Journal of Healthcare Engineering

Journal of Healthcare Engineering / 2011 / Article

Research Article | Open Access

Volume 2 |Article ID 875406 | https://doi.org/10.1260/2040-2295.2.4.427

Wujie Zhang, Xiaoming He, "Microencapsulating and Banking Living Cells for Cell-Based Medicine", Journal of Healthcare Engineering, vol. 2, Article ID 875406, 20 pages, 2011. https://doi.org/10.1260/2040-2295.2.4.427

Microencapsulating and Banking Living Cells for Cell-Based Medicine

Received01 Mar 2011
Accepted01 Aug 2011

Abstract

A major challenge to the eventual success of the emerging cell-based medicine such as tissue engineering, regenerative medicine, and cell transplantation is the limited availability of the desired cell sources. This challenge can be addressed by cell microencapsulation to overcome the undesired immune response (i.e., to achieve immunoisolation) so that non-autologous cells can be used to treat human diseases, and by cell/tissue preservation to bank living cells for wide distribution to end users so that they are readily available when needed in the future. This review summarizes the status quo of research in both cell microencapsulation and banking the microencapsulated cells. It is concluded with a brief outlook of future research directions in this important field.

References

  1. T. M. Chang, “Semipermeable Microcapsules,” Science, vol. 146, pp. 524–525, 1964. View at: Google Scholar
  2. F. Lim and A. M. Sun, “Microencapsulated Islets as Bioartificial Endocrine Pancreas,” Science, vol. 210, no. 4472, pp. 908–910, 1980. View at: Google Scholar
  3. A. Murua, A. Portero, G. Orive, R. M. Hernandez, M. de Castro, and J. L. Pedraz, “Cell microencapsulation technology: towards clinical application,” J Control Release, vol. 132, no. 2, pp. 76–83, 2008. View at: Google Scholar
  4. G. Orive, R. M. Hernandez, A. R. Gascon et al., “Cell encapsulation: promise and progress,” Nat Med, vol. 9, no. 1, pp. 104–107, 2003. View at: Google Scholar
  5. G. Orive, R. M. Hernandez, A. Rodriguez Gascon et al., “History challenges and perspectives of cell microencapsulation,” Trends Biotechnol, vol. 22, no. 2, pp. 87–92, 2004. View at: Google Scholar
  6. H. Uludag, P. De Vos, and P. A. Tresco, “Technology of mammalian cell encapsulation,” Adv Drug Deliv Rev, vol. 42, no. 1-2, pp. 29–64, 2000. View at: Google Scholar
  7. J. T. Wilson and E. L. Chaikof, “Challenges and emerging technologies in the immunoisolation of cells and tissues,” Adv Drug Deliv Rev, vol. 60, no. 2, pp. 124–145, 2008. View at: Google Scholar
  8. E. H. Nafea, A. M. Poole-Warren, and P. J. Martens, “Immunoisolating semi-permeable membranes for cell encapsulation: Focus on hydrogels,” J Control Release, vol. 154, no. 2, pp. 110–122, 2011. View at: Google Scholar
  9. R. M. Hernandez, G. Orive, A. Murua, and J. L. Pedraz, “Microcapsules and microcarriers for in situ cell delivery,” Adv Drug Deliv Rev, vol. 62, no. 7-8, pp. 711–730, 2010. View at: Google Scholar
  10. E. V. Batrakova, H. E. Gendelman, and A. V. Kabanov, “Cell-mediated drug delivery,” Expert Opin Drug Deliv, vol. 8, no. 4, pp. 415–433, 2011. View at: Google Scholar
  11. E. Santos, J. Zarate, G. Orive, R. M. Hernandez, and J. L. Pedraz, “Biomaterials in cell microencapsulation,” Adv Exp Med Biol, vol. 670, pp. 5–21, 2010. View at: Google Scholar
  12. Y. Teramura and H. Iwata, “Bioartificial pancreas microencapsulation and conformal coating of islet of Langerhans,” Adv Drug Deliv Rev, vol. 62, no. 7-8, pp. 827–840, 2010. View at: Google Scholar
  13. Y. Teramura, L. N. Minh, T. Kawamoto, and H. Iwata, “Microencapsulation of islets with living cells using polyDNA-PEG-lipid conjugate,” Bioconjug Chem, vol. 21, no. 4, pp. 792–796, 2010. View at: Google Scholar
  14. O. Smidsrød and G. Skjåk-Braek, “Alginate as immobilization matrix for cells,” Trends in Biotechnology, vol. 8, no. 3, pp. 71–78, 1990. View at: Google Scholar
  15. P. de Vos, M. M. Faas, B. Strand, and R. Calafiore, “Alginate-based microcapsules for immunoisolation of pancreatic islets,” Biomaterials, vol. 27, no. 32, pp. 5603–5617, 2006. View at: Google Scholar
  16. Y. A. Morch, I. Donati, B. L. Strand, and G. Skjak-Braek, “Effect of Ca2+, Ba2+, and Sr2+ on alginate microbeads. Biomacromolecules,” vol. 7, no. 5, pp. 1471–1480, 2006. View at: Google Scholar
  17. H. Zimmermann, D. Zimmermann, R. Reuss et al., “Towards a medically approved technology for alginatebased microcapsules allowing long-term immunoisolated transplantation,” J Mater Sci Mater Med, vol. 16, no. 6, pp. 491–501, 2005. View at: Google Scholar
