Stem cells and development2017; 26(13); 964-972; doi: 10.1089/scd.2017.0017

Equine Mesenchymal Stromal Cells Retain a Pericyte-Like Phenotype.

Abstract: Mesenchymal stem/stromal cells (MSCs) have been used in human and equine regenerative medicine, and interest in exploiting their potential has increased dramatically over the years. Despite significant effort to characterize equine MSCs, the actual origin of these cells and how much of their native phenotype is maintained in culture have not been determined. In this study, we investigated the relationship between MSCs, derived from adipose tissue (AT) and bone marrow (BM), and pericytes in the horse. Both pericyte (CD146, NG2, and αSMA) and MSC (CD29, CD90, and CD73) markers were detected in equine AT and colocalized around blood vessels. Importantly, as assessed by flow cytometry, both pericyte (CD146, NG2, and αSMA) and MSC (CD29, CD44, CD90, and CD105) markers were present in a majority (≥90%) of cells in cultures of AT-MSCs and BM-MSCs; however, levels of pericyte markers were variable within each of those populations. Moreover, the expression of pericyte markers was maintained for at least eight passages in both AT-MSCs and BM-MSCs. Hematopoietic (CD45) and endothelial (CD144) markers were also detected at low levels in MSCs by quantitative polymerase chain reaction (qPCR). Finally, in coculture experiments, AT-MSCs closely associated with networks produced by endothelial cells, resembling the natural perivascular location of pericytes in vivo. Our results indicate that equine MSCs originate from perivascular cells and moreover maintain a pericyte-like phenotype in culture. Therefore, we suggest that, in addition to classical MSC markers, pericyte markers such as CD146 could be used when assessing and characterizing equine MSCs.
Publication Date: 2017-05-09 PubMed ID: 28376684PubMed Central: PMC5510672DOI: 10.1089/scd.2017.0017Google Scholar: Lookup
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  • Journal Article

Summary

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The research examines the origin and nature of equine Mesenchymal stem/stromal cells (MSCs), finding that these cells derive from perivascular cells and maintain a pericyte-like phenotype in culture. The authors suggest considering pericyte markers like CD146 for assessing and characterizing these cells.

Study Objectives and Approach

  • The main aim of the study was to ascertain the actual origin of equine Mesenchymal stem/stromal cells (MSCs), which have become increasingly important in human and equine regenerative medicine.
  • The researchers were also interested in understanding how much of the cells’ original phenotype is kept when in culture.
  • To achieve this, the researchers studied MSCs derived from adipose tissue (AT) and bone marrow (BM), specifically examining the relationship between these cells and pericytes in horses.

Methodology and Key Findings

  • Markers for both pericytes (CD146, NG2, and αSMA) and MSCs (CD29, CD90, and CD73) were found in equine AT and colocalized around blood vessels, indicating a close relationship between pericytes and MSCs.
  • Flow cytometry revealed that the majority (90% or more) of cells in AT-MSC and BM-MSC cultures possessed both pericyte and MSC markers.
  • The levels of pericyte markers were found to be inconsistent within each of those cell groups – AT-MSCs and BM-MSCs.
  • The research discovered that the expression of pericyte markers was preserved through at least eight passages in the AT-MSC and BM-MSC cultures.
  • Hematopoietic (CD45) and endothelial (CD144) markers were also present at low levels in MSCs, as revealed by quantitative polymerase chain reaction (qPCR).
  • In coculture experiments, AT-MSCs were seen aligning closely with networks produced by endothelial cells, which resembles the natural perivascular location of pericytes within a body – further supporting their origin from perivascular cells.

Implications

  • These findings suggest that equine MSCs retain a pericyte-like phenotype in culture and originate from perivascular cells.
  • As such, the researchers suggest that pericyte markers like CD146 could be used alongside classical MSC markers to assess and characterize equine MSCs more accurately.
  • This information could be crucial in the fields of human and equine regenerative medicine, potentially leading to improved procedures and treatments.

