Pages: 25

Researcher Affiliations

Barberini, Danielle Jaqueta
    Freitas, Natália Pereira Paiva
      Magnoni, Mariana Sartori
        Maia, Leandro
          Listoni, Amanda Jerônimo
            Heckler, Marta Cristina
              Sudano, Mateus Jose
                Golim, Marjorie Assis
                  da Cruz Landim-Alvarenga, Fernanda
                    Amorim, Rogério Martins

                      MeSH Terms

                      • Adipose Tissue / cytology
                      • Animals
                      • Antigens, CD34 / genetics
                      • Antigens, CD34 / metabolism
                      • Cell Differentiation
                      • Cells, Cultured
                      • Female
                      • HLA-DR alpha-Chains / genetics
                      • HLA-DR alpha-Chains / metabolism
                      • Horses
                      • Hyaluronan Receptors / genetics
                      • Hyaluronan Receptors / metabolism
                      • Immunophenotyping
                      • Male
                      • Mesenchymal Stem Cells / cytology
                      • Mesenchymal Stem Cells / immunology
                      • Mesenchymal Stem Cells / metabolism
                      • Thy-1 Antigens / genetics
                      • Thy-1 Antigens / metabolism
                      • Umbilical Cord / cytology

                      References

                      This article includes 51 references
                      1. Chamberlain G, Fox J, Ashton B, Middleton J. Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing.. Stem Cells 2007 Nov;25(11):2739-49.
                        doi: 10.1634/stemcells.2007-0197pubmed: 17656645google scholar: lookup
                      2. Nöth U, Rackwitz L, Steinert AF, Tuan RS. Cell delivery therapeutics for musculoskeletal regeneration.. Adv Drug Deliv Rev 2010 Jun 15;62(7-8):765-83.
                        doi: 10.1016/j.addr.2010.04.004pubmed: 20398712google scholar: lookup
                      3. Taylor SE, Smith RK, Clegg PD. Mesenchymal stem cell therapy in equine musculoskeletal disease: scientific fact or clinical fiction?. Equine Vet J 2007 Mar;39(2):172-80.
                        doi: 10.2746/042516407X180868pubmed: 17378447google scholar: lookup
                      4. Guest DJ, Smith MR, Allen WR. Monitoring the fate of autologous and allogeneic mesenchymal progenitor cells injected into the superficial digital flexor tendon of horses: preliminary study.. Equine Vet J 2008 Mar;40(2):178-81.
                        doi: 10.2746/042516408X276942pubmed: 18267891google scholar: lookup
                      5. Carrade DD, Owens SD, Galuppo LD, Vidal MA, Ferraro GL, Librach F, Buerchler S, Friedman MS, Walker NJ, Borjesson DL. Clinicopathologic findings following intra-articular injection of autologous and allogeneic placentally derived equine mesenchymal stem cells in horses.. Cytotherapy 2011 Apr;13(4):419-30.
                        doi: 10.3109/14653249.2010.536213pubmed: 21105841google scholar: lookup
                      6. Chen Y, Shao JZ, Xiang LX, Dong XJ, Zhang GR. Mesenchymal stem cells: a promising candidate in regenerative medicine.. Int J Biochem Cell Biol 2008;40(5):815-20.
                        doi: 10.1016/j.biocel.2008.01.007pubmed: 18295530google scholar: lookup
                      7. Wu XB, Tao R. Hepatocyte differentiation of mesenchymal stem cells.. Hepatobiliary Pancreat Dis Int 2012 Aug 15;11(4):360-71.
                        doi: 10.1016/S1499-3872(12)60193-3pubmed: 22893462google scholar: lookup
                      8. Reed SA, Johnson SE. Equine umbilical cord blood contains a population of stem cells that express Oct4 and differentiate into mesodermal and endodermal cell types.. J Cell Physiol 2008 May;215(2):329-36.
                        doi: 10.1002/jcp.21312pubmed: 17929245google scholar: lookup
                      9. Gutierrez-Nibeyro SD. Commercial cell-based therapies for musculoskeletal injuries in horses.. Vet Clin North Am Equine Pract 2011 Aug;27(2):363-71.
                        doi: 10.1016/j.cveq.2011.04.001pubmed: 21872764google scholar: lookup
                      10. Sole A, Spriet M, Galuppo LD, Padgett KA, Borjesson DL, Wisner ER, Brosnan RJ, Vidal MA. Scintigraphic evaluation of intra-arterial and intravenous regional limb perfusion of allogeneic bone marrow-derived mesenchymal stem cells in the normal equine distal limb using (99m) Tc-HMPAO.. Equine Vet J 2012 Sep;44(5):594-9.
                        doi: 10.1111/j.2042-3306.2011.00530.xpubmed: 22212017google scholar: lookup
                      11. de Mattos Carvalho A, Alves AL, Golim MA, Moroz A, Hussni CA, de Oliveira PG, Deffune E. Isolation and immunophenotypic characterization of mesenchymal stem cells derived from equine species adipose tissue.. Vet Immunol Immunopathol 2009 Dec 15;132(2-4):303-6.
                        doi: 10.1016/j.vetimm.2009.06.014pubmed: 19647331google scholar: lookup
                      12. Ranera B, Lyahyai J, Romero A, Vázquez FJ, Remacha AR, Bernal ML, Zaragoza P, Rodellar C, Martín-Burriel I. Immunophenotype and gene expression profiles of cell surface markers of mesenchymal stem cells derived from equine bone marrow and adipose tissue.. Vet Immunol Immunopathol 2011 Nov 15;144(1-2):147-54.
