Immunobiology of naïve and genetically modified HLA-class-I-knockdown human embryonic stem cells

Journal of Cell Science

Volumn 124, Issue 17, 2011, Pages 3029-3037

  Deuse, Tobias ^a,b   Seifert, Martina ^c   Phillips, Neil ^d   Fire, Andrew ^d   Tyan, Dolly ^d   Kay, Mark ^d   Tsao, Philip S ^e   Hua, Xiaoqin ^b   Velden, Joachim ^b   Eiermann, Thomas ^b   Volk, Hans Dieter ^c   Reichenspurner, Hermann ^b   Robbins, Robert C ^a   Schrepfer, Sonja ^a,b  

^a STANFORD UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d STANFORD UNIVERSITY   (United States)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

HLA class I knockdown; Human embryonic stem cells; Immunology; Rejection

Indexed keywords

CELL ANTIBODY; HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIGEN RECOGNITION; ARTICLE; BAGG ALBINO MOUSE; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; EMBRYONIC STEM CELL; GENE SILENCING; GRAFT REJECTION; HISTOLOGY; HUMAN; HUMAN CELL; IMMUNOBIOLOGY; IMMUNOCOMPETENT CELL; MACROPHAGE; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SCID MOUSE; STEM CELL TRANSPLANTATION; SURGE CAPACITY; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH2 CELL; TRANSGENIC ANIMAL;

ANIMALS; EMBRYONIC STEM CELLS; GENE KNOCKDOWN TECHNIQUES; GRAFT REJECTION; HLA ANTIGENS; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, SCID; TRANSPLANTATION, HETEROLOGOUS;

MUS;

EID: 80053937187     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.087718     Document Type: Article

References (61)

