Current status on immunoprotection of transplanted islets: Focus on islet microencapsulation

Micro and Nanosystems

Volumn 5, Issue 3, 2013, Pages 168-176

  Lacík, Igor ^a  

^a INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

Bioartifical pancreas; Conformal coating; Diabetes; Islet encapsulation; Islet immunoprotection; Macrocapsule; Microbead; Microcapsule

Indexed keywords

BIOARTIFICAL PANCREAS; CONFORMAL COATINGS; IMMUNOPROTECTION; ISLET ENCAPSULATIONS; MACROCAPSULE; MICROBEADS; MICROCAPSULES;

BIOLOGICAL MATERIALS; MEDICAL PROBLEMS;

MICROENCAPSULATION;

EID: 84892982430     PISSN: 18764029     EISSN: 18764037     Source Type: Journal    
DOI: 10.2174/1876402911305030004     Document Type: Article

References (144)

1. Shapiro, A. M.; Lakey, J. R.; Ryan, E. A.; Korbutt, G. S.; Toth, E.; Warnock, G. L.; Kneteman, N. M.; Rajotte, R. V. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N. Engl. J. Med., 2000, 343(4), 230-238.
2. Barton, F. B.; Rickels, M. R.; Alejandro, R.; Hering, B. J.; Wease, S.; Naziruddin, B.; Oberholzer, J.; Odorico, J. S.; Garfinkel, M. R.; Levy, M.; Pattou, F.; Berney, T.; Secchi, A.; Messinger, S.; Senior, P. A.; Maffi, P.; Posselt, A.; Stock, P. G.; Kaufman, D. B.; Luo, X.; Kandeel, F.; Cagliero, E.; Turgeon, N. A.; Witkowski, P.; Naji, A.; O'Connell, P. J.; Greenbaum, C.; Kudva, Y. C.; Brayman, K. L.; Aull, M. J.; Larsen, C.; Kay, T. W. H.; Fernandez, L. A.; Vantyghem, M.-C.; Bellin, M.; Shapiro, A. M. J. Improvement in outcomes of clinical islet transplantation: 1999-2010. Diabetes Care, 2012, 35(7), 1436-1445.
3. Tiwari, J. L.; Schneider, B.; Barton, F.; Anderson, S. A. Islet cell transplantation in type 1 diabetes: An analysis of efficacy outcomes and considerations for trial designs. Am. J. Transplant., 2012, 12(7), 1898-1907.
4. Chang, T. M. S. Semipermeable microcapsules. Science, 1964, 146(3643), 524-525.
5. Chick, W. L.; Like, A. A.; Lauris, V. Beta cell culture on synthetic capillaries: an artificial endocrine pancreas. Science, 1975, 187(4179), 847-848.
6. Lim, F.; Sun, A. M. Microencapsulated islets as bioartificial endocrine pancreas. Science, 1980, 210(4472), 908-909.
7. Ratner, B. D.; Hoffman, A. S.; Schoen, F. J.; Lemons, J. E. Biomaterials science: An introduction to materials in medicine, 2nd ed., Elsevier Academic Press: Amsterdam, 2004.
8. Halle, J. P.; de Vos, P.; Rosenberg, L. The bioartificial pancreas and other biohybrid therapies; Transworld Research Network; Kerala, 2009.
9. Mikos, A. G.; Papadaki, M. G.; Kouvroukoglou, S.; Ishaug, S. L.; Thomson, R. C. Mini-review: Islet transplantation to create a bioartificial pancreas. Biotechnol. Bioeng., 1994, 43(7), 673-677.
10. Lacík, I. Polymer chemistry in diabetes treatment by encapsulated islets of Langerhans: Sum-up in year 2006. Austr. J. Chem., 2006, 59(8), 508-524.
11. O'Sullivan, E. S.; Vegas, A.; Anderson, D. G.; Weir, G. C. Islets transplanted in immunoisolation devices: A review of the progress and the challenges that remain. Endocr. Rev., 2011, 32(6), 827-844.
12. Giraldo, J. A.; Weaver, J. D.; Stabler, C. L. Tissue engineering approaches to enhancing clinical islet transplantation through tissue engineering strategies. J. Diabetes Sci. Technol., 2010, 4(5), 1238-1247.
13. Vaithilingam, V.; Tuch, B. E. Islet transplantation and encapsulation: An update on recent developments. Rev. Diabet. Stud., 2011, 8(1), 51-67.
14. Basta, G., Calafiore, R. Immunoisolation of pancreatic islet grafts with no recipient's immunosuppression: Actual and future perspectives. Curr. Diab. Rep., 2011, 11(5), 384-391.
15. Borg, D. J.; Bonifacio, E. The use of biomaterials in islet transplantation. Curr. Diab. Rep., 2011, 11(5), 434-444.
16. Hernández, R. M.; Orive, G.; Murua, A.; Pedraz, J. L. Microcapsules and microcarriers for in situ cell delivery. Adv. Drug Deliv. Rev., 2010, 62(7-8), 711-730.
17. Sakata, N.; Sumi, S.; Yoshimatsu, G.; Goto, M.; Egawa, S.; Unno M. Encapsulated islets transplantation: Past, present and future. World J. Gastrointest. Pathophysiol., 2012, 3(1), 19-26.
