Analyze Diet
BMC cell biology2009; 10; 29; doi: 10.1186/1471-2121-10-29

Horse bone marrow mesenchymal stem cells express embryo stem cell markers and show the ability for tenogenic differentiation by in vitro exposure to BMP-12.

Abstract: Mesenchymal stem cells (MSCs) have been recently investigated for their potential use in regenerative medicine. MSCs, in particular, have great potential, as in various reports they have shown pluripotency for differentiating into many different cell types. However, the ability of MSCs to differentiate into tendon cells in vitro has not been fully investigated. Results: In this study, we show that equine bone marrow mesenchymal stem cells (BM-MSCs), defined by their expression of markers such as Oct4, Sox-2 and Nanog, have the capability to differentiate in tenocytes. These differentiated cells express tendon-related markers including tenomodulin and decorin. Moreover we show that the same BM-MSCs can differentiate in osteocytes, as confirmed by alkaline phosphatase and von Kossa staining. Conclusions: As MSCs represent an attractive tool for tendon tissue repair strategies, our data suggest that bone marrow should be considered the preferred MSC source for therapeutic approaches.
Publication Date: 2009-04-22 PubMed ID: 19383177PubMed Central: PMC2678092DOI: 10.1186/1471-2121-10-29Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

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

The research article explores the potential of a certain type of horse stem cells in regenerating tissues, particularly tendons.

Introduction and Aim

  • The research delves into the potential of Mesenchymal stem cells (MSCs) – a specific kind of stem cells in regenerative medicine. Stem cells are cells with the potential to develop into many different types of cells in the body.
  • The researchers specifically aim to investigate the ability of these MSCs to differentiate into tendon cells when cultured in a lab.

Results and Findings

  • The study shows that certain markers specifically Oct4, Sox-2, and Nanog, are expressed by the equine bone marrow mesenchymal stem cells (BM-MSCs), these indicate their stemness or the ability to change into different types of cells.
  • The researchers claim that these BM-MSCs can differentiate into tenocytes or tendon cells. These differentiated cells were observed to express tenomodulin and decorin which are specific to tendon-related cells.
  • The study also reveals that the same BM-MSCs have the ability to differentiate into osteocytes or bone cells. Alkaline phosphatase and von Kossa staining, common techniques to validate bone cells, were used to confirm this differentiation.

Conclusions

  • The researchers conclude that MSCs have a promising significance in tendon tissue repair strategies. They suggest that the bone marrow, based on their findings, should be considered as a primary source of MSCs for such therapeutic approaches.

Cite This Article

APA
Violini S, Ramelli P, Pisani LF, Gorni C, Mariani P. (2009). Horse bone marrow mesenchymal stem cells express embryo stem cell markers and show the ability for tenogenic differentiation by in vitro exposure to BMP-12. BMC Cell Biol, 10, 29. https://doi.org/10.1186/1471-2121-10-29

Publication

ISSN: 1471-2121
NlmUniqueID: 100966972
Country: England
Language: English
Volume: 10
Pages: 29

Researcher Affiliations

Violini, Stefania
  • Livestock Genomics Unit, Parco Tecnologico Padano, CERSA, Via Einstein, Loc Cascina Codazza, , Lodi 26900, Italy. stefania.violini@tecnoparco.org
Ramelli, Paola
    Pisani, Laura F
      Gorni, Chiara
        Mariani, Paola

          MeSH Terms

          • Animals
          • Biomarkers / metabolism
          • Bone Marrow Cells / cytology
          • Bone Morphogenetic Proteins / metabolism
          • Bone Morphogenetic Proteins / pharmacology
          • Cell Differentiation
          • Decorin
          • Embryonic Stem Cells / metabolism
          • Extracellular Matrix Proteins / metabolism
          • Gene Expression Regulation
          • Homeodomain Proteins / metabolism
          • Horses
          • Membrane Proteins / metabolism
          • Mesenchymal Stem Cells / cytology
          • Octamer Transcription Factor-3 / metabolism
          • Proteoglycans / metabolism
          • SOXB1 Transcription Factors / metabolism
          • Tendons / cytology

