Tolerance induction to human stem cell transplants with extension to their differentiated progeny

Nature Communications

Volumn 5, Issue , 2014, Pages

  Lui, Kathy O ^a,b,c   Howie, Duncan ^a   Ng, Shu Wing ^d   Liu, Shubai ^d   Chien, Kenneth R ^c,e   Waldmann, Herman ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Harvard University   (United States)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIBODY; CD40 LIGAND MONOCLONAL ANTIBODY; CD8 ANTIBODY; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; ANTIGEN;

ANTIGEN; GENE EXPRESSION; GENETIC DIFFERENTIATION; GERM CELL; IMMUNE RESPONSE; IMMUNE SYSTEM; TOLERANCE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY SPECIFICITY; ANTIGEN ANTIBODY REACTION; ANTIGEN EXPRESSION; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENGRAFTMENT; GENE EXPRESSION PROFILING; GRAFT RECIPIENT; GRAFT REJECTION; GRAFT SURVIVAL; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPHOCYTE DIFFERENTIATION; MALE; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PROGENY; STEM CELL TRANSPLANTATION; T LYMPHOCYTE; TRANSPLANTATION TOLERANCE; ALLOTRANSPLANTATION; ANIMAL; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; TRANSPLANTATION; XENOGRAFT;

MURINAE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; HUMANS; IMMUNE TOLERANCE; INDUCED PLURIPOTENT STEM CELLS; MICE; STEM CELL TRANSPLANTATION; T-LYMPHOCYTES; TRANSPLANTATION TOLERANCE; TRANSPLANTATION, HETEROLOGOUS; TRANSPLANTATION, HOMOLOGOUS;

EID: 84922666459     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6629     Document Type: Article

References (44)

