Xenografted human amniotic membrane-derived mesenchymal stem cells are immunologically tolerated and transdifferentiated into cardiomyocytes

Circulation Research

Volumn 106, Issue 10, 2010, Pages 1613-1623

  Tsuji, Hiroko ^a,f   Miyoshi, Shunichiro ^b,e   Ikegami, Yukinori ^b,f   Hida, Naoko ^b,f   Asada, Hironori ^a   Togashi, Ikuko ^b   Suzuki, Junshi ^b   Satake, Masaki ^b   Nakamizo, Hikaru ^b   Tanaka, Mamoru ^a,c   Mori, Taisuke ^a   Segawa, Kaoru ^d   Nishiyama, Nobuhiro ^b,f   Inoue, Junko ^g   Makino, Hatsune ^f   Miyado, Kenji ^f   Ogawa, Satoshi ^b   Yoshimura, Yasunori ^a   Umezawa, Akihiro ^f  

^a Departments of Obstetrics   (United States)

^b Departments of Cardiology   (United States)

^c Departments of Pathology   (United States)

^d Departments of Microbiology and Immunology   (United States)

^e KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^f Department of Reproductive Biology and Pathology ^*  (United States)

^g National Research Institute for Child Health and Development   (United States)

Author keywords

Cardiomyogenesis; Cell based therapy; Human mesenchymal stem cell; Immunologic tolerance; Myocardial infarction

Indexed keywords

HLA G ANTIGEN; INTERLEUKIN 10; MAJOR HISTOCOMPATIBILITY ANTIGEN; PROGESTERONE; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CELL SURVIVAL; CELL TRANSDIFFERENTIATION; CONTROLLED STUDY; DRUG MECHANISM; FETUS; HEART CONTRACTION; HEART INFARCTION; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HUMAN; HUMAN AMNIOTIC MEMBRANE DERIVED MESENCHYMAL STEM CELL; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; MALE; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; REGENERATIVE ABILITY; REGULATORY T LYMPHOCYTE; SURVIVAL TIME; T LYMPHOCYTE ACTIVATION; TREATMENT RESPONSE; XENOGRAFT;

AMNION; ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; DELIVERY, OBSTETRIC; ECHOCARDIOGRAPHY; FEMALE; GRAFT REJECTION; HEART; HUMANS; INFANT, NEWBORN; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MICE; MYOCYTES, CARDIAC; PREGNANCY; RATS; RATS, WISTAR; TRANSPLANTATION TOLERANCE; TRANSPLANTATION, HETEROLOGOUS; VENTRICULAR FUNCTION, LEFT;

EID: 77952999205     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.109.205260     Document Type: Article

References (38)

