Effect of human bone marrow mesenchymal stromal cells on cytokine production by peripheral blood naive, memory, and effector T cells

Stem Cell Research and Therapy

Volumn 6, Issue 1, 2015, Pages

  Laranjeira, Paula ^a   Pedrosa, Monia ^a,b   Pedreiro, Susana ^a   Gomes, Joana ^a,b   Martinho, Antonio ^a   Antunes, Brigida ^c   Ribeiro, Tania ^c   Santos, Francisco ^c   Trindade, Helder ^a   Paiva, Artur ^a  

^a IP   (Portugal)

^b UNIVERSITY OF AVEIRO   (Portugal)

^c Biocant   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 9; IONOMYCIN; MESSENGER RNA; PHORBOL 13 ACETATE 12 MYRISTATE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; IL17A PROTEIN, HUMAN; TNF PROTEIN, HUMAN; TUMOR NECROSIS FACTOR;

ADULT; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EFFECTOR CELL; FEMALE; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPHENOTYPING; IN VITRO STUDY; MALE; MEMORY T LYMPHOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; BONE MARROW CELL; COCULTURE; CYTOLOGY; DRUG EFFECTS; GENETICS; LYMPHOCYTE ACTIVATION; MESENCHYMAL STROMA CELL; METABOLISM; MIDDLE AGED; MONONUCLEAR CELL;

ADULT; BONE MARROW CELLS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; COCULTURE TECHNIQUES; CYTOKINES; FEMALE; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-17; INTERLEUKIN-2; IONOMYCIN; LEUKOCYTES, MONONUCLEAR; LYMPHOCYTE ACTIVATION; MALE; MESENCHYMAL STROMAL CELLS; MIDDLE AGED; RNA, MESSENGER; TETRADECANOYLPHORBOL ACETATE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84928713603     PISSN: None     EISSN: 17576512     Source Type: Journal    
DOI: 10.1186/scrt537     Document Type: Article

References (45)

