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Cell Therapy pp 121-138 | Cite as

Encapsulation Approaches to Cell Therapy

  • Paul de VosEmail author
Chapter
Part of the Molecular and Translational Medicine book series (MOLEMED)

Abstract

The principle of immunoisolation of cells is based on envelopment of cells in immunoprotective but semipermeable capsules that protect cells from immune attack by the host. Many different concepts in different geometries have been introduced in the past two decades and are here discussed in view of future application in humans.

Although much progress has been accomplished in producing capsules that elicit not more than minimal immune responses, it has, at the same time, been demonstrated that for longevity of the grafts, the capsules need significant adaptations to facilitate long-term functional survival of the enveloped tissue. Items such as mechanotransduction, an optimal intracapsular environment, as well as prevention of release of danger-associated molecular patterns (DAMPs) require adaptations of the currently applied systems.

It is concluded that although the proof of principle of applicability of encapsulated grafts merits optimism about its clinical potential, current challenges are to innovate on properties of capsules to enhance cell survival.

Keywords

Encapsulation Insulin Alginate Biocompatibility Biotolerability 

Notes

Acknowledgments

PdV is grateful for financial support from the Dutch Diabetes Foundation and Juvenile Diabetes Research Foundation.

References

  1. 1.
    Ascha MS, Ascha ML, Hanouneh IA. Management of immunosuppressant agents following liver transplantation: less is more. World J Hepatol. 2016;8(3):148–61. doi: 10.4254/wjh.v8.i3.148.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Bamoulid J, Staeck O, Halleck F, Khadzhynov D, Brakemeier S, Durr M, Budde K. The need for minimization strategies: current problems of immunosuppression. Transpl Int. 2015;28(8):891–900. doi: 10.1111/tri.12553.PubMedCrossRefGoogle Scholar
  3. 3.
    Park CG, Bottino R, Hawthorne WJ. Current status of islet xenotransplantation. Int J Surg. 2015;23(Pt B):261–6. doi: 10.1016/j.ijsu.2015.07.703.PubMedCrossRefGoogle Scholar
  4. 4.
    Bottino R, Trucco M. Use of genetically-engineered pig donors in islet transplantation. World J Transpl. 2015;5(4):243–50. doi: 10.5500/wjt.v5.i4.243.CrossRefGoogle Scholar
  5. 5.
    Cooper DK, Ekser B, Ramsoondar J, Phelps C, Ayares D. The role of genetically engineered pigs in xenotransplantation research. J Pathol. 2016;238(2):288–99. doi: 10.1002/path.4635.PubMedCrossRefGoogle Scholar
  6. 6.
    Johnson JD. A practical guide to genetic engineering of pancreatic beta-cells in vivo: getting a grip on RIP and MIP. Islets. 2014;6(3):e944439. doi: 10.4161/19382014.2014.944439.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Barkai U, Rotem A, de Vos P. Survival of encapsulated islets: more than a membrane story. World J Transpl. 2016;6(1):69–90. doi: 10.5500/wjt.v6.i1.69.CrossRefGoogle Scholar
  8. 8.
    Hashemi M, Kalalinia F. Application of encapsulation technology in stem cell therapy. Life Sci. 2015;143:139–46. doi: 10.1016/j.lfs.2015.11.007.PubMedCrossRefGoogle Scholar
  9. 9.
    Krishnan R, Ko D, Foster CE 3rd, Liu W, Smink AM, de Haan B, De Vos P, Lakey JR. Immunological challenges facing translation of alginate encapsulated porcine islet xenotransplantation to human clinical trials. Methods Mol Biol. 2017;1479:305–33. doi: 10.1007/978.1.4939.6364.5.24.PubMedCrossRefGoogle Scholar
  10. 10.
    Orive G, Santos E, Poncelet D, Hernandez RM, Pedraz JL, Wahlberg LU, De Vos P, Emerich D. Cell encapsulation: technical and clinical advances. Trends Pharmacol Sci. 2015;36(8):537–46. doi: 10.1016/j.tips.2015.05.003.PubMedCrossRefGoogle Scholar
  11. 11.
    Tomei AA, Villa C, Ricordi C. Development of an encapsulated stem cell-based therapy for diabetes. Expert Opin Biol Ther. 2015;15(9):1321–36. doi: 10.1517/14712598.2015.1055242.PubMedCrossRefGoogle Scholar
  12. 12.
    Bisceglie VV. Uber die antineoplastische Immunitat. Krebsforsch. 1933;40:141–58.CrossRefGoogle Scholar
  13. 13.
    Algire GH, Weaver JM, Prehn RT. Growth of cells in vivo in diffusion chambers. I survival of homografts in mice. J Natl Cancer Inst. 1954;15:493–507.PubMedGoogle Scholar
  14. 14.