Cite This Article

APA
Esteves CL, Sheldrake TA, Dawson L, Menghini T, Rink BE, Amilon K, Khan N, Pu00e9ault B, Donadeu FX. (2017). Equine Mesenchymal Stromal Cells Retain a Pericyte-Like Phenotype. Stem Cells Dev, 26(13), 964-972. https://doi.org/10.1089/scd.2017.0017

Publication

ISSN: 1557-8534
NlmUniqueID: 101197107
Country: United States
Language: English
Volume: 26
Issue: 13
Pages: 964-972

Researcher Affiliations

Esteves, Cristina L
  • 1 The Roslin Institute, University of Edinburgh , Edinburgh, United Kingdom .
Sheldrake, Tara A
  • 1 The Roslin Institute, University of Edinburgh , Edinburgh, United Kingdom .
Dawson, Lucy
  • 1 The Roslin Institute, University of Edinburgh , Edinburgh, United Kingdom .
Menghini, Timothy
  • 1 The Roslin Institute, University of Edinburgh , Edinburgh, United Kingdom .
Rink, Burgunde Elisabeth
  • 1 The Roslin Institute, University of Edinburgh , Edinburgh, United Kingdom .
Amilon, Karin
  • 1 The Roslin Institute, University of Edinburgh , Edinburgh, United Kingdom .
Khan, Nusrat
  • 2 Centre for Regenerative Medicine, University of Edinburgh , Edinburgh, United Kingdom .
Pu00e9ault, Bruno
  • 2 Centre for Regenerative Medicine, University of Edinburgh , Edinburgh, United Kingdom .
  • 3 Orthopaedic Hospital Research Centre, University of California , Los Angeles, California.
Donadeu, Francesc Xavier
  • 1 The Roslin Institute, University of Edinburgh , Edinburgh, United Kingdom .

MeSH Terms

  • Adipose Tissue / metabolism
  • Adipose Tissue / parasitology
  • Animals
  • Antigens, CD / genetics
  • Antigens, CD / metabolism
  • Blood Vessels / metabolism
  • Bone Marrow Cells / metabolism
  • CD146 Antigen / genetics
  • CD146 Antigen / metabolism
  • Cadherins / genetics
  • Cadherins / metabolism
  • Coculture Techniques
  • Flow Cytometry
  • Horses
  • Humans
  • Leukocyte Common Antigens / genetics
  • Leukocyte Common Antigens / metabolism
  • Mesenchymal Stem Cells / metabolism
  • Pericytes / metabolism
  • Phenotype
  • Regenerative Medicine

Grant Funding

  • G1000816 / Medical Research Council
  • Biotechnology and Biological Sciences Research Council

Conflict of Interest Statement

B.P. is coinventor of human perivascular stem cell-related patents filed from University of California, Los Angeles. The other authors declare no competing interests.

