Table of Contents Author Guidelines Submit a Manuscript
Table of Contents Alerts

To receive news and publication updates for Stem Cells International, enter your email address in the box below.

Stem Cells International
Volume 2017, Article ID 9542702, 13 pages
https://doi.org/10.1155/2017/9542702
Research Article

Paracrine Potential of the Human Adipose Tissue-Derived Stem Cells to Modulate Balance between Matrix Metalloproteinases and Their Inhibitors in the Osteoarthritic Cartilage In Vitro

Jaroslav Denkovskij,1 Edvardas Bagdonas,1 Ilona Kusleviciute,1 Zygmunt Mackiewicz,1 Ausra Unguryte,1 Narunas Porvaneckas,2 Sandrine Fleury,3 Algirdas Venalis,1 Christian Jorgensen,4 and Eiva Bernotiene1

1Department of Regenerative Medicine, State Research Institute Centre for Innovative Medicine, Vilnius, Lithuania
2Clinic of Rheumatology, Orthopaedics-Traumatology and Reconstructive Surgery, Vilnius University Faculty of Medicine, Vilnius, Lithuania
3EFS Pyrénéés-Méditerranéé, Toulouse, France
4INSERM U844, Hôpital Saint-Eloi and Hôpital Lapeyronie, Université Montpellier 1, Montpellier, France

Correspondence should be addressed to Eiva Bernotiene; tl.sartnecmi@eneitonreb.avie

Received 24 January 2017; Revised 10 April 2017; Accepted 15 May 2017; Published 27 July 2017

