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Stem cell research & therapy2017; 8(1); 80; doi: 10.1186/s13287-017-0525-2

Isolation and characterization of equine native MSC populations.

Abstract: In contrast to humans in which mesenchymal stem/stromal cell (MSC) therapies are still largely in the clinical trial phase, MSCs have been used therapeutically in horses for over 15 years, thus constituting a valuable preclinical model for humans. In human tissues, MSCs have been shown to originate from perivascular cells, namely pericytes and adventitial cells, which are identified by the presence of the cell surface markers CD146 and CD34, respectively. In contrast, the origin of MSCs in equine tissues has not been established, preventing the isolation and culture of defined cell populations in that species. Moreover, a comparison between perivascular CD146 and CD34 cell populations has not been performed in any species. Immunohistochemistry was used to identify adventitial cells (CD34) and pericytes (CD146) and to determine their localization in relation to MSCs in equine tissues. Isolation of CD34 (CD34/CD146/CD144/CD45) and CD146 (CD146/CD34/CD144/CD45) cell fractions from equine adipose tissue was achieved by fluorescence-activated cell sorting. The isolated cell fractions were cultured and analyzed for the expression of MSC markers, using qPCR and flow cytometry, and for the ability to undergo trilineage differentiation. Angiogenic properties were analyzed in vivo using a chorioallantoic membrane (CAM) assay. Both CD34 and CD146 cells displayed typical MSC features, namely growth in uncoated tissue culture dishes, clonal growth when seeded at low density, expression of typical MSC markers, and multipotency shown by the capacity for trilineage differentiation. Of note, CD146 cells were distinctly angiogenic compared with CD34 and non-sorted cells (conventional MSCs), demonstrated by the induction of blood vessels in a CAM assay, expression of elevated levels of VEGFA and ANGPT1, and association with vascular networks in cocultures with endothelial cells, indicating that CD146 cells maintain a pericyte phenotype in culture. This study reports for the first time the successful isolation and culture of CD146 and CD34 cell populations from equine tissues. Characterization of these cells evidenced their distinct properties and MSC-like phenotype, and identified CD146 cells as distinctly angiogenic, which may provide a novel source for enhanced regenerative therapies.
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Publication Date: 2017-04-18 PubMed ID: 28420427PubMed Central: PMC5395828DOI: 10.1186/s13287-017-0525-2Google 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 article discusses a research that studies the origin of Mesenchymal Stem/Stromal Cells (MSCs) in equines or horses. The researchers have successfully identified and characterised equine MSCs that originate from perivascular cells, a feature previously unidentified in equines. Notably, they found that CD146 cells, a type of perivascular cell, are distinctly angiogenic, suggesting possible applications in improved regenerative therapies.

Objective and Methodology

  • This research aimed to understand the origin of mesenchymal stem/stromal cells (MSCs) in horses, which was unknown till now. This is important to enable the isolation and culture of defined cell populations in horses.
  • The research methodology involved the use of immunohistochemistry to identify perivascular cells, specifically pericytes (CD146) and adventitial cells (CD34) in horse tissues. These cells were compared for the first time in any species.
  • Fluorescence-activated cell sorting was used to isolate CD34 and CD146 cell fractions from equine adipose tissue.
  • The isolated cell fractions were cultured and analysed for the expression of MSC marker cells, their capacity for trilineage differentiation, and angiogenic properties.

Results and Findings

  • The research found that both CD34 and CD146 cells displayed typical characteristics of MSCs, including growth in uncoated tissue culture dishes, clonal growth when seeded at low density, and expression of typical MSC markers. They also showed multipotency – the capacity for trilineage differentiation.
  • Significantly, CD146 cells were found to be distinctly angiogenic compared to CD34 and non-sorted cells (conventional MSCs). Angiogenic cells stimulate the growth of new blood vessels.
  • The angiogenic nature of CD146 cells was demonstrated by the induction of blood vessels in a chorioallantoic membrane (CAM) assay, expression of elevated levels of VEGFA and ANGPT1, and association with vascular networks in cocultures with endothelial cells. This indicates that CD146 cells maintain a pericyte phenotype in culture.