1. Anderson, D., Self, T., Mellor, I. R., Goh, G., Hill, S. J. and Denning, C. (2007). Transgenic enrichment of cardiomyocytes from human embryonic stem cells. Mol. Ther. 15, 2027-2036.
2. Beggs, K. J., Lyubimov, A., Borneman, J. N., Bartholomew, A., Moseley, A., Dodds, R., Archambault, M. P., Smith, A. K. and McIntosh, K. R. (2006). Immunologic consequences of multiple, high-dose administration of allogeneic mesenchymal stem cells to baboons. Cell Transplant. 15, 711-721.
3. Beyer, F., Doebis, C., Busch, A., Ritter, T., Mhashilkar, A., Marasco, W. M., Laube, H., Volk, H. D. and Seifert, M. (2004). Decline of surface MHC I by adenoviral gene transfer of anti-MHC I intrabodies in human endothelial cells-new perspectives for the generation of universal donor cells for tissue transplantation. J. Gene Med. 6, 616-623.
4. Bonde, S. and Zavazava, N. (2006). Immunogenicity and engraftment of mouse embryonic stem cells in allogeneic recipients. Stem Cells 24, 2192-2201.
5. Bryceson, Y. T., March, M. E., Ljunggren, H. G. and Long, E. O. (2006). Activation, coactivation, and costimulation of resting human natural killer cells. Immunol. Rev. 214, 73-91.
6. Burridge, P. W., Anderson, D., Priddle, H., Barbadillo Munoz, M. D., Chamberlain, S., Allegrucci, C., Young, L. E. and Denning, C. (2007). Improved human embryonic stem cell embryoid body homogeneity and cardiomyocyte differentiation from a novel V-96 plate aggregation system highlights interline variability. Stem Cells 25, 929-938.
7. Busch, A., Marasco, W. A., Doebis, C., Volk, H. D. and Seifert, M. (2004). MHC class I manipulation on cell surfaces by gene transfer of anti-MHC class I intrabodies-a tool for decreased immunogenicity of allogeneic tissue and cell transplants. Methods 34, 240-249.
8. Campeau, E., Ruhl, V. E., Rodier, F., Smith, C. L., Rahmberg, B. L., Fuss, J. O., Campisi, J., Yaswen, P., Cooper, P. K. and Kaufman, P. D. (2009). A versatile viral system for expression and depletion of proteins in mammalian cells. PLoS ONE 4, e6529.
9. Cao, F., Lin, S., Xie, X., Ray, P., Patel, M., Zhang, X., Drukker, M., Dylla, S. J., Connolly, A. J., Chen, X. et al. (2006). In vivo visualization of embryonic stem cell survival, proliferation, and migration after cardiac delivery. Circulation 113, 1005-1014.
10. Caplen, N. J., Parrish, S., Imani, F., Fire, A. and Morgan, R. A. (2001). Specific inhibition of gene expression by small double-stranded RNAs in invertebrate and vertebrate systems. Proc. Natl. Acad. Sci. USA 98, 9742-9747.
11. Caspi, O., Huber, I., Kehat, I., Habib, M., Arbel, G., Gepstein, A., Yankelson, L., Aronson, D., Beyar, R. and Gepstein, L. (2007). Transplantation of human embryonic stem cell-derived cardiomyocytes improves myocardial performance in infarcted rat hearts. J. Am. College Cardiol. 50, 1884-1893.
12. Cerwenka, A., Baron, J. L. and Lanier, L. L. (2001). Ectopic expression of retinoic acid early inducible-1 gene (RAE-1) permits natural killer cell-mediated rejection of a MHC class I-bearing tumor in vivo. Proc. Natl. Acad. Sci. USA 98, 11521-11526.
13. Chidgey, A. P., Layton, D., Trounson, A. and Boyd, R. L. (2008). Tolerance strategies for stem-cell-based therapies. Nature 453, 330-337.
14. Cho, P. S., Messina, D. J., Hirsh, E. L., Chi, N., Goldman, S. N., Lo, D. P., Harris, I. R., Popma, S. H., Sachs, D. H. and Huang, C. A. (2008). Immunogenicity of umbilical cord tissue derived cells. Blood 111, 430-438.
15. Daley, G. Q. and Scadden, D. T. (2008). Prospects for stem cell-based therapy. Cell 132, 544-548.