Academic Editor: Heinrich Sauer

Copyright © 2017 Jaroslav Denkovskij et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. D. Sandy, “Editorial - a contentious issue finds some clarity: on the independent and complementary roles of aggrecanase activity and MMP activity in human joint aggrecanolysis,” Osteoarthritis and Cartilage, vol. 14, pp. 95–100, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. P. S. Burrage, K. S. Mix, and C. E. Brinckerhoff, “Matrix metalloproteinases: role in arthritis,” Frontiers in Bioscience, vol. 11, pp. 529–543, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. L. Xu, Q. Wang, F. Xu, Z. Ye, Y. Zhou, and W. S. Tan, “Mesenchymal stem cells downregulate articular chondrocyte differentiation in noncontact coculture systems: implications in cartilage tissue regeneration,” Stem Cells and Development, vol. 22, pp. 1657–1669, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Martel-Pelletier, R. McCollum, N. Fujimoto, K. Obata, J. M. Cloutier, and J. P. Pelletier, “Excess of metalloproteases over tissue inhibitor of metalloprotease may contribute to cartilage degradation in osteoarthritis and rheumatoid arthritis,” Laboratory Investigation, vol. 70, pp. 807–815, 1994. View at Google Scholar
  5. C. Manferdini, M. Maumus, E. Gabusi et al., “Adipose-derived mesenchymal stem cells exert anti-inflammatory effects on chondrocytes and synoviocytes from osteoarthritis patients through prostaglandin E2,” Arthritis and Rheumatism, vol. 65, pp. 1271–1281, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. J. Gimble and F. Guilak, “Adipose-derived adult stem cells: isolation, characterization, and differentiation potential,” Cytotherapy, vol. 5, pp. 362–369, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. J. A. Anderson, D. Little, A. P. Toth et al., “Stem cell therapies for knee cartilage repair: the current status of preclinical and clinical studies,” The American Journal of Sports Medicine, vol. 42, pp. 2253–2261, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. J. M. Gimble, B. A. Bunnell, and F. Guilak, “Human adipose-derived cells: an update on the transition to clinical translation,” Regenerative Medicine, vol. 7, pp. 225–235, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. Y. M. Pers, M. Ruiz, D. Noel, and C. Jorgensen, “Mesenchymal stem cells for the management of inflammation in osteoarthritis: state of the art and perspectives,” Osteoarthritis and Cartilage, vol. 23, pp. 2027–2035, 2015. View at Publisher · View at Google Scholar · View at Scopus
  10. E. K. Moo, N. A. Osman, and B. Pingguan-Murphy, “The metabolic dynamics of cartilage explants over a long-term culture period,” Clinics, vol. 66, pp. 1431–1436, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. M. Goldring, “Osteoarthritis and cartilage: the role of cytokines,” Current Rheumatology Reports, vol. 2, pp. 459–465, 2000. View at Publisher · View at Google Scholar
  12. I. Takahashi, G. H. Nuckolls, K. Takahashi et al., “Compressive force promotes sox9, type II collagen and aggrecan and inhibits IL-1beta expression resulting in chondrogenesis in mouse embryonic limb bud mesenchymal cells,” Journal of Cell Science, vol. 111, Part 14, pp. 2067–2076, 1998. View at Google Scholar
  13. I. M. Khan, L. Francis, P. S. Theobald et al., “In vitro growth factor-induced bio engineering of mature articular cartilage,” Biomaterials, vol. 34, pp. 1478–1487, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. D. R. Eyre, M. A. Weis, and J. J. Wu, “Articular cartilage collagen: an irreplaceable framework?” European Cells & Materials, vol. 12, pp. 57–63, 2006. View at Publisher · View at Google Scholar
  15. M. D'Angelo, Z. Yan, M. Nooreyazdan et al., “MMP-13 is induced during chondrocyte hypertrophy,” Journal of Cellular Biochemistry, vol. 77, pp. 678–693, 2000. View at Publisher · View at Google Scholar
  16. N. Fekete, M. Gadelorge, D. Furst et al., “Platelet lysate from whole blood-derived pooled platelet concentrates and apheresis-derived platelet concentrates for the isolation and expansion of human bone marrow mesenchymal stromal cells: production process, content and identification of active components,” Cytotherapy, vol. 14, pp. 540–554, 2012. View at Google Scholar
  17. E. Hedbom and H. J. Hauselmann, “Molecular aspects of pathogenesis in osteoarthritis: the role of inflammation,” Cellular and Molecular Life Sciences, vol. 59, pp. 45–53, 2002. View at Google Scholar
  18. C. Candrian, E. Bonacina, J. A. Frueh et al., “Intra-individual comparison of human ankle and knee chondrocytes in vitro: relevance for talar cartilage repair,” Osteoarthritis and Cartilage, vol. 17, pp. 489–496, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. P. Bourin, J. A. Peyrafitte, and S. Fleury-Cappellesso, “A first approach for the production of human adipose tissue-derived stromal cells for therapeutic use,” Methods in Molecular Biology, vol. 702, pp. 331–343, 2011. View at Google Scholar
