The potential for immunogenicity of autologous induced pluripotent stem cell-derived therapies

Journal of Biological Chemistry

Volumn 289, Issue 8, 2014, Pages 4571-4577

  Scheiner, Zachary S ^a   Talib, Sohel ^a   Feigal, Ellen G ^a  

^a California Institute for Regenerative Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

STEM CELLS;

CELL THERAPY; CLINICAL TESTING; DEVELOPING STRATEGY; IMMUNE RESPONSE; IMMUNOGENICITY; INDUCED PLURIPOTENT STEM CELLS; PLURIPOTENT;

DISEASE CONTROL;

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1;

AUTOLOGOUS STEM CELL TRANSPLANTATION; CELLULAR IMMUNITY; DOPAMINERGIC NERVE CELL; EMBRYONIC STEM CELL; GENE EXPRESSION; HUMAN; IMMUNOGENICITY; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTIC INFILTRATION; NATURAL KILLER CELL; NONHUMAN; PARKINSON DISEASE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TERATOMA;

CELL THERAPY; CELLULAR IMMUNE RESPONSE; HUMORAL RESPONSE; INDUCED PLURIPOTENT STEM CELLS; INNATE IMMUNITY; IPSC;

ANIMALS; CLINICAL TRIALS AS TOPIC; HUMANS; INDUCED PLURIPOTENT STEM CELLS; STEM CELL TRANSPLANTATION; TRANSPLANTATION, AUTOLOGOUS;

EID: 84894433856     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.R113.509588     Document Type: Review

References (66)

