Heterelogous expression of mutated HLA-G decreases immunogenicity of human embryonic stem cells and their epidermal derivatives

Stem Cell Research

Volumn 13, Issue 2, 2014, Pages 342-354

  Zhao, Longmei ^a   Teklemariam, Takele ^a   Hantash, Basil M ^a,b  

^a Escape Therapeutics Inc   (United States)

^b Elixir Institute of Regenerative Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; CYTOKERATIN 14; OCTAMER TRANSCRIPTION FACTOR 4; STAGE SPECIFIC EMBRYO ANTIGEN 4; TELOMERASE; BIOLOGICAL MARKER; ELONGATION FACTOR 1; HLA G ANTIGEN; IL2RG PROTEIN, MOUSE; INTERLEUKIN 2 RECEPTOR GAMMA; NERVE PROTEIN; PGBD1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY ASSAY; EMBRYO; EMBRYOID BODY; EMBRYONIC STEM CELL; ENZYME ACTIVITY; EPIDERMIS CELL; FLOW CYTOMETRY; GENE STRUCTURE; HESC DERIVED EPIDERMAL PROGENITOR; HETEROLOGOUS EXPRESSION; HUMAN; HUMAN CELL; HUMAN LEUKOCYTE ANTIGEN G GENE; IMMUNOFLUORESCENCE; IMMUNOGENICITY; KARYOTYPE; KERATINOCYTE; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; MIXED T LYMPHOCYTE; MOUSE; MUTATOR GENE; NATURAL KILLER CELL; NONHUMAN; PLURIPOTENT STEM CELL; PROMOTER REGION; STABLE EXPRESSION; STEM CELL; T LYMPHOCYTE; TERATOMA; TRANSPOSON; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SHAPE; CELL SURVIVAL; CYTOLOGY; CYTOTOXICITY; DEFICIENCY; EPIDERMIS; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; GENOTYPE; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MUTATION; NONOBESE DIABETIC MOUSE; PHENOTYPE; SCID MOUSE;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SHAPE; CELL SURVIVAL; CELLS, CULTURED; CYTOTOXICITY, IMMUNOLOGIC; EMBRYONIC STEM CELLS; EPIDERMIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOTYPE; HLA-G ANTIGENS; HUMANS; IMMUNE TOLERANCE; INTERLEUKIN RECEPTOR COMMON GAMMA SUBUNIT; KARYOTYPE; KILLER CELLS, NATURAL; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, SCID; MUTATION; NERVE TISSUE PROTEINS; PEPTIDE ELONGATION FACTOR 1; PHENOTYPE; PLURIPOTENT STEM CELLS; PROMOTER REGIONS, GENETIC; TELOMERASE; TERATOMA; TRANSFECTION;

EID: 84909949508     PISSN: 18735061     EISSN: 18767753     Source Type: Journal    
DOI: 10.1016/j.scr.2014.08.004     Document Type: Article

References (66)

