Similar articles

Abstract: The potential use of allogeneic islet transplantation in curing type 1 diabetes mellitus has been adequately demonstrated, but its large-scale application is limited by the short supply of donor islets and the need for sustained and heavy immunosuppressive therapy. encapsulation of pig islets was therefore suggested with a view to providing a possible alternative source of islet grafts and avoiding chronic immunosuppression and associated adverse or toxic effects. Nevertheless, several vital elements should be taken into account before this therapy becomes a clinical reality, including cell sources, encapsulation approaches, and implantation sites. This paper provides a comprehensive review of xenotransplantation of encapsulated pig islets for the treatment of type 1 diabetes mellitus, including current research findings and suggestions for future studies.

胶囊猪胰岛移植治疗糖尿病：现况与进展

[1]Abalovich, A.G., Bacque, M.C., Grana, D., et al., 2009. Pig pancreatic islet transplantation into spontaneously diabetic dogs. Transplant. Proc., 41(1):328-330.

[2]Bai, L., Tuch, B.E., Hering, B., et al., 2002. Fetal pig β cells are resistant to the toxic effects of human cytokines. Transplantation, 73(5):714-722.

[3]Barkai, U., Weir, G.C., Colton, C.K., et al., 2013. Enhanced oxygen supply improves islet viability in a new bioartificial pancreas. Cell Transplant., 22(8):1463-1476.

[4]Beck, J., Angus, R., Madsen, B., et al., 2007. Islet encapsulation: strategies to enhance islet cell functions. Tissue Eng., 13(3):589-599.

[5]Borg, D.J., Bonifacio, E., 2011. The use of biomaterials in islet transplantation. Curr. Diabetes Rep., 11(5):434-444.

[6]Bottino, R., Balamurugan, A.N., Smetanka, C., et al., 2007. Isolation outcome and functional characteristics of young and adult pig pancreatic islets for transplantation studies. Xenotransplantation, 14(1):74-82.

[7]Bottino, R., Wijkstrom, M., van der Windt, D.J., et al., 2014. Pig-to-monkey islet xenotransplantation using multi-transgenic pigs. Am. J. Transplant., 14(10):2275-2287.

[8]Buder, B., Alexander, M., Krishnan, R., et al., 2013. Encapsulated islet transplantation: strategies and clinical trials. Immune Netw., 13(6):235-239.

[9]Cabric, S., Sanchez, J., Lundgren, T., et al., 2007. Islet surface heparinization prevents the instant blood-mediated inflammatory reaction in islet transplantation. Diabetes, 56(8):2008-2015.

[10]Calafiore, R., Basta, G., 2014. Clinical application of microencapsulated islets: actual prospectives on progress and challenges. Adv. Drug Deliv. Rev., 67-68:84-92.

[11]Casu, A., Bottino, R., Balamurugan, A.N., et al., 2008. Metabolic aspects of pig-to-monkey (Macaca fascicularis) islet transplantation: implications for translation into clinical practice. Diabetologia, 51(1):120-129.

[12]Christoffersson, G., Henriksnas, J., Johansson, L., et al., 2010. Clinical and experimental pancreatic islet transplantation to striated muscle: establishment of a vascular system similar to that in native islets. Diabetes, 59(10):2569-2578.

[13]Contreras, J.L., Xie, D., Mays, J., et al., 2004. A novel approach to xenotransplantation combining surface engineering and genetic modification of isolated adult porcine islets. Surgery, 136(3):537-547.

[14]Cooper, D.K., Casu, A., 2009. The International Xenotransplantation Association consensus statement on conditions for undertaking clinical trials of porcine islet products in type 1 diabetes—Chapter 4: Pre-clinical efficacy and complication data required to justify a clinical trial. Xenotransplantation, 16(4):229-238.

[15]Cruise, G.M., Hegre, O.D., Scharp, D.S., et al., 1998. A sensitivity study of the key parameters in the interfacial photopolymerization of poly (ethylene glycol) diacrylate upon porcine islets. Biotechnol. Bioeng., 57(6):655-665.

