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Stem cell research & therapy2016; 7; 35; doi: 10.1186/s13287-016-0294-3

Comparative study of equine mesenchymal stem cells from healthy and injured synovial tissues: an in vitro assessment.

Abstract: Bone marrow and adipose tissues are known sources of mesenchymal stem cells (MSCs) in horses; however, synovial tissues might be a promising alternative. The aim of this study was to evaluate phenotypic characteristics and differentiation potential of equine MSCs from synovial fluid (SF) and synovial membrane (SM) of healthy joints (SF-H and SM-H), joints with osteoarthritis (SF-OA and SM-OA) and joints with osteochondritis dissecans (SF-OCD and SM-OCD) to determine the most suitable synovial source for an allogeneic therapy cell bank. Methods: Expression of the markers CD90, CD105, CD44, and CD34 in SF-H, SM-H, SF-OA, SM-OA, SF-OCD and SM-OCD was verified by flow cytometry, and expression of cytokeratin, vimentin, PGP 9.5, PCNA, lysozyme, nanog, and Oct4 was verified by immunocytochemistry. MSCs were cultured and evaluated for their chondrogenic, osteogenic and adipogenic differentiation potential. Final quantification of extracellular matrix and mineralized matrix was determined using AxioVision software. A tumorigenicity test was conducted in Balb-C(nu/nu) mice to verify the safety of the MSCs from these sources. Results: Cultured cells from SF and SM exhibited fibroblastoid morphology and the ability to adhere to plastic. The time elapsed between primary culture and the third passage was approximately 73 days for SF-H, 89 days for SF-OCD, 60 days for SF-OA, 68 days for SM-H, 57 days for SM-OCD and 54 days for SM-OA. The doubling time for SF-OCD was higher than that for other cells at the first passage (P < 0.05). MSCs from synovial tissues showed positive expression of the markers CD90, CD44, lysozyme, PGP 9.5, PCNA and vimentin and were able to differentiate into chondrogenic (21 days) and osteogenic (21 days) lineages, and, although poorly, into adipogenic lineages (14 days). The areas staining positive for extracellular matrix in the SF-H and SM-H groups were larger than those in the SF-OA and SM-OA groups (P < 0.05). The positive mineralized matrix area in the SF-H group was larger than those in all the other groups (P < 0.05). The studied cells exhibited no tumorigenic effects. Conclusions: SF and SM are viable sources of equine MSCs. All sources studied provide suitable MSCs for an allogeneic therapy cell bank; nevertheless, MSCs from healthy joints may be preferable for cell banking purposes because they exhibit better chondrogenic differentiation capacity.
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Publication Date: 2016-03-05 PubMed ID: 26944403PubMed Central: PMC4779201DOI: 10.1186/s13287-016-0294-3Google Scholar: Lookup
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  • Comparative Study
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

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.

This research study seeks to determine if synovial fluid and synovial membranes from healthy and injured horse joints could be a potential source of mesenchymal stem cells for therapeutic cell bank. The stem cells from the synovial tissues were assessed for phenotypic characteristics and differentiation potential, and the results suggested that healthy tissues may provide a better source of cells for therapeutic purposes.

Research Methods

  • The researchers investigated the different potential sources of mesenchymal stem cells (MSCs) in horses, focusing on synovial fluid (SF) and synovial membrane (SM) from healthy joints, and joints with osteoarthritis (OA) and osteochondritis dissecans (OCD).
  • They evaluated the expression of markers, such as CD90, CD105, CD44, and CD34, in the SF and SM from healthy, OA, and OCD samples using flow cytometry.
  • Using immunocytochemistry, they also verified the expression of cytokeratin, vimentin, PGP 9.5, PCNA, lysozyme, nanog, and Oct4 – proteins that indicate the MSCs’ characteristics and their capacity for differentiation.
  • They then cultured released MSCs from these tissues and assessed their capacity to differentiate into chondrogenic, osteogenic and adipogenic lineages.
  • Furthermore, a tumorigenicity test was conducted using Balb-C(nu/nu) mice to check for potential tumour-inducing capabilities of the sourced MSCs.

