Stem cell research & therapy2014; 5(1); 6; doi: 10.1186/scrt395

Characterization and profiling of immunomodulatory genes of equine mesenchymal stromal cells from non-invasive sources.

Abstract: Mesenchymal stromal cells (MSCs) have been extensively studied for their promising capabilities in regenerative medicine. Although bone marrow is the best-known source for isolating equine MSCs, non-invasive alternative sources such as umbilical cord blood (UCB), umbilical cord matrix (UCM), and peripheral blood (PB) have also been reported. Methods: Equine MSCs from three non-invasive alternative sources were isolated from six individual mares (PB) and their foals (UCB and UCM) at parturition. To minimize inter-horse variability, the samples from the three sources were matched within the same mare and for UCB and UCM even within the same foal from that specific mare. The following parameters were analyzed: (i) success rate of isolation, (ii) proliferation capacity, (iii) tri-lineage differentiation ability, (iv) immunophenotypical protein, and (v) immunomodulatory mRNA profiles. Linear regression models were fit to determine the association between the source of MSCs (UCB, UCM, PB) and (i) the moment of first observation, (ii) the moment of first passage, (iii) cell proliferation data, (iv) the expression of markers related to cell immunogenicity, and (v) the mRNA profile of immunomodulatory factors, except for hepatocyte growth factor (HGF) as no normal distribution could be obtained for the latter variable. To evaluate the association between the source of MSCs and the mRNA expression of HGF, the non-parametric Kruskal-Wallis test was performed instead. Results: While equine MSCs could be isolated from all the UCB and PB samples, isolation from UCM was successful in only two samples because of contamination issues. Proliferation data showed that equine MSCs from all three sources could be easily expanded, although UCB-derived MSCs appeared significantly faster in culture than PB- or UCM-derived MSCs. Equine MSCs from both UCB and PB could be differentiated toward the osteo-, chondro-, and adipogenic lineage, in contrast to UCM-derived MSCs in which only chondro- and adipogenic differentiation could be confirmed. Regardless of the source, equine MSCs expressed the immunomodulatory genes CD40, CD80, HGF, and transforming growth factor-beta (TGFβ). In contrast, no mRNA expression was found for CD86, indoleamine 2,3-dioxygenase (IDO), and tumor necrosis factor-alpha (TNFα). Conclusions: Whereas UCM seems less feasible because of the high contamination risks and low isolation success rates, UCB seems a promising alternative MSC source, especially when considering allogeneic MSC use.
Publication Date: 2014-01-13 PubMed ID: 24418262PubMed Central: PMC4055120DOI: 10.1186/scrt395Google Scholar: Lookup
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  • Journal Article

Summary

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The research investigates the properties of equine Mesenchymal stromal cells (MSCs) as isolated from non-invasive sources such as umbilical cord blood (UCB), umbilical cord matrix (UCM) and equine peripheral blood (PB). It finds that UCB and PB are promising sources for these cells, while UCM was less successful due to contamination risks.

Research Methods

  • The MSCs were collected from three non-invasive sources and from six individual mares, minimizing variability by matching samples from the same mare and for UCB and UCM, the same foal.
  • The researchers analyzed the success rate of isolation, proliferation capacity, tri-lineage differentiation ability, immunophenotypic protein, and immunomodulatory mRNA profiles of these MSCs.
  • Linear regression models were used to determine the association between the source of MSCs and a variety of factors, such as the moment of first observation, the moment of first passage, cell proliferation data, the expression of markers related to cell immunogenicity, and the mRNA profile of immunomodulatory factors.
  • Hepatocyte growth factor (HGF) was excluded as no normal distribution could be obtained. The non-parametric Kruskal-Wallis test was used instead to evaluate the association between the MSC source and HGF mRNA expression.

Findings

  • The study found that MSCs could be successfully isolated from UCB and PB samples, but not from UCM due to contamination issues.
  • The researchers found that UCB-derived MSCs proliferated significantly quicker than PB or UCM-derived MSCs.
  • Both UCB and PB-derived MSCs demonstrated the ability to be differentiated toward the osteo-, chondro-, and adipogenic lineage, whereas UCM-derived MSCs only showed potential for chondro- and adipogenic differentiation.
  • Irrespective of the source, the MSCs expressed immunomodulatory genes such as CD40, CD80, HGF, and TGFβ. However, no mRNA expression was found for CD86, IDO, and TNFα.