  18. M. Qi, B. L. Strand, Y. Morch et al., “Encapsulation of human islets in novel inhomogeneous alginate-ca2+/ba2+ microbeads: in vitro and in vivo function,” Artif Cells Blood Substit Immobil Biotechnol, vol. 36, no. 5, pp. 403–420, 2008. View at: Google Scholar
  19. W. J. Zhang, B. G. Li, C. Zhang, X. H. Xie, and T. T. Tang, “Biocompatibility and membrane strength of C3H10T1/2 cell-loaded alginate-based microcapsules,” Cytotherapy, vol. 10, no. 1, pp. 90–97, 2008. View at: Google Scholar
  20. G. Orive, S. K. Tam, J. L. Pedraz, and J. P. Halle, “Biocompatibility of alginate-poly-L-lysine microcapsules for cell therapy,” Biomaterials, vol. 27, no. 20, pp. 3691–3700, 2006. View at: Google Scholar
  21. R. van Schilfgaarde and P. de Vos Factors, “influencing the properties and performance of microcapsules for immunoprotection of pancreatic islets,” J Mol Med, vol. 77, no. 1, pp. 199–205, 1999. View at: Google Scholar
  22. H. A. Clayton, N. J. London, P. S. Colloby, P. R. Bell, and R. F. James, “The effect of capsule composition on the biocompatibility of alginate-poly-l-lysine capsules,” J Microencapsul, vol. 8, no. 2, pp. 221–233, 1991. View at: Google Scholar
  23. A. G. Mallett and G. S. Korbutt, “Alginate modification improves long-term survival and function of transplanted encapsulated islets,” Tissue Eng Part A, vol. 15, no. 6, pp. 1301–1309, 2009. View at: Google Scholar
  24. M. Menard, J. Dusseault, G. Langlois et al., “Role of protein contaminants in the immunogenicity of alginates,” J Biomed Mater Res B Appl Biomater, vol. 93, no. 2, pp. 333–340, 2010. View at: Google Scholar
  25. B. Thu, P. Bruheim, T. Espevik, O. Smidsrod, P. Soon-Shiong, and G. Skjak-Braek, “Alginate polycation microcapsules. I. Interaction between alginate and polycation,” Biomaterials, vol. 17, no. 10, pp. 1031–1040, 1996. View at: Google Scholar
  26. B. Thu, P. Bruheim, T. Espevik, O. Smidsrod, P. Soon-Shiong, and G. Skjak-Braek, “Alginate polycation microcapsules. II. Some functional properties,” Biomaterials, vol. 17, no. 11, pp. 1069–1079, 1996. View at: Google Scholar
  27. S. De and D. Robinson, “Polymer relationships during preparation of chitosan-alginate and poly-l-lysinealginate nanospheres,” J Control Release, vol. 89, no. 1, pp. 101–112, 2003. View at: Google Scholar
  28. H. J. Chung, D. H. Go, J. W. Bae, I. K. Jung, J. W. Lee, and K. D. Park, “Synthesis and characterization of Pluronic((R)) grafted chitosan copolymer as a novel injectable biomaterial,” Current Applied Physics, vol. 5, no. 5, pp. 485–488, 2005. View at: Google Scholar
  29. L. Baruch and M. Machluf, “Alginate-chitosan complex coacervation for cell encapsulation: effect on mechanical properties and on long-term viability,” Biopolymers, vol. 82, no. 6, pp. 570–579, 2006. View at: Google Scholar
  30. T. Chandy, D. L. Mooradian, and G. H. Rao, “Evaluation of modified alginate-chitosan-polyethylene glycol microcapsules for cell encapsulation,” Artif Organs, vol. 23, no. 10, pp. 894–903, 1999. View at: Google Scholar
  31. T. Haque, H. Chen, W. Ouyang et al., “Investigation of a new microcapsule membrane combining alginate, chitosan, polyethylene glycol and poly-L-lysine for cell transplantation applications,” Int J Artif Organs, vol. 28, no. 6, pp. 631–637, 2005. View at: Google Scholar
  32. T. Haque, H. Chen, W. Ouyang et al., “In vitro study of alginate-chitosan microcapsules: an alternative to liver cell transplants for the treatment of liver failure,” Biotechnol Lett, vol. 27, no. 5, pp. 317–322, 2005. View at: Google Scholar
  33. E. Marsich, M. Borgogna, I. Donati et al., “Alginate/lactose-modified chitosan hydrogels: A bioactive biomaterial for chondrocyte encapsulation,” Journal of Biomedical Materials Research Part A, vol. 84A, no. 2, pp. 364–376, 2008. View at: Google Scholar
  34. A. Paul, D. Shum-Tim, and S. Prakash, “Investigation on PEG Integrated Alginate–Chitosan Microcapsules for Myocardial Therapy Using Marrow Stem Cells Genetically Modified by Recombinant Baculovirus,” Cardiovascular Engineering and Technology, vol. 1, no. 2, pp. 154–164, 2010. View at: Google Scholar
  35. B. A. Zielinski and P. Aebischer, “Chitosan as a matrix for mammalian cell encapsulation,” Biomaterials, vol. 15, no. 13, pp. 1049–1056, 1994. View at: Google Scholar
  36. G. Orive, A. Bartkowiak, S. Lisiecki et al., “Biocompatible oligochitosans as cationic modifiers of alginate/Ca microcapsules,” Journal of Biomedical Materials Research Part B-Applied Biomaterials, vol. 74B, no. 1, pp. 429–439, 2005. View at: Google Scholar
