FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Sci Rep / Differences in the intrinsic chondrogenic potential of equin...
Scientific reports2018; 8(1); 13799; doi: 10.1038/s41598-018-28164-9

Differences in the intrinsic chondrogenic potential of equine umbilical cord matrix and cord blood mesenchymal stromal/stem cells for cartilage regeneration.

Abstract: Umbilical cord blood mesenchymal stromal/stem cells (UCB-MSCs) and umbilical cord matrix MSCs (UCM-MSCs) have chondrogenic potential and are alternative sources to standard surgically derived bone marrow or adipose tissue collection for cartilage engineering. However, the majority of comparative studies explore neonatal MSCs potential only on ISCT benchmark assays accounting for some bias in the reproducibility between in vitro and in clinical studies. Therefore, we characterized equine UCB-MSCs and UCM-MSCs and investigated with particular attention their chondrogenesis potential in 3D culture with BMP-2 + TGF-ß1 in normoxia or hypoxia. We carried out an exhaustive characterization of the extracellular matrix generated by both these two types of MSCs after the induction of chondrogenesis through evaluation of hyaline cartilage, hypertrophic and osteogenic markers (mRNA, protein and histology levels). Some differences in hypoxia sensitivity and chondrogenesis were observed. UCB-MSCs differentiated into chondrocytes express an abundant, dense and a hyaline-like cartilage matrix. By contrast, despite their expression of cartilage markers, UCM-MSCs failed to express a relevant cartilage matrix after chondrogenic induction. Both MSCs types also displayed intrinsic differences at their undifferentiated basal status, UCB-MSCs expressing higher levels of chondrogenic markers whereas UCM-MSCs synthesizing higher amounts of osteogenic markers. Our results suggest that UCB-MSCs should be preferred for ex-vivo horse cartilage engineering. How those results should be translated to in vivo direct cartilage regeneration remains to be determined through dedicated study.
Get Full Text
Publication Date: 2018-09-14 PubMed ID: 30217993PubMed Central: PMC6138671DOI: 10.1038/s41598-018-28164-9Google 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.
LinkedInCopy
  • 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 investigates the potential for using two types of stem cells (mesenchymal stromal stem cells from umbilical cord blood and umbilical cord matrix) for cartilage regeneration in horses, finding that umbilical cord blood stem cells show superior results for this purpose.

Introduction to the Research

  • This article takes a deep dive into the potential of mesenchymal stromal/stem cells (MSCs) which are derived from umbilical cord blood (UCB) and umbilical cord matrix (UCM) to regenerate cartilage cells.
  • Researchers have considered these types of stem cells as an alternative approach to commonly used surgical methods for collecting bone marrow or adipose tissue which are used in cartilage engineering.

Methodology and Testing

  • The researchers used specific tests to characterize the equine-derivative of these two types of MSCs, and they examined their potential for generating cartilage cells.
  • They used 3D culture with specific growth factors (BMP-2 + TGF-ß1) in different oxygen conditions (normoxia or hypoxia) to observe the behavior of the cells.
  • They analyzed the extracellular matrix generated by both types of MSCs after inducing them to become chondrocytes (cartilage cells).
  • The analysis involved assessing markers associated with hyaline cartilage, hypertrophic markers, and osteogenic markers at various levels (mRNA, protein, and histology).

Findings and Differences between the MSCs

  • There were some differences observed in how the two types of stem cells reacted under low oxygen conditions and their ability to transform into cartilage cells.
  • UCB-MSCs showed promising results as they transformed into chondrocytes and produced an abundant and dense hyaline-like cartilage matrix.
  • The UCM-MSCs exhibited expression of cartilage biomarkers, but they did not create a significant cartilage matrix even after they were induced to become chondrocytes.
  • Moreover, the two types of MSCs showed intrinsic differences even in their undifferentiated states, with UCB-MSCs expressing higher levels of cartilage markers and UCM-MSCs producing higher amounts of markers associated with bone formation.

Conclusion and Future Directions

  • Based on the findings, the researchers suggested that UCB-MSCs could be a more suitable choice for engineering horse cartilage in lab settings.
  • However, it is not established how these results can be applied to direct cartilage regeneration in a live organism, which requires further investigation.