                        doi: 10.1016/j.vetimm.2011.06.033pubmed: 21782255google scholar: lookup
                      13. Lange-Consiglio A, Corradetti B, Meucci A, Perego R, Bizzaro D, Cremonesi F. Characteristics of equine mesenchymal stem cells derived from amnion and bone marrow: in vitro proliferative and multilineage potential assessment.. Equine Vet J 2013 Nov;45(6):737-44.
                        doi: 10.1111/evj.12052pubmed: 23527626google scholar: lookup
                      14. Rogers I, Casper RF. Umbilical cord blood stem cells.. Best Pract Res Clin Obstet Gynaecol 2004 Dec;18(6):893-908.
                        doi: 10.1016/j.bpobgyn.2004.06.004pubmed: 15582545google scholar: lookup
                      15. Guest DJ, Ousey JC, Smith MR. Defining the expression of marker genes in equine mesenchymal stromal cells.. Stem Cells Cloning 2008;1:1-9.
                        pmc: PMC3781685pubmed: 24198500doi: 10.2147/sccaa.s3824google scholar: lookup
                      16. Pascucci L, Curina G, Mercati F, Marini C, Dall'Aglio C, Paternesi B, Ceccarelli P. Flow cytometric characterization of culture expanded multipotent mesenchymal stromal cells (MSCs) from horse adipose tissue: towards the definition of minimal stemness criteria.. Vet Immunol Immunopathol 2011 Dec 15;144(3-4):499-506.
                        doi: 10.1016/j.vetimm.2011.07.017pubmed: 21839521google scholar: lookup
                      17. De Schauwer C, Meyer E, Van de Walle GR, Van Soom A. Markers of stemness in equine mesenchymal stem cells: a plea for uniformity.. Theriogenology 2011 May;75(8):1431-43.
                        pubmed: 21196039doi: 10.1016/j.theriogenology.2010.11.008google scholar: lookup
                      18. Borjesson DL, Peroni JF. The regenerative medicine laboratory: facilitating stem cell therapy for equine disease.. Clin Lab Med 2011 Mar;31(1):109-23.
                        doi: 10.1016/j.cll.2010.12.001pubmed: 21295725google scholar: lookup
                      19. Burk J, Badylak SF, Kelly J, Brehm W. Equine cellular therapy--from stall to bench to bedside?. Cytometry A 2013 Jan;83(1):103-13.
                        pubmed: 23081833doi: 10.1002/cyto.a.22216google scholar: lookup
                      20. 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
                      21. Ranera B, Ordovás L, Lyahyai J, Bernal ML, Fernandes F, Remacha AR, Romero A, Vázquez FJ, Osta R, Cons C, Varona L, Zaragoza P, Martín-Burriel I, Rodellar C. Comparative study of equine bone marrow and adipose tissue-derived mesenchymal stromal cells.. Equine Vet J 2012 Jan;44(1):33-42.
                        doi: 10.1111/j.2042-3306.2010.00353.xpubmed: 21668489google scholar: lookup
                      22. Hoynowski SM, Fry MM, Gardner BM, Leming MT, Tucker JR, Black L, Sand T, Mitchell KE. Characterization and differentiation of equine umbilical cord-derived matrix cells.. Biochem Biophys Res Commun 2007 Oct 19;362(2):347-53.
                        doi: 10.1016/j.bbrc.2007.07.182pubmed: 17719011google scholar: lookup
                      23. Lovati AB, Corradetti B, Lange Consiglio A, Recordati C, Bonacina E, Bizzaro D, Cremonesi F. Comparison of equine bone marrow-, umbilical cord matrix and amniotic fluid-derived progenitor cells.. Vet Res Commun 2011 Feb;35(2):103-21.
                        doi: 10.1007/s11259-010-9457-3pubmed: 21193959google scholar: lookup
                      24. De Schauwer C, Piepers S, Van de Walle GR, Demeyere K, Hoogewijs MK, Govaere JL, Braeckmans K, Van Soom A, Meyer E. In search for cross-reactivity to immunophenotype equine mesenchymal stromal cells by multicolor flow cytometry.. Cytometry A 2012 Apr;81(4):312-23.
                        doi: 10.1002/cyto.a.22026pubmed: 22411893google scholar: lookup
                      25. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop Dj, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement.. Cytotherapy 2006;8(4):315-7.
                        doi: 10.1080/14653240600855905pubmed: 16923606google scholar: lookup
                      26. Bourin P, Bunnell BA, Casteilla L, Dominici M, Katz AJ, March KL, Redl H, Rubin JP, Yoshimura K, Gimble JM. Stromal cells from the adipose tissue-derived stromal vascular fraction and culture expanded adipose tissue-derived stromal/stem cells: a joint statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapy (ISCT).. Cytotherapy 2013 Jun;15(6):641-8.
                        doi: 10.1016/j.jcyt.2013.02.006pmc: PMC3979435pubmed: 23570660google scholar: lookup
                      27. Burk J, Ribitsch I, Gittel C, Juelke H, Kasper C, Staszyk C, Brehm W. Growth and differentiation characteristics of equine mesenchymal stromal cells derived from different sources.. Vet J 2013 Jan;195(1):98-106.