          References

          This article includes 57 references
          1. Stevens M. Stem cells in regenerative medicine. The Pharmaceutical Journal 2005;275:695–698.
          2. Mimeault M, Batra SK. Concise review: recent advances on the significance of stem cells in tissue regeneration and cancer therapies.. Stem Cells 2006 Nov;24(11):2319-45.
            doi: 10.1634/stemcells.2006-0066pubmed: 16794264google scholar: lookup
          3. Kemp KC, Hows J, Donaldson C. Bone marrow-derived mesenchymal stem cells.. Leuk Lymphoma 2005 Nov;46(11):1531-44.
            doi: 10.1080/10428190500215076pubmed: 16236607google scholar: lookup
          4. Helder MN, Knippenberg M, Klein-Nulend J, Wuisman PI. Stem cells from adipose tissue allow challenging new concepts for regenerative medicine.. Tissue Eng 2007 Aug;13(8):1799-808.
            doi: 10.1089/ten.2006.0165pubmed: 17518736google scholar: lookup
          5. Weiss ML, Troyer DL. Stem cells in the umbilical cord.. Stem Cell Rev 2006;2(2):155-62.
            pmc: PMC3753204pubmed: 17237554doi: 10.1007/s12015-006-0022-ygoogle scholar: lookup
          6. Ilancheran S, Michalska A, Peh G, Wallace EM, Pera M, Manuelpillai U. Stem cells derived from human fetal membranes display multilineage differentiation potential.. Biol Reprod 2007 Sep;77(3):577-88.
            doi: 10.1095/biolreprod.106.055244pubmed: 17494917google scholar: lookup
          7. Herzog EL, Chai L, Krause DS. Plasticity of marrow-derived stem cells.. Blood 2003 Nov 15;102(10):3483-93.
            doi: 10.1182/blood-2003-05-1664pubmed: 12893756google scholar: lookup
          8. Holtorf HL, Jansen JA, Mikos AG. Flow perfusion culture induces the osteoblastic differentiation of marrow stroma cell-scaffold constructs in the absence of dexamethasone.. J Biomed Mater Res A 2005 Mar 1;72(3):326-34.
            pubmed: 15657936doi: 10.1002/jbm.a.30251google scholar: lookup
          9. Bernardo ME, Emons JA, Karperien M, Nauta AJ, Willemze R, Roelofs H, Romeo S, Marchini A, Rappold GA, Vukicevic S, Locatelli F, Fibbe WE. Human mesenchymal stem cells derived from bone marrow display a better chondrogenic differentiation compared with other sources.. Connect Tissue Res 2007;48(3):132-40.
            doi: 10.1080/03008200701228464pubmed: 17522996google scholar: lookup
          10. Yoon YS, Lee N, Scadova H. Myocardial regeneration with bone-marrow-derived stem cells.. Biol Cell 2005 Apr;97(4):253-63.
            doi: 10.1042/BC20040099pubmed: 15762847google scholar: lookup
          11. Potapova IA, Gaudette GR, Brink PR, Robinson RB, Rosen MR, Cohen IS, Doronin SV. Mesenchymal stem cells support migration, extracellular matrix invasion, proliferation, and survival of endothelial cells in vitro.. Stem Cells 2007 Jul;25(7):1761-8.
            doi: 10.1634/stemcells.2007-0022pubmed: 17395769google scholar: lookup
          12. Bianco P, Riminucci M, Gronthos S, Robey PG. Bone marrow stromal stem cells: nature, biology, and potential applications.. Stem Cells 2001;19(3):180-92.
            doi: 10.1634/stemcells.19-3-180pubmed: 11359943google scholar: lookup
          13. Bernard-Beaubois K, Hecquet C, Houcine O, Hayem G, Adolphe M. Culture and characterization of juvenile rabbit tenocytes.. Cell Biol Toxicol 1997 Feb;13(2):103-13.
          14. Kannus P. Structure of the tendon connective tissue.. Scand J Med Sci Sports 2000 Dec;10(6):312-20.
          15. Rees SG, Flannery CR, Little CB, Hughes CE, Caterson B, Dent CM. Catabolism of aggrecan, decorin and biglycan in tendon.. Biochem J 2000 Aug 15;350 Pt 1(Pt 1):181-8.
            doi: 10.1042/0264-6021:3500181pmc: PMC1221240pubmed: 10926842google scholar: lookup
          16. Goh JC, Ouyang HW, Teoh SH, Chan CK, Lee EH. Tissue-engineering approach to the repair and regeneration of tendons and ligaments.. Tissue Eng 2003;9 Suppl 1:S31-44.
            doi: 10.1089/10763270360696969pubmed: 14511469google scholar: lookup
          17. Ahmed T, Lutton JD, Feldman E, Tani K, Asano S, Abraham NG. Gene transfer of alpha interferon into hematopoietic stem cells.. Leuk Res 1998 Feb;22(2):119-24.
            doi: 10.1016/S0145-2126(97)00133-1pubmed: 9593468google scholar: lookup
          18. Woo SL, Hildebrand K, Watanabe N, Fenwick JA, Papageorgiou CD, Wang JH. Tissue engineering of ligament and tendon healing.. Clin Orthop Relat Res 1999 Oct;(367 Suppl):S312-23.
          19. Cao Y, Vacanti JP, Ma X, Paige KT, Upton J, Chowanski Z, Schloo B, Langer R, Vacanti CA. Generation of neo-tendon using synthetic polymers seeded with tenocytes.. Transplant Proc 1994 Dec;26(6):3390-2.
