The potential of endothelial colony-forming cells to improve early graft loss after intraportal islet transplantation

Cell Transplantation

Volumn 23, Issue 3, 2014, Pages 273-283

  Jung, Hye Seung ^a,b   Kim, Min Joo ^a   Hong, Shin Hee ^b   Lee, Ye Jin ^b   Kang, Shiane ^a   Lee, Hakmo ^b   Chung, Sung Soo ^b   Park, Joong Shin ^a   Park, Kyong Soo ^b  

^a Seoul National University College of Medicine   (South Korea)

^b Seoul National University Hospital   (South Korea)

Author keywords

Early graft loss; Endothelial colony forming cells (ECFCs); Endothelial progenitor cell; High mobility group box 1 (HMGB1); Instant blood mediated inflammatory reaction (IBMIR); Islet transplantation (ITx)

Indexed keywords

CD11B ANTIGEN; CD41A ANTIGEN; COMPLEMENT MEMBRANE ATTACK COMPLEX; FIBRINOGEN RECEPTOR; GAMMA INTERFERON; GLUCOSE; HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 12; INTERLEUKIN 1BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL VIABILITY; COCULTURE; COLONY FORMING CELL; CONTROLLED STUDY; CYTOKINE RELEASE; ENDOTHELIAL COLONY FORMING CELL; ENDOTHELIUM CELL; EXPERIMENTAL DIABETES MELLITUS; FEMALE; GLUCOSE BLOOD LEVEL; GRAFT FAILURE; HUMAN; HUMAN CELL; INFLAMMATION; LIVER; MALE; MOUSE; NONHUMAN; NUDE MOUSE; PANCREAS ISLET TRANSPLANTATION; PORTAL VEIN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHAM PROCEDURE; SWINE; UMBILICAL CORD BLOOD;

ANIMALS; BLOOD GLUCOSE; CELLS, CULTURED; COCULTURE TECHNIQUES; DIABETES MELLITUS, EXPERIMENTAL; ENDOTHELIAL CELLS; GRAFT REJECTION; HMGB1 PROTEIN; HUMANS; INFLAMMATION; ISLETS OF LANGERHANS; ISLETS OF LANGERHANS TRANSPLANTATION; MICE; MICE, NUDE; STEM CELLS; SWINE; TRANSPLANTATION, HETEROLOGOUS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84895869118     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368912X661364     Document Type: Article

References (53)