18. Nafea, E. H.; Marson, A.; Poole-Warren, L. A.; Martens, P. J. Immunoisolating semi-permeable membranes for cell encapsulation: focus on hydrogels. J. Control. Release, 2011, 154(2), 110-122.
19. Zanin, M. P.; Pettingill, L. N.; Harvey, A. R.; Emerich, D. F.; Thanos, C. G.; Shepherd, R. K. The development of encapsulated cell technologies as therapies for neurological and sensory diseases. J. Control. Release, 2012, 160(1), 3-13.
20. Halban, P. A.; German, M. S.; Kahn, S. E.; Weir, G. C. Current status of islet cell replacement and regeneration therapy. J. Clin. Endocrinol. Metab., 2010, 95(3), 1034-1043.
21. Kerby, A.; Bohman, S.; Westberg, H.; Jones, P.; King, A. Immunoisolation of islets in high guluronic acid barium-alginate microcapsules does not improve graft outcome at the subcutaneous site. Artif. Organs, 2012, 36(6), 564-570.
22. O'Sullivan, E. S.; Johnson, A. S.; Omer, A.; Hollister-Lock, J.; Bonner-Weir, S.; Colton, C. K.; Weir, G. C. Rat islet cell aggregates are superior to islets for transplantation in microcapsules. Diabetologia, 2010, 53(5), 937-945.
23. Mallett, A. G.; Korbutt, G. S. Alginate modification improves longterm survival and function of transplanted encapsulated islets. Tissue Eng. Part A, 2009, 15(6), 1301-1309.
24. Duvivier-Kali, V. F.; Omer, A.; Parent, R. J.; O'Neil, J. J.; Weir, G. C. Complete protection of islets against allorejection and autoimmunity by a simple barium membrane. Diabetes, 2001, 50(8), 1698-1705.
25. Omer, A.; Duvivier-Kali, V. F.; Trivedi, N.; Wilmot, K.; Bonner-Weir, S.; Weir, G. C. Survival and maturation of microencapsulated porcine neonatal pancreatic cell clusters transplanted into immunocompetent diabetic mice. Diabetes, 2003, 52(1), 69-75.
26. Duvivier-Kali, V. F.; Omer, A.; Lopez-Avalos, M. D.; O'Neil, J. J.; Weir, G. C. Survival of microencapsulated adult pig islets in mice in spite of an antibody response. Am. J. Transplant., 2004, 4(12), 1991-2000.
27. 2+microbeads: In vitro and in vivo function. Artif. Cells Blood Substit. Biotechnol., 2008, 36(5), 403-420.
28. 2+. Xenotransplantation, 2012, 19(6), 355-364.
29. Vaithilingam, V.; Quayum, N.; Joglekar, M. V.; Jensen, J.; Hardikar, A. A.; Oberholzer, J.; Guillemin, G. J.; Tuch, B. E. Effect of alginate encapsulation on the cellular transcriptome of human islets. Biomaterials, 2011, 32(33), 8416-8425.
30. Tuch, B. E.; Keogh, G. W.; Williams, L. J.; Wu, W.; Foster, J. L.; Vaithilingam, V.; Philips, R. Safety and viability of microencapsulated human islets transplanted into diabetic humans. Diabetes Care, 2009, 32(10), 1887-1889.
31. Novamatrix: Ultrapure Biopolymer Systems. http://www. novamatrix. biz/Products. aspx (Accessed November 11, 2012).
32. Strand, B. L.; Ryan, T. L.; In't, V. P.; Kulseng, B.; Rokstad, A. M.; Skjåk-Bræk, G.; Espevik, T. Poly-L-lysine induces fibrosis on alginate microcapsules via the induction of cytokines. Cell Transplant., 2001, 10(3), 263-275.
33. Rokstad, A. M.; Brekke, O. L.; Steinkjer, B.; Ryan, L.; Kollarikova, G.; Strand, B. L.; Skjåk-Bræk, G.; Lacík, I.; Espevik, T.; Mollnes, T. E. Alginate microbeads are complement compatible, in contrast to polycation containing microcapsules, as revealed in a human whole blood model. Acta Biomater., 2011, 7(6), 2566-2578.
34. Rokstad, A. M.; Brekke, O. L.; Steinkjer, B.; Ryan, L.; Kollarikova, G.; Strand, B. L.; Skjåk-Bræk, G.; Lambris, J. D.; Lacík, I.; Mollnes, T. E.; Espevik, T. The induction of cytokines by polycation containing microspheres by a complement dependent mechanism. Biomaterials, 2013, 34, 621-630.
35. 2+ on alginate microbeads. Biomacromolecules, 2006, 7(5), 1471-1480.
36. Tam, S. K.; Dusseault, J.; Bilodeau, S.; Langlois, G.; Hallé, J.-P.; Yahia, L. Factors influencing alginate gel biocompatibility. J. Biomed. Mater. Res. A, 2011, 98(1), 40-52.
37. Langlois, G.; Dusseault, J.; Bilodeau, S.; Tam, S. K.; Magassouba, D.; Hallé, J.-P. Direct effect of alginate purification on the survival of islets immobilized in alginate-based microcapsules. Acta Biomater., 5(9), 3433-3440.
38. Mørch, Y. A.; Qi, M.; Gundersen, P. O. M; Formo, K.; Lacík, I.; Skjåk-Bræk, G.; Oberholzer, J.; Strand, B. L. Binding and leakage of barium in alginate microbeads. J. Biomed. Mater. Res. A, 2012, 100(11), 2939-2947.
