Surface expression of HLA-G is involved in mediating immunomodulatory effects of placenta-derived multipotent cells (PDMCs) towards natural killer lymphocytes

Cell Transplantation

Volumn 20, Issue 11-12, 2011, Pages 1721-1730

  Liu, Ko Jiunn ^a,b,c   Wang, Chia Jen ^d   Chang, Chan Jung ^e   Hu, Hsin I ^e   Hsu, Pei Ju ^e   Wu, Yu Chen ^a   Bai, Chyi Huey ^c   Sytwu, Huey Kang ^d,f   Linju Yen, B ^e,g,h  

^a NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^e National Health Research Institutes NHRI   (Taiwan)

^f TRI SERVICE GENERAL HOSPITAL   (Taiwan)

^g CHINA MEDICAL UNIVERSITY   (Taiwan)

^h CATHAY GENERAL HOSPITAL   (Taiwan)

Author keywords

HLA G; Immunomodulation; Mesenchymal stem cells (MSCs); Natural killer lymphocytes; Placenta

Indexed keywords

CD9 ANTIGEN; GAMMA INTERFERON; HLA G ANTIGEN; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; STAGE SPECIFIC EMBRYO ANTIGEN 4;

ADIPOCYTE; ANTIGEN EXPRESSION; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CELL INTERACTION; CELL LINEAGE; CHONDROGENESIS; CONTROLLED STUDY; CYTOLYSIS; CYTOTOXICITY; DOWN REGULATION; FEMALE; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNOMODULATION; MAJOR HISTOCOMPATIBILITY COMPLEX; MULTIPOTENT STEM CELL; NATURAL KILLER T CELL; PHENOTYPE; PLACENTA; PLACENTA DERIVED MULTIPOTENT CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CELL DIFFERENTIATION; CELLS, CULTURED; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; HLA-G ANTIGENS; HUMANS; IMMUNOSUPPRESSION; INTERFERON-GAMMA; INTERLEUKIN-2; K562 CELLS; KILLER CELLS, NATURAL; MULTIPOTENT STEM CELLS; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; PLACENTA; PREGNANCY; RECEPTORS, CELL SURFACE;

EID: 84863011834     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368911X580590     Document Type: Article

References (44)

