Tolerance induction and reversal of diabetes in mice transplanted with human embryonic stem cell-derived pancreatic endoderm

Cell Stem Cell

Volumn 16, Issue 2, 2015, Pages 148-157

  Szot, Gregory L ^a   Yadav, Mahesh ^a   Lang, Jiena ^a   Kroon, Evert ^b   Kerr, Justin ^b   Kadoya, Kuniko ^b   Brandon, Eugene P ^b   Baetge, Emmanuel E ^b   Bour Jordan, Hélène ^a   Bluestone, Jeffrey A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Georgia Biobusiness Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABATACEPT; GLUCAGON; GLUCOSE; HUMAN INSULIN; SOMATOSTATIN;

ANIMAL EXPERIMENT; ARTICLE; EMBRYONIC STEM CELL; EMBRYONIC STEM CELL DERIVED PANCREATIC ENDODERM TRANSPLANTATION; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN CELL; IMMUNOGENICITY; IMMUNOTHERAPY; IN VIVO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; STEM CELL TRANSPLANTATION; T LYMPHOCYTE; ANIMAL; CYTOLOGY; DIABETES MELLITUS, TYPE 1; ENDODERM; HUMAN EMBRYONIC STEM CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; KNOCKOUT MOUSE; NONOBESE DIABETIC MOUSE; PANCREAS; PATHOLOGY; SCID MOUSE; TRANSPLANTATION; XENOGRAFT;

MUS;

ANIMALS; DIABETES MELLITUS, TYPE 1; ENDODERM; HUMAN EMBRYONIC STEM CELLS; HUMANS; IMMUNE TOLERANCE; MICE; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; PANCREAS; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION, HETEROLOGOUS;

EID: 84924977469     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2014.12.001     Document Type: Article

References (59)

