Early islet damage after direct exposure of pig islets to blood: Has humoral immunity been underestimated?

Cell Transplantation

Volumn 21, Issue 8, 2012, Pages 1791-1802

  van der Windt, Dirk J ^a,b   Marigliano, Marco ^a,c   He, Jing ^a   Votyakova, Tatyana V ^a   Echeverri, Gabriel J ^d,e   Ekser, Burcin ^e   Ayares, David ^f   Lakkis, Fadi G ^d,g   Cooper, David K C ^d   Trucco, Massimo ^a   Bottino, Rita ^a  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b ERASMUS MEDICAL CENTER   (Netherlands)

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

^d UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^e FUNDACIÓN VALLE DEL LILI   (Colombia)

^f REVIVICOR INC   (United States)

^g UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Antibodies; Complement activation; Humoral immunity; IBMIR; Islet xenotransplantation

Indexed keywords

C PEPTIDE; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M;

ANIMAL CELL; ARTICLE; BLOOD; BLOOD CLOTTING; CELL DAMAGE; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IN VITRO STUDY; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; SWINE;

ANIMALS; BLOOD COAGULATION; C-PEPTIDE; CELL MEMBRANE; COMPLEMENT ACTIVATION; COMPLEMENT MEMBRANE ATTACK COMPLEX; HUMANS; IMMUNITY, HUMORAL; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; ISLETS OF LANGERHANS; MITOCHONDRIA; SWINE;

SUIDAE; SUS;

EID: 84868088689     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368912X653011     Document Type: Article

References (48)

