Recent Advances in the Use of Encapsulated Cells for Effective Delivery of Therapeutics

• Saltzman WL , OlbrichtW. Building drug delivery into tissue engineering. Nat. Rev. Drug Discov.1, 177–186 (2002).
   PubMed Web of Science ®Google Scholar
• Orive G , AnituaE, PedrazJL, EmerichE. Advances in biomaterials for promoting brain repair and regeneration. Nat. Rev. Neurosci.10, 682–692 (2009).
   PubMed Web of Science ®Google Scholar
• Street J , BaoM, de Guzman L et al. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc. Natl Acad. Sci. USA99, 9656–9661 (2002).
   PubMed Web of Science ®Google Scholar
• Basu P . Technologies that deliver. Nat. Med.9, 1100–1101 (2003).
   PubMed Web of Science ®Google Scholar
• Biondi M , UngaroF, QuagliaF, NettiPA. Controlled drug delivery in tissue engineering. Adv. Drug Deliv. Rev.2, 229–242 (2008).
   Google Scholar
• Anitua E , SánchezM, OriveG, AndiaI. Delivering growth factors for therapeutics. Trends. Pharmacol. Sci29, 37–41 (2008).
   PubMed Web of Science ®Google Scholar
• Tessmar JK , GöpferichAM. Matrices and scaffolds for protein delivery in tissue engineering. Adv. Drug Deliv. Rev.59, 274–291 (2007).
   PubMed Web of Science ®Google Scholar
• Orive G , HernándezRM, GascónAR, Domínguez-GilA, PedrazJL. Drug delivery in biotechnology: present and future. Curr. Opin. Biotechnol.14, 659–664 (2003).
   PubMed Web of Science ®Google Scholar
• Orive G , GascónAR, HernándezRM, Domínguez-GilA, PedrazJL. Techniques: new approaches to the delivery of biopharmaceuticals. Trends Pharmacol. Sci.25, 382–387 (2004).
   PubMed Web of Science ®Google Scholar
• Bisceglie V . Uber die antineoplastische immunitat; heterologe Einpflnzung von Tumoren in Huhner-embryonen. Ztschr Krebsforsch40, 122–140 (1933).
   Google Scholar
• Chang TMS . Semipermeable microcapsules. Science146, 524–525 (1964).
   PubMed Web of Science ®Google Scholar
• Chick WL , LikeAA, LaurisV. β cell culture on synthetic capillaries: an artificial endocrine pancreas. Science187, 847–848 (1975).
   PubMed Web of Science ®Google Scholar
• Lim F , SunAM. Microencapsulated islets as bioartificial endocrine pancreas. Science210, 908–909 (1980).
   PubMed Web of Science ®Google Scholar
• Prakash S , ChangTMS. Microencapsulated genetically engineered live E. coli DH5 cells administered orally to maintain normal plasma urea level in uremic rats. Nat. Med.2, 883–887 (1996).
   PubMed Web of Science ®Google Scholar
• Sun Y , MaX, ZhouD, VacekI, SunAM. Normalization of diabetes in spontaneously diabetic cynomologous monkeys by xenografts of microencapsulated porcine islets without immunosuppression. J. Clin. Invest.98, 1417–1422 (1996).
   PubMed Web of Science ®Google Scholar
• Hortelano G , Al-HendyA, OfosuFA, ChangPL. Delivery of human factor IX in mice by encapsulated recombinant myoblasts: a novel approach towards allogeneic gene therapy of hemophilia B. Blood87, 5095–5103 (1996).
   PubMed Web of Science ®Google Scholar
• Soon-Shiong P , HeintzRE, MeridethNet al. Insulin independence in a type 1 diabetic patient after encapsulated islet transplantation. Lancet 343, 950–951 (1994).
   PubMed Web of Science ®Google Scholar
• Calafiore R , BastaG, LucaGet al. Microencapsulated pancreatic islet allografts into nonimmunosuppressed patients with Type 1 diabetes: first two cases. Diabetes Care 1, 137–138 (2006).
   Google Scholar
• Löhr M , HoffmeyerA, KrögerJet al. Microencapsulated cell-mediated treatment of inoperable pancreatic carcinoma. Lancet 357, 1591–1592 (2001).
   PubMed Web of Science ®Google Scholar
• Orive G , HernándezRM, GascónARet al. Cell encapsulation: promise and progress. Nat. Med. 9, 104–107 (2003).
   PubMed Web of Science ®Google Scholar
• Orive G , HernándezRM, GascónARet al. History, challenges and perspectives of cell microencapsulation. Trends Biotechnol. 22, 87–92 (2004).
