Table of Contents Author Guidelines Submit a Manuscript
Stem Cells International
Volume 2017, Article ID 9303598, 11 pages
https://doi.org/10.1155/2017/9303598
Research Article

Polysaccharide Hydrogels Support the Long-Term Viability of Encapsulated Human Mesenchymal Stem Cells and Their Ability to Secrete Immunomodulatory Factors

1INSERM, UMR 1229, Regenerative Medicine and Skeleton (RMeS), Université de Nantes, ONIRIS, 44042 Nantes, France
2UFR Sciences Biologiques et Pharmaceutiques, Université de Nantes, 44035 Nantes, France
3UFR Odontologie, Université de Nantes, 44042 Nantes, France
4CHU Nantes, Pharmacie Centrale, PHU 11, 44093 Nantes, France
5INSERM, UMS 016, CNRS 3556, Structure Fédérative de Recherche François Bonamy, Micropicell Facility, CHU Nantes, Université de Nantes, 44042 Nantes, France
6CHU Nantes, PHU 4 OTONN, 44093 Nantes, France

Correspondence should be addressed to Jérôme Guicheux; rf.mresni@xuehciug.emorej

Received 25 May 2017; Revised 3 August 2017; Accepted 8 August 2017; Published 11 October 2017

Academic Editor: Celeste Scotti

Copyright © 2017 Fahd Hached 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. M. F. Pittenger, A. M. Mackay, S. C. Beck et al., “Multilineage potential of adult human mesenchymal stem cells,” Science, vol. 284, pp. 143–147, 1999. View at Publisher · View at Google Scholar · View at Scopus
  2. C. Vinatier, D. Mrugala, C. Jorgensen, J. Guicheux, and D. Noël, “Cartilage engineering: a crucial combination of cells, biomaterials and biofactors,” Trends in Biotechnology, vol. 27, pp. 307–314, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. A. I. Caplan and D. Correa, “The MSC: an injury drugstore,” Cell Stem Cell, vol. 9, pp. 11–15, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. F. Djouad, C. Bouffi, S. Ghannam, D. Noël, and C. Jorgensen, “Mesenchymal stem cells: innovative therapeutic tools for rheumatic diseases,” Nature Reviews Rheumatology, vol. 5, pp. 392–399, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. B. Kronsteiner, S. Wolbank, A. Peterbauer et al., “Human mesenchymal stem cells from adipose tissue and amnion influence T-cells depending on stimulation method and presence of other immune cells,” Stem Cells and Development, vol. 20, pp. 2115–2126, 2011. View at Publisher · View at Google Scholar · View at Scopus
  6. M. E. Bernardo and W. E. Fibbe, “Mesenchymal stromal cells: sensors and switchers of inflammation,” Cell Stem Cell, vol. 13, pp. 392–402, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. R. Meisel, A. Zibert, M. Laryea, U. Göbel, W. Däubener, and D. Dilloo, “Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation,” Blood, vol. 103, pp. 4619–4621, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. G. M. Spaggiari, H. Abdelrazik, F. Becchetti, and L. Moretta, “MSCs inhibit monocyte-derived DC maturation and function by selectively interfering with the generation of immature DCs: central role of MSC-derived prostaglandin E2,” Blood, vol. 113, pp. 6576–6583, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. B. A. Aguado, W. Mulyasasmita, J. Su, K. J. Lampe, and S. C. Heilshorn, “Improving viability of stem cells during syringe needle flow through the design of hydrogel cell carriers,” Tissue Engineering, Part A, vol. 18, pp. 806–815, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. O. Detante, A. Moisan, J. Dimastromatteo et al., “Intravenous administration of 99mTc-HMPAO-labeled human mesenchymal stem cells after stroke: in vivo imaging and biodistribution,” Cell Transplantation, vol. 18, pp. 1369–1379, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. K. Toupet, M. Maumus, J.-A. Peyrafitte et al., “Long-term detection of human adipose-derived mesenchymal stem cells after intraarticular injection in SCID mice,” Arthritis and Rheumatism, vol. 65, pp. 1786–1794, 2013. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Blocki, S. Beyer, J.-Y. Dewavrin et al., “Microcapsules engineered to support mesenchymal stem cell (MSC) survival and proliferation enable long-term retention of MSCs in infarcted myocardium,” Biomaterials, vol. 53, pp. 12–24, 2015. View at Publisher · View at Google Scholar · View at Scopus
