Proinflammatory stimuli induce galectin-9 in human mesenchymal stromal cells to suppress T-cell proliferation

European Journal of Immunology

Volumn 43, Issue 10, 2013, Pages 2741-2749

  Gieseke, Friederike ^a   Kruchen, Anne ^a   Tzaribachev, Nikolay ^b   Bentzien, Frank ^c   Dominici, Massimo ^d   Müller, Ingo ^c  

^a Research Institute Children's Cancer Center   (Germany)

^b Center for Rheumatic Diseases   (Germany)

^c UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^d UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

Galectin 9; Immunosuppressive effects; Mesenchymal stromal cells; Proinflammatory stimuli; T cell proliferation

Indexed keywords

ECALECTIN; GAMMA INTERFERON; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOMODULATION; INFLAMMATION; LYMPHOCYTE PROLIFERATION; MESENCHYMAL STROMA CELL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN SECRETION; SUPERNATANT; T LYMPHOCYTE; UPREGULATION;

GALECTIN-9; IMMUNOSUPPRESSIVE EFFECTS; MESENCHYMAL STROMAL CELLS; PROINFLAMMATORY STIMULI; T-CELL PROLIFERATION;

AUTOIMMUNE DISEASES; CELL PROLIFERATION; CELLS, CULTURED; GALECTINS; HUMANS; IMMUNOSUPPRESSION; INFLAMMATION; INTERFERON-GAMMA; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STROMAL CELLS; RNA, SMALL INTERFERING; T-LYMPHOCYTES; TOLL-LIKE RECEPTORS; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84885748555     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343335     Document Type: Article

References (40)

