Immunogenicity of in vitro maintained and matured populations: Potential barriers to engraftment of human pluripotent stem cell derivatives

Methods in Molecular Biology

Volumn 1029, Issue , 2013, Pages 17-31

  Tang, Chad ^a   Weissman, Irving L ^a   Drukker, Micha ^a  

^a NONE

Author keywords

Antigen presentation; Episomal; Immune surveillance; Non integrating; Sialic acid; Teratomas; Xenoantigen

Indexed keywords

ANTIGEN; CYCLOSPORIN; DEXAMETHASONE; FETAL ANTIGEN; RAPAMYCIN; TACROLIMUS;

ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; ANTIGENICITY; APOPTOSIS; CELL DIFFERENTIATION; CELL MATURATION; ENGRAFTMENT; HUMAN; IMMUNOGENICITY; IMMUNOSURVEILLANCE; IN VITRO STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SOMATIC CELL; T LYMPHOCYTE; TERATOMA;

ANTIGEN PRESENTATION; CELL DIFFERENTIATION; HUMANS; IMMUNITY; IMMUNOSUPPRESSION; KILLER CELLS, NATURAL; PLURIPOTENT STEM CELLS;

EID: 84934434430     PISSN: 10643745     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-62703-478-4_2     Document Type: Review

References (104)