  13. S. J. Bidarra, C. C. Barrias, and P. L. Granja, “Injectable alginate hydrogels for cell delivery in tissue engineering,” Acta Biomaterialia, vol. 10, pp. 1646–1662, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. K. Xu, D. A. Cantu, Y. Fu et al., “Thiol-ene Michael-type formation of gelatin/poly(ethylene glycol) biomatrices for three-dimensional mesenchymal stromal/stem cell administration to cutaneous wounds,” Acta Biomaterialia, vol. 9, pp. 8802–8814, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. L. Gasperini, J. F. Mano, and R. L. Reis, “Natural polymers for the microencapsulation of cells,” Journal of the Royal Society Interface, vol. 11, article 20140817, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. G. Orive, E. Santos, D. Poncelet et al., “Cell encapsulation: technical and clinical advances,” Trends in Pharmacological Sciences, vol. 36, pp. 537–546, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. H. Zhou and H. H. K. Xu, “The fast release of stem cells from alginate-fibrin microbeads in injectable scaffolds for bone tissue engineering,” Biomaterials, vol. 32, pp. 7503–7513, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. G. Chan and D. J. Mooney, “Ca2+ released from calcium alginate gels can promote inflammatory responses in vitro and in vivo,” Acta Biomaterialia, vol. 9, pp. 9281–9291, 2013. View at Publisher · View at Google Scholar · View at Scopus
  19. C. Merceron, S. Portron, M. Masson et al., “The effect of two- and three-dimensional cell culture on the chondrogenic potential of human adipose-derived mesenchymal stem cells after subcutaneous transplantation with an injectable hydrogel,” Cell Transplantation, vol. 20, pp. 1575–1588, 2011. View at Publisher · View at Google Scholar
  20. S. Portron, C. Merceron, O. Gauthier et al., “Effects of in vitro low oxygen tension preconditioning of adipose stromal cells on their in vivo chondrogenic potential: application in cartilage tissue repair,” PLoS One, vol. 8, article e62368, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. V. F. T. Teixeira, N. R. Pereira, W. R. Waldman, A. L. C. D. Ávila, V. H. Pérez, and R. J. S. Rodríguez, “Ion exchange kinetics of magnetic alginate ferrogel beads produced by external gelation,” Carbohydrate Polymers, vol. 111, pp. 198–205, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. C. Vinatier, D. Magne, P. Weiss et al., “A silanized hydroxypropyl methylcellulose hydrogel for the three-dimensional culture of chondrocytes,” Biomaterials, vol. 26, pp. 6643–6651, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. C. Merceron, S. Portron, C. Vignes-Colombeix et al., “Pharmacological modulation of human mesenchymal stem cell chondrogenesis by a chemically oversulfated polysaccharide of marine origin: potential application to cartilage regenerative medicine,” Stem Cells, vol. 30, pp. 471–480, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. L. A. Bosworth, S. R. Rathbone, and S. H. Cartmell, “Optimizing attachment of human mesenchymal stem cells on poly(ε-caprolactone) electrospun yarns,” Journal of Visualized Experiments, vol. 98, 2015. View at Publisher · View at Google Scholar · View at Scopus
  25. R. A. Thibault, L. Scott Baggett, A. G. Mikos, and F. K. Kasper, “Osteogenic differentiation of mesenchymal stem cells on pregenerated extracellular matrix scaffolds in the absence of osteogenic cell culture supplements,” Tissue Engineering Part A, vol. 16, pp. 431–440, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. M. François, R. Romieu-Mourez, M. Li, and J. Galipeau, “Human MSC suppression correlates with cytokine induction of indoleamine 2,3-dioxygenase and bystander M2 macrophage differentiation,” Molecular Therapy, vol. 20, pp. 187–195, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. B. B. Lee, P. Ravindra, and E. S. Chan, “Size and shape of calcium alginate beads produced by extrusion dripping,” Chemical Engineering and Technology, vol. 36, pp. 1627–1642, 2013. View at Publisher · View at Google Scholar · View at Scopus
  28. T. N. Salthouse, “Some aspects of macrophage behavior at the implant interface,” Journal of Biomedical Materials Research, vol. 18, pp. 395–401, 1984. View at Publisher · View at Google Scholar · View at Scopus
  29. B. F. Matlaga, L. P. Yasenchak, and T. N. Salthouse, “Tissue response to implanted polymers: the significance of sample shape,” Journal of Biomedical Materials Research, vol. 10, pp. 391–397, 1976. View at Publisher · View at Google Scholar · View at Scopus
  30. S. W. Kim, Y. H. Bae, and T. Okano, “Hydrogels: swelling, drug loading, and release,” Pharmaceutical Research, vol. 9, pp. 283–290, 1992. View at Publisher · View at Google Scholar · View at Scopus
  31. A. G. Lee, C. P. Arena, D. J. Beebe, and S. P. Palecek, “Development of macroporous poly(ethylene glycol) hydrogel arrays within microfluidic channels,” Biomacromolecules, vol. 11, pp. 3316–3324, 2010. View at Publisher · View at Google Scholar · View at Scopus