   PubMed Web of Science ®Google Scholar
• Zimmermann U , KlockG, FederlinKet al. Production of mitogen-contamination free alginates with variable ratios of mannuronic acid to guluronic acid by free flow electrophoresis. Electrophoresis 13, 269–274 (1992).
   PubMed Web of Science ®Google Scholar
• De Vos P , De Haan BJ, Wolters GHJ, Strubbe JH, Van Schilfgaarde R. Improved biocompatibility but limited graft survival after purification of alginate for microencapsulation of pancreatic islets. Diabetologia40, 262–270 (1997).
   PubMed Web of Science ®Google Scholar
• Lacík I . Polymer chemistry in diabetes treatment by encapsulated islets of Langerhans. Aust. J. Chem.59, 508–524 (2006).
   Web of Science ®Google Scholar
• De Vos P , GemeinerP, BuckoMet al. Multiscale requirements for bioencapsulation in biomedicine and biotechnology. Biomaterials 30, 2559–2570 (2009).
   PubMed Web of Science ®Google Scholar
• Chang PL , BowieKMM. Development of engineered cells for implantation in gene therapy. Adv. Drug Deliv. Rev.33, 31–43 (1998).
   PubMed Web of Science ®Google Scholar
• Orive G , De Castro M, Ponce S, Hernández RM, Gascón AR, Pedraz JL. Long-term expression of erythopoietin from myoblasts immobilized in biocompatible and neovascularized microcapsules. Mol. Ther.12, 283–289 (2005).
   PubMed Web of Science ®Google Scholar
• Murua A , De Castro M, Orive G, Hernández RM, Pedraz JL. In vitro characterization and in vivo functionality of erythropoietin-secreting cells immobilized in alginate poly-L-lysine alginate microcapsules. Biomacromolecules8, 3302–3307 (2007).
   PubMed Web of Science ®Google Scholar
• Orive G , De Castro M, Kong J et al. Bioactive cell-hydrogel microcapsules for cell-based drug delivery. J. Control. Release135, 203–210 (2009).
   PubMed Web of Science ®Google Scholar
• Murua A , OriveG, HernándezRM, PedrazJL. Xenogeneic transplantation of Epo-secreting cells immobilized in microcapsules using transient immunosuppression. J. Control Release137, 174–178 (2009).
   PubMed Web of Science ®Google Scholar
• Xu W , LiuL, CharlesIG. Microencapsulated iNOS-expressing cells cause tumor suppression in mice. FASEB J.16, 213–215 (2002).
   PubMedGoogle Scholar
• Cirone P , BourgeoisJM, AustinRC, ChangPL. A novel approach to tumor suppression with microencapsulated recombinant cells. Hum. Gene Ther.13, 1157–1166 (2002).
   PubMed Web of Science ®Google Scholar
• Benoit DS , SchwartzMP, DurneyAR, AnsethKS. Small functional groups for controlled differentiation of hydrogel-encapsulated human mesenchymal stem cells. Nat. Mater.7, 816–823 (2008).
   PubMed Web of Science ®Google Scholar
• Lund AW , BushJA, PlopperGE, StegemannJP. Osteogenic differentiation of mesenchymal stem cells in defined protein beads. J. Biomed. Mater. Res. B Appl. Biomater.87, 213–221 (2008).
   PubMedGoogle Scholar
• Ding HF , LiuR, LiBG, LouJR, DaiKR, TangTT. Biologic effect and immunoisolating behavior of BMP-2 gene-transfected bone marrow-derived mesenchymal stem cells in APA microcapsules. Biochem. Biophys. Res. Commun.362, 923–927 (2007).
   PubMed Web of Science ®Google Scholar
• Babister JC , TareRS, GreenDW, InglisS, MannS, OreffoROC. Genetic manipulation of human mesenchymal progenitors to promote chondrogenesis using ‘bead-in-bead‘ polysaccharide capsules. Biomaterials29, 58–65 (2008).
   PubMed Web of Science ®Google Scholar
• Goren A , DahanN, GorenE, BaruchL, MachlufM. Encapsulated human mesenchymal stem cells: a unique hypoimmunogenic platform for long-term cellular therapy. FASEB J.24, 22–31 (2010).
   PubMed Web of Science ®Google Scholar
• Hernández RM , OriveG, MuruaA, PedrazJL. Microcapsules and microcarriers for in situ cell delivery. Adv. Drug Deliv. Rev. (2010) (In Press).