1. Nankivell BJ, Alexander SI (2010) Rejection of the kidney allograft. N Engl J Med 363:1451-1462
2. Drukker M, Katz G, Urbach A, Schuldiner M, Markel G et al (2002) Characterization of the expression of MHC proteins in human embryonic stem cells. Proc Natl Acad Sci U S A 99:9864-9869
3. Draper JS, Pigott C, Thomson JA, Andrews PW (2002) Surface antigens of human embryonic stem cells: changes upon differentiation in culture. J Anat 200:249-258
4. Drukker M (2008) Immunological considerations for cell therapy using human embryonic stem cell derivatives.
5. Revazova ES, Turovets NA, Kochetkova OD, Kindarova LB, Kuzmichev LN et al (2007) Patient-specific stem cell lines derived from human parthenogenetic blastocysts. Cloning Stem Cells 9:432-449
6. McCreath KJ, Howcroft J, Campbell KH, Colman A, Schnieke AE et al (2000) Production of gene-targeted sheep by nuclear transfer from cultured somatic cells. Nature 405:1066-1069
7. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T et al (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861-872
8. Drukker M (2004) Immunogenicity of human embryonic stem cells: can we achieve tolerance? Springer Semin Immunopathol 26:201-213
9. Drukker M, Benvenisty N (2004) The immunogenicity of human embryonic stem-derived cells. Trends Biotechnol 22:136-141
10. Martin MJ, Muotri A, Gage F, Varki A (2005) Human embryonic stem cells express an immunogenic nonhuman sialic acid. Nat Med 11:228-232
11. Heiskanen A, Satomaa T, Tiitinen S, Laitinen A, Mannelin S et al (2007) N-glycolylneuraminic acid xenoantigen contamination of human embryonic and mesenchymal stem cells is substantially reversible. Stem Cells 25:197-202
12. Chung TL, Turner JP, Thaker N, Kolle G, Cooper-White JJ et al (2010) Ascorbate promotes epigenetic activation of CD30 in human embryonic stem cells. Stem Cells 28(10):1782-1793
13. Draper JS, Smith K, Gokhale P, Moore HD, Maltby E et al (2004) Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nat Biotechnol 22:53-54
14. Spits C, Mateizel I, Geens M, Mertzanidou A, Staessen C et al (2008) Recurrent chromosomal abnormalities in human embryonic stem cells. Nat Biotechnol 26:1361-1363
15. Kim K, Doi A, Wen B, Ng K, Zhao R et al (2010) Epigenetic memory in induced pluripotent stem cells. Nature 467:285-290
16. Fernandez N, Cooper J, Sprinks M, AbdElrahman M, Fiszer D et al (1999) A critical review of the role of the major histocompatibility complex in fertilization, preimplantation development and feto-maternal interactions. Hum Reprod Update 5: 234-248
17. Lei T, Jacob S, Ajil-Zaraa I, Dubuisson JB, Irion O et al (2007) Xeno-free derivation and culture of human embryonic stem cells: current status, problems and challenges. Cell Res 17:682-688
18. Tangvoranuntakul P, Gagneux P, Diaz S, Bardor M, Varki N et al (2003) Human uptake and incorporation of an immunogenic nonhuman dietary sialic acid. Proc Natl Acad Sci U S A 100:12045-12050
19. Chou HH, Takematsu H, Diaz S, Iber J, Nickerson E et al (1998) A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence. Proc Natl Acad Sci U S A 95:11751-11756
20. Cerdan C, Bendall SC, Wang L, Stewart M, Werbowetski T et al (2006) Complement targeting of nonhuman sialic acid does not mediate cell death of human embryonic stem cells. Nat Med 12:1113-1114, author reply 1115
21. Ludwig TE, Levenstein ME, Jones JM, Berggren WT, Mitchen ER et al (2006) Derivation of human embryonic stem cells in defined conditions. Nat Biotechnol 24: 185-187
22. Mallon BS, Park KY, Chen KG, Hamilton RS, McKay RD (2006) Toward xeno-free culture of human embryonic stem cells. Int J Biochem Cell Biol 38:1063-1075
23. Xu C, Inokuma MS, Denham J, Golds K, Kundu P et al (2001) Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 19:971-974
24. Prowse AB, Doran MR, Cooper-White JJ, Chong F, Munro TP et al (2010) Long term culture of human embryonic stem cells on recombinant vitronectin in ascorbate free media. Biomaterials 31:8281-8288
25. Rajala K, Hakala H, Panula S, Aivio S, Pihlajamaki H et al (2007) Testing of nine different xeno-free culture media for human embryonic stem cell cultures. Hum Reprod 22:1231-1238
26. Newman AM, Cooper JB (2010) Lab-specific gene expression signatures in pluripotent stem cells. Cell Stem Cell 7:258-262
27. Lefort N, Feyeux M, Bas C, Feraud O, Bennaceur-Griscelli A et al (2008) Human embryonic stem cells reveal recurrent genomic instability at 20q11.21. Nat Biotechnol 26:1364-1366
28. Werbowetski-Ogilvie TE, Bosse M, Stewart M, Schnerch A, Ramos-Mejia V et al (2009) Characterization of human embryonic stem cells with features of neoplastic progression. Nat Biotechnol 27:91-97