1. Takahashi, K., and Yamanaka, S. (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663-676
2. Takahashi, K., Tanabe, K., Ohnuki, M., Narita, M., Ichisaka, T., Tomoda, K., and Yamanaka, S. (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131, 861-872
3. Nishikawa, S., Goldstein, R. A., and Nierras, C. R. (2008) The promise of human induced pluripotent stem cells for research and therapy. Nat. Rev. Mol. Cell Biol. 9, 725-729
4. Yamanaka, S. (2008) Pluripotency and nuclear reprogramming. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363, 2079-2087
5. Zhao, R., and Daley, G. Q. (2008) From fibroblasts to iPS cells: induced pluripotency by defined factors. J. Cell. Biochem. 105, 949-955
6. Fairchild, P. J. (2010) The challenge of immunogenicity in the quest for induced pluripotency. Nat. Rev. Immunol. 10, 868-875
7. Kadereit, S., and Trounson, A. (2011) In vitro immunogenicity of undifferentiated pluripotent stem cells (PSC) and derived lineages. Semin. Immunopathol. 33, 551-562
8. Tang, C., and Drukker, M. (2011) Potential barriers to therapeutics utilizing pluripotent cell derivatives: intrinsic immunogenicity of in vitro maintained and matured populations. Semin. Immunopathol. 33, 563-572
9. Zhao, T., Zhang, Z. N., Rong, Z., and Xu, Y. (2011) Immunogenicity of induced pluripotent stem cells. Nature 474, 212-215
10. Araki, R., Uda, M., Hoki, Y., Sunayama, M., Nakamura, M., Ando, S., Sugiura, M., Ideno, H., Shimada, A., Nifuji, A., and Abe, M. (2013) Negligible immunogenicity of terminally differentiated cells derived from induced pluripotent or embryonic stem cells. Nature 494, 100-104
11. Guha, P., Morgan, J. W., Mostoslavsky, G., Rodrigues, N. P., and Boyd, A. S. (2013) Lack of immune response to differentiated cells derived from syngeneic induced pluripotent stem cells. Cell Stem Cell 12, 407-412
12. Morizane, A., Doi, D., Kikuchi, T., Okita, K., Hotta, A., Kawasaki, T., Hayashi, T., Onoe, H., Shiina, T., Yamanaka, S., and Takahashi, J. (2013) Direct comparison of autologous and allogeneic transplantation of iPSCderived neural cells in the brain of a nonhuman primate. Stem Cell Rep. 1, 283-292
13. Okita, K., Nagata, N., and Yamanaka, S. (2011) Immunogenicity of induced pluripotent stem cells. Circ. Res. 109, 720-721
14. Barrilleaux, B., and Knoepfler, P. S. (2011) Inducing iPSCs to escape the dish. Cell Stem Cell 9, 103-111
15. Freed, C. R., Greene, P. E., Breeze, R. E., Tsai, W. Y., DuMouchel, W., Kao, R., Dillon, S., Winfield, H., Culver, S., Trojanowski, J. Q., Eidelberg, D., and Fahn, S. (2001) Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N. Engl. J. Med. 344, 710-719
16. Kordower, J. H., Chu, Y., Hauser, R. A., Freeman, T. B., and Olanow, C. W. (2008) Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat. Med. 14, 504-506
17. Mendez, I., Viñuela, A., Astradsson, A., Mukhida, K., Hallett, P., Robertson, H., Tierney, T., Holness, R., Dagher, A., Trojanowski, J. Q., and Isacson, O. (2008) Dopamine neurons implanted into people with Parkinson's disease survive without pathology for 14 years. Nat. Med. 14, 507-509
18. Prokhorova, T. A., Harkness, L. M., Frandsen, U., Ditzel, N., Schrøder, H. D., Burns, J. S., and Kassem, M. (2009) Teratoma formation by human embryonic stem cells is site dependent and enhanced by the presence of Matrigel. Stem Cells Dev. 18, 47-54
19. Mummery, C. L., Zhang, J., Ng, E. S., Elliott, D. A., Elefanty, A. G., and Kamp, T. J. (2012) Differentiation of human embryonic stem cells and induced pluripotent stem cells to cardiomyocytes: a methods overview. Circ. Res. 111, 344-358