   PubMedGoogle Scholar
• Tam SK , DusseaultJ, PolizuS, MénardM, HalléJP, YahiaL. Impact of residual contamination on the biofunctional properties of purified alginates used for cell encapsulation. Biomaterials27, 1296–1305 (2006).
   PubMed Web of Science ®Google Scholar
• Orive G , TamSK., Pedraz JL, Hallé JP. Biocompatibility of alginate-poly-L-lysine microcapsules for cell therapy. Biomaterials27, 3691–3700 (2006).
   PubMed Web of Science ®Google Scholar
• Langlois G , DusseaultJ, BilodeauS, TamSK, MagassoubaD, HalléJP. Direct effect of alginate purification on the survival of islets immobilized in alginate-based microcapsules. Acta Biomater.5, 3433–3440 (2009).
   PubMed Web of Science ®Google Scholar
• Schnoll-Bitai I , UllmerR, HrebicekT, RizziA, LacikI. Characterization of the molecular mass distribution of pullulans bymatrix-assisted laser desorption/ionization time-of-flight mass spectrometry using 2,5-dihydroxybenzoic acid butylamine (DHBB) as liquidmatrix. Rapid Commun. Mass Spectrom.22, 2961–2970 (2008).
   PubMed Web of Science ®Google Scholar
• Grasdalen H , LarsenB, SmidsrodO. 13C-NMR studies of monomeric composition and sequence in alginate. Carbohydr. Res.89, 179–191 (1981).
   Web of Science ®Google Scholar
• Brissova M , LacikI, PowersAC, AnilkumarAV, WangT. Control and measurement of permeability for design of microcapsule cell delivery system. J. Biomed. Mater. Res.39, 61–70 (1998).
   PubMed Web of Science ®Google Scholar
• Kulseng B , ThuB, EspevikT, Skjåk-BrækG. Alginate polylysine microcapsules as immune barrier: permeability of cytokines and immunoglobulins over the capsule membrane. Cell Transplant.6, 387–394 (1997).
   PubMed Web of Science ®Google Scholar
• Morch YA , DonatiI, StrandBL, Skjåk-BrækG. Effect of Ca, Ba and Sr on alginate microbeads. Biomacromolecules7, 1471–1480 (2006).
   PubMed Web of Science ®Google Scholar
• De Castro M , OriveG, HernandezRM, GasconAR, PedrazJL. Comparative study of microcapsules elaborated with three polycations (PLL, PDL, PLO) for cell immobilization. J. Microencapsul.22, 303–315 (2005).
   PubMed Web of Science ®Google Scholar
• Thanos CG , BintzBE, EmerichDF. Stability of alginate–polyornithine microcapsules is profoundly dependent on the site of transplantation. J. Biomed. Mater. Res.A 81, 1–11 (2007).
   Google Scholar
• Kim K , LiuX, ZhangY, ChengJ, YuWX, SunY. Elastic and viscoelastic characterization of microcapsules for drug delivery using a force-feedback MEMS microgripper. Biomed. Microdevices11, 421–127 (2009).
   PubMed Web of Science ®Google Scholar
• 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.80, 813–819 (2007).
   Google Scholar
• Tam SK , DusseaultJ, PolizuS, MenardM, HalleJP, YahiaL. Physicochemical model of alginate-poly-L-lysine microcapsules defined at the micrometric/nanometric scale using ATR-FTIR, XPS, and ToF-SIMS. Biomaterials26, 6950–6961 (2005).
   PubMed Web of Science ®Google Scholar
• Dufrane D , SteenbergheM, GoebbelsRM, SaliezA, GuiotY, GianelloP. The influence of implantation site on the biocompatibility and survival of alginate encapsulated pig islets in rats. Biomaterials27, 3201–3208 (2006).
   PubMed Web of Science ®Google Scholar
• Sakai S , MuC, KawabataK, HashimotoI, KawakamiK. Biocompatibility of subsieve-size capsules versus conventional-size microcapsules. J. Biomed. Mater. Res.78A, 394–398 (2006).
   Web of Science ®Google Scholar
• Bunger CM , TiefenbachB, JahnkeAet al. Deletion of the tissue response against alginate-PLL capsules by temporary release of co-encapsulated steroids. Biomaterials 26, 2353–2360 (2005).
   PubMed Web of Science ®Google Scholar
• Risbud MV , BhargavaS, BhondeRR. In vivo biocompatibility evaluation of cellulose macrocapsules for islet immunoisolation: implications of low molecular weight cut-off. J. Biomed. Mater. Res.6, 86–92 (2003).