Research Findings

  • The researchers found that the stem cells sourced from SF and SM had fibroblastoid (fibroblast-like) morphology and could adhere to plastic – typical characteristics of MSCs.
  • Average time elapsed between the primary culture and the third passage varied for each group, with MSCs from osteoarthritis joints showing the quickest growth rates.
  • The MSCs demonstrated the ability to differentiate into chondrogenic and osteogenic lineages, and showed partial capability to differentiate into adipogenic lineages.
  • Healthy joint-derived MSCs exhibited larger areas positive for extracellular matrix (ECM), implying better ability to generate structural support for tissues.
  • Mesenchymal stem cells from all synovial tissues, whether healthy or diseased, did not induce any tumorigenic effects in mice, which emphasizes their safety as a source for MSCs.

Conclusion

  • Both synovial fluid and synovial membrane in horses, irrespective of the health status of the joint, are viable and safe sources of mesenchymal stem cells.
  • However, MSCs derived from healthy joints performed better in the aspect of chondrogenic differentiation, making them potentially more suitable for cell banking purposes, particularly for treatments aimed at cartilage regeneration.

Cite This Article

APA
Fülber J, Maria DA, da Silva LC, Massoco CO, Agreste F, Baccarin RY. (2016). Comparative study of equine mesenchymal stem cells from healthy and injured synovial tissues: an in vitro assessment. Stem Cell Res Ther, 7, 35. https://doi.org/10.1186/s13287-016-0294-3

Publication

Stem cell research & therapy
ISSN: 1757-6512
NlmUniqueID: 101527581
Country: England
Language: English
Volume: 7
Pages: 35
PII: 35

Researcher Affiliations

Fülber, Joice
  • Department of Internal Medicine, School of Veterinary Medicine and Animal Science, University of São Paulo (USP), Avenida Prof. Orlando Marques de Paiva, 87, 05508-270, São Paulo, SP, Brazil. fulberjoice@yahoo.com.br.
Maria, Durvanei A
  • Laboratory of Biochemistry and Biophysics, Butantan Institute, Avenida Vital Brasil 1500, São Paulo, 05503-900, SP, Brazil. durvanei.maria@butantan.gov.br.
da Silva, Luis Cláudio Lopes Correia
  • Department of Surgery, School of Veterinary Medicine and Animal Science, University of São Paulo (USP), Avenida Prof. Orlando Marques de Paiva, 87, SP, 05508-270, SP, Brazil. silvalc@usp.br.
Massoco, Cristina O
  • Department of Pathology, School of Veterinary Medicine and Animal Science, University of São Paulo (USP), Avenida Prof. Orlando Marques de Paiva, 87, São Paulo, 05508-270, SP, Brazil. cmassoco@gmail.com.
Agreste, Fernanda
  • Department of Internal Medicine, School of Veterinary Medicine and Animal Science, University of São Paulo (USP), Avenida Prof. Orlando Marques de Paiva, 87, 05508-270, São Paulo, SP, Brazil. fe_nandara@hotmail.com.
Baccarin, Raquel Y Arantes
  • Department of Internal Medicine, School of Veterinary Medicine and Animal Science, University of São Paulo (USP), Avenida Prof. Orlando Marques de Paiva, 87, 05508-270, São Paulo, SP, Brazil. baccarin@usp.br.

