Progress in Clinical Encapsulated Islet Xenotransplantation

Transplantation

Volumn 100, Issue 11, 2016, Pages 2301-2308

  Cooper, David K C ^a   Matsumoto, Shinichi ^b   Abalovich, Adrian ^c   Itoh, Takeshi ^d   Mourad, Nizar I ^e   Gianello, Pierre R ^e   Wolf, Eckhard ^f   Cozzi, Emanuele ^g  

^a UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^b OTSUKA PHARMACEUTICAL CO LTD   (Japan)

^c Hospital Eva Peron   (Argentina)

^d FUKUOKA UNIVERSITY   (Japan)

^e UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^f UNIVERSITY OF MUNICH   (Germany)

^g UNIVERSITY HOSPITAL OF PADOVA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINATE POLY ORNITHINE ALGINATE; ALGINIC ACID; GAMMA INTERFERON; HEMOGLOBIN A1C; HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; INSULIN;

ANXIETY DISORDER; APPLICATION SITE DISCOMFORT; BIOACCUMULATION; BIOCOMPATIBILITY; CLINICAL TRIAL (TOPIC); DENDRITIC CELL; DEPRESSION; DNA MODIFICATION; FLUORESCENCE ACTIVATED CELL SORTING; GENETIC ENGINEERING; GLUCOSE TRANSPORT; GRAFT SURVIVAL; HUMAN; HYPOGLYCEMIA; IN VITRO STUDY; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RELEASE; MACROPHAGE; MICROENCAPSULATION; NEUTROPHIL; NONHUMAN; PANCREAS ISLET TRANSPLANTATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; ADVERSE EFFECTS; ANIMAL; PIG; SECRETION (PROCESS); XENOGRAFT;

ANIMALS; CLINICAL TRIALS AS TOPIC; HUMANS; INFLAMMATION; INSULIN; ISLETS OF LANGERHANS TRANSPLANTATION; SWINE; TRANSPLANTATION, HETEROLOGOUS;

EID: 84980340462     PISSN: 00411337     EISSN: None     Source Type: Journal    
DOI: 10.1097/TP.0000000000001371     Document Type: Review

References (89)

