Immunomodulatory effects of foreskin mesenchymal stromal cells on natural killer cells

Journal of Cellular Physiology

Volumn 233, Issue 7, 2018, Pages 5243-5254

  Najar, Mehdi ^a   Fayyad Kazan, Mohammad ^b   Meuleman, Nathalie ^a   Bron, Dominique ^a   Fayyad Kazan, Hussein ^c   Lagneaux, Laurence ^a  

^a JULES BORDET INSTITUTE   (Belgium)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c LEBANESE UNIVERSITY   (Lebanon)

Author keywords

FSK MSCs; immunomodulation; NK cells

Indexed keywords

5' NUCLEOTIDASE; CD155 LIGAND; ENDOGLIN; GAMMA INTERFERON; GRANZYME; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 2; INTERLEUKIN 21; LEUKOCYTE ASSOCIATED IMMUNOGLOBULIN LIKE RECEPTOR; LIGAND; NECTIN 2; PERFORIN; REACTIVE OXYGEN METABOLITE; RECEPTOR; THY 1 MEMBRANE GLYCOPROTEIN; TUMOR NECROSIS FACTOR; ULPB 3 LIGAND; UNCLASSIFIED DRUG; SERINE PROTEINASE INHIBITOR;

ARTICLE; CELL ACTIVATION; CELL INTERACTION; CONTROLLED STUDY; CYTOTOXICITY; DEGRANULATION; HUMAN; HUMAN CELL; IMMUNOMODULATION; MESENCHYMAL STROMA CELL; NATURAL KILLER CELL; PREPUCE; PRIORITY JOURNAL; PROTEIN SECRETION; BIOLOGICAL THERAPY; CELL PROLIFERATION; COCULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; MALE; MESENCHYMAL STEM CELL; METABOLISM; PROCEDURES;

CELL PROLIFERATION; CELL- AND TISSUE-BASED THERAPY; COCULTURE TECHNIQUES; FORESKIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IMMUNOMODULATION; IMMUNOTHERAPY; INTERFERON-GAMMA; INTERLEUKIN-2; KILLER CELLS, NATURAL; LIGANDS; LYMPHOCYTE ACTIVATION; MALE; MESENCHYMAL STEM CELLS; SERPINS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85040712039     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.26305     Document Type: Article

References (58)