1. A.B. Adams, N. Shirasugi, T.R. Jones, M.M. Durham, E.A. Strobert, S. Cowan, P. Rees, R. Hendrix, K. Price, and N.S. Kenyon Development of a chimeric anti-CD40 monoclonal antibody that synergizes with LEA29Y to prolong islet allograft survival J. Immunol. 174 2005 542 550
2. H. Arefanian, E.B. Tredget, R.V. Rajotte, R.G. Gill, G.S. Korbutt, and G.R. Rayat Short-term administrations of a combination of anti-LFA-1 and anti-CD154 monoclonal antibodies induce tolerance to neonatal porcine islet xenografts in mice Diabetes 59 2010 958 966
3. F.B. Barton, M.R. Rickels, R. Alejandro, B.J. Hering, S. Wease, B. Naziruddin, J. Oberholzer, J.S. Odorico, M.R. Garfinkel, and M. Levy Improvement in outcomes of clinical islet transplantation: 1999-2010 Diabetes Care 35 2012 1436 1445
4. M.D. Bellin, F.B. Barton, A. Heitman, J.V. Harmon, R. Kandaswamy, A.N. Balamurugan, D.E. Sutherland, R. Alejandro, and B.J. Hering Potent induction immunotherapy promotes long-term insulin independence after islet transplantation in type 1 diabetes Am. J. Transplant. 12 2012 1576 1583
5. B. Benda, H.G. Ljunggren, R. Peach, J.O. Sandberg, and O. Korsgren Co-stimulatory molecules in islet xenotransplantation: CTLA4Ig treatment in CD40 ligand-deficient mice Cell Transplant. 11 2002 715 720
6. J.A. Bluestone, K. Herold, and G. Eisenbarth Genetics, pathogenesis and clinical interventions in type 1 diabetes Nature 464 2010 1293 1300
7. L. Chatenoud Chemical immunosuppression in islet transplantation-friend or foe? N. Engl. J. Med. 358 2008 1192 1193
8. K.A. D'Amour, A.D. Agulnick, S. Eliazer, O.G. Kelly, E. Kroon, and E.E. Baetge Efficient differentiation of human embryonic stem cells to definitive endoderm Nat. Biotechnol. 23 2005 1534 1541
9. K.A. D'Amour, A.G. Bang, S. Eliazer, O.G. Kelly, A.D. Agulnick, N.G. Smart, M.A. Moorman, E. Kroon, M.K. Carpenter, and E.E. Baetge Production of pancreatic hormone-expressing endocrine cells from human embryonic stem cells Nat. Biotechnol. 24 2006 1392 1401
10. P.E. de Almeida, J.D. Ransohoff, A. Nahid, and J.C. Wu Immunogenicity of pluripotent stem cells and their derivatives Circ. Res. 112 2013 549 561
11. T. Deuse, M. Seifert, N. Phillips, A. Fire, D. Tyan, M. Kay, P.S. Tsao, X. Hua, J. Velden, and T. Eiermann Human leukocyte antigen I knockdown human embryonic stem cells induce host ignorance and achieve prolonged xenogeneic survival Circulation 124 2011 S3 S9
12. T. Deuse, M. Seifert, D. Tyan, P.S. Tsao, X. Hua, J. Velden, T. Eiermann, H.D. Volk, H. Reichenspurner, R.C. Robbins, and S. Schrepfer Immunobiology of naïve and genetically modified HLA-class-I-knockdown human embryonic stem cells J. Cell Sci. 124 2011 3029 3037
13. R. Dressel, J. Nolte, L. Elsner, P. Novota, K. Guan, K. Streckfuss-Bömeke, G. Hasenfuss, R. Jaenisch, and W. Engel Pluripotent stem cells are highly susceptible targets for syngeneic, allogeneic, and xenogeneic natural killer cells FASEB J. 24 2010 2164 2177
14. M. Drukker, H. Katchman, G. Katz, S. Even-Tov Friedman, E. Shezen, E. Hornstein, O. Mandelboim, Y. Reisner, and N. Benvenisty Human embryonic stem cells and their differentiated derivatives are less susceptible to immune rejection than adult cells Stem Cells 24 2006 221 229
15. A. Eshpeter, J. Jiang, M. Au, R.V. Rajotte, K. Lu, J.S. Lebkowski, A.S. Majumdar, and G.S. Korbutt In vivo characterization of transplanted human embryonic stem cell-derived pancreatic endocrine islet cells Cell Prolif. 41 2008 843 858