  37. M. De Castro, G. Orive, R. M. Hernandez, A. Bartkowiak, W. Brylak, and J. L. Pedraz, “Biocompatibility and in vivo evaluation of oligochitosans as cationic modifiers of alginate/Ca microcapsules,” J Biomed Mater Res A, vol. 91, no. 4, pp. 1119–1130, 2009. View at: Google Scholar
  38. P. de Vos, M. Bucko, P. Gemeiner et al., “Multiscale requirements for bioencapsulation in medicine and biotechnology,” Biomaterials, vol. 30, no. 13, pp. 2559–2570, 2009. View at: Google Scholar
  39. J. P. Acker, “Biopreservation of cells and engineered tissues,” Adv Biochem Eng Biotechnol, vol. 103, pp. 157–187, 2007. View at: Google Scholar
  40. J. M. Rabanel, X. Banquy, H. Zouaoui, M. Mokhtar, and P. Hildgen, “Progress technology in microencapsulation methods for cell therapy,” Biotechnol Prog, vol. 25, no. 4, pp. 946–963, 2009. View at: Google Scholar
  41. S. Koch, C. Schwinger, J. Kressler, C. Heinzen, and N. G. Rainov, “Alginate encapsulation of genetically engineered mammalian cells: comparison of production devices, methods and microcapsule characteristics,” J Microencapsul, vol. 20, no. 3, pp. 303–316, 2003. View at: Google Scholar
  42. H. Iwata, T. Takagi, H. Amemiya et al., “Agarose for a bioartificial pancreas,” J Biomed Mater Res, vol. 26, no. 7, pp. 967–977, 1992. View at: Google Scholar
  43. S. Sugiura, T. Oda, Y. Aoyagi et al., “Microfabricated airflow nozzle for microencapsulation of living cells into 150 micrometer microcapsules,” Biomed Microdevices, vol. 9, no. 1, pp. 91–99, 2007. View at: Google Scholar
  44. S. Haeberle, L. Naegele, R. Burger, F. von Stetten, R. Zengerle, and J. Ducree, “Alginate bead fabrication and encapsulation of living cells under centrifugally induced artificial gravity conditions,” J Microencapsul, vol. 25, no. 4, pp. 267–274, 2008. View at: Google Scholar
  45. A. Batorsky, J. Liao, A. W. Lund, G. E. Plopper, and J. P. Stegemann, “Encapsulation of adult human mesenchymal stem cells within collagen-agarose microenvironments,” Biotechnol Bioeng, vol. 92, no. 4, pp. 492–500, 2005. View at: Google Scholar
  46. L. Wang and J. P. Stegemann, “Thermogelling chitosan and collagen composite hydrogels initiated with beta-glycerophosphate for bone tissue engineering,” Biomaterials, vol. 31, no. 14, pp. 3976–3985, 2010. View at: Google Scholar
  47. C. Kim, K. S. Lee, Y. E. Kim et al., “Rapid exchange of oil-phase in microencapsulation chip to enhance cell viability,” Lab Chip, vol. 9, no. 9, pp. 1294–1297, 2009. View at: Google Scholar
  48. B. G. Li, T. C. Hua, H. D. Zhang, Y. F. Wang, and G. X. Wang, “Cryopreservation and xenotransplantation studies of microencapsulated rat pancreatic islets,” Cryo Letters, vol. 23, no. 1, pp. 47–54, 2002. View at: Google Scholar
  49. Y. T. Kim, R. Hitchcock, K. W. Broadhead, D. J. Messina, and P. A. Tresco, “A cell encapsulation device for studying soluble factor release from cells transplanted in the rat brain,” J Control Release, vol. 102, no. 1, pp. 101–111, 2005. View at: Google Scholar
  50. M. Hu, M. Kurisawa, R. Deng et al., “Cell immobilization in gelatin-hydroxyphenylpropionic acid hydrogel fibers,” Biomaterials, vol. 30, no. 21, pp. 3523–3531, 2009. View at: Google Scholar
  51. C. A. Hoesli, M. Luu, and J. M. Piret, “A novel alginate hollow fiber bioreactor process for cellular therapy applications,” Biotechnol Prog, vol. 25, no. 6, pp. 1740–1751, 2009. View at: Google Scholar
  52. H. F. Ding, R. Liu, B. G. Li, J. R. Lou, K. R. Dai, and T. T. Tang, “Biologic effect and immunoisolating behavior of BMP-2 gene-transfected bone marrow-derived mesenchymal stem cells in APA microcapsules,” Biochem Biophys Res Commun, vol. 362, no. 4, pp. 923–927, 2007. View at: Google Scholar
  53. S. Bohman and A. J. King, “Islet alpha cell number is maintained in microencapsulated islet transplantation,” Biochem Biophys Res Commun, vol. 377, no. 2, pp. 729–733, 2008. View at: Google Scholar
  54. Y. Teramura and H. Iwata, “Islet encapsulation with living cells for improvement of biocompatibility,” Biomaterials, vol. 30, no. 12, pp. 2270–2275, 2009. View at: Google Scholar
  55. E. S. O'Sullivan, A. S. Johnson, A. Omer et al., “Rat islet cell aggregates are superior to islets for transplantation in microcapsules,” Diabetologia, vol. 53, no. 5, pp. 937–945, 2010. View at: Google Scholar
  56. S. Schneider, M. A. von Mach, O. Kraus, P. Kann, and P. J. Feilen, “Intraportal transplantation of allogenic pancreatic islets encapsulated in barium alginate beads in diabetic rats,” Artif Organs, vol. 27, no. 11, pp. 1053–1056, 2003. View at: Google Scholar