Cite This Article

APA
Rakic R, Bourdon B, Demoor M, Maddens S, Saulnier N, Galéra P. (2018). Differences in the intrinsic chondrogenic potential of equine umbilical cord matrix and cord blood mesenchymal stromal/stem cells for cartilage regeneration. Sci Rep, 8(1), 13799. https://doi.org/10.1038/s41598-018-28164-9

Publication

Scientific reports
ISSN: 2045-2322
NlmUniqueID: 101563288
Country: England
Language: English
Volume: 8
Issue: 1
Pages: 13799
PII: 13799

Researcher Affiliations

Rakic, Rodolphe
  • Normandie Univ, Unicaen, Biotargen, Caen, 14000 Caen, France.
  • Vetbiobank, 69280, Marcy l'Etoile, France.
Bourdon, Bastien
  • Normandie Univ, Unicaen, Biotargen, Caen, 14000 Caen, France.
Demoor, Magali
  • Normandie Univ, Unicaen, Biotargen, Caen, 14000 Caen, France.
Maddens, Stéphane
  • Vetbiobank, 69280, Marcy l'Etoile, France.
Saulnier, Nathalie
  • Vetbiobank, 69280, Marcy l'Etoile, France.
Galéra, Philippe
  • Normandie Univ, Unicaen, Biotargen, Caen, 14000 Caen, France. philippe.galera@unicaen.fr.

MeSH Terms

  • Animals
  • Bone Morphogenetic Protein 2 / metabolism
  • Cartilage / metabolism
  • Cell Differentiation / drug effects
  • Cells, Cultured
  • Chondrocytes / metabolism
  • Chondrogenesis / genetics
  • Chondrogenesis / physiology
  • Collagen Type I / metabolism
  • Extracellular Matrix / chemistry
  • Extracellular Matrix / metabolism
  • Fetal Blood / cytology
  • Fetal Blood / physiology
  • Horses
  • Hyaline Cartilage / metabolism
  • Mesenchymal Stem Cells / physiology
  • Osteogenesis / drug effects
  • Regeneration / drug effects
  • Reproducibility of Results
  • Tissue Engineering / methods
  • Transforming Growth Factor beta1 / metabolism
  • Umbilical Cord / cytology
  • Umbilical Cord / physiology