1. Markmann JF, Bartlett ST, Johnson P, et al. Executive summary of IPITA-TTS opinion leaders report on the future of β-cell replacement. Transplantation. 2016;7:1453-1459.
2. Hering BJ, Cooper DK, Cozzi E, et al. The International Xenotransplanta-tion Association consensus statement on conditions for undertaking clinical trials of porcine islet products in type 1 diabetes-executive summary. Xenotransplantation. 2009;16:196-202.
3. Hering BJ, Cozzi E, Spizzo T, et al. First update of the International Xeno-transplantation Association consensus statement on conditions for undertaking clinical trials of porcine islet products in type 1 diabetes-executive summary. Xenotransplantation. 2016;23:3-13.
4. van der Windt DJ, Bottino R, Kumar G, et al. Clinical islet xenotransplanta-tion: how close are we? Diabetes. 2012;61:3046-3055.
5. Bottino R, Wijkstrom M, van der Windt DJ, et al. Pig-to-monkey islet xeno-transplantation using multi-transgenic pigs. Am J Transplant. 2014;14: 2275-2287.
6. Shin JS, Kim JM, Kim JS, et al. Long-term control of diabetes in immuno-suppressed nonhuman primates (NHP) bythe transplantationofadult porcine islets. Am J Transplant. 2015;15:2837-2850.
7. Dufrane D, Goebbels RM, Gianello P. Alginate macroencapsulation of pig islets allows correction of streptozotocin-induced diabetes in primates up to 6 months without immunosuppression. Transplantation. 2010;90: 1054-1062.
8. Matsumoto S, Tan P, Baker J, et al. Clinical porcine islet xenotrans-plantation under comprehensive regulation. Transplant Proc. 2014; 46:1992-1995.
9. Krishnan R, Truong N, Gerges M, et al. Impact of donor age and weaning status onpancreatic exocrine and endocrine tissue maturation in pigs. Xe-notransplantation. 2015;22:356-367.
10. Caumo A, Maffi P, Nano R, et al. Comparative evaluation of simple indices of graft function after islet transplantation. Transplantation. 2011;92: 815-821.
11. Dufrane D, Gianello P. Macro-or microencapsulation of pig islets to cure type 1 diabetes. World J Gastroenterol. 2012;18:6885-6893.
12. Sun Y, Ma X, Zhou D, et al. Normalization of diabetes in spontaneously diabetic cynomologus monkeys by xenografts of microencap-sulated porcine islets without immunosuppression. J Clin Invest. 1996;98:1417-1422.
13. Sakata N, Sumi S, Yoshimatsu G, et al. Encapsulated islets transplanta-tion: past, present and future. World J Gastrointest Pathophysiol. 2012; 3:19-26.
14. Vaithilingam V, Tuch BE. Islet transplantation and encapsulation:an update on recent developments. Rev Diabet Stud. 2011;8:51-67.
15. Scharp DW, Marchetti P. Encapsulated islets for diabetes therapy: history, current progress, and critical issues requiring solution. Adv Drug Deliv Rev. 2014;67-68:35-73.
16. Thanos CG, Elliott RB. Encapsulated porcine islet transplantation: an evolving therapy for the treatment of type I diabetes. Expert Opin Biol Ther. 2009;9:29-44.
17. Wang H, Bloom O, Zhang M, et al. HMG-1 asa late mediatorof endotoxin lethality in mice. Science. 1999;285:248-251.
18. Chavan SS, Huerta PT, Robbiati S, et al. HMGB1 mediates cognitive impairment in sepsis survivors. Mol Med. 2012;18:930-937.
19. Matsuoka N, Itoh T, Watarai H, et al. High-mobility group box 1 is involved in the initial events of early loss of transplanted islets in mice. J Clin Invest. 2010;120:735-743.
20. Itoh T, Takita M, SoRelle JA, et al. Correlation of released HMGB1 levels with the degree of islet damage in mice and humans and with the outcomes of islet transplantation in mice. Cell Transplant. 2012; 21:1371-1381.
21. Itoh T, Iwahashi S, Kanak MA, et al. Elevation of high-mobility group box 1 after clinical autologous islet transplantation and its inverse correlation with outcomes. Cell Transplant. 2014;23:153-165.
22. Itoh T, Nitta T, Nishinakamura H, et al. HMGB1-mediated early loss of transplanted islets is prevented by anti-IL-6R antibody in mice. Pancreas. 2015;44:166-171.
23. Mera T, Itoh T, Kita S, et al. Pretreatment of donor islets with the Na(+)/Ca (2+) exchanger inhibitor improves the efficiency of islet transplantation. Am J Transplant. 2013;13:2154-2160.
24. van der Windt DJ, Bottino R, Casu A, et al. Long-term controlled normoglycemia in diabetic non-human primates after transplantation with hCD46 transgenic porcine islets. Am J Transplant. 2009; 9:2716-2726.