    Vaithilingam V, Tuch BE. Islet transplantation and encapsulation: an update on recent developments. Rev Diabet Stud. 2011;8(1):51–67.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    de Vos P, Lazarjani HA, Poncelet D, Faas MM. Polymers in cell encapsulation from an enveloped cell perspective. Adv Drug Deliv Rev. 2014;67-68:15–34. doi: 10.1016/j.addr.2013.11.005.PubMedCrossRefGoogle Scholar
  16. 16.
    Liu HW, Ofosu FA, Chang PL. Expression of human factor IX by microencapsulated recombinant fibroblasts. Hum Gene Ther. 1993;4:291–301.PubMedCrossRefGoogle Scholar
  17. 17.
    Koo J, Chang TSM. Secretion of erythropoietin from microencapsulated rat kidney cells. Int J Artif Organs. 1993;16:557–60.PubMedGoogle Scholar
  18. 18.
    Chang PL, Shen N, Westcott AJ. Delivery of recombinant gene products with microencapsulated cells in vivo. Hum Gene Ther. 1993;4:433–40.PubMedCrossRefGoogle Scholar
  19. 19.
    Cieslinski DA, David Humes H. Tissue engineering of a bioartificial kidney. Biotechnol Bioeng. 1994;43(7):678–81. doi: 10.1002/bit.260430718.PubMedCrossRefGoogle Scholar
  20. 20.
    Uludag H, Sefton MV. Microencapsulated human hepatoma (HepG2) cells: in vitro growth and protein release. J Biomed Mater Res. 1993;27(10):1213–24.PubMedCrossRefGoogle Scholar
  21. 21.
    Colton CK. Implantable biohybrid artificial organs. Cell Transplant. 1995;4:415–36.PubMedCrossRefGoogle Scholar
  22. 22.
    Aebischer P, Goddard M, Signore AP, Timpson RL. Functional recovery in hemiparkinsonian primates transplanted with polymer-encapsulated PC12 cells. Exp Neurol. 1994;126:151–8.PubMedCrossRefGoogle Scholar
  23. 23.
    Lim F, Sun AM. Microencapsulated islets as bioartificial endocrine pancreas. Science. 1980;210:908–10.PubMedCrossRefGoogle Scholar
  24. 24.
    Opara EC, Kendall WF Jr. Immunoisolation techniques for islet cell transplantation. Expert Opin Biol Ther. 2002;2(5):503–11.PubMedCrossRefGoogle Scholar
  25. 25.
    Uludag H, De Vos P, Tresco PA. Technology of mammalian cell encapsulation. Adv Drug Deliv Rev. 2000;42(1-2):29–64.PubMedCrossRefGoogle Scholar
  26. 26.
    De Vos P, Marchetti P. Encapsulation of pancreatic islets for transplantation in diabetes: the untouchable islets. Trends Mol Med. 2002;8(8):363–6.PubMedCrossRefGoogle Scholar
  27. 27.
    Wilson JT, Chaikof EL. Challenges and emerging technologies in the immunoisolation of cells and tissues. Adv Drug Deliv Rev. 2008;60(2):124–45. doi: 10.1016/j.addr.2007.08.034.PubMedCrossRefGoogle Scholar
  28. 28.
    Aebischer P, Pochon NAM, Heyd B, DÇglon N, Joseph JM, Zurn AD, Baetge EE, Hammang JP, Goddard M, Lysaght M, Kaplan F, Kato AC, Schluep M, Hirt L, Regli F, Porchet F, De Tribolet N. Gene therapy for amyotrophic lateral sclerosis (ALS) using a polymer encapsulated xenogenic cell line engineered to secrete hCNTF. Hum Gene Ther. 1996;7:851–60.PubMedCrossRefGoogle Scholar
  29. 29.
    Haisch A, Groger A, Radke C, Ebmeyer J, Sudhoff H, Grasnick G, Jahnke V, Burmester GR, Sittinger M. Macroencapsulation of human cartilage implants: pilot study with polyelectrolyte complex membrane encapsulation. Biomaterials. 2000;21(15):1561–6.PubMedCrossRefGoogle Scholar
  30. 30.
    Risbud MV, Bhargava S, Bhonde RR. In vivo biocompatibility evaluation of cellulose macrocapsules for islet immunoisolation: implications of low molecular weight cut-off. J Biomed Mater Res A. 2003;66(1):86–92. doi: 10.1002/jbm.a.10522.PubMedCrossRefGoogle Scholar
  31. 31.
    Prochorov AV, Tretjak SI, Goranov VA, Glinnik AA, Goltsev MV. Treatment of insulin dependent diabetes mellitus with intravascular transplantation of pancreatic islet cells without immunosuppressive therapy. Adv Med Sci. 2008;53(2):240–4.PubMedCrossRefGoogle Scholar
  32. 32.