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 63 references
  1. Uccelli A, Moretta L, Pistoia V. Mesenchymal stem cells in health and disease.. Nat Rev Immunol 2008 Sep;8(9):726-36.
    pubmed: 19172693doi: 10.1038/nri2395google scholar: lookup
  2. Choudhery MS, Badowski M, Muise A, Pierce J, Harris DT. Donor age negatively impacts adipose tissue-derived mesenchymal stem cell expansion and differentiation.. J Transl Med 2014 Jan 7;12:8.
    pmc: PMC3895760pubmed: 24397850doi: 10.1186/1479-5876-12-8google scholar: lookup
  3. Stolzing A, Jones E, McGonagle D, Scutt A. Age-related changes in human bone marrow-derived mesenchymal stem cells: consequences for cell therapies.. Mech Ageing Dev 2008 Mar;129(3):163-73.
    pubmed: 18241911doi: 10.1016/j.mad.2007.12.002google scholar: lookup
  4. Mareschi K, Ferrero I, Rustichelli D, Aschero S, Gammaitoni L, Aglietta M, Madon E, Fagioli F. Expansion of mesenchymal stem cells isolated from pediatric and adult donor bone marrow.. J Cell Biochem 2006 Mar 1;97(4):744-54.
    pubmed: 16229018doi: 10.1002/jcb.20681google scholar: lookup
  5. Kern S, Eichler H, Stoeve J, Klüter H, Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue.. Stem Cells 2006 May;24(5):1294-301.
    pubmed: 16410387doi: 10.1634/stemcells.2005-0342google scholar: lookup
  6. Carlin R, Davis D, Weiss M, Schultz B, Troyer D. Expression of early transcription factors Oct-4, Sox-2 and Nanog by porcine umbilical cord (PUC) matrix cells.. Reprod Biol Endocrinol 2006 Feb 6;4:8.
    pmc: PMC1373634pubmed: 16460563doi: 10.1186/1477-7827-4-8google scholar: lookup
  7. Nekanti U, Mohanty L, Venugopal P, Balasubramanian S, Totey S, Ta M. Optimization and scale-up of Wharton's jelly-derived mesenchymal stem cells for clinical applications.. Stem Cell Res 2010 Nov;5(3):244-54.
    pubmed: 20880767doi: 10.1016/j.scr.2010.08.005google scholar: lookup
  8. 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.
    pmc: PMC1904213pubmed: 17537254doi: 10.1186/1472-6750-7-26google scholar: lookup
  9. Iacono E, Brunori L, Pirrone A, Pagliaro PP, Ricci F, Tazzari PL, Merlo B. Isolation, characterization and differentiation of mesenchymal stem cells from amniotic fluid, umbilical cord blood and Wharton's jelly in the horse.. Reproduction 2012 Apr;143(4):455-68.
    pubmed: 22274885doi: 10.1530/rep-10-0408google scholar: lookup
  10. De Schauwer C, van de Walle GR, Piepers S, Hoogewijs MK, Govaere JL, Meyer E, van Soom A. Successful isolation of equine mesenchymal stromal cells from cryopreserved umbilical cord blood-derived mononuclear cell fractions.. Equine Vet J 2013 Jul;45(4):518-22.
    pubmed: 23206252doi: 10.1111/evj.12003google scholar: lookup
  11. 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.
    pmc: PMC4960129pubmed: 25487085doi: 10.1007/s10616-014-9831-zgoogle scholar: lookup
  12. 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.
    pubmed: 21193959doi: 10.1007/s11259-010-9457-3google scholar: lookup
  13. 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.
    pubmed: 21948689doi: 10.1002/term.465google scholar: lookup
  14. Carrade DD, Owens SD, Galuppo LD, Vidal MA, Ferraro GL, Librach F, Buerchler S, Friedman MS, Walker NJ, Borjesson DL. Clinicopathologic findings following intra-articular injection of autologous and allogeneic placentally derived equine mesenchymal stem cells in horses.. Cytotherapy 2011 Apr;13(4):419-30.
    pubmed: 21105841doi: 10.3109/14653249.2010.536213google scholar: lookup
  15. Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, Deans RJ, Krause DS, Keating A. Clarification of the nomenclature for MSC: The International Society for Cellular Therapy position statement.. Cytotherapy 2005;7(5):393-5.
    pubmed: 16236628doi: 10.1080/14653240500319234google scholar: lookup