Significance and Implications

  • This research constitutes the first successful isolation and culture of CD146 and CD34 cell populations from equine tissues.
  • The distinct properties and MSC-like phenotype of these cells were characterized and CD146 cells identified as distinctly angiogenic.
  • The angiogenic CD146 cells could provide a novel source for enhanced regenerative therapies, thus having significant implications for veterinary medicine and potential parallels in human medicine.

Cite This Article

APA
Esteves CL, Sheldrake TA, Mesquita SP, Pesántez JJ, Menghini T, Dawson L, Péault B, Donadeu FX. (2017). Isolation and characterization of equine native MSC populations. Stem Cell Res Ther, 8(1), 80. https://doi.org/10.1186/s13287-017-0525-2

Publication

Stem cell research & therapy
ISSN: 1757-6512
NlmUniqueID: 101527581
Country: England
Language: English
Volume: 8
Issue: 1
Pages: 80
PII: 80

Researcher Affiliations

Esteves, Cristina L
  • The Roslin Institute, University of Edinburgh, Edinburgh, UK. cristina.esteves@roslin.ed.ac.uk.
  • The Roslin Institute, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG, UK. cristina.esteves@roslin.ed.ac.uk.
Sheldrake, Tara A
  • The Roslin Institute, University of Edinburgh, Edinburgh, UK.
Mesquita, Simone P
  • The Roslin Institute, University of Edinburgh, Edinburgh, UK.
Pesántez, Juan J
  • The Roslin Institute, University of Edinburgh, Edinburgh, UK.
Menghini, Timothy
  • The Roslin Institute, University of Edinburgh, Edinburgh, UK.
Dawson, Lucy
  • The Roslin Institute, University of Edinburgh, Edinburgh, UK.
Péault, Bruno
  • Centre for Regenerative Medicine, University of Edinburgh, Edinburgh, UK.
  • Orthopaedic Hospital Research Centre, University of California, Los Angeles, CA, USA.
Donadeu, F Xavier
  • The Roslin Institute, University of Edinburgh, Edinburgh, UK.

MeSH Terms

  • Adipose Tissue / cytology
  • Angiopoietin-1 / genetics
  • Angiopoietin-1 / metabolism
  • Animals
  • Antigens, CD34 / genetics
  • Antigens, CD34 / metabolism
  • CD146 Antigen / genetics
  • CD146 Antigen / metabolism
  • Cells, Cultured
  • Horses
  • Mesenchymal Stem Cells / cytology
  • Mesenchymal Stem Cells / metabolism
  • Pericytes / cytology
  • Pericytes / metabolism
  • Primary Cell Culture / veterinary
  • Vascular Endothelial Growth Factor A / genetics
  • Vascular Endothelial Growth Factor A / metabolism

