Decidual stromal cells promote regulatory T cells and suppress alloreactivity in a cell contact-dependent manner

Stem Cells and Development

Volumn 22, Issue 19, 2013, Pages 2596-2605

  Erkers, Tom ^a   Nava, Silvia ^a   Yosef, Jena ^a   Ringdén, Olle ^a   Kaipe, Helen ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; GAMMA INTERFERON; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 2 RECEPTOR ALPHA; PROSTAGLANDIN E2; TRANSCRIPTION FACTOR FOXP3;

ALLOIMMUNITY; ARTICLE; CELL CONTACT; DECIDUAL STROMAL CELL; FETUS MEMBRANE; GRAFT VERSUS HOST REACTION; HUMAN; HUMAN CELL; HUMAN TISSUE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; STROMA CELL;

ADULT; ANTIGENS, CD274; CELL COMMUNICATION; CELL PROLIFERATION; CELL- AND TISSUE-BASED THERAPY; DECIDUA; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GRAFT VS HOST DISEASE; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERFERON-GAMMA; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LYMPHOCYTE CULTURE TEST, MIXED; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; PROSTAGLANDINS E; T-LYMPHOCYTES, REGULATORY;

EID: 84884551847     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2013.0079     Document Type: Article

References (62)

1. Trowsdale J and AG Betz. (2006). Mother's little helpers: Mechanisms of maternal-fetal tolerance. Nat Immunol 7:241-246.
2. Munoz-Suano A, AB Hamilton and AG Betz. (2011). Gimme shelter: The immune system during pregnancy. Immunol Rev 241:20-38.
3. Kanematsu D, T Shofuda, A Yamamoto, C Ban, T Ueda, M Yamasaki and Y Kanemura. (2011). Isolation and cellular properties of mesenchymal cells derived from the decidua of human term placenta. Differentiation 82:77-88.
4. Karlsson H, T Erkers, S Nava, S Ruhm, M Westgren and O Ringden. (2012). Stromal cells from term fetal membrane are highly suppressive in allogeneic settings in vitro. Clin Exp Immunol 167:543-555.
5. Thomas ED, CD Buckner, M Banaji, RA Clift, A Fefer, N Flournoy, BW Goodell, RO Hickman, KG Lerner, et al. (1977). One hundred patients with acute leukemia treated by chemotherapy, total body irradiation, and allogeneic marrow transplantation. Blood 49:511-533.
6. Hoogerbrugge PM, OF Brouwer, P Bordigoni, O Ringden, P Kapaun, JJ Ortega, A O'Meara, G Cornu, G Souillet, et al. (1995). Allogeneic bone marrow transplantation for lysosomal storage diseases. The European Group for Bone Marrow Transplantation. Lancet 345:1398-1402.
7. Ringden O and B Nilsson. (1985). Death by graft-versus-host disease associated with HLA mismatch, high recipient age, low marrow cell dose, and splenectomy. Transplantation 40:39-44.
8. Roelen DL, BJ van der Mast, PS ińt Anker, C Kleijburg, M Eikmans, E van Beelen, GM de Groot-Swings, WE Fibbe, HH Kanhai, SA Scherjon and FH Claas. (2009). Differential immunomodulatory effects of fetal versus maternal multipotent stromal cells. Hum Immunol 70:16-23.
9. Chang CJ, ML Yen, YC Chen, CC Chien, HI Huang, CH Bai and BL Yen. (2006). Placenta-derived multipotent cells exhibit immunosuppressive properties that are enhanced in the presence of interferon-gamma. Stem Cells 24:2466-2477.
10. Le Blanc K, F Frassoni, L Ball, F Locatelli, H Roelofs, I Lewis, E Lanino, B Sundberg, ME Bernardo, et al. (2008). Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: A phase II study. Lancet 371:1579-1586.