1. Abdelrazik, H., Spaggiari, G. M., Chiossone, L., & Moretta, L. (2011). Mesenchymal stem cells expanded in human platelet lysate display a decreased inhibitory capacity on T- and NK-cell proliferation and function. European Journal of Immunology, 41, 3281–3290. https://doi.org/10.1002/eji.201141542
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. Almeida, C. R., Vasconcelos, D. P., Gonçalves, R. M., & Barbosa, M. A. (2012). Enhanced mesenchymal stromal cell recruitment via natural killer cells by incorporation of inflammatory signals in biomaterials. Journal of the Royal Society, Interface, 9, 261–271. https://doi.org/10.1098/rsif.2011.0357
4. Alter, G., Malenfant, J. M., & Altfeld, M. (2004). CD107a as a functional marker for the identification of natural killer cell activity. Journal of Immunological Methods, 294, 15–22. https://doi.org/10.1016/j.jim.2004.08.008
5. Auletta, J. J., Eid, S. K., Wuttisarnwattana, P., Silva, I., Metheny, L., Keller, M. D., … Cooke, K. R. (2015). Human mesenchymal stromal cells attenuate graft-Versus-Host disease and maintain graft-versus-Leukemia activity following experimental allogeneic bone marrow transplantation. Stem Cells, 33, 601–614. https://doi.org/10.1002/stem.1867
6. Biron, C. A., Nguyen, K. B., Pien, G. C., Cousens, L. P., & Salazar-Mather, T. P. (1999). Natural killer cells in antiviral defense: Function and regulation by innate cytokines. Annual Review of Immunology, 17, 189–220. https://doi.org/10.1146/annurev.immunol.17.1.189
7. Blanco, B., Herrero-Sánchez, M. C., Rodríguez-Serrano, C., García-Martínez, M. L., Blanco, J. F., Muntión, S., … del Cañizo, C. (2016). Immunomodulatory effects of bone marrow versus adipose tissue derived mesenchymal stromal cells on NK cells: Implications in the transplantation setting. European Journal of Haematology, 97, 528–537. https://doi.org/10.1111/ejh.12765
8. Bottino, C., Castriconi, R., Pende, D., Rivera, P., Nanni, M., Carnemolla, B., … Moretta, A. (2003). Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. The Journal of Experimental Medicine, 198, 557–567. https://doi.org/10.1084/jem.20030788
9. Bouchlaka, M. N., Redelman, D., & Murphy, W. J. (2010). Immunotherapy following hematopoietic stem cell transplantation: Potential for synergistic effects. Immunotherapy, 2, 399–418. https://doi.org/10.2217/imt.10.20
10. Chatterjee, D., Marquardt, N., Tufa, D. M., Beauclair, G., Low, H. Z., Hatlapatka, T., … Jacobs, R. (2014a). Role of gamma-secretase in human umbilical-cord derived mesenchymal stem cell mediated suppression of NK cell cytotoxicity. Cell Communication and Signaling, 12, 63. https://doi.org/10.1186/s12964-014-0063-9
11. 3 production by natural killer cells. Frontiers in Immunology, 5, 662. https://doi.org/10.3389/fimmu.2014.00662
12. Chen, X., Song, M., Zhang, B., & Zhang, Y. (2016). Reactive oxygen species regulate t cell immune response in the tumor microenvironment. Oxidative Medicine and Cellular Longevity, 2016, 1–10. https://doi.org/10.1155/2016/1580967
13. Chieregato, K., Albiero, E., Castegnaro, S., Bernardi, M., d'Amore, E. S. G., Zanon, C., … Astori, G. (2012). A study on mutual interaction between cytokine induced killer cells and umbilical cord-derived mesenchymal cells: Implication for their in-vivo use. Blood Cells, Molecules and Diseases, 49, 159–165. https://doi.org/10.1016/j.bcmd.2012.05.009
14. Crop, M. J., Korevaar, S. S., de Kuiper, R., Ijzermans, J. N. M., van Besouw, N. M., Baan, C. C., … Hoogduijn, M. J. (2011). Human mesenchymal stem cells are susceptible to lysis by CD8(+) T cells and NK cells. Cell Transplantation, 20, 1547–1559. https://doi.org/10.3727/096368910×564076