39. Vaithilingam, V.; Kollarikova, G.; Qi, M.; Lacík, I.; Oberholzer, J.; Guillemin, G. J.; Tuch, B. E. Effect of prolonged gelling time on the intrinsic properties of barium alginate microcapsules and its biocompatibility. J. Microencapsulation, 2011, 28(6), 499-507.
40. Mørch, Y. A.; Donati, I.; Strand, B. L.; Skjåk-Braek, G. Molecular engineering as an approach to design new functional properties of alginate. Biomacromolecules, 2007, 8(9), 2809-2814.
41. Hoesli, C. A.; Raghuram, K.; Kiang, R. L.; Mocinecová, D.; Hu, X.; Johnson, J. D.; Lacík, I.; Kieffer, T. J.; Piret, J. M. Pancreatic cell immobilization in alginate beads produced by emulsion and internal gelation. Biotechnol. Bioeng. 2011, 108(2), 424-434.
42. Hoesli, C. A.; Kiang, R. L. J.; Mocinecová, D.; Speck, M.; Moýková, D. J.; Donald-Hague, C.; Lacík, I.; Kieffer, T. J.; Piret, J. M. Reversal of diabetes by αTC3 cells encapsulated in alginate beads generated by emulsion and internal gelation. J. Biomed. Mater. Res. B Appl. Biomater., 2012, 100(4), 1017-1028.
43. Hall, K. K.; Gattás-Asfura, K. M.; Stabler, C. L. Microencapsulation of islets within alginate/poly(ethylene glycol) gels cross-linked via Staudinger ligation. Acta Biomater., 2011, 7(2), 614-624.
44. Gattás-Asfura, K. M.; Fraker, C. A.; Stabler, C. L. Covalent stabilization of alginate hydrogel baeads via Staudinger ligation: Assessment of poly(ethylene glycol) and alginate crosslinkers. J. Biomed. Mater. Res. A, 2011, 99(1), 47-57.
45. Mahou, R.; Wandrey, C. Alginate-poly(ethylene glycol) hybrid microspheres with adjustable physical properties. Macromolecules, 2010, 43(3), 1371-1378.
46. Gattás-Asfura, K. M.; Fraker, C. A.; Stabler, C. L. Perfluorinated alginate for cellular encapsulation. J. Biomed. Mater. Res. A, 2012, 100(8), 1963-1971.
47. Johnson, A. S.; O'Sullivan, E.; D'Aoust, L. N.; Omer, A.; Bonner-Weir, S.; Fisher, R. J.; Weir, G. C.; Colton, C. K. Quantitative assessment of islets of Langerhans encapsulated in alginate. Tissue Eng. C Methods, 2011, 17(4), 435-449.
48. Calafiore, R.; Basta, G.; Falorni, A.; Picchio, M. L.; Gambelunghe, G.; Del Sindaco, P.; Brunetti, P. Fabrication of high performance microcapsules for pancreatic islet transplantation. Diab. Nutr. Metab. 1992, 5(Suppl. 1), 173-176.
49. Ponce, S.; Orive, G.; Hernandez, R.; Gascon, A. R.; Pedraz, J. L.; De Haan B. J.; Faas, M. M.; Mathieu, H. J.; de Vos, P. Chemistry and the biological response against immunoisolating alginatepolycation capsules of different composition. Biomaterials, 2006, 27(28), 4831-4839.
50. Montanucci, P.; Pennoni, I.; Pescara, T.; Blasi, P.; Bistoni, G.; Basta, G.; Calafiore, R. The functional performance of microencapsulated human pancreatic islet-derived precursor cells. Biomaterials, 2011, 32(35), 9254-9262.
51. Loh, Q. L.; Wong, Y. Y.; Choong, C. Combinatorial effect of different alginate compositions, polycations, and gelling ions on microcapsule properties. Colloid Polym. Sci., 2012, 290(7), 619-629.
52. Calafiore, R.; Basta, G.; Luca, G.; Lemmi, A.; Montanucci, M. P.; Calabrese, G.; Racanicchi, L.; Mancuso, F.; Brunetti, P. Microencapsulated pancreatic islet allografts into nonimmunosuppressed patients with type 1 diabetes-First two cases. Diabetes Care, 2006, 29(1), 137-138.
53. Basta, G.; Montanucci, P.; Luca, G.; Boselli, C.; Noya, G.; Barbaro, B.; Qi, M.; Kinzer, K. P.; Oberholzer, J.; Calafiore, R. Longterm metabolic and immunological follow-up of nonimmunosuppressed patients with type 1 diabetes treated with microencapsulated islet allografts: Four cases. Diabetes Care, 2011, 34(11), 2406-2409.
54. Living Cell Technologies. http://www. lctglobal. com/Media-And-News/Latest-News/(Accessed November 11, 2012).
55. Hillberg, A. L.; Kathirgamanathan, K.; Lam Janice, B. B.; Law, L. Y.; Garkavenko, O.; Elliott, R. B. Improving alginate-poly-Lornithine-alginate capsule biocompatibility through genipin crosslinking. J. Biomed. Mater. Res. B Appl. Biomater., 2013, 101(2), 258-268.
56. Khanna, O.; Moya, M. L.; Opara, E. C.; Brey, E. M. Synthesis of multilayered alginate microcapsules for the sustained release of fibroblast growth factor-1. J. Biomed. Mater. Res. A, 2010, 95(2), 632-640.