11. Le Blanc K, I Rasmusson, B Sundberg, C Gotherstrom, M Hassan, M Uzunel and O Ringden. (2004). Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 363:1439-1441.
12. Ringden O, M Uzunel, I Rasmusson, M Remberger, B Sundberg, H Lonnies, HU Marschall, A Dlugosz, A Szakos, et al. (2006). Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation 81:1390-1397.
13. Nagamatsu T, DJ Schust, J Sugimoto and BF Barrier. (2009). Human decidual stromal cells suppress cytokine secretion by allogenic CD4+ T cells via PD-1 ligand interactions. Hum Reprod 24:3160-3171.
14. Shiokawa S,YYoshimura, SNagamatsu,HSawa,HHanashi,T Oda, Y Katsumata, N Koyama and Y Nakamura. (1996). Expression of beta 1 integrins in human endometrial stromal and decidual cells. J Clin Endocrinol Metab 81:1533-1540.
15. Parolini O, F Alviano, GP Bagnara, G Bilic, H-J Bühring, M Evangelista, S Hennerbichler, B Liu, M Magatti, et al. (2008). Concise review: Isolation and characterization of cells from human term placenta: Outcome of the first international workshop on placenta derived stem cells. Stem Cells 26:300-311.
16. Ilancheran S, Y Moodley and U Manuelpillai. (2009). Human fetal membranes: A source of stem cells for tissue regeneration and repair?. Placenta 30:2-10.
17. Bailo M, M Soncini, E Vertua, PB Signoroni, S Sanzone, G Lombardi, D Arienti, F Calamani, D Zatti, et al. (2004). Engraftment potential of human amnion and chorion cells derived from term placenta. Transplantation 78:1439-1448.
18. Augello A, R Tasso, SM Negrini, A Amateis, F Indiveri, R Cancedda and G Pennesi. (2005). Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur J Immunol 35:1482-1490.
19. Krampera M, L Cosmi, R Angeli, A Pasini, F Liotta, A Andreini, V Santarlasci, B Mazzinghi, G Pizzolo, et al. (2006). Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 24:386-398.
20. Ryan JM, F Barry, JM Murphy and BP Mahon. (2007). Interferon-gamma does not break, but promotes the immunosuppressive capacity of adult human mesenchymal stem cells. Clin Exp Immunol 149:353-363.
21. Aggarwal S and MF Pittenger. (2005). Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105:1815-1822.
22. Selmani Z, A Naji, E Gaiffe, L Obert, P Tiberghien, N Rouas-Freiss, ED Carosella and F Deschaseaux. (2009). HLA-G is a crucial immunosuppressive molecule secreted by adult human mesenchymal stem cells. Transplantation 87:S62-S66.
23. Sioud M, A Mobergslien, A Boudabous and Y Floisand. (2010). Evidence for the involvement of galectin-3 in mesenchymal stem cell suppression of allogeneic T-cell proliferation. Scand J Immunol 71:267-274.
24. Gieseke F, J Bohringer, R Bussolari, M Dominici, R Handgretinger and I Muller. (2010). Human multipotent mesenchymal stromal cells use galectin-1 to inhibit immune effector cells. Blood 116:3770-3779.
25. Ryan JM, FP Barry, JM Murphy and BP Mahon. (2005). Mesenchymal stem cells avoid allogeneic rejection. J Inflamm 2:8.
26. Di Nicola M, C Carlo-Stella, M Magni, M Milanesi, PD Longoni, P Matteucci, S Grisanti and AM Gianni. (2002). Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99:3838-3843.
27. Meisel R, A Zibert, M Laryea, U Gobel, W Daubener and D Dilloo. (2004). Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenasemediated tryptophan degradation. Blood 103:4619-4621.
28. Kesting MR, KD Wolff, B Hohlweg-Majert and L Steinstraesser. (2008). The role of allogenic amniotic membrane in burn treatment. J Burn Care Res 29:907-916.