    McQuilling JP, Arenas-Herrera J, Childers C, Pareta RA, Khanna O, Jiang B, Brey EM, Farney AC, Opara EC. New alginate microcapsule system for angiogenic protein delivery and immunoisolation of islets for transplantation in the rat omentum pouch. Transplant Proc. 2011;43(9):3262–4. doi: 10.1016/j.transproceed.2011.10.030.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Opara EC, McQuilling JP, Farney AC. Microencapsulation of pancreatic islets for use in a bioartificial pancreas. Methods Mol Biol. 2013;1001:261–6. doi: 10.1007/978.1.62703.363.3.21.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Pareta R, McQuilling JP, Sittadjody S, Jenkins R, Bowden S, Orlando G, Farney AC, Brey EM, Opara EC. Long-term function of islets encapsulated in a redesigned alginate microcapsule construct in omentum pouches of immune-competent diabetic rats. Pancreas. 2014;43(4):605–13. doi: 10.1097/mpa.0000000000000107.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Bilensoy E, Hincal AA. Recent advances and future directions in amphiphilic cyclodextrin nanoparticles. Expert Opin Drug Deliv. 2009;6(11):1161–73.PubMedCrossRefGoogle Scholar
  36. 36.
    Cheung CY, Anseth KS (2009) Immunoisolative encapsulation system. CO, US Patent US 20090028945.Google Scholar
  37. 37.
    Cornolti R, Figliuzzi M, Remuzzi A. Effect of micro- and macroencapsulation on oxygen consumption by pancreatic islets. Cell Transplant. 2009;18(2):195–201.PubMedCrossRefGoogle Scholar
  38. 38.
    Pattani A, Patravale VB, Panicker L, Potdar PD. Immunological effects and membrane interactions of chitosan nanoparticles. Mol Pharm. 2009;6(2):345–52.PubMedCrossRefGoogle Scholar
  39. 39.
    Tam SK, Dusseault J, Bilodeau S, Langlois G, Halle JP, Yahia L. Factors influencing alginate gel biocompatibility. J Biomed Mater Res A. 2011;98(1):40–52.PubMedCrossRefGoogle Scholar
  40. 40.
    Avgoustiniatos ES, Colton CK. Effect of external oxygen mass transfer resistances on viability of immunoisolated tissue. Ann N Y Acad Sci. 1997;31(831):145–67.Google Scholar
  41. 41.
    Dionne KE, Colton CK, Yarmush ML. Effect of hypoxia on insulin secretion by isolated rat and canine islets of Langerhans. Diabetes. 1993;42(1):12–21.PubMedCrossRefGoogle Scholar
  42. 42.
    Ludwig B, Rotem A, Schmid J, Weir GC, Colton CK, Brendel MD, Neufeld T, Block NL, 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 AV, Bornstein SR, 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):5022–7. doi: 10.1073/pnas.1201868109.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Gandhi JK, Opara EC, Brey EM. Alginate-based strategies for therapeutic vascularization. Ther Deliv. 2013;4(3):327–41. doi: 10.4155/tde.12.163.PubMedCrossRefGoogle Scholar
  44. 44.
    Khanna O, Moya ML, Greisler HP, Opara EC, Brey EM. Multilayered microcapsules for the sustained-release of angiogenic proteins from encapsulated cells. Am J Surg. 2010;200(5):655–8. doi: 10.1016/j.amjsurg.2010.08.001.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Khanna O, Moya ML, Opara EC, Brey EM. Synthesis of multilayered alginate microcapsules for the sustained release of fibroblast growth factor-1. J Biomed Mater Res A. 2010;95(2):632–40. doi: 10.1002/jbm.a.32883.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Sakai S, Ono T, Ijima H, Kawakami K. Control of molecular weight cut-off for immunoisolation by multilayering glycol chitosan-alginate polyion complex on alginate-based microcapsules. J Microencapsul. 2000;17(6):691–9.PubMedCrossRefGoogle Scholar
  47. 47.
    Chia SM, Wan AC, Quek CH, Mao HQ, Xu X, Shen L, Ng ML, Leong KW, Yu H. Multi-layered microcapsules for cell encapsulation. Biomaterials. 2002;23(3):849–56.PubMedCrossRefGoogle Scholar
  48. 48.
    Khattak SF, Chin KS, Bhatia SR, Roberts SC. Enhancing oxygen tension and cellular function in alginate cell encapsulation devices through the use of perfluorocarbons. Biotechnol Bioeng. 2007;96(1):156–66. doi: 10.1002/bit.21151.PubMedCrossRefGoogle Scholar
  49. 49.
    Barkai U, Weir GC, Colton CK, Ludwig B, Bornstein SR, Brendel MD, Neufeld T, Bremer C, Leon A, Evron Y, Yavriyants K, Azarov D, Zimermann B, Maimon S, Shabtay N, Balyura M, Rozenshtein T, Vardi P, Bloch K, de Vos P, Rotem A. Enhanced oxygen supply improves islet viability in a new bioartificial pancreas. Cell Transplant. 2013;22(8):1463–76. doi: 10.3727/096368912x657341.PubMedCrossRefGoogle Scholar
  50. 50.
    Evron Y, Zimermann B, Ludwig B, Barkai U, Colton CK, Weir GC, Arieli B, Maimon S, Shalev N, Yavriyants K, Goldman T, Gendler Z, Eizen L, Vardi P, Bloch K, Barthel A, Bornstein SR, Rotem A. Oxygen supply by photosynthesis to an implantable islet cell device. Horm Metab Res. 2015;47(1):24–30. doi: 10.1055/s-0034-1394375.PubMedGoogle Scholar
  51. 51.