1. Boheler KR, Czyz J, Tweedie D, Yang HT, Anisimov SV, Wobus AM. Differentiation of pluripotent embryonic stem cells into cardiomyocytes. Circ Res. 2002;91:189-201.
2. Okita K, Ichisaka T, Yamanaka S. Generation of germline-competent induced pluripotent stem cells. Nature. 2007;448:313-317.
3. Andrews PW. From teratocarcinomas to embryonic stem cells. Philos Trans R Soc Lond B Biol Sci. 2002;357:405-417.
4. Chen SL, Fang WW, Ye F, Liu YH, Qian J, Shan SJ, Zhang JJ, Chunhua RZ, Liao LM, Lin S, Sun JP. Effect on left ventricular function of intracoronary transplantation of autologous bone marrow mesenchymal stem cell in patients with acute myocardial infarction. Am J Cardiol. 2004;94:92-95. (Pubitemid 38813459)
5. Hou M, Yang KM, Zhang H, Zhu WQ, Duan FJ, Wang H, Song YH, Wei YJ, Hu SS. Transplantation of mesenchymal stem cells from human bone marrow improves damaged heart function in rats. Int J Cardiol. 2007; 115:220-228.
6. Takeda Y, Mori T, Imabayashi H, Kiyono T, Gojo S, Miyoshi S, Hida N, Ita M, Segawa K, Ogawa S, Sakamoto M, Nakamura S, Umezawa A. Can the life span of human marrow stromal cells be prolonged by bmi-1, E6, E7, and/or telomerase without affecting cardiomyogenic differentiation? J Gene Med. 2004;6:833-845.
7. Hida N, Nishiyama N, Miyoshi S, Kira S, Segawa K, Uyama T, Mori T, Miyado K, Ikegami Y, Cui C, Kiyono T, Kyo S, Shimizu T, Okano T, Sakamoto M, Ogawa S, Umezawa A. Novel cardiac precursor-like cells from human menstrual blood-derived mesenchymal cells. Stem Cells. 2008;26:1695-1704.
8. Nishiyama N, Miyoshi S, Hida N, Uyama T, Okamoto K, Ikegami Y, Miyado K, Segawa K, Terai M, Sakamoto M, Ogawa S, Umezawa A. The Significant Cardiomyogenic Potential of Human Umbilical cord blood-derived Mesen-chymal Stem Cells in Vitro. Stem Cells. 2007;25:2017-2024. (Pubitemid 47258179)
9. Okamoto K, Miyoshi S, Toyoda M, Hida N, Ikegami Y, Makino H, Nishiyama N, Tsuji H, Cui CH, Segawa K, Uyama T, Kami D, Miyado K, Asada H, Matsumoto K, Saito H, Yoshimura Y, Ogawa S, Aeba R, Yozu R, Umezawa A. 'Working' cardiomyocytes exhibiting plateau action potentials from human placenta-derived extraembryonic meso-dermal cells. Exp Cell Res. 2007;313:2550-2562.
10. Fadini GP, Miorin M, Facco M, Bonamico S, Baesso I, Grego F, Menegolo M, de Kreutzenberg SV, Tiengo A, Agostini C, Avogaro A. Circulating endothelial progenitor cells are reduced in peripheral vascular complications of type 2 diabetes mellitus. J Am Coll Cardiol. 2005;45: 1449-1457.
11. Heiss C, Keymel S, Niesler U, Ziemann J, Kelm M, Kalka C. Impaired progenitor cell activity in age-related endothelial dysfunction. J Am Coll Cardiol. 2005;45:1441-1448.
12. Terai M, Uyama T, Sugiki T, Li X, Umezawa A, Kiyono T. Immortalization of human fetal cells: the life span of umbilical cord blood-derived cells can be prolonged without manipulating p16INK4a/RB braking pathway. Mol Biol Cell. 2005;16:1491-1499.
13. Shake JG, Gruber PJ, Baumgartner WA, Senechal G, Meyers J, Redmond JM, Pittenger MF, Martin BJ. Mesenchymal stem cell implantation in a swine myocardial infarct model: engraftment and functional effects. Ann Thorac Surg. 2002;73:1919-1926.
14. Zhao P, Ise H, Hongo M, Ota M, Konishi I, Nikaido T. Human amniotic mesenchymal cells have some characteristics of cardiomyo-cytes. Transplantation. 2005;79:528-535.
15. Miki T, Lehmann T, Cai H, Stolz DB, Strom SC. Stem cell characteristics of amniotic epithelial cells. Stem Cells. 2005;23:1549-1559.
16. Fujimoto KL, Miki T, Liu LJ, Hashizume R, Strom SC, Wagner WR, Keller BB, Tobita K. Naive rat amnion-derived cell transplantation improved left ventricular function and reduced myocardial scar of postin-farcted heart. Cell Transplant. 2009;18:477-486.
17. Portmann-Lanz CB, Schoeberlein A, Huber A, Sager R, Malek A, Hol-zgreve W, Surbek DV. Placental mesenchymal stem cells as potential autologous graft for pre-and perinatal neuroregeneration. Am J Obstet Gynecol. 2006;194:664-673.
18. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y. 'Green mice' as a source of ubiquitous green cells. FEBS Lett. 1997;407: 313-319.
19. Furuta A, Miyoshi S, Itabashi Y, Shimizu T, Kira S, Hayakawa K, Nishiyama N, Tanimoto K, Hagiwara Y, Satoh T, Fukuda K, Okano T, Ogawa S. Pulsatile cardiac tissue grafts using a novel three-dimensional cell sheet manipulation technique functionally integrates with the host heart, in vivo. Circ Res. 2006;98:705-712.