MeSH Terms

  • Animals
  • Antigens, CD / metabolism
  • Carcinogenicity Tests
  • Cells, Cultured
  • Female
  • Horse Diseases / pathology
  • Horse Diseases / therapy
  • Horses
  • Male
  • Mesenchymal Stem Cell Transplantation
  • Mesenchymal Stem Cells / physiology
  • Mice, Inbred BALB C
  • Mice, Nude
  • Osteoarthritis / pathology
  • Osteoarthritis / therapy
  • Osteoarthritis / veterinary
  • Synovial Fluid

References

This article includes 51 references
  1. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells.. Science 1999 Apr 2;284(5411):143-7.
    doi: 10.1126/science.284.5411.143pubmed: 10102814google scholar: lookup
  2. Rozemuller H, Prins HJ, Naaijkens B, Staal J, Bühring HJ, Martens AC. Prospective isolation of mesenchymal stem cells from multiple mammalian species using cross-reacting anti-human monoclonal antibodies.. Stem Cells Dev 2010 Dec;19(12):1911-21.
    doi: 10.1089/scd.2009.0510pubmed: 20367498google scholar: lookup
  3. 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.
    doi: 10.1186/scrt414pmc: PMC4055040pubmed: 24559797google scholar: lookup
  4. De Bari C, Dell'Accio F, Tylzanowski P, Luyten FP. Multipotent mesenchymal stem cells from adult human synovial membrane.. Arthritis Rheum 2001 Aug;44(8):1928-42.
    doi: 10.1002/1529-0131(200108)44:8<1928::AID-ART331>3.0.CO;2-Ppubmed: 11508446google scholar: lookup
  5. 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
  6. 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
  7. 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
  8. 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
  9. 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
  10. 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
  11. 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
  12. Murata D, Miyakoshi D, Hatazoe T, Miura N, Tokunaga S, Fujiki M, Nakayama K, Misumi K. Multipotency of equine mesenchymal stem cells derived from synovial fluid.. Vet J 2014 Oct;202(1):53-61.
    doi: 10.1016/j.tvjl.2014.07.029pubmed: 25151209google scholar: lookup
  13. Prado AA, Favaron PO, da Silva LC, Baccarin RY, Miglino MA, Maria DA. Characterization of mesenchymal stem cells derived from the equine synovial fluid and membrane.. BMC Vet Res 2015 Nov 10;11:281.
    doi: 10.1186/s12917-015-0531-5pmc: PMC4640348pubmed: 26555093google scholar: lookup
  14. Mochizuki T, Muneta T, Sakaguchi Y, Nimura A, Yokoyama A, Koga H, Sekiya I. Higher chondrogenic potential of fibrous synovium- and adipose synovium-derived cells compared with subcutaneous fat-derived cells: distinguishing properties of mesenchymal stem cells in humans.. Arthritis Rheum 2006 Mar;54(3):843-53.
    doi: 10.1002/art.21651pubmed: 16508965google scholar: lookup
  15. Arufe MC, De la Fuente A, Fuentes-Boquete I, De Toro FJ, Blanco FJ. Differentiation of synovial CD-105(+) human mesenchymal stem cells into chondrocyte-like cells through spheroid formation.. J Cell Biochem 2009 Sep 1;108(1):145-55.