1. Akima, S.; Hawthorne, W. J.; Favaloro, E.; Patel, A.; Blyth, K.; Mudaliar, Y.; Chapman, J. R.; O'Connell, P. J. Tirofiban and activated protein C synergistically inhibit the instant blood mediated inflammatory reaction (IBMIR) from allogeneic islet cells exposure to human blood. Am. J. Transplant. 9(7):1533-1540; 2009
2. Barilla-LaBarca, M. L.; Liszewski, M. K.; Lambris, J. D.; Hourcade, D.; Atkinson, J. P. Role of membrane cofactor protein (CD46) in regulation of C4b and C3b deposited on cells. J. Immunol. 168(12):6298-6304; 2002
3. Bennet, W.; Bjorkland, A.; Sundberg, B.; Brandhorst, D.; Brendel, M. D.; Richards, A.; White, D. J.; Nilsson, B.; Groth, C. G.; Korsgren, O. Expression of complement regulatory proteins on islets of Langerhans: A comparison between human islets and islets isolated from normal and hDAF transgenic pigs. Transplantation 72(2):312-319; 2001
4. Bennet, W.; Sundberg, B.; Groth, C. G.; Brendel, M. D.; Brandhorst, D.; Brandhorst, H.; Bretzel, R. G.; Elgue, G.; Larsson, R.; Nilsson, B.; Korsgren, O. Incompatibility between human blood and isolated islets of Langerhans: A finding with implications for clinical intraportal islet transplantation? Diabetes 48(10):1907-1914; 1999
5. Bennet, W.; Sundberg, B.; Lundgren, T.; Tibell, A.; Groth, C. G.; Richards, A.; White, D. J.; Elgue, G.; Larsson, R.; Nilsson, B.; Korsgren, O. Damage to porcine islets of Langerhans after exposure to human blood in vitro, or after intraportal transplantation to cynomologus monkeys: Protective effects of sCR1 and heparin. Transplantation 69(5):711-719; 2000
6. Beuneu, C.; Vosters, O.; Ling, Z.; Pipeleers, D.; Pradier, O.; Goldman, M.; Verhasselt, V. N-acetylcysteine derivative inhibits procoagulant activity of human islet cells. Diabetologia 50(2):343-347; 2007
7. Bottino R.; Balamurugan, A. N.; Bertera, S.; Pietropaolo, M.; Trucco, M.; Piganelli, J. D. Preservation of human islet cell functional mass by anti-oxidative action of a novel SOD mimic compound. Diabetes 51(8):2561-2567; 2002
8. Bottino, R.; Balamurugan, A. N.; Smetanka, C.; Bertera, S.; He, J.; Rood, P. P.; Cooper, D. K.; Trucco, M. Isolation outcome and functional characteristics of young and adult pig pancreatic islets for transplantation studies. Xenotransplantation 14(1):74-82; 2007
9. Bottino, R.; Fernandez, L. A.; Ricordi, C.; Lehmann, R.; Tsan, M. F.; Oliver, R.; Inverardi, L. Transplantation of allogeneic islets of Langerhans in the rat liver: Effects of macrophage depletion on graft survival and microenvironment activation. Diabetes 47(3):316-323; 1998
10. Cabric, S.; Sanchez, J.; Lundgren, T.; Foss, A.; Felldin, M.; Källen, R.; Salmela, K.; Tibell, A.; Tufveson, G.; Larsson, R.; Korsgren, O.; Nilsson B. Islet surface heparinization prevents the instant blood-mediated inflammatory reaction in islet transplantation. Diabetes 56(8):2008-2015; 2007
11. Cardona, K.; Korbutt, G. S.; Milas, Z.; Lyon, J.; Cano, J.; Jiang, W.; Bello-Laborn, H.; Hacquoil, B.; Strobert, E.; Gangappa, S.; Weber, C. J.; Pearson, T. C.; Rajotte, R. V.; Larsen, C. P. Long-term survival of neonatal porcine islets in nonhuman primates by targeting costimulation pathways. Nat. Med. 12(3):304-306; 2006
12. Carlsson, P. O.; Palm, F.; Andersson, A.; Liss, P. Markedly decreased oxygen tension in transplanted rat pancreatic islets irrespective of the implantation site. Diabetes 50(3):489-495; 2001
13. Cui, W.; Angsana, J.; Wen, J.; Chaikof, E. L. Liposomal formulations of thrombomodulin increase engraftment after intraportal islet transplantation. Cell Transplant. 19(11):1359-1367; 2010
14. Dor, F. J.; Cheng J.; Alt, A.; Cooper, D. K.; Schuurman, H. J. Gal alpha 1,3Gal expression on porcine pancreatic islets, testis, spleen, and thymus. Xenotransplantation 11(1):101-106; 2004
15. Dufrane, D.; Goebbels, R. M.; Saliez, A.; Guiot, Y.; Gianello, P. Six-month survival of microencapsulated pig islets and alginate biocompatibility in primates: Proof of concept. Transplantation 81(9):1345-1353; 2006