References

This article includes 42 references
  1. Smith RK, Garvican ER, Fortier LA. The current 'state of play' of regenerative medicine in horses: what the horse can tell the human.. Regen Med 2014;9(5):673-85.
    pubmed: 25372081doi: 10.2217/rme.14.42google scholar: lookup
  2. Donadeu FX. and Esteves CL. (2016). Stem cells and equine health. www.eurostemcell.org/factsheet/stem-cells-and-equine-health
  3. Pacini S, Spinabella S, Trombi L, Fazzi R, Galimberti S, Dini F, Carlucci F, Petrini M. Suspension of bone marrow-derived undifferentiated mesenchymal stromal cells for repair of superficial digital flexor tendon in race horses.. Tissue Eng 2007 Dec;13(12):2949-55.
    pubmed: 17919069doi: 10.1089/ten.2007.0108google scholar: lookup
  4. Smith RK. Mesenchymal stem cell therapy for equine tendinopathy.. Disabil Rehabil 2008;30(20-22):1752-8.
    pubmed: 18608378doi: 10.1080/09638280701788241google scholar: lookup
  5. Gittel C, Burk J, Ribitsch I. and Brehm W. (2011). Efficiency of adipogenic differentiation methods in mesenchymal stromal cells from diverse sources. Regen Med 6:203
  6. Godwin EE, Young NJ, Dudhia J, Beamish IC, Smith RK. Implantation of bone marrow-derived mesenchymal stem cells demonstrates improved outcome in horses with overstrain injury of the superficial digital flexor tendon.. Equine Vet J 2012 Jan;44(1):25-32.
  7. Smith RK, Korda M, Blunn GW, Goodship AE. Isolation and implantation of autologous equine mesenchymal stem cells from bone marrow into the superficial digital flexor tendon as a potential novel treatment.. Equine Vet J 2003 Jan;35(1):99-102.
    pubmed: 12553472doi: 10.2746/042516403775467388google scholar: lookup
  8. 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.
    pubmed: 17692415doi: 10.1016/j.tibtech.2007.07.009google 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.
    pubmed: 18267891doi: 10.2746/042516408X276942google scholar: lookup
  10. Crovace A, Lacitignola L, Rossi G, Francioso E. Histological and immunohistochemical evaluation of autologous cultured bone marrow mesenchymal stem cells and bone marrow mononucleated cells in collagenase-induced tendinitis of equine superficial digital flexor tendon.. Vet Med Int 2010;2010:250978.
    pmc: PMC2859019pubmed: 20445779doi: 10.4061/2010/250978google scholar: lookup
  11. Schnabel LV, Fortier LA, McIlwraith CW, Nobert KM. Therapeutic use of stem cells in horses: which type, how, and when?. Vet J 2013 Sep;197(3):570-7.
    pubmed: 23778257doi: 10.1016/j.tvjl.2013.04.018google scholar: lookup
  12. Frisbie DD, Smith RK. Clinical update on the use of mesenchymal stem cells in equine orthopaedics.. Equine Vet J 2010 Jan;42(1):86-9.
    pubmed: 20121921doi: 10.2746/042516409X477263google scholar: lookup
  13. Clegg PD, Pinchbeck GL. Evidence-based medicine and stem cell therapy: how do we know such technologies are safe and efficacious?. Vet Clin North Am Equine Pract 2011 Aug;27(2):373-82.
    pubmed: 21872765doi: 10.1016/j.cveq.2011.04.002google scholar: lookup
  14. Taylor SE, Clegg PD. Collection and propagation methods for mesenchymal stromal cells.. Vet Clin North Am Equine Pract 2011 Aug;27(2):263-74.
    pubmed: 21872758doi: 10.1016/j.cveq.2011.05.003google scholar: lookup
  15. 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.
    pubmed: 16923606doi: 10.1080/14653240600855905google scholar: lookup