  16. Samsonraj RM, Rai B, Sathiyanathan P, Puan KJ, Rötzschke O, Hui JH, Raghunath M, Stanton LW, Nurcombe V, Cool SM. Establishing criteria for human mesenchymal stem cell potency.. Stem Cells 2015 Jun;33(6):1878-91.
    pmc: PMC5363381pubmed: 25752682doi: 10.1002/stem.1982google scholar: lookup
  17. Branly T, Bertoni L, Contentin R, Rakic R, Gomez-Leduc T, Desancé M, Hervieu M, Legendre F, Jacquet S, Audigié F, Denoix JM, Demoor M, Galéra P. Characterization and use of Equine Bone Marrow Mesenchymal Stem Cells in Equine Cartilage Engineering. Study of their Hyaline Cartilage Forming Potential when Cultured under Hypoxia within a Biomaterial in the Presence of BMP-2 and TGF-ß1.. Stem Cell Rev Rep 2017 Oct;13(5):611-630.
    pubmed: 28597211doi: 10.1007/s12015-017-9748-ygoogle scholar: lookup
  18. Kopesky PW, Lee HY, Vanderploeg EJ, Kisiday JD, Frisbie DD, Plaas AH, Ortiz C, Grodzinsky AJ. Adult equine bone marrow stromal cells produce a cartilage-like ECM mechanically superior to animal-matched adult chondrocytes.. Matrix Biol 2010 Jun;29(5):427-38.
    pmc: PMC2894996pubmed: 20153827doi: 10.1016/j.matbio.2010.02.003google scholar: lookup
  19. Watts AE, Ackerman-Yost JC, Nixon AJ. A comparison of three-dimensional culture systems to evaluate in vitro chondrogenesis of equine bone marrow-derived mesenchymal stem cells.. Tissue Eng Part A 2013 Oct;19(19-20):2275-83.
    pmc: PMC3761431pubmed: 23725547doi: 10.1089/ten.tea.2012.0479google scholar: lookup
  20. Lo WC, Chen WH, Lin TC, Hwang SM, Zeng R, Hsu WC, Chiang YM, Liu MC, Williams DF, Deng WP. Preferential therapy for osteoarthritis by cord blood MSCs through regulation of chondrogenic cytokines.. Biomaterials 2013 Jul;34(20):4739-48.
    pubmed: 23557858doi: 10.1016/j.biomaterials.2013.03.016google scholar: lookup
  21. Zhang X, Hirai M, Cantero S, Ciubotariu R, Dobrila L, Hirsh A, Igura K, Satoh H, Yokomi I, Nishimura T, Yamaguchi S, Yoshimura K, Rubinstein P, Takahashi TA. Isolation and characterization of mesenchymal stem cells from human umbilical cord blood: reevaluation of critical factors for successful isolation and high ability to proliferate and differentiate to chondrocytes as compared to mesenchymal stem cells from bone marrow and adipose tissue.. J Cell Biochem 2011 Apr;112(4):1206-18.
    pubmed: 21312238doi: 10.1002/jcb.23042google scholar: lookup
  22. Bailey MM, Wang L, Bode CJ, Mitchell KE, Detamore MS. A comparison of human umbilical cord matrix stem cells and temporomandibular joint condylar chondrocytes for tissue engineering temporomandibular joint condylar cartilage.. Tissue Eng 2007 Aug;13(8):2003-10.
    pubmed: 17518722doi: 10.1089/ten.2006.0150google scholar: lookup
  23. Bosch J, Houben AP, Radke TF, Stapelkamp D, Bünemann E, Balan P, Buchheiser A, Liedtke S, Kögler G. Distinct differentiation potential of "MSC" derived from cord blood and umbilical cord: are cord-derived cells true mesenchymal stromal cells?. Stem Cells Dev 2012 Jul 20;21(11):1977-88.
    pubmed: 22087798doi: 10.1089/scd.2011.0414google scholar: lookup
  24. Chen X, Zhang F, He X, Xu Y, Yang Z, Chen L, Zhou S, Yang Y, Zhou Z, Sheng W, Zeng Y. Chondrogenic differentiation of umbilical cord-derived mesenchymal stem cells in type I collagen-hydrogel for cartilage engineering.. Injury 2013 Apr;44(4):540-9.
    pubmed: 23337703doi: 10.1016/j.injury.2012.09.024google scholar: lookup
  25. Liu S, Hou KD, Yuan M, Peng J, Zhang L, Sui X, Zhao B, Xu W, Wang A, Lu S, Guo Q. Characteristics of mesenchymal stem cells derived from Wharton's jelly of human umbilical cord and for fabrication of non-scaffold tissue-engineered cartilage.. J Biosci Bioeng 2014 Feb;117(2):229-235.
    pubmed: 23899897doi: 10.1016/j.jbiosc.2013.07.001google scholar: lookup