                        doi: 10.1016/j.tvjl.2012.06.004pubmed: 22841420google scholar: lookup
                      28. Richardson LE, Dudhia J, Clegg PD, Smith R. Stem cells in veterinary medicine--attempts at regenerating equine tendon after injury.. Trends Biotechnol 2007 Sep;25(9):409-16.
                        doi: 10.1016/j.tibtech.2007.07.009pubmed: 17692415google scholar: lookup
                      29. Nixon AJ, Dahlgren LA, Haupt JL, Yeager AE, Ward DL. Effect of adipose-derived nucleated cell fractions on tendon repair in horses with collagenase-induced tendinitis.. Am J Vet Res 2008 Jul;69(7):928-37.
                        doi: 10.2460/ajvr.69.7.928pubmed: 18593247google scholar: lookup
                      30. Kern S, Eichler H, Stoeve J, Klüter H, Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue.. Stem Cells 2006 May;24(5):1294-301.
                        doi: 10.1634/stemcells.2005-0342pubmed: 16410387google scholar: lookup
                      31. Carrade DD, Affolter VK, Outerbridge CA, Watson JL, Galuppo LD, Buerchler S, Kumar V, Walker NJ, Borjesson DL. Intradermal injections of equine allogeneic umbilical cord-derived mesenchymal stem cells are well tolerated and do not elicit immediate or delayed hypersensitivity reactions.. Cytotherapy 2011 Nov;13(10):1180-92.
                        doi: 10.3109/14653249.2011.602338pubmed: 21899391google scholar: lookup
                      32. Peroni JF, Borjesson DL. Anti-inflammatory and immunomodulatory activities of stem cells.. Vet Clin North Am Equine Pract 2011 Aug;27(2):351-62.
                        doi: 10.1016/j.cveq.2011.06.003pubmed: 21872763google scholar: lookup
                      33. Ryan JM, Barry FP, Murphy JM, Mahon BP. Mesenchymal stem cells avoid allogeneic rejection.. J Inflamm (Lond) 2005 Jul 26;2:8.
                        doi: 10.1186/1476-9255-2-8pmc: PMC1215510pubmed: 16045800google scholar: lookup
                      34. Maia L, Landim-Alvarenga FC, Da Mota LS, De Assis Golim M, Laufer-Amorim R, De Vita B, Barberini DJ, Listoni AJ, De Moraes CN, Heckler MC, Amorim RM. Immunophenotypic, immunocytochemistry, ultrastructural, and cytogenetic characterization of mesenchymal stem cells from equine bone marrow.. Microsc Res Tech 2013 Jun;76(6):618-24.
                        doi: 10.1002/jemt.22208pubmed: 23533133google scholar: lookup
                      35. Corradetti B, Lange-Consiglio A, Barucca M, Cremonesi F, Bizzaro D. Size-sieved subpopulations of mesenchymal stem cells from intervascular and perivascular equine umbilical cord matrix.. Cell Prolif 2011 Aug;44(4):330-42.
                        doi: 10.1111/j.1365-2184.2011.00759.xpmc: PMC6496711pubmed: 21645152google scholar: lookup
                      36. Bartholomew S, Owens SD, Ferraro GL, Carrade DD, Lara DJ, Librach FA, Borjesson DL, Galuppo LD. Collection of equine cord blood and placental tissues in 40 thoroughbred mares.. Equine Vet J 2009 Nov;41(8):724-8.
                        doi: 10.2746/042516409X429446pubmed: 20095217google scholar: lookup
                      37. Koerner J, Nesic D, Romero JD, Brehm W, Mainil-Varlet P, Grogan SP. Equine peripheral blood-derived progenitors in comparison to bone marrow-derived mesenchymal stem cells.. Stem Cells 2006 Jun;24(6):1613-9.
                        doi: 10.1634/stemcells.2005-0264pubmed: 16769763google scholar: lookup
                      38. Colleoni S, Bottani E, Tessaro I, Mari G, Merlo B, Romagnoli N, Spadari A, Galli C, Lazzari G. Isolation, growth and differentiation of equine mesenchymal stem cells: effect of donor, source, amount of tissue and supplementation with basic fibroblast growth factor.. Vet Res Commun 2009 Dec;33(8):811-21.
                        doi: 10.1007/s11259-009-9229-0pubmed: 19472068google scholar: lookup
                      39. Vidal MA, Walker NJ, Napoli E, Borjesson DL. Evaluation of senescence in mesenchymal stem cells isolated from equine bone marrow, adipose tissue, and umbilical cord tissue.. Stem Cells Dev 2012 Jan 20;21(2):273-83.
                        doi: 10.1089/scd.2010.0589pubmed: 21410356google scholar: lookup
                      40. Toupadakis CA, Wong A, Genetos DC, Cheung WK, Borjesson DL, Ferraro GL, Galuppo LD, Leach JK, Owens SD, Yellowley CE. Comparison of the osteogenic potential of equine mesenchymal stem cells from bone marrow, adipose tissue, umbilical cord blood, and umbilical cord tissue.. Am J Vet Res 2010 Oct;71(10):1237-45.
                        doi: 10.2460/ajvr.71.10.1237pubmed: 20919913google scholar: lookup
                      41. Raabe O, Reich C, Wenisch S, Hild A, Burg-Roderfeld M, Siebert HC, Arnhold S. Hydrolyzed fish collagen induced chondrogenic differentiation of equine adipose tissue-derived stromal cells.. Histochem Cell Biol 2010 Dec;134(6):545-54.