  32. D. Mawad, R. Odell, and L. A. Poole-Warren, “Network structure and macromolecular drug release from poly(vinyl alcohol) hydrogels fabricated via two crosslinking strategies,” International Journal of Pharmaceutics, vol. 366, pp. 31–37, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. J. M. Ziebell and M. C. Morganti-Kossmann, “Involvement of pro- and anti-inflammatory cytokines and chemokines in the pathophysiology of traumatic brain injury,” Neurotherapeutics, vol. 7, pp. 22–30, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. S. M. Opal and V. A. DePalo, “Anti-inflammatory cytokines,” Chest, vol. 117, pp. 1162–1172, 2000. View at Publisher · View at Google Scholar
  35. C. A. Feghali and T. M. Wright, “Cytokines in acute and chronic inflammation,” Frontiers in Bioscience, vol. 2, pp. d12–d26, 1997. View at Publisher · View at Google Scholar
  36. B. Wright, R. A. Cave, J. P. Cook et al., “Enhanced viability of corneal epithelial cells for efficient transport/storage using a structurally modified calcium alginate hydrogel,” Regenerative Medicine, vol. 7, pp. 295–307, 2012. View at Publisher · View at Google Scholar · View at Scopus
  37. J. L. Wilson, M. A. Najia, R. Saeed, and T. C. McDevitt, “Alginate encapsulation parameters influence the differentiation of microencapsulated embryonic stem cell aggregates,” Biotechnology and Bioengineering, vol. 111, pp. 618–631, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. M. J. Webber, E. A. Appel, E. W. Meijer, and R. Langer, “Supramolecular biomaterials,” Nature Materials, vol. 15, pp. 13–26, 2016. View at Publisher · View at Google Scholar · View at Scopus
  39. C. Ceccaldi, S. G. Fullana, C. Alfarano et al., “Alginate scaffolds for mesenchymal stem cell cardiac therapy: influence of alginate composition,” Cell Transplantation, vol. 21, pp. 1969–1984, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. J. Yu, K. T. Du, Q. Fang et al., “The use of human mesenchymal stem cells encapsulated in RGD modified alginate microspheres in the repair of myocardial infarction in the rat,” Biomaterials, vol. 31, pp. 7012–7020, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. L. Moussa, G. Pattappa, B. Doix et al., “A biomaterial-assisted mesenchymal stromal cell therapy alleviates colonic radiation-induced damage,” Biomaterials, vol. 115, pp. 40–52, 2017. View at Publisher · View at Google Scholar
  42. M. ter Huurne, R. Schelbergen, R. Blattes et al., “Antiinflammatory and chondroprotective effects of intraarticular injection of adipose-derived stem cells in experimental osteoarthritis,” Arthritis and Rheumatism, vol. 64, pp. 3604–3613, 2012. View at Publisher · View at Google Scholar · View at Scopus
  43. C. Manferdini, M. Maumus, E. Gabusi et al., “Adipose-derived mesenchymal stem cells exert antiinflammatory 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
  44. M. Maumus, C. Manferdini, K. Toupet et al., “Adipose mesenchymal stem cells protect chondrocytes from degeneration associated with osteoarthritis,” Stem Cell Research, vol. 11, pp. 834–844, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. M. W. Klinker and C.-H. Wei, “Mesenchymal stem cells in the treatment of inflammatory and autoimmune diseases in experimental animal models,” World Journal of Stem Cells, vol. 7, pp. 556–567, 2015. View at Publisher · View at Google Scholar
  46. L.-T. Wang, C.-H. Ting, M.-L. Yen et al., “Human mesenchymal stem cells (MSCs) for treatment towards immune- and inflammation-mediated diseases: review of current clinical trials,” Journal of Biomedical Science, vol. 23, p. 76, 2016. View at Publisher · View at Google Scholar · View at Scopus
  47. R. E. Newman, D. Yoo, M. A. LeRoux, and A. Danilkovitch-Miagkova, “Treatment of inflammatory diseases with mesenchymal stem cells,” Inflammation & Allergy Drug Targets, vol. 8, pp. 110–123, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. K. Németh, A. Leelahavanichkul, P. S. T. Yuen et al., “Bone marrow stromal cells attenuate sepsis via prostaglandin E2-dependent reprogramming of host macrophages to increase their interleukin-10 production,” Nature Medicine, vol. 15, pp. 42–49, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. E. Singhal, P. Kumar, and P. Sen, “A novel role for Bruton’s tyrosine kinase in hepatocyte growth factor-mediated immunoregulation of dendritic cells,” The Journal of Biological Chemistry, vol. 286, pp. 32054–32063, 2011. View at Publisher · View at Google Scholar · View at Scopus