Characterisation of the Xenogeneic Immune Response to Microencapsulated Fetal Pig Islet-Like Cell Clusters Transplanted into Immunocompetent C57BL/6 Mice

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Vaithilingam, Vijayaganapathy ^a,c   Fung, Cherry ^a   Ratnapala, Sabina ^a   Foster, Jayne ^a   Vaghjiani, Vijesh ^b   Manuelpillai, Ursula ^b   Tuch, Bernard E ^a,c  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c CSIRO   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

C PEPTIDE; HEAT SHOCK PROTEIN 90; HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 8; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CELL VIABILITY; COLLAGEN METABOLISM; CONTROLLED STUDY; CYTOKINE PRODUCTION; FETUS; GENE EXPRESSION; HEAT SHOCK PROTEIN 90 GENE; HIGH MOBILITY GROUP B1 GENE; HOST CELL; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; INTERLEUKIN 8 GENE; MACROPHAGE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA GENE; MALE; MICROENCAPSULATION; MOUSE; MYOFIBROBLAST; NONHUMAN; PANCREAS ISLET CELL; PERITONEAL CAVITY; SWINE; XENOTRANSPLANTATION;

ALGINATES; ANIMALS; ANTIGENS; BIOLOGICAL MARKERS; CELL MOVEMENT; CYTOKINES; FETUS; GLUCURONIC ACID; GRAFT REJECTION; HEXURONIC ACIDS; IMMUNOCOMPETENCE; INSULIN; ISLETS OF LANGERHANS; ISLETS OF LANGERHANS TRANSPLANTATION; MACROPHAGES; MICE; MYOFIBROBLASTS; PERITONEAL CAVITY; SWINE; TRANSPLANTATION, HETEROLOGOUS; TRANSPLANTATION, HETEROTOPIC;

EID: 84875014924     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059120     Document Type: Article

References (47)