  16. 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 jointu00a0statement of the International Federation for Adipose Therapeutics and Science (IFATS) and the International Society for Cellular Therapyu00a0(ISCT).. Cytotherapy 2013 Jun;15(6):641-8.
    pmc: PMC3979435pubmed: 23570660doi: 10.1016/j.jcyt.2013.02.006google 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.
  18. 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.
    pmc: PMC3138180pubmed: 19604071doi: 10.1089/scd.2009.0091google scholar: lookup
  19. 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
  20. Ranera B, Lyahyai J, Romero A, Vu00e1zquez FJ, Remacha AR, Bernal ML, Zaragoza P, Rodellar C, Martu00edn-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.
    pubmed: 21782255doi: 10.1016/j.vetimm.2011.06.033google scholar: lookup
  21. 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
  22. Armulik A, Genovu00e9 G, Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises.. Dev Cell 2011 Aug 16;21(2):193-215.
    pubmed: 21839917doi: 10.1016/j.devcel.2011.07.001google scholar: lookup
  23. Chen WC, Park TS, Murray IR, Zimmerlin L, Lazzari L, Huard J, Pu00e9ault B. Cellular kinetics of perivascular MSC precursors.. Stem Cells Int 2013;2013:983059.
    pmc: PMC3760099pubmed: 24023546doi: 10.1155/2013/983059google scholar: lookup
  24. Murray IR, West CC, Hardy WR, James AW, Park TS, Nguyen A, Tawonsawatruk T, Lazzari L, Soo C, Pu00e9ault B. Natural history of mesenchymal stem cells, from vessel walls to culture vessels.. Cell Mol Life Sci 2014 Apr;71(8):1353-74.
    pubmed: 24158496doi: 10.1007/s00018-013-1462-6google scholar: lookup
  25. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L, Norotte C, Teng PN, Traas J, Schugar R, Deasy BM, Badylak S, Buhring HJ, Giacobino JP, Lazzari L, Huard J, Pu00e9ault B. A perivascular origin for mesenchymal stem cells in multiple human organs.. Cell Stem Cell 2008 Sep 11;3(3):301-13.
    pubmed: 18786417doi: 10.1016/j.stem.2008.07.003google scholar: lookup
  26. Esteves CL, Kelly V, Bu00e9gay V, Lillico SG, Leutz A, Seckl JR, Chapman KE. Stable conditional expression and effect of C/ebpu03b2-LIP in adipocytes using the pSLIK system.. J Mol Endocrinol 2013;51(1):91-8.
    pmc: PMC3672996pubmed: 23620165doi: 10.1530/JME-13-0029google scholar: lookup
  27. Crisan M, Chen CW, Corselli M, Andriolo G, Lazzari L, Pu00e9ault B. Perivascular multipotent progenitor cells in human organs.. Ann N Y Acad Sci 2009 Sep;1176:118-23.
  28. Sobiesiak M, Sivasubramaniyan K, Hermann C, Tan C, Orgel M, Treml S, Cerabona F, de Zwart P, Ochs U, Mu00fcller CA, Gargett CE, Kalbacher H, Bu00fchring HJ. The mesenchymal stem cell antigen MSCA-1 is identical to tissue non-specific alkaline phosphatase.. Stem Cells Dev 2010 May;19(5):669-77.
    pubmed: 19860546doi: 10.1089/scd.2009.0290google scholar: lookup
  29. Zimmerlin L, Donnenberg VS, Rubin JP, Donnenberg AD. Mesenchymal markers on human adipose stem/progenitor cells.. Cytometry A 2013 Jan;83(1):134-40.
    pmc: PMC4157311pubmed: 23184564doi: 10.1002/cyto.a.22227google scholar: lookup
  30. Zimmerlin L, Donnenberg VS, Pfeifer ME, Meyer EM, Pu00e9ault B, Rubin JP, Donnenberg AD. Stromal vascular progenitors in adult human adipose tissue.. Cytometry A 2010 Jan;77(1):22-30.
    pmc: PMC4148047pubmed: 19852056doi: 10.1002/cyto.a.20813google scholar: lookup
