Inhibition of T-cell activation by retinal pigment epithelial cells derived from induced pluripotent stem cells

Investigative Ophthalmology and Visual Science

Volumn 56, Issue 2, 2015, Pages 1051-1062

  Sugita, Sunao ^a   Kamao, Hiroyuki ^a   Iwasaki, Yuko ^a   Okamoto, Satoshi ^a,b   Hashiguchi, Tomoyo ^a   Iseki, Kyoko ^a   Hayashi, Naoko ^a   Mandai, Michiko ^a   Takahashi, Masayo ^a  

^a RIKEN   (Japan)

^b KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Cytokine; PS cells; TGF

Indexed keywords

CD4 ANTIGEN; CD40 LIGAND; CHEMOKINE RECEPTOR CCR4; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 21; INTERLEUKIN 22; INTERLEUKIN 6; INTERLEUKIN 8; INTERLEUKIN 9; MONOCYTE CHEMOTACTIC PROTEIN 1; MONOCYTE CHEMOTACTIC PROTEIN 3; OCTAMER TRANSCRIPTION FACTOR 4; ORGANIC CATION TRANSPORTER 3; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR T BET; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; UNINDEXED DRUG; VASCULOTROPIN A; DNA;

ARTICLE; CELL DIFFERENTIATION; CELL PHAGOCYTOSIS; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ELECTROPORATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; PERIPHERAL BLOOD MONONUCLEAR CELL; PIGMENT EPITHELIUM; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RETINA PIGMENT CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; BIOSYNTHESIS; CELL CULTURE; CELLULAR IMMUNITY; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

CELL PROLIFERATION; CELLS, CULTURED; DNA; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, CELLULAR; IMMUNOHISTOCHEMISTRY; INDUCED PLURIPOTENT STEM CELLS; LYMPHOCYTE ACTIVATION; REAL-TIME POLYMERASE CHAIN REACTION; RETINAL PIGMENT EPITHELIUM; T-LYMPHOCYTES; TRANSFORMING GROWTH FACTOR BETA;

EID: 84923013801     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.14-15619     Document Type: Article

References (32)