1. Shi, Y., Su, J., Roberts, A. I., Shou, P., Rabson, A. B. and Ren, G., How mesenchymal stem cells interact with tissue immune responses. Trends Immunol. 2012. 33: 136-143.
2. English, K., French, A. and Wood, K. J., Mesenchymal stromal cells: facilitators of successful transplantation? Cell Stem Cell 2010. 7: 431-442.
3. Bartholomew, A., Sturgeon, C., Siatskas, M., Ferrer, K., McIntosh, K., Patil, S. and Hardy, W., Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp. Hematol. 2002. 30: 42-48.
4. Di Nicola, M., Carlo-Stella, C., Magni, M., Milanesi, M., Longoni, P. D., Matteucci, P. and Grisanti, S., Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 2002. 99: 3838-3843.
5. Le Blanc, K., Rasmusson, I., Sundberg, B., Gotherstrom, C., Hassan, M., Uzunel, M. and Ringden, O., Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004. 363: 1439-1441.
6. Kebriaei, P., Isola, L., Bahceci, E., Holland, K., Rowley, S., McGuirk, J. and Devetten, M., Adult human mesenchymal stem cells added to corticosteroid therapy for the treatment of acute graft-versus-host disease. Biol. Blood Marrow Transplant. 2009. 15: 804-811.
7. Prasad, V. K., Lucas, K. G., Kleiner, G. I., Talano, J. A., Jacobsohn, D., Broadwater, G. and Monroy, R., Efficacy and safety of ex vivo cultured adult human mesenchymal stem cells (Prochymal) in pediatric patients with severe refractory acute graft-versus-host disease in a compassionate use study. Biol. Blood Marrow Transplant. 2011. 17: 534-541.
8. Aggarwal, S. and Pittenger, M. F., Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005. 105: 1815-1822.
9. Meisel, R., Zibert, A., Laryea, M., Gobel, U., Daubener, W. and Dilloo, D., Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2, 3-dioxygenase-mediated tryptophan degradation. Blood 2004. 103: 4619-4621.
10. Chabannes, D., Hill, M., Merieau, E., Rossignol, J., Brion, R., Soulillou, J. P. and Anegon, I., A role for heme oxygenase-1 in the immunosuppressive effect of adult rat and human mesenchymal stem cells. Blood 2007. 110: 3691-3694.
11. Selmani, Z., Naji, A., Zidi, I., Favier, B., Gaiffe, E., Obert, L. and Borg, C., 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.
12. Gieseke, F., Bohringer, J., Bussolari, R., Dominici, M., Handgretinger, R. and Müller, I., Human multipotent mesenchymal stromal cells use galectin-1 to inhibit immune effector cells. Blood 2010. 116: 3770-3779.
13. Krampera, M., Cosmi, L., Angeli, R., Pasini, A., Liotta, F., Andreini, A. and Santarlasci, V., Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 2006. 24: 386-398.
14. Ren, G., Zhang, L., Zhao, X., Xu, G., Zhang, Y., Roberts, A. I. and Zhao, R. C., Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2008. 2: 141-150.
15. Thijssen, V. L., Poirier, F., Baum, L. G. and Griffioen, A. W., Galectins in the tumor endothelium: opportunities for combined cancer therapy. Blood 2007. 110: 2819-2827.
16. Yang, R. Y., Rabinovich, G. A. and Liu, F. T., Galectins: structure, function and therapeutic potential. Expert Rev. Mol. Med. 2008. 10: e17.
17. Chabot, S., Kashio, Y., Seki, M., Shirato, Y., Nakamura, K., Nishi, N. and Nakamura, T., Regulation of galectin-9 expression and release in Jurkat T cell line cells. Glycobiology 2002. 12: 111-118.
18. Tureci, O., Schmitt, H., Fadle, N., Pfreundschuh, M. and Sahin, U., Molecular definition of a novel human galectin which is immunogenic in patients with Hodgkin's disease. J. Biol. Chem. 1997. 272: 6416-6422.
19. Hirashima, M., Kashio, Y., Nishi, N., Yamauchi, A., Imaizumi, T. A., Kageshita, T. and Saita, N., Galectin-9 in physiological and pathological conditions. Glycoconj. J. 2004. 19: 593-600.
20. Zhu, C., Anderson, A. C., Schubart, A., Xiong, H., Imitola, J., Khoury, S. J. and Zheng, X. X., The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat. Immunol. 2005. 6: 1245-1252.
21. Cedeno-Laurent, F. and Dimitroff, C. J., Evidence of a novel galectin-9-binding membrane glycoprotein ligand on T helper cells. Clin. Immunol. 2012. 143: 6-7.
22. Rodriguez-Manzanet, R., DeKruyff, R., Kuchroo, V. K. and Umetsu, D. T., The costimulatory role of TIM molecules. Immunol. Rev. 2009. 229: 259-270.
23. Gupta, S., Thornley, T. B., Gao, W., Larocca, R., Turka, L. A., Kuchroo, V. K. and Strom, T. B., Allograft rejection is restrained by short-lived TIM-3+PD-1+Foxp3+ Tregs. J. Clin. Invest. 2012. 122: 2395-2404.
24. Seki, M., Oomizu, S., Sakata, K. M., Sakata, A., Arikawa, T., Watanabe, K. and Ito, K., Galectin-9 suppresses the generation of Th17, promotes the induction of regulatory T cells, and regulates experimental autoimmune arthritis. Clin. Immunol. 2008. 127: 78-88.
25. Oomizu, S., Arikawa, T., Niki, T., Kadowaki, T., Ueno, M., Nishi, N. and Yamauchi, A., Galectin-9 suppresses Th17 cell development in an IL-2-dependent but Tim-3-independent manner. Clin. Immunol. 2012. 143: 51-58.
26. Bi, S., Earl, L. A., Jacobs, L. and Baum, L. G., Structural features of galectin-9 and galectin-1 that determine distinct T cell death pathways. J. Biol. Chem. 2008. 283: 12248-12258.
27. Oomizu, S., Arikawa, T., Niki, T., Kadowaki, T., Ueno, M., Nishi, N. and Yamauchi, A., Cell surface galectin-9 expressing Th cells regulate Th17 and Foxp3+ Treg development by galectin-9 secretion. PLoS ONE 2012. 7: e48574.
28. Wiersma, V. R., de Bruyn, M., Helfrich, W. and Bremer, E., Therapeutic potential of galectin-9 in human disease. Med. Res. Rev. 2013. 33(Suppl 1): E102-E126.
29. Sakai, K., Kawata, E., Ashihara, E., Nakagawa, Y., Yamauchi, A., Yao, H. and Nagao, R., Galectin-9 ameliorates acute GVH disease through the induction of T-cell apoptosis. Eur. J. Immunol. 2011. 41: 67-75.
30. Krampera, M., Mesenchymal stromal cell 'licensing': a multistep process. Leukemia 2011. 25: 1408-1414.
31. Sato, M., Nishi, N., Shoji, H., Seki, M., Hashidate, T., Hirabayashi, J. and Kasai Ki, K., Functional analysis of the carbohydrate recognition domains and a linker peptide of galectin-9 as to eosinophil chemoattractant activity. Glycobiology 2002. 12: 191-197.
32. Imaizumi, T., Kumagai, M., Sasaki, N., Kurotaki, H., Mori, F., Seki, M. and Nishi, N., Interferon-gamma stimulates the expression of galectin-9 in cultured human endothelial cells. J. Leukoc. Biol. 2002. 72: 486-491.
33. Asakura, H., Kashio, Y., Nakamura, K., Seki, M., Dai, S., Shirato, Y. and Abedin, M. J., Selective eosinophil adhesion to fibroblast via IFN-gamma-induced galectin-9. J. Immunol. 2002. 169: 5912-5918.
34. Kasamatsu, A., Uzawa, K., Shimada, K., Shiiba, M., Otsuka, Y., Seki, N. and Abiko, Y., Elevation of galectin-9 as an inflammatory response in the periodontal ligament cells exposed to Porphylomonas gingivalis lipopolysaccharide in vitro and in vivo. Int. J. Biochem. Cell Biol. 2005. 37: 397-408.
35. Anderson, A. C., Anderson, D. E., Bregoli, L., Hastings, W. D., Kassam, N., Lei, C. and Chandwaskar, R., Promotion of tissue inflammation by the immune receptor Tim-3 expressed on innate immune cells. Science 2007. 318: 1141-1143.
36. Imaizumi, T., Yoshida, H., Nishi, N., Sashinami, H., Nakamura, T., Hirashima, M. and Ohyama, C., Double-stranded RNA induces galectin-9 in vascular endothelial cells: involvement of TLR3, PI3K, and IRF3 pathway. Glycobiology 2007. 17: 12C-15C.
37. DelaRosa, O. and Lombardo, E., Modulation of adult mesenchymal stem cells activity by toll-like receptors: implications on therapeutic potential. Mediators Inflamm. 2010. 2010: 865601.
38. Rabinovich, G. A. and Toscano, M. A., Turning 'sweet' on immunity: galectin-glycan interactions in immune tolerance and inflammation. Nat. Rev. Immunol. 2009. 9: 338-352.
39. Sabatos, C. A., Chakravarti, S., Cha, E., Schubart, A., Sanchez-Fueyo, A., Zheng, X. X. and Coyle, A. J., Interaction of Tim-3 and Tim-3 ligand regulates T helper type 1 responses and induction of peripheral tolerance. Nat. Immunol. 2003. 4: 1102-1110.
40. Brummelkamp, T. R., Bernards, R. and Agami, R., A system for stable expression of short interfering RNAs in mammalian cells. Science 2002. 296: 550-553.