[16]Cui, H., Tucker-Burden, C., Cauffiel, S.M., et al., 2009. Long-term metabolic control of autoimmune diabetes in spontaneously diabetic nonobese diabetic mice by nonvascularized microencapsulated adult porcine islets. Transplantation, 88(2):160-169.

[17]de Groot, M., Schuurs, T.A., van Schilfgaarde, R., 2004. Causes of limited survival of microencapsulated pancreatic islet grafts. J. Surg. Res., 121(1):141-150.

[18]de Vos, P., Spasojevic, M., Faas, M.M., 2010. Treatment of diabetes with encapsulated islets. Adv. Exp. Med. Biol., 670:38-53.

[19]de Vos, P., Lazarjani, H.A., Poncelet, D., et al., 2014. Polymers in cell encapsulation from an enveloped cell perspective. Adv. Drug Deliv. Rev., 67-68:15-34.

[20]Dufrane, D., Gianello, P., 2012. Macro- or microencapsulation of pig islets to cure type 1 diabetes. World J. Gastroenterol., 18(47):6885-6893.

[21]Dufrane, D., Goebbels, R.M., Fdilat, I., et al., 2005. Impact of porcine islet size on cellular structure and engraftment after transplantation: adult versus young pigs. Pancreas, 30(2):138-147.

[22]Dufrane, D., Steenberghe, M., Goebbels, R.M., et al., 2006a. The influence of implantation site on the biocompatibility and survival of alginate encapsulated pig islets in rats. Biomaterials, 27(17):3201-3208.

[23]Dufrane, D., Goebbels, R.M., Saliez, A., et al., 2006b. Six-month survival of microencapsulated pig islets and alginate biocompatibility in primates: proof of concept. Transplantation, 81(9):1345-1353.

[24]Dufrane, D., Goebbels, R.M., Gianello, P., 2010. Alginate macroencapsulation of pig islets allows correction of streptozotocin-induced diabetes in primates up to 6 months without immunosuppression. Transplantation, 90(10):1054-1062.

[25]Elliott, R.B., Escobar, L., Garkavenko, O., et al., 2000. No evidence of infection with porcine endogenous retrovirus in recipients of encapsulated porcine islet xenografts. Cell Transplant., 9(6):895-901.

[26]Elliott, R.B., Escobar, L., Calafiore, R., et al., 2005a. Transplantation of micro- and macroencapsulated piglet islets into mice and monkeys. Transplant. Proc., 37(1):466-469.

[27]Elliott, R.B., Escobar, L., Tan, P.L., et al., 2005b. Intraperitoneal alginate-encapsulated neonatal porcine islets in a placebo-controlled study with 16 diabetic cynomolgus primates. Transplant. Proc., 37(8):3505-3508.

[28]Elliott, R.B., Escobar, L., Tan, P.L., et al., 2007. Live encapsulated porcine islets from a type 1 diabetic patient 9.5 yr after xenotransplantation. Xenotransplantation, 14(2):157-161.

[29]Espes, D., Eriksson, O., Lau, J., et al., 2011. Striated muscle as implantation site for transplanted pancreatic islets. J. Transplant., 2011:352043.

[30]Foster, J.L., Williams, G., Williams, L.J., et al., 2007. Differentiation of transplanted microencapsulated fetal pancreatic cells. Transplantation, 83(11):1440-1448.

[31]Gattás-Asfura, K.M., Stabler, C.L., 2013. Bioorthogonal layer-by-layer encapsulation of pancreatic islets via hyperbranched polymers. ACS Appl. Mater. Interfaces, 5(20):9964-9974.

[32]Grundfest-Broniatowski, S.F., Tellioglu, G., Rosenthal, K.S., et al., 2009. A new bioartificial pancreas utilizing amphiphilic membranes for the immunoisolation of porcine islets: a pilot study in the canine. ASAIO J., 55(4):400-405.

[33]Hatziavramidis, D.T., Karatzas, T.M., Chrousos, G.P., 2013. Pancreatic islet cell transplantation: an update. Ann. Biomed. Eng., 41(3):469-476.

[34]Hering, B.J., Wijkstrom, M., Graham, M.L., et al., 2006. Prolonged diabetes reversal after intraportal xenotransplantation of wild-type porcine islets in immunosuppressed nonhuman primates. Nat. Med., 12(3):301-303.

