Fol. Biol. 2016, 62, 120-130

https://doi.org/10.14712/fb2016062030120

The Quality Control of Mesenchymal Stromal Cells by in Vitro Testing of Their Immunomodulatory Effect on Allogeneic Lymphocytes

Daniel Lysák1, L. Koutová1, M. Holubová1, T. Vlas2, M. Miklíková3, P. Jindra4

1Department of Haematology and Oncology, and University Hospital in Pilsen, Pilsen, Czech Republic
2Institute of Immunology and Allergology, Charles University in Prague, Faculty of Medicine in Pilsen and University Hospital in Pilsen, Pilsen, Czech Republic
3Biomedical Centre, Charles University in Prague, Faculty of Medicine in Pilsen, Pilsen, Czech Republic
4Czech National Marrow Donor Registry (CS-2), Pilsen, Czech Republic

Received August 2014
Accepted April 2016

References

1. Abdallah, B. M., Kassem, M. (2008) Human mesenchymal stem cells: from basic biology to clinical applications. Gene Ther. 15, 109-116. <https://doi.org/10.1038/sj.gt.3303067>
2. Aggarwal, S., Pittenger, M. F. (2005) Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105, 1815-1822. <https://doi.org/10.1182/blood-2004-04-1559>
3. Arvå, E., Andersson, B. (1999) Kinetics of cytokine release and expression of lymphocyte cell-surface activation markers after in vitro stimulation of human peripheral blood mononuclear cells with Streptococcus pneumoniae. Scand. J. Immunol. 49, 237-243. <https://doi.org/10.1046/j.1365-3083.1999.00470.x>
4. Caruso, A., Licenziati, S., Corulli, M., Canaris, A. D., De Francesco, M. A., Fiorentini, S., Peroni, L., Fallacara, F., Dima, F., Balsari, A., Turano, A. (1997) Flow cytometric analysis of activation markers on stimulated T cells and their correlation with cell proliferation. Cytometry 27, 71-76. <https://doi.org/10.1002/(SICI)1097-0320(19970101)27:1<71::AID-CYTO9>3.0.CO;2-O>
5. Cavet, J., Dickinson, A. M., Norden, J., Taylor, P. R., Jackson, G. H., Middleton, P. G. (2001) Interferon-γ and interleukin- 6 gene polymorphisms associate with graft-versus-host disease in HLA-matched sibling bone marrow transplantation. Blood 98, 1594-1600. <https://doi.org/10.1182/blood.V98.5.1594>
6. Di Nicola, M., Carlo-Stella, C., Magni, M., Milanesi, M., Longoni, P. D., Matteucci, P., Grisanti, S., Gianni, A. M. (2002) Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99, 3838-3843. <https://doi.org/10.1182/blood.V99.10.3838>
7. Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D., Horwitz, E. (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8, 315-317. <https://doi.org/10.1080/14653240600855905>
8. Durant, L., Watford, W. T., Ramos, H. L., Laurence, A., Vahedi, G., Wei, L., Takahashi, H., Sun, H. W., Kanno, Y., Powrie, F., O’Shea, J. J. (2010) Diverse targets of the transcription factor STAT3 contribute to T cell pathogenicity and homeostasis. Immunity 32, 605-615. <https://doi.org/10.1016/j.immuni.2010.05.003>
9. Gibbons, D. C., Evans, T. G. (1996) CD69 expression after antigenic stimulation. Cytometry 23, 260-261.
10. Glennie, S., Soeiro, I., Dyson, P. J., Lam, E. W., Dazzi, F. (2005) Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 105, 2821-2827. <https://doi.org/10.1182/blood-2004-09-3696>