16. B.T. Fife, and J.A. Bluestone Control of peripheral T-cell tolerance and autoimmunity via the CTLA-4 and PD-1 pathways Immunol. Rev. 224 2008 166 182
17. L.P. Frenzel, Z. Abdullah, A.K. Kriegeskorte, R. Dieterich, N. Lange, D.H. Busch, M. Krönke, O. Utermöhlen, J. Hescheler, and T. Sarić Role of natural-killer group 2 member D ligands and intercellular adhesion molecule 1 in natural killer cell-mediated lysis of murine embryonic stem cells and embryonic stem cell-derived cardiomyocytes Stem Cells 27 2009 307 316
18. K.H. Grinnemo, R. Genead, M. Kumagai-Braesch, A. Andersson, C. Danielsson, A. Månsson-Broberg, G. Dellgren, A.M. Strömberg, H. Ekberg, and O. Hovatta Costimulation blockade induces tolerance to HESC transplanted to the testis and induces regulatory T-cells to HESC transplanted into the heart Stem Cells 26 2008 1850 1857
19. M.D. Hazenberg, and H. Spits Human innate lymphoid cells Blood 124 2014 700 709
20. M. Hebrok Generating β cells from stem cells-the story so far Cold Spring Harb. Perspect. Med. 2 2012 a007674
21. S.J. Holditch, A. Terzic, and Y. Ikeda Concise review: pluripotent stem cell-based regenerative applications for failing β-cell function Stem Cells Transl. Med. 3 2014 653 661
22. M. Hosokawa, W. Dolci, and B. Thorens Differential sensitivity of GLUT1-and GLUT2-expressing beta cells to streptozotocin Biochem. Biophys. Res. Commun. 289 2001 1114 1117
23. B.C. Huber, J.D. Ransohoff, K.J. Ransohoff, J. Riegler, A. Ebert, K. Kodo, Y. Gong, V. Sanchez-Freire, D. Dey, and N.G. Kooreman Costimulation-adhesion blockade is superior to cyclosporine A and prednisone immunosuppressive therapy for preventing rejection of differentiated human embryonic stem cells following transplantation Stem Cells 31 2013 2354 2363
24. J. Jiang, M. Au, K. Lu, A. Eshpeter, G. Korbutt, G. Fisk, and A.S. Majumdar Generation of insulin-producing islet-like clusters from human embryonic stem cells Stem Cells 25 2007 1940 1953
25. T. Kanmaz, J.J. Fechner Jr., J. Torrealba, H.T. Kim, Y. Dong, T.D. Oberley, J.M. Schultz, D.D. Bloom, M. Katayama, and W. Dar Monotherapy with the novel human anti-CD154 monoclonal antibody ABI793 in rhesus monkey renal transplantation model Transplantation 77 2004 914 920
26. N.S. Kenyon, L.A. Fernandez, R. Lehmann, M. Masetti, A. Ranuncoli, M. Chatzipetrou, G. Iaria, D. Han, J.L. Wagner, and P. Ruiz Long-term survival and function of intrahepatic islet allografts in baboons treated with humanized anti-CD154 Diabetes 48 1999 1473 1481
27. E.S. Kilpatrick, A.S. Rigby, and S.L. Atkin The Diabetes Control and Complications Trial: the gift that keeps giving Nat. Rev. Endocrinol. 5 2009 537 545
28. E. Kroon, L.A. Martinson, K. Kadoya, A.G. Bang, O.G. Kelly, S. Eliazer, H. Young, M. Richardson, N.G. Smart, and J. Cunningham Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo Nat. Biotechnol. 26 2008 443 452
29. D.J. Lenschow, Y. Zeng, J.R. Thistlethwaite, A. Montag, W. Brady, M.G. Gibson, P.S. Linsley, and J.A. Bluestone Long-term survival of xenogeneic pancreatic islet grafts induced by CTLA4lg Science 257 1992 789 792
30. M.G. Levisetti, P.A. Padrid, G.L. Szot, N. Mittal, S.M. Meehan, C.L. Wardrip, G.S. Gray, D.S. Bruce, J.R. Thistlethwaite Jr., and J.A. Bluestone Immunosuppressive effects of human CTLA4Ig in a non-human primate model of allogeneic pancreatic islet transplantation J. Immunol. 159 1997 5187 5191