29. Herszfeld D, Wolvetang E, Langton-Bunker E, Chung TL, Filipczyk AA et al (2006) CD30 is a survival factor and a biomarker for transformed human pluripotent stem cells. Nat Biotechnol 24:351-357
30. Al-Shamkhani A (2004) The role of CD30 in the pathogenesis of haematopoietic malignancies. Curr Opin Pharmacol 4:355-359
31. Marchetto MC, Yeo GW, Kainohana O, Marsala M, Gage FH et al (2009) Transcriptional signature and memory retention of human-induced pluripotent stem cells. PLoS One 4:e7076
32. Zhao T, Zhang ZN, Rong Z, Xu Y (2011) Immunogenicity of induced pluripotent stem cells. Nature 474:212-215
33. Stelzer Y, Yanuka O, Benvenisty N (2011) Global analysis of parental imprinting in human parthenogenetic induced pluripotent stem cells. Nat Struct Mol Biol 18:735-741
34. Guenther MG, Frampton GM, Soldner F, Hockemeyer D, Mitalipova M et al (2010) Chromatin structure and gene expression programs of human embryonic and induced pluripotent stem cells. Cell Stem Cell 7:249-257
35. Hochedlinger K, Jaenisch R (2003) Nuclear transplantation, embryonic stem cells, and the potential for cell therapy. N Engl J Med 349:275-286
36. Adewumi O, Aflatoonian B, Ahrlund-Richter L, Amit M, Andrews PW et al (2007) Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat Biotechnol 25:803-816
37. Moore JC, Sadowy S, Alikani M, Toro-Ramos AJ, Swerdel MR et al (2010) A high- resolution molecular-based panel of assays for identification and characterization of human embryonic stem cell lines. Stem Cell Res 4:92-106
38. Akopian V, Andrews PW, Beil S, Benvenisty N, Brehm J et al (2010) Comparison of defined culture systems for feeder cell free propagation of human embryonic stem cells. In Vitro Cell Dev Biol Anim 46:247-258
39. Zeng F, Zhou Q, Tannenbaum S (2009) Consensus guidance for banking and supply of human embryonic stem cell lines for research purposes. Stem Cell Rev 5:301-314
40. Sprinks MT, Sellens MH, Dealtry GB, Fernandez N (1993) Preimplantation mouse embryos express Mhc class I genes before the first cleavage division. Immunogenetics 38: 35-40
41. Cooper JC, Fernandez N, Joly E, Dealtry GB (1998) Regulation of major histocompatibility complex and TAP gene products in preimplantation mouse stage embryos. Am J Reprod Immunol 40:165-171
42. Suarez-Alvarez B, Rodriguez RM, Calvanese V, Blanco-Gelaz MA, Suhr ST et al (2010) Epigenetic mechanisms regulate MHC and antigen processing molecules in human embryonic and induced pluripotent stem cells. PLoS One 5:e10192
43. Jurisicova A, Casper RF, MacLusky NJ, Mills GB, Librach CL (1996) HLA-G expression during preimplantation human embryo development. Proc Natl Acad Sci U S A 93: 161-165
44. Drukker M, Katchman H, Katz G, Even-Tov Friedman S, Shezen E et al (2006) Human embryonic stem cells and their differentiated derivatives are less susceptible to immune rejection than adult cells. Stem Cells 24:221-229
45. Mammolenti M, Gajavelli S, Tsoulfas P, Levy R (2004) Absence of major histocompatibility complex class I on neural stem cells does not permit natural killer cell killing and prevents recognition by alloreactive cytotoxic T lymphocytes in vitro. Stem Cells 22:1101-1110
46. Wu DC, Boyd AS, Wood KJ (2008) Embryonic stem cells and their differentiated derivatives have a fragile immune privilege but still represent novel targets of immune attack. Stem Cells 26:1939-1950
47. Boyd AS, Wood KJ (2009) Variation in MHC expression between undifferentiated mouse ES cells and ES cell-derived insulin-producing cell clusters. Transplantation 87:1300-1304
48. Lampton PW, Crooker RJ, Newmark JA, Warner CM (2008) Expression of major histocompatibility complex class I proteins and their antigen processing chaperones in mouse embryonic stem cells from fertilized and parthenogenetic embryos. Tissue Antigens 72:448-457
49. Utermohlen O, Baschuk N, Abdullah Z, Engelmann A, Siebolts U et al (2009) Immunologic hurdles of therapeutic stem cell transplantation. Biol Chem 390:977-983
50. Dressel R, Guan K, Nolte J, Elsner L, Monecke S et al (2009) Multipotent adult germ-line stem cells, like other pluripotent stem cells, can be killed by cytotoxic T lymphocytes despite low expression of major histocompatibility complex class I molecules. Biol Direct 4:31
51. Robertson NJ, Brook FA, Gardner RL, Cobbold SP, Waldmann H et al (2007) Embryonic stem cell-derived tissues are immunogenic but their inherent immune privilege promotes the induction of tolerance. Proc Natl Acad Sci U S A 104:20920-20925