  26. Reppel L, Schiavi J, Charif N, Leger L, Yu H, Pinzano A, Henrionnet C, Stoltz JF, Bensoussan D, Huselstein C. Chondrogenic induction of mesenchymal stromal/stem cells from Wharton's jelly embedded in alginate hydrogel and without added growth factor: an alternative stem cell source for cartilage tissue engineering.. Stem Cell Res Ther 2015 Dec 30;6:260.
    pmc: PMC4697319pubmed: 26718750doi: 10.1186/s13287-015-0263-2google scholar: lookup
  27. Demoor M, Ollitrault D, Gomez-Leduc T, Bouyoucef M, Hervieu M, Fabre H, Lafont J, Denoix JM, Audigié F, Mallein-Gerin F, Legendre F, Galera P. Cartilage tissue engineering: molecular control of chondrocyte differentiation for proper cartilage matrix reconstruction.. Biochim Biophys Acta 2014 Aug;1840(8):2414-40.
    pubmed: 24608030doi: 10.1016/j.bbagen.2014.02.030google scholar: lookup
  28. Yang L, Tsang KY, Tang HC, Chan D, Cheah KS. Hypertrophic chondrocytes can become osteoblasts and osteocytes in endochondral bone formation.. Proc Natl Acad Sci U S A 2014 Aug 19;111(33):12097-102.
    pmc: PMC4143064pubmed: 25092332doi: 10.1073/pnas.1302703111google scholar: lookup
  29. Ghone NV, Grayson WL. Recapitulation of mesenchymal condensation enhances in vitro chondrogenesis of human mesenchymal stem cells.. J Cell Physiol 2012 Nov;227(11):3701-8.
    pubmed: 22378248doi: 10.1002/jcp.24078google scholar: lookup
  30. Handorf AM, Li WJ. Induction of mesenchymal stem cell chondrogenesis through sequential administration of growth factors within specific temporal windows.. J Cell Physiol 2014 Feb;229(2):162-71.
    pubmed: 23996894doi: 10.1002/jcp.24428google scholar: lookup
  31. Lee HH, Chang CC, Shieh MJ, Wang JP, Chen YT, Young TH, Hung SC. Hypoxia enhances chondrogenesis and prevents terminal differentiation through PI3K/Akt/FoxO dependent anti-apoptotic effect.. Sci Rep 2013;3:2683.
    pmc: PMC3775095pubmed: 24042188doi: 10.1038/srep02683google scholar: lookup
  32. Gómez-Leduc T, Hervieu M, Legendre F, Bouyoucef M, Gruchy N, Poulain L, de Vienne C, Herlicoviez M, Demoor M, Galéra P. Chondrogenic commitment of human umbilical cord blood-derived mesenchymal stem cells in collagen matrices for cartilage engineering.. Sci Rep 2016 Sep 8;6:32786.
    pmc: PMC5015060pubmed: 27604951doi: 10.1038/srep32786google scholar: lookup
  33. Rakic R, Bourdon B, Hervieu M, Branly T, Legendre F, Saulnier N, Audigié F, Maddens S, Demoor M, Galera P. RNA Interference and BMP-2 Stimulation Allows Equine Chondrocytes Redifferentiation in 3D-Hypoxia Cell Culture Model: Application for Matrix-Induced Autologous Chondrocyte Implantation.. Int J Mol Sci 2017 Aug 24;18(9).
    pmc: PMC5618491pubmed: 28837082doi: 10.3390/ijms18091842google scholar: lookup
  34. Tiaden AN, Breiden M, Mirsaidi A, Weber FA, Bahrenberg G, Glanz S, Cinelli P, Ehrmann M, Richards PJ. Human serine protease HTRA1 positively regulates osteogenesis of human bone marrow-derived mesenchymal stem cells and mineralization of differentiating bone-forming cells through the modulation of extracellular matrix protein.. Stem Cells 2012 Oct;30(10):2271-82.
    pubmed: 22865667doi: 10.1002/stem.1190google scholar: lookup
  35. Frisbie DD, Bowman SM, Colhoun HA, DiCarlo EF, Kawcak CE, McIlwraith CW. Evaluation of autologous chondrocyte transplantation via a collagen membrane in equine articular defects: results at 12 and 18 months.. Osteoarthritis Cartilage 2008 Jun;16(6):667-79.
    pubmed: 18042409doi: 10.1016/j.joca.2007.09.013google scholar: lookup
  36. Makris EA, Gomoll AH, Malizos KN, Hu JC, Athanasiou KA. Repair and tissue engineering techniques for articular cartilage.. Nat Rev Rheumatol 2015 Jan;11(1):21-34.
    pmc: PMC4629810pubmed: 25247412doi: 10.1038/nrrheum.2014.157google scholar: lookup
