Pig-to-nonhuman primates pancreatic islet xenotransplantation: An overview

Current Diabetes Reports

Volumn 11, Issue 5, 2011, Pages 402-412

  Marigliano, Marco ^a,b   Bertera, Suzanne ^a   Grupillo, Maria ^a,c   Trucco, Massimo ^a   Bottino, Rita ^a  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b Regional Center for Diabetes in Children and Adolescents   (Italy)

^c RiMED Foundation   (Italy)

Author keywords

cell replacement; Islet xenotransplantation; Non human primates; Pancreas; Type 1 diabetes

Indexed keywords

ABATACEPT; AZATHIOPRINE; BASILIXIMAB; BELATACEPT; CD20 ANTIBODY; CD40 LIGAND MONOCLONAL ANTIBODY; COBROTOXIN; CYCLOSPORIN A; DEXTRAN SULFATE; EVEROLIMUS; FINGOLIMOD; INTERLEUKIN 2 RECEPTOR ANTIBODY; LEFLUNOMIDE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; RAPAMYCIN; TACROLIMUS; THYMOCYTE ANTIBODY;

ANTIGEN RECOGNITION; GRAFT REJECTION; GRAFT SURVIVAL; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOSUPPRESSIVE TREATMENT; INSULIN DEPENDENCE; INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET TRANSPLANTATION; PIG TO NONHUMAN PRIMATE PANCREATIC ISLET XENOTRANSPLANTATION; REVIEW; SURGICAL TECHNIQUE; SWINE;

ANIMALS; DIABETES MELLITUS, TYPE 1; HUMANS; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS TRANSPLANTATION; PRIMATES; SWINE; TRANSPLANTATION, HETEROLOGOUS;

EID: 80755145988     PISSN: 15344827     EISSN: 15390829     Source Type: Journal    
DOI: 10.1007/s11892-011-0213-z     Document Type: Review

References (60)

