Human bone marrow stromal cells and skin fibroblasts inhibit natural killer cell proliferation and cytotoxic activity

Cell Transplantation

Volumn 20, Issue 5, 2011, Pages 681-691

  Pradier, Amandine ^a   Passweg, Jakob ^a   Villard, Jean ^a   Kindler, Vincent ^a  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

Graft versus host disease (GVHD); Graft versus leukemia (GVL); Immunoregulation; Mesenchymal stromal cells (MSCs); Skin fibroblast; Soluble inhibitor

Indexed keywords

INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 15; INTERLEUKIN 2; KYNURENINE; PERFORIN;

ARTICLE; CELL ACTIVATION; CELL CULTURE; CELL FUNCTION; CELL PROLIFERATION; CYTOTOXICITY; ENDOTHELIUM CELL; EXOCYTOSIS; HUMAN; HUMAN CELL; IMMUNOREGULATION; MESENCHYME CELL; NATURAL KILLER CELL; PRIORITY JOURNAL; SKIN FIBROBLAST; STROMA CELL;

BONE MARROW CELLS; CELL LINEAGE; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELIAL CELLS; EXOCYTOSIS; FIBROBLASTS; HUMANS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INTERLEUKIN-15; INTERLEUKIN-2; KILLER CELLS, NATURAL; KYNURENINE; MESENCHYMAL STROMAL CELLS; PERFORIN;

EID: 79960004933     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368910X536545     Document Type: Article

References (45)