20. Panopoulos, A. D., and Belmonte, J. C. (2012) Induced pluripotent stem cells in clinical hematology: potentials, progress, and remaining obstacles. Curr. Opin. Hematol. 19, 256-260
21. Rountree, C. B., Mishra, L., and Willenbring, H. (2012) Stem cells in liver diseases and cancer: recent advances on the path to new therapies. Hepatology 55, 298-306
22. Mayhew, C. N., and Wells, J. M. (2010) Converting human pluripotent stem cells into beta-cells: recent advances and future challenges. Curr. Opin. Organ Transplant. 15, 54-60
23. Hanna, J., Wernig, M., Markoulaki, S., Sun, C. W., Meissner, A., Cassady, J. P., Beard, C., Brambrink, T., Wu, L. C., Townes, T. M., and Jaenisch, R. (2007) Treatment of sickle cell anemia mouse model with iPS cells generated from autologous skin. Science 318, 1920-1923
24. Simpson, A. J., Caballero, O. L., Jungbluth, A., Chen, Y. T., and Old, L. J. (2005) Cancer/testis antigens, gametogenesis and cancer. Nat. Rev. Cancer 5, 615-625
25. Tchabo, N. E., Mhawech-Fauceglia, P., Caballero, O. L., Villella, J., Beck, A. F., Miliotto, A. J., Liao, J., Andrews, C., Lele, S., Old, L. J., and Odunsi, K. (2009) Expression and serum immunoreactivity of developmentally restricted differentiation antigens in epithelial ovarian cancer. Cancer Immun. 9, 6
26. Kim, K., Zhao, R., Doi, A., Ng, K., Unternaehrer, J., Cahan, P., Huo, H., Loh, Y. H., Aryee, M. J., Lensch, M. W., Li, H., Collins, J. J., Feinberg, A. P., and Daley, G. Q. (2011) Donor cell type can influence the epigenome and differentiation potential of human induced pluripotent stem cells. Nat. Biotechnol. 29, 1117-1119
27. Chin, M. H., Mason, M. J., Xie, W., Volinia, S., Singer, M., Peterson, C., Ambartsumyan, G., Aimiuwu, O., Richter, L., Zhang, J., Khvorostov, I., Ott, V., Grunstein, M., Lavon, N., Benvenisty, N., Croce, C. M., Clark, A. T., Baxter, T., Pyle, A. D., Teitell, M. A., Pelegrini, M., Plath, K., and Lowry, W. E. (2009) Induced pluripotent stem cells and embryonic stem cells are distinguished by gene expression signatures. Cell Stem Cell 5, 111-123
28. Doi, A., Park, I. H., Wen, B., Murakami, P., Aryee, M. J., Irizarry, R., Herb, B., Ladd-Acosta, C., Rho, J., Loewer, S., Miller, J., Schlaeger, T., Daley, G. Q., and Feinberg, A. P. (2009) Differential methylation of tissue-and cancer-specific CpG island shores distinguishes human induced pluripotent stem cells, embryonic stem cells and fibroblasts. Nat. Genet. 41, 1350-1353
29. Kim, K., Doi, A., Wen, B., Ng, K., Zhao, R., Cahan, P., Kim, J., Aryee, M. J., Ji, H., Ehrlich, L. I., Yabuuchi, A., Takeuchi, A., Cunniff, K. C., Hongguang, H., McKinney-Freeman, S., Naveiras, O., Yoon, T. J., Irizarry, R. A., Jung, N., Seita, J., Hanna, J., Murakami, P., Jaenisch, R., Weissleder, R., Orkin, S. H., Weissman, I. L., Feinberg, A. P., and Daley, G. Q. (2010) Epigenetic memory in induced pluripotent stem cells. Nature 467, 285-290
30. Lister, R., Pelizzola, M., Kida, Y. S., Hawkins, R. D., Nery, J. R., Hon, G., Antosiewicz-Bourget, J., O'Malley, R., Castanon, R., Klugman, S., Downes, M., Yu, R., Stewart, R., Ren, B., Thomson, J. A., Evans, R. M., and Ecker, J. R. (2011) Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 471, 68-73
31. Gore, A., Li, Z., Fung, H. L., Young, J. E., Agarwal, S., Antosiewicz-Bourget, J., Canto, I., Giorgetti, A., Israel, M. A., Kiskinis, E., Lee, J. H., Loh, Y. H., Manos, P. D., Montserrat, N., Panopoulos, A. D., Ruiz, S., Wilbert, M. L., Yu, J., Kirkness, E. F., Izpisua Belmonte, J. C., Rossi, D. J., Thomson, J. A., Eggan, K., Daley, G. Q., Goldstein, L. S., and Zhang, K. (2011) Somatic coding mutations in human induced pluripotent stem cells. Nature 471, 63-67