1. Aggarwal, S.; Pittenger, M. F. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105:1815-1822; 2005.
2. Apps, R.; Gardner, L.; Moffett, A. A critical look at HLA-G. Trends Immunol. 29:313-321; 2008.
3. Barker, J. N.; Wagner, J. E. Umbilical cord blood transplantation: Current practice and future innovations. Crit. Rev. Oncol. Hematol. 48:35-43; 2003.
4. Beggs, K. J.; Lyubimov, A.; Borneman, J. N.; Bartholomew, A.; Moseley, A.; Dodds, R.; Archambault, M. P.; Smith, A. K.; McIntosh, K. R. Immunologic consequences of multiple, high-dose administration of allogeneic mesen-chymal stem cells to baboons. Cell Transplant. 15:711- 721; 2006.
5. Blaschitz, A.; Juch, H.; Volz, A.; Hutter, H.; Daxboeck, C.; Desoye, G.; Dohr, G. The soluble pool of HLA-G produced by human trophoblasts does not include detectable levels of the intron 4-containing HLA-G5 and HLA-G6 isoforms. Mol. Hum. Reprod. 11:699-710; 2005.
6. Carosella, E. D.; Favier, B.; Rouas-Freiss, N.; Moreau, P.; Lemaoult, J. Beyond the increasing complexity of the immunomodulatory HLA-G molecule. Blood 111:4862- 4870; 2008.
7. Chang, C. J.; Yen, M. L.; Chen, Y. C.; Chien, C. C.; Huang, H. I.; Bai, C. H.; Yen, B. L. Placenta-derived multipotent cells exhibit immunosuppressive properties that are enhanced in the presence of interferon-gamma. Stem Cells 24:2466-2477; 2006.
8. Chen, L.; Tredget, E. E.; Liu, C.; Wu, Y. Analysis of allo-genicity of mesenchymal stem cells in engraftment and wound healing in mice. PLoS One 4:e7119; 2009.
9. Dormeyer, W.; van Hoof, D.; Braam, S. R.; Heck, A. J.; Mummery, C. L.; Krijgsveld, J. Plasma membrane proteo-mics of human embryonic stem cells and human embryonal carcinoma cells. J. Proteome Res. 7:2936-2951; 2008.
10. Drukker, M.; Katchman, H.; Katz, G.; Even-Tov Friedman, S.; Shezen, E.; Hornstein, E.; Mandelboim, O.; Reisner, Y.; Benvenisty, N. Human embryonic stem cells and their differentiated derivatives are less susceptible to immune rejection than adult cells. Stem Cells 24:221- 229; 2006.
11. Drukker, M.; Katz, G.; Urbach, A.; Schuldiner, M.; Markel, G.; Itskovitz-Eldor, J.; Reubinoff, B.; Mandel-boim, O.; Benvenisty, N. Characterization of the expres- sion of MHC proteins in human embryonic stem cells. Proc. Natl. Acad. Sci. USA 99:9864-9869; 2002.
12. Epple-Farmer, J.; Debeb, B. G.; Smithies, O.; Binas, B. Gender-dependent survival of allogeneic trophoblast stem cells in liver. Cell Transplant. 18:769-776; 2009.
13. Fukuchi, Y.; Nakajima, H.; Sugiyama, D.; Hirose, I.; Kita-mura, T.; Tsuji, K. Human placenta-derived cells have mesenchymal stem/progenitor cell potential. Stem Cells 22:649-658; 2004.
14. Gaunt, G.; Ramin, K. Immunological tolerance of the human fetus. Am. J. Perinatol. 18:299-312; 2001.
15. Gotherstrom, C.; Ringden, O.; Tammik, C.; Zetterberg, E.; Westgren, M.; Le Blanc, K. Immunologic properties of human fetal mesenchymal stem cells. Am. J. Obstet. Gyn-ecol. 190:239-245; 2004.
16. Hunt, J. S.; Geraghty, D. E. Soluble HLA-G isoforms: Technical deficiencies lead to misinterpretations. Mol. Hum. Reprod. 11:715-717; 2005.
17. In't Anker, P. S.; Scherjon, S. A.; Kleijburg-van der Keur, C.; de Groot-Swings, G. M.; Claas, F. H.; Fibbe, W. E.; Kanhai, H. H. Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells 22: 1338-1345; 2004.
18. Iyer, S. S.; Rojas, M. Anti-inflammatory effects of mesen-chymal stem cells: Novel concept for future therapies. Expert Opin. Biol. Ther. 8:569-581; 2008.
19. Karre, K.; Ljunggren, H. G.; Piontek, G.; Kiessling, R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 319: 675-678; 1986.
20. Keyser, K. A.; Beagles, K. E.; Kiem, H. P. Comparison of mesenchymal stem cells from different tissues to suppress T-cell activation. Cell Transplant. 16:555-562; 2007.
21. Kitchens, W. H.; Uehara, S.; Chase, C. M.; Colvin, R. B.; Russell, P. S.; Madsen, J. C. The changing role of natural killer cells in solid organ rejection and tolerance. Transplantation 81:811-817; 2006.
22. Krampera, M.; Cosmi, L.; Angeli, R.; Pasini, A.; Liotta, F.; Andreini, A.; Santarlasci, V.; Mazzinghi, B.; Pizzolo, G.; Vinante, F.; Romagnani, P.; Maggi, E.; Romagnani, S.; Annunziato, F. Role for interferon-gamma in the im-munomodulatory activity of human bone marrow mesen-chymal stem cells. Stem Cells 24:386-398; 2006.