52. Swijnenburg RJ, Schrepfer S, Govaert JA, Cao F, RansohoffK et al (2008) Immunosuppressive therapy mitigates immunological rejection of human embryonic stem cell xenografts. Proc Natl Acad Sci U S A 105:12991-12996
53. Yen BL, Chang CJ, Liu KJ, Chen YC, Hu HI et al (2009) Brief report-human embryonic stem cell-derived mesenchymal progenitors possess strong immunosuppressive effects toward natural killer cells as well as T lymphocytes. Stem Cells 27:451-456
54. Rideout WM III, Hochedlinger K, Kyba M, Daley GQ, Jaenisch R (2002) Correction of a genetic defect by nuclear transplantation and combined cell and gene therapy. Cell 109:17-27
55. Evans MJ, Gurer C, Loike JD, Wilmut I, Schnieke AE et al (1999) Mitochondrial DNA genotypes in nuclear transfer-derived cloned sheep. Nat Genet 23:90-93
56. Lanza RP, Chung HY, Yoo JJ, Wettstein PJ, Blackwell C et al (2002) Generation of histocompatible tissues using nuclear transplantation. Nat Biotechnol 20:689-696
57. Lui KO, Boyd AS, Cobbold SP, Waldmann H, Fairchild PJ (2010) A role for regulatory T cells in acceptance of embryonic stem cellderived tissues transplanted across an MHC barrier. Stem Cells 28(10):1905-1914
58. Grinnemo KH, Genead R, Kumagai-Braesch M, Andersson A, Danielsson C et al (2008) Costimulation blockade induces tolerance to HESC transplanted to the testis and induces regulatory T-cells to HESC transplanted into the heart. Stem Cells 26:1850-1857
59. Nitta T, Murata S, Ueno T, Tanaka K, Takahama Y (2008) Thymic microenvironments for T-cell repertoire formation. Adv Immunol 99:59-94
60. Gardner JM, Fletcher AL, Anderson MS, Turley SJ (2009) AIRE in the thymus and beyond. Curr Opin Immunol 21:582-589
61. Res P, Spits H (1999) Developmental stages in the human thymus. Semin Immunol 11:39-46
62. Haynes BF, Heinly CS (1995) Early human T cell development: analysis of the human thymus at the time of initial entry of hematopoietic stem cells into the fetal thymic microenvironment. J Exp Med 181:1445-1458
63. Nagano K, Yoshida Y, Isobe T (2008) Cell surface biomarkers of embryonic stem cells. Proteomics 8:4025-4035
64. Kannagi R, Cochran NA, Ishigami F, Hakomori S, Andrews PW et al (1983) Stagespecific embryonic antigens (SSEA-3 and -4) are epitopes of a unique globo-series ganglioside isolated from human teratocarcinoma cells. EMBO J 2:2355-2361
65. Shevinsky LH, Knowles BB, Damjanov I, Solter D (1982) Monoclonal antibody to murine embryos defines a stage-specific embryonic antigen expressed on mouse embryos and human teratocarcinoma cells. Cell 30:697-705
66. Tang C, Lee AS, Volkmer JP, Sahoo D, Nag D et al (2011) An antibody against SSEA-5 glycan on human pluripotent stem cells enables removal of teratoma-forming cells. Nat Biotechnol 29(9):829-834
67. Schopperle WM, DeWolf WC (2007) The TRA-1-60 and TRA-1-81 human pluripotent stem cell markers are expressed on podocalyxin in embryonal carcinoma. Stem Cells 25:723-730
68. Brimble SN, Sherrer ES, Uhl EW, Wang E, Kelly S et al (2007) The cell surface glycosphingolipids SSEA-3 and SSEA-4 are not essential for human ESC pluripotency. Stem Cells 25:54-62
69. Li Y, Zeng H, Xu RH, Liu B, Li Z (2009) Vaccination with human pluripotent stem cells generates a broad spectrum of immunological and clinical responses against colon cancer. Stem Cells 27:3103-3111
70. Siegel S, Wagner A, Kabelitz D, Marget M, Coggin J Jr et al (2003) Induction of cytotoxic T-cell responses against the oncofetal antigen-immature laminin receptor for the treatment of hematologic malignancies. Blood 102:4416-4423
71. Zelle-Rieser C, Barsoum AL, Sallusto F, Ramoner R, Rohrer JW et al (2001) Expression and immunogenicity of oncofetal antigen-immature laminin receptor in human renal cell carcinoma. J Urol 165:1705-1709
72. Tchabo NE, Mhawech-Fauceglia P, Caballero OL, Villella J, Beck AF et al (2009) Expression and serum immunoreactivity of developmentally restricted differentiation antigens in epithelial ovarian cancer. Cancer Immun 9:6
73. Dong W, Du J, Shen H, Gao D, Li Z et al (2010) Administration of embryonic stem cells generates effective antitumor immunity in mice with minor and heavy tumor load. Cancer Immunol Immunother 59:1697-1705
74. Jonsson AH, Yokoyama WM (2009) Natural killer cell tolerance licensing and other mechanisms. Adv Immunol 101:27-79
75. Yokoyama WM, Kim S (2006) How do natural killer cells find self to achieve tolerance? Immunity 24:249-257
76. Orr MT, Lanier LL (2010) Natural killer cell education and tolerance. Cell 142:847-856
77. Borrego F (2006) The first molecular basis of the "missing self" hypothesis. J Immunol 177:5759-5760