57. Opara, E. C.; Mirmalek-Sani, S.-H.; Khanna, O.; Moya, M. L.; Brey, E. M. Design of a bioartificial pancreas. J. Investig. Med., 2010, 58(7), 831-837.
58. McQuilling, J. P.; Arenas-Herrera, J.; Childers, C.; Pareta, R. A.; Khanna, O.; Jiang, B.; Brey, E. M.; Farney, A. C.; Opara, E. C. New alginate microcapsule system for angiogenic protein delivery and immunoisolation of islets for transplantation in the rat omentum pouch. Transplant. Proc., 2011, 43(9), 3262-3264.
59. Abalovich, A. G.; Bacqué, M. C.; Grana, D.; Milei, J. Pig pancreatic islet transplantation into spontaneously diabetic dogs. Transplant. Proc., 2009, 41(1), 328-330.
60. deVos, P.; Spasojevic, M.; de Haan, B. J.; Faas, M. M. The association between in vivo physicochemical changes and inflammatory responses against alginate based microcapsules. Biomaterials, 2012, 33, 5552-5559.
61. Mazumder, M. A. J.; Burke, N. A. D.; Shen, F.; Potter, M. A.; Stöver, H. D. H. Core-cross-linked alginate microcapsules for cell encapsulation. Biomacromolecules, 2009, 10(6), 1365-1373.
62. Shen, F.; Mazumder, M. A. J.; Burke, N. A. D.; Stöver, H. D. H.; Potter, M. A. Mechanically enhanced microcapsules for cellular gene therapy. J. Biomed. Mater. Res. B Appl. Biomater., 2009, 90(1), 350-361.
63. Arifin, D. R.; Manek, S.; Call, E.; Arepally, A.; Bulte, J. W. M. Microcapsules with intrinsic barium radiopacity for immunoprotection and X-ray/CT imaging of pancreatic islet cells. Biomaterials, 2012, 33(18), 4681-4689.
64. Antosiak-Iwariska, M.; Sitarek, E.; Sabat, M.; Godlewska, E.; Kinasiewicz, J.; Werynski, A. Isolation, banking, encapsulation and transplantation of different types of Langerhans islets. Pol. Arch. Med. Wewn., 2009, 119(5), 311-317.
65. Chen, X.; Zhang, L.; Qi, Z.; Guo, B.; Zhong, L.; Shen, B.; Yan, Z.; Zhang, J. Novel sulfated glucomannan-barium-alginate microcapsules in islet transplantation: significantly decreased the secretion of monocyte chemotactic protein 1 and improved the activity of islet in rats. Transplant. Proc., 2009, 41(10), 4307-4312.
66. Qi, M.; Lacík, I.; Kollarikova, G.; Strand, B. L.; Formo, K.; Wang, Y.; Marchese, E.; Mendoza-Elias, J. E.; Kinzer, K. P.; Gatti, F.; Paushter, D.; Patel, S.; Oberholzer. J. A recommended laparoscopic procedurefor implantation of microcapsules in the peritoneal cavity of non-human primates. J. Surgical Res., 2011, 168(1), 117-123.
67. Wang, T. G.; Lacík, I.; Briýýová, M.; Anilkumar, A. V.; Prokop, A.; Hunkeler, D.; Green, R.; Shahrokhi, K.; Powers, A. C. An encapsulation system for the immunoizolation of pancreatic islets. Nature Biotechnol., 1997, 15(4), 358-362.
68. Lacík, I.; Briýýová, M.; Anilkumar, A. V.; Powers, A. C.; Wang T. G. New capsule with tailored properties for the encapsulation of living cells. J. Biomed. Mater. Res., 1998, 39(1), 52-60.
69. Wang, T.; Adcock, J.; Kühtreiber, W.; Qiang, D.; Salleng, K. J.; Trenary, I.; Williams, P. Successful allotransplantation of encapsulated islets in pancreatectomized canines for diabetic management without the use of immunosuppression. Transplantation., 2008, 85(3), 331-337.
70. Lin, C. C.; Anseth, K. S. Cell-cell communication mimicry with poly(ethylene glycol) hydrogels for enhancing α-cell function. Proc. Natl. Acad. Sci. U. S. A., 2011, 108(16), 6380-6385.
71. Su, J.; Hu, B.-H.; Lowe, W. L.; Kaufman, D. B.; Messersmith, P. B. Anti-inflammatory peptide-functionalized hydrogels for insulinsecreting cell encapsulation. Biomaterials, 2010, 31(2), 308-314.
72. Hume, P. S.; Anseth, K. S. Polymerizable superoxide dismutase mimetic protects cells encapsulated in poly(ethylene glycol) hydrogels from reactive oxygen species-mediated damage. J. Biomed. Mater. Res. A, 2011, 99(1), 29-37.
73. Lin, C. C.; Metters, A. T.; Anseth, K. S. Functional PEG-peptide hydrogels to modulate local inflammation induced by the proinflammatory cytokine TNF-cc. Biomaterials, 2009, 30(28), 4907-4914.
74. Lin, C. C.; Boyer, P. D.; Aimetti, A. A.; Anseth, K. S. RegulatingMCP-1diffusion in affinity hydrogels for enhancing immunoisolation. J. Control. Release, 2010, 142(3), 384-391.