            pubmed: 7998187
          20. Awad HA, Butler DL, Boivin GP, Smith FN, Malaviya P, Huibregtse B, Caplan AI. Autologous mesenchymal stem cell-mediated repair of tendon.. Tissue Eng 1999 Jun;5(3):267-77.
            doi: 10.1089/ten.1999.5.267pubmed: 10434073google scholar: lookup
          21. Koob TJ, Willis TA, Qiu YS, Hernandez DJ. Biocompatibility of NDGA-polymerized collagen fibers. II. Attachment, proliferation, and migration of tendon fibroblasts in vitro.. J Biomed Mater Res 2001 Jul;56(1):40-8.
          22. Józsa L, Kvist M, Kannus P, Vieno T, Järvinen M, Lehto M. Structure and macromolecular composition of the myotendineal junction. Histochemical, immunohistochemical and electron microscopic study of the rat calf muscles.. Acta Morphol Hung 1991;39(4):287-97.
            pubmed: 1844341
          23. Schwarz R, Colarusso L, Doty P. Maintenance of differentiation in primary cultures of avian tendon cells.. Exp Cell Res 1976 Oct 1;102(1):63-71.
            doi: 10.1016/0014-4827(76)90299-8pubmed: 976346google scholar: lookup
          24. Friedman MS, Long MW, Hankenson KD. Osteogenic differentiation of human mesenchymal stem cells is regulated by bone morphogenetic protein-6.. J Cell Biochem 2006 Jun 1;98(3):538-54.
            doi: 10.1002/jcb.20719pubmed: 16317727google scholar: lookup
          25. Wozney JM. Bone morphogenetic proteins.. Prog Growth Factor Res 1989;1(4):267-80.
            doi: 10.1016/0955-2235(89)90015-Xpubmed: 2491264google scholar: lookup
          26. Yu Y, Bliss JP, Bruce WJ, Walsh WR. Bone morphogenetic proteins and Smad expression in ovine tendon-bone healing.. Arthroscopy 2007 Feb;23(2):205-10.
            pubmed: 17276229doi: 10.1016/j.arthro.2006.08.023google scholar: lookup
          27. Wang QW, Chen ZL, Piao YJ. Mesenchymal stem cells differentiate into tenocytes by bone morphogenetic protein (BMP) 12 gene transfer.. J Biosci Bioeng 2005 Oct;100(4):418-22.
            doi: 10.1263/jbb.100.418pubmed: 16310731google scholar: lookup
          28. Lou J, Tu Y, Burns M, Silva MJ, Manske P. BMP-12 gene transfer augmentation of lacerated tendon repair.. J Orthop Res 2001 Nov;19(6):1199-202.
            doi: 10.1016/S0736-0266(01)00042-0pubmed: 11781024google scholar: lookup
          29. Mays RW, van't Hof W, Ting AE, Perry R, Deans R. Development of adult pluripotent stem cell therapies for ischemic injury and disease.. Expert Opin Biol Ther 2007 Feb;7(2):173-84.
            doi: 10.1517/14712598.7.2.173pubmed: 17250456google scholar: lookup
          30. Shi W, Wang H, Pan G, Geng Y, Guo Y, Pei D. Regulation of the pluripotency marker Rex-1 by Nanog and Sox2.. J Biol Chem 2006 Aug 18;281(33):23319-25.
            doi: 10.1074/jbc.M601811200pubmed: 16714766google scholar: lookup
          31. Shukunami C, Takimoto A, Oro M, Hiraki Y. Scleraxis positively regulates the expression of tenomodulin, a differentiation marker of tenocytes.. Dev Biol 2006 Oct 1;298(1):234-47.
            doi: 10.1016/j.ydbio.2006.06.036pubmed: 16876153google scholar: lookup
          32. Docheva D, Hunziker EB, Fässler R, Brandau O. Tenomodulin is necessary for tenocyte proliferation and tendon maturation.. Mol Cell Biol 2005 Jan;25(2):699-705.
          33. Franchi M, Trirè A, Quaranta M, Orsini E, Ottani V. Collagen structure of tendon relates to function.. ScientificWorldJournal 2007 Mar 30;7:404-20.
            pmc: PMC5901217pubmed: 17450305doi: 10.1100/tsw.2007.92google scholar: lookup
          34. Crossett B, Allen WR, Stewart F. A 19 kDa protein secreted by the endometrium of the mare is a novel member of the lipocalin family.. Biochem J 1996 Nov 15;320 ( Pt 1)(Pt 1):137-43.
            pmc: PMC1217908pubmed: 8947478doi: 10.1042/bj3200137google scholar: lookup
          35. 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
          36. 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.
            doi: 10.2746/042516403775467388pubmed: 12553472google scholar: lookup
          37. Fortier LA, Nixon AJ, Williams J, Cable CS. Isolation and chondrocytic differentiation of equine bone marrow-derived mesenchymal stem cells.. Am J Vet Res 1998 Sep;59(9):1182-7.
            pubmed: 9736400
          38. Vidal MA, Kilroy GE, Johnson JR, Lopez MJ, Moore RM, Gimble JM. Cell growth characteristics and differentiation frequency of adherent equine bone marrow-derived mesenchymal stromal cells: adipogenic and osteogenic capacity.. Vet Surg 2006 Oct;35(7):601-10.