11. Groh, M. E., Maitra, B., Szekely, E., Koc, O. N. (2005) Human mesenchymal stem cells require monocyte-mediated activation to suppress alloreactive T cells. Exp. Hematol. 33, 928-934. <https://doi.org/10.1016/j.exphem.2005.05.002>
12. Jui, H. S., Lin, C. H., Hsu, W. T., Liu, Y. R., Hsu, R. B., Chiang, B. L., Tseng, W. Y., Chen, M. F., Wu, K. K., Lee, C. M. (2012) Autologous mesenchymal stem cells prevent transplant arteriosclerosis by enhancing local expression of interleukin- 10, interferon-γ, and indoleamine 2,3-dioxygenase. Cell Transplant. 21, 971-984. <https://doi.org/10.3727/096368911X627525>
13. Le Blanc, K., Tammik, L., Sundberg, B., Haynesworth, S. E., Ringdén, O. (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. <https://doi.org/10.1046/j.1365-3083.2003.01176.x>
14. Le Blanc, K., Gotherstrom, C., Rasmusson, I., Seidel, C., Sundberg, B., Sundin, M., Rosendahl, K., Tammik, C., Ringdén, O. (2004) Mesenchymal stem cell inhibit the expression of CD25 (IL-2 receptor) and CD38 on phytohaemagglutinin activated lymphocytes. Scand. J. Immunol. 60, 307-315. <https://doi.org/10.1111/j.0300-9475.2004.01483.x>
15. Le Blanc, K., Pittenger, M. F. (2005) Mesenchymal stem cells: progress toward promise. Cytotherapy 7, 36-45. <https://doi.org/10.1016/S1465-3249(05)70787-8>
16. Le Blanc, K., Ringdén, O. (2007) Immunomodulation by mesenchymal stem cells and clinical experience. J. Intern. Med. 262, 509-525. <https://doi.org/10.1111/j.1365-2796.2007.01844.x>
17. 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., Ringdén, O. (2008) Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 371, 1579-1586. <https://doi.org/10.1016/S0140-6736(08)60690-X>
18. Maccario, R., Podestà, M., Moretta, A., Cometa, A., Comoli, P., Montagna, D., Daudt, L., Ibatici, A., Piaggio, G., Pozz, S., Frassoni, F., Locatelli, F. (2005) Interaction of human mesenchymal stem cells with cells involved in alloantigen- specific immune response favors the differentiation of CD4+ T-cell subsets expressing a regulatory/suppressive phenotype. Haematologica 90, 516-525.
19. Melief, S. M., Geutskens, S. B., Fibbe, W., Roelofs, H. (2013) Multipotent stromal cells skew monocytes towards an antiinflammatory interleukin-10-producing phenotype by induction of interleukin-6. Haematologica 98, 888-895. <https://doi.org/10.3324/haematol.2012.078055>
20. Morris, E. S., Hill, G. R. (2007) Advances in the understanding of acute graft-versus-host disease. Br. J. Haematol. 137, 3-19. <https://doi.org/10.1111/j.1365-2141.2007.06510.x>
21. Najar, M., Rouas, R., Raicevic, G., Boufker, H. I., Lewalle, P., Meuleman, N., Bron, D., Toungouz, M., Martiat, P., Lagneaux, L. (2009) Mesenchymal stromal cells promote or suppress the proliferation of T lymphocytes from cord blood and peripheral blood: the importance of low cell ratio and role of interleukin-6. Cytotherapy 11, 570-583. <https://doi.org/10.1080/14653240903079377>
22. O’Shea, J. J., Plenge, R. (2012) JAKs and STATs in immunoregulation and immune-mediated disease. Immunity 36, 542-550. <https://doi.org/10.1016/j.immuni.2012.03.014>
23. Ramasamy, R., Tong, C. K., Seow, H. F., Vidyadaran, S., Dazz, F. (2008) The immunosuppressive effects of human bone marrow-derived mesenchymal stem cells target T cell proliferation but not its effector function. Cell. Immunol. 251, 131-136. <https://doi.org/10.1016/j.cellimm.2008.04.009>