                        doi: 10.1007/s00418-010-0760-4pubmed: 21076963google scholar: lookup
                      42. Vidal MA, Kilroy GE, Lopez MJ, Johnson JR, Moore RM, Gimble JM. Characterization of equine adipose tissue-derived stromal cells: adipogenic and osteogenic capacity and comparison with bone marrow-derived mesenchymal stromal cells.. Vet Surg 2007 Oct;36(7):613-22.
                        doi: 10.1111/j.1532-950X.2007.00313.xpubmed: 17894587google scholar: lookup
                      43. Troyer DL, Weiss ML. Wharton's jelly-derived cells are a primitive stromal cell population.. Stem Cells 2008 Mar;26(3):591-9.
                        doi: 10.1634/stemcells.2007-0439pmc: PMC3311226pubmed: 18065397google scholar: lookup
                      44. Iacono E, Brunori L, Pirrone A, Pagliaro PP, Ricci F, Tazzari PL, Merlo B. Isolation, characterization and differentiation of mesenchymal stem cells from amniotic fluid, umbilical cord blood and Wharton's jelly in the horse.. Reproduction 2012 Apr;143(4):455-68.
                        doi: 10.1530/REP-10-0408pubmed: 22274885google scholar: lookup
                      45. Xie L, Zhang N, Marsano A, Vunjak-Novakovic G, Zhang Y, Lopez MJ. In vitro mesenchymal trilineage differentiation and extracellular matrix production by adipose and bone marrow derived adult equine multipotent stromal cells on a collagen scaffold.. Stem Cell Rev Rep 2013 Dec;9(6):858-72.
                        doi: 10.1007/s12015-013-9456-1pmc: PMC3834181pubmed: 23892935google scholar: lookup
                      46. Vidal MA, Robinson SO, Lopez MJ, Paulsen DB, Borkhsenious O, Johnson JR, Moore RM, Gimble JM. Comparison of chondrogenic potential in equine mesenchymal stromal cells derived from adipose tissue and bone marrow.. Vet Surg 2008 Dec;37(8):713-24.
                        doi: 10.1111/j.1532-950X.2008.00462.xpmc: PMC2746327pubmed: 19121166google scholar: lookup
                      47. Radcliffe CH, Flaminio MJ, Fortier LA. Temporal analysis of equine bone marrow aspirate during establishment of putative mesenchymal progenitor cell populations.. Stem Cells Dev 2010 Feb;19(2):269-82.
                        doi: 10.1089/scd.2009.0091pmc: PMC3138180pubmed: 19604071google scholar: lookup
                      48. Braun J, Hack A, Weis-Klemm M, Conrad S, Treml S, Kohler K, Walliser U, Skutella T, Aicher WK. Evaluation of the osteogenic and chondrogenic differentiation capacities of equine adipose tissue-derived mesenchymal stem cells.. Am J Vet Res 2010 Oct;71(10):1228-36.
                        doi: 10.2460/ajvr.71.10.1228pubmed: 20919912google scholar: lookup
                      49. Secco M, Zucconi E, Vieira NM, Fogaça LL, Cerqueira A, Carvalho MD, Jazedje T, Okamoto OK, Muotri AR, Zatz M. Multipotent stem cells from umbilical cord: cord is richer than blood!. Stem Cells 2008 Jan;26(1):146-50.
                        doi: 10.1634/stemcells.2007-0381pubmed: 17932423google scholar: lookup
                      50. De Vita B, Campos LL, Listoni AJ, Maia L, Sudano MJ, Curcio BR, Landim-Alvarenga FC, Prestes NC. Isolamento, caracterização ediferenciação de células-tronco mesenquimais do líquido amniótico equino obtido em diferentes idades gestacionais.. Pesq Vet Bras 2013;33:535–542.
                        doi: 10.1590/S0100-736X2013000400019google scholar: lookup
                      51. Mambelli LI, Santos EJ, Frazão PJ, Chaparro MB, Kerkis A, Zoppa AL, Kerkis I. Characterization of equine adipose tissue-derived progenitor cells before and after cryopreservation.. Tissue Eng Part C Methods 2009 Mar;15(1):87-94.
                        pubmed: 19196122doi: 10.1089/ten.tec.2008.0186google scholar: lookup

                      Citations

                      This article has been cited 56 times.
                      1. Sindeeva OA, Demina PA, Kozyreva ZV, Muslimov AR, Gusliakova OI, Laushkina VO, Mordovina EA, Tsyupka D, Epifanovskaya OS, Sapach AY, Goryacheva IY, Sukhorukov GB. Labeling and Tracking of Individual Human Mesenchymal Stromal Cells Using Photoconvertible Fluorescent Microcapsules. Int J Mol Sci 2023 Sep 4;24(17).
                        doi: 10.3390/ijms241713665pubmed: 37686471google scholar: lookup
                      2. Petrova V, Yonkova P, Simeonova G, Vachkova E. Horse serum potentiates cellular viability and improves indomethacin-induced adipogenesis in equine subcutaneous adipose-derived stem cells (ASCs). Int J Vet Sci Med 2023;11(1):94-105.