Conclusions

  • The research concluded that although UCM was less viable due to high contamination risks and low success rates, UCB and PB emerged as promising alternative sources of MSCs, particularly considering the use of allogenic MSCs for future therapeutical applications.

Cite This Article

APA
De Schauwer C, Goossens K, Piepers S, Hoogewijs MK, Govaere JL, Smits K, Meyer E, Van Soom A, Van de Walle GR. (2014). Characterization and profiling of immunomodulatory genes of equine mesenchymal stromal cells from non-invasive sources. Stem Cell Res Ther, 5(1), 6. https://doi.org/10.1186/scrt395

Publication

ISSN: 1757-6512
NlmUniqueID: 101527581
Country: England
Language: English
Volume: 5
Issue: 1
Pages: 6

Researcher Affiliations

De Schauwer, Catharina
    Goossens, Karen
      Piepers, Sofie
        Hoogewijs, Maarten K
          Govaere, Jan L J
            Smits, Katrien
              Meyer, Evelyne
                Van Soom, Ann
                  Van de Walle, Gerlinde R

                    MeSH Terms

                    • Adipogenesis
                    • Animals
                    • B7-1 Antigen / genetics
                    • B7-1 Antigen / metabolism
                    • B7-2 Antigen / genetics
                    • B7-2 Antigen / metabolism
                    • CD40 Antigens / genetics
                    • CD40 Antigens / metabolism
                    • Cells, Cultured
                    • Female
                    • Fetal Blood / cytology
                    • Gene Expression Profiling
                    • Hepatocyte Growth Factor / genetics
                    • Hepatocyte Growth Factor / metabolism
                    • Horses
                    • Indoleamine-Pyrrole 2,3,-Dioxygenase / genetics
                    • Indoleamine-Pyrrole 2,3,-Dioxygenase / metabolism
                    • Mesenchymal Stem Cells / cytology
                    • Mesenchymal Stem Cells / immunology
                    • Mesenchymal Stem Cells / metabolism
                    • Osteogenesis
                    • RNA, Messenger / genetics
                    • RNA, Messenger / metabolism
                    • Transforming Growth Factor beta / genetics
                    • Transforming Growth Factor beta / metabolism
                    • Tumor Necrosis Factor-alpha / genetics
                    • Tumor Necrosis Factor-alpha / metabolism
                    • Umbilical Cord / cytology