32. Ruiz, S., Gore, A., Li, Z., Panopoulos, A. D., Montserrat, N., Fung, H. L., Giorgetti, A., Bilic, J., Batchelder, E. M., Zaehres, H., Schöler, H. R., Zhang, K., and Izpisua Belmonte, J. C. (2013) Analysis of protein-coding mutations in hiPSCs and their possible role during somatic cell reprogramming. Nat. Commun. 4, 1382
33. Taapken, S. M., Nisler, B. S., Newton, M. A., Sampsell-Barron, T. L., Leonhard, K. A., McIntire, E. M., and Montgomery, K. D. (2011) Karotypic abnormalities in human induced pluripotent stem cells and embryonic stem cells. Nat. Biotechnol. 29, 313-314
34. Draper, J. S., Smith, K., Gokhale, P., Moore, H. D., Maltby, E., Johnson, J., Meisner, L., Zwaka, T. P., Thomson, J. A., and Andrews, P. W. (2004) Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nat. Biotechnol. 22, 53-54
35. Martins-Taylor, K., Nisler, B. S., Taapken, S. M., Compton, T., Crandall, L., Montgomery, K. D., Lalande, M., and Xu, R. H. (2011) Recurrent copy number variations in human induced pluripotent stem cells. Nat. Biotechnol. 29, 488-491
36. Martin, M. J., Muotri, A., Gage, F., and Varki, A. (2005) Human embryonic stem cells express an immunogenic nonhuman sialic acid. Nat. Med. 11, 228-232
37. Tangvoranuntakul, P., Gagneux, P., Diaz, S., Bardor, M., Varki, N., Varki, A., and Muchmore, E. (2003) Human uptake and incorporation of an immunogenic nonhuman dietary sialic acid. Proc. Natl. Acad. Sci. U.S.A. 100, 12045-12050
38. Hayashi, Y., Chan, T., Warashina, M., Fukuda, M., Ariizumi, T., Okabayashi, K., Takayama, N., Otsu, M., Eto, K., Furue, M. K., Michiue, T., Ohnuma, K., Nakauchi, H., and Asashima, M. (2010) Reduction of Nglycolylneuraminic acid in human induced pluripotent stem cells generated or cultured under feeder-and serum-free defined conditions. PLoS ONE 5, e14099
39. Rodríguez-Pizà, I., Richaud-Patin, Y., Vassena, R., González, F., Barrero, M. J., Veiga, A., Raya, A., and Izpisúa Belmonte, J. C. (2010) Reprogramming of human fibroblasts to induced pluripotent stem cells under xenofree conditions. Stem Cells 28, 36-44
40. Swistowski, A., Peng, J., Liu, Q., Mali, P., Rao, M. S., Cheng, L., and Zeng, X. (2010) Efficient generation of functional dopaminergic neurons from human induced pluripotent stem cells under defined conditions. Stem Cells 28, 1893-1904
41. Chung, T. L., Turner, J. P., Thaker, N. Y., Kolle, G., Cooper-White, J. J., Grimmond, S. M., Pera, M. F., and Wolvetang, E. J. (2010) Ascorbate promotes epigenetic activation of CD30 in human embryonic stem cells. Stem Cells 28, 1782-1793
42. Wang, J., Lozier, J., Johnson, G., Kirshner, S., Verthelyi, D., Pariser, A., Shores, E., and Rosenberg, A. (2008) Neutralizing antibodies to therapeutic enzymes: considerations for testing, prevention and treatment. Nat. Biotechnol. 26, 901-908
43. Rock, K. L., and Kono, H. (2008) The inflammatory response to cell death. Annu. Rev. Pathol. 3, 99-126
44. Gebauer, B. S., Hricik, D. E., Atallah, A., Bryan, K., Riley, J., Tary-Lehmann, M., Greenspan, N. S., Dejelo, C., Boehm, B. O., Hering, B. J., and Heeger, P. S. (2002) Evolution of the enzyme-linked immunosorbent spot assay for post-transplant alloreactivity as a potentially useful immune monitoring tool. Am. J. Transplant. 2, 857-866
45. Augustine, J. J., and Hricik, D. E. (2012) T-cell immune monitoring by the ELISPOT assay for interferon. Clin. Chim. Acta 413, 1359-1363
46. Okamura, R. M., Lebkowski, J., Au, M., Priest, C. A., Denham, J., and Majumdar, A. S. (2007) Immunological properties of human embryonic stem cell-derived oligodendrocyte progenitor cells. J. Neuroimmunol. 192, 134-144
47. Bruckner, S., Wang, L., Yuan, R., Haaland, P., and Gaur, A. (2011) Flowbased combinatorial antibody profiling: an integrated approach to cell characterization. Methods Mol. Biol. 699, 97-118