                        doi: 10.1080/23144599.2023.2248805pubmed: 37655053google scholar: lookup
                      3. Savva A, Saez J, Withers A, Barberio C, Stoeger V, Elias-Kirma S, Lu Z, Moysidou CM, Kallitsis K, Pitsalidis C, Owens RM. 3D organic bioelectronics for electrical monitoring of human adult stem cells. Mater Horiz 2023 Aug 29;10(9):3589-3600.
                        doi: 10.1039/d3mh00785epubmed: 37318042google scholar: lookup
                      4. El-Husseiny HM, Kaneda M, Mady EA, Yoshida T, Doghish AS, Tanaka R. Impact of Adipose Tissue Depot Harvesting Site on the Multilineage Induction Capacity of Male Rat Adipose-Derived Mesenchymal Stem Cells: An In Vitro Study. Int J Mol Sci 2023 Apr 19;24(8).
                        doi: 10.3390/ijms24087513pubmed: 37108673google scholar: lookup
                      5. Ferreira LVO, Kamura BDC, Oliveira JPM, Chimenes ND, Carvalho M, Santos LAD, Dias-Melicio LA, Amorim RL, Amorim RM. In Vitro Transdifferentiation Potential of Equine Mesenchymal Stem Cells into Schwann-Like Cells. Stem Cells Dev 2023 Jul;32(13-14):422-432.
                        doi: 10.1089/scd.2022.0274pubmed: 37071193google scholar: lookup
                      6. Heilen LB, Roßgardt J, Dern-Wieloch J, Vogelsberg J, Staszyk C. Isolation and cultivation as well as in situ identification of MSCs from equine dental pulp and periodontal ligament. Front Vet Sci 2023;10:1116671.
                        doi: 10.3389/fvets.2023.1116671pubmed: 36968463google scholar: lookup
                      7. Szydlak R. Mesenchymal stem cells in ischemic tissue regeneration. World J Stem Cells 2023 Feb 26;15(2):16-30.
                        doi: 10.4252/wjsc.v15.i2.16pubmed: 36909782google scholar: lookup
                      8. 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
                      9. Bagge J, Berg LC, Janes J, MacLeod JN. Donor age effects on in vitro chondrogenic and osteogenic differentiation performance of equine bone marrow- and adipose tissue-derived mesenchymal stromal cells. BMC Vet Res 2022 Nov 3;18(1):388.
                        doi: 10.1186/s12917-022-03475-2pubmed: 36329434google scholar: lookup
                      10. Trachsel DS, Stage HJ, Rausch S, Trappe S, Söllig K, Sponder G, Merle R, Aschenbach JR, Gehlen H. Comparison of Sources and Methods for the Isolation of Equine Adipose Tissue-Derived Stromal/Stem Cells and Preliminary Results on Their Reaction to Incubation with 5-Azacytidine. Animals (Basel) 2022 Aug 11;12(16).
                        doi: 10.3390/ani12162049pubmed: 36009640google scholar: lookup
                      11. Margiana R, Markov A, Zekiy AO, Hamza MU, Al-Dabbagh KA, Al-Zubaidi SH, Hameed NM, Ahmad I, Sivaraman R, Kzar HH, Al-Gazally ME, Mustafa YF, Siahmansouri H. Clinical application of mesenchymal stem cell in regenerative medicine: a narrative review. Stem Cell Res Ther 2022 Jul 28;13(1):366.
                        doi: 10.1186/s13287-022-03054-0pubmed: 35902958google scholar: lookup
                      12. Nino-Fong R, Esparza Gonzalez BP, Rodriguez-Lecompte JC, Montelpare W, McD￮ L. Development of a biologically immortalized equine stem cell line. Can J Vet Res 2021 Oct;85(4):293-301.
                        pubmed: 34602734
                      13. Hendawy H, Kaneda M, Metwally E, Shimada K, Tanaka T, Tanaka R. A Comparative Study of the Effect of Anatomical Site on Multiple Differentiation of Adipose-Derived Stem Cells in Rats. Cells 2021 Sep 18;10(9).
                        doi: 10.3390/cells10092469pubmed: 34572123google scholar: lookup
                      14. Garnica-Galvez S, Korntner SH, Skoufos I, Tzora A, Diakakis N, Prassinos N, Zeugolis DI. Hyaluronic Acid as Macromolecular Crowder in Equine Adipose-Derived Stem Cell Cultures. Cells 2021 Apr 9;10(4).
                        doi: 10.3390/cells10040859pubmed: 33918830google scholar: lookup
                      15. Okamoto-Okubo CE, Cassu RN, Joaquim JGF, Reis Mesquita LD, Rahal SC, Oliveira HSS, Takahira R, Arruda I, Maia L, Cruz Landim FD, Luna SPL. Chronic pain and gait analysis in dogs with degenerative hip joint disease treated with repeated intra-articular injections of platelet-rich plasma or allogeneic adipose-derived stem cells. J Vet Med Sci 2021 Jun 2;83(5):881-888.
                        doi: 10.1292/jvms.20-0730pubmed: 33814521google scholar: lookup
                      16. Wright A, Arthaud-Day ML, Weiss ML. Therapeutic Use of Mesenchymal Stromal Cells: The Need for Inclusive Characterization Guidelines to Accommodate All Tissue Sources and Species. Front Cell Dev Biol 2021;9:632717.