1. Alter, G.; Malenfant, J. M.; Altfeld, M. CD107a as a functional marker for the identification of natural killer cell activity. J. Immunol. Methods 294:15-22; 2004.
2. Bartholomew, A.; Sturgeon, C.; Siatskas, M.; Ferrer, K.; McIntosh, K.; Patil, S.; Hardy, W.; Devine, S.; Ucker, D.; Deans, R.; Moseley, A.; Hoffman, R. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp. Hematol. 30:42-48; 2002.
3. Benvenuto, F.; Ferrari, S.; Gerdoni, E.; Gualandi, F.; Frassoni, F.; Pistoia, V.; Mancardi, G.; Uccelli, A. Human mesenchymal stem cells promote survival of T cells in a quiescent state. Stem Cells 25:1753-1760; 2007.
4. Blankenstein, T. The role of tumor stroma in the interaction between tumor and immune system. Curr. Opin. Immunol. 17:180-186; 2005.
5. Bryceson, Y. T.; March, M. E.; Ljunggren, H. G.; Long, E. O. Activation, coactivation, and costimulation of resting human natural killer cells. Immunol. Rev. 214:73-91; 2006.
6. Bryceson, Y. T.; Rudd, E.; Zheng, C.; Edner, J.; Ma, D.; Wood, S. M.; Bechensteen, A. G.; Boelens, J. J.; Celkan, T.; Farah, R. A.; Hultenby, K.; Winiarski, J.; Roche, P. A.; Nordenskjold, M.; Henter, J. I.; Long, E. O.; Ljung-gren, H. G. Defective cytotoxic lymphocyte degranulation in syntaxin-11 deficient familial hemophagocytic lymphohistiocytosis 4 (FHL4) patients. Blood 110:1906-1915; 2007.
7. Centeno, C. J.; Schultz, J. R.; Cheever, M.; Robinson, B.; Freeman, M.; Marasco, W. Safety and complications reporting on the re-implantation of culture-expanded mesenchymal stem cells using autologous platelet lysate tech-nique. Curr. Stem Cell Res. Ther. 5:81-93; 2010.
8. da Silva Meirelles, L.; Chagastelles, P. C.; Nardi, N. B. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J. Cell Sci. 119:2204-2213; 2006.
9. Della Chiesa, M.; Carlomagno, S.; Frumento, G.; Balsamo, M.; Cantoni, C.; Conte, R.; Moretta, L.; Moretta, A.; Vitale, M. The tryptophan catabolite L-kynurenine inhibits the surface expression of NKp46- and NKG2D-activating receptors and regulates NK-cell function. Blood 108:4118-4125; 2006.
10. Doucet, C.; Ernou, I.; Zhang, Y.; Llense, J. R.; Begot, L.; Holy, X.; Lataillade, J. J. Platelet lysates promote mesenchymal stem cell expansion: A safety substitute for animal serum in cell-based therapy applications. J. Cell. Physiol. 205:228-236; 2005.
11. Garvy, B. A.; Telford, W. G.; King, L. E.; Fraker, P. J. Glucocorticoids and irradiation-induced apoptosis in normal murine bone marrow B-lineage lymphocytes as determined by flow cytometry. Immunology 79:270-277; 1993.
12. Haniffa, M. A.; Collin, M. P.; Buckley, C. D.; Dazzi, F. Mesenchymal stem cells: The fibroblasts' new clothes? Haematologica 94:258-263; 2009.
13. Johann, S.; Blumel, G.; Lipp, M.; Forster, R. A versatile flow cytometry-based assay for the determination of shortand long-term natural killer cell activity. J. Immunol. Methods 185:209-216; 1995.
14. Jones, S.; Horwood, N.; Cope, A.; Dazzi, F. The antipro-liferative effect of mesenchymal stem cells is a fundamental property shared by all stromal cells. J. Immunol. 179: 2824-2831; 2007.
15. Karnoub, A. E.; Dash, A. B.; Vo, A. P.; Sullivan, A.; Brooks, M. W.; Bell, G. W.; Richardson, A. L.; Polyak, K.; Tubo, R.; Weinberg, R. A. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449:557-563; 2007.
16. Krampera, M.; Cosmi, L.; Angeli, R.; Pasini, A.; Liotta, F.; Andreini, A.; Santarlasci, V.; Mazzinghi, B.; Pizzolo, G.; Vinante, F.; Romagnani, P.; Maggi, E.; Romagnani, S.; Annunziato, F. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 24:386-398; 2006.
17. Kudo, Y.; Boyd, C. A. Human placental indoleamine 2,3-dioxygenase: Cellular localization and characterization of an enzyme preventing fetal rejection. Biochim. Biophys. Acta 1500:119-124; 2000.
18. Kuo, T. K.; Ho, J. H.; Lee, O. K. Mesenchymal stem cell therapy for nonmusculoskeletal diseases: Emerging applications. Cell Transplant. 18:1013-1028; 2009.
19. Laconi, E. The evolving concept of tumor microenvironments. Bioessays 29:738-744; 2007.
20. 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.; Ringden, O. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: A phase II study. Lancet 371:1579-1586; 2008.
21. Le Blanc, K.; Rasmusson, I.; Sundberg, B.; Gotherstrom, C.; Hassan, M.; Uzunel, M.; Ringden, O. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 363:1439-1441; 2004.
22. Lyons, A. B.; Parish, C. R. Determination of lymphocyte division by flow cytometry. J. Immunol. Methods 171: 131-137; 1994.
23. Meads, M. B.; Hazlehurst, L. A.; Dalton, W. S. The bone marrow microenvironment as a tumor sanctuary and contributor to drug resistance. Clin. Cancer Res. 14:2519-2526; 2008.
24. Moretta, A.; Bottino, C.; Vitale, M.; Pende, D.; Biassoni, R.; Mingari, M. C.; Moretta, L. Receptors for HLA class- I molecules in human natural killer cells. Annu. Rev. Immunol. 14:619-648; 1996.