16. Domian, I. J., Chiravuri, M., van der Meer, P., Feinberg, A. W., Shi, X., Shao, Y., Wu, S. M., Parker, K. K. and Chien, K. R. (2009). Generation of functional ventricular heart muscle from mouse ventricular progenitor cells. Science 326, 426-429.
17. Dressel, R., Schindehutte, J., Kuhlmann, T., Elsner, L., Novota, P., Baier, P. C., Schillert, A., Bickeboller, H., Herrmann, T., Trenkwalder, C. 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.
18. Dressel, R., Nolte, J., Elsner, L., Novota, P., Guan, K., Streckfuss-Bomeke, K., Hasenfuss, G., Jaenisch, R. and Engel, W. (2010). Pluripotent stem cells are highly susceptible targets for syngeneic, allogeneic, and xenogeneic natural killer cells. FASEB J. 24, 2164-2177.
19. Drukker, M. and Benvenisty, N. (2004). The immunogenicity of human embryonic stem-derived cells. Trends Biotechnol. 22, 136-141.
20. Drukker, M., Katz, G., Urbach, A., Schuldiner, M., Markel, G., Itskovitz-Eldor, J., Reubinoff, B., Mandelboim, O. and Benvenisty, N. (2002). Characterization of the expression of MHC proteins in human embryonic stem cells. Proc. Natl. Acad. Sci. USA 99, 9864-9869.
21. Drukker, M., Katchman, H., Katz, G., Friedman, S., Shezen, E., Hornstein, E., Mandelboim, O., Reisner, Y. and Benvenisty, N. (2006). Human embryonic stem cells and their differentiated derivatives are less susceptible to immune rejection than adult cells. Stem Cells 24, 221-229.
22. Elsner, L., Muppala, V., Gehrmann, M., Lozano, J., Malzahn, D., Bickeboller, H., Brunner, E., Zientkowska, M., Herrmann, T., Walter, L. et al. (2007). The heat shock protein HSP70 promotes mouse NK cell activity against tumors that express inducible NKG2D ligands. J. Immunol. 179, 5523-5533.
23. Frenzel, L. P., Abdullah, Z., Kriegeskorte, A. K., Dieterich, R., Lange, N., Busch, D. H., Kronke, M., Utermohlen, O., Hescheler, J. and Saric, T. (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.
24. Gonzalez, S., Castanotto, D., Li, H., Olivares, S., Jensen, M. C., Forman, S. J., Rossi, J. J. and Cooper, L. J. (2005). Amplification of RNAi-targeting HLA mRNAs. Mol. Ther. 11, 811-818.
25. Grinnemo, K. H., Genead, R., Kumagai-Braesch, M., Andersson, A., Danielsson, C., Mansson-Broberg, A., Dellgren, G., Stromberg, A. M., Ekberg, H., Hovatta, O. 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.
26. Hattori, F., Chen, H., Yamashita, H., Tohyama, S., Satoh, Y. S., Yuasa, S., Li, W., Yamakawa, H., Tanaka, T., Onitsuka, T. et al. (2010). Nongenetic method for purifying stem cell-derived cardiomyocytes. Nat. Methods 7, 61-66.
27. Kessler, L., Parissiadis, A., Bayle, F., Moreau, F., Pinget, M., Froelich, N., Cazenave, J. P., Berney, T., Benhamou, P. Y. and Hanau, D. (2009). Evidence for humoral rejection of a pancreatic islet graft and rescue with rituximab and IV immunoglobulin therapy. Am. J. Transplant. 9, 1961-1966.
28. Koch, C. A., Jordan, C. E. and Platt, J. L. (2006). Complement-dependent control of teratoma formation by embryonic stem cells. J. Immunol. 177, 4803-4809.
29. Koch, C. A., Geraldes, P. and Platt, J. L. (2008). Immunosuppression by embryonic stem cells. Stem Cells 26, 89-98.
30. Kolls, J., Peppel, K., Silva, M. and Beutler, B. (1994). Prolonged and effective blockade of tumor necrosis factor activity through adenovirus-mediated gene transfer. Proc. Natl. Acad. Sci. USA 91, 215-219.
31. Kolossov, E., Bostani, T., Roell, W., Breitbach, M., Pillekamp, F., Nygren, J. M., Sasse, P., Rubenchik, O., Fries, J. W., Wenzel, D. et al. (2006). Engraftment of engineered ES cell-derived cardiomyocytes but not BM cells restores contractile function to the infarcted myocardium. J. Exp. Med. 203, 2315-2327.