  57. R. Calafiore, G. Basta, G. Luca et al., “Standard technical procedures for microencapsulation of human islets for graft into nonimmunosuppressed patients with type 1 diabetes mellitus,” Transplant Proc, vol. 38, no. 4, pp. 1156–1157, 2006. View at: Google Scholar
  58. R. Calafiore, G. Basta, G. Luca et al., “Microencapsulated pancreatic islet allografts into nonimmunosuppressed patients with type 1 diabetes: first two cases,” Diabetes Care, vol. 29, no. 1, pp. 137–138, 2006. View at: Google Scholar
  59. D. F. Emerich, C. G. Thanos, M. Goddard et al., “Extensive neuroprotection by choroid plexus transplants in excitotoxin lesioned monkeys,” Neurobiol Dis, vol. 23, no. 2, pp. 471–480, 2006. View at: Google Scholar
  60. Y. Jeon, K. Kwak, S. Kim, Y. Kim, J. Lim, and W. Baek, “Intrathecal implants of microencapsulated xenogenic chromaffin cells provide a long-term source of analgesic substances,” Transplant Proc, vol. 38, no. 9, pp. 3061–3065, 2006. View at: Google Scholar
  61. X. L. Shi, Y. Zhang, J. Y. Gu, and Y. T. Ding, “Coencapsulation of hepatocytes with bone marrow mesenchymal stem cells improves hepatocyte-specific functions,” Transplantation, vol. 88, no. 10, pp. 1178–1185, 2009. View at: Google Scholar
  62. Y. Teng, Y. Wang, S. Li et al., “Treatment of acute hepatic failure in mice by transplantation of mixed microencapsulation of rat hepatocytes and transgenic human fetal liver stromal cells,” Tissue Eng Part C Methods, vol. 16, no. 5, pp. 1125–1134, 2010. View at: Google Scholar
  63. J. P. Miranda, A. Rodrigues, R. M. Tostoes et al., “Extending hepatocyte functionality for drug-testing applications using high-viscosity alginate-encapsulated three-dimensional cultures in bioreactors,” Tissue Eng Part C Methods, vol. 16, no. 6, pp. 1223–1232, 2010. View at: Google Scholar
  64. R. M. Tostoes, S. B. Leite, J. P. Miranda et al., “Perfusion of 3D encapsulated hepatocytes—a synergistic effect enhancing long-term functionality in bioreactors,” Biotechnol Bioeng, vol. 108, no. 1, pp. 41–49, 2011. View at: Google Scholar
  65. M. Dvir-Ginzberg, A. Konson, S. Cohen, and R. Agbaria, “Entrapment of retroviral vector producer cells in three-dimensional alginate scaffolds for potential use in cancer gene therapy,” J Biomed Mater Res B Appl Biomater, vol. 80, no. 1, pp. 59–66, 2007. View at: Google Scholar
  66. Y. F. Han, Y. Q. Han, Y. G. Pan, Y. L. Chen, and J. K. Chai, “Transplantation of microencapsulated cells expressing VEGF improves angiogenesis in implanted xenogeneic acellular dermis on wound,” Transplant Proc, vol. 42, no. 5, pp. 1935–1943, 2010. View at: Google Scholar
  67. A. Murua, G. Orive, R. M. Hernandez, and J. L. Pedraz, “Epo delivery by genetically engineered C2C12 myoblasts immobilized in microcapsules,” Adv Exp Med Biol, vol. 670, pp. 54–67, 2010. View at: Google Scholar
  68. H. Nakama, K. Ohsugi, T. Otsuki et al., “Encapsulation cell therapy for mucopolysaccharidosis type VII using genetically engineered immortalized human amniotic epithelial cells,” Tohoku J Exp Med, vol. 209, no. 1, pp. 23–32, 2006. View at: Google Scholar
  69. B. Salmons and W. H. Gunzburg, “Therapeutic application of cell microencapsulation in cancer,” Adv Exp Med Biol, vol. 670, pp. 92–103, 2010. View at: Google Scholar
  70. C. G. Thanos, B. Bintz, and D. F. Emerich, “Microencapsulated choroid plexus epithelial cell transplants for repair of the brain,” Adv Exp Med Biol, vol. 670, pp. 80–91, 2010. View at: Google Scholar
  71. T. Yasuhara and I. Date, “Intracerebral transplantation of genetically engineered cells for Parkinson's disease: toward clinical application,” Cell Transplant, vol. 16, no. 2, pp. 125–132, 2007. View at: Google Scholar
  72. H. Zhang, S. J. Zhu, W. Wang, Y. J. Wei, and S. S. Hu, “Transplantation of microencapsulated genetically modified xenogeneic cells augments angiogenesis and improves heart function,” Gene Ther, vol. 15, no. 1, pp. 40–48, 2008. View at: Google Scholar
  73. R. M. Olabisi, Z. W. Lazard, C. L. Franco et al., “Hydrogel microsphere encapsulation of a cell-based gene therapy system increases cell survival of injected cells, transgene expression, and bone volume in a model of heterotopic ossification,” Tissue Eng Part A, vol. 16, no. 12, pp. 3727–3736, 2010. View at: Google Scholar
  74. D. E. Awrey, M. Tse, G. Hortelano, and P. L. Chang, “Permeability of alginate microcapsules to secretory recombinant gene products,” Biotechnol Bioeng, vol. 52, no. 4, pp. 472–484, 1996. View at: Google Scholar