78. Frenzel LP, Abdullah Z, Kriegeskorte AK, Dieterich R, Lange N et al (2009) 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 27:307-316
79. Preynat-Seauve O, de Rham C, Tirefort D, Ferrari-Lacraz S, Krause KH et al (2009) Neural progenitors derived from human embryonic stem cells are targeted by allogeneic T and natural killer cells. J Cell Mol Med 13:3556-3569
80. Dressel R, Schindehutte J, Kuhlmann T, Elsner L, Novota P et al (2008) The tumorigenicity of mouse embryonic stem cells and in vitro differentiated neuronal cells is controlled by the recipients' immune response. PLoS One 3:e2622
81. Dressel R, Nolte J, Elsner L, Novota P, Guan K et al (2010) Pluripotent stem cells are highly susceptible targets for syngeneic, allogeneic, and xenogeneic natural killer cells. FASEB J 24(7):2164-2177
82. Trowsdale J, Betz AG (2006) Mother's little helpers: mechanisms of maternal-fetal tolerance. Nat Immunol 7:241-246
83. Revazova ES, Turovets NA, Kochetkova OD, Agapova LS, Sebastian JL et al (2008) HLA homozygous stem cell lines derived from human parthenogenetic blastocysts. Cloning Stem Cells 10:11-24
84. Kovats S, Main EK, Librach C, Stubblebine M, Fisher SJ et al (1990) A class I antigen, HLA-G, expressed in human trophoblasts. Science 248:220-223
85. Magliocca JF, Held IK, Odorico JS (2006) 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 15:707-717
86. Li L, Baroja ML, Majumdar A, Chadwick K, Rouleau A et al (2004) Human embryonic stem cells possess immune-privileged properties. Stem Cells 22:448-456
87. Guller S, LaChapelle L (1999) The role of placental Fas ligand in maintaining immune privilege at maternal-fetal interfaces. Semin Reprod Endocrinol 17:39-44
88. Yachimovich-Cohen N, Even-Ram S, Shufaro Y, Rachmilewitz J, Reubinoff B (2010) Human embryonic stem cells suppress T cell responses via arginase I-dependent mechanism. J Immunol 184:1300-1308
89. Bronte V, Zanovello P (2005) Regulation of immune responses by L-arginine metabolism. Nat Rev Immunol 5:641-654
90. Ishikawa T, Harada T, Koi H, Kubota T, Azuma H et al (2007) Identification of arginase in human placental villi. Placenta 28:133-138
91. Kropf P, Baud D, Marshall SE, Munder M, Mosley A et al (2007) Arginase activity mediates reversible T cell hyporesponsiveness in human pregnancy. Eur J Immunol 37:935-945
92. Koch CA, Geraldes P, Platt JL (2008) Immunosuppression by embryonic stem cells. Stem Cells 26:89-98
93. Trigona WL, Porter CM, Horvath- Arcidiacono JA, Majumdar AS, Bloom ET (2007) Could heme-oxygenase-1 have a role in modulating the recipient immune response to embryonic stem cells? Antioxid Redox Signal 9:751-756
94. Fandrich F, Lin X, Chai GX, Schulze M, Ganten D et al (2002) Preimplantation-stage stem cells induce long-term allogeneic graft acceptance without supplementary host conditioning. Nat Med 8:171-178
95. Fabricius D, Bonde S, Zavazava N (2005) Induction of stable mixed chimerism by embryonic stem cells requires functional Fas/FasL engagement. Transplantation 79: 1040-1044
96. Bonde S, Zavazava N (2006) Immunogenicity and engraftment of mouse embryonic stem cells in allogeneic recipients. Stem Cells 24:2192-2201
97. Hunt JS, Vassmer D, Ferguson TA, Miller L (1997) Fas ligand is positioned in mouse uterus and placenta to prevent trafficking of activated leukocytes between the mother and the conceptus. J Immunol 158: 4122-4128
98. Brunlid G, Pruszak J, Holmes B, Isacson O, Sonntag KC (2007) Immature and neurally differentiated mouse embryonic stem cells do not express a functional Fas/Fas ligand system. Stem Cells 25:2551-2558
99. Lee AS, Tang C, Cao F, Xie X, van der Bogt K et al (2009) Effects of cell number on teratoma formation by human embryonic stem cells. Cell Cycle 8:2608-2612
100. Pearl JI, Lee AS, Leveson-Gower DB, Sun N, Ghosh Z et al (2011) Short-term immunosuppression promotes engraftment of embryonic and induced pluripotent stem cells. Cell Stem Cell 8:309-317
101. Matzinger P, Kamala T (2011) Tissue-based class control: the other side of tolerance. Nat Rev Immunol 11:221-230
102. Ferguson TA, Griffith TS (2006) A vision of cell death: Fas ligand and immune privilege 10 years later. Immunol Rev 213: 228-238
103. Engelhardt B, Coisne C (2011) Fluids and barriers of the CNS establish immune privilege by confining immune surveillance to a two-walled castle moat surrounding the CNS castle. Fluids Barriers CNS 8:4
104. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ et al (1998) Embryonic stem cell lines derived from human blastocysts. Science 282:1145-114