    Neufeld T, Ludwig B, Barkai U, Weir GC, Colton CK, Evron Y, Balyura M, Yavriyants K, Zimermann B, Azarov D, Maimon S, Shabtay N, Rozenshtein T, Lorber D, Steffen A, Willenz U, Bloch K, Vardi P, Taube R, de Vos P, Lewis EC, Bornstein SR, Rotem A. The efficacy of an immunoisolating membrane system for islet xenotransplantation in minipigs. PLoS One. 2013;8(8):e70150. doi: 10.1371/journal.pone.0070150.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Rokstad AM, Lacik I, de Vos P, Strand BL. Advances in biocompatibility and physico-chemical characterization of microspheres for cell encapsulation. Adv Drug Deliv Rev. 2014;67-68:111–30. doi: 10.1016/j.addr.2013.07.010.PubMedCrossRefGoogle Scholar
  53. 53.
    Paredes-Juarez GA, de Haan BJ, Faas MM, de Vos P. The role of pathogen-associated molecular patterns in inflammatory responses against alginate based microcapsules. J Control Release. 2013;172(3):983–92. doi: 10.1016/j.jconrel.2013.09.009.PubMedCrossRefGoogle Scholar
  54. 54.
    Williams DF. On the mechanisms of biocompatibility. Biomaterials. 2008;29(20):2941–53. doi: 10.1016/j.biomaterials.2008.04.023.PubMedCrossRefGoogle Scholar
  55. 55.
    Paredes-Juarez GA, Sahasrabudhe NM, Tjoelker RS, de Haan BJ, Faas MM, de Vos P. Danger-associated molecular patterns production by human pancreatic islets under low oxygen and nutrient conditions in the presence and absence of an immunoisolating capsule and necrostatin-1. Sci Rep. 2015;5:14623.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Paredes Juarez GA, Spasojevic M, Faas MM, de Vos P. Immunological and technical considerations in application of alginate-based microencapsulation systems. Front Bioeng Biotechnol. 2014;2:26. doi: 10.3389/fbioe.2014.00026.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    Orive G, Emerich D, De Vos P. Encapsulate this: the do’s and dont’s. Nat Med. 2014;20(3):233. doi: 10.1038/nm.3486.PubMedCrossRefGoogle Scholar
  58. 58.
    Paredes-Juarez GA, Sahasrabudhe NM, Tjoelker RS, de Haan BJ, Engelse MA, de Koning EJ, Faas MM, de Vos P. DAMP production by human islets under low oxygen and nutrients in the presence or absence of an immunoisolating-capsule and necrostatin-1. Sci Rep. 2015;5:14623. doi: 10.1038/srep14623.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Smink AM, de Haan BJ, Paredes-Juarez GA, Wolters AH, Kuipers J, Giepmans BN, Schwab L, Engelse MA, van Apeldoorn AA, de Koning E, Faas MM, de Vos P. Selection of polymers for application in scaffolds applicable for human pancreatic islet transplantation. Biomed Mater. 2016;11(3):035006. doi: 10.1088/1748-6041/11/3/035006.PubMedCrossRefGoogle Scholar
  60. 60.
    de Vos P, Smink AM, Paredes G, Lakey JR, Kuipers J, Giepmans BN, de Haan BJ, Faas MM. Enzymes for pancreatic islet isolation impact chemokine-production and polarization of insulin-producing beta-cells with reduced functional survival of immunoisolated rat islet-allografts as a consequence. PLoS One. 2016;11(1):e0147992. doi: 10.1371/journal.pone.0147992.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Dempsey A, Bowie AG. Innate immune recognition of DNA: a recent history. Virology. 2015;479-480:146–52. doi: 10.1016/j.virol.2015.03.013.PubMedCrossRefGoogle Scholar
  62. 62.
    Freitag J, Castro CN, Berod L, Lochner M, Sparwasser T. Microbe-associated immunomodulatory metabolites: influence on T cell fate and function. Mol Immunol. 2015;68:575–84. doi: 10.1016/j.molimm.2015.07.025.PubMedCrossRefGoogle Scholar
  63. 63.
    Iwasaki A, Medzhitov R. Control of adaptive immunity by the innate immune system. Nat Immunol. 2015;16(4):343–53. doi: 10.1038/ni.3123.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Jaeger M, Stappers MH, Joosten LA, Gyssens IC, Netea MG. Genetic variation in pattern recognition receptors: functional consequences and susceptibility to infectious disease. Future Microbiol. 2015;10(6):989–1008. doi: 10.2217/fmb.15.37.PubMedCrossRefGoogle Scholar
  65. 65.
    Sellge G, Kufer TA. PRR-signaling pathways: learning from microbial tactics. Semin Immunol. 2015;27(2):75–84. doi: 10.1016/j.smim.2015.03.009.PubMedCrossRefGoogle Scholar
  66. 66.