1. Bottino R, Balamurugan AN, Smetanka C, Bertera S, He J, et al. (2007) Isolation outcome and functional characteristics of young and adult pig pancreatic islets for transplantation studies. Xenotransplantation 14: 74-82.
2. Korbutt GS, Elliott JF, Ao Z, Smith DK, Warnock GL, et al. (1996) Large Scale Isolation, Growth, and Function of Porcine Neonatal Islet Cells. J. Clin. Invest. 97: 2119-2129.
3. Trivedi N, Hollister-Lock J, Lopez-Avalos MD, O'Neil JJ, Keegan M, et al. (2001) Increase in β-Cell Mass in Transplanted Porcine Neonatal Pancreatic Cell Clusters Is Due to Proliferation of β-Cells and Differentiation of Duct Cells. Endocrinology 142: 2115-2122.
4. Korsgren O, Jansson L, Eizirik D, Andersson A, (1991) Functional and morphological differentiation of fetal porcine islet-like cell clusters after transplantation into nude mice. Diabetologia 34: 379-386.
5. Bai L, Tuch BE, Hering B, Simpson AM, (2002) Fetal pig beta cells are resistant to the toxic effects of human cytokines. Transplantation 73: 714-722.
6. Bai L, Maedler K, Donath M, Tuch BE, (2004) Expression of Fas but not Fas ligand on fetal pig β cells. Xenotransplantation 11: 426-435.
7. Tu J, Khoury P, Williams L, Tuch BE, (2004) Comparison of fetal porcine aggregates of purified beta-cells versus islet-like cell clusters as a treatment of diabetes. Cell Transplant 13: 525-534.
8. Vo L, Tuch BE, Wright DC, Keogh GW, Roberts S, et al. (2001) Lowering of blood glucose to nondiabetic levels in a hyperglycemic pig by allografting of fetal pig islet-like cell clusters. Transplantation 71: 1671-1677.
9. Groth CG, Korsgren O, Tibell A, Tollemar J, Moller E, et al. (1994) Transplantation of porcine fetal pancreas to diabetic patients. Lancet 344: 1402-1404.
10. Reinholt FP, Hultenby K, Tibell A, Korsgren O, Groth CG, (1998) Survival of fetal porcine pancreatic islet tissue transplanted to a diabetic patient: Findings by ultrastructural immunocytochemistry. Xenotransplantation 5: 222-225.
11. Lanza RP, Jackson R, Sullivan A, Ringeling J, McGrath C, et al. (1999) Xenotransplantation of cells using biodegradable microcapsules. Transplantation 67: 1105-1111.
12. Foster JL, Williams G, Williams LJ, Tuch BE, (2007) Differentiation of transplanted microencapsulated fetal pancreatic cells. Transplantation 83: 1440-1448.
13. Rayat GR, Rajotte RV, Ao Z, Korbutt GS, (2000) Microencapsulation of neonatal porcine islets: protection from human antibody/complement-mediated cytolysis in vitro and long-term reversal of diabetes in nude mice. Transplantation 69: 1084-1090.
14. Duvivier-Kali VF, Omer A, Lopez-Avalos MD, O'Neil JJ, Weir GC, (2004) Survival of Microencapsulated Adult Pig Islets in Mice In Spite of an Antibody Response. Am J Transplant. 4: 1991-2000.
15. Omer A, Duvivier-Kali VF, Trivedi N, Wilmot K, Bonner-Weir S, et al. (2003) Survival and maturation of microencapsulated porcine neonatal pancreatic cell clusters transplanted into immunocompetent diabetic mice. Diabetes 52: 69-75.
16. Sun Y, Ma X, Zhou D, Vacek I, Sun AM, (1996) Normalization of Diabetes in Spontaneously Diabetic Cynomologus Monkeys by Xenografts of Microencapsulated Porcine Islets without Immunosuppression. J. Clin. Invest. 98: 1417-1422.
17. Kobayashi T, Harb G, Rajotte RV, Korbutt GS, Mallett AG, et al. (2006) Immune mechanisms associated with the rejection of encapsulated neonatal porcine islet xenografts. Xenotransplantation 13: 547-559.
18. Kobayashi T, Harb G, Rayat GR, (2005) Prolonged survival of microencapsulated neonatal porcine islets in mice treated with a combination of anti-CD154 and anti-LFA-1 monoclonal antibodies. Transplantation 80: 821-827.
19. Elliott RB, Escobar L, Tan PLJ, Muzina M, Zwain S, et al. (2007) Live encapsulated porcine islets from a type 1 diabetic patient 9.5 yr after xenotransplantation. Xenotransplantation 14: 157-161.
20. Weinhaus AJ, Tabiin MT, Poronnik P, Palma CA, Cook DI, et al. (2003) Insulin secretagogues, but not glucose, stimulate an increase in [Ca2+]i in the fetal human and porcine beta-cell. J Clin Endocrinol Metab. 88: 2753-2759.
21. Vaithilingam V, Oberholzer J, Guillemin GJ, Tuch BE, (2010) The humanized NOD/SCID mouse as a preclinical model to study the fate of encapsulated human islets. Rev Diabet Stud. 7: 62-73.
22. Tuch BE, Tabiin MT, Casamento FM, Yao M, Georges P, et al. (2001) Role of pancreatic polypeptide as a marker of transplanted insulin-producing fetal pig cells. Cell Transplant. 10: 285-93.
23. Solomon MF, Kuziel WA, Mann DA, Simeonovic CJ, (2003) The role of chemokines and their receptors in the rejection of pig islet tissue xenografts. Xenotransplantation 10: 164-177.