25. Ramasamy, R.; Lam, E. W.; Soeiro, I.; Tisato, V.; Bonnet, D.; Dazzi, F. Mesenchymal stem cells inhibit proliferation and apoptosis of tumor cells: Impact on in vivo tumor growth. Leukemia 21:304-310; 2007.
26. Rasmusson, I.; Ringden, O.; Sundberg, B.; Le Blanc, K. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation 76:1208-1213; 2003.
27. Rosland, G. V.; Svendsen, A.; Torsvik, A.; Sobala, E.; McCormack, E.; Immervoll, H.; Mysliwietz, J.; Tonn, J. C.; Goldbrunner, R.; Lonning, P. E.; Bjerkvig, R.; Schichor, C. Long-term cultures of bone marrow-derived human mesenchymal stem cells frequently undergo spontaneous malignant transformation. Cancer Res. 69:5331-5339; 2009.
28. Rubio, D.; Garcia-Castro, J.; Martin, M. C.; de la Fuente, R.; Cigudosa, J. C.; Lloyd, A. C.; Bernad, A. Spontaneous human adult stem cell transformation. Cancer Res. 65: 3035-3039; 2005.
29. Ruggeri, L.; Mancusi, A.; Capanni, M.; Urbani, E.; Caro-tti, A.; Aloisi, T.; Stern, M.; Pende, D.; Perruccio, K.; Burchielli, E.; Topini, F.; Bianchi, E.; Aversa, F.; Martelli, M. F.; Velardi, A. Donor natural killer cell allorecognition of missing self in haploidentical hematopoietic transplantation for acute myeloid leukemia: Challenging its predictive value. Blood 110:433-440; 2007.
30. Schallmoser, K.; Bartmann, C.; Rohde, E.; Bork, S.; Guelly, C.; Obenauf, A. C.; Reinisch, A.; Horn, P.; Ho, A. D.; Strunk, D.; Wagner, W. Replicative senescenceassociated gene expression changes in mesenchymal stro-mal cells are similar under different culture conditions. Haematologica 95:867-874; 2010.
31. Schmid, I.; Uittenbogaart, C. H.; Keld, B.; Giorgi, J. V. A rapid method for measuring apoptosis and dual-color immunofluorescence by single laser flow cytometry. J. Immunol. Methods 170:145-157; 1994.
32. Selmani, Z.; Naji, A.; Zidi, I.; Favier, B.; Gaiffe, E.; Obert, L.; Borg, C.; Saas, P.; Tiberghien, P.; Rouas-Freiss, N.; Carosella, E. D.; 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 26:212-222; 2008.
33. Smith, T. J. Insights into the role of fibroblasts in human autoimmune diseases. Clin. Exp. Immunol. 141:388-397; 2005.
34. Sotiropoulou, P. A.; Perez, S. A.; Gritzapis, A. D.; Baxe-vanis, C. N.; Papamichail, M. Interactions between human mesenchymal stem cells and natural killer cells. Stem Cells 24:74-85; 2006.
35. Spaeth, E.; Klopp, A.; Dembinski, J.; Andreeff, M.; Marini, F. Inflammation and tumor microenvironments: Defining the migratory itinerary of mesenchymal stem cells. Gene Ther. 15:730-738; 2008.
36. Spaggiari, G. M.; Capobianco, A.; Abdelrazik, H.; Becchetti, F.; Mingari, M. C.; Moretta, L. 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; 2008.
37. Spaggiari, G. M.; Capobianco, A.; Becchetti, S.; Mingari, M. C.; Moretta, L. Mesenchymal stem cell-natural kiler 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; 2006.
38. Stepp, S. E.; Dufourcq-Lagelouse, R.; Le Deist, F.; Bhawan, S.; Certain, S.; Mathew, P. A.; Henter, J. I.; Bennett, M.; Fischer, A.; de Saint Basile, G.; Kumar, V. Perforin gene defects in familial hemophagocytic lymphohistiocytosis. Science 286:1957-1959; 1999.
39. Suva, D.; Garavaglia, G.; Menetrey, J.; Chapuis, B.; Hoff-meyer, P.; Bernheim, L.; Kindler, V. Non-hematopoietic human bone marrow contains long-lasting, pluripotential mesenchymal stem cells. J. Cell. Physiol. 198:110-118; 2004.
40. Suva, D.; Passweg, J.; Arnaudeau, S.; Hoffmeyer, P.; Kindler, V. In vitro activated human T lymphocytes very efficiently attach to allogenic multipotent mesenchymal stromal cells and transmigrate under them. J. Cell. Physiol. 214:588-594; 2008.
41. Tabera, S.; Perez-Simon, J. A.; Diez-Campelo, M.; Sanchez-Abarca, L. I.; Blanco, B.; Lopez, A.; Benito, A.; Ocio, E.; Sanchez-Guijo, F. M.; Canizo, C.; San Miguel, J. F. The effect of mesenchymal stem cells on the viability, proliferation and differentiation of B-lymphocytes. Haematologica 93:1301-1309; 2008.
42. Tarte, K.; Gaillard, J.; Lataillade, J. J.; Fouillard, L.; Becker, M.; Mossafa, H.; Tchirkov, A.; Rouard, H.; Henry, C.; Splingard, M.; Dulong, J.; Monnier, D.; Gourmelon, P.; Gorin, N. C.; Sensebe, L. Clinical-grade pro-duction of human mesenchymal stromal cells: Occurrence of aneuploidy without transformation. Blood 115:1549-1553; 2009
43. Trapani, J. A.; Smyth, M. J. Functional significance of the perforin/granzyme cell death pathway. Nat. Rev. Immunol. 2:735-747; 2002.
44. Uccelli, A.; Moretta, L.; Pistoia, V. Mesenchymal stem cells in health and disease. Nat. Rev. Immunol. 8:726-736; 2008.
45. Zhang, S.; Jia, Z.; Ge, J.; Gong, L.; Ma, Y.; Li, T.; Guo, J.; Chen, P.; Hu, Q.; Zhang, P.; Liu, Y.; Li, Z.; Ma, K.; Li, L.; Zhou, C. Purified human bone marrow multipotent mesenchymal stem cells regenerate infarcted myocardium in experimental rats. Cell Transplant. 14:787-798; 2005.