  75. P. A. Sieving, R. C. Caruso, W. Tao et al., “Ciliary neurotrophic factor (CNTF) for human retinal degeneration: phase I trial of CNTF delivered by encapsulated cell intraocular implants,” Proc Natl Acad Sci U S A, vol. 103, no. 10, pp. 3896–3901, 2006. View at: Google Scholar
  76. A. Paul, Y. Ge, S. Prakash, and D. Shum-Tim, “Microencapsulated stem cells for tissue repairing: implications in cell-based myocardial therapy,” Regen Med, vol. 4, no. 5, pp. 733–745, 2009. View at: Google Scholar
  77. Z. C. Liu and T. M. Chang, “Artificial cell microencapsulated stem cells in regenerative medicine, tissue engineering and cell therapy,” Adv Exp Med Biol, vol. 670, pp. 68–79, 2010. View at: Google Scholar
  78. H. R. Moyer, R. C. Kinney, K. A. Singh, J. K. Williams, Z. Schwartz, and B. D. Boyan, “Alginate microencapsulation technology for the percutaneous delivery of adipose-derived stem cells,” Ann Plast Surg, vol. 65, no. 5, pp. 497–503, 2010. View at: Google Scholar
  79. A. M. Heile, C. Wallrapp, P. M. Klinge et al., “Cerebral transplantation of encapsulated mesenchymal stem cells improves cellular pathology after experimental traumatic brain injury,” Neurosci Lett, vol. 463, no. 3, pp. 176–181, 2009. View at: Google Scholar
  80. P. M. Klinge, K. Harmening, M. C. Miller et al., “Encapsulated native and glucagon-like peptide-1 transfected human mesenchymal stem cells in a transgenic mouse model of Alzheimer's disease,” Neurosci Lett, vol. 497, no. 1, pp. 6–10, 2011. View at: Google Scholar
  81. M. Chayosumrit, B. Tuch, and K. Sidhu, “Alginate microcapsule for propagation and directed differentiation of hESCs to definitive endoderm,” Biomaterials, vol. 31, no. 3, pp. 505–514, 2010. View at: Google Scholar
  82. S. K. Dean, Y. Yulyana, G. Williams, K. S. Sidhu, and B. E. Tuch, “Differentiation of encapsulated embryonic stem cells after transplantation,” Transplantation, vol. 82, no. 9, pp. 1175–1184, 2006. View at: Google Scholar
  83. M. B. Evangelista, S. X. Hsiong, R. Fernandes et al., “Upregulation of bone cell differentiation through immobilization within a synthetic extracellular matrix,” Biomaterials, vol. 28, no. 25, pp. 3644–3655, 2007. View at: Google Scholar
  84. T. Maguire, A. E. Davidovich, E. J. Wallenstein et al., “Control of hepatic differentiation via cellular aggregation in an alginate microenvironment,” Biotechnol Bioeng, vol. 98, no. 3, pp. 631–644, 2007. View at: Google Scholar
  85. E. K. Yim, A. C. Wan, C. Le Visage, I. C. Liao, and K. W. Leong, “Proliferation and differentiation of human mesenchymal stem cell encapsulated in polyelectrolyte complexation fibrous scaffold,” Biomaterials, vol. 27, no. 36, pp. 6111–6122, 2006. View at: Google Scholar
  86. B. P. Chan, T. Y. Hui, M. Y. Wong, K. H. Yip, and G. C. Chan, “Mesenchymal stem cell-encapsulated collagen microspheres for bone tissue engineering,” Tissue Eng Part C Methods, vol. 16, no. 2, pp. 225–235, 2010. View at: Google Scholar
  87. A. T. Mehlhorn, H. Schmal, S. Kaiser et al., “Mesenchymal stem cells maintain TGF-beta-mediated chondrogenic phenotype in alginate bead culture,” Tissue Eng, vol. 12, no. 6, pp. 1393–1403, 2006. View at: Google Scholar
  88. L. Penolazzi, E. Tavanti, R. Vecchiatini et al., “Encapsulation of mesenchymal stem cells from Wharton's jelly in alginate microbeads,” Tissue Eng Part C Methods, vol. 16, no. 1, pp. 141–155, 2010. View at: Google Scholar
  89. E. Trouche, S. G. Fullana, C. Mias et al., “Evaluation of alginate microspheres for mesenchymal stem cells engraftment on solid organ,” Cell Transplant, vol. 19, no. 12, pp. 1623–1633, 2010. View at: Google Scholar
  90. J. S. Park, H. N. Yang, D. G. Woo, H. Kim, K. Na, and K. H. Park, “Multi-lineage differentiation of hMSCs encapsulated in thermo-reversible hydrogel using a co-culture system with differentiated cells,” Biomaterials, vol. 31, no. 28, pp. 7275–7287, 2010. View at: Google Scholar
  91. N. Siti-Ismail, A. E. Bishop, J. M. Polak, and A. Mantalaris, “The benefit of human embryonic stem cell encapsulation for prolonged feeder-free maintenance,” Biomaterials, vol. 29, no. 29, pp. 3946–3952, 2008. View at: Google Scholar
  92. D. Jing, A. Parikh, and E. S. Tzanakakis, “Cardiac Cell Generation from Encapsulated Embryonic Stem Cells in Static and Scalable Culture Systems,” Cell Transplant, vol. 19, no. 11, pp. 1397–1412, 2010. View at: Google Scholar