1. Aluigi M., Fogli M., Curti A., et al. Nucleofection is an efficient nonviral transfection technique for human bone marrow-derived mesenchymal stem cells. Stem Cells 2006, 24(2):454-461.
2. Apps R., Gardner L., Moffett A. A critical look at HLA-G. Trends Immunol. 2008, 29(7):313-321.
3. Aslan H., Zilberman Y., Arbeli V., et al. Nucleofection-based ex vivo nonviral gene delivery to human stem cells as a platform for tissue regeneration. Tissue Eng. 2006, 12(4):877-889.
4. Bahri R., Hirsch F., Josse A., et al. Soluble HLA-G inhibits cell cycle progression in human alloreactive T lymphocytes. J. Immunol. 2006, 176(3):1331-1339.
5. Bradley Ja, Bolton Em, Pedersen Ra Stem cell medicine encounters the immune system. Nat. Rev. Immunol. 2002, 2(11):859-871.
6. Brakebusch C., Grose R., Quondamatteo F., et al. Skin and hair follicle integrity is crucially dependent on beta 1 integrin expression on keratinocytes. EMBO J. 2000, 19(15):3990-4003.
7. Brehm Ma, Shultz Ld Human allograft rejection in humanized mice: a historical perspective. Cell. Mol. Immunol. 2012, 9(3):225-231.
8. Carosella Ed, Dausset J., Kirszenbaum M. HLA-G revisited. Immunol. Today 1996, 17(9):407-409.
9. Carvajal-Vergara X., Sevilla A., D'souza Sl, et al. Patient-specific induced pluripotent stem-cell-derived models of LEOPARD syndrome. Nature 2010, 465(7299):808-812.
10. Castelli Ec, Moreau P., Oya E., Chiromatzo A., et al. In silico analysis of microRNAS targeting the HLA-G 3' untranslated region alleles and haplotypes. Hum. Immunol. 2009, 70(12):1020-1025.
11. Castelli Ec, Mendes-Junior Ct, Deghaide Nh., et al. The genetic structure of 3' untranslated region of the HLA-G gene: polymorphisms and haplotypes. Genes Immun. 2010, 11(2):134-141.
12. Caumartin J., Favier B., Daouya M., et al. Trogocytosis-based generation of suppressive NK cells. EMBO J. 2007, 26(5):1423-1433.
13. Chan Kk, Wu Sm, Nissom Pm, Oh Sk, Choo Ab Generation of high-level stable transgene expressing human embryonic stem cell lines using Chinese hamster elongation factor-1 alpha promoter system. Stem Cells Dev. 2008, 17(4):825-836.
14. Chen Yt, Dejosez M., Zwaka Tp, Behringer Rr H1 and H9 human embryonic stem cell lines are heterozygous for the ABO locus. Stem Cells Dev. 2008, 17(5):853-855.
15. Chin Mh., Mason Mj, Xie W., et al. Induced pluripotent stem cells and embryonic stem cells are distinguished by gene expression signatures. Cell Stem Cell 2009, 5(1):111-123.
16. Doi A., Park Ih., Wen B., et al. Differential methylation of tissue- and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat. Genet. 2009, 41(12):1350-1353.
17. Feng Q., Lu Sj, Klimanskaya I., et al. Hemangioblastic derivatives from human induced pluripotent stem cells exhibit limited expansion and early senescence. Stem Cells 2010, 28(4):704-712.
18. Geraghty De, Koller Bh., Orr Ht A human major histocompatibility complex class I gene that encodes a protein with a shortened cytoplasmic segment. Proc. Natl. Acad. Sci. U. S. A. 1987, 84(24):9145-9149.
19. Grez M., Akgun E., Hilberg F., Ostertag W. Embryonic stem cell virus, a recombinant murine retrovirus with expression in embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 1990, 87(23):9202-9206.
20. Guenther Mg, Frampton Gm, Soldner F., et al. Chromatin structure and gene expression programs of human embryonic and induced pluripotent stem cells. Cell Stem Cell 2010, 7(2):249-257.
21. Horuzsko A., Lenfant F., Munn Dh., Mellor Al Maturation of antigen-presenting cells is compromised in HLA-G transgenic mice. Int. Immunol. 2001, 13(3):385-394.
22. Hviid Tv, Hylenius S., Rorbye C., Nielsen Lg HLA-G allelic variants are associated with differences in the HLA-G mRNA isoform profile and HLA-G mRNA levels. Immunogenetics 2003, 55(2):63-79.
23. Ishitani A., Geraghty De Alternative splicing of HLA-G transcripts yields proteins with primary structures resembling both class I and class II antigens. Proc. Natl. Acad. Sci. U. S. A. 1992, 89(9):3947-3951.