25. Thompson P, Badell IR, Lowe M, et al. Islet xenotransplantation using gal-deficient neonatal donors improves engraftment and function. Am J Transplant. 2011;11:2593-2602.
26. Casu A, Bottino R, Balamurugan AN, et al. Metabolic aspects of pig-to-monkey (Macaca fascicularis) islet transplantation: implications for translation into clinical practice. Diabetologia. 2008;51:120-129.
27. Greenspan FS, Gardner DG. Normal hormone reference ranges. In: Greenspan FS, Gardner DG (eds) Basic and Clinical Endocrinology, 7th edn. McGraw-Hill Companies, New York 7th ed 2006:920-938.
28. Genuth S, Alberti KG, Bennett P, et al. Follow-up reportonthe diagnosis of diabetes mellitus. Diabetes Care. 2003;26:3160-3167.
29. Graham ML, Bellin MD, Papas KK, et al. Species incompatibilities in the pig-to-macaque islet xenotransplant model affect transplant outcome: a comparison with allotransplantation. Xenotransplantation. 2011;18:328-342.
30. Graham ML, Schuurman HJ. The usefulness and limitations ofthe diabetic macaque model in evaluating long-term porcine islet xenograft survival. Xenotransplantation. 2013;20:5-17.
31. Mueller KR, Balamurugan AN, Cline GW, et al. Differences in glucose-stimulated insulin secretion in vitro of islets from human, nonhuman primate, and porcine origin. Xenotransplantation. 2013; 20:75-81.
32. Casu A, Echeverri GJ, Bottino R, et al. Insulin secretion and glucose me-tabolism in alpha 1, 3-galactosyltransferase knock-out pigs compared to wild-type pigs. Xenotransplantation. 2010;17:131-139.
33. Wijkstrom M, Bottino R, Iwase H, et al. Glucose metabolism in pigs ex-pressing human genes under an insulin promoter. Xenotransplantation. 2015;22:70-79.
34. Dufrane D, Gianello P. Pig islet for xenotransplantation in human: structural and physiological compatibility for human clinical application. Transplant Rev (Orlando). 2012;26:183-188.
35. Thompson P, Cardona K, Russell M, et al. CD40-specific costimulation blockade enhances neonatal porcine islet survival in nonhuman primates. Am J Transplant. 2011;11:947-957.
36. Bertuzzi F, Zacchetti D, Berra C, et al. Intercellular Ca2+ waves sustain coordinate insulin secretion in pig islets of Langerhans. FEBS Lett. 1996; 379:21-25.
37. Krickhahn M, Meyer T, Bühler C, et al. Highly efficient isolation of porcine islets of Langerhans for xenotransplantation: numbers, purity, yield and in vitro function. Ann Transplant. 2001;6:48-54.
38. Dufrane D, Nenquin M, Henquin JC. Nutrient control of insulin secretion in perifused adult pig islets. Diabetes Metab. 2007;33:430-438.
39. Mueller KR, Balamurugan AN, Cline GW, et al. Differences in glucose-stimulated insulin secretion in vitro of islets from human, nonhuman primate, and porcine origin. Xenotransplantation. 2013;20:75-81.
40. Rabuazzo AM, Davalli AM, Buscema M, et al. Glucose transport, phos-phorylation, and utilization in isolated porcine pancreatic islets. Metabolism. 1995;44:261-266.
41. O'Neil JJ, Stegemann JP, Nicholson DT, et al. The isolation and function of porcine islets from market weight pigs. Cell Transplant. 2001;10:235-246.
42. Bottino R, Balamurugan AN, Smetanka C, et al. Isolation outcome and functional characteristics of young and adult pig pancreatic islets for transplantation studies. Xenotransplantation. 2007;14:74-82.
43. Mourad NI, Nenquin M, Henquin JC. cAMP-mediated and metabolic amplification of insulin secretion are distinct pathways sharing independence of β-cell microfilaments. Endocrinology. 2012;153:4644-4654.
44. Mourad NI, Nenquin M, Henquin JC. Amplification of insulin secretion by acetylcholine or phorbol ester is independent of β-cell microfila-ments and distinct from metabolic amplification. Mol Cell Endocrinol. 2013;367:11-20.
45. Yang Y, Gillis KD. A highly Ca2+-sensitive pool of granules is regulated by glucose and protein kinases in insulin-secreting INS-1 cells. J Gen Physiol. 2004;124:641-651.
46. Kawai T, Andrews D, Colvin RB, et al. Thromboembolic complications after treatment with monoclonal antibody against CD40 ligand. Nat Med. 2000;6:114.
47. Koyama I, Kawai T, Andrews D, et al. Thrombophilia associated with anti-CD154 monoclonal antibody treatment and its prophylaxis in nonhuman primates. Transplantation. 2004;77:460-462.
48. Boumpas DT, Furie R, Manzi S, et al. A short course of BG9588 (anti-CD40 ligand antibody) improves serologic activity and decreases hematu-ria in patients with proliferative lupus glomerulonephritis. Arthritis Rheum. 2003;48:719-727.