31. L. Li, M.L. Baroja, A. Majumdar, K. Chadwick, A. Rouleau, L. Gallacher, I. Ferber, J. Lebkowski, T. Martin, J. Madrenas, and M. Bhatia Human embryonic stem cells possess immune-privileged properties Stem Cells 22 2004 448 456
32. K. Ljung, O.E. Simonson, U. Felldin, E. Wärdell, C. Ibarra, L. Antonsson, M. Kumagai-Braesch, O. Hovatta, R. Lampela, K.H. Grinnemo, and M. Corbascio Costimulation blockade induces foxp3(+) regulatory T cells to human embryonic stem cells Biores. Open Access 2 2013 455 458
33. K.O. Lui, A.S. Boyd, S.P. Cobbold, H. Waldmann, and P.J. Fairchild A role for regulatory T cells in acceptance of ESC-derived tissues transplanted across an major histocompatibility complex barrier Stem Cells 28 2010 1905 1914
34. M. Ma, S. Ding, A. Lundqvist, H. San, F. Fang, M. Konoplyannikov, C. Berry, L.E. Beltran, G. Chen, J.C. Kovacic, and M. Boehm Major histocompatibility complex-I expression on embryonic stem cell-derived vascular progenitor cells is critical for syngeneic transplant survival Stem Cells 28 2010 1465 1475
35. R. Maehr, S. Chen, M. Snitow, T. Ludwig, L. Yagasaki, R. Goland, R.L. Leibel, and D.A. Melton Generation of pluripotent stem cells from patients with type 1 diabetes Proc. Natl. Acad. Sci. USA 106 2009 15768 15773
36. J.F. Magliocca, I.K. Held, and J.S. Odorico Undifferentiated murine embryonic stem cells cannot induce portal tolerance but may possess immune privilege secondary to reduced major histocompatibility complex antigen expression Stem Cells Dev. 15 2006 707 717
37. J. Nussbaum, E. Minami, M.A. Laflamme, J.A. Virag, C.B. Ware, A. Masino, V. Muskheli, L. Pabon, H. Reinecke, and C.E. Murry Transplantation of undifferentiated murine embryonic stem cells in the heart: teratoma formation and immune response FASEB J. 21 2007 1345 1357
38. F.W. Pagliuca, J.R. Millman, M. Gürtler, M. Segel, A. Van Dervort, J.H. Ryu, Q.P. Peterson, D. Greiner, and D.A. Melton Generation of functional human pancreatic β cells in vitro Cell 159 2014 428 439
39. J.I. Pearl, A.S. Lee, D.B. Leveson-Gower, N. Sun, Z. Ghosh, F. Lan, J. Ransohoff, R.S. Negrin, M.M. Davis, and J.C. Wu Short-term immunosuppression promotes engraftment of embryonic and induced pluripotent stem cells Cell Stem Cell 8 2011 309 317
40. A.M. Posselt, M.D. Bellin, M. Tavakol, G.L. Szot, L.A. Frassetto, U. Masharani, R.K. Kerlan, L. Fong, F.G. Vincenti, and B.J. Hering Islet transplantation in type 1 diabetics using an immunosuppressive protocol based on the anti-LFA-1 antibody efalizumab Am. J. Transplant. 10 2010 1870 1880
41. A.M. Posselt, G.L. Szot, L.A. Frassetto, U. Masharani, M. Tavakol, R. Amin, J. McElroy, M.D. Ramos, R.K. Kerlan, and L. Fong Islet transplantation in type 1 diabetic patients using calcineurin inhibitor-free immunosuppressive protocols based on T-cell adhesion or costimulation blockade Transplantation 90 2010 1595 1601
42. A. Rezania, J.E. Bruin, M.J. Riedel, M. Mojibian, A. Asadi, J. Xu, R. Gauvin, K. Narayan, F. Karanu, and J.J. O'Neil Maturation of human embryonic stem cell-derived pancreatic progenitors into functional islets capable of treating pre-existing diabetes in mice Diabetes 61 2012 2016 2029
43. A. Rezania, J.E. Bruin, P. Arora, A. Rubin, I. Batushansky, A. Asadi, S. O'Dwyer, N. Quiskamp, M. Mojibian, and T. Albrecht Reversal of diabetes with insulin-producing cells derived in vitro from human pluripotent stem cells Nat. Biotechnol. 32 2014 1121 1133
44. N.J. Robertson, F.A. Brook, R.L. Gardner, S.P. Cobbold, H. Waldmann, and P.J. Fairchild Embryonic stem cell-derived tissues are immunogenic but their inherent immune privilege promotes the induction of tolerance Proc. Natl. Acad. Sci. USA 104 2007 20920 20925