  37. Suzuki S, Muneta T, Tsuji K, Ichinose S, Makino H, Umezawa A, Sekiya I. Properties and usefulness of aggregates of synovial mesenchymal stem cells as a source for cartilage regeneration.. Arthritis Res Ther 2012 Jun 7;14(3):R136.
    pmc: PMC3446519pubmed: 22676383doi: 10.1186/ar3869google scholar: lookup
  38. Ortega N, Behonick DJ, Werb Z. Matrix remodeling during endochondral ossification.. Trends Cell Biol 2004 Feb;14(2):86-93.
    pmc: PMC2779708pubmed: 15102440doi: 10.1016/j.tcb.2003.12.003google scholar: lookup
  39. Holt DW, Henderson ML, Stockdale CE, Farrell JT, Kooyman DL, Bridgewater LC, Seegmiller RE. Osteoarthritis-like changes in the heterozygous sedc mouse associated with the HtrA1-Ddr2-Mmp-13 degradative pathway: a new model of osteoarthritis.. Osteoarthritis Cartilage 2012 May;20(5):430-439.
    pubmed: 22155431doi: 10.1016/j.joca.2011.11.008google scholar: lookup
  40. Tiaden AN, Breiden M, Mirsaidi A, Weber FA, Bahrenberg G, Glanz S, Cinelli P, Ehrmann M, Richards PJ. Human serine protease HTRA1 positively regulates osteogenesis of human bone marrow-derived mesenchymal stem cells and mineralization of differentiating bone-forming cells through the modulation of extracellular matrix protein.. Stem Cells 2012 Oct;30(10):2271-82.
    pubmed: 22865667doi: 10.1002/stem.1190google scholar: lookup
  41. Xu L, Golshirazian I, Asbury BJ, Li Y. Induction of high temperature requirement A1, a serine protease, by TGF-beta1 in articular chondrocytes of mouse models of OA.. Histol Histopathol 2014 May;29(5):609-18.
    pubmed: 24135912doi: 10.14670/hh-29.10.609google scholar: lookup
  42. Legendre F, Ollitrault D, Gomez-Leduc T, Bouyoucef M, Hervieu M, Gruchy N, Mallein-Gerin F, Leclercq S, Demoor M, Galéra P. Enhanced chondrogenesis of bone marrow-derived stem cells by using a combinatory cell therapy strategy with BMP-2/TGF-β1, hypoxia, and COL1A1/HtrA1 siRNAs.. Sci Rep 2017 Jun 13;7(1):3406.
    pmc: PMC5469741pubmed: 28611369doi: 10.1038/s41598-017-03579-ygoogle scholar: lookup
  43. Tiaden AN, Bahrenberg G, Mirsaidi A, Glanz S, Blüher M, Richards PJ. Novel Function of Serine Protease HTRA1 in Inhibiting Adipogenic Differentiation of Human Mesenchymal Stem Cells via MAP Kinase-Mediated MMP Upregulation.. Stem Cells 2016 Jun;34(6):1601-14.
    pubmed: 26864869doi: 10.1002/stem.2297google scholar: lookup
  44. De Bari C, Dell'Accio F, Luyten FP. Failure of in vitro-differentiated mesenchymal stem cells from the synovial membrane to form ectopic stable cartilage in vivo.. Arthritis Rheum 2004 Jan;50(1):142-50.
    pubmed: 14730610doi: 10.1002/art.11450google scholar: lookup
  45. Eames BF, Sharpe PT, Helms JA. Hierarchy revealed in the specification of three skeletal fates by Sox9 and Runx2.. Dev Biol 2004 Oct 1;274(1):188-200.
    pubmed: 15355797doi: 10.1016/j.ydbio.2004.07.006google scholar: lookup
  46. Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension.. Proc Natl Acad Sci U S A 1995 Jun 6;92(12):5510-4.
    pmc: PMC41725pubmed: 7539918doi: 10.1073/pnas.92.12.5510google scholar: lookup
  47. Wang Y, Blasioli DJ, Kim HJ, Kim HS, Kaplan DL. Cartilage tissue engineering with silk scaffolds and human articular chondrocytes.. Biomaterials 2006 Sep;27(25):4434-42.
    pubmed: 16677707doi: 10.1016/j.biomaterials.2006.03.050google scholar: lookup
  48. 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
  49. Su X, Zuo W, Wu Z, Chen J, Wu N, Ma P, Xia Z, Jiang C, Ye Z, Liu S, Liu J, Zhou G, Wan C, Qiu G. CD146 as a new marker for an increased chondroprogenitor cell sub-population in the later stages of osteoarthritis.. J Orthop Res 2015 Jan;33(1):84-91.
    pubmed: 25266708doi: 10.1002/jor.22731google scholar: lookup