24. Koulmanda M, Laufer TM, Auchincloss H, Smith RN, (2004) Prolonged survival of fetal pig islet xenografts in mice lacking the capacity for an indirect response. Xenotransplantation 11: 525-530.
25. Krook H, Hagberg A, Song Z, Landegren U, Wennberg L, et al. (2002) A Distinct Th1 Immune Response Precedes the Described Th2 Response in Islet Xenograft Rejection. Diabetes 51: 79-86.
26. Vaithilingam V, Kollarikova G, Qi M, Lacik I, Oberholzer J, et al. (2011) Effect of prolonged gelling time on the intrinsic properties of barium alginate microcapsules and its biocompatibility. J Microencapsul. 28: 499-507.
27. Siebers U, Horcher A, Brandhorst H, Brandhorst D, Hering B, et al. (1999) Analysis of the cellular reaction towards microencapsulated xenogeneic islets after intraperitoneal transplantation. J Mol Med. 77: 215-218.
28. Weber CJ, Zabinski S, Koschitzky T, Wicker L, Rajotte R, et al. (1990) The role of CD4+ helper T cells in the destruction of microencapsulated islet xenografts in nod mice. Transplantation 49: 396-404.
29. Candinas D, Belliveau S, Koyamada N, Miyatake T, Hechenleitner P, (1996) T cell independence of macrophage and natural killer cell infiltration, cytokine production, and endothelial activation during delayed xenograft rejection. Transplantation 62: 1920-1927.
30. Lin Y, Vandeputte M, Waer M, (1997) Natural killer cell- and macrophage-mediated rejection of concordant xenografts in the absence of T and B cell responses. J Immunol 158: 5658-5667.
31. Solomon MF, Kuziel WA, Mann DA, Simeonovic CJ, (2003) The role of chemokines and their receptors in the rejection of pig islet tissue xenografts. Xenotransplantation 10: 164-177.
32. Basu S, Binder RJ, Suto R, Anderson KM, Srivastava PK, (2000) Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-kappa B pathway. Int Immunol 12: 1539-1546.
33. Byrd CA, Bornmann W, Erdjument-Bromage H, Tempst P, Pavletich N, (1999) Heat shock protein 90 mediates macrophage activation by Taxol and bacterial lipopolysaccharide. Proc Natl Acad Sci 96: 5645-5650.
34. El-Ouaghlidi A, Jahr H, Pfeiffer G, Hering BJ, Brandhorst D, et al. (1999) Cytokine mRNA expression in peripheral blood cells of immuno-suppressed human islet transplant recipients. J Mol Med 77: 115-117.
35. Bottino R, Fernandez LA, Ricordi C, Lehmann R, Tsan MF, et al. (1998) Transplantation of allogeneic islets of Langerhans in the rat liver. Diabetes 47: 316-323.
36. Simeonovic CJ, Townsend MJ, Morris CF, Hapel AJ, Fung MC, et al. (1999) Immune mechanisms associated with the rejection of fetal murine proislet allografts and pig proislet xenografts: comparison of intragraft cytokine mRNA profiles. Transplantation 67: 963-971.
37. Morris CF, Simeonovic CJ, Fung MC, Wilson JD, Hapel AJ, (1995) Intragraft expression of cytokine transcripts during pig proislet xenograft rejection and tolerance in mice. J Immunol 154: 2470-2482.
38. Kovarik J, Koulmanda M, Mandel TE, (1997) The role of cytokines during rejection of foetal pig and foetal mouse pancreas grafts in nonobese diabetic mice. Transpl Immunol 5: 307-314.
39. Zamorano J, Rivas MD, Perez G, (2003) Interleukin-4: A multifunctional cytokine. Immunologia 22: 215-224.
40. Simeonovic CJ, Townsend MJ, Morris CF, Hapel AJ, Fung MC, (1999) Immune mechanisms associated with the rejection of fetal murine proislet allografts and pig proislet xenografts: comparison of intragraft cytokine mRNA profiles. Transplantation 67: 963-971.
41. Morris CF, Simeonovic CJ, Fung MC, Wilson JD, Hapel AJ, (1995) Intragraft expression of cytokine transcripts during pig proislet xenograft rejection and tolerance in mice. J Immunol. 154: 2470-2482.
42. Vilcek J, Palombella VJ, Henriksen-DeStefano D, Swenson C, Feinman R, et al. (1986) Fibroblast growth enhancing activity of tumor necrosis factor and its relationship to other polypeptide growth factors. J Exp Med 163: 632-643.
43. Amaratunga A, Tuch BE, Han XG, Georges P, Dean SK, Scott H, (2001) Secretion of pancreatic icosapeptide from porcine pancreas. Endocrinology 12: 4314-4319.
44. Bai L, Tuch BE, Hering B, Simpson AM, (2002) Fetal pig ß cells are resistant to the toxic effects of human cytokines. Transplantation 73: 714-722.
45. Cole DR, Waterfall M, McIntyre M, Baird JD, (1992) Microencapsulated islet grafts in the BB/E rat: a possible role for cytokines in graft failure. Diabetologia 35: 231-237.
46. King A, Sandler S, Andersson A, (2001) The effect of host factors and capsule composition on the cellular overgrowth on implanted alginate capsules. J Biomed Mater Res 57: 374-383.
47. Omer A, Keegan M, Czismadia E, de Vos P, van Rooijen N, et al. (2003) Macrophage depletion improves survival of porcine neonatal pancreatic cell clusters contained in alginate macrocapsules transplanted into rats. Xenotransplantation 10: 240-251.