  20. A. Bura, V. Planat-Benard, P. Bourin et al., “Phase I trial: the use of autologous cultured adipose-derived stroma/stem cells to treat patients with non-revascularizable critical limb ischemia,” Cytotherapy, vol. 16, pp. 245–257, 2014. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Unguryte, E. Bernotiene, E. Bagdonas, S. Garberyte, N. Porvaneckas, and C. Jorgensen, “Human articular chondrocytes with higher aldehyde dehydrogenase activity have stronger expression of COL2A1 and SOX9,” Osteoarthritis and Cartilage, vol. 24, pp. 873–882, 2016. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Ramakers, J. M. Ruijter, R. H. Deprez, and A. F. Moorman, “Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data,” Neuroscience Letters, vol. 339, pp. 62–66, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. M. W. Pfaffl, “A new mathematical model for relative quantification in real-time RT-PCR,” Nucleic Acids Research, vol. 29, p. e45, 2001. View at Publisher · View at Google Scholar
  24. G. Schett, S. Kiechl, E. Bonora et al., “Vascular cell adhesion molecule 1 as a predictor of severe osteoarthritis of the hip and knee joints,” Arthritis and Rheumatism, vol. 60, pp. 2381–2389, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. K. Gelse, P. Klinger, M. Koch et al., “Thrombospondin-1 prevents excessive ossification in cartilage repair tissue induced by osteogenic protein-1,” Tissue Engineering. Part A, vol. 17, pp. 2101–2112, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. T. Schubert, J. Schlegel, R. Schmid et al., “Modulation of cartilage differentiation by melanoma inhibiting activity/cartilage-derived retinoic acid-sensitive protein (MIA/CD-RAP),” Experimental & Molecular Medicine, vol. 42, pp. 166–174, 2010. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Rastogi, H. Kim, J. D. Twomey, and A. H. Hsieh, “MMP-2 mediates local degradation and remodeling of collagen by annulus fibrosus cells of the intervertebral disc,” Arthritis Research & Therapy, vol. 15, p. R57, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. G. I. Goldberg, A. Strongin, I. E. Collier, L. T. Genrich, and B. L. Marmer, “Interaction of 92-kDa type IV collagenase with the tissue inhibitor of metalloproteinases prevents dimerization, complex formation with interstitial collagenase, and activation of the proenzyme with stromelysin,” The Journal of Biological Chemistry, vol. 267, pp. 4583–4591, 1992. View at Google Scholar
  29. R. L. Smith, “Degradative enzymes in osteoarthritis,” Frontiers in Bioscience, vol. 4, pp. D704–D712, 1999. View at Google Scholar
  30. Y. Ding, D. Xu, G. Feng, A. Bushell, R. J. Muschel, and K. J. Wood, “Mesenchymal stem cells prevent the rejection of fully allogenic islet grafts by the immunosuppressive activity of matrix metalloproteinase-2 and -9,” Diabetes, vol. 58, pp. 1797–1806, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Efimenko, E. Starostina, N. Kalinina, and A. Stolzing, “Angiogenic properties of aged adipose derived mesenchymal stem cells after hypoxic conditioning,” Journal of Translational Medicine, vol. 9, p. 10, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. G. M. van Buul, E. Villafuertes, P. K. Bos et al., “Mesenchymal stem cells secrete factors that inhibit inflammatory processes in short-term osteoarthritic synovium and cartilage explant culture,” Osteoarthritis and Cartilage, vol. 20, pp. 1186–1196, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. A. M. Freyria and F. Mallein-Gerin, “Chondrocytes or adult stem cells for cartilage repair: the indisputable role of growth factors,” Injury, vol. 43, pp. 259–265, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Schinhan, M. Gruber, R. Dorotka et al., “Matrix-associated autologous chondrocyte transplantation in a compartmentalized early stage of osteoarthritis,” Osteoarthritis and Cartilage/OARS, Osteoarthritis Research Society, vol. 21, pp. 217–225, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Roberts, J. Menage, L. J. Sandell, E. H. Evans, and J. B. Richardson, “Immunohistochemical study of collagen types I and II and procollagen IIA in human cartilage repair tissue following autologous chondrocyte implantation,” The Knee, vol. 16, pp. 398–404, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. P. H. Ousema, F. T. Moutos, B. T. Estes et al., “The inhibition by interleukin 1 of MSC chondrogenesis and the development of biomechanical properties in biomimetic 3D woven PCL scaffolds,” Biomaterials, vol. 33, pp. 8967–8974, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. R. Fleischmajer, E. D. MacDonald, J. S. Perlish, R. E. Burgeson, and L. W. Fisher, “Dermal collagen fibrils are hybrids of type I and type III collagen molecules,” Journal of Structural Biology, vol. 105, pp. 162–169, 1990. View at Publisher · View at Google Scholar · View at Scopus
  38. J. J. Wu, M. A. Weis, L. S. Kim, and D. R. Eyre, “Type III collagen, a fibril network modifier in articular cartilage,” The Journal of Biological Chemistry, vol. 285, pp. 18537–18544, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. J. Scheller, A. Chalaris, D. Schmidt-Arras, and S. Rose-John, “The pro- and anti-inflammatory properties of the cytokine interleukin-6,” Biochimica et Biophysica Acta, vol. 2011, pp. 878–888, 1813. View at Google Scholar
  40. M. Lotz, S. Hashimoto, and K. Kuhn, “Mechanisms of chondrocyte apoptosis,” Osteoarthritis and Cartilage, vol. 7, pp. 389–391, 1999. View at Publisher · View at Google Scholar · View at Scopus