1. Duffy MM, Ritter T, Ceredig R, Griffin MD: Mesenchymal stem cell effects on T-cell effector pathways. Stem Cell Res Ther 2011, 2:34-42.
2. Chen PM, Yen ML, Liu KJ, Sytwu HK, Yen BL: Immunomodulatory properties of human adult and fetal multipotent mesenchymal stem cells. J Biomed Sci 2011, 18:49-59.
3. Spaggiari GM, Abdelrazik H, Becchetti F, Moretta L: MSCs inhibit monocyte-derived DC maturation and function by selectively interfering with the generation of immature DCs: central role of MSC-derived prostaglandin E2. Blood 2009, 113:6576-83.
4. Nauta AJ, Kruisselbrink AB, Lurvink E, Willemze R, Fibbe WE: Mesenchymal stem cells inhibit generation and function of both CD34∈+∈-derived and monocyte-derived dendritic cells. J Immunol 2006, 177:2080-7.
5. Jiang XX, Zhang Y, Liu B, Zhang SX, Wu Y, Yu XD, et al.: Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 2005, 105:4120-6.
6. Dazzi F, Lopes L, Weng L: Mesenchymal stromal cells: a key player in 'innate tolerance'? Immunology 2012, 137:206-13.
7. Beyth S, Borovsky Z, Mevorach D, Liebergall M, Gazit Z, Aslan H, et al.: Human mesenchymal stem cells alter antigen-presenting cell maturation and induce T-cell unresponsiveness. Blood 2005, 105:2214-9.
8. Melief SM, Geutskens SB, Fibbe WE, Roelofs H: Multipotent stromal cells skew monocytes towards an anti-inflammatory interleukin-10-producing phenotype by production of interleukin-6. Haematologica 2013, 98:888-95.
9. Kim J, Hematti P: Mesenchymal stem cell-educated macrophages: a novel type of alternatively activated macrophages. Exp Hematol 2009, 37:1445-53.
10. Kronsteiner B, Wolbank S, Peterbauer A, Hackl C, Redl H, van Griensven M, et al.: Human mesenchymal stem cells from adipose tissue and amnion influence T-cells depending on stimulation method and presence of other immune cells. Stem Cells Dev 2011, 20:2115-26.
11. Ribeiro A, Laranjeira P, Mendes S, Velada I, Leite C, Andrade P, et al.: 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 Res Ther 2013, 4:125-40.
12. 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 2003, 76:1208-13.
13. Najar M, Raicevic G, Id Boufker H, Stamatopoulos B, De Bruyn C, Meuleman N, et al.: Modulated expression of adhesion molecules and galectin-1: role during mesenchymal stromal cell immunoregulatory functions. Exp Hematol 2010, 38:922-32.
14. Luz-Crawford P, Noel D, Fernandez X, Khoury M, Figueroa F, Carrion F, et al.: Mesenchymal stem cells repress Th17 molecular program through the PD-1 pathway. PLoS One 2012, 7:e45272.
15. Duffy MM, Pindjakova J, Hanley SA, McCarthy C, Weidhofer GA, Sweeney EM, et al.: Mesenchymal stem cell inhibition of T-helper 17 cell- differentiation is triggered by cell-cell contact and mediated by prostaglandin E2 via the EP4 receptor. Eur J Immunol 2011, 41:2840-51.
16. Ghannam S, Pene J, Torcy-Moquet G, Jorgensen C, Yssel H: Mesenchymal stem cells inhibit human Th17 cell differentiation and function and induce a T regulatory cell phenotype. J Immunol 2010, 185:302-12.
17. Lee JJ, Jeong HJ, Kim MK, Wee WR, Lee WW, Kim SU, et al.: CD39-mediated effect of human bone marrow-derived mesenchymal stem cells on the human Th17 cell function. Purinergic Signal 2014, 10:357-65.
18. Gonzalez MA, Gonzalez-Rey E, Rico L, Buscher D, Delgado M: Treatment of experimental arthritis by inducing immune tolerance with human adipose-derived mesenchymal stem cells. Arthritis Rheum 2009, 60:1006-19.
19. Chen QQ, Yan L, Wang CZ, Wang WH, Shi H, Su BB, et al.: Mesenchymal stem cells alleviate TNBS-induced colitis by modulating inflammatory and autoimmune responses. World J Gastroenterol 2013, 19:4702-17.
20. Carrion F, Nova E, Luz P, Apablaza F, Figueroa F: Opposing effect of mesenchymal stem cells on Th1 and Th17 cell polarization according to the state of CD4+ T cell activation. Immunol Lett 2011, 135:10-6.
21. Eljaafari A, Tartelin ML, Aissaoui H, Chevrel G, Osta B, Lavocat F, et al.: Bone marrow-derived and synovium-derived mesenchymal cells promote Th17 cell expansion and activation through caspase 1 activation: contribution to the chronicity of rheumatoid arthritis. Arthritis Rheum 2012, 64:2147-57.
22. Guo Z, Zheng C, Chen Z, Gu D, Du W, Ge J, et al.: Fetal BM-derived mesenchymal stem cells promote the expansion of human Th17 cells, but inhibit the production of Th1 cells. Eur J Immunol 2009, 39:2840-9.