          39. Lee RH, Kim B, Choi I, Kim H, Choi HS, Suh K, Bae YC, Jung JS. Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue.. Cell Physiol Biochem 2004;14(4-6):311-24.
            doi: 10.1159/000080341pubmed: 15319535google scholar: lookup
          40. Winter A, Breit S, Parsch D, Benz K, Steck E, Hauner H, Weber RM, Ewerbeck V, Richter W. Cartilage-like gene expression in differentiated human stem cell spheroids: a comparison of bone marrow-derived and adipose tissue-derived stromal cells.. Arthritis Rheum 2003 Feb;48(2):418-29.
            doi: 10.1002/art.10767pubmed: 12571852google scholar: lookup
          41. Kisiday JD, Kopesky PW, Evans CH, Grodzinsky AJ, McIlwraith CW, Frisbie DD. Evaluation of adult equine bone marrow- and adipose-derived progenitor cell chondrogenesis in hydrogel cultures.. J Orthop Res 2008 Mar;26(3):322-31.
            doi: 10.1002/jor.20508pubmed: 17960654google scholar: lookup
          42. 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
          43. Richardson LE, Dudhia J, Clegg PD, Smith R. Stem cells in veterinary medicine--attempts at regenerating equine tendon after injury.. Trends Biotechnol 2007 Sep;25(9):409-16.
            doi: 10.1016/j.tibtech.2007.07.009pubmed: 17692415google scholar: lookup
          44. Reed SA, Johnson SE. Equine umbilical cord blood contains a population of stem cells that express Oct4 and differentiate into mesodermal and endodermal cell types.. J Cell Physiol 2008 May;215(2):329-36.
            doi: 10.1002/jcp.21312pubmed: 17929245google scholar: lookup
          45. Kadiyala S, Young RG, Thiede MA, Bruder SP. Culture expanded canine mesenchymal stem cells possess osteochondrogenic potential in vivo and in vitro.. Cell Transplant 1997 Mar-Apr;6(2):125-34.
            doi: 10.1016/S0963-6897(96)00279-5pubmed: 9142444google scholar: lookup
          46. Izadpanah R, Joswig T, Tsien F, Dufour J, Kirijan JC, Bunnell BA. Characterization of multipotent mesenchymal stem cells from the bone marrow of rhesus macaques.. Stem Cells Dev 2005 Aug;14(4):440-51.
            doi: 10.1089/scd.2005.14.440pubmed: 16137233google scholar: lookup
          47. Saito S, Sawai K, Minamihashi A, Ugai H, Murata T, Yokoyama KK. Derivation, maintenance, and induction of the differentiation in vitro of equine embryonic stem cells.. Methods Mol Biol 2006;329:59-79.
            pubmed: 16845984doi: 10.1385/1-59745-037-5:59google scholar: lookup
          48. 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
          49. Anjos-Afonso F, Bonnet D. Nonhematopoietic/endothelial SSEA-1+ cells define the most primitive progenitors in the adult murine bone marrow mesenchymal compartment.. Blood 2007 Feb 1;109(3):1298-306.
            doi: 10.1182/blood-2006-06-030551pubmed: 17003364google scholar: lookup
          50. Chong AK, Ang AD, Goh JC, Hui JH, Lim AY, Lee EH, Lim BH. Bone marrow-derived mesenchymal stem cells influence early tendon-healing in a rabbit achilles tendon model.. J Bone Joint Surg Am 2007 Jan;89(1):74-81.
            doi: 10.2106/JBJS.E.01396pubmed: 17200313google scholar: lookup
          51. Herthel DJ. Enhanced suspenspory ligament healing in 100 horses by stem cell and other bone marrow components. Proceedings of the 47th AAEP Annual Convention 2001;47:319–321.
          52. 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.
            doi: 10.1089/ten.2007.0108pubmed: 17919069google scholar: lookup
          53. Ouyang HW, Goh JC, Mo XM, Teoh SH, Lee EH. The efficacy of bone marrow stromal cell-seeded knitted PLGA fiber scaffold for Achilles tendon repair.. Ann N Y Acad Sci 2002 Jun;961:126-9.
          54. Tasso R, Augello A, Carida' M, Postiglione F, Tibiletti MG, Bernasconi B, Astigiano S, Fais F, Truini M, Cancedda R, Pennesi G. Development of sarcomas in mice implanted with mesenchymal stem cells seeded onto bioscaffolds.. Carcinogenesis 2009 Jan;30(1):150-7.
            doi: 10.1093/carcin/bgn234pubmed: 18849298google scholar: lookup
          55. Horisberger MA. A method for prolonged survival of primary cell lines.. In Vitro Cell Dev Biol Anim 2006 May-Jun;42(5-6):143-8.
            doi: 10.1290/0511081.1pubmed: 16848633google scholar: lookup
          56. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.. Methods 2001 Dec;25(4):402-8.
            doi: 10.1006/meth.2001.1262pubmed: 11846609google scholar: lookup
          57. Sheehan DC, Hrapchak BB. Theory and practice of histotechnology. 2. St. Louis: Mosby; 1980.