    Hilborn J, Bjursten LM. A new and evolving paradigm for biocompatibility. J Tissue Eng Regen Med. 2007;1(2):110–9. doi: 10.1002/term.4.PubMedCrossRefGoogle Scholar
  67. 67.
    Bhujbal SV, de Haan B, Niclou SP, de Vos P. A novel multilayer immunoisolating encapsulation system overcoming protrusion of cells. Sci Rep. 2014;4:6856. doi: 10.1038/srep06856.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Bhujbal SV, Paredes-Juarez GA, Niclou SP, de Vos P. Factors influencing the mechanical stability of alginate beads applicable for immunoisolation of mammalian cells. J Mech Behav Biomed Mater. 2014;37:196–208. doi: 10.1016/j.jmbbm.2014.05.020.PubMedCrossRefGoogle Scholar
  69. 69.
    Tam SK, Bilodeau S, Dusseault J, Langlois G, Halle JP, Yahia LH. Biocompatibility and physicochemical characteristics of alginate-polycation microcapsules. Acta Biomater. 2011;7(4):1683–92. doi: 10.1016/j.actbio.2010.12.006.PubMedCrossRefGoogle Scholar
  70. 70.
    Bunger CM, Gerlach C, Freier T, Schmitz KP, Pilz M, Werner C, Jonas L, Schareck W, Hopt UT, De Vos P. Biocompatibility and surface structure of chemically modified immunoisolating alginate-PLL capsules. J Biomed Mater Res. 2003;67A(4):1219–27.CrossRefGoogle Scholar
  71. 71.
    Van Hoogmoed CG, Busscher HJ, De Vos P. Fourier transform infrared spectroscopy studies of alginate-PLL capsules with varying compositions. J Biomed Mater Res. 2003;67A(1):172–8.CrossRefGoogle Scholar
  72. 72.
    Tam KT, Dusseault J, Polizu S, MÇnard M, HallÇ JP, L'Hocine Y. Physicochemical model of alginate-poly-l-lysine microcapsules defined at the micrometric/nanometric scale using ATR-FTIR, XPS, and ToF-SIMS. Biomaterials. 2005;34:6950–61.CrossRefGoogle Scholar
  73. 73.
    De Vos P, De Haan BJ, Kamps JA, Faas MM, Kitano T. Zeta-potentials of alginate-PLL capsules: a predictive measure for biocompatibility? J Biomed Mater Res A. 2007;80(4):813–9.PubMedCrossRefGoogle Scholar
  74. 74.
    De Vos P, Van Hoogmoed CG, van Zanten J, Netter S, Strubbe JH, Busscher HJ. Long-term biocompatibility, chemistry, and function of microencapsulated pancreatic islets. Biomaterials. 2003;24(2):305–12.PubMedCrossRefGoogle Scholar
  75. 75.
    Ponce S, Orive G, Hernandez R, Gascon AR, Pedraz JL, De Haan BJ, Faas MM, Mathieu HJ, De Vos P. Chemistry and the biological response against immunoisolating alginate-polycation capsules of different composition. Biomaterials. 2006;27(28):4831–9.PubMedCrossRefGoogle Scholar
  76. 76.
    Poncelet D, de Vos P, Suter N, Jayasinghe SN. Bio-electrospraying and cell electrospinning: progress and opportunities for basic biology and clinical sciences. Adv Healthc Mater. 2012;1(1):27–34. doi: 10.1002/adhm.201100001.PubMedCrossRefGoogle Scholar
  77. 77.
    De Vos P, De Haan BJ, Van Schilfgaarde R. Upscaling the production of encapsulated islets. Biomaterials. 1997;18:1085–90.PubMedCrossRefGoogle Scholar
  78. 78.
    Zimmermann U, Thurmer F, Jork A, Weber M, Mimietz S, Hillgartner M, Brunnenmeier F, Zimmermann H, Westphal I, Fuhr G, Noth U, Haase A, Steinert A, Hendrich C. A novel class of amitogenic alginate microcapsules for long-term immunoisolated transplantation. Ann N Y Acad Sci. 2001;944:199–215.PubMedCrossRefGoogle Scholar
  79. 79.
    Hasse C, Zielke A, Klock G, Schlosser A, Barth P, Zimmermann U, Sitter H, Lorenz W, Rothmund M. Amitogenic alginates: key to first clinical application of microencapsulation technology. World J Surg. 1998;22:659–65.PubMedCrossRefGoogle Scholar
  80. 80.
    De Vos P, Vegter D, Strubbe JH, De Haan BJ, Van Schilfgaarde R. Impaired glucose tolerance in recipients of an intraperitoneally implanted microencapsulated islet allograft is caused by the slow diffusion of insulin through the peritoneal membrane. Transplant Proc. 1997;29:756–7.PubMedCrossRefGoogle Scholar
  81. 81.
    Klôck G, Pfeffermann A, Ryser C, Grîhn P, Kuttler B, Hahn HJ, Zimmermann U. Biocompatibility of mannuronic acid-rich alginates. Biomaterials. 1997;18:707–13.PubMedCrossRefGoogle Scholar
  82. 82.