49. Mohiuddin MM, Singh AK, Corcoran PC, et al. Genetically engineered pigs and target-specific immunomodulation provide significant graft survival and hope for clinical cardiac xenotransplantation. J Thorac Cardiovasc Surg. 2014;148:1106-1113; discussion 1113-1104.
50. Mohiuddin MM, Singh AK, Corcoran PC, et al. Role of anti-CD40 antibody-mediated costimulation blockade on non-Gal antibody production and heterotopic cardiac xenograft survival in a GTKO.hCD46Tg pig-to-baboon model. Xenotransplantation. 2014;21:35-45.
51. Mohiuddin MM, Singh AK, Corcoran PC, et al. One-year heterotopic cardiac xenograft survival in a pig to baboon model. Am J Transplant. 2014; 14:488-489.
52. Iwase H, Ekser B, Satyananda V, et al. Pig-to-baboon heterotopic heart transplantation-exploratory preliminary experience with pigs transgenic for human thrombomodulin and comparison of three costimulation blockade-based regimens. Xenotransplantation. 2015; 22:211-220.
53. Iwase H, Liu H, Wijkstrom M, et al. Pig kidney graft survival in a baboon for 136 days: longest life-supporting organ graft survival to date. Xenotrans-plantation. 2015;22:302-309.
54. Iwase H, Satyananda V, Zhou H, et al. Initial in vivo experience of pig artery patch transplantation in baboons using mutant MHC (CIITA-DN) pigs. Transpl Immunol. 2015;32:99-108.
55. Wilhite T, Ezzelarab C, Hara H, et al. The effect of Gal expression on pig cells on the human T-cell xenoresponse. Xenotransplantation. 2012;19: 56-63.
56. Ezzelarab MB, Ayares D, Cooper DK. Transgenic expression of human CD46: does it reduce the primate T-cell response to pig endothelial cells? Xenotransplantation. 2015;22:487-489.
57. Satyananda V, Hara H, Ezzelarab MB, et al. New concepts of immune modulation in xenotransplantation. Transplantation. 2013; 96:937-945.
58. Rayat GR, Rajotte RV, Hering BJ, et al. In vitro and in vivo expression of Galalpha-(1, 3)Gal on porcine islet cells is age dependent. J Endocrinol. 2003;177:127-135.
59. Hawthorne WJ, Salvaris EJ, Phillips P, et al. Control of IBMIR in neonatal porcine islet xenotransplantation in baboons. Am J Transplant. 2014;14: 1300-1309.
60. Klymiuk N, van Buerck L, Bähr A, et al. Xenografted islet cell clusters from INSLEA29Y transgenic pigs rescue diabetes and prevent immune rejection in humanized mice. Diabetes. 2012;61:1527-1532.
61. Plotzki E, Wolf-van Buerck L, Knauf Y, et al. Virus safety of islet cell transplantation from transgenic pigs to marmosets. Virus Res. 2015; 204:95-102.
62. Lutz AJ, Li P, Estrada JL, et al. Double knockout pigs deficient in N-glycolylneuraminic acid and galactose α-1, 3-galactose reduce the humoral barrier to xenotransplantation. Xenotransplantation. 2013; 20:27-35.
63. Byrne GW, Du Z, Stalboerger P, et al. Cloning and expression of porcine β1, 4 N-acetylgalactosaminyl transferase encoding a new xenoreactive antigen. Xenotransplantation. 2014;21:543-554.
64. Byrne GW, McGregor CG, Breimer ME. Recent investigations into pig antigen and anti-pig antibody expression. Int J Surg. 2015;23: 223-228.
65. Estrada JL, Martens G, Li P, et al. Evaluation of human and non-human primate antibody binding to pig cells lacking GGTA1/CMAH/β4GalNT2 genes. Xenotransplantation. 2015;22:194-202.
66. Lee W, Hara H, Ezzelarab MB, et al. Initial in vitro studies on tissues and cells from GTKO/CD46/NeuGcKO pigs. Xenotransplantation. 2016;23: 137-150.
67. Park CG, Bottino R, Hawthorne WJ. Current status of islet xenotransplan-tation. Int J Surg. 2015;23:261-266.
68. Sykes M, d'Apice A, Sandrin M. Position paper of the Ethics Committee of the International Xenotransplantation Association. Xenotransplantation. 2003;10:194-203.
69. Cozzi E, Tallacchini M, Flanagan EB, et al. The International Xeno-transplantation Association consensus statement on conditions for undertaking clinical trials of porcine islet products in type 1 diabetes-chapter 1: key ethical requirements and progress toward the definition of an international regulatory framework. Xenotransplantation. 2009; 16:203-214.
70. PHS. Guideline on infectious disease issues in xenotransplantation. http://www. fda.gov/BiologicsBloodVaccines/GuidanceComplianceRegulatoryInformation/Guidances/Xenotransplantation/ucm074727.htm. 2001, 2016.