                    References

                    This article includes 47 references
                    1. Wang M, Yang Y, Yang D, Luo F, Liang W, Guo S, Xu J. The immunomodulatory activity of human umbilical cord blood-derived mesenchymal stem cells in vitro.. Immunology 2009 Feb;126(2):220-32.
                    2. Yoo KH, Jang IK, Lee MW, Kim HE, Yang MS, Eom Y, Lee JE, Kim YJ, Yang SK, Jung HL, Sung KW, Kim CW, Koo HH. Comparison of immunomodulatory properties of mesenchymal stem cells derived from adult human tissues.. Cell Immunol 2009;259(2):150-6.
                      doi: 10.1016/j.cellimm.2009.06.010pubmed: 19608159google scholar: lookup
                    3. 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
                    4. Kode JA, Mukherjee S, Joglekar MV, Hardikar AA. Mesenchymal stem cells: immunobiology and role in immunomodulation and tissue regeneration.. Cytotherapy 2009;11(4):377-91.
                      doi: 10.1080/14653240903080367pubmed: 19568970google scholar: lookup
                    5. Deuse T, Stubbendorff M, Tang-Quan K, Phillips N, Kay MA, Eiermann T, Phan TT, Volk HD, Reichenspurner H, Robbins RC, Schrepfer S. Immunogenicity and immunomodulatory properties of umbilical cord lining mesenchymal stem cells.. Cell Transplant 2011;20(5):655-67.
                      doi: 10.3727/096368910X536473pubmed: 21054940google scholar: lookup
                    6. Prasanna SJ, Gopalakrishnan D, Shankar SR, Vasandan AB. Pro-inflammatory cytokines, IFNgamma and TNFalpha, influence immune properties of human bone marrow and Wharton jelly mesenchymal stem cells differentially.. PLoS One 2010 Feb 2;5(2):e9016.
                    7. Alves H, Dechering K, Van Blitterswijk C, De Boer J. High-throughput assay for the identification of compounds regulating osteogenic differentiation of human mesenchymal stromal cells.. PLoS One 2011;6(10):e26678.
                    8. Moroni L, Fornasari PM. Human mesenchymal stem cells: a bank perspective on the isolation, characterization and potential of alternative sources for the regeneration of musculoskeletal tissues.. J Cell Physiol 2013 Apr;228(4):680-7.
                      doi: 10.1002/jcp.24223pubmed: 22949310google scholar: lookup
                    9. 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
                    10. 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
                    11. 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
                    12. Berg L, Koch T, Heerkens T, Bessonov K, Thomsen P, Betts D. Chondrogenic potential of mesenchymal stromal cells derived from equine bone marrow and umbilical cord blood.. Vet Comp Orthop Traumatol 2009;22(5):363-70.
                      pubmed: 19750290doi: 10.3415/VCOT-08-10-0107google scholar: lookup
                    13. Martinello T, Bronzini I, Maccatrozzo L, Iacopetti I, Sampaolesi M, Mascarello F, Patruno M. Cryopreservation does not affect the stem characteristics of multipotent cells isolated from equine peripheral blood.. Tissue Eng Part C Methods 2010 Aug;16(4):771-81.
                      doi: 10.1089/ten.tec.2009.0512pubmed: 19839741google scholar: lookup
                    14. Spaas JH, De Schauwer C, Cornillie P, Meyer E, Van Soom A, Van de Walle GR. Culture and characterisation of equine peripheral blood mesenchymal stromal cells.. Vet J 2013 Jan;195(1):107-13.
                      doi: 10.1016/j.tvjl.2012.05.006pubmed: 22717781google scholar: lookup
                    15. Koch TG, Heerkens T, Thomsen PD, Betts DH. Isolation of mesenchymal stem cells from equine umbilical cord blood.. BMC Biotechnol 2007 May 30;7:26.
                      doi: 10.1186/1472-6750-7-26pmc: PMC1904213pubmed: 17537254google scholar: lookup
                    16. Bieback K, Kern S, Klu00fcter H, Eichler H. Critical parameters for the isolation of mesenchymal stem cells from umbilical cord blood.. Stem Cells 2004;22(4):625-34.
                      doi: 10.1634/stemcells.22-4-625pubmed: 15277708google scholar: lookup
                    17. 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
                    18. De Schauwer C, Meyer E, Cornillie P, De Vliegher S, van de Walle GR, Hoogewijs M, Declercq H, Govaere J, Demeyere K, Cornelissen M, Van Soom A. Optimization of the isolation, culture, and characterization of equine umbilical cord blood mesenchymal stromal cells.. Tissue Eng Part C Methods 2011 Nov;17(11):1061-70.
                      doi: 10.1089/ten.tec.2011.0052pubmed: 21870941google scholar: lookup
                    19. Mitchell KE, Weiss ML, Mitchell BM, Martin P, Davis D, Morales L, Helwig B, Beerenstrauch M, Abou-Easa K, Hildreth T, Troyer D, Medicetty S. Matrix cells from Wharton's jelly form neurons and glia.. Stem Cells 2003;21(1):50-60.
                      doi: 10.1634/stemcells.21-1-50pubmed: 12529551google scholar: lookup
                    20. 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
                    21. 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.
                      pubmed: 22411893doi: 10.1002/cyto.a.22026google scholar: lookup
                    22. Bogaert L, Van Poucke M, De Baere C, Peelman L, Gasthuys F, Martens A. Selection of a set of reliable reference genes for quantitative real-time PCR in normal equine skin and in equine sarcoids.. BMC Biotechnol 2006 Apr 27;6:24.
                      doi: 10.1186/1472-6750-6-24pmc: PMC1484482pubmed: 16643647google scholar: lookup
                    23. Smits K, Goossens K, Van Soom A, Govaere J, Hoogewijs M, Vanhaesebrouck E, Galli C, Colleoni S, Vandesompele J, Peelman L. Selection of reference genes for quantitative real-time PCR in equine in vivo and fresh and frozen-thawed in vitro blastocysts.. BMC Res Notes 2009 Dec 11;2:246.