  50. Nombela-Arrieta C, Ritz J, Silberstein LE. The elusive nature and function of mesenchymal stem cells.. Nat Rev Mol Cell Biol 2011 Feb;12(2):126-31.
    pmc: PMC3346289pubmed: 21253000doi: 10.1038/nrm3049google scholar: lookup
  51. Islam A, Hansen AK, Mennan C, Martinez-Zubiaurre I. Mesenchymal stromal cells from human umbilical cords display poor chondrogenic potential in scaffold-free three dimensional cultures.. Eur Cell Mater 2016 May 27;31:407-24.
    pubmed: 27232667doi: 10.22203/ecm.v031a26google scholar: lookup
  52. Lo Iacono M. Perinatal and Wharton’s Jelly-Derived Mesenchymal Stem Cells in Cartilage Regenerative Medicine and Tissue Engineering Strategies. Open Tissue Eng. Regen. Med. J. 2011;4:72–81.
  53. Aleksander-Konert E, Paduszyński P, Zajdel A, Dzierżewicz Z, Wilczok A. In vitro chondrogenesis of Wharton's jelly mesenchymal stem cells in hyaluronic acid-based hydrogels.. Cell Mol Biol Lett 2016;21:11.
    pmc: PMC5415830pubmed: 28536614doi: 10.1186/s11658-016-0016-ygoogle scholar: lookup
  54. Tanthaisong P, Imsoonthornruksa S, Ngernsoungnern A, Ngernsoungnern P, Ketudat-Cairns M, Parnpai R. Enhanced Chondrogenic Differentiation of Human Umbilical Cord Wharton's Jelly Derived Mesenchymal Stem Cells by GSK-3 Inhibitors.. PLoS One 2017;12(1):e0168059.
    pmc: PMC5217863pubmed: 28060847doi: 10.1371/journal.pone.0168059google scholar: lookup
  55. Sarugaser R, Lickorish D, Baksh D, Hosseini MM, Davies JE. Human umbilical cord perivascular (HUCPV) cells: a source of mesenchymal progenitors.. Stem Cells 2005 Feb;23(2):220-9.
    pubmed: 15671145doi: 10.1634/stemcells.2004-0166google scholar: lookup
  56. Grayson WL, Zhao F, Izadpanah R, Bunnell B, Ma T. Effects of hypoxia on human mesenchymal stem cell expansion and plasticity in 3D constructs.. J Cell Physiol 2006 May;207(2):331-9.
    pubmed: 16331674doi: 10.1002/jcp.20571google scholar: lookup
  57. Bigot N, Mouche A, Preti M, Loisel S, Renoud ML, Le Guével R, Sensebé L, Tarte K, Pedeux R. Hypoxia Differentially Modulates the Genomic Stability of Clinical-Grade ADSCs and BM-MSCs in Long-Term Culture.. Stem Cells 2015 Dec;33(12):3608-20.
    pubmed: 26422646doi: 10.1002/stem.2195google scholar: lookup
  58. Amarilio R, Viukov SV, Sharir A, Eshkar-Oren I, Johnson RS, Zelzer E. HIF1alpha regulation of Sox9 is necessary to maintain differentiation of hypoxic prechondrogenic cells during early skeletogenesis.. Development 2007 Nov;134(21):3917-28.
    pubmed: 17913788doi: 10.1242/dev.008441google scholar: lookup
  59. Cipolleschi MG, Dello Sbarba P, Olivotto M. The role of hypoxia in the maintenance of hematopoietic stem cells.. Blood 1993 Oct 1;82(7):2031-7.
    pubmed: 8104535
  60. Rosová I, Dao M, Capoccia B, Link D, Nolta JA. Hypoxic preconditioning results in increased motility and improved therapeutic potential of human mesenchymal stem cells.. Stem Cells 2008 Aug;26(8):2173-82.
    pmc: PMC3017477pubmed: 18511601doi: 10.1634/stemcells.2007-1104google scholar: lookup
  61. Ak A, Ogun CO, Bayir A, Kayis SA, Koylu R. Prediction of arterial blood gas values from venous blood gas values in patients with acute exacerbation of chronic obstructive pulmonary disease.. Tohoku J Exp Med 2006 Dec;210(4):285-90.
    pubmed: 17146193doi: 10.1620/tjem.210.285google scholar: lookup
  62. Gómez-Leduc T, Desancé M, Hervieu M, Legendre F, Ollitrault D, de Vienne C, Herlicoviez M, Galéra P, Demoor M. Hypoxia Is a Critical Parameter for Chondrogenic Differentiation of Human Umbilical Cord Blood Mesenchymal Stem Cells in Type I/III Collagen Sponges.. Int J Mol Sci 2017 Sep 8;18(9).
    pmc: PMC5618582pubmed: 28885597doi: 10.3390/ijms18091933google scholar: lookup
  63. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method.. Nat Protoc 2008;3(6):1101-8.
    pubmed: 18546601doi: 10.1038/nprot.2008.73google scholar: lookup