[35]Hsu, B.R., Chang, F.H., Juang, J.H., et al., 1999. The rescue effect of 15-deoxyspergualin on intraperitoneal microencapsulated xenoislets. Cell Transplant., 8(3):307-315.

[36]Jeong, J.H., Yook, S., Hwang, J.W., et al., 2013. Synergistic effect of surface modification with poly (ethylene glycol) and immunosuppressants on repetitive pancreatic islet transplantation into antecedently sensitized rat. Transplant. Proc., 45(2):585-590.

[37]Jung, Y.S., Jeong, J.H., Yook, S., et al., 2012. 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, 33(1):295-303.

[38]Kim, H.I., Lee, S.Y., Jin, S.M., et al., 2009. Parameters for successful pig islet isolation as determined using 68 specific-pathogen-free miniature pigs. Xenotransplantation, 16(1):11-18.

[39]Kim, J.H., Kim, H.I., Lee, K.W., et al., 2007. Influence of strain and age differences on the yields of porcine islet isolation: extremely high islet yields from SPF CMS miniature pigs. Xenotransplantation, 14(1):60-66.

[40]Kin, T., Nakajima, Y., Aomatsu, Y., et al., 2000. Humoral human xenoreactivity against isolated pig pancreatic islets. Surg. Today, 30(9):821-826.

[41]Kin, T., Iwata, H., Aomatsu, Y., et al., 2002. Xenotransplantation of pig islets in diabetic dogs with use of a microcapsule composed of agarose and polystyrene sulfonic acid mixed gel. Pancreas, 25(1):94-100.

[42]Kirk, K., Hao, E., Lahmy, R., et al., 2014. Human embryonic stem cell derived islet progenitors mature inside an encapsulation device without evidence of increased biomass or cell escape. Stem Cell Res, 12(3):807-814.

[43]Kizilel, S., Scavone, A., Liu, X., et al., 2010. Encapsulation of pancreatic islets within nano-thin functional polyethylene glycol coatings for enhanced insulin secretion. Tissue Eng. Part A, 16(7):2217-2228.

[44]Koulmanda, M., Qipo, A., Smith, R.N., et al., 2003. Pig islet xenografts are resistant to autoimmune destruction by non-obese diabetic recipients after anti-CD4 treatment. Xenotransplantation, 10(2):178-184.

[45]Kumagai-Braesch, M., Jacobson, S., Mori, H., et al., 2013. The theracyte device protects against islet allograft rejection in immunized hosts. Cell Transplant., 22(7):1137-1146.

[46]Lanza, R.P., Butler, D.H., Borland, K.M., et al., 1991. Xenotransplantation of canine, bovine, and porcine islets in diabetic rats without immunosuppression. PNAS, 88(24):11100-11104.

[47]Lanza, R.P., Hayes, J.L., Chick, W.L., 1996. Encapsulated cell technology. Nat. Biotechnol., 14(9):1107-1111.

[48]Lanza, R.P., Jackson, R., Sullivan, A., et al., 1999. Xenotransplantation of cells using biodegradable microcapsules. Transplantation, 67(8):1105-1111.

[49]Lee, D.Y., Nam, J.H., Byun, Y., 2004. Effect of polyethylene glycol grafted onto islet capsules on prevention of splenocyte and cytokine attacks. J. Biomater. Sci. Polym. Ed., 15(6):753-766.

[50]Lee, D.Y., Park, S.J., Nam, J.H., et al., 2006a. A combination therapy of pegylation and immunosuppressive agent for successful islet transplantation. J. Control. Release, 110(2):290-295.

[51]Lee, D.Y., Park, S.J., Nam, J.H., et al., 2006b. A new strategy toward improving immunoprotection in cell therapy for diabetes mellitus: long-functioning pegylated islets in vivo. Tissue Eng., 12(3):615-623.

[52]Leitão, C.B., Cure, P., Tharavanij, T., et al., 2008. Current challenges in islet transplantation. Curr. Diabetes Rep., 8(4):324-331.