  31. Nehls V, Drenckhahn D. The versatility of microvascular pericytes: from mesenchyme to smooth muscle?. Histochemistry 1993 Jan;99(1):1-12.
    pubmed: 8468190doi: 10.1007/BF00268014google scholar: lookup
  32. Li Q, Wang Z. Influence of mesenchymal stem cells with endothelial progenitor cells in co-culture on osteogenesis and angiogenesis: an in vitro study.. Arch Med Res 2013 Oct;44(7):504-13.
    pubmed: 24120387doi: 10.1016/j.arcmed.2013.09.009google scholar: lookup
  33. Aguirre A, Planell JA, Engel E. Dynamics of bone marrow-derived endothelial progenitor cell/mesenchymal stem cell interaction in co-culture and its implications in angiogenesis.. Biochem Biophys Res Commun 2010 Sep 17;400(2):284-91.
    pubmed: 20732306doi: 10.1016/j.bbrc.2010.08.073google scholar: lookup
  34. Chen WC, Baily JE, Corselli M, Du00edaz ME, Sun B, Xiang G, Gray GA, Huard J, Pu00e9ault B. Human myocardial pericytes: multipotent mesodermal precursors exhibiting cardiac specificity.. Stem Cells 2015 Feb;33(2):557-73.
    pmc: PMC4762368pubmed: 25336400doi: 10.1002/stem.1868google scholar: lookup
  35. Blocki A, Wang Y, Koch M, Peh P, Beyer S, Law P, Hui J, Raghunath M. Not all MSCs can act as pericytes: functional in vitro assays to distinguish pericytes from other mesenchymal stem cells in angiogenesis.. Stem Cells Dev 2013 Sep 1;22(17):2347-55.
    pmc: PMC3749721pubmed: 23600480doi: 10.1089/scd.2012.0415google scholar: lookup
  36. Russell KC, Phinney DG, Lacey MR, Barrilleaux BL, Meyertholen KE, O'Connor KC. In vitro high-capacity assay to quantify the clonal heterogeneity in trilineage potential of mesenchymal stem cells reveals a complex hierarchy of lineage commitment.. Stem Cells 2010 Apr;28(4):788-98.
    pubmed: 20127798doi: 10.1002/stem.312google scholar: lookup
  37. Barberini DJ, Freitas NP, Magnoni MS, Maia L, Listoni AJ, Heckler MC, Sudano MJ, Golim MA, da Cruz Landim-Alvarenga F, Amorim RM. Equine mesenchymal stem cells from bone marrow, adipose tissue and umbilical cord: immunophenotypic characterization and differentiation potential.. Stem Cell Res Ther 2014 Feb 21;5(1):25.
    pmc: PMC4055040pubmed: 24559797doi: 10.1186/scrt414google scholar: lookup
  38. Paebst F, Piehler D, Brehm W, Heller S, Schroeck C, Tu00e1rnok A, Burk J. Comparative immunophenotyping of equine multipotent mesenchymal stromal cells: an approach toward a standardized definition.. Cytometry A 2014 Aug;85(8):678-87.
    pubmed: 24894974doi: 10.1002/cyto.a.22491google scholar: lookup
  39. Ranera B, Ordovu00e1s L, Lyahyai J, Bernal ML, Fernandes F, Remacha AR, Romero A, Vu00e1zquez FJ, Osta R, Cons C, Varona L, Zaragoza P, Martu00edn-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.
  40. Braun J, Kurtz A, Barutcu N, Bodo J, Thiel A, Dong J. Concerted regulation of CD34 and CD105 accompanies mesenchymal stromal cell derivation from human adventitial stromal cell.. Stem Cells Dev 2013 Mar 1;22(5):815-27.
    pubmed: 23072708doi: 10.1089/scd.2012.0263google scholar: lookup
  41. Choudhary RK. Mammary stem cells: expansion and animal productivity.. J Anim Sci Biotechnol 2014;5(1):36.
    pmc: PMC4107933pubmed: 25057352doi: 10.1186/2049-1891-5-36google scholar: lookup
  42. Kassem M, Bianco P. Skeletal stem cells in space and time.. Cell 2015 Jan 15;160(1-2):17-9.
    pubmed: 25594172doi: 10.1016/j.cell.2014.12.034google scholar: lookup