  93. M. Endres, N. Wenda, H. Woehlecke et al., “Microencapsulation and chondrogenic differentiation of human mesenchymal progenitor cells from subchondral bone marrow in Ca-alginate for cell injection,” Acta Biomater, vol. 6, no. 2, pp. 436–444, 2010. View at: Google Scholar
  94. Z. Chang Liu and T. M. Chang, “Coencapsulation of hepatocytes and bone marrow cells: in vitro and in vivo studies,” Biotechnol Annu Rev, vol. 12, pp. 137–151, 2006. View at: Google Scholar
  95. Z. C. Liu and T. M. Chang, “Coencapsulation of hepatocytes and bone marrow stem cells: in vitro conversion of ammonia and in vivo lowering of bilirubin in hyperbilirubemia Gunn rats,” Int J Artif Organs, vol. 26, no. 6, pp. 491–497, 2003. View at: Google Scholar
  96. Y. S. Hwang, J. Cho, F. Tay et al., “The use of murine embryonic stem cells, alginate encapsulation, and rotary microgravity bioreactor in bone tissue engineering,” Biomaterials, vol. 30, no. 4, pp. 499–507, 2009. View at: Google Scholar
  97. S. Sakai, I. Hashimoto, and K. Kawakami, “Production of cell-enclosing hollow-core agarose microcapsules via jetting in water-immiscible liquid paraffin and formation of embryoid body-like spherical tissues from mouse ES cells enclosed within these microcapsules,” Biotechnol Bioeng, vol. 99, no. 1, pp. 235–243, 2008. View at: Google Scholar
  98. A. H. Al Kindi, J. F. Asenjo, Y. Ge et al., “Microencapsulation to reduce mechanical loss of microspheres: implications in myocardial cell therapy,” Eur J Cardiothorac Surg, vol. 39, no. 2, pp. 241–247, 2010. View at: Google Scholar
  99. 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, no. 27, pp. 7012–7020, 2010. View at: Google Scholar
  100. T. Maguire, E. Novik, R. Schloss, and M. Yarmush, “Alginate-PLL microencapsulation: effect on the differentiation of embryonic stem cells into hepatocytes,” Biotechnol Bioeng, vol. 93, no. 3, pp. 581–591, 2006. View at: Google Scholar
  101. X. Wang, W. Wang, J. Ma, X. Guo, X. Yu, and X. Ma, “Proliferation and differentiation of mouse embryonic stem cells in APA microcapsule: A model for studying the interaction between stem cells and their niche,” Biotechnol Prog, vol. 22, no. 3, pp. 791–800, 2006. View at: Google Scholar
  102. S. Sakai and K. Kawakami, “Development of subsieve-size capsules and application to cell therapy,” Adv Exp Med Biol, vol. 670, pp. 22–30, 2010. View at: Google Scholar
  103. S. Sakai, K. Kawabata, T. Ono, H. Ijima, and K. Kawakami, “Preparation of mammalian cell-enclosing subsieve-sized capsules (<100 microm) in a coflowing stream,” Biotechnol Bioeng, vol. 86, no. 2, pp. 168–173, 2004. View at: Google Scholar
  104. B. L. Strand, O. Gaserod, B. Kulseng, T. Espevik, and G. Skjak-Baek, “Alginate-polylysine-alginate microcapsules: effect of size reduction on capsule properties,” J Microencapsul, vol. 19, no. 5, pp. 615–630, 2002. View at: Google Scholar
  105. C. J. Ross and P. L. Chang, “Development of small alginate microcapsules for recombinant gene product delivery to the rodent brain,” J Biomater Sci Polym Ed, vol. 13, no. 8, pp. 953–962, 2002. View at: Google Scholar
  106. S. Sakai, C. Mu, K. Kawabata, I. Hashimoto, and K. Kawakami, “Biocompatibility of subsieve-size capsules versus conventional-size microcapsules,” J Biomed Mater Res A, vol. 78, no. 2, pp. 394–398, 2006. View at: Google Scholar
  107. S. Sakai, K. Kawabata, S. Tanaka et al., “Subsieve-size agarose capsules enclosing ifosfamide-activating cells: a strategy toward chemotherapeutic targeting to tumors,” Mol Cancer Ther, vol. 4, no. 11, pp. 1786–1790, 2005. View at: Google Scholar
  108. R. Robitaille, J. F. Pariseau, F. A. Leblond, M. Lamoureux, Y. Lepage, and J. P. Halle, “Studies on small (<350 microm) alginate-poly-L-lysine microcapsules. III. Biocompatibility Of smaller versus standard microcapsules,” J Biomed Mater Res, vol. 44, no. 1, pp. 116–120, 1999. View at: Google Scholar
  109. B. Chin Heng, H. Yu, and S. Chye Ng, “Strategies for the cryopreservation of microencapsulated cells,” Biotechnol Bioeng, vol. 85, no. 2, pp. 202–213, 2004. View at: Google Scholar
  110. X. He, E. Y. Park, A. Fowler, M. L. Yarmush, and M. Toner, “Vitrification by ultra-fast cooling at a low concentration of cryoprotectants in a quartz micro-capillary: a study using murine embryonic stem cells,” Cryobiology, vol. 56, no. 3, pp. 223–232, 2008. View at: Google Scholar
  111. V. Berejnov, N. S. Husseini, O. A. Alsaied, and R. E. Thorne, “Effects of cryoprotectant concentration and cooling rate on vitrification of aqueous solutions,” Journal of Applied Crystallography, vol. 39, pp. 39–244, 2006. View at: Google Scholar