Grant Funding

  • G1000816 / Medical Research Council

References

This article includes 53 references
  1. Donadeu FX, Esteves CL. Stem cells and equine health. Euro Stem Cells 2015.
  2. 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.
    doi: 10.2217/rme.14.42pubmed: 25372081google scholar: lookup
  3. 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.
    doi: 10.1002/cyto.a.22216pubmed: 23081833google scholar: lookup
  4. Ranera B, Barry F. A horse of a different color.. Cytometry A 2014 Aug;85(8):658-9.
    doi: 10.1002/cyto.a.22496pubmed: 24953483google scholar: lookup
  5. Brehm W, Burk J, Delling U. Application of stem cells for the treatment of joint disease in horses.. Methods Mol Biol 2014;1213:215-28.
    doi: 10.1007/978-1-4939-1453-1_18pubmed: 25173386google scholar: lookup
  6. Donadeu FX, Esteves CL. Prospects and Challenges of Induced Pluripotent Stem Cells in Equine Health.. Front Vet Sci 2015;2:59.
    doi: 10.3389/fvets.2015.00059pmc: PMC4672244pubmed: 26664986google scholar: lookup
  7. Breton A, Sharma R, Diaz AC, Parham AG, Graham A, Neil C, Whitelaw CB, Milne E, Donadeu FX. Derivation and characterization of induced pluripotent stem cells from equine fibroblasts.. Stem Cells Dev 2013 Feb 15;22(4):611-21.
    doi: 10.1089/scd.2012.0052pmc: PMC3564467pubmed: 22897112google scholar: lookup
  8. Sharma R, Livesey MR, Wyllie DJ, Proudfoot C, Whitelaw CB, Hay DC, Donadeu FX. Generation of functional neurons from feeder-free, keratinocyte-derived equine induced pluripotent stem cells.. Stem Cells Dev 2014 Jul 1;23(13):1524-34.
    doi: 10.1089/scd.2013.0565pubmed: 24548115google scholar: lookup
  9. 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
  10. Smith RK. Mesenchymal stem cell therapy for equine tendinopathy.. Disabil Rehabil 2008;30(20-22):1752-8.
    doi: 10.1080/09638280701788241pubmed: 18608378google scholar: lookup
  11. 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
  12. 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.
    doi: 10.1016/j.theriogenology.2010.11.008pubmed: 21196039google scholar: lookup
  13. Esteves CL, Sharma R, Dawson L, Taylor SE, Pearson G, Keen JA, McDonald K, Aurich C, Donadeu FX. Expression of putative markers of pluripotency in equine embryonic and adult tissues.. Vet J 2014 Dec;202(3):533-5.
    doi: 10.1016/j.tvjl.2014.08.026pubmed: 25241949google scholar: lookup
  14. Sah RL, Ratcliffe A. Translational models for musculoskeletal tissue engineering and regenerative medicine.. Tissue Eng Part B Rev 2010 Feb;16(1):1-3.
    pmc: PMC2865991pubmed: 19905871doi: 10.1089/ten.teb.2009.0726google scholar: lookup
  15. 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, Péault B. A perivascular origin for mesenchymal stem cells in multiple human organs.. Cell Stem Cell 2008 Sep 11;3(3):301-13.
    doi: 10.1016/j.stem.2008.07.003pubmed: 18786417google scholar: lookup
  16. Crisan M, Chen CW, Corselli M, Andriolo G, Lazzari L, Péault B. Perivascular multipotent progenitor cells in human organs.. Ann N Y Acad Sci 2009 Sep;1176:118-23.
    doi: 10.1111/j.1749-6632.2009.04967.xpubmed: 19796239google scholar: lookup
  17. Corselli M, Chen CW, Sun B, Yap S, Rubin JP, Péault B. The tunica adventitia of human arteries and veins as a source of mesenchymal stem cells.. Stem Cells Dev 2012 May 20;21(8):1299-308.
    doi: 10.1089/scd.2011.0200pmc: PMC3353742pubmed: 21861688google scholar: lookup
  18. 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
  19. 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
  20. James AW, Zara JN, Corselli M, Askarinam A, Zhou AM, Hourfar A, Nguyen A, Megerdichian S, Asatrian G, Pang S, Stoker D, Zhang X, Wu B, Ting K, Péault B, Soo C. An abundant perivascular source of stem cells for bone tissue engineering.. Stem Cells Transl Med 2012 Sep;1(9):673-84.
    doi: 10.5966/sctm.2012-0053pmc: PMC3659737pubmed: 23197874google scholar: lookup