[53]Luan, N.M., Iwata, H., 2013. Inhibition of instant blood-mediated inflammatory responses by co-immobilization of sCR1 and heparin on islets. Biomaterials, 34(21):5019-5024.

[54]Ludwig, B., Zimerman, B., Steffen, A., et al., 2010. A novel device for islet transplantation providing immune protection and oxygen supply. Horm. Metab. Res., 42(13):918-922.

[55]Ludwig, B., Reichel, A., Steffen, A., et al., 2013. Transplantation of human islets without immunosuppression. PNAS, 110(47):19054-19058.

[56]Maki, T., Monaco, A.P., 1997. Porcine islet xenotransplantation utilizing a vascularized bioartificial pancreas. Ann. Transplant., 2(3):69-71.

[57]Maki, T., Monaco, A.P., Mullon, C.J., et al., 1996. Early treatment of diabetes with porcine islets in a bioartificial pancreas. Tissue Eng., 2(4):299-306.

[58]Malavasi, N.V., Rodrigues, D.B., Chammas, R., et al., 2010. Continuous and high-level in vivo delivery of endostatin from recombinant cells encapsulated in theracyte immunoisolation devices. Cell Transplant., 19(3):269-277.

[59]Marigliano, M., Bertera, S., Grupillo, M., et al., 2011. Pig-to-nonhuman primates pancreatic islet xenotransplantation: an overview. Curr. Diabetes Rep., 11(5):402-412.

[60]Meier, R.P., Seebach, J.D., Morel, P., et al., 2014. Survival of free and encapsulated human and rat islet xenografts transplanted into the mouse bone marrow. PLoS ONE, 9(3):e91268.

[61]Nagaraju, S., Bottino, R., Wijkstrom, M., et al., 2015. Islet xenotransplantation: what is the optimal age of the islet-source pig? Xenotransplantation, 22(1):7-19.

[62]Neufeld, T., Ludwig, B., Barkai, U., et al., 2013. The efficacy of an immunoisolating membrane system for islet xenotransplantation in minipigs. PLoS ONE, 8(8):e70150.

[63]O'Connell, P.J., Cowan, P.J., Hawthorne, W.J., et al., 2013. Transplantation of xenogeneic islets: are we there yet? Curr. Diabetes Rep., 13(5):687-694.

[64]O'Sullivan, E.S., Vegas, A., Anderson, D.G., et al., 2011. Islets transplanted in immunoisolation devices: a review of the progress and the challenges that remain. Endocr. Rev., 32(6):827-844.

[65]Omer, A., Keegan, M., Czismadia, E., et al., 2003a. Macrophage depletion improves survival of porcine neonatal pancreatic cell clusters contained in alginate macrocapsules transplanted into rats. Xenotransplantation, 10(3):240-251.

[66]Omer, A., Duvivier-Kali, V.F., Trivedi, N., et al., 2003b. Survival and maturation of microencapsulated porcine neonatal pancreatic cell clusters transplanted into immunocompetent diabetic mice. Diabetes, 52(1):69-75.

[67]Orlando, G., Gianello, P., Salvatori, M., et al., 2014. Cell replacement strategies aimed at reconstitution of the β-cell compartment in type 1 diabetes. Diabetes, 63(5):1433-1444.

[68]Petruzzo, P., Pibiri, L., de Giudici, M.A., et al., 1991. Xenotransplantation of microencapsulated pancreatic islets contained in a vascular prosthesis: preliminary results. Transpl. Int., 4(1):200-204.

[69]Potter, K.J., Abedini, A., Marek, P., et al., 2010. Islet amyloid deposition limits the viability of human islet grafts but not porcine islet grafts. PNAS, 107(9):4305-4310.

[70]Prochorov, A.V., Tretjak, S.I., Goranov, V.A., et al., 2008. Treatment of insulin dependent diabetes mellitus with intravascular transplantation of pancreatic islet cells without immunosuppressive therapy. Adv. Med. Sci., 53(2):240-244.

[71]Ramesh, A., Chhabra, P., Brayman, K.L., 2013. Pancreatic islet transplantation in type 1 diabetes mellitus: an update on recent developments. Curr. Diabetes Rev., 9(4):294-311.