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. Basire, A.; Sabatier, F.; Ravet, S.; Lamy, E.; Mialhe, A.; Zabouo, G.; Paul, P.; Gurewich, V.; Sampol, J.; Dignat-George, F. High urokinase expression contributes to the angiogenic properties of endothelial cells derived from circulating progenitors. Thromb. Haemost. 95(4):678-688; 2006.
3. Bendelac, A.; Rivera, M. N.; Park, S. H.; Roark, J. H. Mouse CD1-specific NK1 T cells: Development, specificity, and function. Annu. Rev. Immunol. 15:535-562; 1997.
4. Berman, D. M.; Cabrera, O.; Kenyon, N. M.; Miller, J.; Tam, S. H.; Khandekar, V. S.; Picha, K. M.; Soderman, A. R.; Jordan, R. E.; Bugelski, P. J.; Horninger, D.; Lark, M.; Davis, J. E.; Alejandro, R.; Berggren, P. O.; Zimmerman, M.; O'Neil, J. J.; Ricordi, C.; Kenyon, N. S. Interference with tissue factor prolongs intrahepatic islet allograft survival in a nonhuman primate marginal mass model. Transplantation 84(3):308-315; 2007.
5. Brandhorst, D.; Brandhorst, H.; Zwolinski, A.; Nahidi, F.; Bretzel, R. G. Prevention of early islet graft failure by selective inducible nitric oxide synthase inhibitors after pig to nude rat intraportal islet transplantation. Transplantation 71(2):179-184; 2001.
6. Chen, C.; Kuehn, C.; Bretzel, R. G.; Linn, T. Antiinflammatory thalidomide improves islet grafts survival and functions in a xenogenic environment. PLoS One 4(7):e6312; 2009.
7. Contreras, J. L.; Eckstein, C.; Smyth, C. A.; Bilbao, G.; Vilatoba, M.; Ringland, S. E.; Young, C.; Thompson, J. A.; Fernandez, J. A.; Griffin, J. H.; Eckhoff, D. E. Activated protein C preserves functional islet mass after intraportal transplantation: A novel link between endothelial cell activation, thrombosis, inflammation, and islet cell death. Diabetes 53(11):2804-2814; 2004.
8. Contreras, J. L.; Smyth, C. A.; Eckstein, C.; Bilbao, G.; Thompson, J. A.; Young, C. J.; Eckhoff, D. E. Peripheral mobilization of recipient bone marrow-derived endothelial progenitor cells enhances pancreatic islet revascularization and engraftment after intraportal transplantation. Surgery 134(2):390-398; 2003.
9. Cui, W.; Wilson, J. T.; Wen, J.; Angsana, J.; Qu, Z.; Haller, C. A.; Chaikof, E. L. Thrombomodulin improves early outcomes after intraportal islet transplantation. Am. J. Transplant. 9(6):1308-1316; 2009.
10. Daculsi, R.; Remy-Zolghadri, M.; Grellier, M.; Conrad, V.; Fernandez, P.; Bareille, R.; Bordenave, L. Signal transduction and procoagulant state of human cord blood-progenitor-derived endothelial cells after interleukin-1alpha stimulation. Endothelium 14(3):163-171; 2007.
11. Gao, Q.; Ma, L. L.; Gao, X.; Yan, W.; Williams, P.; Yin, D. P. TLR4 mediates early graft failure after intraportal islet transplantation. Am. J. Transplant. 10(7):1588-1596; 2010.
12. Goto, M.; Groth, C. G.; Nilsson, B.; Korsgren, O. Intraportal pig islet xenotransplantation into athymic mice as an in vivo model for the study of the instant blood-mediated inflammatory reaction. Xenotransplantation 11(2):195-202; 2004.
13. Goto, M.; Johansson, H.; Maeda, A.; Elgue, G.; Korsgren, O.; Nilsson, B. Low molecular weight dextran sulfate prevents the instant blood-mediated inflammatory reaction induced by adult porcine islets. Transplantation 77(5):741-747; 2004.
14. 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.
15. Graham, M. L.; Bellin, M. D.; Papas, K. K.; Hering, B. J.; Schuurman, H. J. Species incompatibilities in the pig-to-macaque islet xenotransplant model affect transplant outcome: A comparison with allotransplantation. Xenotransplantation 18(6):328-342; 2011.
16. He, T.; Peterson, T. E.; Holmuhamedov, E. L.; Terzic, A.; Caplice, N. M.; Oberley, L. W.; Katusic, Z. S. Human endothelial progenitor cells tolerate oxidative stress due to intrinsically high expression of manganese superoxide dismutase. Arterioscler. Thromb. Vasc. Biol. 24(11):2021-2027; 2004.
17. Hering, B. J.; Geier, C.; Schultz, A. O.; Bretzel, R. G.; Federlin, K. International Islet Transplant Registry 5:1; 1995.