  21. Tawonsawatruk T, West CC, Murray IR, Soo C, Péault B, Simpson AH. Adipose derived pericytes rescue fractures from a failure of healing--non-union.. Sci Rep 2016 Mar 21;6:22779.
    doi: 10.1038/srep22779pmc: PMC4800389pubmed: 26997456google scholar: lookup
  22. Chen CW, Okada M, Proto JD, Gao X, Sekiya N, Beckman SA, Corselli M, Crisan M, Saparov A, Tobita K, Péault B, Huard J. Human pericytes for ischemic heart repair.. Stem Cells 2013 Feb;31(2):305-16.
    doi: 10.1002/stem.1285pmc: PMC3572307pubmed: 23165704google scholar: lookup
  23. West CC, Hardy WR, Murray IR, James AW, Corselli M, Pang S, Black C, Lobo SE, Sukhija K, Liang P, Lagishetty V, Hay DC, March KL, Ting K, Soo C, Péault B. Prospective purification of perivascular presumptive mesenchymal stem cells from human adipose tissue: process optimization and cell population metrics across a large cohort of diverse demographics.. Stem Cell Res Ther 2016 Mar 30;7:47.
    doi: 10.1186/s13287-016-0302-7pmc: PMC4815276pubmed: 27029948google scholar: lookup
  24. 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
  25. Esteves CL, Kelly V, Breton A, Taylor AI, West CC, Donadeu FX, Péault B, Seckl JR, Chapman KE. Proinflammatory cytokine induction of 11β-hydroxysteroid dehydrogenase type 1 (11β-HSD1) in human adipocytes is mediated by MEK, C/EBPβ, and NF-κB/RelA.. J Clin Endocrinol Metab 2014 Jan;99(1):E160-8.
    doi: 10.1210/jc.2013-1708pubmed: 24243637google scholar: lookup
  26. Esteves CL, Kelly V, Bégay V, Man TY, Morton NM, Leutz A, Seckl JR, Chapman KE. Regulation of adipocyte 11β-hydroxysteroid dehydrogenase type 1 (11β-HSD1) by CCAAT/enhancer-binding protein (C/EBP) β isoforms, LIP and LAP.. PLoS One 2012;7(5):e37953.
    doi: 10.1371/journal.pone.0037953pmc: PMC3360670pubmed: 22662254google scholar: lookup
  27. Esteves CL, Kelly V, Bégay V, Lillico SG, Leutz A, Seckl JR, Chapman KE. Stable conditional expression and effect of C/ebpβ-LIP in adipocytes using the pSLIK system.. J Mol Endocrinol 2013;51(1):91-8.
    doi: 10.1530/JME-13-0029pmc: PMC3672996pubmed: 23620165google scholar: lookup
  28. Ribatti D, Nico B, Vacca A, Presta M. The gelatin sponge-chorioallantoic membrane assay.. Nat Protoc 2006;1(1):85-91.
    doi: 10.1038/nprot.2006.13pubmed: 17406216google scholar: lookup
  29. Dohle DS, Pasa SD, Gustmann S, Laub M, Wissler JH, Jennissen HP, Dünker N. Chick ex ovo culture and ex ovo CAM assay: how it really works.. J Vis Exp 2009 Nov 30;(33).
    pmc: PMC3157849pubmed: 19949373doi: 10.3791/1620google scholar: lookup
  30. Zimmerlin L, Donnenberg VS, Pfeifer ME, Meyer EM, Péault 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. Sidney LE, Branch MJ, Dunphy SE, Dua HS, Hopkinson A. Concise review: evidence for CD34 as a common marker for diverse progenitors.. Stem Cells 2014 Jun;32(6):1380-9.
    pmc: PMC4260088pubmed: 24497003doi: 10.1002/stem.1661google scholar: lookup
  32. 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.
    doi: 10.1089/scd.2012.0263pubmed: 23072708google scholar: lookup
  33. 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
  34. Edwards SS, Zavala G, Prieto CP, Elliott M, Martínez S, Egaña JT, Bono MR, Palma V. Functional analysis reveals angiogenic potential of human mesenchymal stem cells from Wharton's jelly in dermal regeneration.. Angiogenesis 2014 Oct;17(4):851-66.
    doi: 10.1007/s10456-014-9432-7pubmed: 24728929google scholar: lookup
  35. Bronckaers A, Hilkens P, Fanton Y, Struys T, Gervois P, Politis C, Martens W, Lambrichts I. Angiogenic properties of human dental pulp stem cells.. PLoS One 2013;8(8):e71104.
    doi: 10.1371/journal.pone.0071104pmc: PMC3737205pubmed: 23951091google scholar: lookup
  36. Wang CH, Wang TM, Young TH, Lai YK, Yen ML. The critical role of ECM proteins within the human MSC niche in endothelial differentiation.. Biomaterials 2013 Jun;34(17):4223-34.
    doi: 10.1016/j.biomaterials.2013.02.062pubmed: 23489927google scholar: lookup