45. Z. Rong, M. Wang, Z. Hu, M. Stradner, S. Zhu, H. Kong, H. Yi, A. Goldrath, Y.G. Yang, Y. Xu, and X. Fu An effective approach to prevent immune rejection of human ESC-derived allografts Cell Stem Cell 14 2014 121 130
46. B. Salomon, and J.A. Bluestone Complexities of CD28/B7: CTLA-4 costimulatory pathways in autoimmunity and transplantation Annu. Rev. Immunol. 19 2001 225 252
47. T.C. Schulz, H.Y. Young, A.D. Agulnick, M.J. Babin, E.E. Baetge, A.G. Bang, A. Bhoumik, I. Cepa, R.M. Cesario, and C. Haakmeester A scalable system for production of functional pancreatic progenitors from human embryonic stem cells PLoS ONE 7 2012 e37004
48. A.M.J. Shapiro, and C. Ricordi Long-term Outcomes after Islet Transplantation A. Kirk, Textbook of Organ Transplantation 2014 John Wiley & Sons, Ltd Chichester, West Sussex, UK 1314 1333
49. A.M. Shapiro, J.R. Lakey, E.A. Ryan, G.S. Korbutt, E. Toth, G.L. Warnock, N.M. Kneteman, and R.V. Rajotte Islet transplantation in seven patients with type 1 diabetes mellitus using a glucocorticoid-free immunosuppressive regimen N. Engl. J. Med. 343 2000 230 238
50. L.D. Shultz, M.A. Brehm, J.V. Garcia-Martinez, and D.L. Greiner Humanized mice for immune system investigation: progress, promise and challenges Nat. Rev. Immunol. 12 2012 786 798
51. R.J. Swijnenburg, S. Schrepfer, J.A. Govaert, F. Cao, K. Ransohoff, A.Y. Sheikh, M. Haddad, A.J. Connolly, M.M. Davis, R.C. Robbins, and J.C. Wu Immunosuppressive therapy mitigates immunological rejection of human embryonic stem cell xenografts Proc. Natl. Acad. Sci. USA 105 2008 12991 12996
52. G.L. Szot, P. Koudria, and J.A. Bluestone Transplantation of pancreatic islets into the kidney capsule of diabetic mice J. Vis. Exp. 9 2007 404
53. Q. Tang, J.A. Bluestone, and S.M. Kang CD4(+)Foxp3(+) regulatory T cell therapy in transplantation J. Mol. Cell Biol. 4 2012 11 21
54. T. Thatava, Y.C. Kudva, R. Edukulla, K. Squillace, J.G. De Lamo, Y.K. Khan, T. Sakuma, S. Ohmine, A. Terzic, and Y. Ikeda Intrapatient variations in type 1 diabetes-specific iPS cell differentiation into insulin-producing cells Mol. Ther. 21 2013 228 239
55. P. Thompson, K. Cardona, M. Russell, I.R. Badell, V. Shaffer, G. Korbutt, G.R. Rayat, J. Cano, M. Song, and W. Jiang CD40-specific costimulation blockade enhances neonatal porcine islet survival in nonhuman primates Am. J. Transplant. 11 2011 947 957
56. J.L. Tiwari, B. Schneider, F. Barton, and S.A. Anderson Islet cell transplantation in type 1 diabetes: an analysis of efficacy outcomes and considerations for trial designs Am. J. Transplant. 12 2012 1898 1907
57. D. Van Hoof, K.A. D'Amour, and M.S. German Derivation of insulin-producing cells from human embryonic stem cells Stem Cell Res. (Amst.) 3 2009 73 87
58. F. Vendrame, A. Pileggi, E. Laughlin, G. Allende, A. Martin-Pagola, R.D. Molano, S. Diamantopoulos, N. Standifer, K. Geubtner, and B.A. Falk Recurrence of type 1 diabetes after simultaneous pancreas-kidney transplantation, despite immunosuppression, is associated with autoantibodies and pathogenic autoreactive CD4 T-cells Diabetes 59 2010 947 957
59. D.C. Wu, J. Hester, S.N. Nadig, W. Zhang, P. Trzonkowski, D. Gray, S. Hughes, P. Johnson, and K.J. Wood Ex vivo expanded human regulatory T cells can prolong survival of a human islet allograft in a humanized mouse model Transplantation 96 2013 707 716