Human embryonic stem cells prevent T-cell activation by suppressing dendritic cells function via tgf-beta signaling pathway

Stem Cells

Volumn 32, Issue 12, 2014, Pages 3137-3149

  Leshansky, Lucy ^a   Aberdam, Daniel ^a,b,c   Itskovitz Eldor, Joseph ^a   Berrih Aknin, Sonia ^d,e,f,g  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b SAINT LOUIS HOSPITAL   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e Sorbonne Université   (France)

^f CNRS   (France)

^g Institute of Myology   (France)

Author keywords

Embryonic stem cells; Immunosuppression; T cells; TGF

Indexed keywords

B7 ANTIGEN; CASPASE 3; CD45RO ANTIGEN; FAS ANTIGEN; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TRANSFORMING GROWTH FACTOR BETA; LEUKOCYTE ANTIGEN;

ARTICLE; CD4+ T LYMPHOCYTE; CELL DEATH; CELL FUNCTION; CELL SIZE; CELL STRUCTURE; COCULTURE; CONTROLLED STUDY; DENDRITIC CELL; DOWN REGULATION; EMBRYONIC STEM CELL; ENZYME ACTIVITY; GLUTATHIONE METABOLISM; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOREGULATION; IMMUNOSURVEILLANCE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MONOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROCESSING; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; UPREGULATION; CELL DIFFERENTIATION; CYTOLOGY; HUMAN EMBRYONIC STEM CELL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PHYSIOLOGY; PROCEDURES; T LYMPHOCYTE;

ANTIGENS, CD; CELL DIFFERENTIATION; COCULTURE TECHNIQUES; DENDRITIC CELLS; HUMAN EMBRYONIC STEM CELLS; HUMANS; LYMPHOCYTE ACTIVATION; MONOCYTES; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSFORMING GROWTH FACTOR BETA;

EID: 84912112002     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1833     Document Type: Article

References (51)

1. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. Embryonic stem cell lines derived from human blastocysts. Science (New York, NY) 1998; 282: 1145-1147.
2. Grinnemo KH, Sylven C, Hovatta O, et al. Immunogenicity of human embryonic stem cells. Cell Tissue Res 2008; 331: 67-78.
3. Zhao T, Zhang ZN, Rong Z, et al. Immunogenicity of induced pluripotent stem cells. Nature 2011; 474: 212-215.
4. Cao F, van der Bogt KE, Sadrzadeh A, et al. Spatial and temporal kinetics of teratoma formation from murine embryonic stem cell transplantation. Stem Cells Dev 2007; 16: 883-891.
5. Drukker M, Katchman H, Katz G, et al. Human embryonic stem cells and their differentiated derivatives are less susceptible to immune rejection than adult cells. Stem Cells (Dayton, Ohio) 2006; 24: 221-229.
6. Carette JE, Pruszak J, Varadarajan M, et al. Generation of iPSCs from cultured human malignant cells. Blood 115: 4039-4042.
7. Knoepfler PS,. Deconstructing stem cell tumorigenicity: A roadmap to safe regenerative medicine. Stem Cells (Dayton, Ohio) 2009; 27: 1050-1056.
8. Blum B, Benvenisty N,. The tumorigenicity of human embryonic stem cells. Adv Cancer Res 2008; 100: 133-158.
9. Koch CA, Platt JL,. T cell recognition and immunity in the fetus and mother. Cell Immunol 2007; 248: 12-17.
10. Li L, Baroja ML, Majumdar A, et al. Human embryonic stem cells possess immune-privileged properties. Stem Cells (Dayton, Ohio) 2004; 22: 448-456.
11. Grinnemo KH, Genead R, Kumagai-Braesch M, et al. Costimulation blockade induces tolerance to HESC transplanted to the testis and induces regulatory T-cells to HESC transplanted into the heart. Stem Cells (Dayton, Ohio) 2008; 26: 1850-1857.
12. Robertson NJ, Brook FA, Gardner RL, et al. Embryonic stem cell-derived tissues are immunogenic but their inherent immune privilege promotes the induction of tolerance. Proc Natl Acad Sci USA 2007; 104: 20920-20925.
13. Cabrera CM, Nieto A, Cortes JL, et al. The low rate of HLA class I molecules on the human embryonic stem cell line HS293 is associated with the APM components' expression level. Cell Biol Int 2007; 31: 1072-1078.
14. Drukker M, Katz G, Urbach A, et al. Characterization of the expression of MHC proteins in human embryonic stem cells. Proc Natl Acad Sci USA 2002; 99: 9864-9869.
15. Yachimovich-Cohen N, Even-Ram S, Shufaro Y, et al. Human embryonic stem cells suppress T cell responses via arginase I-dependent mechanism. J Immunol 2010; 184: 1300-1308.
16. Moulian N, Truffault F, Gaudry-Talarmain YM, et al. In vivo and in vitro apoptosis of human thymocytes are associated with nitrotyrosine formation. Blood 2001; 97: 3521-3530.
17. Siegel RM, Chan FK, Chun HJ, et al. The multifaceted role of Fas signaling in immune cell homeostasis and autoimmunity. Nat Immunol 2000; 1: 469-474.
18. Michie CA, McLean A, Alcock C, et al. Lifespan of human lymphocyte subsets defined by CD45 isoforms. Nature 1992; 360: 264-265.
19. Penninger JM, Irie-Sasaki J, Sasaki T, et al. CD45: New jobs for an old acquaintance. Nat Immunol 2001; 2: 389-396.
20. Ristich V, Liang S, Zhang W, et al. Tolerization of dendritic cells by HLA-G. Eur J Immunol 2005; 35: 1133-1142.
21. Yoshimura A, Muto G,. TGF-beta function in immune suppression. Curr Top Microbiol Immunol 2011; 350: 127-147.
22. Puceat M,. TGF beta in the differentiation of embryonic stem cells. Cardiovasc Res 2007; 74: 256-261.
23. Shiraki N, Lai CJ, Hishikari Y, et al. TGF-beta signaling potentiates differentiation of embryonic stem cells to Pdx-1 expressing endodermal cells. Genes Cells 2005; 10: 503-516.
24. Willems E, Cabral-Teixeira J, Schade D, et al. Small molecule-mediated TGF-beta type II receptor degradation promotes cardiomyogenesis in embryonic stem cells. Cell Stem Cell 2012; 11: 242-252.
25. Wang MK, Sun HQ, Xiang YC, et al. Different roles of TGF-beta in the multi-lineage differentiation of stem cells. World J Stem Cells 2012; 4: 28-34.
26. Angelini G, Gardella S, Ardy M, et al. Antigen-presenting dendritic cells provide the reducing extracellular microenvironment required for T lymphocyte activation. Proc Natl Acad Sci USA 2002; 99: 1491-1496.
27. Yan Z, Garg SK, Kipnis J, et al. Extracellular redox modulation by regulatory T cells. Nat Chem Biol 2009; 5: 721-723.