    doi: 10.1002/jcb.22238pubmed: 19544399google scholar: lookup
  16. Jones E. Synovial mesenchymal stem cells in vivo: potential key players for joint regeneration.. World J Rheumatol 2011;1:4.
    doi: 10.5499/wjr.v1.i1.4google scholar: lookup
  17. Krawetz RJ, Wu YE, Martin L, Rattner JB, Matyas JR, Hart DA. Synovial fluid progenitors expressing CD90+ from normal but not osteoarthritic joints undergo chondrogenic differentiation without micro-mass culture.. PLoS One 2012;7(8):e43616.
    doi: 10.1371/annotation/ace75296-7ec7-4193-ac91-5d68cfe5073epmc: PMC3430696pubmed: 22952721google scholar: lookup
  18. McGonagle D, Jones E. A potential role for synovial fluid mesenchymal stem cells in ligament regeneration.. Rheumatology (Oxford) 2008 Aug;47(8):1114-6.
    doi: 10.1093/rheumatology/ken236pubmed: 18579618google scholar: lookup
  19. Hermida-Gómez T, Fuentes-Boquete I, Gimeno-Longas MJ, Muiños-López E, Díaz-Prado S, de Toro FJ, Blanco FJ. Quantification of cells expressing mesenchymal stem cell markers in healthy and osteoarthritic synovial membranes.. J Rheumatol 2011 Feb;38(2):339-49.
    doi: 10.3899/jrheum.100614pubmed: 21078714google scholar: lookup
  20. Lee DH, Sonn CH, Han SB, Oh Y, Lee KM, Lee SH. Synovial fluid CD34⁻ CD44⁺ CD90⁺ mesenchymal stem cell levels are associated with the severity of primary knee osteoarthritis.. Osteoarthritis Cartilage 2012 Feb;20(2):106-9.
    doi: 10.1016/j.joca.2011.11.010pubmed: 22155731google scholar: lookup
  21. Lee JC, Lee SY, Min HJ, Han SA, Jang J, Lee S, Seong SC, Lee MC. Synovium-derived mesenchymal stem cells encapsulated in a novel injectable gel can repair osteochondral defects in a rabbit model.. Tissue Eng Part A 2012 Oct;18(19-20):2173-86.
    doi: 10.1089/ten.tea.2011.0643pubmed: 22765885google scholar: lookup
  22. Santhagunam A, Dos Santos F, Madeira C, Salgueiro JB, Cabral JM. Isolation and ex vivo expansion of synovial mesenchymal stromal cells for cartilage repair.. Cytotherapy 2014 Apr;16(4):440-53.
    doi: 10.1016/j.jcyt.2013.10.010pubmed: 24364906google scholar: lookup
  23. Morito T, Muneta T, Hara K, Ju YJ, Mochizuki T, Makino H, Umezawa A, Sekiya I. Synovial fluid-derived mesenchymal stem cells increase after intra-articular ligament injury in humans.. Rheumatology (Oxford) 2008 Aug;47(8):1137-43.
    doi: 10.1093/rheumatology/ken114pubmed: 18390894google scholar: lookup
  24. Roth V. 2006. http://www.doubling-time.com/compute.php. Accessed 3 Nov 2015.
  25. 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
  26. Koga H, Muneta T, Ju YJ, Nagase T, Nimura A, Mochizuki T, Ichinose S, von der Mark K, Sekiya I. Synovial stem cells are regionally specified according to local microenvironments after implantation for cartilage regeneration.. Stem Cells 2007 Mar;25(3):689-96.
    doi: 10.1634/stemcells.2006-0281pubmed: 17138960google scholar: lookup