                      doi: 10.1186/1756-0500-2-246pmc: PMC2797813pubmed: 20003356google scholar: lookup
                    24. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.. Genome Biol 2002 Jun 18;3(7):RESEARCH0034.
                    25. Primer3. http://frodo.wi.mit.edu/primer3/
                    26. National Center for Biotechnology information. http://www.ncbi.nlm.nih.gov/
                    27. The UNAFold Web Server. http://frontend.bioinfo.rpi.edu/applications/mfold.
                    28. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments.. Clin Chem 2009 Apr;55(4):611-22.
                      doi: 10.1373/clinchem.2008.112797pubmed: 19246619google scholar: lookup
                    29. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data.. Genome Biol 2007;8(2):R19.
                      doi: 10.1186/gb-2007-8-2-r19pmc: PMC1852402pubmed: 17291332google scholar: lookup
                    30. 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
                    31. De Schauwer C, van de Walle GR, Piepers S, Hoogewijs MK, Govaere JL, Meyer E, van Soom A. Successful isolation of equine mesenchymal stromal cells from cryopreserved umbilical cord blood-derived mononuclear cell fractions.. Equine Vet J 2013 Jul;45(4):518-22.
                      doi: 10.1111/evj.12003pubmed: 23206252google scholar: lookup
                    32. Ahern BJ, Schaer TP, Terkhorn SP, Jackson KV, Mason NJ, Hankenson KD. Evaluation of equine peripheral blood apheresis product, bone marrow, and adipose tissue as sources of mesenchymal stem cells and their differentation potential.. Am J Vet Res 2011 Jan;72(1):127-33.
                      doi: 10.2460/ajvr.72.1.127pubmed: 21194345google scholar: lookup
                    33. Passeri S, Nocchi F, Lamanna R, Lapi S, Miragliotta V, Giannessi E, Abramo F, Stornelli MR, Matarazzo M, Plenteda D, Urciuoli P, Scatena F, Coli A. Isolation and expansion of equine umbilical cord-derived matrix cells (EUCMCs).. Cell Biol Int 2009 Jan;33(1):100-5.
                      doi: 10.1016/j.cellbi.2008.10.012pubmed: 18996215google scholar: lookup
                    34. 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
                    35. 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
                    36. 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
                    37. Dhar M, Neilsen N, Beatty K, Eaker S, Adair H, Geiser D. Equine peripheral blood-derived mesenchymal stem cells: isolation, identification, trilineage differentiation and effect of hyperbaric oxygen treatment.. Equine Vet J 2012 Sep;44(5):600-5.
                    38. 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
                    39. Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringdu00e9n O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells.. Exp Hematol 2003 Oct;31(10):890-6.
                      doi: 10.1016/S0301-472X(03)00110-3pubmed: 14550804google scholar: lookup
                    40. Loewendorf A, Csete M. Concise review: immunologic lessons from solid organ transplantation for stem cell-based therapies.. Stem Cells Transl Med 2013 Feb;2(2):136-42.
                      doi: 10.5966/sctm.2012-0125pmc: PMC3659757pubmed: 23349327google scholar: lookup
                    41. Klyushnenkova E, Mosca JD, Zernetkina V, Majumdar MK, Beggs KJ, Simonetti DW, Deans RJ, McIntosh KR. T cell responses to allogeneic human mesenchymal stem cells: immunogenicity, tolerance, and suppression.. J Biomed Sci 2005;12(1):47-57.
                      doi: 10.1007/s11373-004-8183-7pubmed: 15864738google scholar: lookup
                    42. Gu00f6therstru00f6m C, West A, Liden J, Uzunel M, Lahesmaa R, Le Blanc K. Difference in gene expression between human fetal liver and adult bone marrow mesenchymal stem cells.. Haematologica 2005 Aug;90(8):1017-26.
                      pubmed: 16079100
                    43. Chang CJ, Yen ML, Chen YC, Chien CC, Huang HI, Bai CH, Yen BL. Placenta-derived multipotent cells exhibit immunosuppressive properties that are enhanced in the presence of interferon-gamma.. Stem Cells 2006 Nov;24(11):2466-77.
                      doi: 10.1634/stemcells.2006-0071pubmed: 17071860google scholar: lookup
                    44. Chen PM, Yen ML, Liu KJ, Sytwu HK, Yen BL. Immunomodulatory properties of human adult and fetal multipotent mesenchymal stem cells.. J Biomed Sci 2011 Jul 18;18(1):49.
                      doi: 10.1186/1423-0127-18-49pmc: PMC3156728pubmed: 21762539google scholar: lookup
                    45. Hass R, Kasper C, Bu00f6hm S, Jacobs R. Different populations and sources of human mesenchymal stem cells (MSC): A comparison of adult and neonatal tissue-derived MSC.. Cell Commun Signal 2011 May 14;9:12.
                      doi: 10.1186/1478-811X-9-12pmc: PMC3117820pubmed: 21569606google scholar: lookup
                    46. Raicevic G, Najar M, Stamatopoulos B, De Bruyn C, Meuleman N, Bron D, Toungouz M, Lagneaux L. The source of human mesenchymal stromal cells influences their TLR profile as well as their functional properties.. Cell Immunol 2011;270(2):207-16.
                      doi: 10.1016/j.cellimm.2011.05.010pubmed: 21700275google scholar: lookup
                    47. Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, Grisanti S, Gianni AM. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli.. Blood 2002 May 15;99(10):3838-43.
                      doi: 10.1182/blood.V99.10.3838pubmed: 11986244google scholar: lookup