  112. J. F. Edd, D. Di Carlo, K. J. Humphry et al., “Controlled encapsulation of single-cells into monodisperse picolitre drops,” Lab Chip, vol. 8, no. 8, pp. 1262–1264, 2008. View at: Google Scholar
  113. S. Sugiura, T. Oda, Y. Izumida et al., “Size control of calcium alginate beads containing living cells using micro-nozzle array,” Biomaterials, vol. 26, no. 16, pp. 3327–3331, 2005. View at: Google Scholar
  114. H. Shintaku, T. Kuwabara, S. Kawano, T. Suzuki, I. Kanno, and H. Kotera, “Micro cell encapsulation and its hydrogel-beads production using microfluidic device,” Microsystem Technologies-Micro-and Nanosystems-Information Storage and Processing Systems, vol. 13, no. 8–10, pp. 951–958, 2007. View at: Google Scholar
  115. K. S. Huang, M. K. Liu, C. H. Wu, Y. T. Yen, and Y. C. Lin, “Calcium alginate microcapsule generation on a microfluidic system fabricated using the optical disk process,” J Micromech Microeng, vol. 17, no. 8, pp. 1428–1434, 2007. View at: Google Scholar
  116. G. Karoubi, M. L. Ormiston, D. J. Stewart, and D. W. Courtman, “Single-cell hydrogel encapsulation for enhanced survival of human marrow stromal cells,” Biomaterials, vol. 30, no. 29, pp. 5445–5455, 2009. View at: Google Scholar
  117. W. Zhang and X. He, “Encapsulation of living cells in small ( approximately 100 microm) alginate microcapsules by electrostatic spraying: a parametric study,” J Biomech Eng, vol. 131, no. 7:074515, 2009. View at: Google Scholar
  118. B. C. Heng, Y. J. Yu, and S. C. Ng, “Slow-cooling protocols for microcapsule cryopreservation,” J Microencapsul, vol. 21, no. 4, pp. 455–467, 2004. View at: Google Scholar
  119. V. Stensvaag, T. Furmanek, K. Lonning, A. J. Terzis, R. Bjerkvig, and T. Visted, “Cryopreservation of alginate-encapsulated recombinant cells for antiangiogenic therapy,” Cell Transplant, vol. 13, no. 1, pp. 35–44, 2004. View at: Google Scholar
  120. Y. Wu, H. Yu, S. Chang, R. Magalhaes, and L. L. Kuleshova, “Vitreous cryopreservation of cell-biomaterial constructs involving encapsulated hepatocytes,” Tissue Eng, vol. 13, no. 3, pp. 649–658, 2007. View at: Google Scholar
  121. L. Canaple, N. Nurdin, N. Angelova, D. Saugy, D. Hunkeler, and B. Desvergne, “Maintenance of primary murine hepatocyte functions in multicomponent polymer capsules—in vitro cryopreservation studies,” J Hepatol, vol. 34, no. 1, pp. 11–18, 2001. View at: Google Scholar
  122. D. Zhou, I. Vacek, and A. M. Sun, “Cryopreservation of microencapsulated porcine pancreatic islets: in vitro and in vivo studies,” Transplantation, vol. 64, no. 8, pp. 1112–1116, 1997. View at: Google Scholar
  123. P. B. Stiegler, V. Stadlbauer, S. Schaffellner et al., “Cryopreservation of insulin-producing cells microencapsulated in sodium cellulose sulfate,” Transplant Proc, vol. 38, no. 9, pp. 3026–3030, 2006. View at: Google Scholar
  124. M. Murakami, H. Satou, T. Kimura et al., “Effects of micro-encapsulation on morphology and endocrine function of cryopreserved neonatal porcine islet-like cell clusters,” Transplantation, vol. 70, no. 8, pp. 1143–1148, 2000. View at: Google Scholar
  125. E. J. Woods, J. Liu, M. A. Zieger, J. R. Lakey, and J. K. Critser, “The effects of microencapsulation on pancreatic islet osmotically induced volumetric response,” Cell Transplant, vol. 8, no. 6, pp. 699–708, 1999. View at: Google Scholar
  126. Y. Matsumoto, Y. Morinaga, M. Ujihira, K. Oka, and K. Tanishita, “Improvement in the viability of cryopreserved cells by microencapsulation,” JSME International Journal Series C, Mechanical Systems, Machine Elements and Manufacturing, vol. 67, no. 654, pp. 580–587, 2001. View at: Google Scholar
  127. A. Murua, G. Orive, R. M. Hernandez, and J. L. Pedraz, “Cryopreservation based on freezing protocols for the long-term storage of microencapsulated myoblasts,” Biomaterials, vol. 30, no. 20, pp. 3495–3501, 2009. View at: Google Scholar
  128. R. Malpique, L. M. Osorio, D. S. Ferreira et al., “Alginate Encapsulation as a Novel Strategy for the Cryopreservation of Neurospheres,” Tissue Eng Part C Methods, vol. 16, no. 5, pp. 965–977, 2010. View at: Google Scholar
  129. GLP-1 CellBeads® for the Treatment of Stroke Patients With Space-occupying Intracerebral Hemorrhage, http://www.clinicaltrials.gov, ID: NCT01298830.
  130. G. M. Fahy, D. R. MacFarlane, C. A. Angell, and H. T. Meryman, “Vitrification as an approach to cryopreservation,” Cryobiology, vol. 21, no. 4, pp. 407–426, 1984. View at: Google Scholar