48. Swijnenburg, R. J., Schrepfer, S., Govaert, J. A., Cao, F., Ransohoff, K., Sheikh, A. Y., Haddad, M., Connolly, A. J., Davis, M. M., Robbins, R. C., and Wu, J. C. (2008) Immunosuppressive therapy mitigates immunological rejection of human embryonic stem cell xenografts. Proc. Natl. Acad. Sci. U.S.A. 105, 12991-12996
49. Gutierrez-Dalmau, A., and Campistol, J. M. (2007) Immunosuppressive therapy and malignancy in organ transplant recipients: a systematic review. Drugs 67, 1167-1198
50. Pearl, J. I., Lee, A. S., Leveson-Gower, D. B., Sun, N., Ghosh, Z., Lan, F., Ransohoff, J., Negrin, R. S., Davis, M. M., and Wu, J. C. (2011) Short-term immunosuppression promotes engraftment of embryonic and induced pluripotent stem cells. Cell Stem Cell 8, 309-317
51. Dhodapkar, M. V., and Steinman, R. M. (2002) Antigen-bearing immature dendritic cells induce peptide-specific CD8+ regulatory T cells in vivo in humans. Blood 100, 174-177
52. Anderson, G., Lane, P. J., and Jenkinson, E. J. (2007) Generating intrathymic microenvironments to establish T-cell tolerance. Nat. Rev. Immunol. 7, 954-963
53. Parent, A. V., Russ, H. A., Khan, I. S., LaFlam, T. N., Metzger, T. C., Anderson, M. S., and Hebrok, M. (2013) Generation of functional thymic epithelium from human embryonic stem cells that supports host T cell development. Cell Stem Cell 13, 219-229
54. Sun, X.,Xu, J., Lu,H., Liu, W., Miao, Z., Sui, X., Liu, H., Su, L., Du, W., He, Q., Chen, F., Shi, Y., and Deng, H. (2013) Directed differentiation of human embryonic stem cells into thymic epithelial progenitor-like cells reconstitutes the thymic microenvironment in vivo. Cell Stem Cell 13, 230-236
55. Bluestone, J. A., St. Clair, E. W., and Turka, L. A. (2006) CTLA4Ig: bridging the basic immunology with clinical application. Immunity 24, 233-238
56. Freeman, G. J., Long, A. J., Iwai, Y., Bourque, K., Chernova, T., Nishimura, H., Fitz, L. J., Malenkovich, N., Okazaki, T., Byrne, M. C., Horton, H. F., Fouser, L., Carter, L., Ling, V., Bowman, M. R., Carreno, B. M., Collins, M., Wood, C. R., and Honjo, T. (2000) Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J. Exp. Med. 192, 1027-1034
57. Ravishankar, B., Liu, H., Shinde, R., Chandler, P., Baban, B., Tanaka, M., Munn, D. H., Mellor, A. L., Karlsson, M. C., and McGaha, T. L. (2012) Tolerance to apoptotic cells is regulated by indoleamine 2,3-dioxygenase. Proc. Natl. Acad. Sci. U.S.A. 109, 3909-3914
58. Taylor, C. J., Peacock, S., Chaudhry, A. N., Bradley, J. A., and Bolton, E. M. (2012) Generating an iPSC bank for HLA-matched tissue transplantation based on known donor and recipient HLA types. Cell Stem Cell 11, 147-152
59. Nakatsuji, N., Nakajima, F., and Tokunaga, K. (2008) HLA-haplotype banking and iPS cells. Nat. Biotechnol. 26, 739-740
60. Gourraud, P. A., Gilson, L., Girard, M., and Peschanski, M. (2012) The role of human leukocyte antigen matching in the development of multiethnic "haplobank" of induced pluripotent stem cell lines. Stem Cells 30, 180-186
61. Baker, M. (2011) Reprogramming Rx. Nat. Med. 17, 241-243
62. Garber, K. (2013) Inducing translation. Nat. Biotechnol. 31, 483-486
63. Cyranoski, D. (2013) iPS cells in humans. Nat. Biotechnol. 31, 775
64. Cyranoski, D. (2013) Stem cells cruise to clinic. Nature 494, 413
65. Rozman, P. (2002) Platelet antigens. The role of human platelet alloantigens (HPA) in blood transfusion and transplantation. Transpl. Immunol. 10, 165-181
66. Lee, A. S., Tang, C., Rao, M. S., Weissman, I. L., and Wu, J. C. (2013) Tumorigenicity as a clinical hurdle for pluripotent stem cell therapies. Nat. Med. 19, 998-1004