          Citations

          This article has been cited 68 times.
          1. Jiang L, Lu J, Chen Y, Lyu K, Long L, Wang X, Liu T, Li S. Mesenchymal stem cells: An efficient cell therapy for tendon repair (Review).. Int J Mol Med 2023 Aug;52(2).
            doi: 10.3892/ijmm.2023.5273pubmed: 37387410google scholar: lookup
          2. Miescher I, Rieber J, Calcagni M, Buschmann J. In Vitro and In Vivo Effects of IGF-1 Delivery Strategies on Tendon Healing: A Review.. Int J Mol Sci 2023 Jan 25;24(3).
            doi: 10.3390/ijms24032370pubmed: 36768692google scholar: lookup
          3. Li ZJ, Yang QQ, Zhou YL. Biological and Mechanical Factors and Epigenetic Regulation Involved in Tendon Healing.. Stem Cells Int 2023;2023:4387630.
            doi: 10.1155/2023/4387630pubmed: 36655033google scholar: lookup
          4. Hafeez MN, d'Avanzo N, Russo V, Di Marzio L, Cilurzo F, Paolino D, Fresta M, Barboni B, Santos HA, Celia C. Tendon Tissue Repair in Prospective of Drug Delivery, Regenerative Medicines, and Innovative Bioscaffolds.. Stem Cells Int 2021;2021:1488829.
            doi: 10.1155/2021/1488829pubmed: 34824586google scholar: lookup
          5. Roberts JH, Halper J. Growth Factor Roles in Soft Tissue Physiology and Pathophysiology.. Adv Exp Med Biol 2021;1348:139-159.
            doi: 10.1007/978-3-030-80614-9_6pubmed: 34807418google scholar: lookup
          6. Zhang BY, Xu P, Luo Q, Song GB. Proliferation and tenogenic differentiation of bone marrow mesenchymal stem cells in a porous collagen sponge scaffold.. World J Stem Cells 2021 Jan 26;13(1):115-127.
            doi: 10.4252/wjsc.v13.i1.115pubmed: 33584983google scholar: lookup
          7. Yang F, Richardson DW. Comparative Analysis of Tenogenic Gene Expression in Tenocyte-Derived Induced Pluripotent Stem Cells and Bone Marrow-Derived Mesenchymal Stem Cells in Response to Biochemical and Biomechanical Stimuli.. Stem Cells Int 2021;2021:8835576.
            doi: 10.1155/2021/8835576pubmed: 33510795google scholar: lookup
          8. Lu M, Guo J, Wu B, Zhou Y, Wu M, Farzaneh M, Khoshnam SE. Mesenchymal Stem Cell-Mediated Mitochondrial Transfer: a Therapeutic Approach for Ischemic Stroke.. Transl Stroke Res 2021 Apr;12(2):212-229.
            doi: 10.1007/s12975-020-00853-6pubmed: 32975692google scholar: lookup
          9. Citeroni MR, Ciardulli MC, Russo V, Della Porta G, Mauro A, El Khatib M, Di Mattia M, Galesso D, Barbera C, Forsyth NR, Maffulli N, Barboni B. In Vitro Innovation of Tendon Tissue Engineering Strategies.. Int J Mol Sci 2020 Sep 14;21(18).
            doi: 10.3390/ijms21186726pubmed: 32937830google scholar: lookup
          10. Fan XL, Zhang Y, Li X, Fu QL. Mechanisms underlying the protective effects of mesenchymal stem cell-based therapy.. Cell Mol Life Sci 2020 Jul;77(14):2771-2794.
            doi: 10.1007/s00018-020-03454-6pubmed: 31965214google scholar: lookup
          11. Kim SE, Kim JG, Park K. Biomaterials for the Treatment of Tendon Injury.. Tissue Eng Regen Med 2019 Oct;16(5):467-477.
            doi: 10.1007/s13770-019-00217-8pubmed: 31624702google scholar: lookup
          12. Saud B, Malla R, Shrestha K. A Review on the Effect of Plant Extract on Mesenchymal Stem Cell Proliferation and Differentiation.. Stem Cells Int 2019;2019:7513404.
            doi: 10.1155/2019/7513404pubmed: 31428160google scholar: lookup
          13. 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
          14. Shojaee A, Parham A. Strategies of tenogenic differentiation of equine stem cells for tendon repair: current status and challenges.. Stem Cell Res Ther 2019 Jun 18;10(1):181.
            doi: 10.1186/s13287-019-1291-0pubmed: 31215490google scholar: lookup
          15. Rajpar I, Barrett JG. Optimizing growth factor induction of tenogenesis in three-dimensional culture of mesenchymal stem cells.. J Tissue Eng 2019 Jan-Dec;10:2041731419848776.
            doi: 10.1177/2041731419848776pubmed: 31205672google scholar: lookup
          16. 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
          17. Yu Y, Lee SY, Yang EJ, Kim HY, Jo I, Shin SJ. Expression of tenocyte lineage-related factors from tonsil-derived mesenchymal stem cells.. Tissue Eng Regen Med 2016 Apr;13(2):162-170.
            doi: 10.1007/s13770-016-9134-xpubmed: 30603396google scholar: lookup
          18. Pauly S, Klatte-Schulz F, Stahnke K, Scheibel M, Wildemann B. The effect of autologous platelet rich plasma on tenocytes of the human rotator cuff.. BMC Musculoskelet Disord 2018 Nov 30;19(1):422.
            doi: 10.1186/s12891-018-2339-5pubmed: 30497435google scholar: lookup
          19. Rink BE, Beyer T, French HM, Watson E, Aurich C, Donadeu FX. The Fate of Autologous Endometrial Mesenchymal Stromal Cells After Application in the Healthy Equine Uterus.. Stem Cells Dev 2018 Aug 1;27(15):1046-1052.