Citations

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  1. Phyo H, Aburza A, Mellanby K, Esteves CL. Characterization of canine adipose- and endometrium-derived Mesenchymal Stem/Stromal Cells and response to lipopolysaccharide.. Front Vet Sci 2023;10:1180760.
    doi: 10.3389/fvets.2023.1180760pubmed: 37275605google scholar: lookup
  2. Zhang Y, Yi Y, Xiao X, Hu L, Xu J, Zheng D, Koc HC, Chan UI, Meng Y, Lu L, Liu W, Xu X, Shao N, Cheung ECW, Xu RH, Chen G. Definitive Endodermal Cells Supply an in vitro Source of Mesenchymal Stem/Stromal Cells.. Commun Biol 2023 May 1;6(1):476.
    doi: 10.1038/s42003-023-04810-5pubmed: 37127734google scholar: lookup
  3. Heilen LB, Rou00dfgardt 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
  4. Zamith Cunha R, Zannoni A, Salamanca G, De Silva M, Rinnovati R, Gramenzi A, Forni M, Chiocchetti R. Expression of cannabinoid (CB1 and CB2) and cannabinoid-related receptors (TRPV1, GPR55, and PPARu03b1) in the synovial membrane of the horse metacarpophalangeal joint.. Front Vet Sci 2023;10:1045030.
    doi: 10.3389/fvets.2023.1045030pubmed: 36937015google scholar: lookup
  5. Hagen A, Niebert S, Brandt VP, Holland H, Melzer M, Wehrend A, Burk J. Functional properties of equine adipose-derived mesenchymal stromal cells cultured with equine platelet lysate.. Front Vet Sci 2022;9:890302.
    doi: 10.3389/fvets.2022.890302pubmed: 36016806google scholar: lookup
  6. Jones OY, Yeralan S. Is Long COVID a State of Systemic Pericyte Disarray?. J Clin Med 2022 Jan 24;11(3).
    doi: 10.3390/jcm11030572pubmed: 35160024google scholar: lookup
  7. 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
  8. Zha K, Tian G, Yang Z, Sun Z, Liu S, Guo Q. [The role of CD146 in mesenchymal stem cells].. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi 2021 Feb 15;35(2):227-233.
    doi: 10.7507/1002-1892.202005110pubmed: 33624479google scholar: lookup
  9. Weatherall EL, Avilkina V, Cortes-Araya Y, Dan-Jumbo S, Stenhouse C, Donadeu FX, Esteves CL. Differentiation Potential of Mesenchymal Stem/Stromal Cells Is Altered by Intrauterine Growth Restriction.. Front Vet Sci 2020;7:558905.
    doi: 10.3389/fvets.2020.558905pubmed: 33251256google scholar: lookup
  10. Mannino G, Gennuso F, Giurdanella G, Conti F, Drago F, Salomone S, Furno DL, Bucolo C, Giuffrida R. Pericyte-like differentiation of human adipose-derived mesenchymal stem cells: An in vitro study.. World J Stem Cells 2020 Oct 26;12(10):1152-1170.
    doi: 10.4252/wjsc.v12.i10.1152pubmed: 33178398google scholar: lookup
  11. Kamm JL, Parlane NA, Riley CB, Gee EK, Dittmer KE, McIlwraith CW. Blood type and breed-associated differences in cell marker expression on equine bone marrow-derived mesenchymal stem cells including major histocompatibility complex class II antigen expression.. PLoS One 2019;14(11):e0225161.
    doi: 10.1371/journal.pone.0225161pubmed: 31747418google scholar: lookup
  12. Nakagomi T, Takagi T, Beppu M, Yoshimura S, Matsuyama T. Neural regeneration by regionally induced stem cells within post-stroke brains: Novel therapy perspectives for stroke patients.. World J Stem Cells 2019 Aug 26;11(8):452-463.
    doi: 10.4252/wjsc.v11.i8.452pubmed: 31523366google scholar: lookup
  13. Stephens CJ, Spector JA, Butcher JT. Biofabrication of thick vascularized neo-pedicle flaps for reconstructive surgery.. Transl Res 2019 Sep;211:84-122.
    doi: 10.1016/j.trsl.2019.05.003pubmed: 31170376google scholar: lookup
  14. Meyers CA, Casamitjana J, Chang L, Zhang L, James AW, Pu00e9ault B. Pericytes for Therapeutic Bone Repair.. Adv Exp Med Biol 2018;1109:21-32.
    doi: 10.1007/978-3-030-02601-1_3pubmed: 30523587google scholar: lookup
  15. 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
  16. Takagi T, Yoshimura S, Sakuma R, Nakano-Doi A, Matsuyama T, Nakagomi T. Novel Regenerative Therapies Based on Regionally Induced Multipotent Stem Cells in Post-Stroke Brains: Their Origin, Characterization, and Perspective.. Transl Stroke Res 2017 Dec;8(6):515-528.
    doi: 10.1007/s12975-017-0556-0pubmed: 28744717google scholar: lookup