1. Shapiro AM, Lakey JR, Ryan EA, Korbutt GS, Toth E, Warnock GL, et al. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N Engl J Med. 2000;343:230-8. (Pubitemid 30490390)
2. Cooper DK, Gollackner B, Knosalla C, Teranishi K. Xenotransplantation-, how far have we come? Transpl Immunol. 2002;9:251-6.
3. Ryan EA, Paty BW, Senior PA, et al. Five-year follow-up after clinical islet transplantation. Diabetes. 2005;54:2060-9. (Pubitemid 40911269)
4. Koulmanda M, Qipo A, Smith RN, Auchincloss Jr H. Pig islet xenografts are resistant to autoimmune destruction by non-obese diabetic recipients after anti-CD4 treatment. Xenotransplantation. 2003;10:178-84. (Pubitemid 36903787)
5. Potter KJ, Abedini A, Marek P, Klimek AM, Butterworth S, et al. Islet amyloid deposition limits the viability of human islet grafts but not porcine islet grafts. Proc Natl Acad Sci USA. 2010;107 (9):4305-10. Epub 2010 Feb 16.
6. Hering BJ, Cooper DKC, Cozzi E. Schuurman H-J, Korbutt GS, Denner J, et al. The International Xenotransplantation Association consensus statement on conditions for undertaking clinical trials of porcine islet products in type 1 diabetes- Executive summary. Xenotransplantation. 2009;16:196-202. This paper shows a current consensus statement on islet xenoTx and describes the conditions for undertaking clinical trials of porcine islet products in T1D.
7. Shapiro AM, Ricordi C, Hering BJ, Auchincloss H, Lindblad R, Robertson RP, et al. International trial of the Edmonton protocol for islet transplantation. N Engl J Med. 2006;355(13):01318-30.
8. Hogan A, Pileggi A, Ricordi C. Transplantation: current developments and future directions; the future of clinical islet transplantation as a cure for diabetes. Front Biosci. 2008;13:1192-205. (Pubitemid 351606121)
9. Pambianco G, Costacou T, Ellis D, Becker DJ, Klein R, Orchard TJ. The30-yearnatural history of type 1 diabetes complications: the Pittsburgh Epidemiology of Diabetes Complications Study experience. Diabetes. 2006;55(5):1463-9. (Pubitemid 44195388)
10. Prabhakaran S, Hering BJ. What strain of pig should be used? Xenotransplantation. 2008;15:83.
11. Koulmanda M, Qipo A, Smith RN, Auchincloss Jr H. Pig islet xenografts are resistant to autoimmune destruction by non-obese diabetic recipients after anti-CD4 treatment. Xenotransplantation. 2003;10(2):178-84. (Pubitemid 36903787)
12. Appel MC, Banuelos SJ, Greiner DL, Shultz LD, Mordes JP, Rossini AA. Prolonged survival of neonatal porcine islet xenografts in mice treated with a donor-specific transfusion and anti-CD154 antibody. Transplantation. 2004;77(9):1341-9. (Pubitemid 38668425)
13. Rood PP, Bottino R, Balamurugan AN, et al. Reduction of early graft loss after intraportal porcine islet transplantation in monkeys. Transplantation. 2007;83:202-10. (Pubitemid 46185211)
14. Morsiani E, Fogli L, Lanza Jr G, et al. Long-term insulin independence following repeated islet transplantation in totally pancreatectomized diabetic pigs. Cell Transplant. 2002;11:55-66. (Pubitemid 34242240)
15. van der Windt DJ, Bottino R, Casu A, Campanile N, Smetanka C, He J, et al. Long-term controlled normoglycemia in diabetic non-human primates after transplantation with hCD46 transgenic porcine islets. Am J Transplant. 2009;12:2716-26. This paper shows successful islet xenoTx in diabetic NHPs and, in particular, one transplanted diabetic monkey that remained exogenous insulin-free for more than 1 year.
16. Cardona K, Korbutt GS, Milas Z, et al. Long-term survival of neonatal porcine islets in nonhuman primates by targeting costimulation pathways. Nat Med. 2006;12:304-6. (Pubitemid 43355077)
17. Hering BJ, Wijkstrom M, Graham ML, et al. Prolonged diabetes reversal after intraportal xenotransplantation of wild-type porcine islets in immunosuppressed nonhuman primates. Nat Med. 2006;12:301-3. (Pubitemid 43355076)
18. Ricordi C, Finke EH, Lacy PE. A method for the mass isolation of islets from the adult pig pancreas. Diabetes. 1986;35:649-53. (Pubitemid 16088341)
19. Mandel TE. Fetal islet xenotransplantation in rodents and primates. J Mol Med. 1999;77:155-60. (Pubitemid 29146208)
20. Sandler S, Andersson A, Eizirik DL, et al. Assessment of insulin secretion in vitro from microencapsulated fetal porcine islet-like cell clusters and rat, mouse, and human pancreatic islets. Transplantation. 1997;63:1712.