  27. Kurth T, Hedbom E, Shintani N, Sugimoto M, Chen FH, Haspl M, Martinovic S, Hunziker EB. Chondrogenic potential of human synovial mesenchymal stem cells in alginate.. Osteoarthritis Cartilage 2007 Oct;15(10):1178-89.
    doi: 10.1016/j.joca.2007.03.015pubmed: 17502159google scholar: lookup
  28. Jones EA, English A, Henshaw K, Kinsey SE, Markham AF, Emery P, McGonagle D. Enumeration and phenotypic characterization of synovial fluid multipotential mesenchymal progenitor cells in inflammatory and degenerative arthritis.. Arthritis Rheum 2004 Mar;50(3):817-27.
    doi: 10.1002/art.20203pubmed: 15022324google scholar: lookup
  29. Matsukura Y, Muneta T, Tsuji K, Koga H, Sekiya I. Mesenchymal stem cells in synovial fluid increase after meniscus injury.. Clin Orthop Relat Res 2014 May;472(5):1357-64.
    doi: 10.1007/s11999-013-3418-4pmc: PMC3971249pubmed: 24338094google scholar: lookup
  30. 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
  31. 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
  32. 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
  33. 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
  34. Kobayashi S, Takebe T, Inui M, Iwai S, Kan H, Zheng YW, Maegawa J, Taniguchi H. Reconstruction of human elastic cartilage by a CD44+ CD90+ stem cell in the ear perichondrium.. Proc Natl Acad Sci U S A 2011 Aug 30;108(35):14479-84.
    doi: 10.1073/pnas.1109767108pmc: PMC3167558pubmed: 21836053google 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. Sakaguchi Y, Sekiya I, Yagishita K, Muneta T. Comparison of human stem cells derived from various mesenchymal tissues: superiority of synovium as a cell source.. Arthritis Rheum 2005 Aug;52(8):2521-9.
    doi: 10.1002/art.21212pubmed: 16052568google scholar: lookup
  37. Zhang S, Muneta T, Morito T, Mochizuki T, Sekiya I. Autologous synovial fluid enhances migration of mesenchymal stem cells from synovium of osteoarthritis patients in tissue culture system.. J Orthop Res 2008 Oct;26(10):1413-8.
    doi: 10.1002/jor.20659pubmed: 18418888google scholar: lookup
  38. Sekiya I, Ojima M, Suzuki S, Yamaga M, Horie M, Koga H, Tsuji K, Miyaguchi K, Ogishima S, Tanaka H, Muneta T. Human mesenchymal stem cells in synovial fluid increase in the knee with degenerated cartilage and osteoarthritis.. J Orthop Res 2012 Jun;30(6):943-9.
    doi: 10.1002/jor.22029pubmed: 22147634google scholar: lookup
  39. Sun YP, Zheng YH, Liu WJ, Zheng YL, Zhang ZG. Synovium fragment-derived cells exhibit characteristics similar to those of dissociated multipotent cells in synovial fluid of the temporomandibular joint.. PLoS One 2014;9(7):e101896.
    doi: 10.1371/journal.pone.0101896pmc: PMC4087006pubmed: 25003199google scholar: lookup
  40. Kitamura HP, Yanase H, Kitamura H, Iwanaga T. Unique localization of protein gene product 9.5 in type B synoviocytes in the joints of the horse.. J Histochem Cytochem 1999 Mar;47(3):343-52.