75. Steele, J. A. M.; Barron, A. E.; Carmona, E.; Hallé, J.-P.; Neufeld, R. J. Encapsulation of protein microfiber networks supporting pancreatic islets. J. Biomed. Mater. Res. A, 2012, 100(12), 3384-3391.
76. Davis, N. E.; Beenken-Rothkopf, L. N.; Mirsoian, A.; Kojic, N.; Kaplan, D. L.; Barron, A. E.; Fontaine, M. J. Enhanced function of pancreatic islets co-encapsulated with ECM proteins and mesenchymal stromal cells in a silk hydrogel. Biomaterials, 2012, 33(28), 6691-6697.
77. Rackham, C. L.; Chagastelles, P. C.; Nardi, N. B.; Hauge-Evans, A. C.; Jones, P. M.; King, A. J. Co-transplantation of mesenchymal stem cells maintains islet organisation and morphology in mice. Diabetologia, 2011, 54(5), 1127-1135.
78. Ding, Y.; Xu, D.; Feng, G.; Bushell, A.; Muschel, R. J.; Wood, K. J. Mesenchymal stem cells prevent the rejection of fully allogenic islet grafts by the immunosuppressive activity of matrix metalloproteinase-2 and-9. Diabetes, 2009, 58(8), 1797-1806.
79. Bhaiji, T.; Zhi, Z.-L.; Pickup, J. C. Improving cellular function and immune protection via layer-by-layer nanocoating of pancreatic islet α-cell spheroids cocultured with mesenchymal stem cells. J. Biomed. Mater. Res. Part A2012, 100(6), 1628-1636.
80. Vériter, S.; Aouassar, N.; Adnet, P. Y.; Paridaens, M. S.; Stuckman, C.; Jordan, B.; Karroum, O.; Gallez, B.; Gianello, P.; Dufrane, D. The impact of hyperglycemia and the presence of encapsulated islets on oxygenation within a bioartificial pancreas in the presence of mesenchymal stem cells in a diabetic Wistar rat model. Biomaterials, 2011, 32(26), 5945-5956.
81. Sun, Y.; Liang, X.; Zhu, M.; Zhao, J.; Cheng, Y.; Duan, Y. Characterization and bioactivity of alginate-quaternized chitosan microcapsules. J. Macromol. Sci. Part A Pure Appl. Chem., 2012, 49(6), 483-489.
82. De Castro, M.; Orive, G.; Hernández, R. M.; Bartkowiak, A.; Brylak, W.; Pedraz, J. L. Biocompatibility and in vivo evaluation of oligochitosans as cationic modifiers of alginate/Ca microcapsules. J. Biomed. Mater. Res. Part A, 2009, 91(4), 1119-1130.
83. Luna, S. M.; Gomes, M. E.; Mano, J. F.; Reis, R. L. Development of a Novel Cell Encapsulation System Based on Natural Origin Polymers for Tissue Engineering Applications. J. Bioactive Compat. Polym., 2010, 25(4), 341-359.
84. Luan, N. M.; Iwata, H. Xenotransplantation of islets enclosed in agarose microcapsule carrying soluble complement receptor 1. Biomaterials, 2012, 33(32), 8075-8081.
85. Goldberg, M.; Mahon, K.; Anderson, D. Combinatorial and rational approaches to polymer synthesis for medicine. Adv. Drug Deliv. Rev., 2008, 60(9), 971-978.
86. Ma, M.; Liu, W. F.; Hill, P. S.; Bratlie, K. M.; Siegwart, D. J.; Chin, J.; Park, M.; Guerreiro, J.; Anderson, D. G. Development of cationic polymer coatings to regulate foreign-body responses. Adv. Mater., 2011, 23(24), 189-194.
87. Lee, J. I.; Kim, H. W.; Kim, J. Y.; Bae, S. J.; Joo, D. J.; Huh, K. H.; Fang, Y. H.; Jeong, J. H.; Kim, M. S.; Kim, Y. S. Microencapsulation of pancreatic islets with canine ear cartilage for immunoisolation. Transplant. Proc., 2012, 44(4), 1091-1094.
88. Kim, J. Y.; Lee, J. I.; Jeong, J. H.; Park, Y. J.; Kim, S. J.; Fang, Y. H.; Cho, Y.; Huh, K. H.; Joo, D. J.; Kim, M. S.; Kim, Y. S. Functional evaluation of chondrocyte sheeting immunodelusive immunoisolated bioartificial pancreas. Transplant. Proc., 2010, 42(3), 903-906.
89. Lee, J. I.; Kim, J. Y.; Kim, H. W.; Bae, S. J.; Joo, D. J.; Huh, K. H.; Fang, Y. H.; Jeong, J. H.; Kim, M. S.; Kim, Y. S. Long-term viability of transplanted hybrid cellular spheroids within chondrocyte sheets. Transplant. Proc., 2012, 44(4), 1162-1165.
90. Sakai, S.; Inagaki, H.; Inamoto, K.; Taya, M. Wrapping tissues with a pre-established cage-like layer composed of living cells. Biomaterials, 2012, 33(28), 6721-6727.
91. Teramura, Y.; Iwata, H. Islet encapsulation with living cells for improvement of biocompatibility. Biomaterials, 2009, 30(12), 2270-2275.
92. Dufrane, D.; Goebbels, R. M.; Gianello, P. Alginate macroencapsulation of pig islets allows correction of streptozotocin-induced diabetes in primates up to 6 months without immunosuppression. Transplantation, 2010, 90(10), 1054-1062.