71. FDA. Guidance for industry: source animals, product, preclinical, and clinical issues concerning the use of xenotransplantation products in human. http://www.fda.gov/BiologicsBloodVaccines/GuidanceComplianceRegulatoryInformation/Guidances/Xenotransplan-tation/ucm074354.htm. Published 2003. Accessed 2016.
72. FDA. Guidance for industry: public health issues posed by the use of non-human primate xenografts in humans. http://www.fda.gov/BiologicsBloodVaccines/GuidanceComplianceRegulatoryInformation/Guidances/Xenotransplantation/ucm074730.htm. Published 1999. Accessed 2016.
73. FDA. Draft guidance for industry: precautionary measures to reduce the possible risk of transmission of zoonoses by blood and blood products from xenotransplantation product recipients and their intimate contacts. http://www.fda.gov/BiologicsBloodVaccines/guidanceComplianceRegulatoryInformation/. Published 2002. Accessed 2016.
74. Arcidiacono JA, Evdokimov E, Lee MH, et al. Regulation of xenogeneic porcine pancreatic islets. Xenotransplantation. 2010;17:329-337.
75. Directive 2001/18/EC of the European Parliament and of the Council of 12 March 2001 on the deliberate release into the environment of genetically modified organisms and repealing Council Directive 90/220/EEC-Commission Declaration http://eur-lex.europa.eu/LexUriServ/LexUriServ. do?uri=CELEX:32001L0018:EN:HTML. Published 2001. Accessed 2016.
76. Directive 2001/20/EC of the European Parliament and of the Council of 4 April 2001 on the approximation of the laws, regulations and administrative provisions of the member states relating to the implementation of Good Clinical Practice in the conduct of clinical trials on medicinal products for human use. Med Etika Bioet. 2002;9:12-19.
77. The European Parliament and the Council of the European Union. Regulation (EC) No 1394/2007 of the European Parliament and of the Council of 13 November 2007 on advanced therapy medicinal prod-ucts and amending Directive 2001/83/EC and Regulation (EC) No 726/2004. http://ec.europa.eu/health/files/eudralex/vol-1/reg-2007- 1394-cons-2012-07/reg-2007-1394-cons-2012-07-en.pdf. Published 2007. Accessed 2016.
78. CHMP. Guideline on xenogeneic cell-based medicinal products 2009; http://www.ema.europa.eu/docs/en-GB/document-library/Scientific- guideline/2009/09/WC500003832.pdf. Published 2009. Accessed 2016.
79. Verordnung über die Transplantation von tierischen Organen, Geweben und Zellen. (This document is only available in German, French, and Italian languages). https://www.admin.ch/opc/de/classified-compila-tion/20051808/index.html. Published 2005. Accessed 2016.
80. MHLW. Medical Care. http://www.mhlw.go.jp/english/policy/health-medi-cal/medical-care/. Published 2010. Accessed 2016.
81. Institutional Framework for Promoting the Future Implementation of Regenerative Medicine. http://www.mhlw.go.jp/english/policy/health-medical/medical-care/dl/150407-01.pdf. Published 2013. Accessed 2016.
82. World Health Organization. First WHO Global Consultation on Regu-latory Requirements for Xenotransplantation Clinical Trials. http://www.who.int/transplantation/xeno/ChangshaCommunique.pdf? ua=1. PUblished 2008. Accessed 2016.
83. World Health Organization. Second WHO Global Consultation on Regulatory Requirements for Xenotransplantation Clinical Trials. http://www.who. int/transplantation/xeno/report2nd-global-consultation-xtx.pdf. Published 2011. Accessed 2016.
84. Veiseh O, Doloff JC, Ma M, et al. Size-and shape-dependent foreign body immune response to materials implanted in rodents and non-human primates. Nat Mater. 2015;14:643-651.
85. Vegas AJ, Veiseh O, Doloff JC, et al. Combinatorial hydrogel library en-ables identification of materials that mitigate the foreign body response in primates. Nat Biotechnol. 2016;34:345-352.
86. Vegas AJ, Veiseh O, Gurtler M, et al. Long-term glycemic control using polymer-encapsulated human stem cell-derived beta cells in immune-competent mice. Nat Med. 2016;22:306-311.
87. Tomei AA, Manzoli V, Fraker CA, et al. Device design and materials op-timization of conformal coating for islets of Langerhans. Proc Natl Acad Sci USA. 2014;111:10514-10519.
88. Cosgun KN, Rahmig S, Mende N, et al. Kit regulates HSC engraftment across the human-mouse species barrier. Cell Stem Cell. 2014;15: 227-238.
89. Renner S, Braun-Reichhart C, Blutke A, et al. Permanent neonatal diabetes in INS(C94Y) transgenic pigs. Diabetes. 2013;62:1505-1511.