    doi: 10.1177/002215549904700308pubmed: 10026236google scholar: lookup
  41. Mapp PI, Revell PA. Ultrastructural localisation of muramidase in the human synovial membrane.. Ann Rheum Dis 1987 Jan;46(1):30-7.
    doi: 10.1136/ard.46.1.30pmc: PMC1002054pubmed: 3813672google scholar: lookup
  42. De Vita B, Campo LL, Listoni AJ, Maia L, Sudano MJ, Curcio BR. Isolamento, caracterização e diferenciação de células-tronco mesenquimais do líquido amniótico equino obtido em diferentes idades gestacionais.. Pesq Vet Bras 2013;33:535–42.
    doi: 10.1590/S0100-736X2013000400019google scholar: lookup
  43. Pratheesh MD, Gade NE, Katiyar AN, Dubey PK, Sharma B, Saikumar G, Amarpal, Sharma GT. Isolation, culture and characterization of caprine mesenchymal stem cells derived from amniotic fluid.. Res Vet Sci 2013 Apr;94(2):313-9.
    doi: 10.1016/j.rvsc.2012.08.002pubmed: 23017255google scholar: lookup
  44. Gao S, Zhao P, Lin C, Sun Y, Wang Y, Zhou Z, Yang D, Wang X, Xu H, Zhou F, Cao L, Zhou W, Ning K, Chen X, Xu J. Differentiation of human adipose-derived stem cells into neuron-like cells which are compatible with photocurable three-dimensional scaffolds.. Tissue Eng Part A 2014 Apr;20(7-8):1271-84.
    doi: 10.1089/ten.tea.2012.0773pmc: PMC3993073pubmed: 24251600google scholar: lookup
  45. Yoshimura H, Muneta T, Nimura A, Yokoyama A, Koga H, Sekiya I. Comparison of rat mesenchymal stem cells derived from bone marrow, synovium, periosteum, adipose tissue, and muscle.. Cell Tissue Res 2007 Mar;327(3):449-62.
    doi: 10.1007/s00441-006-0308-zpubmed: 17053900google scholar: lookup
  46. Giovannini S, Brehm W, Mainil-Varlet P, Nesic D. Multilineage differentiation potential of equine blood-derived fibroblast-like cells.. Differentiation 2008 Feb;76(2):118-29.
    doi: 10.1111/j.1432-0436.2007.00207.xpubmed: 17697129google scholar: lookup
  47. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses.. Blood 2005 Feb 15;105(4):1815-22.
    doi: 10.1182/blood-2004-04-1559pubmed: 15494428google scholar: lookup
  48. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells.. Blood 2007 Nov 15;110(10):3499-506.
    pubmed: 17664353doi: 10.1182/blood-2007-02-069716google scholar: lookup
  49. 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
  50. van Lent PL, van den Berg WB. Mesenchymal stem cell therapy in osteoarthritis: advanced tissue repair or intervention with smouldering synovial activation?. Arthritis Res Ther 2013 Mar 20;15(2):112.
    doi: 10.1186/ar4190pmc: PMC3672811pubmed: 23521980google scholar: lookup
  51. Pezzanite LM, Fortier LA, Antczak DF, Cassano JM, Brosnahan MM, Miller D, Schnabel LV. Equine allogeneic bone marrow-derived mesenchymal stromal cells elicit antibody responses in vivo.. Stem Cell Res Ther 2015 Apr 12;6(1):54.
    doi: 10.1186/s13287-015-0053-xpmc: PMC4414005pubmed: 25889095google scholar: lookup