  37. Sorrentino A, Ferracin M, Castelli G, Biffoni M, Tomaselli G, Baiocchi M, Fatica A, Negrini M, Peschle C, Valtieri M. Isolation and characterization of CD146+ multipotent mesenchymal stromal cells.. Exp Hematol 2008 Aug;36(8):1035-46.
    doi: 10.1016/j.exphem.2008.03.004pubmed: 18504067google scholar: lookup
  38. 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
  39. 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
  40. Lange-Consiglio A, Corradetti B, Bizzaro D, Magatti M, Ressel L, Tassan S, Parolini O, Cremonesi F. Characterization and potential applications of progenitor-like cells isolated from horse amniotic membrane.. J Tissue Eng Regen Med 2012 Aug;6(8):622-35.
    doi: 10.1002/term.465pubmed: 21948689google scholar: lookup
  41. Mettouchi A, Meneguzzi G. Distinct roles of beta1 integrins during angiogenesis.. Eur J Cell Biol 2006 Apr;85(3-4):243-7.
    doi: 10.1016/j.ejcb.2005.09.010pubmed: 16546568google scholar: lookup
  42. Zhang B. CD73: a novel target for cancer immunotherapy.. Cancer Res 2010 Aug 15;70(16):6407-11.
    doi: 10.1158/0008-5472.CAN-10-1544pmc: PMC2922475pubmed: 20682793google scholar: lookup
  43. Narravula S, Lennon PF, Mueller BU, Colgan SP. Regulation of endothelial CD73 by adenosine: paracrine pathway for enhanced endothelial barrier function.. J Immunol 2000 Nov 1;165(9):5262-8.
    doi: 10.4049/jimmunol.165.9.5262pubmed: 11046060google scholar: lookup
  44. Nassiri F, Cusimano MD, Scheithauer BW, Rotondo F, Fazio A, Yousef GM, Syro LV, Kovacs K, Lloyd RV. Endoglin (CD105): a review of its role in angiogenesis and tumor diagnosis, progression and therapy.. Anticancer Res 2011 Jun;31(6):2283-90.
    pubmed: 21737653
  45. Hofmeister V, Schrama D, Becker JC. Anti-cancer therapies targeting the tumor stroma.. Cancer Immunol Immunother 2008 Jan;57(1):1-17.
    doi: 10.1007/s00262-007-0365-5pubmed: 17661033google scholar: lookup
  46. Carmeliet P. Angiogenesis in health and disease.. Nat Med 2003 Jun;9(6):653-60.
    doi: 10.1038/nm0603-653pubmed: 12778163google scholar: lookup
  47. Auerbach R, Lewis R, Shinners B, Kubai L, Akhtar N. Angiogenesis assays: a critical overview.. Clin Chem 2003 Jan;49(1):32-40.
    doi: 10.1373/49.1.32pubmed: 12507958google scholar: lookup
  48. Murphy MB, Moncivais K, Caplan AI. Mesenchymal stem cells: environmentally responsive therapeutics for regenerative medicine.. Exp Mol Med 2013 Nov 15;45(11):e54.
    doi: 10.1038/emm.2013.94pmc: PMC3849579pubmed: 24232253google scholar: lookup
  49. Murray IR, West CC, Hardy WR, James AW, Park TS, Nguyen A, Tawonsawatruk T, Lazzari L, Soo C, Péault B. Natural history of mesenchymal stem cells, from vessel walls to culture vessels.. Cell Mol Life Sci 2014 Apr;71(8):1353-74.
    doi: 10.1007/s00018-013-1462-6pubmed: 24158496google scholar: lookup
  50. 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.2014-0138pmc: PMC4250216pubmed: 25313202google scholar: lookup
  51. Pascucci L, Alessandri G, Dall'Aglio C, Mercati F, Coliolo P, Bazzucchi C, Dante S, Petrini S, Curina G, Ceccarelli P. Membrane vesicles mediate pro-angiogenic activity of equine adipose-derived mesenchymal stromal cells.. Vet J 2014 Nov;202(2):361-6.
    doi: 10.1016/j.tvjl.2014.08.021pubmed: 25241947google scholar: lookup
  52. Park TS, Gavina M, Chen CW, Sun B, Teng PN, Huard J, Deasy BM, Zimmerlin L, Péault B. Placental perivascular cells for human muscle regeneration.. Stem Cells Dev 2011 Mar;20(3):451-63.
    doi: 10.1089/scd.2010.0354pmc: PMC3120979pubmed: 20923371google scholar: lookup
  53. Campagnolo P, Cesselli D, Al Haj Zen A, Beltrami AP, Kränkel N, Katare R, Angelini G, Emanueli C, Madeddu P. Human adult vena saphena contains perivascular progenitor cells endowed with clonogenic and proangiogenic potential.. Circulation 2010 Apr 20;121(15):1735-45.
    doi: 10.1161/CIRCULATIONAHA.109.899252pmc: PMC2917746pubmed: 20368523google scholar: lookup

Citations

This article has been cited 24 times.
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