93. Vériter, S.; Mergen, J.; Goebbels, R.-M.; Aouassar, N.; Grégoire, C.; Jordan, B.; Levêque, P.; Gallez, B.; Gianello, P.; Dufrane, D. In vivo selection of biocompatible alginates for islet encapsulation and subcutaneous transplantation. Tissue Eng. Part A, 2010, 16(5), 1503-1513.
94. Viacyte. http://www. viacyte. com/tech/encapsulation. html (Accessed November 11, 2012).
95. JDRF to Support ViaCyte's Development of Innovative Encapsulated Beta Cell Replacement Therapy for Diabetes. http://www. jdrf. org/index. cfm?pageid=116710 (Accessed November 11, 2012).
96. Erdodi, G.; Kennedy, J. P. Amphiphilic conetworks: Definition, synthesis, applications. Prog. Polym. Sci., 2006, 31(1), 1-18.
97. Erdodi, G.; Kang, J.; Yalcin, B.; Cakmak, M.; Rosenthal, K. S.; Grundfest-Broniatowski, S.; Kennedy, J. P. A novel macroencapsulating immunoisolatory device: The preparation and properties of nanomat-reinforced amphiphilic co-networks deposited on perforated metal scaffold. Biomed. Microdevices, 2009, 11(1), 297-312.
98. Kang, J.; Erdodi, G.; Kennedy, J. P.; Chou, H.; Lu, L.; Grundfest-Broniatowski, S. Toward a bioartificial pancreas: Diffusion of insulin and IgG across immunoprotective membranes with controlled hydrophilic channel diameters. Macromol. Biosci., 2010, 10(4), 369-377.
99. Pedraza, E.; Coronel, M. M.; Fraker, C. A.; Ricordi, C.; Stabler, C. L. Preventing hypoxia-induced cell death in beta cells and islets via hydrolytically activated, oxygen-generating biomaterials. Proc. Natl. Acad. Sci. U. S. A., 2012, 109(11), 4245-4250.
100. Ludwig, B.; Zimerman, B.; Steffen, A.; Yavriants, K.; Azarov, D.; Reichel, A.; Vardi, P.; German, T.; Shabtay, N.; Rotem, A.; Evron, Y.; Neufeld, T.; Mimon, S.; Ludwig, S.; Brendel, M. D.; Bornstein, S. R.; Barkai, U. A novel device for islet transplantation providing immune protection and oxygen supply. Horm. Metab. Res., 2010, 42(13), 918-922.
101. Ludwig, B.; Rotem, A.; Schmid, J.; Weir, G. C.; Colton, C. K.; Brendel, M. D.; Neufeld, T.; Block, N. L.; Yavriyants, K.; Steffen, A.; Ludwig, S.; Chavakis, T.; Reichel, A.; Azarov, D.; Zimermann, B.; Maimon, S.; Balyura, M.; Rozenshtein, T.; Shabtay, N.; Vardi, P.; Bloch, K.; de Vos, P.; Schally, A. V.; Bornstein, S. R.; Barkai, U. Improvement of islet function in a bioartificial pancreas by enhanced oxygen supply and growth hormone releasing hormone agonist. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(13), 5022-5027.
102. Muthyala, S.; Raj, V. R. R.; Mohanty, M.; Mohanan, P. V.; Nair, P. D. The reversal of diabetes in rat model using mouse insulin producing cells-A combination approach of tissue engineering and macroencapsulation. Acta Biomater., 2011, 7(5), 2153-2162.
103. Lee, S.-H.; Hao, E.; Savinov, A. Y.; Geron, I.; Strongin, A. Y.; Itkin-Ansari, P. Human α-cell precursors mature into functional insulin-producing cells in an immunoisolation device: Implications for diabetes cell therapies. Transplantation, 2009, 87(7), 983-991.
104. Lamb, M.; Storrs, R.; Li, S.; Liang, O.; Laugenour, K.; Dorian, R.; Chapman, D.; Ichii, H.; Imagawa, D.; Foster III, C.; King, S.; Lakey, J. R. T. Function and viability of human islets encapsulated in alginate sheets: In vitro and in vivo culture. Transplant. Proc., 2011, 43(9), 3265-3266.
105. Ader, M.; Storrs, R.; Endres, J.; Lamb, M.; Paredes, E. M.; Bergman, R. N.; Lakey, J. R. T. Testing in vivo functionality of alginateencapsulated pancreatic islets: advancing to the surgically-induced diabetic canine model. Diabetologia, 2012, 55(Suppl 1), S185.
106. Gimi, B.; Kwon, J.; Kuznetsov, A.; Vachha, B.; Magin, R. L.; Philipson, L. H.; Lee, J. B. A nanoporous, transparent microcontainer for encapsulated islet therapy. J. Diabetes Sci. Technol., 2009, 3(2), 297-303.
107. Kwon, J.; Trivedi, K.; Krishnamurthy, N. V.; Hu, W.; Lee, J.-B.; Gimi, B. SU-8-based immunoisolative microcontainer with nanoslots defined by nanoimprint lithography. J. Vac. Sci. Technol. B Microelectron. Nanometer Struct. Process Meas. Phenom., 2009, 27(6), 2795-2800.