    De Vos P, Van Hoogmoed CG, Busscher HJ. Chemistry and biocompatibility of alginate-PLL capsules for immunoprotection of mammalian cells. J Biomed Mater Res. 2002;60:252–9.PubMedCrossRefGoogle Scholar
  83. 83.
    Paredes Juarez GA, De Haan BJ, Faas MM, De Vos P. A technology platform to test the efficacy of purification of alginate. Materials. 2014;7:2087–103. doi: 10.3390/ma7032087.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Tang D, Kang R, Coyne CB, Zeh HJ, Lotze MT. PAMPs and DAMPs: signal 0s that spur autophagy and immunity. Immunol Rev. 2012;249(1):158–75. doi: 10.1111/j.1600-065X.2012.01146.x.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Kawai T, Akira S. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol. 2010;11(5):373–84. doi: 10.1038/ni.1863.PubMedCrossRefGoogle Scholar
  86. 86.
    Bauer S, Muller T, Hamm S. Pattern recognition by Toll-like receptors. Adv Exp Med Biol. 2009;653:15–34.PubMedCrossRefGoogle Scholar
  87. 87.
    Zeuthen LH, Fink LN, Frokiaer H. Toll-like receptor 2 and nucleotide-binding oligomerization domain-2 play divergent roles in the recognition of gut-derived lactobacilli and bifidobacteria in dendritic cells. Immunology. 2008;124(4):489–502. doi: 10.1111/j.1365-2567.2007.02800.x.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    de Vos P, Bucko M, Gemeiner P, Navratil M, Svitel J, Faas M, Strand BL, Skjak-Braek G, Morch YA, Vikartovska A, Lacik I, Kollarikova G, Orive G, Poncelet D, Pedraz JL, Ansorge-Schumacher MB. Multiscale requirements for bioencapsulation in medicine and biotechnology. Biomaterials. 2009;30(13):2559–70. doi: 10.1016/j.biomaterials.2009.01.014.PubMedCrossRefGoogle Scholar
  89. 89.
    Mahou R, Tran NM, Dufresne M, Legallais C, Wandrey C. Encapsulation of hHuh-7 cells within alginate-poly(ethylene glycol) hybrid microspheres. J Mater Sci Mater Med. 2012;23(1):171–9. doi: 10.1007/s10856-011-4512-3.PubMedCrossRefGoogle Scholar
  90. 90.
    Yang D, Guo S, Qiao J, Nie J. Investigation on the preparation and application of chitosan/alginate microcapsules. J Control Release. 2011;152(Suppl 1):e71–2. doi: 10.1016/j.jconrel.2011.08.130.PubMedCrossRefGoogle Scholar
  91. 91.
    Rokstad AM, Brekke OL, Steinkjer B, Ryan L, Kollarikova G, Strand BL, Skjak-Braek G, Lacik I, Espevik T, Mollnes TE. Alginate microbeads are complement compatible, in contrast to polycation containing microcapsules, as revealed in a human whole blood model. Acta Biomater. 2011;7(6):2566–78. doi: 10.1016/j.actbio.2011.03.011.PubMedCrossRefGoogle Scholar
  92. 92.
    Mazzitelli S, Luca G, Mancuso F, Calvitti M, Calafiore R, Nastruzzi C, Johnson S, Badylak SF. Production and characterization of engineered alginate-based microparticles containing ECM powder for cell/tissue engineering applications. Acta Biomater. 2011;7(3):1050–62. doi: 10.1016/j.actbio.2010.10.005.PubMedCrossRefGoogle Scholar
  93. 93.
    Gardner CM, Burke NA, Chu T, Shen F, Potter MA, Stover HD. Poly(methyl vinyl ether-alt-maleic acid) polymers for cell encapsulation. J Biomater Sci Polym Ed. 2011;22(16):2127–45. doi: 10.1163/092050610x535149.PubMedCrossRefGoogle Scholar
  94. 94.
    de Haan BJ, Rossi A, Faas MM, Smelt MJ, 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.PubMedCrossRefGoogle Scholar
  95. 95.
    Santos E, Zarate J, Orive G, Hernandez RM, Pedraz JL. Biomaterials in cell microencapsulation. Adv Exp Med Biol. 2010;670:5–21.PubMedCrossRefGoogle Scholar
  96. 96.
    Tam SK, de Haan BJ, Faas MM, Halle JP, Yahia L, de Vos P. Adsorption of human immunoglobulin to implantable alginate-poly-L-lysine microcapsules: effect of microcapsule composition. J Biomed Mater Res A. 2009;89(3):609–15. doi: 10.1002/jbm.a.32002.PubMedCrossRefGoogle Scholar
  97. 97.