15. Cui, R., Rekasi, H., Hepner-Schefczyk, M., Fessmann, K., Petri, R. M., Bruderek, K., … Flohé, S. B. (2016). Human mesenchymal stromal/stem cells acquire immunostimulatory capacity upon cross-talk with natural killer cells and might improve the NK cell function of immunocompromised patients. Stem Cell Research & Therapy, 7, 88. https://doi.org/10.1186/s13287-016-0353-9
16. Cullen, S. P., Brunet, M., & Martin, S. J. (2010). Granzymes in cancer and immunity. Cell Death & Differentiation, 17, 616–623. https://doi.org/10.1038/cdd.2009.206
17. DelaRosa, O., Sánchez-Correa, B., Morgado, S., Ramírez, C., del Río, B., Menta, R., … Casado, J. G. (2012). Human adipose-derived stem cells impair natural killer cell function and exhibit low susceptibility to natural killer-mediated lysis. Stem Cells and Development, 21, 1333–1343. https://doi.org/10.1089/scd.2011.0139
18. de Rham, C., Ferrari-Lacraz, S., Jendly, S., Schneiter, G., Dayer, J.-M., & Villard, J. (2007). The proinflammatory cytokines IL-2, IL-15 and IL-21 modulate the repertoire of mature human natural killer cell receptors. Arthritis Research & Therapy, 9, R125. https://doi.org/10.1186/ar2336
19. de Witte, S. F. H., Merino, A. M., Franquesa, M., Strini, T., van Zoggel, J. A. A., Korevaar, S. S., … Hoogduijn, M. J. (2017). Cytokine treatment optimises the immunotherapeutic effects of umbilical cord-derived MSC for treatment of inflammatory liver disease. Stem Cell Research & Therapy, 8, 140. https://doi.org/10.1186/s13287-017-0590-6
20. Dominici, M., Le Blanc, K., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, 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
21. El Haddad, N., Moore, R., Heathcote, D., Mounayar, M., Azzi, J., Mfarrej, B., … Abdi, R. (2011). The novel role of SERPINB9 in cytotoxic protection of human mesenchymal stem cells. The Journal of Immunology, 187, 2252–2260. https://doi.org/10.4049/jimmunol.1003981
22. Fu, Q., Man, X., Yu, M., Chu, Y., Luan, X., Piao, H., … Jin, C. (2017). Human decidua mesenchymal stem cells regulate decidual natural killer cell function via interactions between collagen and leukocyte-associated immunoglobulin-like receptor 1. Molecular Medicine Reports, 16, 2791–2798. https://doi.org/10.3892/mmr.2017.6921
23. Giuliani, M., Bennaceur-Griscelli, A., Nanbakhsh, A., Oudrhiri, N., Chouaib, S., Azzarone, B., … Lataillade, J.-J. (2014). TLR ligands stimulation protects MSC from NK killing. Stem Cells, 32, 290–300. https://doi.org/10.1002/stem.1563
24. Giuliani, M., & Oudrhiri, N. (2011). Human mesenchymal stem cells derived from induced pluripotent stem cells down-regulate NK-cell cytolytic machinery. Blood, 118, 3254–3262. https://doi.org/10.1182/blood-2010-12-325324
25. Götherström, C., Lundqvist, A., Duprez, I. R., Childs, R., Berg, L., & le Blanc, K. (2011). Fetal and adult multipotent mesenchymal stromal cells are killed by different pathways. Cytotherapy, 13, 269–278. https://doi.org/10.3109/14653249.2010.523077
26. Hoogduijn, M. J., Roemeling-van Rhijn, M., Korevaar, S. S., Engela, A. U., Weimar, W., & Baan, C. C. (2011). Immunological aspects of allogeneic and autologous mesenchymal stem cell therapies. Human Gene Therapy, 22, 1587–1591. https://doi.org/10.1089/hum.2011.039
27. Jewett, A., Arasteh, A., Tseng, H. C., Behel, A., Arasteh, H., Yang, W., … Paranjpe, A. (2010). Strategies to rescue mesenchymal stem cells (MSCs) and dental pulp stem cells (DPSCs) from NK cell mediated cytotoxicity. PLoS One, 5, 1–14. https://doi.org/10.1371/journal.pone.0009874
28. Joyce, M. G., & Sun, P. D. (2011). The structural basis of ligand recognition by natural killer cell receptors. Journal of Biomedicine and Biotechnology, 2011, 203628. https://doi.org/10.1155/2011/203628