28. Yan Z, Garg SK, Banerjee R,. Regulatory T cells interfere with glutathione metabolism in dendritic cells and T cells. J Biol Chem 2010; 285: 41525-41532.
29. Liu RM, Vayalil PK, Ballinger C, et al. Transforming growth factor beta suppresses glutamate-cysteine ligase gene expression and induces oxidative stress in a lung fibrosis model. Free Radic Biol Med 2012; 53: 554-563.
30. Liu RM, Gaston Pravia KA,. Oxidative stress and glutathione in TGF-beta-mediated fibrogenesis. Free Radic Biol Med 2010; 48: 1-15.
31. Franklin CC, Rosenfeld-Franklin ME, White C, et al. TGFbeta1-induced suppression of glutathione antioxidant defenses in hepatocytes: Caspase-dependent post-translational and caspase-independent transcriptional regulatory mechanisms. FASEB J 2003; 17: 1535-1537.
32. Wong SH, Santambrogio L, Strominger JL,. Caspases and nitric oxide broadly regulate dendritic cell maturation and surface expression of class II MHC proteins. Proc Natl Acad Sci USA 2004; 101: 17783-17788.
33. Santambrogio L, Potolicchio I, Fessler SP, et al. Involvement of caspase-cleaved and intact adaptor protein 1 complex in endosomal remodeling in maturing dendritic cells. Nat Immunol 2005; 6: 1020-1028.
34. Huang D, Cai DT, Chua RY, et al. Nitric-oxide synthase 2 interacts with CD74 and inhibits its cleavage by caspase during dendritic cell development. J Biol Chem 2008; 283: 1713-1722.
35. Hof-Nahor I, Leshansky L, Shivtiel S, et al. Human mesenchymal stem cells shift CD8+ T cells towards a suppressive phenotype by inducing tolerogenic monocytes. J Cell Sci 2012; 125: 4640-4650.
36. Ben-Ami E, Miller A, Berrih-Aknin S,. T cells from autoimmune patients display reduced sensitivity to immunoregulation by mesenchymal stem cells: Role of IL-2. Autoimmun Rev 2014; 13: 187-196.
37. Dimitriadis E, White CA, Jones RL, et al. Cytokines, chemokines and growth factors in endometrium related to implantation. Hum Reprod Update 2005; 11: 613-630.
38. Guerin LR, Prins JR, Robertson SA,. Regulatory T-cells and immune tolerance in pregnancy: A new target for infertility treatment? Hum Reprod Update 2009; 15: 517-535.
39. Ernerudh J, Berg G, Mjosberg J,. Regulatory T helper cells in pregnancy and their roles in systemic versus local immune tolerance. Am J Reprod Immunol 2011; 66 (suppl 1): 31-43.
40. Banchereau J, Steinman RM,. Dendritic cells and the control of immunity. Nature 1998; 392: 245-252.
41. Mellman I, Steinman RM,. Dendritic cells: Specialized and regulated antigen processing machines. Cell 2001; 106: 255-258.
42. Geissmann F, Auffray C, Palframan R, et al. Blood monocytes: Distinct subsets, how they relate to dendritic cells, and their possible roles in the regulation of T-cell responses. Immunol Cell Biol 2008; 86: 398-408.
43. Mohib K, Allan D, Wang L,. Human embryonic stem cell-extracts inhibit the differentiation and function of monocyte-derived dendritic cells. Stem Cell Rev 2010; 6: 611-621.
44. Mohib K, AlKhamees B, Zein HS, et al. Embryonic stem cell-derived factors inhibit T effector activation and induce T regulatory cells by suppressing PKC-theta activation. PLoS One 2012; 7: e32420.
45. Sahaf B, Heydari K, Herzenberg LA, et al. Lymphocyte surface thiol levels. Proc Natl Acad Sci USA 2003; 100: 4001-4005.
46. Gelderman KA, Hultqvist M, Holmberg J, et al. T cell surface redox levels determine T cell reactivity and arthritis susceptibility. Proc Natl Acad Sci USA 2006; 103: 12831-12836.
47. Yan Z, Banerjee R,. Redox remodeling as an immunoregulatory strategy. Biochemistry 2010; 49: 1059-1066.
48. Ballatori N, Krance SM, Notenboom S, et al. Glutathione dysregulation and the etiology and progression of human diseases. Biol Chem 2009; 390: 191-214.
49. Franklin CC, Backos DS, Mohar I, et al. Structure, function, and post-translational regulation of the catalytic and modifier subunits of glutamate cysteine ligase. Mol Aspects Med 2009; 30: 86-98.
50. D'Angelo JA, Dehlink E, Platzer B, et al. The cystine/glutamate antiporter regulates dendritic cell differentiation and antigen presentation. J Immunol 2010; 185: 3217-3226.
51. Aukrust P, Svardal AM, Muller F, et al. Increased levels of oxidized glutathione in CD4+ lymphocytes associated with disturbed intracellular redox balance in human immunodeficiency virus type 1 infection. Blood 1995; 86: 258-267.