Citations

This article has been cited 12 times.
  1. Linkova N, Khavinson V, Diatlova A, Myakisheva S, Ryzhak G. Peptide Regulation of Chondrogenic Stem Cell Differentiation.. Int J Mol Sci 2023 May 8;24(9).
    doi: 10.3390/ijms24098415pubmed: 37176122google scholar: lookup
  2. Jammes M, Contentin R, Cassé F, Galéra P. Equine osteoarthritis: Strategies to enhance mesenchymal stromal cell-based acellular therapies.. Front Vet Sci 2023;10:1115774.
    doi: 10.3389/fvets.2023.1115774pubmed: 36846261google scholar: lookup
  3. Hassan TA, Maher MA, El Karmoty AF, Ahmed ZSO, Ibrahim MA, Rizk H, Reyad AT. Auricular cartilage regeneration using different types of mesenchymal stem cells in rabbits.. Biol Res 2022 Dec 26;55(1):40.
    doi: 10.1186/s40659-022-00408-zpubmed: 36572914google scholar: lookup
  4. Heyman E, Meeremans M, Devriendt B, Olenic M, Chiers K, De Schauwer C. Validation of a color deconvolution method to quantify MSC tri-lineage differentiation across species.. Front Vet Sci 2022;9:987045.
    doi: 10.3389/fvets.2022.987045pubmed: 36311666google scholar: lookup
  5. 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
  6. Wang Z, Wang Z, Zhang B, Zhao Q, Liu Y, Qi W. Effect of Activated Platelet-Rich Plasma on Chondrogenic Differentiation of Rabbit Bone Marrow-Derived Mesenchymal Stem Cells.. Stem Cells Int 2021;2021:9947187.
    doi: 10.1155/2021/9947187pubmed: 34484349google scholar: lookup
  7. Mok CH, MacLeod JN. Kinetics of Gene Expression Changes in Equine Fetal Interzone and Anlagen Cells Over 14 Days of Induced Chondrogenesis.. Front Vet Sci 2021;8:722324.
    doi: 10.3389/fvets.2021.722324pubmed: 34434986google scholar: lookup
  8. Um S, Ha J, Choi SJ, Oh W, Jin HJ. Prospects for the therapeutic development of umbilical cord blood-derived mesenchymal stem cells.. World J Stem Cells 2020 Dec 26;12(12):1511-1528.
    doi: 10.4252/wjsc.v12.i12.1511pubmed: 33505598google scholar: lookup
  9. Bourdon B, Contentin R, Cassé F, Maspimby C, Oddoux S, Noël A, Legendre F, Gruchy N, Galéra P. Marine Collagen Hydrolysates Downregulate the Synthesis of Pro-Catabolic and Pro-Inflammatory Markers of Osteoarthritis and Favor Collagen Production and Metabolic Activity in Equine Articular Chondrocyte Organoids.. Int J Mol Sci 2021 Jan 8;22(2).
    doi: 10.3390/ijms22020580pubmed: 33430111google scholar: lookup
  10. Arrigoni C, D'Arrigo D, Rossella V, Candrian C, Albertini V, Moretti M. Umbilical Cord MSCs and Their Secretome in the Therapy of Arthritic Diseases: A Research and Industrial Perspective.. Cells 2020 May 28;9(6).
    doi: 10.3390/cells9061343pubmed: 32481562google scholar: lookup
  11. Contentin R, Demoor M, Concari M, Desancé M, Audigié F, Branly T, Galéra P. Comparison of the Chondrogenic Potential of Mesenchymal Stem Cells Derived from Bone Marrow and Umbilical Cord Blood Intended for Cartilage Tissue Engineering.. Stem Cell Rev Rep 2020 Feb;16(1):126-143.
    doi: 10.1007/s12015-019-09914-2pubmed: 31745710google scholar: lookup
  12. Magri C, Schramme M, Febre M, Cauvin E, Labadie F, Saulnier N, François I, Lechartier A, Aebischer D, Moncelet AS, Maddens S. Comparison of efficacy and safety of single versus repeated intra-articular injection of allogeneic neonatal mesenchymal stem cells for treatment of osteoarthritis of the metacarpophalangeal/metatarsophalangeal joint in horses: A clinical pilot study.. PLoS One 2019;14(8):e0221317.
    doi: 10.1371/journal.pone.0221317pubmed: 31465445google scholar: lookup
Subscribe to our newsletter
Join 99,357 horse owners like you who receive our email updates on horse health and nutrition.