18. Hering, B. J.; Kandaswamy, R.; Ansite, J. D.; Eckman, P. M.; Nakano, M.; Sawada, T.; Matsumoto, I.; Ihm, S. H.; Zhang, H. J.; Parkey, J.; Hunter, D. W.; Sutherland, D. E. Single-donor, marginal-dose islet transplantation in patients with type 1 diabetes. JAMA 293(7):830-835; 2005.
19. Hur, J.; Yoon, C. H.; Kim, H. S.; Choi, J. H.; Kang, H. J.; Hwang, K. K.; Oh, B. H.; Lee, M. M.; Park, Y. B. Characterization of two types of endothelial progenitor cells and their different contributions to neovasculogenesis. Arterioscler. Thromb. Vasc. Biol. 24(2):288-293; 2004.
20. Johansson, H.; Lukinius, A.; Moberg, L.; Lundgren, T.; Berne, C.; Foss, A.; Felldin, M.; Kallen, R.; Salmela, K.; Tibell, A.; Tufveson, G.; Ekdahl, K. N.; Elgue, G.; Korsgren, O.; Nilsson, B. Tissue factor produced by the endocrine cells of the islets of Langerhans is associated with a negative outcome of clinical islet transplantation. Diabetes 54(6):1755-1762; 2005.
21. Johansson, U.; Elgue, G.; Nilsson, B.; Korsgren O. Composite islet-endothelial cell grafts: A novel approach to counteract innate immunity in islet transplantation. Am. J. Transplant. 5(11):2632-2639; 2005.
22. Jung, H. S.; Ahn, Y. R.; Oh, S. H.; Kim, Y. S.; No, H.; Lee, M. K.; Kim, K. W. Enhancement of beta-cell regeneration by islet transplantation after partial pancreatectomy in mice. Transplantation 88(3):354-359; 2009.
23. Jung, H. S.; Chung, K. W.; Won Kim, J.; Kim, J.; Komatsu, M.; Tanaka, K.; Nguyen, Y. H.; Kang, T. M.; Yoon, K. H.; Kim, J. W.; Jeong, Y. T.; Han, M. S.; Lee, M. K.; Kim, K. W.; Shin, J.; Lee, M. S. Loss of autophagy diminishes pancreatic beta cell mass and function with resultant hyperglycemia. Cell Metab. 8(4):318-324; 2008.
24. Kang, S.; Park, H. S.; Jo, A.; Hong, S. H.; Lee, H. N.; Lee, Y. Y.; Park, J. S.; Jung, H. S.; Chung, S. S.; Park, K. S. Endothelial progenitor cell cotransplantation enhances islet engraftment by rapid revascularization. Diabetes 61(4):866-876; 2012.
25. 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.
26. Kim, J. H.; Kim, H. I.; Lee, K. W.; Yu, J. E.; Kim, S. H.; Park, H. S.; Park, C. G.; Ihm, S. H.; Ha, J.; Kim, S. J.; Lee, H. K.; Ahn, C.; Park, K. S. 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; 2007.
27. Kim, J. H.; Oh, B. J.; Lee, H. N.; Park, H. S.; Park, S. G.; Park, K. S. Endothelial colony-forming cell coating of pig islets prevents xenogeneic instant blood-mediated inflammatory reaction. Cell Transplant. 20(11-12):1805-1815; 2011.
28. Kim, J. H.; Park, S. G.; Lee, H. N.; Lee, Y. Y.; Park, H. S.; Kim, H. I.; Yu, J. E.; Kim, S. H.; Park, C. G.; Ha, J.; Kim, S. J.; Park, K. S. ATP measurement predicts porcine islet transplantation outcome in nude mice. Transplantation 87(2):166-169; 2009.
29. Lacy, P. E.; Davie, J. M.; Finke, E.H. Prolongation of islet xenograft survival (rat to mouse). Diabetes 30(4):285-291; 1981.
30. Lau, J.; Henriksnäs, J.; Svensson, J.; Carlsson P. O. Oxygenation of islets and its role in transplantation. Curr. Opin. Organ Transplant. 14(6):688-693; 2009.
31. Linn, T.; Schneider, K.; Hammes, H. P.; Preissner, K. T.; Brandhorst, H.; Morgenstern, E.; Kiefer, F.; Bretzel, R. G. Angiogenic capacity of endothelial cells in islets of Langerhans. FASEB J. 17(8):881-883; 2003.
32. Lotze, M. T.; Tracey, K. J. High-mobility group box 1 protein (HMGB1): Nuclear weapon in the immune arsenal. Nat. Rev. Immunol. 5(4):331-342; 2005.
33. Mathews, V.; Hanson, P. T.; Ford, E.; Fujita, J.; Polonsky, K. S.; Graubert, T. A. Recruitment of bone marrow-derived endothelial cells to sites of pancreatic beta-cell injury. Diabetes 53(1):91-98; 2004.
34. Matsumoto, S. Clinical allogeneic and autologous islet cell transplantation: Update. Diabetes Metab. J. 35(3):199-206; 2011.
35. Matsuoka, N.; Itoh, T.; Watarai, H.; Sekine-Kondo, E.; Nagata, N.; Okamoto, K.; Mera, T.; Yamamoto, H.; Yamada, S.; Maruyama, I.; Taniguchi, M.; Yasunami, Y. High-mobility group box 1 is involved in the initial events of early loss of transplanted islets in mice. J. Clin. Invest. 120(3):735-743; 2010.