    Gattas-Asfura KM, Stabler CL. Chemoselective cross-linking and functionalization of alginate via Staudinger ligation. Biomacromolecules. 2009;10(11):3122–9. doi: 10.1021/bm900789a.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    De Castro M, Orive G, Hernandez RM, Bartkowiak A, Brylak W, Pedraz JL. Biocompatibility and in vivo evaluation of oligochitosans as cationic modifiers of alginate/Ca microcapsules. J Biomed Mater Res A. 2009;91(4):1119–30. doi: 10.1002/jbm.a.32270.PubMedCrossRefGoogle Scholar
  99. 99.
    Qi M, Strand BL, Morch Y, Lacik I, Wang Y, Salehi P, Barbaro B, Gangemi A, Kuechle J, Romagnoli T, Hansen MA, Rodriguez LA, Benedetti E, Hunkeler D, Skjak-Braek G, Oberholzer J. Encapsulation of human islets in novel inhomogeneous alginate-ca2+/ba2+ microbeads: in vitro and in vivo function. Artif Cells Blood Substit Immobil Biotechnol. 2008;36(5):403–20. doi: 10.1080/10731190802369755.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Marsich E, Borgogna M, Donati I, Mozetic P, Strand BL, Salvador SG, Vittur F, Paoletti S. Alginate/lactose-modified chitosan hydrogels: a bioactive biomaterial for chondrocyte encapsulation. J Biomed Mater Res A. 2008;84(2):364–76.PubMedCrossRefGoogle Scholar
  101. 101.
    Thanos CG, Calafiore R, Basta G, Bintz BE, Bell WJ, Hudak J, Vasconcellos A, Schneider P, Skinner SJ, Geaney M, Tan P, Elliot RB, Tatnell M, Escobar L, Qian H, Mathiowitz E, Emerich DF. Formulating the alginate-polyornithine biocapsule for prolonged stability: evaluation of composition and manufacturing technique. J Biomed Mater Res A. 2007;83(1):216–24.PubMedCrossRefGoogle Scholar
  102. 102.
    Baruch L, Machluf M. Alginate-chitosan complex coacervation for cell encapsulation: effect on mechanical properties and on long-term viability. Biopolymers. 2006;82(6):570–9. doi: 10.1002/bip.20509.PubMedCrossRefGoogle Scholar
  103. 103.
    Shen F, Li AA, Cornelius RM, Cirone P, Childs RF, Brash JL, Chang PL. Biological properties of photocrosslinked alginate microcapsules. J Biomed Mater Res. 2005;75B(2):425–34.CrossRefGoogle Scholar
  104. 104.
    Orive G, Carcaboso AM, Hernandez RM, Gascon AR, Pedraz JL. Biocompatibility evaluation of different alginates and alginate-based microcapsules. Biomacromolecules. 2005;6(2):927–31.PubMedCrossRefGoogle Scholar
  105. 105.
    Orive G, Bartkowiak A, Lisiecki S, De CM, Hernandez RM, Gascon AR, Pedraz JL. Biocompatible oligochitosans as cationic modifiers of alginate/Ca microcapsules. J Biomed Mater Res B Appl Biomater. 2005;74(1):429–39.PubMedCrossRefGoogle Scholar
  106. 106.
    Bernards M, He Y. Polyampholyte polymers as a versatile zwitterionic biomaterial platform. J Biomater Sci Polym Ed. 2014;25(14-15):1479–88. doi: 10.1080/09205063.2014.938976.PubMedCrossRefGoogle Scholar
  107. 107.
    Jiang H, Xu FJ. Biomolecule-functionalized polymer brushes. Chem Soc Rev. 2013;42(8):3394–426. doi: 10.1039/c2cs35453e.PubMedCrossRefGoogle Scholar
  108. 108.
    Liao J, Wang C, Wang Y, Luo F, Qian Z. Recent advances in formation, properties, and applications of polymersomes. Curr Pharm Des. 2012;18(23):3432–41.PubMedCrossRefGoogle Scholar
  109. 109.
    Moroni L, Klein Gunnewiek M, Benetti EM. Polymer brush coatings regulating cell behavior: passive interfaces turn into active. Acta Biomater. 2014;10(6):2367–78. doi: 10.1016/j.actbio.2014.02.048.PubMedCrossRefGoogle Scholar
  110. 110.
    Spasojevic M, Bhujbal S, Paredes G, de Haan BJ, Schouten AJ, de Vos P. Considerations in binding diblock copolymers on hydrophilic alginate beads for providing an immunoprotective membrane. J Biomed Mater Res A. 2013;102(6):1887–96. doi: 10.1002/jbm.a.34863.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Spasojevic M, Paredes-Juarez GA, Vorenkamp J, de Haan BJ, Schouten AJ, de Vos P. Reduction of the inflammatory responses against alginate-poly-L-lysine microcapsules by anti-biofouling surfaces of PEG-b-PLL diblock copolymers. PLoS One. 2014;9(10):e109837. doi: 10.1371/journal.pone.0109837.PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Spasojevic M, Vorenkamp J, Jansen M, de Vos P, Schouten AJ. Synthesis and phase behavior of poly(N-isopropylacrylamide)-b-poly(L-lysine hydrochloride) and poly(N-isopropylacrylamide-co-acrylamide)-b-poly(L-lysine hydrochloride). Materials. 2014;7(7):5305–26. doi: 10.3390/ma7075305.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Gasparski AN, Beningo KA. Mechanoreception at the cell membrane: more than the integrins. Arch Biochem Biophys. 2015;586:20–6. doi: 10.1016/j.abb.2015.07.017.PubMedCrossRefGoogle Scholar
  114. 114.