29. von Versen-Hoynck F, U Hesselbarth and DE Moller. (2004). Application of sterilised human amnion for reconstruction of the ocular surface. Cell Tissue Banking 5:57-65.
30. Moodley Y, S Ilancheran, C Samuel, V Vaghjiani, D Atienza, ED Williams, G Jenkin, E Wallace, A Trounson and U Manuelpillai. (2010). Human amnion epithelial cell transplantation abrogates lung fibrosis and augments repair. Am J Respir Crit Care Med 182:643-651.
31. Silini A, O Parolini, B Huppertz and I Lang. (2013). Soluble factors of amnion-derived cells in treatment of inflammatory and fibrotic pathologies. Curr Stem Cell Res Ther 8:6-14.
32. Ringdén O, T Erkers, S Nava, M Uzunel, E Iwarsson, R Conrad, M Westgren, J Mattsson and H Kaipe. (2013). Fetal membrane cells for treatment of steroid-refractory acute graft-versus-host disease. Stem Cells 31:592-601.
33. Le Blanc K, L Tammik, B Sundberg, SE Haynesworth and O Ringden. (2003). Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol 57:11-20.
34. Miki T, F Marongiu, E Ellis and C Strom S. (2007). Isolation of amniotic epithelial stem cells. Curr Protoc Stem Cell Biol Chapter 1:Unit 1E 3.
35. Reddy P, M de Lima and J Koreth. (2012). Emerging therapies in hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 18:S125-S131.
36. Harris AC, JL Ferrara, TM Braun, E Holler, T Teshima, JE Levine, SW Choi, K Landfried, K Akashi, et al. (2012). Plasma biomarkers of lower gastrointestinal and liver acute GVHD. Blood 119:2960-2963.
37. Magatti M, S De Munari, E Vertua, L Gibelli, GS Wengler and O Parolini. (2008). Human amnion mesenchyme harbors cells with allogeneic T-cell suppression and stimulation capabilities. Stem Cells 26:182-192.
38. Banas RA, C Trumpower, C Bentlejewski, V Marshall, G Sing and A Zeevi. (2008). Immunogenicity and immunomodulatory effects of amnion-derived multipotent progenitor cells. Hum Immunol 69:321-328.
39. Rasmusson I, O Ringden, B Sundberg and K Le Blanc. (2003). Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation 76:1208-1213.
40. Munn DH, M Zhou, JT Attwood, I Bondarev, SJ Conway, B Marshall, C Brown and AL Mellor. (1998). Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281:1191-1193.
41. Kamimura S, K Eguchi, M Yonezawa and K Sekiba. (1991). Localization and developmental change of indoleamine 2,3-dioxygenase activity in the human placenta. Acta Med Okayama 45:135-139.
42. Prasanna SJ, D Gopalakrishnan, SR Shankar and AB Vasandan. (2010). Pro-inflammatory cytokines, IFNgamma and TNFalpha, influence immune properties of human bone marrow and Wharton jelly mesenchymal stem cells differentially. PloS One 5:e9016.
43. Polchert D, J Sobinsky, G Douglas, M Kidd, A Moadsiri, E Reina, K Genrich, S Mehrotra, S Setty, B Smith and A Bartholomew. (2008). IFN-gamma activation of mesenchymal stem cells for treatment and prevention of graft versus host disease. Eur J Immunol 38:1745-1755.
44. Mellor J and A Morillon. (2004). ISWI complexes in Saccharomyces cerevisiae. Biochim Biophys Acta 1677:100-112.
45. Le Blanc K, C Tammik, K Rosendahl, E Zetterberg and O Ringden. (2003). HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol 31:890-896.
46. Ren G, X Zhao, L Zhang, J Zhang, A L'Huillier, W Ling, AI Roberts, AD Le, S Shi, C Shao and Y Shi. (2010). Inflammatory cytokine-induced intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in mesenchymal stem cells are critical for immunosuppression. J Immunol 184:2321-2328.