108. Qi, Z.; Yamamoto, C.; Imori, N.; Kinukawa, A.; Yang, K.; Yanai, G.; Ikenoue, E.; Shen, Y.; Shirouzu, Y.; Hiura, A.; Inoue, K.; Sumi, S. Immunoisolation effect of polyvinyl alcohol (PVA) macroencapsulated islets in type 1 diabetes therapy. Cell Transplant., 2012, 21(2-3), 525-534.
109. Kriz, J.; Vilk, G.; Mazzuca, D. M.; Toleikis, P. M.; Foster, P. J.; White, D. J. G. A novel technique for the transplantation of pancreatic islets within a vascularized device into the greater omentum to achieve insulin independence. Am. J. Surg., 2012, 203(6), 793-797.
110. Yang, K. C.; Wu, C. C.; Lin, S. C.; Sumi, S.; Lin, F. H. The in vivo performance of bioartificial pancreas in bone marrow cavity: A case report of a spontaneous diabetic feline. Biochem. Biophys. Res. Commun., 2010, 393(3), 362-364.
111. Yang, K. C.; Wu, C. C.; Lin, S. C.; Sumi, S.; Lin, F. H. Intramedullary cavity as an implant site for bioartificial pancreas: an in vivo study on diabetic canine. Transplantation, 2010, 90(6), 604-611.
112. Chen, J. P.; Chang, F. N. Preparation and characterization of hydroxyapatite/gelatin composite membranes for immunoisolation. Appl. Surf. Sci., 2012, 261, 176-183.
113. Lin, C. C.; Raza, A.; Shih, H. PEG hydrogels formed by thiol-ene photo-click chemistry and their effect on the formation and recovery of insulin-secreting cell spheroids. Biomaterials, 2011, 32(36), 9685-9695.
114. Krishnan, L.; Clayton, L. R.; Boland, E. D.; Reed, R. M.; Hoying, J. B.; Williams, S. K. Cellular immunoisolation for islet transplanta tion by a novel dual porosity electrospun membrane. Transplant. Proc., 2011, 43(9), 3256-3261.
115. Sernova Corp. http://www. sernova. com/s/Home. asp (Accessed November 11, 2012).
116. Teramura, Y.; Iwata, H. Bioartificial pancreas. Microencapsulation and conformal coating of islet of Langerhans. Adv. Drug Deliv. Rev., 2010, 62(7-8), 827-840.
117. Zhi, Z. L.; Kerby, A.; King, A. J. F.; Jones, P. M.; Pickup, J. C. Nanoscale encapsulation enhances allograft survival and function of islets transplanted in a mouse model of diabetes. Diabetologia, 2012, 55(4), 1081-1090.
118. Bhaiji, T.; Zhi, Z. L.; Pickup, J. C. Improving cellular function and immune protection via layer-by-layer nanocoating of pancreatic islet α-cell spheroids cocultured with mesenchymal stem cells. J. Biomed. Mater. Res. A., 2012, 100(6), 1628-1636.
119. Kizilel, S.; Scavone, A.; Liu, X.; Nothias, J. M.; Ostrega, D.; Witkowski, P.; Millis, M. Encapsulation of pancreatic islets within nano-thin functional polyethylene glycol coatings for enhanced insulin secretion. Tissue Eng. Part A, 2010, 16(7), 2217-2228.
120. Luan, N. M.; Teramura, Y.; Iwata H. Immobilization of the soluble domain of human complement receptor 1 on agarose-encapsulated islets for the prevention of complement activation. Biomaterials, 2010, 31(34), 8847-8853.
121. Kozlovskaya, V.; Zavgorodnya, O.; Chen, Y.; Ellis, K.; Tse, H. M.; Cui, W.; Thompson, J. A.; Kharlampieva, E. Ultrathin polymeric coatings based on hydrogen-bonded polyphenol for protection of pancreatic islet cells. Adv. Funct. Mater., 2012, 22(16), 3389-3398.
122. Lee, D. Y.; Byun, Y. Pancreatic islet PEGylation as an immunological polymeric restraint Biotechnol. Bioprocess Eng., 2010, 15(1), 76-85.
123. Jung, Y. S.; Jeong, J. H.; Yook, S.; Im, B.-H.; Seo, J.; Hong, S. W.; Park, J. B.; Yang, V. C.; Lee, D. Y.; Byun, Y. Surface modification of pancreatic islets using heparin-DOPA conjugate and anti-CD154 mAb for the prolonged survival of intrahepatic transplanted islets in a xenograft model. Biomaterials, 2012, 33(1), 295-303.
124. Jeong, J. H.; Yook, S.; Hwang, J. W.; Jung, M. J.; Moon, H. T.; Lee, D. Y.; Byun, Y. Synergistic effect of surface modification with poly(ethylene glycol) and immunosuppressants on repetitive pancreatic islet transplantation into antecedently sensitized rat. Transplant. Proc., 2013, 45(2), 585-590.
125. Teramura, Y.; Oommen, O. P.; Olerud, J.; Hilborn, J.; Nilsson, B. Microencapsulation of cells, including islets, within stable ultrathin membranes of maleimide-conjugated PEG-lipid with multifunctional crosslinkers. Biomaterials, 2013, 34(11), 2683-2693.
126. deVos, P.; Bucko, M.; Gemeiner, P.; Navratil, M.; Svitel, J.; Faas, M.; Strand, B. L.; Skjåk-Bræk, G.; Mørch, Y. A.; Vikartovska, A.; Lacík, I.; Kollarikova, G.; Orive, G.; Poncelet, D.; Pedraz, J. L.; Ansorge-Schumacher, M. B. Multiscale requirements for bioencapsulation in medicine and biotechnology. Biomaterials, 2009, 30 (13), 2559-2570.