            doi: 10.1089/scd.2018.0056pubmed: 29790424google scholar: lookup
          20. Zhang YJ, Chen X, Li G, Chan KM, Heng BC, Yin Z, Ouyang HW. Concise Review: Stem Cell Fate Guided By Bioactive Molecules for Tendon Regeneration.. Stem Cells Transl Med 2018 May;7(5):404-414.
            doi: 10.1002/sctm.17-0206pubmed: 29573225google scholar: lookup
          21. Pöschke A, Krähling B, Failing K, Staszyk C. Molecular Characteristics of the Equine Periodontal Ligament.. Front Vet Sci 2017;4:235.
            doi: 10.3389/fvets.2017.00235pubmed: 29376061google scholar: lookup
          22. Yan Z, Yin H, Nerlich M, Pfeifer CG, Docheva D. Boosting tendon repair: interplay of cells, growth factors and scaffold-free and gel-based carriers.. J Exp Orthop 2018 Jan 5;5(1):1.
            doi: 10.1186/s40634-017-0117-1pubmed: 29330711google scholar: lookup
          23. Ishikawa S, Horinouchi C, Mizoguchi R, Senokuchi A, Kamikakimoto R, Murata D, Hatazoe T, Tozaki T, Misumi K, Hobo S. Isolation of equine peripheral blood stem cells from a Japanese native horse.. J Equine Sci 2017;28(4):153-158.
            doi: 10.1294/jes.28.153pubmed: 29270073google scholar: lookup
          24. Chiu CH, Lei KF, Yeh WL, Chen P, Chan YS, Hsu KY, Chen AC. Comparison between xCELLigence biosensor technology and conventional cell culture system for real-time monitoring human tenocytes proliferation and drugs cytotoxicity screening.. J Orthop Surg Res 2017 Oct 16;12(1):149.
            doi: 10.1186/s13018-017-0652-6pubmed: 29037195google scholar: lookup
          25. Ide J, Mochizuki Y, van Noort A, Ochi H, Sridharan S, Itoi E, Greiner S. Local rhBMP-12 on an Absorbable Collagen Sponge as an Adjuvant Therapy for Rotator Cuff Repair-A Phase 1, Randomized, Standard of Care Control, Multicenter Study: Part 2-A Pilot Study of Functional Recovery and Structural Outcomes.. Orthop J Sports Med 2017 Sep;5(9):2325967117726740.
            doi: 10.1177/2325967117726740pubmed: 28932752google scholar: lookup
          26. Geburek F, Roggel F, van Schie HTM, Beineke A, Estrada R, Weber K, Hellige M, Rohn K, Jagodzinski M, Welke B, Hurschler C, Conrad S, Skutella T, van de Lest C, van Weeren R, Stadler PM. Effect of single intralesional treatment of surgically induced equine superficial digital flexor tendon core lesions with adipose-derived mesenchymal stromal cells: a controlled experimental trial.. Stem Cell Res Ther 2017 Jun 5;8(1):129.
            doi: 10.1186/s13287-017-0564-8pubmed: 28583184google scholar: lookup
          27. Grafe I, Alexander S, Peterson JR, Snider TN, Levi B, Lee B, Mishina Y. TGF-β Family Signaling in Mesenchymal Differentiation.. Cold Spring Harb Perspect Biol 2018 May 1;10(5).
            doi: 10.1101/cshperspect.a022202pubmed: 28507020google scholar: lookup
          28. Zahedi M, Parham A, Dehghani H, Mehrjerdi HK. Stemness Signature of Equine Marrow-derived Mesenchymal Stem Cells.. Int J Stem Cells 2017 May 30;10(1):93-102.
            doi: 10.15283/ijsc16036pubmed: 28222255google scholar: lookup
          29. Ishikawa S, Horinouchi C, Murata D, Matsuzaki S, Misumi K, Iwamoto Y, Korosue K, Hobo S. Isolation and characterization of equine dental pulp stem cells derived from Thoroughbred wolf teeth.. J Vet Med Sci 2017 Jan 20;79(1):47-51.
            doi: 10.1292/jvms.16-0131pubmed: 27818457google scholar: lookup
          30. Yang G, Rothrauff BB, Lin H, Yu S, Tuan RS. Tendon-Derived Extracellular Matrix Enhances Transforming Growth Factor-β3-Induced Tenogenic Differentiation of Human Adipose-Derived Stem Cells.. Tissue Eng Part A 2017 Feb;23(3-4):166-176.
            doi: 10.1089/ten.TEA.2015.0498pubmed: 27809678google scholar: lookup
          31. Walden G, Liao X, Donell S, Raxworthy MJ, Riley GP, Saeed A. A Clinical, Biological, and Biomaterials Perspective into Tendon Injuries and Regeneration.. Tissue Eng Part B Rev 2017 Feb;23(1):44-58.
            doi: 10.1089/ten.TEB.2016.0181pubmed: 27596929google scholar: lookup
          32. Ridzuan N, Al Abbar A, Yip WK, Maqbool M, Ramasamy R. Characterization and Expression of Senescence Marker in Prolonged Passages of Rat Bone Marrow-Derived Mesenchymal Stem Cells.. Stem Cells Int 2016;2016:8487264.
            doi: 10.1155/2016/8487264pubmed: 27579045google scholar: lookup
          33. Murata D, Yamasaki A, Matsuzaki S, Sunaga T, Fujiki M, Tokunaga S, Misumi K. Characteristics and multipotency of equine dedifferentiated fat cells.. J Equine Sci 2016;27(2):57-65.
            doi: 10.1294/jes.27.57pubmed: 27330399google scholar: lookup
          34. Zhang X, Lin YC, Rui YF, Xu HL, Chen H, Wang C, Teng GJ. Therapeutic Roles of Tendon Stem/Progenitor Cells in Tendinopathy.. Stem Cells Int 2016;2016:4076578.
            doi: 10.1155/2016/4076578pubmed: 27195010google scholar: lookup