Citations

This article has been cited 17 times.
  1. Ouzin M, Kogler G. Mesenchymal Stromal Cells: Heterogeneity and Therapeutical Applications. Cells 2023 Aug 10;12(16).
    doi: 10.3390/cells12162039pubmed: 37626848google scholar: lookup
  2. Leal Reis I, Lopes B, Sousa P, Sousa AC, Branquinho M, Caseiro AR, Pedrosa SS, Rêma A, Oliveira C, Porto B, Atayde L, Amorim I, Alvites R, Santos JM, Maurício AC. Allogenic Synovia-Derived Mesenchymal Stem Cells for Treatment of Equine Tendinopathies and Desmopathies-Proof of Concept. Animals (Basel) 2023 Apr 11;13(8).
    doi: 10.3390/ani13081312pubmed: 37106875google scholar: lookup
  3. Liu TP, Ha P, Xiao CY, Kim SY, Jensen AR, Easley J, Yao Q, Zhang X. Updates on mesenchymal stem cell therapies for articular cartilage regeneration in large animal models. Front Cell Dev Biol 2022;10:982199.
    doi: 10.3389/fcell.2022.982199pubmed: 36147737google scholar: lookup
  4. Łabuś W, Kitala D, Szapski M, Klama-Baryła A, Kraut M, Smętek W. Tissue Engineering in Skin Substitute. Adv Exp Med Biol 2021;1345:193-208.
    doi: 10.1007/978-3-030-82735-9_16pubmed: 34582024google scholar: lookup
  5. Fülber J, Agreste FR, Seidel SRT, Sotelo EDP, Barbosa ÂP, Michelacci YM, Baccarin RYA. Chondrogenic potential of mesenchymal stem cells from horses using a magnetic 3D cell culture system. World J Stem Cells 2021 Jun 26;13(6):645-658.
    doi: 10.4252/wjsc.v13.i6.645pubmed: 34249233google scholar: lookup
  6. 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
  7. Zha K, Li X, Yang Z, Tian G, Sun Z, Sui X, Dai Y, Liu S, Guo Q. Heterogeneity of mesenchymal stem cells in cartilage regeneration: from characterization to application. NPJ Regen Med 2021 Mar 19;6(1):14.
    doi: 10.1038/s41536-021-00122-6pubmed: 33741999google scholar: lookup
  8. To K, Zhang B, Romain K, Mak C, Khan W. Synovium-Derived Mesenchymal Stem Cell Transplantation in Cartilage Regeneration: A PRISMA Review of in vivo Studies. Front Bioeng Biotechnol 2019;7:314.
    doi: 10.3389/fbioe.2019.00314pubmed: 31803726google scholar: lookup
  9. Yang Q, Pinto VMR, Duan W, Paxton EE, Dessauer JH, Ryan W, Lopez MJ. In vitro Characteristics of Heterogeneous Equine Hoof Progenitor Cell Isolates. Front Bioeng Biotechnol 2019;7:155.
    doi: 10.3389/fbioe.2019.00155pubmed: 31355191google 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. Gale AL, Linardi RL, McClung G, Mammone RM, Ortved KF. Comparison of the Chondrogenic Differentiation Potential of Equine Synovial Membrane-Derived and Bone Marrow-Derived Mesenchymal Stem Cells. Front Vet Sci 2019;6:178.
    doi: 10.3389/fvets.2019.00178pubmed: 31245393google scholar: lookup
  12. Gale AL, Mammone RM, Dodson ME, Linardi RL, Ortved KF. The effect of hypoxia on chondrogenesis of equine synovial membrane-derived and bone marrow-derived mesenchymal stem cells. BMC Vet Res 2019 Jun 14;15(1):201.
    doi: 10.1186/s12917-019-1954-1pubmed: 31200719google scholar: lookup
  13. de Sousa EB, Dos Santos Junior GC, Aguiar RP, da Costa Sartore R, de Oliveira ACL, Almeida FCL, Neto VM, Aguiar DP. Osteoarthritic Synovial Fluid Modulates Cell Phenotype and Metabolic Behavior In Vitro. Stem Cells Int 2019;2019:8169172.
    doi: 10.1155/2019/8169172pubmed: 30766606google scholar: lookup
  14. Yamasaki A, Omura T, Murata D, Kobayashi M, Sunaga T, Kusano K, Ueno Y, Kuramoto T, Hobo S, Misumi K. A pilot study of regenerative therapy by implanting synovium-derived mesenchymal stromal cells in equine osteochondral defect models. J Equine Sci 2018 Dec;29(4):117-122.
    doi: 10.1294/jes.29.117pubmed: 30607136google scholar: lookup
  15. Neybecker P, Henrionnet C, Pape E, Mainard D, Galois L, Loeuille D, Gillet P, Pinzano A. In vitro and in vivo potentialities for cartilage repair from human advanced knee osteoarthritis synovial fluid-derived mesenchymal stem cells. Stem Cell Res Ther 2018 Nov 28;9(1):329.
    doi: 10.1186/s13287-018-1071-2pubmed: 30486903google scholar: lookup
  16. Santos VH, Pfeifer JPH, de Souza JB, Milani BHG, de Oliveira RA, Assis MG, Deffune E, Moroz A, Alves ALG. Culture of mesenchymal stem cells derived from equine synovial membrane in alginate hydrogel microcapsules. BMC Vet Res 2018 Mar 27;14(1):114.
    doi: 10.1186/s12917-018-1425-0pubmed: 29587733google scholar: lookup
  17. Nascimento C, Saraiva MVA, Pereira VM, de Brito DCC, de Aguiar FLN, Alves BG, Roballo KCS, de Figueiredo JR, Ambrósio CE, Rodrigues APR. Addition of synthetic polymer in the freezing solution of mesenchymal stem cells from equine adipose tissue as a future perspective for reducing of DMSO concentration. Braz J Vet Med 2023;45:e002523.
    doi: 10.29374/2527-2179.bjvm002523pubmed: 38162818google scholar: lookup
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