127. Mercadé-Prieto, R.; Zhang, Z. Mechanical characterization of microspheres capsules, cells and beads: A review. J. Microencapsulation, 2012, 29(3), 277-285.
128. Mollnes, T. E.; Brekke, O. L.; Fung, M.; Fure, H.; Christiansen, D.; Bergseth, G.; Videm, V.; Lappegård, K. T.; Köhl, J.; Lambris, J. D. Essential role of the C5a receptor in E coli-induced oxidative burst and phagocytosis revealed by a novel lepirudin-based human whole blood model of inflammation. Blood, 2002, 100(5), 1869-1877.
129. Sokolov, A.; Hellerud, B. C.; Pharo, A.; Johannessen, E. A.; Mollnes T. E. Complement activation by candidate biomaterials of an implantable microfabricated medical device. J. Biomed. Mater. Res. B Appl. Biomater., 2011, 98(2), 323-329.
130. deHaan, B. J.; Rossi, A.; Faas, M. M.; Smelt, M. J.; Sonvico, F.; Colombo, P.; de Vos, P. Structural surface changes and inflammatory responses against alginate-based microcapsules after exposure to human peritoneal fluid. J. Biomed. Mater. Res. A., 2011, 98(3), 394-403.
131. Kitzmann, J. P.; Law, L.; Shome, A.; Muzina, M.; Elliott, R. B.; Mueller, K. R.; Schuurman, H.-J.; Papas, K. K. Real-time assessment of encapsulated neonatal porcine islets prior to clinical xenotransplantation. Xenotransplantation, 2012, 19(6), 333-336.
132. Wang, Y.; Lo, J. F.; Mendoza-Elias, J. E.; Adewola, A. F.; Harvat, T. A.; Kinzer, K. P.; Lee, D.; Qi, M.; Eddington, D. T.; Oberholzer, J. Application of microfluidic technology to pancreatic islet research: first decade of endeavor. Bioanalysis, 2010, 2(10), 1729-1744.
133. Chen, W.; Lisowski, M.; Khalil, G.; Sweet, I. R.; Shen, A. Q. Microencapsulated 3-dimensional sensor for the measurement of oxygen in single isolated pancreatic islets. PLoS ONE, 2012, 7(3), e33070.
134. Wang, Y.; Mendoza-Elias, J. E.; Qi, M.; Harvat, T. A.; Ahn, S. J.; Lee, D.; Gutierrez, D.; Jeon, H.; Paushter, D.; Oberholzer, J. Implication of mitochondrial cytoprotection in human islet isolation and transplantation. Biochem. Res. Int., 2012, 2012, Article ID 395974, 16 pages.
135. Johnson, A. S.; Fisher, R. J.; Weir, G. C.; Colton, C. K. Oxygen consumption and diffusion in assemblages of respiring spheres: Performance enhancement of a bioartificial pancreas. Chem. Eng. Sci., 2009, 64(22), 4470-4487.
136. Cornolti, R.; Figliuzzi, M.; Remuzzi, A. Effect of micro-and macroencapsulation on oxygen consumption by pancreatic islets. Cell Transplant., 2009, 18(2), 195-201.
137. Gallego-Perez, D.; Higuita-Castro, N.; Reen, R. K.; Palacio-Ochoa, M.; Sharma, S.; Lee, L. J.; Lannutti, J. J.; Hansford, D. J.; Gooch, K. J. Micro/nanoscale technologies for the development of hormone-expressing islet-like cell clusters. Biomed. Microdevices, 2012, 14(4), 779-789.
138. Nadithe, V.; Mishra, D.; Bae, Y. H. Poly(ethylene glycol) crosslinked hemoglobin with antioxidant enzymes protects pancreatic islets from hypoxic and free radical stress and extends islet functionality. Biotechnol. Bioeng., 2012, 109(9), 2392-2401.
139. Vaithilingam, V.; Oberholzer, J.; Guillemin, G. J.; Tuch, B. E. Beneficial effects of desferrioxamine on encapsulated human isletsin vitro and in vivo study. Am. J. Transplant., 2012, 10(9), 1961-1969.
140. 2 carrier. Am. J. Transplant., 2006, 6(12), 2861-2870.
141. Dang, T. T.; Xu, Q.; Bratlie, K. M.; O'Sullivan, E. S.; Chen, X. Y.; Langer, R.; Anderson, D. G. Microfabrication of homogenous, asymmetric cell-laden hydrogel capsules. Biomaterials, 2009, 30(36), 6896-6902.
142. Tendulkar, S; Mirmalek-Sani, S.-H.; Childers, C.; Saul, J.; Opara, E. C.; Ramasubramanian, M. K. A three-dimensional microfluidic approach to scaling up microencapsulation of cells. Biomed. Microdevices, 2012, 14(3), 461-469.
143. Wiedemeier, S.; Ehrhart, F.; Mettler, E.; Gastrock, G.; Forst, T.; Weber, M. M.; Zimmermann, H.; Metze, J. Encapsulation of Langerhans' islets: Microtechnological developments for transplantation. Eng. Life Sci., 2011, 11(2), 165-173.
144. The Chicago Diabetes Project. http://www. chicagodiabetesproject. org/(Accessed November 11, 2012).