    Ivanovska IL, Shin JW, Swift J, Discher DE. Stem cell mechanobiology: diverse lessons from bone marrow. Trends Cell Biol. 2015;25(9):523–32. doi: 10.1016/j.tcb.2015.04.003.PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Jansen KA, Donato DM, Balcioglu HE, Schmidt T, Danen EH, Koenderink GH. A guide to mechanobiology: where biology and physics meet. Biochim Biophys Acta. 2015;1853:3043–52. doi: 10.1016/j.bbamcr.2015.05.007.PubMedCrossRefGoogle Scholar
  116. 116.
    Schaefer A, Hordijk PL. Cell-stiffness-induced mechanosignaling—a key driver of leukocyte transendothelial migration. J Cell Sci. 2015;128(13):2221–30. doi: 10.1242/jcs.163055.PubMedCrossRefGoogle Scholar
  117. 117.
    Tsimbouri PM. Adult stem cell responses to nanostimuli. J Funct Biomater. 2015;6(3):598–622. doi: 10.3390/jfb6030598.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Walsh CM, Bautista DM, Lumpkin EA. Mammalian touch catches up. Curr Opin Neurobiol. 2015;34:133–9. doi: 10.1016/j.conb.2015.05.003.PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Bi Y, Hubbard C, Purushotham P, Zimmer J. Insights into the structure and function of membrane-integrated processive glycosyltransferases. Curr Opin Struct Biol. 2015;34:78–86. doi: 10.1016/j.sbi.2015.07.008.PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Iozzo RV, Schaefer L. Proteoglycan form and function: a comprehensive nomenclature of proteoglycans. Matrix Biol. 2015;42:11–55. doi: 10.1016/j.matbio.2015.02.003.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Kuehn C, Vermette P, Fulop T. Cross talk between the extracellular matrix and the immune system in the context of endocrine pancreatic islet transplantation. A review article. Pathol Biol. 2014;62(2):67–78. doi: 10.1016/j.patbio.2014.01.001.PubMedCrossRefGoogle Scholar
  122. 122.
    Teschler JK, Zamorano-Sanchez D, Utada AS, Warner CJ, Wong GC, Linington RG, Yildiz FH. Living in the matrix: assembly and control of Vibrio cholerae biofilms. Nat Rev Microbiol. 2015;13(5):255–68. doi: 10.1038/nrmicro3433.PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Dufrane D, Steenberghe M, Goebbels RM, Saliez A, Guiot Y, Gianello P. The influence of implantation site on the biocompatibility and survival of alginate encapsulated pig islets in rats. Biomaterials. 2006;27(17):3201–8.PubMedCrossRefGoogle Scholar
  124. 124.
    Dufrane D, Goebbels RM, Saliez A, Guiot Y, Gianello P. Six-month survival of microencapsulated pig islets and alginate biocompatibility in primates: proof of concept. Transplantation. 2006;81(9):1345–53.PubMedCrossRefGoogle Scholar
  125. 125.
    Llacua A, de Haan BJ, Smink SA, de Vos P. Extracellular matrix components supporting human islet function in alginate-based immunoprotective microcapsules for treatment of diabetes. J Biomed Mater Res A. 2016;104(7):1788–96. doi: 10.1002/jbm.a.35706.PubMedCrossRefGoogle Scholar
  126. 126.
    Del-Guerra S, Bracci C, Nilsson K, Belcourt A, Kessler L, Lupi R, Marselli L, De Vos P, Marchetti P. Entrapment of dispersed pancreatic islet cells in CultiSpher-S macroporous gelatin microcarriers: preparation, in vitro characterization, and microencapsulation. Biotechnol Bioeng. 2001;75(6):741–4.PubMedCrossRefGoogle Scholar
  127. 127.
    Ludwig B, Reichel A, Steffen A, Zimerman B, Schally AV, Block NL, Colton CK, Ludwig S, Kersting S, Bonifacio E, Solimena M, Gendler Z, Rotem A, Barkai U, Bornstein SR. Transplantation of human islets without immunosuppression. Proc Natl Acad Sci U S A. 2013;110(47):19054–8. doi: 10.1073/pnas.1317561110.PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Basta G, Montanucci P, Luca G, Boselli C, Noya G, Barbaro B, Qi M, Kinzer KP, Oberholzer J, Calafiore R. Long-term metabolic and immunological follow-up of nonimmunosuppressed patients with type 1 diabetes treated with microencapsulated islet allografts: four cases. Diabetes Care. 2011;34(11):2406–9. doi: 10.2337/dc11-0731.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Pathology and Medical Biology, Section of ImmunoendocrinologyUniversity of GroningenGroningenThe Netherlands

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