[72]Safley, S.A., Kapp, L.M., Tucker-Burden, C., et al., 2005. Inhibition of cellular immune responses to encapsulated porcine islet xenografts by simultaneous blockade of two different costimulatory pathways. Transplantation, 79(4):409-418.

[73]Sakata, N., Sumi, S., Yoshimatsu, G., et al., 2012. Encapsulated islets transplantation: past, present and future. World J. Gastrointest. Pathophysiol., 3(1):19-26.

[74]Scalea, J., Hanecamp, I., Robson, S.C., et al., 2012. T-cell-mediated immunological barriers to xenotransplantation. Xenotransplantation, 19(1):23-30.

[75]Scharp, D.W., Marchetti, P., 2014. Encapsulated islets for diabetes therapy: history, current progress, and critical issues requiring solution. Adv. Drug Deliv. Rev., 67-68:35-73.

[76]Sefton, M.V., May, M.H., Lahooti, S., et al., 2000. Making microencapsulation work: conformal coating, immobilization gels and in vivo performance. J. Control. Release, 65(1-2):173-186.

[77]Semaan, M., Kaulitz, D., Petersen, B., et al., 2012. Long-term effects of PERV-specific RNA interference in transgenic pigs. Xenotransplantation, 19(2):112-121.

[78]Shapiro, A.M., Lakey, J.R., Ryan, E.A., et al., 2000. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N. Engl. J. Med., 343(4):230-238.

[79]Shin, J.S., Kim, J.S., Kim, J.M., et al., 2014. Minimizing immunosuppression in islet xenotransplantation. Immunotherapy, 6(4):419-430.

[80]Shin, S., Shin, J.E., Yoo, Y.J., 2013. Attachment of alginate microcapsules onto plasma-treated PDMS sheet for retrieval after transplantation. Biotechnol. Appl. Biochem., 60(6):617-622.

[81]Sörenby, A.K., Kumagai-Braesch, M., Sharma, A., et al., 2008. Preimplantation of an immunoprotective device can lower the curative dose of islets to that of free islet transplantation: studies in a rodent model. Transplantation, 86(2):364-366.

[82]Sun, Y., Ma, X., Zhou, D., et al., 1996. Normalization of diabetes in spontaneously diabetic cynomologus monkeys by xenografts of microencapsulated porcine islets without immunosuppression. J. Clin. Invest., 98(6):1417-1422.

[83]Tan, P.L., 2010. Company profile: tissue regeneration for diabetes and neurological diseases at living cell technologies. Regen. Med., 5(2):181-187.

[84]Teramura, Y., Iwata, H., 2008. Islets surface modification prevents blood-mediated inflammatory responses. Bioconjug. Chem., 19(7):1389-1395.

[85]Teramura, Y., Iwata, H., 2009. Surface modification of islets with peg-lipid for improvement of graft survival in intraportal transplantation. Transplantation, 88(5):624-630.

[86]Thompson, P., Cardona, K., Russell, M., et al., 2011a. CD40-specific costimulation blockade enhances neonatal porcine islet survival in nonhuman primates. Am. J. Transplant., 11(5):947-957.

[87]Thompson, P., Badell, I.R., Lowe, M., et al., 2011b. Islet xenotransplantation using gal-deficient neonatal donors improves engraftment and function. Am. J. Transplant., 11(12):2593-2602.

[88]Thompson, P., Badell, I.R., Lowe, M., et al., 2012. Alternative immunomodulatory strategies for xenotransplantation: CD40/154 pathway-sparing regimens promote xenograft survival. Am. J. Transplant., 12(7):1765-1775.

[89]Tomei, A.A., Manzoli, V., Fraker, C.A., et al., 2014. Device design and materials optimization of conformal coating for islets of langerhans. PNAS, 111(29):10514-10519.

[90]Vaithilingam, V., Fung, C., Ratnapala, S., et al., 2013. Characterisation of the xenogeneic immune response to microencapsulated fetal pig islet-like cell clusters transplanted into immunocompetent C57BL/6 mice. PLoS ONE, 8(3):e59120.