24. Rasmusson, I. Ringdén, O., Sundberg, B., Le Blanc, K. (2005) Mesenchymal stem cells inhibit lymphocyte proliferation by mitogens and alloantigens by different mechanisms. Exp. Cell Res. 305, 33-41. <https://doi.org/10.1016/j.yexcr.2004.12.013>
25. Reddy, M., Eirikis, E., Davis, C., Davis, H. M., Prabhakar, U. (2004) Comparative analysis of lymphocyte activation markers expression and cytokine secretion profile in stimulated human peripheral blood mononuclear cell cultures: an in vitro model to monitor cellular immune functions. J. Immunol. Methods 293, 127-142. <https://doi.org/10.1016/j.jim.2004.07.006>
26. Ringdén, O., Keating, A. (2011) Mesenchymal stromal cells as treatment for chronic GVHD. Bone Marrow Transplant. 46, 163-164. <https://doi.org/10.1038/bmt.2010.275>
27. Ross, J. A., Nagy, Z. S., Cheng, H., Stepkowski, S. M., Kirken, R. (2007) Regulation of T cell homeostasis by JAK and STATs. Arch. Immunol. Ther. Exp. 55, 231-245. <https://doi.org/10.1007/s00005-007-0030-x>
28. Saldanha-Araujo, F. S., Haddad, R., de Farias, K. C. R. M., Souza, A. P. A., Palma, P. V., Araujo, A. G., Orellana, M. D., Voltarelli, J. C., Covas, D. T., Zago, M. A., Panepucci, R. A. (2012) Mesenchymal stem cells promote the sustained expression of CD69 on activated T lymphocytes: roles of canonical and non-canonical NF-κB signaling. J. Cell. Mol. Med. 16, 1232-1244. <https://doi.org/10.1111/j.1582-4934.2011.01391.x>
29. Schindler, C., Levy, D. E., Decker, T. (2007) JAK-STAT signaling: from interferons to cytokines. J. Biol. Chem. 282, 20059-20063. <https://doi.org/10.1074/jbc.R700016200>
30. Sundin, M., Barrett, A. J., Ringden, O., Uzunel, M., Lonnies, H., Dackland, A. L., Christensson, B., Le Blanc, K. (2009) HSCT recipients have specific tolerance to MSC but not to the MSC donor. J. Immunother. 32, 755-764. <https://doi.org/10.1097/CJI.0b013e3181ab1807>
31. Tawara, I., Koyama, M., Liu, C., Toubai, T., Thomas, D., Evers, R., Chockley, P., Nieves, E., Sun, Y., Lowler, K. P., Malter, C., Nishimoto, N., Hill, G. R., Reddy, P. (2011) Interleukin- 6 modulates graft-versus-host responses after experimental allogeneic bone marrow transplantation. Clin. Cancer Res. 17, 77-88. <https://doi.org/10.1158/1078-0432.CCR-10-1198>
32. Tse, W. T., Pendleton, J. D., Beyer, W. M., Egalka, M. C., Guinan, E. C. (2003) Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 75, 389-397. <https://doi.org/10.1097/01.TP.0000045055.63901.A9>
33. Werfel, T., Boeker, M., Kapp, A. (1997) Rapid expression of the CD69 antigen on T cells and natural killer cells upon antigenic stimulation of peripheral blood mononuclear cells suspensions. Allergy 52, 465-469. <https://doi.org/10.1111/j.1398-9995.1997.tb01031.x>
34. Zheng, Z. H., Li, X. Y., Ding, J., Jia, J. F., Zhu, P. (2008) Allogeneic mesenchymal stem cells and mesenchymal stem cell-differentiated chondrocyte suppress the responses of type II collagen-reactive T cells in rheumatoid arthritis. Rheumatology 47, 22-30. <https://doi.org/10.1093/rheumatology/kem284>
front cover

ISSN 0015-5500 (Print) ISSN 2533-7602 (Online)

Open access journal

Archive