          35. Dex S, Lin D, Shukunami C, Docheva D. Tenogenic modulating insider factor: Systematic assessment on the functions of tenomodulin gene.. Gene 2016 Aug 1;587(1):1-17.
            doi: 10.1016/j.gene.2016.04.051pubmed: 27129941google scholar: lookup
          36. Shikh Alsook MK, Gabriel A, Piret J, Waroux O, Tonus C, Connan D, Baise E, Antoine N. Tissues from equine cadaver ligaments up to 72 hours 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
          37. Lombana KG, Goodrich LR, Phillips JN, Kisiday JD, Ruple-Czerniak A, McIlwraith CW. An Investigation of Equine Mesenchymal Stem Cell Characteristics from Different Harvest Sites: More Similar Than Not.. Front Vet Sci 2015;2:67.
            doi: 10.3389/fvets.2015.00067pubmed: 26664993google scholar: lookup
          38. Li Y, Ramcharan M, Zhou Z, Leong DJ, Akinbiyi T, Majeska RJ, Sun HB. The Role of Scleraxis in Fate Determination of Mesenchymal Stem Cells for Tenocyte Differentiation.. Sci Rep 2015 Aug 20;5:13149.
            doi: 10.1038/srep13149pubmed: 26289033google scholar: lookup
          39. Lin C, Shen M, Chen W, Li X, Luo D, Cai J, Yang Y. Isolation and purification of rabbit mesenchymal stem cells using an optimized protocol.. In Vitro Cell Dev Biol Anim 2015 Nov;51(10):1102-8.
            doi: 10.1007/s11626-015-9933-8pubmed: 26202303google scholar: lookup
          40. Dai L, Hu X, Zhang X, Zhu J, Zhang J, Fu X, Duan X, Ao Y, Zhou C. Different tenogenic differentiation capacities of different mesenchymal stem cells in the presence of BMP-12.. J Transl Med 2015 Jun 24;13:200.
            doi: 10.1186/s12967-015-0560-7pubmed: 26104414google scholar: lookup
          41. 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
          42. Mohamad-Fauzi N, Ross PJ, Maga EA, Murray JD. Impact of source tissue and ex vivo expansion on the characterization of goat mesenchymal stem cells.. J Anim Sci Biotechnol 2015;6(1):1.
            doi: 10.1186/2049-1891-6-1pubmed: 25838897google scholar: lookup
          43. Younesi M, Islam A, Kishore V, Anderson JM, Akkus O. Tenogenic Induction of Human MSCs by Anisotropically Aligned Collagen Biotextiles.. Adv Funct Mater 2014 Sep 24;24(36):5762-5770.
            doi: 10.1002/adfm.201400828pubmed: 25750610google scholar: lookup
          44. Guevara-Alvarez A, Schmitt A, Russell RP, Imhoff AB, Buchmann S. Growth factor delivery vehicles for tendon injuries: Mesenchymal stem cells and Platelet Rich Plasma.. Muscles Ligaments Tendons J 2014 Jul;4(3):378-85.
            pubmed: 25489557
          45. Mohanty N, Gulati BR, Kumar R, Gera S, Kumar S, Kumar P, Yadav PS. Phenotypical and functional characteristics of mesenchymal stem cells derived from equine umbilical cord blood.. Cytotechnology 2016 Aug;68(4):795-807.
            doi: 10.1007/s10616-014-9831-zpubmed: 25487085google scholar: lookup
          46. Docheva D, Müller SA, Majewski M, Evans CH. Biologics for tendon repair.. Adv Drug Deliv Rev 2015 Apr;84:222-39.
            doi: 10.1016/j.addr.2014.11.015pubmed: 25446135google scholar: lookup
          47. Taha MF, Javeri A, Rohban S, Mowla SJ. Upregulation of pluripotency markers in adipose tissue-derived stem cells by miR-302 and leukemia inhibitory factor.. Biomed Res Int 2014;2014:941486.
            doi: 10.1155/2014/941486pubmed: 25147827google scholar: lookup
          48. Schon LC, Gill N, Thorpe M, Davis J, Nadaud J, Kim J, Molligan J, Zhang Z. Efficacy of a mesenchymal stem cell loaded surgical mesh for tendon repair in rats.. J Transl Med 2014 May 2;12:110.
            doi: 10.1186/1479-5876-12-110pubmed: 24884819google scholar: lookup
          49. Cadby JA, Buehler E, Godbout C, van Weeren PR, Snedeker JG. Differences between the cell populations from the peritenon and the tendon core with regard to their potential implication in tendon repair.. PLoS One 2014;9(3):e92474.
            doi: 10.1371/journal.pone.0092474pubmed: 24651449google scholar: lookup
          50. Mohanty N, Gulati BR, Kumar R, Gera S, Kumar P, Somasundaram RK, Kumar S. Immunophenotypic characterization and tenogenic differentiation of mesenchymal stromal cells isolated from equine umbilical cord blood.. In Vitro Cell Dev Biol Anim 2014 Jun;50(6):538-48.
            doi: 10.1007/s11626-013-9729-7pubmed: 24414976google scholar: lookup
          51. Liu Z, Wang W, Gao J, Zhou H, Zhang Y. Isolation, culture, and induced multiple differentiation of Mongolian sheep bone marrow-derived mesenchymal stem cells.. In Vitro Cell Dev Biol Anim 2014;50(5):464-74.
            doi: 10.1007/s11626-013-9725-ypubmed: 24399254google scholar: lookup
          52. Fredriksson M, Li Y, Stålman A, Haldosén LA, Felländer-Tsai L. Diclofenac and triamcinolone acetonide impair tenocytic differentiation and promote adipocytic differentiation of mesenchymal stem cells.. J Orthop Surg Res 2013 Sep 2;8:30.