   Google Scholar
• Robitaille R , LeblondFA, HenleyN, Prud‘hommeGJ, DrobetskyE, HallJP. Alginate-poly-L-lysine microcapsule biocompatibility: a novel RT-PCR method for cytokine gene expression analysis in pericapsular infiltrates. J. Biomed. Mater. Res.45, 223–230 (1999).
   PubMed Web of Science ®Google Scholar
• Luong Van E , GrondahlL, NurcombeV, CoolS. In vitro biocompatibility and bioactivity of microencapsulated heparansulfate. Biomaterials28, 2127–2136 (2007).
   PubMed Web of Science ®Google Scholar
• Ponce S , OriveG, HernandezRMet al. Chemistry and the biological response against immunoisolating alginatepolycation capsules of different composition. Biomaterials 27, 4831–4839 (2006).
   PubMed Web of Science ®Google Scholar
• Juste S , LessardM, HenleyN, MenardM, HalleJP. Effect of poly-L-lysine coating on macrophage activation by alginate-based microcapsules: assessment using a new in vitro method. J. Biomed. Mater. Res.72A, 389–398 (2005).
   Web of Science ®Google Scholar
• Hurteaux R , Edwards Levy F, Laurent Maquin D, Levy MC. Coating alginate microspheres with a serum albumin–alginate membrane: application to the encapsulation of a peptide. Eur. J. Pharm. Sci.24, 187–197 (2005).
   PubMed Web of Science ®Google Scholar
• Elliott RB , EscobarL, TanPL, MuzinaM, ZwineS, BuchananC. Live encapsulated porcine islets from a type 1 diabetic patient 9.5 yr after xenotransplantation. Xenotransplantation14, 157–161 (2007).
   PubMed Web of Science ®Google Scholar
• Lee DY , NamJH, ByunY. Functional and histological evaluation of transplanted pancreatic islets immunoprotected by PEGylation and cyclosporine for 1 year. Biomaterials28, 1957–1966 (2007).
   PubMed Web of Science ®Google Scholar
• Bikram M , Fouletier-DillingC, HippJAet al. Endochondral bone formation from hydrogel carriers loaded with BMP2-transduced cells. Ann. Biomed. Eng. 35, 796–807 (2007).
   PubMed Web of Science ®Google Scholar
• Grellier M , GranjaPL, FricainJet al. The effect of the co-immobilization of human osteoprogenitors and endotelial cells within alginate microspheres on mineralization in a bone defect. Biomaterials 30, 3271–3278 (2009).
   PubMed Web of Science ®Google Scholar
• Wang C , GongY, ZhongY, YaoY, SuK, WangD. The control of anchorage-dependent cell behaviour within a hydrogel/microcarrier system in a osteogenic model. Biomaterials30, 2259–2269 (2009).
   PubMed Web of Science ®Google Scholar
• Kindi A , ChenGY, AsenjoJFet al. Microencapsulation to reduce mechanical loss of microspheres: implications in myocardial cell therapy. Presented at: Canadian Cardiovascular Congress. Quebec City, PQ, Canada, 20–24 October 2007.
   Google Scholar
• Kindi A , ChenGY, AsenjoJFet al. Cellular cardiomyoplasty: optimizing cellular dosage and retention by microencapsulation. Presented at: American Heart Association Scientific Sessions. Orlando, FL, USA, 4–7 November 2007.
   Google Scholar
• Paul A , GeY, PrakashS, Shum-TimD. Microencapsulated stem cells for tissue repairing: implications in cell-based myocardial therapy. Regen. Med.4, 733–745 (2009).
   PubMed Web of Science ®Google Scholar
• Stover NP , WattsRL. Spheramine for treatment of Parkinson‘s disease, Neurotherapeutics5, 252–259 (2008).
   PubMed Web of Science ®Google Scholar
• Wang T , AdcockJ, KühtreiberWet al. Successful allotransplantation of encapsulated islets in pancreatectomized canines for diabetic management without the use of immunosuppression. Transplantation 85 331–337 (2008).
   PubMed Web of Science ®Google Scholar
• Zang H , ZhuSJ, WangW, WeyYJ, HuSS. Transplantation of microencapsulated genetically modified xenogenic cells augments angiogenesis and improves heart function. Gene Ther.15, 40–48 (2008).
   PubMed Web of Science ®Google Scholar

Websites

• Clinical trial number NCT00940173 www.clinicaltrials.gov
   Google Scholar
• Clinical trial number NCT00260234 www.clinicaltrials.gov
   Google Scholar