24. Itskovitz-Eldor J., Schuldiner M., Karsenti D., et al. Differentiation of human embryonic stem cells into embryoid bodies compromising the three embryonic germ layers. Mol. Med. 2000, 6(2):88-95.
25. Jaenisch R., Young R. Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 2008, 132(4):567-582.
26. Ji L., Allen-Hoffmann Bl, De Pablo Jj, Palecek Sp Generation and differentiation of human embryonic stem cell-derived keratinocyte precursors. Tissue Eng. 2006, (4):665-679.
27. Jiang S., Zhao L., Purandare B. Hantash Bm: Differential expression of stem cell markers in human follicular bulge and interfollicular epidermal compartments. Histochem. Cell. Biol. 2010, 133(4):455-465.
28. Kirszenbaum M., Moreau P., Gluckman E., Dausset J., Carosella E. An alternatively spliced form of HLA-G mRNA in human trophoblasts and evidence for the presence of HLA-G transcript in adult lymphocytes. Proc. Natl. Acad. Sci. U. S. A. 1994, 91(10):4209-4213.
29. Lacoste A., Berenshteyn F., Brivanlou Ah. An efficient and reversible transposable system for gene delivery and lineage-specific differentiation in human embryonic stem cells. Cell Stem Cell 2009, 5(3):332-342.
30. Lakshmipathy U., Pelacho B., Sudo K., et al. Efficient transfection of embryonic and adult stem cells. Stem Cells 2004, 22(4):531-543.
31. Lemaitre G., Nissan X., Baldeschi C., Peschanski M. Concise review: epidermal grafting: the case for pluripotent stem cells. Stem Cells 2011, 29(6):895-899.
32. Lemaoult J., Caumartin J., Daouya M., et al. Immune regulation by pretenders: cell-to-cell transfers of HLA-G make effector T cells act as regulatory cells. Blood 2007, 109(5):2040-2048.
33. Li X., Harrell Ra, Handler Am, Beam T., Hennessy K., Fraser Mj PiggyBac internal sequences are necessary for efficient transformation of target genomes. Insect Mol. Biol. 2005, 14(1):17-30.
34. Lu Sj, Feng Q., Park Js, et al. Biologic properties and enucleation of red blood cells from human embryonic stem cells. Blood 2008, 112(12):4475-4484.
35. Metallo Cm, Ji L., De Pablo Jj, Palecek Sp Directed differentiation of human embryonic stem cells to epidermal progenitors. Methods Mol. Biol. 2010, 585:83-92.
36. Narsinh K., Narsinh Kh., Wu Jc Derivation of human induced pluripotent stem cells for cardiovascular disease modeling. Circ. Res. 2011, 108(9):1146-1156.
37. Nussbaum J., Minami E., Laflamme Ma, et al. Transplantation of undifferentiated murine embryonic stem cells in the heart: teratoma formation and immune response. FASEB J. 2007, 21(7):1345-1357.
38. Osborne Cs, Pasceri P., Singal R., Sukonnik T., Ginder Gd, Ellis J. Amelioration of retroviral vector silencing in locus control region beta-globin-transgenic mice and transduced F9 embryonic cells. J. Virol. 1999, 73(7):5490-5496.
39. Oue M., Handa H., Matsuzaki Y., Suzue K., Murakami H., Hirai H. The murine stem cell virus promoter drives correlated transgene expression in the leukocytes and cerebellar Purkinje cells of transgenic mice. PLoS One 2012, 7(11):e51015.
40. Park B., Lee S., Kim E., Chang S., Jin M., Ahn K. The truncated cytoplasmic tail of HLA-G serves a quality-control function in post-ER compartments. Immunity 2001, 15(2):213-224.
41. Puymirat E., Geha R., Tomescot A., et al. Can mesenchymal stem cells induce tolerance to cotransplanted human embryonic stem cells?. Mol. Ther. 2009, 17(1):176-182.
42. Ran D., Shia Wj., Lo Mc., et al. RUNX1a enhances hematopoietic lineage commitment from human embryonic stem cells and inducible pluripotent stem cells. Blood 2013, 121(15):2882-2890.
43. Reubinoff Be, Pera Mf, Fong Cy, Trounson A., Bongso A. Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat. Biotechnol. 2000, 18(4):399-404.
44. Riteau B., Menier C., Khalil-Daher I., et al. HLA-G inhibits the allogeneic proliferative response. J. Reprod. Immunol. 1999, 43(2):203-211.