32. Komatsu, M., Mammolenti, M., Jones, M., Jurecic, R., Sayers, T. J. and Levy, R. B. (2003). Antigen-primed CD8+ T cells can mediate resistance, preventing allogeneic marrow engraftment in the simultaneous absence of perforin-, CD95L-, TNFR1-, and TRAIL-dependent killing. Blood 101, 3991-3999.
33. Laflamme, M. A., Chen, K. Y., Naumova, A. V., Muskheli, V., Fugate, J. A., Dupras, S. K., Reinecke, H., Xu, C., Hassanipour, M., Police, S. et al. (2007). Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat. Biotechnol. 25, 1015-1024.
34. Lee, A. S., Tang, C., Cao, F., Xie, X., van der Bogt, K., Hwang, A., Connolly, A. J., Robbins, R. C. and Wu, J. C. (2009). Effects of cell number on teratoma formation by human embryonic stem cells. Cell Cycle 8, 2608-2612.
35. Leffell, M. S., Cao, K., Coppage, M., Hansen, J. A., Hart, J. M., Pereira, N., Pereira, S., Reinsmoen, N. L., Senitzer, D., Smith, A. et al. (2009). Incidence of humoral sensitization in HLA partially mismatched hematopoietic stem cell transplantation. Tissue Antigens 74, 494-498.
36. Lin, G., Xie, Y., Ouyang, Q., Qian, X., Xie, P., Zhou, X., Xiong, B., Tan, Y., Li, W., Deng, L. et al. (2009). HLA-matching potential of an established human embryonic stem cell bank in China. Cell Stem Cell 5, 461-465.
37. Lui, K., Waldmann, H. and Fairchild, P. (2009). Embryonic stem cells: overcoming the immunological barriers to cell replacement therapy. Curr. Stem Cell Res. Ther. 4, 70-80.
38. Mammolenti, M., Gajavelli, S., Tsoulfas, P. and 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.
39. Mohanakumar, T., Narayanan, K., Desai, N., Ramachandran, S., Shenoy, S., Jendrisak, M., Susskind, B. M., Olack, B., Benshoff, N., Phelan, D. L. et al. (2006). A significant role for histocompatibility in human islet transplantation. Transplantation 82, 180-187.
40. Muller, Y. D., Mai, G., Morel, P., Serre-Beinier, V., Gonelle-Gispert, C., Yung, G. P., Ehirchiou, D., Wyss, J. C., Bigenzahn, S., Irla, M. et al. (2010). Anti-CD154 mAb and rapamycin induce T regulatory cell mediated tolerance in rat-to-mouse islet transplantation. PLoS ONE 5, e10352.
41. Mummery, C. (2010). Sorting cardiomyocytes: a simple solution after all? Nat. Methods 7, 40-42.
42. Nomi, H., Tashiro-Yamaji, J., Yamamoto, Y., Miura-Takeda, S., Miyoshi-Higashino, M., Takahashi, T., Azuma, H., Ueda, H., Katsuoka, Y., Kubota, T. et al. (2007). Acute rejection of allografted CTL-susceptible leukemia cells from perforin/Fas ligand double-deficient mice. J. Immunol. 179, 2180-2186.
43. Papassavas, A. C., Barnardo, M. C., Bunce, M. and Welsh, K. I. (2002). Is there MHC Class II restriction of the response to MHC Class I in transplant patients? Transplantation 73, 642-651.
44. Passier, R., Oostwaard, D., Snapper, J., Kloots, J., Hassink, R., Kuijk, E., Roelen, B., de la Riviere, A. and Mummery, C. (2005). Increased cardiomyocyte differentiation from human embryonic stem cells in serum-free cultures. Stem Cells 23, 772-780.
45. 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.
46. Poncelet, A. J., Nizet, Y., Vercruysse, J., Hiel, A. L., Saliez, A. and Gianello, P. (2008). Inhibition of humoral response to allogeneic porcine mesenchymal stem cell with 12 days of tacrolimus. Transplantation 86, 1586-1595.
47. Preynat-Seauve, O., de Rham, C., Tirefort, D., Ferrari-Lacraz, S., Krause, K. H. and Villard, J. (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.
48. Robertson, N. J., Brook, F. A., Gardner, R. L., Cobbold, S. P., Waldmann, H. and Fairchild, P. J. (2007). Embryonic stem cell-derived tissues are immunogenic but their inherent immune privilege promotes the induction of tolerance. Proc. Natl. Acad. Sci. USA 104, 20920-20925.