20. Fukuda Y, Miyoshi S, Tanimoto K, Oota K, Fujikura K, Iwata M, Baba A, Hagiwara Y, Yoshikawa T, Mitamura H, Ogawa S. Autoimmunity against the second extracellular loop of beta(1)-adrenergic receptors induces early afterdepolarization and decreases in K-channel density in rabbits. J Am Coll Cardiol. 2004;43:1090-1100.
21. Hagiwara Y, Miyoshi S, Fukuda K, Nishiyama N, Ikegami Y, Tanimoto K, Murata M, Takahashi E, Shimoda K, Hirano T, Mitamura H, Ogawa S. SHP2-mediated signaling cascade through gp130 is essential for LIF-dependent I CaL, [Ca2 +]i transient, and APD increase in cardiomyo-cytes. JMol Cell Cardiol. 2007;43:710-716.
22. Kannagi R, Cochran NA, Ishigami F, Hakomori S, Andrews PW, Knowles BB, Solter D. Stage-specific embryonic antigens (SSEA-3 and-4) are epitopes of a unique globo-series ganglioside isolated from human teratocarcinoma cells. EMBO J. 1983;2:2355-2361.
23. Brulport M, Schormann W, Bauer A, Hermes M, Elsner C, Hammersen FJ, Beerheide W, Spitkovsky D, Hartig W, Nussler A, Horn LC, Edelmann J, Pelz-Ackermann O, Petersen J, Kamprad M, von Mach M, Lupp A, Zulewski H, Hengstler JG. Fate of extrahepatic human stem and precursor cells after transplantation into mouse livers. Hepatology. 2007; 46:861-870. (Pubitemid 47436132)
24. Gnecchi M, He H, Liang O, Melo L, Morello F, Mu H, Noiseux N, Zhang L, Pratt R, Ingwall J, Dzau V. Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells. Nat Med. 2005;11:367-368.
25. Gojo S, Gojo N, Takeda Y, Mori T, Abe H, Kyo S, Hata J, Umezawa A. In vivo cardiovasculogenesis by direct injection of isolated adult mesenchymal stem cells. Exp Cell Res. 2003;288:51-59.
26. Kocher AA, Schuster MD, Szabolcs MJ, Takuma S, Burkhoff D, Wang J, Homma S, Edwards NM, Itescu S. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents car-diomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med. 2001;7:430-436.
27. Ljunggren HG, Karre K. In search of the 'missing self: MHC molecules and NK cell recognition. Immunol Today. 1990;11:237-244
28. 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 USA. 1997;94:11520-11525.
29. Pazmany L, Mandelboim O, Vales-Gomez M, Davis DM, Reyburn HT, Strominger JL. Protection from natural killer cell-mediated lysis by HLA-G expression on target cells. Science. 1996;274:792-795.
30. Selmani Z, Naji A, Zidi I, Favier B, Gaiffe E, Obert L, Borg C, Saas P, Tiberghien P, Rouas-Freiss N, Carosella ED, Deschaseaux F. Human leukocyte antigen-G5 secretion by human mesenchymal stem cells is required to suppress T lymphocyte and natural killer function and to induce CD4 + CD25highFOXP3+ regulatory T cells. Stem Cells. 2008; 26:212-222.
31. Yoshizawa A, Ito A, Li Y, Koshiba T, Sakaguchi S, Wood KJ, Tanaka K. The roles of CD25 + CD4+ regulatory T cells in operational tolerance after living donor liver transplantation. Transplant Proc. 2005;37:37-39.
32. Fernandez N, Cooper J, Sprinks M, AbdElrahman M, Fiszer D, Kurpisz M, Dealtry G. A critical review of the role of the major histocompatibility complex in fertilization, preimplantation development and feto-maternal interactions. Hum Reprod Update. 1999;5:234-248.
33. Hutter H, Hammer A, Blaschitz A, Hartmann M, Ebbesen P, Dohr G, Ziegler A, Uchanska-Ziegler B. Expression of HLA class I molecules in human first trimester and term placenta trophoblast Cell Tissue Res. 1996;286:439-447.
34. Fiorentino DF, Bond MW, Mosmann TR. Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med. 1989;170:2081-2095.
35. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol. 2001;19:683-765.
36. Chaouat G, Assal Meliani A, Martal J, Raghupathy R, Elliott JF, Mosmann T, Wegmann TG. IL-10 prevents naturally occurring fetal loss in the CBA x DBA/2 mating combination, and local defect in IL-10 production in this abortion-prone combination is corrected by in vivo injection of IFN-tau. J Immunol. 1995;154:4261-4268.
37. Piccinni MP, Giudizi MG, Biagiotti R, Beloni L, Giannarini L, Sam-pognaro S, Parronchi P, Manetti R, Annunziato F, Livi C, et al. Progesterone favors the development of human T helper cells producing Th2-type cytokines and promotes both IL-4 production and membrane CD30 expression in established Th1 cell clones. J Immunol. 1995;155: 128-133.
38. Falk CS, Steinle A, Schendel DJ. Expression of HLA-C molecules confers target cell resistance to some non-major histocompatibility complex-restricted T cells in a manner analogous to allospecific natural killer cells. J Exp Med. 1995;182:1005-1018.