21. Hawthorne WJ, Simond DM, Stokes R, Patel AT, Walters S, Burgess J, et al. Subcapsular fetal pig pancreas fragment transplantation provides normal blood glucose control in a preclinical model of diabetes. Transplantation. 2011;91:515-21.
22. Hardikar AA, Wang XY, Williams LJ, Kwok J, Wong R, Yao M, et al. Functional maturation of fetal porcine beta-cells by glucagonlike peptide 1 and cholecystokinin. Endocrinology. 2002;143:3505-14. (Pubitemid 34925725)
23. Bennet W, Björkland A, Sundberg B, Davies H, Liu J, Holgersson J, et al. A comparison of fetal and adult porcine islets with regard to Gal alpha (1,3)Gal expression and the role of human immunoglobulins and complement in islet cell cytotoxicity. Transplantation. 2000;69:1711-7.
24. Korbutt GS, Elliott JF, Ao Z, et al. Large scale isolation, growth, and function of porcine neonatal islet cells. J Clin Invest. 1996;97:2119-29. (Pubitemid 26143967)
25. Vizzardelli C, Molano RD, Pileggi A, Berney T, Cattan P, Fenjves ES, et al. Neonatal porcine pancreatic cell clusters as a potential source for transplantation in humans: characterization of proliferation, apoptosis, xenoantigen expression and gene delivery with recombinant AAV. Xenotransplantation. 2002;9:14-24. (Pubitemid 36358220)
26. Collares-Buzato CB, Leite AR, Boschero AC. Modulation of gap and adherens junctional proteins in cultured neonatal pancreatic islets. Pancreas. 2001;23:177-85. (Pubitemid 32692127)
27. 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. (Pubitemid 46051372)
28. Dufrane D, D'Hoore W, Goebbels RM, et al. Parameters favouring successful adult pig islet isolations for xenotransplantation in pig-toprimate models. Xenotransplantation. 2006;13:204-14. (Pubitemid 43824210)
29. Yonekawa Y, Matsumoto S, Okitsu T, et al. Effective islet isolation method with extremely high islet yields from adult pigs. Cell Transplant. 2005;14:757-62. (Pubitemid 43152980)
30. Echeverri GJ, McGrath K, Bottino R, Hara H, Dons EM, van der Windt DJ, et al. Endoscopic Gastric Submucosal Transplantation of Islets (ENDO-STI): technique and initial results in diabetic pigs. Am J Transplant. 2009;9:2485-96.
31. Toso C, Brandhorst D, Oberholzer J, Triponez F, Buhler L, Morel P. Isolation of adult porcine islets of Langerhans. Cell Transplant. 2000;9:297-305. (Pubitemid 30655682)
32. Humphrey RK, Smith MS, Kwok J, Si Z, Tuch BE, Simpson AM. In vitro dedifferentiation of fetal porcine pancreatic tissue prior to transplantation as islet-like cell clusters. Cells Tissues Organs. 2001;168:158-69. (Pubitemid 32171060)
33. Wagner JD, Carlson CS, O'Brien TD, et al. Diabetes mellitus and islet amyloidosis in cynomolgus monkeys. Lab Anim Sci. 1996;46:36-41.
34. Szkudelski T. The mechanism of alloxan and streptozo- tocin action in B cells of the rat pancreas. Physiol Res. 2001;50:537-46. (Pubitemid 34087272)
35. Theriault BR, Thistlethwaite Jr JR, Levisetti MG, Wardrip CL, Szot G, Bruce DS, et al. Induction, maintenance, and reversal of streptozotocin-induced insulin-dependent diabetes mellitus in the juvenile cynomolgus monkey (Macaca fascilularis). Transplantation. 1999;68:331-7. (Pubitemid 29384099)
36. Bottino R, Criscimanna A, Casu A, He J, Van der Windt DJ, Rudert WA, et al. Recovery of endogenous ?-cell function in nonhuman primates after chemical diabetes induction and islet transplantation. Diabetes. 2009;58:442-7.
37. Casu A, Bottino R, Balamurugan AN, Hara H, van der Windt DJ, Campanile N, et al. Metabolic aspects of pig-to-monkey (Macaca fascicularis) islet transplantation: implications for translation into clinical practice. Diabetologia. 2008;51:120-9. (Pubitemid 350197988)
38. Marigliano M, Casu A, Bertera S, Trucco M, Bottino R. Hemoglobin A1C percentage in Non-Human Primates: a useful tool to monitor diabetes before and after porcine pancreatic Islet Xenotransplantation. J Transplant. 2011;in press.
39. Buhler L, Deng S, O'Neil J, Kitamura H, Koulmanda M, Baldi A, et al. Adult porcine islet transplantation in baboons treated with conventional immunosuppression or a non-myeloablative regimen and CD154 blockade. Xenotransplantation. 2002;9:3-13. (Pubitemid 36358219)
40. Cantarovich D, Blancho G, Potiron N, Jugeau N, Fiche M, Chagneau C, et al. Rapid failure of pig islet transplantation in non human primates. Xenotransplantation. 2002;9:25-35. (Pubitemid 36358221)