[91]Valdés-González, R.A., Dorantes, L.M., Garibay, G.N., et al., 2005. Xenotransplantation of porcine neonatal islets of Langerhans and Sertoli cells: a 4-year study. Eur. J. Endocrinol., 153(3):419-427.

[92]Valdés-González, R.A., White, D.J., Dorantes, L.M., et al., 2007. Three-yr follow-up of a type 1 diabetes mellitus patient with an islet xenotransplant. Clin. Transplant., 21(3):352-357.

[93]Valdes-Gonzalez, R., Rodriguez-Ventura, A.L., White, D.J., et al., 2010. Long-term follow-up of patients with type 1 diabetes transplanted with neonatal pig islets. Clin. Exp. Immunol., 162(3):537-542.

[94]van der Windt, D.J., Bottino, R., Casu, A., et al., 2009. Long-term controlled normoglycemia in diabetic non-human primates after transplantation with hCD46 transgenic porcine islets. Am. J. Transplant., 9(12):2716-2726.

[95]van Schilfgaarde, R., de Vos, P., 1999. Factors influencing the properties and performance of microcapsules for immunoprotection of pancreatic islets. J. Mol. Med. (Berl.), 77(1):199-205.

[96]Vériter, S., Gianello, P., Dufrane, D., 2013. Bioengineered sites for islet cell transplantation. Curr. Diabetes Rep., 13(5):745-755.

[97]Vériter, S., Gianello, P., Igarashi, Y., et al., 2014. Improvement of subcutaneous bioartificial pancreas vascularization and function by coencapsulation of pig islets and mesenchymal stem cells in primates. Cell Transplant., 23(11):1349-1364.

[98]Vinerean, H.V., Gazda, L.S., Hall, R.D., et al., 2008. Improved glucose regulation on a low carbohydrate diet in diabetic rats transplanted with macroencapsulated porcine islets. Cell Transplant., 17(5):567-575.

[99]Wang, W., Gu, Y., Tabata, Y., et al., 2002. Reversal of diabetes in mice by xenotransplantation of a bioartificial pancreas in a prevascularized subcutaneous site. Transplantation, 73(1):122-129.

[100]Wang, W., Gu, Y., Hori, H., et al., 2003. Subcutaneous transplantation of macroencapsulated porcine pancreatic endocrine cells normalizes hyperglycemia in diabetic mice. Transplantation, 76(2):290-296.

[101]Weir, G.C., 2013. Islet encapsulation: advances and obstacles. Diabetologia, 56(7):1458-1461.

[102]Wilson, J.T., Cui, W., Chaikof, E.L., 2008. Layer-by-layer assembly of a conformal nanothin PEG coating for intraportal islet transplantation. Nano Lett., 8(7):1940-1948.

[103]Wilson, J.T., Cui, W., Kozlovskaya, V., et al., 2011. Cell surface engineering with polyelectrolyte multilayer thin films. J. Am. Chem. Soc., 133(18):7054-7064.

[104]Wynyard, S., Nathu, D., Garkavenko, O., et al., 2014. Microbiological safety of the first clinical pig islet xenotransplantation trial in New Zealand. Xenotransplantation, 21(4):309-323.

[105]Yonekawa, Y., Matsumoto, S., Okitsu, T., et al., 2005. Effective islet isolation method with extremely high islet yields from adult pigs. Cell Transplant., 14(10):757-762.

[106]Zhi, Z.L., Kerby, A., King, A.J., et al., 2012. Nano-scale encapsulation enhances allograft survival and function of islets transplanted in a mouse model of diabetes. Diabetologia, 55(4):1081-1090.

[107]Zhu, H.T., Yu, L., Lyu, Y., et al., 2014a. Optimal pig donor selection in islet xenotransplantation: current status and future perspectives. J. Zhejiang Univ.-Sci. B (Biomed. & Biotechnol.), 15(8):681-691.

[108]Zhu, H.T., Wang, W.L., Yu, L., et al., 2014b. Pig-islets xenotransplantation: recent progress and current perspectives. Front. Surg., 1:7.

[109]Zimmermann, H., Shirley, S.G., Zimmermann, U., 2007. Alginate-based encapsulation of cells: past, present, and future. Curr. Diabetes Rep., 7(4):314-320.