1. Takebe, T. et al. Vascularized and functional human liver from an iPSC-derived organ bud transplant. Nature 499, 481-484 (2013).
2. Araki, R. et al. Negligible immunogenicity of terminally differentiated cells derived from induced pluripotent or embryonic stem cells. Nature 494, 100-104 (2013).
3. Zhao, T., Zhang, Z. N., Rong, Z. & Xu, Y. Immunogenicity of induced pluripotent stem cells. Nature 474, 212-215 (2011).
4. Lebkowski, J. GRNOPC1: the world's first embryonic stem cell-derived therapy. Interview with Jane Lebkowski. Regen. Med. 6, 11-13 (2011).
5. Schwartz, S. D. et al. Embryonic stem cell trials for macular degeneration: a preliminary report. Lancet 379, 713-720 (2012).
6. Lomax, G. P., Hall, Z. W. & Lo, B. Responsible oversight of human stem cell research: the California Institute for Regenerative Medicine's medical and ethical standards. PLoS Med. 4, e114 (2007).
7. Lui, K. O., Boyd, A. S., Cobbold, S. P., Waldmann, H. & Fairchild, P. J. A role for regulatory T cells in acceptance of ESC-derived tissues transplanted across an major histocompatibility complex barrier. Stem Cells 28, 1905-1914 (2010).
8. Robertson, N. J. et al. Embryonic stem cell-derived tissues are immunogenic but their inherent immune privilege promotes the induction of tolerance. Proc. Natl Acad. Sci. USA 104, 20920-20925 (2007).
9. Waldmann, H., Hilbrands, R., Howie, D. & Cobbold, S. Harnessing FOXP3\+ regulatory T cells for transplantation tolerance. J. Clin. Invest. 124, 1439-1445 (2014).
10. Preynat-Seauve, O. et al. Neural progenitors derived from human embryonic stem cells are targeted by allogeneic T and natural killer cells. J. Cell. Mol. Med. 13, 3556-3569 (2009).
11. Cobbold, S. P. et al. Infectious tolerance via the consumption of essential amino acids and mTOR signaling. Proc. Natl Acad. Sci. USA 106, 12055-12060 (2009).
12. Davies, J. D., Leong, L. Y., Mellor, A., Cobbold, S. P. & Waldmann, H. T cell suppression in transplantation tolerance through linked recognition. J. Immunol. 156, 3602-3607 (1996).
13. Kendal, A. R. et al. Sustained suppression by Foxp3\+ regulatory T cells is vital for infectious transplantation tolerance. J. Exp. Med. 208, 2043-2053 (2011).
14. Qin, S. et al. "Infectious" transplantation tolerance. Science 259, 974-977 (1993).
15. Pearl, J. I. et al. Short-term immunosuppression promotes engraftment of embryonic and induced pluripotent stem cells. Cell Stem Cell 8, 309-317 (2011).
16. Ljung, K. et al. Costimulation blockade induces foxp3(\+) regulatory T cells to human embryonic stem cells. Biores. Open Access 2, 455-458 (2013).
17. Honey, K., Cobbold, S. P. & Waldmann, H. CD40 ligand blockade induces CD4\+ T cell tolerance and linked suppression. J. Immunol. 163, 4805-4810 (1999).
18. Cho, E. G. et al. MEF2C enhances dopaminergic neuron differentiation of human embryonic stem cells in a parkinsonian rat model. PLoS ONE 6, e24027 (2011).
19. Lui, K. O. et al. Driving vascular endothelial cell fate of human multipotent Isl1\+ heart progenitors with VEGF modified mRNA. Cell Res. 23, 1172-1186 (2013).
20. Graca, L., Cobbold, S. P. & Waldmann, H. Identification of regulatory T cells in tolerated allografts. J. Exp. Med. 195, 1641-1646 (2002).
21. Cobbold, S. P. et al. Induction of foxP3\+ regulatory T cells in the periphery of T cell receptor transgenic mice tolerized to transplants. J. Immunol. 172, 6003-6010 (2004).
22. Safford, M. et al. Egr-2 and Egr-3 are negative regulators of T cell activation. Nat. Immunol. 6, 472-480 (2005).
23. Arpaia, N. et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 504, 451-455 (2013).
24. Burzyn, D. et al. A special population of regulatory T cells potentiates muscle repair. Cell 155, 1282-1295 (2013).
25. von Boehmer, H. & Daniel, C. Therapeutic opportunities for manipulating T(Reg) cells in autoimmunity and cancer. Nat. Rev. Drug Discov. 12, 51-63 (2013).
26. Lui, K. O., Waldmann, H. & Fairchild, P. J. Embryonic stem cells: overcoming the immunological barriers to cell replacement therapy. Curr. Stem Cell Res. Ther. 4, 70-80 (2009).
27. Si-Tayeb, K. et al. Highly efficient generation of human hepatocyte-like cells from induced pluripotent stem cells. Hepatology 51, 297-305 (2010).
28. Holderfield, M. T. & Hughes, C. C. Crosstalk between vascular endothelial growth factor, notch, and transforming growth factor-beta in vascular morphogenesis. Circ. Res. 102, 637-652 (2008).
29. James, D. et al. Expansion and maintenance of human embryonic stem cell-derived endothelial cells by TGFbeta inhibition is Id1 dependent. Nat. Biotechnol. 28, 161-166 (2010).
30. Wise, M. P., Bemelman, F., Cobbold, S. P. & Waldmann, H. Linked suppression of skin graft rejection can operate through indirect recognition. J. Immunol. 161, 5813-5816 (1998).
31. Regateiro, F. S. et al. Foxp3 expression is required for the induction of therapeutic tissue tolerance. J. Immunol. 189, 3947-3956 (2012).
32. Daley, S. R., Ma, J., Adams, E., Cobbold, S. P. & Waldmann, H. A key role for TGF-beta signaling to T cells in the long-term acceptance of allografts. J. Immunol. 179, 3648-3654 (2007).
33. Scully, R., Qin, S., Cobbold, S. & Waldmann, H. Mechanisms in CD4 antibodymediated transplantation tolerance: kinetics of induction, antigen dependency and role of regulatory T cells. Eur. J. Immunol. 24, 2383-2392 (1994).
34. Kim, J. M., Rasmussen, J. P. & Rudensky, A. Y. Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat. Immunol. 8, 191-197 (2007).
35. Qin, S. X. et al. Induction of tolerance in peripheral T cells with monoclonal antibodies. Eur. J. Immunol. 20, 2737-2745 (1990).
36. Chen, Z., Cobbold, S., Metcalfe, S. & Waldmann, H. Tolerance in the mouse to major histocompatibility complex-mismatched heart allografts, and to rat heart xenografts, using monoclonal antibodies to CD4 and CD8. Eur. J. Immunol. 22, 805-810 (1992).
37. Sachs, D. H., Kawai, T. & Sykes, M. Induction of tolerance through mixed chimerism. Cold Spring Harb. Perspect. Med. 4, a015529 (2014).
38. Piotti, G., Ma, J., Adams, E., Cobbold, S. & Waldmann, H. Guiding postablative lymphocyte reconstitution as a route toward transplantation tolerance. Am. J. Transplant. 14, 1678-1689 (2014).
39. Kirk, A. D. et al. Renal transplantation using belatacept without maintenance steroids or calcineurin inhibitors. Am. J. Transplant. 14, 1142-1151 (2014).
40. Adini, A. et al. Matrigel cytometry: a novel method for quantifying angiogenesis in vivo. J. Immunol. Methods 342, 78-81 (2009).
41. Noelle, R. J. et al. A 39-kDa protein on activated helper T cells binds CD40 and transduces the signal for cognate activation of B cells. Proc. Natl Acad. Sci. USA 89, 6550-6554 (1992).
42. Qin, S. X., Cobbold, S., Benjamin, R. & Waldmann, H. Induction of classical transplantation tolerance in the adult. J. Exp. Med. 169, 779-794 (1989).
43. Mootha, V. K. et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34, 267-273 (2003).
44. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545-15550 (2005).