36. Moberg, L.; Johansson, H.; Lukinius, A.; Berne, C.; Foss, A.; Kallen, R.; Ostraat, O.; Salmela, K.; Tibell, A.; Tufveson, G.; Elgue, G.; Nilsson Ekdahl, K.; Korsgren, 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.
37. Moberg, L.; Korsgren, O.; Nilsson, B. Neutrophilic granulocytes are the predominant cell type infiltrating pancreatic islets in contact with ABO-compatible blood. Clin. Exp. Immunol. 142(1):125-131; 2005.
38. Montana, E.; Bonner-Weir, S.; Weir, G. C. Beta cell mass and growth after syngeneic islet cell transplantation in normal and streptozocin diabetic C57BL/6 mice. J. Clin. Invest. 91(3):780-787; 1993.
39. Niclauss, N.; Wojtusciszyn, A.; Morel, P.; Demuylder-Mischler, S.; Brault, C.; Parnaud, G.; Ris, F.; Bosco, D.; Badet, L.; Benhamou, P. Y.; Berney, T. Comparative impact on islet isolation and transplant outcome of the preservation solutions Institut Georges Lopez-1, University of Wisconsin, and Celsior. Transplantation 93(7):703-708; 2012.
40. Noguchi, H.; Naziruddin, B.; Jackson, A.; Shimoda, M.; Ikemoto, T.; Fujita, Y.; Chujo, D.; Takita, M.; Kobayashi, N.; Onaca, N.; Levy, M. F.; Matsumoto, S. Low-temperature preservation of isolated islets is superior to conventional islet culture before islet transplantation. Transplantation 89(1):47-54; 2010.
41. 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.
42. Padfield, G. J.; Newby, D. E.; Mills, N. L. Understanding the role of endothelial progenitor cells in percutaneous coronary intervention. J. Am. Coll. Cardiol. 55(15):1553-1565; 2010.
43. Pellicci, D. G.; Hammond, K. J.; Uldrich, A. P.; Baxter, A. G.; Smyth, M. J.; Godfrey, D. I. A natural killer T (NKT) cell developmental pathway iInvolving a thymus-dependent NK1.1(-)CD4(+) CD1d-dependent precursor stage. J. Exp. Med. 195(7):835-844; 2002.
44. Posselt, A. M.; Bellin, M. D.; Tavakol, M.; Szot, G. L.; Frassetto, L. A.; Masharani, U.; Kerlan, R. K.; Fong, L.; Vincenti, F. G.; Hering, B. J.; Bluestone, J. A.; Stock, P. G. Islet transplantation in type 1 diabetics using an immunosuppressive protocol based on the anti-LFA-1 antibody efalizumab. Am. J. Transplant. 10(8):1870-1880; 2010.
45. 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.
46. Seong, S. Y.; Matzinger, P. Hydrophobicity: An ancient damage-associated molecular pattern that initiates innate immune responses. Nat. Rev. Immunol. 4(6):469-478; 2004.
47. 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.
48. Shapiro, A. M,; Ricordi, C.; Hering, B. J.; Auchincloss, H.; Lindblad, R.; Robertson, R. P.; Secchi, A.; Brendel, M. D.; Berney, T.; Brennan, D. C.; Cagliero, E.; Alejandro, R.; Ryan, E. A.; DiMercurio, B.; Morel, P.; Polonsky, K. S.; Reems, J. A.; Bretzel, R. G.; Bertuzzi, F.; Froud, T.; Kandaswamy, R.; Sutherland, D. E.; Eisenbarth, G.; Segal, M.; Preiksaitis, J.; Korbutt, G. S.; Barton, F. B.; Viviano, L.; Seyfert-Margolis, V.; Bluestone, J.; Lakey, J. R. International trial of the Edmonton protocol for islet transplantation. N. Engl. J. Med. 355(13):1318-1330; 2006.
49. Smadja, D. M.; Bieche, I.; Uzan, G.; Bompais, H.; Muller, L.; Boisson-Vidal, C.; Vidaud, M.; Aiach, M.; Gaussem, P. PAR-1 activation on human late endothelial progenitor cells enhances angiogenesis in vitro with upregulation of the SDF-1/CXCR4 system. Arterioscler. Thromb. Vasc. Biol. 25(11):2321-2327; 2005.
50. Wijkstrom, M.; Kenyon, N. S.; Kirchhof, N.; Kenyon, N. M.; Mullon, C.; Lake, P.; Cottens, S.; Ricordi, C.; Hering, B. J. Islet allograft survival in nonhuman primates immunosuppressed with basiliximab, RAD, and FTY720. Transplantation 77(6):827-835; 2004.
51. Wu, H.; Ye, Z.; Mahato, R. I. Genetically modified mesenchymal stem cells for improved islet transplantation. Mol. Pharm. 8(5):1458-1470; 2011.
52. Yang, Z.; Chen, M.; Ellett, J. D.; Carter, J. D.; Brayman, K. L.; Nadler, J. L. Inflammatory blockade improves human pancreatic islet function and viability. Am. J. Transplant. 5(3):475-483; 2005.
53. Yoder, M. C.; Mead, L. E.; Prater, D.; Krier, T. R.; Mroueh, K. N.; Li, F.; Krasich, R.; Temm, C. J.; Prchal, J. T.; Ingram, D. A. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 109(5):1801-1809; 2007.