49. Spellman, S., Bray, R., Rosen-Bronson, S., Haagenson, M., Klein, J., Flesch, S., Vierra-Green, C. and Anasetti, C. (2010). The detection of donor-directed, HLA-specific alloantibodies in recipients of unrelated hematopoietic cell transplantation is predictive of graft failure. Blood 115, 2704-2708.
50. Stangl, S., Gross, C., Pockley, A. G., Asea, A. A. and Multhoff, G. (2008). Influence of Hsp70 and HLA-E on the killing of leukemic blasts by cytokine/Hsp70 peptideactivated human natural killer (NK) cells. Cell Stress Chaperones 13, 221-230.
51. Sun, N., Lee, A. and Wu, J. C. (2009). Long term non-invasive imaging of embryonic stem cells using reporter genes. Nat. Protoc 4, 1192-1201.
52. Swijnenburg, R.-J., Schrepfer, S., Govaert, J., Cao, F., Ransohoff, K., Sheikh, A., Haddad, M., Connolly, A., Davis, M., Robbins, R. et al. (2008a). Immunosuppressive therapy mitigates immunological rejection of human embryonic stem cell xenografts. Proc. Natl. Acad. Sci. USA 105, 12991-12996.
53. Swijnenburg, R. J., Schrepfer, S., Cao, F., Pearl, J. I., Xie, X., Connolly, A. J., Robbins, R. C. and Wu, J. C. (2008b). In vivo imaging of embryonic stem cells reveals patterns of survival and immune rejection following transplantation. Stem Cells Dev. 17, 1023-1029.
54. Tabayoyong, W. B., Salas, J. G., Bonde, S. and Zavazava, N. (2009). HOXB4- transduced embryonic stem cell-derived Lin-c-kit+ and Lin-Sca-1+ hematopoietic progenitors express H60 and are targeted by NK cells. J. Immunol. 183, 5449-5457.
55. Tamaoki, N., Takahashi, K., Tanaka, T., Ichisaka, T., Aoki, H., Takeda-Kawaguchi, T., Iida, K., Kunisada, T., Shibata, T., Yamanaka, S. et al. (2010). Dental pulp cells for induced pluripotent stem cell banking. J. Dent. Res. 89, 773-778.
56. Tseng, H. C., Arasteh, A., Paranjpe, A., Teruel, A., Yang, W., Behel, A., Alva, J. A., Walter, G., Head, C., Ishikawa, T. O. et al. (2010). Increased lysis of stem cells but not their differentiated cells by natural killer cells; de-differentiation or reprogramming activates NK cells. PLoS ONE 5, e11590.
57. van Laake, L., Passier, R., Monshouwer-Kloots, J., Verkleij, A., Lips, D., Freund, C., den Ouden, K., Oostwaard, D., Korving, J., Tertoolen, L. et al. (2007). Human embryonic stem cell-derived cardiomyocytes survive and mature in the mouse heart and transiently improve function after myocardial infarction. Stem Cell Res. 1, 9-24.
58. Xue, T., Cho, H. C., Akar, F. G., Tsang, S. Y., Jones, S. P., Marban, E., Tomaselli, G. F. and Li, R. A. (2005). Functional integration of electrically active cardiac derivatives from genetically engineered human embryonic stem cells with quiescent recipient ventricular cardiomyocytes: insights into the development of cell-based pacemakers. Circulation 111, 11-20.
59. Yen, B. L., Chang, C. J., Liu, K. J., Chen, Y. C., Hu, H. I., Bai, C. H. and Yen, M. L. (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.
60. Yoshimura, M., Ihara, Y., Ohnishi, A., Ijuhin, N., Nishiura, T., Kanakura, Y., Matsuzawa, Y. and Taniguchi, N. (1996). Bisecting N-acetylglucosamine on K562 cells suppresses natural killer cytotoxicity and promotes spleen colonization. Cancer Res. 56, 412-418.
61. Zimmerman, Z., Shatry, A., Deyev, V., Podack, E., Mammolenti, M., Blazar, B. R., Yagita, H. and Levy, R. B. (2005). Effector cells derived from host CD8 memory T cells mediate rapid resistance against minor histocompatibility antigen-mismatched allogeneic marrow grafts without participation of perforin, Fas ligand, and the simultaneous inhibition of 3 tumor necrosis factor family effector pathways. Biol. Blood Marrow Transplant. 11, 576-586.