41. Rijkelijkhuizen JK, Haanstra KG, Wubben J, Tons A, Roos A, Gijlswijk-Janssen DJ, et al. T-cell-specific immunosuppression results in more than 53 days survival of porcine islets of Langerhans in the monkey. Transplantation. 2003;76:1359-68. (Pubitemid 37430724)
42. Kirchhof N, Shibata S, Wijkstrom M, Kulick DM, Salerno CT, Clemmings S, et al. Reversal of diabetes in non-immunosuppressed rhesus macaques by intraportal porcine islet xenografts precedes acute cellular rejection. Xenotransplantation. 2004;11:396-407. (Pubitemid 39128209)
43. Dufrane D, Goebbels RM, Saliez A, Guiot Y, Gianello P. Sixmonth survival of microencapsulated pig islets and alginate biocompatibility in primates: proof of concept. Transplantation. 2006;81:1345-53. (Pubitemid 43804557)
44. Komoda H, Miyagawa S, Omori T, Takahagi Y, Murakami H, Shigehisa T, et al. Survival of adult islet grafts from transgenic pigs with N-acetylglucosaminyl- transferase-III (GnT-III) in cynomolgus monkeys. Xenotransplantation. 2005;12(3):209-16. (Pubitemid 40524981)
45. Cardona K, Milas Z, Strobert E, Cano J, Jiang W, Safley SA, et al. Engraftment of adult porcine islet xenografts in diabetic nonhuman primates through targeting of costimulation pathways. Am J Transplant. 2007;7:2260-8. (Pubitemid 47347856)
46. Ayares D, Phelps C, Vaught T, Ball S. Genetic engineering of pigs for improved transplant outcomes. Xenotransplantation. 2007;14:428.
47. Gianello P, Dufrane D. Encapsulation of pig islets by alginate matrix to correct streptozotocin-induced diabetes in primates without immunosuppression. Xenotransplantation. 2007;14:441.
48. Hecht G, Eventov-Friedman S, Rosen C, Shezen E, Tchorsh D, Aronovich A, et al. Embryonic pig pancreatic tissue for the treatment of diabetes in a nonhuman primate model. Proc Natl Acad Sci USA. 2009;106:8659-64.
49. 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;90:1054-62. This paper assessed the capacity of alginateencapsulated islets to reverse diabetes in a pig-to-primate model up to 6 months even without immunosuppression.
50. Bennet W, Sundberg B, Groth CG, Brendel MD, Brandhorst D, Brandhorst H, et al. Incompatibility between human blood and isolated islets of Langerhans: a finding with implications for clinical intraportal islet transplantation? Diabetes. 1999;48:1907-14. (Pubitemid 29458351)
51. van der Windt DJ, Bottino R, Casu A, Campanile N, Cooper DKC. Rapid loss of intraportally-transplanted islets:an overview of pathophysiology and preventive strategies. Xenotransplantation. 2007;14:288-97. (Pubitemid 47174365)
52. Ji M, Yi S, Smith-Hurst H, Phillips P, Wu J, Hawthorne W, et al. The importance of tissue factor expression by porcine NICC in triggering IBMIR in the xenograft setting. Transplantation. 2011;91:841-6.
53. Goto M, Tjernberg J, Dufrane D, et al. Dissecting the instant blood-mediated inflammatory reaction in islet xenotransplantation. Xenotransplantation. 2008;15:225-34.
54. Gangappa S, Larsen CP. Immunosuppressive protocols for pig-tohuman islet transplantation: lessons from pre-clinical non-human primate models. Xenotransplantation. 2008;15:107-11. (Pubitemid 351601131)
55. Phelps CJ, Ball SF, Vaught TD, Vance AM, Mendicino M, Monahan JA, et al. Production and characterization of transgenic pigs expressing porcine CTLA4-Ig. Xenotransplantation. 2009;16:477-85.
56. Gunji T, Saito T, Sato Y, Matsuyama S, Ise K, Kimura T, et al. Mitomycin-C treatment followed by culture produces long-term survival of islet xenografts in a rat-to mouse model. Cell Transplant. 2008;17:619-29.
57. Yun LD, Hee NJ, Byun Y. Functional and histological evaluation of transplanted pancreatic islets immunoprotected by PEGylation and cyclosporine for 1 year. Biomaterials. 2007;28:1957-66. (Pubitemid 46176171)
58. Ludwig B, Zimerman B, Steffen A, Yavriants K, Azarov D, Reichel A, et al. A novel device for islet transplantation providing immune protection and oxygen supply. Horm Metab Res. 2010;42:918-22.
59. Bloch K, Bloch O, Tarasenko I, Lazard D, Rapoport M, Vardi P. A strategy for the engineering of insulin producing cells with a broad spectrum of defense properties. Biomaterials. 2011;32:1816-25.
60. Ekser B, Cooper DKC. Overcoming the barriers to xenotransplantation: prospects for the future. Expert Rev Clin Immunol. 2010;6:219-30.