45. Riteau B., Rouas-Freiss N., Menier C., Paul P., Dausset J., Carosella Ed HLA-G2, -G3, and -G4 isoforms expressed as nonmature cell surface glycoproteins inhibit NK and antigen-specific CTL cytolysis. J. Immunol. 2001, 166(8):5018-5026.
46. Robertson Nj, Brook Fa, Gardner Rl, Cobbold Sp, Waldmann H., Fairchild Pj Embryonic stem cell-derived tissues are immunogenic but their inherent immune privilege promotes the induction of tolerance. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(52):20920-20925.
47. Rouas-Freiss N., Marchal Re, Kirszenbaum M., Dausset J., Carosella Ed The alpha1 domain of HLA-G1 and HLA-G2 inhibits cytotoxicity induced by natural killer cells: is HLA-G the public ligand for natural killer cell inhibitory receptors?. Proc. Natl. Acad. Sci. U. S. A. 1997, 94(10):5249-5254.
48. Rouas-Freiss N., Goncalves Rm, Menier C., Dausset J., Carosella Ed Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc. Natl. Acad. Sci. U. S. A. 1997, 94(21):11520-11525.
49. Rousseau P., Le Discorde M., Mouillot G., Marcou C., Carosella Ed, Moreau P. The 14bp deletion-insertion polymorphism in the 3' UT region of the HLA-G gene influences HLA-G mRNA stability. Hum. Immunol. 2003, 64(11):1005-1010.
50. Siemen H., Nix M., Endl E., Koch P., Itskovitz-Eldor J., Brustle O. Nucleofection of human embryonic stem cells. Stem Cells Dev. 2005, 14(4):378-383.
51. Singer-Sam J., Keith Dh., Tani K., et al. Sequence of the promoter region of the gene for human X-linked 3-phosphoglycerate kinase. Gene 1984, 32(3):409-417.
52. Suarez-Alvarez B., Rodriguez Rm., Calvanese V., et al. Epigenetic mechanisms regulate MHC and antigen processing molecules in human embryonic and induced pluripotent stem cells. PLoS One 2010, 5(4):e10192.
53. Swijnenburg Rj, Tanaka M., Vogel H., et al. Embryonic stem cell immunogenicity increases upon differentiation after transplantation into ischemic myocardium. Circulation 2005, 112(9 Suppl.):I166-172.
54. Swijnenburg Rj, Schrepfer S., Cao F., et al. In vivo imaging of embryonic stem cells reveals patterns of survival and immune rejection following transplantation. Stem Cells Dev. 2008, 17(6):1023-1029.
55. Swindle Cs, Kim Hg, Klug Ca Mutation of CpGs in the murine stem cell virus retroviral vector long terminal repeat represses silencing in embryonic stem cells. J. Biol. Chem. 2004, 279(1):34-41.
56. Taylor Cm Complement factor H and the haemolytic uraemic syndrome. Lancet 2001, 358(9289):1200-1202.
57. Thomson Ja, Itskovitz-Eldor J., Shapiro Ss, et al. Embryonic stem cell lines derived from human blastocysts. Science 1998, 282(5391):1145-1147.
58. Watanabe K., Ueno M., Kamiya D., et al. A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat. Biotechnol. 2007, 25(6):681-686.
59. Wu Dc, Boyd As, Wood Kj Embryonic stem cells and their differentiated derivatives have a fragile immune privilege but still represent novel targets of immune attack. Stem Cells 2008, 26(8):1939-1950.
60. Yates F., Daley Gq Progress and prospects: gene transfer into embryonic stem cells. Gene Ther. 2006, 13(20):1431-1439.
61. Yu J., Vodyanik Ma, Smuga-Otto K., et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007, 318(5858):1917-1920.
62. Zhao L., Jiang S., Hantash Bm Transforming growth factor beta1 induces osteogenic differentiation of murine bone marrow stromal cells. Tissue Eng. Part A 2010, 16(2):725-733.
63. Zhao T., Zhang Zn, Rong Z., Xu Y. Immunogenicity of induced pluripotent stem cells. Nature 2011, 474(7350):212-215.
64. Zhao L., Purandare B., Zhang J., Hantash Bm beta2-Microglobulin-free HLA-G activates natural killer cells by increasing cytotoxicity and proinflammatory cytokine production. Hum. Immunol. 2012, 74:417-424.
65. Zhao L., Teklemariam T., Hantash Bm Reassessment of HLA-G isoform specificity of MEM-G/9 and 4H84 monoclonal antibodies. Tissue Antigens 2012, 80(3):231-238.
66. Zhu Aj, Haase I., Watt Fm Signaling via beta1 integrins and mitogen-activated protein kinase determines human epidermal stem cell fate in vitro. Proc. Natl. Acad. Sci. U. S. A. 1999, 96(12):6728-6733.