                        doi: 10.3389/fcell.2021.632717pubmed: 33665190google scholar: lookup
                      17. Ribitsch I, Oreff GL, Jenner F. Regenerative Medicine for Equine Musculoskeletal Diseases. Animals (Basel) 2021 Jan 19;11(1).
                        doi: 10.3390/ani11010234pubmed: 33477808google scholar: lookup
                      18. Pu X, Ma S, Gao Y, Xu T, Chang P, Dong L. Mesenchymal Stem Cell-Derived Exosomes: Biological Function and Their Therapeutic Potential in Radiation Damage. Cells 2020 Dec 30;10(1).
                        doi: 10.3390/cells10010042pubmed: 33396665google scholar: lookup
                      19. Nwabo Kamdje AH, Seke Etet PF, Simo Tagne R, Vecchio L, Lukong KE, Krampera M. Tumor Microenvironment Uses a Reversible Reprogramming of Mesenchymal Stromal Cells to Mediate Pro-tumorigenic Effects. Front Cell Dev Biol 2020;8:545126.
                        doi: 10.3389/fcell.2020.545126pubmed: 33330442google scholar: lookup
                      20. Nwabo Kamdje AH, Seke Etet PF, Tagne Simo R, Vecchio L, Lukong KE, Krampera M. Emerging data supporting stromal cell therapeutic potential in cancer: reprogramming stromal cells of the tumor microenvironment for anti-cancer effects. Cancer Biol Med 2020 Nov 15;17(4):828-841.
                        doi: 10.20892/j.issn.2095-3941.2020.0133pubmed: 33299638google scholar: lookup
                      21. Kim KH, Park TS, Cho BW, Kim TM. Nanoparticles from Equine Fetal Bone Marrow-Derived Cells Enhance the Survival of Injured Chondrocytes. Animals (Basel) 2020 Sep 23;10(10).
                        doi: 10.3390/ani10101723pubmed: 32977476google scholar: lookup
                      22. Caffi V, Espinosa G, Gajardo G, Morales N, Durán MC, Uberti B, Morán G, Plaza A, Henríquez C. Pre-conditioning of Equine Bone Marrow-Derived Mesenchymal Stromal Cells Increases Their Immunomodulatory Capacity. Front Vet Sci 2020;7:318.
                        doi: 10.3389/fvets.2020.00318pubmed: 32656251google scholar: lookup
                      23. Mançanares ACF, Cabezas J, Manríquez J, de Oliveira VC, Wong Alvaro YS, Rojas D, Navarrete Aguirre F, Rodriguez-Alvarez L, Castro FO. Edition of Prostaglandin E2 Receptors EP2 and EP4 by CRISPR/Cas9 Technology in Equine Adipose Mesenchymal Stem Cells. Animals (Basel) 2020 Jun 23;10(6).
                        doi: 10.3390/ani10061078pubmed: 32585798google scholar: lookup
                      24. Liang Y, Zhang D, Li L, Xin T, Zhao Y, Ma R, Du J. Exosomal microRNA-144 from bone marrow-derived mesenchymal stem cells inhibits the progression of non-small cell lung cancer by targeting CCNE1 and CCNE2. Stem Cell Res Ther 2020 Feb 26;11(1):87.
                        doi: 10.1186/s13287-020-1580-7pubmed: 32102682google scholar: lookup
                      25. 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.2019.00507pubmed: 32039250google scholar: lookup
                      26. Colbath AC, Dow SW, Hopkins LS, Phillips JN, McIlwraith CW, Goodrich LR. Single and repeated intra-articular injections in the tarsocrural joint with allogeneic and autologous equine bone marrow-derived mesenchymal stem cells are safe, but did not reduce acute inflammation in an experimental interleukin-1β model of synovitis. Equine Vet J 2020 Jul;52(4):601-612.
                        doi: 10.1111/evj.13222pubmed: 31821594google scholar: lookup
                      27. Al Naem M, Bourebaba L, Kucharczyk K, Röcken M, Marycz K. Therapeutic mesenchymal stromal stem cells: Isolation, characterization and role in equine regenerative medicine and metabolic disorders. Stem Cell Rev Rep 2020 Apr;16(2):301-322.
                        doi: 10.1007/s12015-019-09932-0pubmed: 31797146google scholar: lookup
                      28. Gugjoo MB, Fazili MR, Gayas MA, Ahmad RA, Dhama K. Animal mesenchymal stem cell research in cartilage regenerative medicine - a review. Vet Q 2019 Dec;39(1):95-120.
                        doi: 10.1080/01652176.2019.1643051pubmed: 31291836google scholar: lookup
                      29. Pessôa LVF, Pires PRL, Del Collado M, Pieri NCG, Recchia K, Souza AF, Perecin F, da Silveira JC, de Andrade AFC, Ambrosio CE, Bressan FF, Meirelles FV. Generation and miRNA Characterization of Equine Induced Pluripotent Stem Cells Derived from Fetal and Adult Multipotent Tissues. Stem Cells Int 2019;2019:1393791.
                        doi: 10.1155/2019/1393791pubmed: 31191664google scholar: lookup
                      30. Pfeiffenberger M, Bartsch J, Hoff P, Ponomarev I, Barnewitz D, Thöne-Reineke C, Buttgereit F, Gaber T, Lang A. Hypoxia and mesenchymal stromal cells as key drivers of initial fracture healing in an equine in vitro fracture hematoma model. PLoS One 2019;14(4):e0214276.