16. Dwyer, K. M.; Mysore, T. B.; Crikis, S.; Robson, S. C.; Nandurkar, H., Cowan, P. J.; D'Apice, A. J. The transgenic expression of human CD39 on murine islets inhibits clotting of human blood. Transplantation 82(3):428-432; 2006
17. Echeverri, G. J.; McGrath, K.; Bottino, R.; Hara, H.; Dons, E. M.; van der Windt, D. J.; Ekser, B.; Casu, A.; Houser, S.; Ezzelarab, M.; Wagner, R.; Trucco, M.; Lakkis, F. G. Cooper D. K. Endoscopic gastric submucosal transplantation of islets (ENDO-STI): Technique and initial results in diabetic pigs. Am. J. Transplant. 9(11):2485-2496; 2009
18. Ekser, B.; Cooper, D. K. Overcoming the barriers to xenotransplantation: Prospects for the future. Expert Rev. Clin. Immunol. 6(2):219-230; 2010
19. Emamaullee, J. A.; Shapiro, A. M. Interventional strategies to prevent beta-cell apoptosis in islet transplantation. Diabetes 55(7):1907-1914; 2006
20. Gillissen, A.; Jaworska, M.; Orth, M.; Coffiner M.; Maes, P.; App, E. M.; Cantin, A. M.; Schultze-Werninghaus, G. Nacystelyn, a novel lysine salt of N-acetylcysteine, to augment cellular antioxidant defence in vitro. Respir. Med. 91(3):159-168; 1997
21. Gores, P. F.; Sutherland, D. E. Pancreatic islet transplantation: Is purification necessary? Am. J. Surg. 166(5):538-542; 1993
22. Goto, M.; Tjernberg, J.; Dufrane, D.; Elgue, G.; Brandhorst, D.; Ekdahl, K. N.; Brandhorst, H.; Wennberg, L.; Kurokawa, Y.; Satomi, S.; Lambris, J. D.; Gianello, P.; Korsgren, O.; Nilsson, B. Dissecting the instant blood- mediated inflammatory reaction in islet xenotransplantation. Xenotransplantation 15(4):225-234; 2008
23. + T-cells and is expressed by diabetes-suppressive dendritic cells. Diabetes 55(1):158-170; 2006
24. Hering, B. J.; Wijkstrom, M.; Graham, M. L.; Hardstedt, M.; Aasheim, T. C.; Jie, T.; Ansite, J. D.; Nakano, M.; Cheng, J.; Li, W.; Moran, K.; Christians, U.; Finnegan, C.; Mills, C. D.; Sutherland, D. E.; Bansal-Pakala, P.; Murtaugh, M. P.; Kirchhof, N.; Schuurman, H. J. Prolonged diabetes reversal after intraportal xenotransplantation of wild-type porcine islets in immunosuppressed nonhuman primates. Nat. Med. 12(3):301-303; 2006
25. Ichii, H.; Inverardi, L.; Pileggi, A.; Molano, R. D.; Cabrera, O.; Caicedo, A.; Messinger, S.; Kuroda, Y.; Berggren, P. O.; Ricordi, C. A novel method for the assessment of cellular composition and beta-cell viability in human islet preparations. Am. J. Transplant. 5(7):1635-1645; 2005
26. Johansson, H.; Goto, M.; Dufrane, D.; Siegbahn, A.; Elgue, G.; Gianello, P.; Korsgren, O.; Nilsson, B. Low molecular weight dextran sulfate: A strong candidate drug to block IBMIR in clinical islet transplantation. Am. J. Transplant. 6(2):305-312; 2006
27. Johnson, J. D.; Ao, Z.; Ao, P.; Li, H.; Dai, L. J.; He, Z.; Tee, M.; Potter, K. J.; Klimek, A. M.; Meloche, R. M.; Thompson, D. M.; Verchere, C. B.; Warnock, G. L. Different effects of FK506, rapamycin, and mycophenolate mofetil on glucose-stimulated insulin release and apoptosis in human islets. Cell Transplant. 18(8):833-845; 2009
28. Kim, H. I.; Yu, J. E.; Lee, S. Y.; Sul, A. Y.; Jang, M. S.; Rashid, M. A.; Park, S. G.; Kim, S. J.; Park, C. G.; Kim, J. H.; Park, K. S. The effect of composite pig islet-human endothelial cell grafts on the instant blood-mediated inflammatory reaction. Cell Transplant. 18(1):31-37; 2009
29. Korsgren, O.; Nilsson, B.; Berne, C.; Felldin, M.; Foss, A.; Kallen, R.; Lundgren, T.; Salmela, K.; Tibell, A.; Tufveson, G. Current status of clinical islet transplantation. Transplantation 79(10):1289-1293; 2005
30. Latif, Z. A.; Noel, J.; Alejandro, R. A simple method of staining fresh and cultured islets. Transplantation 45(4):827-830; 1988
31. Loveland, B. E.; Milland, J.; Kyriakou, P.; Thorley, B. R.; Christiansen, D.; Lanteri, M. B.; Regensburg, M.; Duffield, M.; French, A. J.; Williams, L.; Baker, L.; Brandon, M. R.; Xing, P. X.; Kahn, D.; McKenzie, I. F. Characterization of a CD46 transgenic pig and protection of transgenic kidneys against hyperacute rejection in non-immunosuppressed baboons. Xenotransplantation 11(2):171-183; 2004