1. Streilein JW. Ocular immune privilege: therapeutic opportunities from an experiment of nature. Nat Rev Immunol. 2003;3: 879–889
2. Niederkorn JY. Immune privilege in the anterior chamber of the eye. Crit Rev Immunol. 2002;22:13–46
3. Sugita S. Role of ocular pigment epithelial cells in immune privilege. Arch Immunol Ther Exp (Warsz). 2009;57:263–268
4. Zamiri P, Sugita S, Streilein JW. Immunosuppressive properties of the pigmented epithelial cells and the subretinal space. Chem Immunol Allergy. 2007;92:86–93
5. Sugita S, Usui Y, Horie S, et al. T-cell suppression by programmed cell death 1 ligand 1 on retinal pigment epithelium during inflammatory conditions. Invest Ophthalmol Vis Sci. 2009;50:2862–2870
6. Sugita S, Ng TF, Lucas PJ, Gress RE, Streilein JW. B7+ iris pigment epithelium induce CD8þ T regulatory cells: both suppress CTLA-4+ T cells. J Immunol. 2006;176:118–127
7. Sugita S, Horie S, Nakamura O, et al. Retinal pigment epithelium-derived CTLA-2alpha induces TGFbeta-producing T regulatory cells. J Immunol. 2008;181:7525–7536
8. Sugita S, Futagami Y, Smith SB, Naggar H, Mochizuki M. Retinal and ciliary body pigment epithelium suppress activation of T lymphocytes via transforming growth factor beta. Exp Eye Res. 2006;83:1459–1471
9. Futagami Y, Sugita S, Vega J, et al. Role of thrombospondin-1 in T cell response to ocular pigment epithelial cells. J Immunol. 2007;178:6994–7005
10. Sugita S, Horie S, Nakamura O, et al. Acquisition of T regulatory function in cathepsin L-inhibited T cells by eyederived CTLA-2alpha during inflammatory conditions. J Immunol. 2009;183:5013–5022
11. Sugita S, Kawazoe Y, Imai A, et al. Mature dendritic cell suppression by IL-1 receptor antagonist on retinal pigment epithelium cells. Invest Ophthalmol Vis Sci. 2013;54:3240–3249
12. Kawazoe Y, Sugita S, Keino H, et al. Retinoic acid from retinal pigment epithelium induces T regulatory cells. Exp Eye Res. 2012;94:32–40
13. Wallace CA, Moir G, Malone DF, Duncan L, Devarajan G, Crane IJ. Regulation of T-lymphocyte CCL3 and CCL4 production by retinal pigment epithelial cells. Invest Ophthalmol Vis Sci. 2013;54:722–730
14. Liversidge J, Grabowski P, Ralston S, Benjamin N, Forrester JV. Rat retinal pigment epithelial cells express an inducible form of nitric oxide synthase and produce nitric oxide in response to inflammatory cytokines and activated T cells. Immunology. 1994;83:404–409
15. Watt FM, Hogan BL. Out of Eden: stem cells and their niches. Science. 2000;287:1427–1430
16. Joe AW, Gregory-Evans K. Mesenchymal stem cells and potential applications in treating ocular disease. Curr Eye Res. 2010;35:941–952
17. Osakada F, Jin ZB, Hirami Y, et al. In vitro differentiation of retinal cells from human pluripotent stem cells by smallmolecule induction. J Cell Sci. 2009;122:3169–3179
18. Peyman GA, Blinder KJ, Paris CL, Alturki W, Nelson NC Jr, Desai U. A technique for retinal pigment epithelium transplantation for age-related macular degeneration secondary to extensive subfoveal scarring. Ophthalmic Surg. 1991;22:102–108
19. Algvere PV. Clinical possibilities in retinal pigment epithelial transplantations. Acta Ophthalmol Scand. 1997;75:1
20. Weisz JM, Humayun MS, De Juan E Jr, et al. Allogenic fetal retinal pigment epithelial cell transplant in a patient with geographic atrophy. Retina. 1999;19:540–545
21. Maekawa M, Yamaguchi K, Nakamura T, et al. Direct reprogramming of somatic cells is promoted by maternal transcription factor Glis1. Nature. 2011;474:225–229
22. Yu J, Hu K, Smuga-Otto K, et al. Human induced pluripotent stem cells free of vector and transgene sequences. Science. 2009;324:797–801
23. Horie S, Sugita S, Futagami Y, Yamada Y, Mochizuki M. Human retinal pigment epithelium-induced CD4+CD25+ regulatory T cells suppress activation of intraocular effector T cells. Clin Immunol. 2010;136:83–95
24. Sugita S, Ng TF, Schwartzkopff J, Streilein JW. CTLA-4+CD8þT cells that encounter B7-2þiris pigment epithelial cells express their own B7-2 to achieve global suppression of T cell activation. J Immunol. 2004;172:4184–4194
25. Okita K, Matsumura Y, Sato Y, et al. A more efficient method to generate integration-free human iPS cells. Nat Methods. 2011; 8:409–412
26. Berglin L, Gouras P, Sheng Y, et al. Tolerance of human fetal retinal pigment epithelium xenografts in monkey retina. Graefes Arch Clin Exp Ophthalmol. 1997;235:103–110
27. Cousins SW, McCabe MM, Danielpour D, Streilein JW. Identification of transforming growth factor-beta as an immunosuppressive factor in aqueous humor. Invest Ophthalmol Vis Sci. 1991;32:2201–2211
28. Grisanti S, Ishioka M, Kosiewicz M, Jiang LQ. Immunity and immune privilege elicited by cultured retinal pigment epithelial cell transplants. Invest Ophthalmol Vis Sci. 1997; 38:1619–1626
29. Wenkel H, Chen PW, Ksander BR, Streilein JW. Immune privilege is extended, then withdrawn, from allogeneic tumor cell grafts placed in the subretinal space. Invest Ophthalmol Vis Sci. 1999;40:3202–3208
30. Zhao T, Zhang ZN, Rong Z, Xu Y. Immunogenicity of induced pluripotent stem cells. Nature. 2011;474:212–215
31. Araki R, Uda M, Hoki Y, et al. Negligible immunogenicity of terminally differentiated cells derived from induced pluripotent or embryonic stem cells. Nature. 2013;494:100–104
32. Nakatsuji N, Nakajima F, Tokunaga K. HLA-haplotype banking and iPS cells. Nat Biotechnol. 2008;26:739–740.