                        doi: 10.1371/journal.pone.0214276pubmed: 30947253google scholar: lookup
                      31. Hill ABT, Bressan FF, Murphy BD, Garcia JM. Applications of mesenchymal stem cell technology in bovine species. Stem Cell Res Ther 2019 Jan 24;10(1):44.
                        doi: 10.1186/s13287-019-1145-9pubmed: 30678726google scholar: lookup
                      32. Pieri NCG, de Souza AF, Botigelli RC, Machado LS, Ambrosio CE, Dos Santos Martins D, de Andrade AFC, Meirelles FV, Hyttel P, Bressan FF. Stem cells on regenerative and reproductive science in domestic animals. Vet Res Commun 2019 Feb;43(1):7-16.
                        doi: 10.1007/s11259-019-9744-6pubmed: 30656543google scholar: lookup
                      33. Desancé M, Contentin R, Bertoni L, Gomez-Leduc T, Branly T, Jacquet S, Betsch JM, Batho A, Legendre F, Audigié F, Galéra P, Demoor M. Chondrogenic Differentiation of Defined Equine Mesenchymal Stem Cells Derived from Umbilical Cord Blood for Use in Cartilage Repair Therapy. Int J Mol Sci 2018 Feb 10;19(2).
                        doi: 10.3390/ijms19020537pubmed: 29439436google scholar: lookup
                      34. Veron AD, Bienboire-Frosini C, Feron F, Codecasa E, Deveze A, Royer D, Watelet P, Asproni P, Sadelli K, Chabaud C, Stamegna JC, Fagot J, Khrestchatisky M, Cozzi A, Roman FS, Pageat P, Mengoli M, Girard SD. Isolation and characterization of olfactory ecto-mesenchymal stem cells from eight mammalian genera. BMC Vet Res 2018 Jan 17;14(1):17.
                        doi: 10.1186/s12917-018-1342-2pubmed: 29343270google scholar: lookup
                      35. Zhang B, Zhang J, Shi H, Mao F, Wang J, Yan Y, Zhang X, Qian H, Xu W. A novel method to isolate mesenchymal stem cells from mouse umbilical cord. Mol Med Rep 2018 Jan;17(1):861-869.
                        doi: 10.3892/mmr.2017.7950pubmed: 29115623google scholar: lookup
                      36. Angelone M, Conti V, Biacca C, Battaglia B, Pecorari L, Piana F, Gnudi G, Leonardi F, Ramoni R, Basini G, Dotti S, Renzi S, Ferrari M, Grolli S. The Contribution of Adipose Tissue-Derived Mesenchymal Stem Cells and Platelet-Rich Plasma to the Treatment of Chronic Equine Laminitis: A Proof of Concept. Int J Mol Sci 2017 Oct 11;18(10).
                        doi: 10.3390/ijms18102122pubmed: 29019941google scholar: lookup
                      37. Nwabo Kamdje AH, Kamga PT, Tagne Simo R, Vecchio L, Seke Etet PF, Muller JM, Bassi G, Lukong E, Goel RK, Amvene JM, Krampera M. Mesenchymal stromal cells' role in tumor microenvironment: involvement of signaling pathways. Cancer Biol Med 2017 May;14(2):129-141.
                        doi: 10.20892/j.issn.2095-3941.2016.0033pubmed: 28607804google scholar: lookup
                      38. Esteves CL, Sheldrake TA, Dawson L, Menghini T, Rink BE, Amilon K, Khan N, Péault B, Donadeu FX. Equine Mesenchymal Stromal Cells Retain a Pericyte-Like Phenotype. Stem Cells Dev 2017 Jul 1;26(13):964-972.
                        doi: 10.1089/scd.2017.0017pubmed: 28376684google scholar: lookup
                      39. Zhuo HL, Bai LP, Liu D, Yu SM, Li DT, Liu Q, Song P, Cao SZ, Shen LH. [Effects of retinol on expressions of epidermal growth factor, stem cell factor, colony-stimulating factor 1 and leukemia inhibitory factor in human umbilical cord-derived mesenchymal stem cells]. Nan Fang Yi Ke Da Xue Xue Bao 2016 Feb 20;37(2):221-225.
                        doi: 10.3969/j.issn.1673-4254.2017.02.13pubmed: 28219867google scholar: lookup
                      40. 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.2016.00121pubmed: 28149840google scholar: lookup
                      41. Maumus M, Roussignol G, Toupet K, Penarier G, Bentz I, Teixeira S, Oustric D, Jung M, Lepage O, Steinberg R, Jorgensen C, Noel D. Utility of a Mouse Model of Osteoarthritis to Demonstrate Cartilage Protection by IFNγ-Primed Equine Mesenchymal Stem Cells. Front Immunol 2016;7:392.
                        doi: 10.3389/fimmu.2016.00392pubmed: 27729913google scholar: lookup
                      42. Dias MC, Landim-Alvarenga FD, de Moraes CN, da Costa LD, Geraldini CM, de Vasconcelos Machado VM, Maia L. Intramuscular Transplantation of Allogeneic Mesenchymal Stromal Cells Derived from Equine Umbilical Cord. Int J Stem Cells 2016 Nov 30;9(2):239-249.
                        doi: 10.15283/ijsc16011pubmed: 27572709google scholar: lookup
                      43. Murata D, Yamasaki A, Matsuzaki S, Sunaga T, Fujiki M, Tokunaga S, Misumi K. Characteristics and multipotency of equine dedifferentiated fat cells. J Equine Sci 2016;27(2):57-65.