32. Makrides, S. C. Therapeutic inhibition of the complement system. Pharmacol. Rev. 50(1):59-87; 1998
33. Meri, S.; Pangburn, M. K. Discrimination between activators and nonactivators of the alternative pathway of complement: Regulation via a sialic acid/polyanion binding site on factor H. Proc. Natl. Acad. Sci. USA 87(10):3982-3986; 1990
34. Moberg, L.; Johansson, H.; Lukinius, A.; Berne, C.; Foss, A.; Källen, R.; Østraat, Ø.; Salmela, K.; Tibell, A.; Tufvenson, G.; Elgue, G.; Nilsson Ekdahl, K.; Korgren, O.; Nilsson, B. Production of tissue factor by pancreatic islet cells as a trigger of detrimental thrombotic reactions in clinical islet transplantation. Lancet 360(9350):2039-2045; 2002
35. Mollnes, T. E.; Brekke, O. L.; Fung, M.; Fure, H.; Christiansen, D.; Bergseth, G.; Videm, V.; Lappegård, K. T.; Köhl, J.; Lambris, J. D. Essential role of the C5a receptor in E. coli-induced oxidative burst and phagocytosis revealed by a novel lepirudin-based human whole blood model of inflammation. Blood 100(5):1869-1877; 2002
36. Nilsson, B.; Larsson, R.; Hong, J.; Elgue, G.; Ekdahl, K. N.; Sahu, A.; Lambris, J. D. Compstatin inhibits complement and cellular activation in whole blood in two models of extracorporeal circulation. Blood 92(5):1661-1667; 1998
37. Ozmen, L.; Ekdahl, K. N.; Elgue, G.; Larsson, R.; Korsgren, O.; Nilsson B. Inhibition of thrombin abrogates the instant blood-mediated inflammatory reaction triggered by isolated human islets: Possible application of the thrombin inhibitor melagatran in clinical islet transplantation. Diabetes 51(6):1779-1784; 2002
38. Phelps, C.; Vaught, T.; Ball, S.; Mendicino, M.; Walters, A.; Monahan, J.; Cooper, D. K.; Ayares, D. Multi-transgenic pigs designed for xenoislet transplants. Xenotransplantation 16(5):374; 2009
39. Ricklin, D.; Lambris, J. D. Compstatin: A complement inhibitor on its way to clinical application. Adv. Exp. Med. Biol. 632:273-292; 2008
40. Ricordi, C.; Lacy, P. E.; Finke, E. H.; Olack, B. J.; Scharp, D. W. Automated method for isolation of human pancreatic islets. Diabetes 37(4):413-420; 1988
41. Rood, P. P.; Bottino, R.; Balamurugan, A. N.; Smetanka, C.; Ayares, D.; Groth, C. G.; Murase, N.; Cooper, D. K.; Trucco, M. Reduction of early graft loss after intraportal porcine islet transplantation in monkeys. Transplantation 83(2):202-210; 2007
42. Shapiro, A. M.; Lakey, J. R.; Ryan E. A; Korbutt, G. S.; Toth, E.; Warnock, G. L.; Kneteman, N. M.; Rajotte R. V. Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen. N. Engl. J. Med. 343(4):230-238; 2000
43. Teramura, Y.; Iwata, H. Surface modification of islets with PEG-lipid for improvement of graft survival in intraportal transplantation. Transplantation 88(5):624-630; 2009
44. Tjernberg, J.; Ekdahl, K. N.; Lambris, J. D.; Korsgren, O.; Nilsson, B. Acute antibody-mediated complement activation mediates lysis of pancreatic islets cells and may cause tissue loss in clinical islet transplantation. Transplantation 85(8):1193-1199; 2008
45. van der Windt, D. J.; Bottino, R.; Casu, A.; Campanile, N.; Cooper, D. K. Rapid loss of intraportally transplanted islets: An overview of pathophysiology and preventive strategies. Xenotransplantation 14(4): 288-297; 2007
46. van der Windt, D. J.; Bottino, R.; Casu, A.; Campanile, N.; Smetanka, C.; He, J.; Murase, N.; Hara, H.; Ball, S.; Loveland, B. E.; Ayares, D.; Lakkis, F. G.; Cooper, D. K.; Trucco, M. Long-term controlled normoglycemia in diabetic nonhuman primates after transplantation with hCD46 transgenic porcine islets. Am. J. Transplant. 9(12):2716-2726; 2009
47. van der Windt, D. J.; Echeverri, G. J.; Ijzermans, J. N.; Cooper, D. K. The choice of anatomical site for islet transplantation. Cell Transplant. 17(9):1005-1014; 2008
48. Zhang, Y.; Shumilina, E.; Häring, H-U.; Lang, F. Ullrich, S. Epinephrine-induced hyperpolarization of pancreatic islet cells is sensitive to PI3K-PDK1 signaling. FEBS Lett. 583:3101-3106; 2009.