23. Le Blanc, K.; Frassoni, F.; Ball, L.; Locatelli, F.; Roelofs, H.; Lewis, I.; Lanino, E.; Sundberg, B.; Bernardo, M. E.; Remberger, M.; Dini, G.; Egeler, R. M.; Bacigalupo, A.; Fibbe, W.; Ringden, O. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: A phase II study. Lancet 371:1579-1586; 2008.
24. Le Blanc, K.; Rasmusson, I.; Sundberg, B.; Gotherstrom, C.; Hassan, M.; Uzunel, M.; Ringden, O. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 363:1439- 1441; 2004.
25. Li, H.; Guo, Z. K.; Li, X. S.; Hou, C. M.; Tang, P. H.; Mao, N. Functional and phenotypic alteration of intras-plenic lymphocytes affected by mesenchymal stem cells in a murine allosplenocyte transfusion model. Cell Transplant. 16:85-95; 2007.
26. Maier, S.; Tertilt, C.; Chambron, N.; Gerauer, K.; Huser, N.; Heidecke, C. D.; Pfeffer, K. Inhibition of natural killer cells results in acceptance of cardiac allografts in CD28-/ - mice. Nat. Med. 7:557-562; 2001.
27. Moffett, A.; Loke, C. Immunology of placentation in eu-therian mammals. Nat. Rev. Immunol. 6:584-594; 2006.
28. Moffett-King, A. Natural killer cells and pregnancy. Nat. Rev. Immunol. 2:656-663; 2002.
29. Nasef, A.; Mathieu, N.; Chapel, A.; Frick, J.; Francois, S.; Mazurier, C.; Boutarfa, A.; Bouchet, S.; Gorin, N. C.; Thierry, D.; Fouillard, L. Immunosuppressive effects of mesenchymal stem cells: Involvement of HLA-G. Transplantation 84:231-237; 2007.
30. Pochampally, R. R.; Smith, J. R.; Ylostalo, J.; Prockop, D. J. Serum deprivation of human marrow stromal cells (hMSCs) selects for a subpopulation of early progenitor cells with enhanced expression of OCT-4 and other embryonic genes. Blood 103:1647-1652; 2004.
31. Rao, M. S.; Mattson, M. P. Stem cells and aging: Expanding the possibilities. Mech. Ageing Dev. 122:713-734; 2001.
32. Rasmusson, I. Immune modulation by mesenchymal stem cells. Exp. Cell. Res. 312:2169-2179; 2006.
33. Rasmusson, I.; Ringden, O.; Sundberg, B.; Le Blanc, K. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation 76:1208-1213; 2003.
34. Rouas-Freiss, N.; Goncalves, R. M.; Menier, C.; Dausset, J.; Carosella, E. D. Direct evidence to support the role of HLA-G in protecting the fetus from maternal uterine natural killer cytolysis. Proc. Natl. Acad. Sci. USA 94:11520- 11525; 1997.
35. Rouas-Freiss, N.; Marchal, R. E.; Kirszenbaum, M.; Daus-set, J.; Carosella, E. D. 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. USA 94: 5249-5254; 1997.
36. Sargent, I. L. Does 'soluble' HLA-G really exist? Another twist to the tale. Mol. Hum. Reprod. 11:695-698; 2005.
37. Sotiropoulou, P. A.; Perez, S. A.; Gritzapis, A. D.; Baxe- vanis, C. N.; Papamichail, M. Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells 24:74-85; 2006.
38. Spaggiari, G. M.; Capobianco, A.; Becchetti, S.; Mingari, M. C.; Moretta, L. Mesenchymal stem cell-natural killer cell interactions: Evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation. Blood 107:1484-1490; 2006.
39. Trinchieri, G.; Perussia, B. Human natural killer cells: Biologic and pathologic aspects. Lab. Invest. 50:489-513; 1984.
40. Wagner, J. E.; Rosenthal, J.; Sweetman, R.; Shu, X. O.; Davies, S. M.; Ramsay, N. K.; McGlave, P. B.; Sender, L.; Cairo, M. S. Successful transplantation of HLA-matched and HLA-mismatched umbilical cord blood from unrelated donors: Analysis of engraftment and acute graft-versus-host disease. Blood 88:795-802; 1996.
41. Yen, B. L.; Chang, C. J.; Liu, K. J.; Chen, Y. C.; Hu, H. I.; Bai, C. H.; Yen, M. L. Human embryonic stem cell-derived mesenchymal progenitors possess strong immuno-suppressive effects toward natural killer cells as well as T lymphocytes. Stem Cells 27:451-456; 2009.
42. Yen, B. L.; Chien, C. C.; Chen, Y. C.; Chen, J. T.; Huang, J. S.; Lee, F. K.; Huang, H. I. Placenta-derived multipo-tent cells differentiate into neuronal and glial cells in vitro. Tissue Eng. Part A 14:9-17; 2008.
43. Yen, B. L.; Huang, H. I.; Chien, C. C.; Jui, H. Y.; Ko, B. S.; Yao, M.; Shun, C. T.; Yen, M. L.; Lee, M. C.; Chen, Y. C. Isolation of multipotent cells from human term placenta. Stem Cells 23:3-9; 2005.
44. Yen, M. L.; Chien, C. C.; Chiu, I. M.; Huang, H. I.; Chen, Y. C.; Hu, H. I.; Yen, B. L. Multilineage differentiation and characterization of the human fetal osteoblastic 1.19 cell line: A possible in vitro model of human mesenchy-mal progenitors. Stem Cells 25:125-131; 2007.