                        doi: 10.1294/jes.27.57pubmed: 27330399google scholar: lookup
                      44. Fülber J, Maria DA, da Silva LC, Massoco CO, Agreste F, Baccarin RY. Comparative study of equine mesenchymal stem cells from healthy and injured synovial tissues: an in vitro assessment. Stem Cell Res Ther 2016 Mar 5;7:35.
                        doi: 10.1186/s13287-016-0294-3pubmed: 26944403google scholar: lookup
                      45. Zhu T, Chen R, Li Z, Tian J, Deng C, Zhang X, Zhang K, Tong L, Yu Y, Bai C. Functional Role of FcγRIIB in the Regulation of Mesenchymal Stem Cell Function. Int J Med Sci 2016;13(2):154-60.
                        doi: 10.7150/ijms.13649pubmed: 26941575google scholar: lookup
                      46. Gomiero C, Bertolutti G, Martinello T, Van Bruaene N, Broeckx SY, Patruno M, Spaas JH. Tenogenic induction of equine mesenchymal stem cells by means of growth factors and low-level laser technology. Vet Res Commun 2016 Mar;40(1):39-48.
                        doi: 10.1007/s11259-016-9652-ypubmed: 26757735google scholar: lookup
                      47. da Costa Kamura B, de Oliveira Ferreira LV, Chimenes ND, de Oliveira JPM, Rodriguez-Sanchez DN, de Carvalho M, Amorim RM. Cannabidiol-rich extract suppresses the activation of proinflammatory genes IL-1β and IL-6 in equine mesenchymal stem cells stimulated with lipopolysaccharide. Vet Res Commun 2026 Feb 24;50(3).
                        doi: 10.1007/s11259-026-11105-7pubmed: 41733607google scholar: lookup
                      48. Marais AL, Logan MG, Mellet J, Ambele MA, Pepper MS. Differentiation of Mesenchymal Stromal/Stem Cells from Induced Pluripotent Stem Cells. Methods Mol Biol 2025;2938:155-170.
                        doi: 10.1007/978-1-0716-4607-6_18pubmed: 40445291google scholar: lookup
                      49. Battistin L, Moya LFA, Ferreira LVO, Braz AMM, Carvalho M, Golim MA, Amorim RM. In Vitro Immunomodulatory Effects of Equine Adipose Tissue-Derived Mesenchymal Stem Cells Primed with a Cannabidiol-Rich Extract. Int J Mol Sci 2025 Apr 29;26(9).
                        doi: 10.3390/ijms26094208pubmed: 40362445google scholar: lookup
                      50. Ferreira LVO, Amorim RM. Perspectives on Schwann-like cells derived from bone marrow-mesenchymal stem cells: Advancing peripheral nerve injury therapies. World J Stem Cells 2025 Feb 26;17(2):102702.
                        doi: 10.4252/wjsc.v17.i2.102702pubmed: 40061268google scholar: lookup
                      51. de Oliveira Ferreira LV, Maia L, de Andrade DGA, da Costa Kamura B, de Carvalho M, Amorim RM. Therapeutic potential of mesenchymal stem cells transplantation on traumatic facial nerve paralysis in two horses. Vet Res Commun 2025 Feb 25;49(2):118.
                        doi: 10.1007/s11259-025-10692-1pubmed: 39998709google scholar: lookup
                      52. Xue C, Yu H, Sun Y, Wang X, Pei X, Chen Y, Guan Y. The Mechanisms of Mesenchymal Stem Cells in the Treatment of Experimental Autoimmune Encephalomyelitis. Curr Stem Cell Res Ther 2025;20(5):524-537.
                        doi: 10.2174/011574888X305349240511125540pubmed: 38778596google scholar: lookup
                      53. Zhang B, Lu Q, Dai G, Zhou Y, Ye Q, Zhou Y, Tan WS. Enhancing mesenchymal stem cells cultivated on microcarriers in spinner flasks via impeller design optimization for aggregated suspensions. Bioresour Bioprocess 2023 Dec 3;10(1):89.
                        doi: 10.1186/s40643-023-00707-7pubmed: 38647954google scholar: lookup
                      54. Hemati S, Ghiasi M, Salimi A. Osteogenic Differentiation of Adipose Tissue-Derived Mesenchymal Stem Cells on Composite Polymeric Scaffolds: A Review. Curr Stem Cell Res Ther 2025;20(1):33-49.
                        doi: 10.2174/011574888X263333231218065453pubmed: 38315659google scholar: lookup
                      55. Ferreira-Baptista C, Ferreira R, Fernandes MH, Gomes PS, Colaço B. Influence of the Anatomical Site on Adipose Tissue-Derived Stromal Cells' Biological Profile and Osteogenic Potential in Companion Animals. Vet Sci 2023 Nov 24;10(12).
                        doi: 10.3390/vetsci10120673pubmed: 38133224google scholar: lookup
                      56. Shehzadi S, Javed M, Ullah A, Bilal Waqar A, Iftikhar Shah F, Ullah S. In-vitro Augmentation of Mesenchymal Stem Cells by Using Adult Bovine Serum. Curr Stem Cell Res Ther 2024;19(9):1286-1292.
                        doi: 10.2174/011574888X260118230927050143pubmed: 37861050google scholar: lookup
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