  131. W. F. Rall and G. M. Fahy, “Ice-free cryopreservation of mouse embryos at -196 degrees C by vitrification,” Nature, vol. 313, no. 6003, pp. 573–575, 1985. View at: Google Scholar
  132. C. A. Agudelo and H. Iwata, “The development of alternative vitrification solutions for microencapsulated islets,” Biomaterials, vol. 29, no. 9, pp. 1167–1176, 2008. View at: Google Scholar
  133. L. L. Kuleshova, X. W. Wang, Y. N. Wu, Y. Zhou, and H. Yu, “Vitrification of encapsulated hepatocytes with reduced cooling and warming rates,” Cryo Letters, vol. 25, no. 4, pp. 241–254, 2004. View at: Google Scholar
  134. W. Zhang, G. Yang, A. Zhang, L. X. Xu, and X. He, “Preferential vitrification of water in small alginate microcapsules significantly augments cell cryopreservation by vitrification,” Biomed Microdevices, vol. 12, no. 1, pp. 89–96, 2010. View at: Google Scholar
  135. G. J. Lim, S. Zare, M. Van Dyke, and A. Atala, “Cell microencapsulation,” Adv Exp Med Biol, vol. 670, pp. 126–136, 2010. View at: Google Scholar
  136. J. van Zanten and P. de Vos, “Regulatory considerations in application of encapsulated cell therapies,” Adv Exp Med Biol, vol. 670, pp. 31–37, 2010. View at: Google Scholar
  137. G. Luca, R. Galafiore, G. Basta et al., “Improved function of rat islets upon co-microencapsulation with Sertoli's cells in alginate/poly-L-ornithine,” AAPS PharmSciTech, vol. 2, no. 3: E15, 2001. View at: Google Scholar
  138. S. K. Tam, S. Bilodeau, J. Dusseault, G. Langlois, J. P. Halle, and L. H. Yahia, “Biocompatibility and physicochemical characteristics of alginate-polycation microcapsules,” Acta Biomater, vol. 7, no. 4, pp. 1683–1692, 2011. View at: Google Scholar
  139. J. S. Moon, H. M. Jeon, W. Meng, T. Akaike, and I. K. Kang, “Morphology and metabolism of hepatocytes microencapsulated with acrylic terpolymer-alginate using gelatin and poly(vinyl alcohol) as extracellular matrices,” J Biomater Sci Polym Ed, vol. 16, no. 10, pp. 1245–1259, 2005. View at: Google Scholar
  140. S. Sakai, I. Hashimoto, S. Tanaka, B. Salmons, and K. Kawakami, “Small agarose microcapsules with cell-enclosing hollow core for cell therapy: transplantation of Ifosfamide-activating cells to the mice with preestablished subcutaneous tumor,” Cell Transplant, vol. 18, no. 8, pp. 933–939, 2009. View at: Google Scholar
  141. T. Ando, H. Yamazoe, K. Moriyasu, Y. Ueda, and H. Iwata, “Induction of dopamine-releasing cells from primate embryonic stem cells enclosed in agarose microcapsules,” Tissue Eng, vol. 13, no. 10, pp. 2539–2547, 2007. View at: Google Scholar
  142. A. Khademhosseini, G. Eng, J. Yeh et al., “Micromolding of photocrosslinkable hyaluronic acid for cell encapsulation and entrapment,” J Biomed Mater Res A, vol. 79, no. 3, pp. 522–532, 2006. View at: Google Scholar
  143. J. K. Kutty and K. Webb, “Vibration stimulates vocal mucosa-like matrix expression by hydrogelencapsulated fibroblasts,” J Tissue Eng Regen Med, vol. 4, no. 1, pp. 62–72, 2010. View at: Google Scholar
  144. M. Qi, Y. Gu, N. Sakata et al., “PVA hydrogel sheet macroencapsulation for the bioartificial pancreas,” Biomaterials, vol. 25, no. 27, pp. 5885–5892, 2004. View at: Google Scholar
  145. H. Nojehdehian, F. Moztarzadeh, H. Baharvand, N. Z. Mehrjerdi, H. Nazarian, and M. Tahriri, “Effect of poly-L-lysine coating on retinoic acid-loaded PLGA microspheres in the differentiation of carcinoma stem cells into neural cells,” Int J Artif Organs, vol. 33, no. 10, pp. 721–730, 2010. View at: Google Scholar
  146. J. Mokry, J. Karbanova, J. Lukas, V. Paleckova, and B. Dvorankova, “Biocompatibility of HEMA copolymers designed for treatment of CNS diseases with polymer-encapsulated cells,” Biotechnol Prog, vol. 16, no. 5, pp. 897–904, 2000. View at: Google Scholar
  147. M. Surzyn, J. Symes, J. A. Medin, and M. V. Sefton, “IL-10 secretion increases signal persistence of HEMAMMA-microencapsulated luciferase-modified CHO fibroblasts in mice,” Tissue Eng Part A, vol. 15, no. 1, pp. 127–136, 2009. View at: Google Scholar

Copyright © 2011 Hindawi Publishing Corporation. 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.


More related articles

 PDF Download Citation Citation
 Order printed copiesOrder
Views461
Downloads440
Citations

Related articles

We are committed to sharing findings related to COVID-19 as quickly as possible. We will be providing unlimited waivers of publication charges for accepted research articles as well as case reports and case series related to COVID-19. Review articles are excluded from this waiver policy. Sign up here as a reviewer to help fast-track new submissions.