29. Kaiserman, D., & Bird, P. I. (2010). Control of granzymes by serpins. Cell Death & Differentiation, 17, 586–595. https://doi.org/10.1038/cdd.2009.169
30. Kim, E.-J., Kim, N., & Cho, S.-G. (2013). The potential use of mesenchymal stem cells in hematopoietic stem cell transplantation. Experimental and Molecular Medicine, 45, e2. https://doi.org/10.1038/emm.2013.2
31. Krampera, M., Galipeau, J., Shi, Y., Tarte, K., & Sensebe, L. (2013). Immunological characterization of multipotent mesenchymal stromal cells-The international society for cellular therapy (ISCT) working proposal. Cytotherapy, 15, 1054–1061. https://doi.org/10.1016/j.jcyt.2013.02.010
32. Krzewski, K., & Coligan, J. E. (2012). Human NK cell lytic granules and regulation of their exocytosis. Frontiers in Immunology, 3(335). https://doi.org/10.3389/fimmu.2012.00335
33. Lebbink, R. J., Bergvan den, MCW, Ruiterde, T., Raynal, N., Roonvan, J. A. G, Lenting, P. J., … Meyaard, L. (2008). The soluble leukocyte-Associated ig-Like receptor (LAIR)-2 antagonizes the collagen/LAIR-1 inhibitory immune interaction. The Journal of Immunology, 180, 1662–1669. https://doi.org/10.4049/jimmunol.180.3.1662
34. Li, Y., Qu, Y., Wu, Y., Wang, X., Wei, J., Huang, W., … Huang, S. (2011). Bone marrow mesenchymal stem cells reduce the antitumor activity of cytokine-induced killer/natural killer cells in K562 NOD/SCID mice. Annals of Hematology, 90, 873–885. https://doi.org/10.1007/s00277-011-1156-9
35. Lupatov, A. Y., Kim, Y. S., Bystrykh, O. A., Vakhrushev, I. V., Pavlovich, S. V., Yarygin, K. N., … Sukhikh, G. T. (2017). Effect of fibroblast-Like cells of mesenchymal origin of cytotoxic activity of lymphocytes against NK-Sensitive target cells. Bulletin of Experimental Biology and Medicine, 162, 552–557. https://doi.org/10.1007/s10517-017-3658-5
36. Moretta, L., & Moretta, A. (2004). Unravelling natural killer cell function: Triggering and inhibitory human NK receptors. EMBO Journal, 23, 255–259. https://doi.org/10.1038/sj.emboj.7600019
37. Moretta, A., Bottino, C., Vitale, M., Pende, D., Cantoni, C., Mingari, M. C., … Moretta, L. (2001). Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annual Review of Immunology, 19, 197–223. https://doi.org/10.1146/annurev.immunol.19.1.197
38. Najar, M., & Lagneaux, L. (2017). Foreskin as a source of immunotherapeutic mesenchymal stromal cells. Immunotherapy, 9, 207–217. https://doi.org/10.2217/imt-2016-0093
39. Najar, M., Raicevic, G., André, T., Fayyad-Kazan, H., Pieters, K., Bron, D., … Lagneaux, L. (2016). Mesenchymal stromal cells from the foreskin: Tissue isolation, cell characterization and immunobiological properties. Cytotherapy, 18, 320–335. https://doi.org/10.1016/j.jcyt.2015.11.013
40. Noone, C., Kihm, A., English, K., O'Dea, S., & Mahon, B. P. (2013). IFN-γ stimulated human umbilical-tissue-derived cells potently suppress NK activation and resist NK-mediated cytotoxicity in vitro. Stem Cells and Development, 22, 3003–3014. https://doi.org/10.1089/scd.2013.0028
41. Padgett, L. E., Broniowska, K. A., Hansen, P. A., Corbett, J. A., & Tse, H. M. (2013). The role of reactive oxygen species and proinflammatory cytokines in type 1 diabetes pathogenesis. Annals of the New York Academy of Sciences, 1281, 16–35. https://doi.org/10.1111/j.1749-6632.2012.06826.x
42. Pazina, T., Shemesh, A., Brusilovsky, M., Porgador, A., & Campbell, K. S. (2017). Regulation of the functions of natural cytotoxicity receptors by interactions with diverse ligands and alterations in splice variant expression. Frontiers in Immunology, 8, 369. https://doi.org/10.3389/fimmu.2017.00369