            doi: 10.1186/1749-799X-8-30pubmed: 24004657google scholar: lookup
          53. Via AG, Frizziero A, Oliva F. Biological properties of mesenchymal Stem Cells from different sources.. Muscles Ligaments Tendons J 2012 Jul;2(3):154-62.
            pubmed: 23738292
          54. Singh J, Mann A, Kumar D, Duhan JS, Yadav PS. Cultured buffalo umbilical cord matrix cells exhibit characteristics of multipotent mesenchymal stem cells.. In Vitro Cell Dev Biol Anim 2013 Jun;49(6):408-16.
            doi: 10.1007/s11626-013-9617-1pubmed: 23708916google scholar: lookup
          55. Lomas AJ, Webb WR, Han J, Chen GQ, Sun X, Zhang Z, El Haj AJ, Forsyth NR. Poly (3-hydroxybutyrate-co-3-hydroxyhexanoate)/collagen hybrid scaffolds for tissue engineering applications.. Tissue Eng Part C Methods 2013 Aug;19(8):577-85.
            doi: 10.1089/ten.TEC.2012.0457pubmed: 23281705google scholar: lookup
          56. Ranera B, Remacha AR, Álvarez-Arguedas S, Romero A, Vázquez FJ, Zaragoza P, Martín-Burriel I, Rodellar C. Effect of hypoxia on equine mesenchymal stem cells derived from bone marrow and adipose tissue.. BMC Vet Res 2012 Aug 22;8:142.
            doi: 10.1186/1746-6148-8-142pubmed: 22913590google scholar: lookup
          57. Khodadadi K, Sumer H, Pashaiasl M, Lim S, Williamson M, Verma PJ. Induction of pluripotency in adult equine fibroblasts without c-MYC.. Stem Cells Int 2012;2012:429160.
            doi: 10.1155/2012/429160pubmed: 22550508google scholar: lookup
          58. Sharma RI, Snedeker JG. Paracrine interactions between mesenchymal stem cells affect substrate driven differentiation toward tendon and bone phenotypes.. PLoS One 2012;7(2):e31504.
            doi: 10.1371/journal.pone.0031504pubmed: 22355373google scholar: lookup
          59. Majewski M, Porter RM, Betz OB, Betz VM, Clahsen H, Flückiger R, Evans CH. Improvement of tendon repair using muscle grafts transduced with TGF-β1 cDNA.. Eur Cell Mater 2012 Feb 16;23:94-101; discussion 101-2.
            doi: 10.22203/ecm.v023a07pubmed: 22354460google scholar: lookup
          60. Kishore V, Bullock W, Sun X, Van Dyke WS, Akkus O. Tenogenic differentiation of human MSCs induced by the topography of electrochemically aligned collagen threads.. Biomaterials 2012 Mar;33(7):2137-44.
          61. Bais MV, Shabin ZM, Young M, Einhorn TA, Kotton DN, Gerstnefeld LC. Role of Nanog in the maintenance of marrow stromal stem cells during post natal bone regeneration.. Biochem Biophys Res Commun 2012 Jan 6;417(1):211-6.
            doi: 10.1016/j.bbrc.2011.11.087pubmed: 22142851google scholar: lookup
          62. Violini S, Gorni C, Pisani LF, Ramelli P, Caniatti M, Mariani P. Isolation and differentiation potential of an equine amnion-derived stromal cell line.. Cytotechnology 2012 Jan;64(1):1-7.
            doi: 10.1007/s10616-011-9398-xpubmed: 21994048google scholar: lookup
          63. Mensing N, Gasse H, Hambruch N, Haeger JD, Pfarrer C, Staszyk C. Isolation and characterization of multipotent mesenchymal stromal cells from the gingiva and the periodontal ligament of the horse.. BMC Vet Res 2011 Aug 2;7:42.
            doi: 10.1186/1746-6148-7-42pubmed: 21810270google scholar: lookup
          64. Raabe O, Shell K, Würtz A, Reich CM, Wenisch S, Arnhold S. Further insights into the characterization of equine adipose tissue-derived mesenchymal stem cells.. Vet Res Commun 2011 Aug;35(6):355-65.
            doi: 10.1007/s11259-011-9480-zpubmed: 21614641google scholar: lookup
          65. Lee JY, Zhou Z, Taub PJ, Ramcharan M, Li Y, Akinbiyi T, Maharam ER, Leong DJ, Laudier DM, Ruike T, Torina PJ, Zaidi M, Majeska RJ, Schaffler MB, Flatow EL, Sun HB. BMP-12 treatment of adult mesenchymal stem cells in vitro augments tendon-like tissue formation and defect repair in vivo.. PLoS One 2011 Mar 11;6(3):e17531.
            doi: 10.1371/journal.pone.0017531pubmed: 21412429google scholar: lookup
          66. Gurkan UA, Cheng X, Kishore V, Uquillas JA, Akkus O. Comparison of morphology, orientation, and migration of tendon derived fibroblasts and bone marrow stromal cells on electrochemically aligned collagen constructs.. J Biomed Mater Res A 2010 Sep 15;94(4):1070-9.
            doi: 10.1002/jbm.a.32783pubmed: 20694974google scholar: lookup
          67. Luo Q, Song G, Song Y, Xu B, Qin J, Shi Y. Indirect co-culture with tenocytes promotes proliferation and mRNA expression of tendon/ligament related genes in rat bone marrow mesenchymal stem cells.. Cytotechnology 2009 Nov;61(1-2):1-10.
            doi: 10.1007/s10616-009-9233-9pubmed: 19842053google scholar: lookup
          68. Abate M, Silbernagel KG, Siljeholm C, Di Iorio A, De Amicis D, Salini V, Werner S, Paganelli R. Pathogenesis of tendinopathies: inflammation or degeneration?. Arthritis Res Ther 2009;11(3):235.
            doi: 10.1186/ar2723pubmed: 19591655google scholar: lookup