47. Freeman GJ, AJ Long, Y Iwai, K Bourque, T Chernova, H Nishimura, LJ Fitz, N Malenkovich, T Okazaki, et al. (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.
48. Nagamatsu T and DJ Schust. (2010). The immunomodulatory roles of macrophages at the maternal-fetal interface. Reprod Sci 17:209-218.
49. Kalinski P. (2012). Regulation of immune responses by prostaglandin E2. J Immunol 188:21-28.
50. von Bergwelt-Baildon MS, A Popov, T Saric, J Chemnitz, S Classen, MS Stoffel, F Fiore, U Roth, M Beyer, et al. (2006). CD25 and indoleamine 2,3-dioxygenase are up-regulated by prostaglandin E2 and expressed by tumor-associated dendritic cells in vivo: Additional mechanisms of T-cell inhibition. Blood 108:228-237.
51. Takahashi T, Y Kuniyasu, M Toda, N Sakaguchi, M Itoh, M Iwata, J Shimizu and S Sakaguchi. (1998). Immunologic selftolerance maintained by CD25 + CD4+ naturally anergic and suppressive T cells: Induction of autoimmune disease by breaking their anergic/suppressive state. Int Immunol 10:1969-1980.
52. Thornton AM and EM Shevach. (1998). CD4 + CD25 + immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med 188:287-296.
53. Asseman C, S Mauze, MW Leach, RL Coffman and F Powrie. (1999). An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J Exp Med 190:995-1004.
54. Fan J, P Nishanian, EC Breen, M McDonald and JL Fahey. (1998). Cytokine gene expression in normal human lymphocytes in response to stimulation. Clin Diagn Lab Immunol 5:335-340.
55. Tilburgs T, DL Roelen, BJ van der Mast, JJ van Schip, C Kleijburg, GM de Groot-Swings, HH Kanhai, FH Claas and SA Scherjon. (2006). Differential distribution of CD4 (+) CD25(bright) and CD8 (+) CD28(-) T-cells in decidua and maternal blood during human pregnancy. Placenta 27 Suppl A:S47-S53.
56. Sindram-Trujillo A, S Scherjon, H Kanhai, D Roelen and F Claas. (2003). Increased T-cell activation in decidua parietalis compared to decidua basalis in uncomplicated human term pregnancy. Am J Reprod Immunol 49:261-268.
57. Mjösberg J, G Berg, MC Jenmalm and J Ernerudh. (2010). FOXP3 + regulatory T cells and T helper 1, T helper 2, and T helper 17 cells in human early pregnancy decidua. Biol Reprod 82:698-705.
58. Fallarino F, U Grohmann, S You, BC McGrath, DR Cavener, C Vacca, C Orabona, R Bianchi, ML Belladonna, et al. (2006). The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor zeta-chain and induce a regulatory phenotype in naive T cells. J Immunol 176:6752-6761.
59. Baban B, PR Chandler, MD Sharma, J Pihkala, PA Koni, DH Munn and AL Mellor. (2009). IDO activates regulatory T cells and blocks their conversion into Th17-like T cells. J Immunol 183:2475-2483.
60. Oderup C, L Cederbom, A Makowska, CM Cilio and F Ivars. (2006). Cytotoxic T lymphocyte antigen-4-dependent downmodulation of costimulatory molecules on dendritic cells in CD4 + CD25 + regulatory T-cell-mediated suppression. Immunology 118:240-249.
61. Grohmann U, C Orabona, F Fallarino, C Vacca, F Calcinaro, A Falorni, P Candeloro, ML Belladonna, R Bianchi, MC Fioretti and P Puccetti. (2002). CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat Immunol 3:1097-1101.
62. Yu J, J Sun, SE Wang, H Li, S Cao, Y Cong, J Liu and X Ren. (2011). Upregulated expression of indoleamine 2, 3-dioxygenase in primary breast cancer correlates with increase of infiltrated regulatory T cells in situ and lymph node metastasis. Clin Dev Immunol 2011:469135.