43. Perussia, (1996). The cytokine profile of resting and activated NK cells. Methods, 9, 370–378.
44. Poggi, A., & Zocchi, M. R. (2014). NK cell autoreactivity and autoimmune diseases. Frontiers in Immunology, 5, 27. https://doi.org/10.3389/fimmu.2014.00027
45. Poggi, A., Prevosto, C., Massaro, A.-M., Negrini, S., Urbani, S., Pierri, I., … Zocchi, M. R. (2005). Interaction between human NK cells and bone marrow stromal cells induces NK cell triggering: Role of NKp30 and NKG2D receptors. The Journal of Immunology, 175, 6352–6360. https://doi.org/10.4049/jimmunol.175.10.6352
46. Pradier, A., Passweg, J., Villard, J., & Kindler, V. (2011). Human bone marrow stromal cells and skin fibroblasts inhibit natural killer cell proliferation and cytotoxic activity. Cell Transplantation, 20, 681–691. https://doi.org/10.3727/096368910×536545
47. Ribeiro, A., Laranjeira, P., Mendes, S., Velada, I., Leite, C., Andrade, P., … Paiva, A. (2013). Mesenchymal stem cells from umbilical cord matrix, adipose tissue and bone marrow exhibit different capability to suppress peripheral blood B, natural killer and T cells. Stem Cell Research & Therapy, 4, 125–141. https://doi.org/10.1186/scrt336
48. Solana, R., Casado, J. G., Delgado, E., DelaRosa, O., Marín, J., Durán, E., … Tarazona, R. (2007). Lymphocyte activation in response to melanoma: Interaction of NK-associated receptors and their ligands. Cancer Immunology, Immunotherapy, 56, 101–109. https://doi.org/10.1007/s00262-006-0141-y
49. Sotiropoulou, P., Perez, S., Gritzapis, A. D., Baxevanis, C. N., & Papamichail, M. (2006). Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells, 24, 74–85. https://doi.org/10.1634/stemcells.2004-0359
50. Spaggiari, G. M., Capobianco, A., Becchetti, S., Mingari, M. C., & Moretta, L. (2006). 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. https://doi.org/10.1182/blood-2005-07-2775.Supported
51. Spaggiari, G. M., Capobianco, A., Abdelrazik, H., Becchetti, F., Mingari, M. C., & Moretta, L. (2008). Mesenchymal stem cells inhibit natural killer-cell proliferation, cytotoxicity, and cytokine production: Role of indoleamine 2, 3-dioxygenase and prostaglandin E2. Blood, 111, 1327–1333. https://doi.org/10.1182/blood-2007-02-074997
52. H Thomas, M Jäger, K Mauel, S Brandau, & S Lask, Interaction with Mesenchymal Stem Cells Provokes Natural Killer Cells for Enhanced IL-12 / IL-18-Induced Interferon-Gamma Secretion 2014; 2014 https://doi.org/10.1155/2014/143463
53. Trapani, J. A., & Smyth, M. J. (2002). Functional significance of the perforin/granzyme cell death pathway. Nature Reviews Immunology, 2, 735–747. https://doi.org/10.1038/nri911
54. Verneris, M. R. (2013). Natural killer cells and regulatory T cells: How to manipulate a graft for optimal GVL. Hematology American Society of Hematology Education Program, 2013, 335–341. https://doi.org/10.1182/asheducation-2013.1.335
55. Warren, H. S. (1996). NK cell proliferation and inflammation. Immunology and Cell Biology, 74, 473–480. https://doi.org/10.1038/icb.1996.78
56. Wu, J., Song, Y., Bakker, A. B., Bauer, S., Spies, T., Lanier, L. L., & Phillips, J. H. (1999). An activating immunoreceptor complex formed by NKG2D and DAP10. Science, 285, 730–732.
57. Yoon, S. R., Kim, T.-D., & Choi, I. (2015). Understanding of molecular mechanisms in natural killer cell therapy. Experimental and Molecular Medicine, 47, e141. https://doi.org/10.1038/emm.2014.114
58. Zhao, Z.-G., Cao, Z., Xu, W., Sun, L., You, Y., Li, F., et al. (2012). Immune protection function of multipotent mesenchymal stromal cells: Role of transforming growth factor-β1. Cancer Investigation, 30, 646–656. https://doi.org/10.3109/07357907.2012.721038