                    Citations

                    This article has been cited 21 times.
                    1. Stage HJ, Trappe S, Su00f6llig K, Trachsel DS, Kirsch K, Zieger C, Merle R, Aschenbach JR, Gehlen H. Multilineage Differentiation Potential of Equine Adipose-Derived Stromal/Stem Cells from Different Sources.. Animals (Basel) 2023 Apr 15;13(8).
                      doi: 10.3390/ani13081352pubmed: 37106915google scholar: lookup
                    2. Cequier A, Vu00e1zquez FJ, Romero A, Vitoria A, Bernad E, Garcu00eda-Martu00ednez M, Gascu00f3n I, Barrachina L, Rodellar C. The immunomodulation-immunogenicity balance of equine Mesenchymal Stem Cells (MSCs) is differentially affected by the immune cell response depending on inflammatory licensing and major histocompatibility complex (MHC) compatibility.. Front Vet Sci 2022;9:957153.
                      doi: 10.3389/fvets.2022.957153pubmed: 36337202google scholar: lookup
                    3. Heyman E, Meeremans M, Devriendt B, Olenic M, Chiers K, De Schauwer C. Validation of a color deconvolution method to quantify MSC tri-lineage differentiation across species.. Front Vet Sci 2022;9:987045.
                      doi: 10.3389/fvets.2022.987045pubmed: 36311666google scholar: lookup
                    4. Harman RM, Churchill KA, Parmar S, Van de Walle GR. Mesenchymal stromal cells isolated from chicken peripheral blood secrete bioactive factors with antimicrobial and regenerative properties.. Front Vet Sci 2022;9:949836.
                      doi: 10.3389/fvets.2022.949836pubmed: 36090169google scholar: lookup
                    5. Wang P, Deng Z, Li A, Li R, Huang W, Cui J, Chen S, Li B, Zhang S. u03b2-Catenin promotes long-term survival and angiogenesis of peripheral blood mesenchymal stem cells via the Oct4 signaling pathway.. Exp Mol Med 2022 Sep;54(9):1434-1449.
                      doi: 10.1038/s12276-022-00839-4pubmed: 36050404google scholar: lookup
                    6. Taylor SD, Serpa PBS, Santos AP, Hart KA, Vaughn SA, Moore GE, Mukhopadhyay A, Page AE. Effects of intravenous administration of peripheral blood-derived mesenchymal stromal cells after infusion of lipopolysaccharide in horses.. J Vet Intern Med 2022 Jul;36(4):1491-1501.
                      doi: 10.1111/jvim.16447pubmed: 35698909google scholar: lookup
                    7. Somal A, Bhat IA, Pandey S, Ansari MM, Indu B, Panda BSK, Bharti MK, Chandra V, Saikumar G, Sharma GT. Comparative analysis of the immunomodulatory potential of caprine fetal adnexa derived mesenchymal stem cells.. Mol Biol Rep 2021 May;48(5):3913-3923.
                      doi: 10.1007/s11033-021-06383-0pubmed: 34050503google scholar: lookup
                    8. Qu HM, Qu LP, Pan XZ, Mu LS. Upregulated miR-222 targets BCL2L11 and promotes apoptosis of mesenchymal stem cells in preeclampsia patients in response to severe hypoxia.. Int J Clin Exp Pathol 2018;11(1):110-119.
                      pubmed: 31938092
                    9. Merlo B, Teti G, Lanci A, Burk J, Mazzotti E, Falconi M, Iacono E. Comparison between adult and foetal adnexa derived equine post-natal mesenchymal stem cells.. BMC Vet Res 2019 Aug 2;15(1):277.
                      doi: 10.1186/s12917-019-2023-5pubmed: 31375144google scholar: lookup
                    10. 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