23. Hsu SC, Wang LT, Yao CL, Lai HY, Chan KY, Liu BS, et al.: Mesenchymal stem cells promote neutrophil activation by inducing IL-17 production in CD4+ CD45RO+ T cells. Immunobiology 2013, 218:90-5.
24. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, et al.: Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006, 8:315-7.
25. Alipour R, Adib M, Masoumi Karimi M, Hashemi-Beni B, Sereshki N: Comparing the immunoregulatory effects of stem cells from human exfoliated deciduous teeth and bone marrow-derived mesenchymal stem cells. Iran J Allergy Asthma Immunol 2013, 12:331-44.
26. Aggarwal S, Pittenger MF: Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 2005, 105:1815-22.
27. Batten P, Sarathchandra P, Antoniw JW, Tay SS, Lowdell MW, Taylor PM, et al.: Human mesenchymal stem cells induce T cell anergy and downregulate T cell allo-responses via the TH2 pathway: relevance to tissue engineering human heart valves. Tissue Eng 2006, 12:2263-73.
28. Zappia E, Casazza S, Pedemonte E, Benvenuto F, Bonanni I, Gerdoni E, et al.: Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 2005, 106:1755-61.
29. Zheng ZH, Li XY, Ding J, Jia JF, Zhu P: Allogeneic mesenchymal stem cell and mesenchymal stem cell-differentiated chondrocyte suppress the responses of type II collagen-reactive T cells in rheumatoid arthritis. Rheumatology (Oxford) 2008, 47:22-30.
30. Gieseke F, Bohringer J, Bussolari R, Dominici M, Handgretinger R, Muller I: Human multipotent mesenchymal stromal cells use galectin-1 to inhibit immune effector cells. Blood 2010, 116:3770-9.
31. Glennie S, Soeiro I, Dyson PJ, Lam EW, Dazzi F: Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 2005, 105:2821-7.
32. Krampera M, Glennie S, Dyson J, Scott D, Laylor R, Simpson E, et al.: Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 2003, 101:3722-9.
33. Chen M, Su W, Lin X, Guo Z, Wang J, Zhang Q, et al.: Adoptive transfer of human gingiva-derived mesenchymal stem cells ameliorates collagen-induced arthritis via suppression of Th1 and Th17 cells and enhancement of regulatory T cell differentiation. Arthritis Rheum 2013, 65:1181-93.
34. Larocca RA, Moraes-Vieira PM, Bassi EJ, Semedo P, de Almeida DC, da Silva MB, et al.: Adipose tissue-derived mesenchymal stem cells increase skin allograft survival and inhibit Th-17 immune response. PLoS One 2013, 8:e76396.
35. Selleri S, Dieng MM, Nicoletti S, Louis I, Beausejour C, Le Deist F, et al.: Cord-Blood-Derived Mesenchymal Stromal Cells Downmodulate CD4(+) T-Cell Activation by Inducing IL-10-Producing Th1 Cells. Stem Cells Dev 2013, 22:1063-75.
36. Wolf J, Rose-John S, Garbers C: Interleukin-6 and its receptors: A highly regulated and dynamic system. Cytokine 2014, 70:11-20.
37. Scheller J, Chalaris A, Schmidt-Arras D, Rose-John S: The pro- and anti-inflammatory properties of the cytokine interleukin-6. Biochim Biophys Acta 1813, 2011:878-88.
38. Goswami R, Kaplan MH: A brief history of IL-9. J Immunol 2011, 186:3283-8.
39. Zhu J, Paul WE: Heterogeneity and plasticity of T helper cells. Cell Res 2010, 20:4-12.
40. Schmitt E, Klein M, Bopp T: Th9 cells, new players in adaptive immunity. Trends Immunol 2014, 35:61-8.
41. Noelle RJ, Nowak EC: Cellular sources and immune functions of interleukin-9. Nat Rev Immunol 2010, 10:683-7.
42. Fu QL, Chow YY, Sun SJ, Zeng QX, Li HB, Shi JB, et al.: Mesenchymal stem cells derived from human induced pluripotent stem cells modulate T-cell phenotypes in allergic rhinitis. Allergy 2012, 67:1215-22.
43. Kavanagh H, Mahon BP: Allogeneic mesenchymal stem cells prevent allergic airway inflammation by inducing murine regulatory T cells. Allergy 2011, 66:523-31.
44. Lathrop MJ, Brooks EM, Bonenfant NR, Sokocevic D, Borg ZD, Goodwin M, et al.: Mesenchymal stromal cells mediate Aspergillus hyphal extract-induced allergic airway inflammation by inhibition of the Th17 signaling pathway. Stem Cells Transl Med 2014, 3:194-205.
45. Nemeth K, Keane-Myers A, Brown JM, Metcalfe DD, Gorham JD, Bundoc VG, et al.: Bone marrow stromal cells use TGF-beta to suppress allergic responses in a mouse model of ragweed-induced asthma. Proc Natl Acad Sci U S A 2010, 107:5652-7.