                    11. Hillmann A, Paebst F, Brehm W, Piehler D, Schubert S, Tu00e1rnok A, Burk J. A novel direct co-culture assay analyzed by multicolor flow cytometry reveals context- and cell type-specific immunomodulatory effects of equine mesenchymal stromal cells.. PLoS One 2019;14(6):e0218949.
                      doi: 10.1371/journal.pone.0218949pubmed: 31247035google scholar: lookup
                    12. Pessu00f4a 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
                    13. Cortu00e9s-Araya Y, Amilon K, Rink BE, Black G, Lisowski Z, Donadeu FX, Esteves CL. Comparison of Antibacterial and Immunological Properties of Mesenchymal Stem/Stromal Cells from Equine Bone Marrow, Endometrium, and Adipose Tissue.. Stem Cells Dev 2018 Nov 1;27(21):1518-1525.
                      doi: 10.1089/scd.2017.0241pubmed: 30044182google scholar: lookup
                    14. Desancu00e9 M, Contentin R, Bertoni L, Gomez-Leduc T, Branly T, Jacquet S, Betsch JM, Batho A, Legendre F, Audigiu00e9 F, Galu00e9ra 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
                    15. Somal A, Bhat IA, B I, Pandey S, Panda BS, Thakur N, Sarkar M, Chandra V, Saikumar G, Sharma GT. A Comparative Study of Growth Kinetics, In Vitro Differentiation Potential and Molecular Characterization of Fetal Adnexa Derived Caprine Mesenchymal Stem Cells.. PLoS One 2016;11(6):e0156821.
                      doi: 10.1371/journal.pone.0156821pubmed: 27257959google scholar: lookup
                    16. Quattrocelli M, Giacomazzi G, Broeckx SY, Ceelen L, Bolca S, Spaas JH, Sampaolesi M. Equine-Induced Pluripotent Stem Cells Retain Lineage Commitment Toward Myogenic and Chondrogenic Fates.. Stem Cell Reports 2016 Jan 12;6(1):55-63.
                      doi: 10.1016/j.stemcr.2015.12.005pubmed: 26771353google scholar: lookup
                    17. Shikh Alsook MK, Gabriel A, Piret J, Waroux O, Tonus C, Connan D, Baise E, Antoine N. Tissues from equine cadaver ligaments up to 72u00a0hours of post-mortem: a promising reservoir of stem cells.. Stem Cell Res Ther 2015 Dec 18;6:253.
                      doi: 10.1186/s13287-015-0250-7pubmed: 26684484google scholar: lookup
                    18. Tessier L, Bienzle D, Williams LB, Koch TG. Phenotypic and immunomodulatory properties of equine cord blood-derived mesenchymal stromal cells.. PLoS One 2015;10(4):e0122954.
                      doi: 10.1371/journal.pone.0122954pubmed: 25902064google scholar: lookup
                    19. Bussche L, Harman RM, Syracuse BA, Plante EL, Lu YC, Curtis TM, Ma M, Van de Walle GR. Microencapsulated equine mesenchymal stromal cells promote cutaneous wound healing in vitro.. Stem Cell Res Ther 2015 Apr 11;6(1):66.
                      doi: 10.1186/s13287-015-0037-xpubmed: 25889766google scholar: lookup
                    20. Bussche L, Van de Walle GR. Peripheral Blood-Derived Mesenchymal Stromal Cells Promote Angiogenesis via Paracrine Stimulation of Vascular Endothelial Growth Factor Secretion in the Equine Model.. Stem Cells Transl Med 2014 Dec;3(12):1514-25.
                      doi: 10.5966/sctm.2014-0138pubmed: 25313202google scholar: lookup
                    21. Paterson YZ, Rash N, Garvican ER, Paillot R, Guest DJ. Equine mesenchymal stromal cells and embryo-derived stem cells are immune privileged in vitro.. Stem Cell Res Ther 2014 Jul 30;5(4):90.
                      doi: 10.1186/scrt479pubmed: 25080326google scholar: lookup