Oral mucosal progenitor cells are potently immunosuppressive in a dose-independent manner

Stem Cells and Development

Volumn 21, Issue 9, 2012, Pages 1478-1487

  Davies, Lindsay C ^a   Lönnies, Helena ^b   Locke, Matthew ^a   Sundberg, Berit ^b   Rosendahl, Kerstin ^b   Götherström, Cecilia ^b   Le Blanc, Katarina ^b   Stephens, Phil ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; CD40 ANTIGEN; CD40 LIGAND; CD86 ANTIGEN; FAS LIGAND; GAMMA INTERFERON; HLA ANTIGEN CLASS 2; MITOGENIC AGENT;

APOPTOSIS; ARTICLE; CELL SURFACE; HUMAN; HUMAN CELL; IMMUNOGENICITY; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; LAMINA PROPRIA; LYMPHOCYTE PROLIFERATION; MESENCHYMAL STEM CELL; MIXED LYMPHOCYTE CULTURE; MOUTH MUCOSA; PRIORITY JOURNAL; STAINING; STEM CELL; TISSUE ENGINEERING;

ANTIGENS, CD; APOPTOSIS; CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; FEMALE; HUMANS; IMMUNE SYSTEM DISEASES; IMMUNE TOLERANCE; INTERFERON-GAMMA; LYMPHOCYTES; MALE; MOUTH MUCOSA; STEM CELLS; TISSUE ENGINEERING;

EID: 84862232008     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2011.0434     Document Type: Article

References (37)

1. Davies LC, M Locke, RD Webb, JT Roberts, M Langley, DW Thomas, CW Archer and P Stephens. (2010). A multipotent neural crest-derived progenitor cell population is resident within the oral mucosa lamina propria. Stem Cells Dev 19:819-830.
2. Kotobuki N, M Hirose, H Funaoka and H Ohgushi. (2004). Enhancement of in vitro osteoblastic potential after selective sorting of osteoblasts with high alkaline phosphatase activity from human osteoblast-like cells. Cell Transplant 13:377-383. (Pubitemid 39163082)
3. Ennis J, C Gotherstrom, K Le Blanc and JE Davies. (2008). In vitro immunologic properties of human umbilical cord perivascular cells. Cytotherapy 10:174-181.
4. Wada N, D Menicanin, S Shi, PM Bartold and S Gronthos. (2009). Immunomodulatory properties of human periodontal ligament stem cells. J Cell Physiol 219:667-676.
5. Wang M, Y Yang, D Yang, F Luo, W Liang, S Guo and J Xu. (2009). The immunomodulatory activity of human umbilical cord blood-derived mesenchymal stem cells in vitro. Immunology 126:220-232.
6. Deans RJ and AB Moseley. (2000). Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol 28:875-884.
7. Pittenger MF, AM Mackay, SC Beck, RK Jaiswal, R Douglas, JD Mosca, MA Moorman, DW Simonetti, S Craig and DR Marshak. (1999). Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147. (Pubitemid 29282067)
8. Tse WT, JD Pendleton, WM Beyer, MC Egalka and EC Guinan. (2003). Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 75:389-397. (Pubitemid 36222968)
9. Ren G, J Su, L Zhang, X Zhao, W Ling, A L'Huillie, J Zhang, Y Lu, AI Roberts, et al. (2009). Species variation in the mechanisms of mesenchymal stem cell-mediated immunosuppression. Stem Cells 27:1954-1962.
10. Le Blanc K, H Samuelsson, B Gustafsson, M Remberger, B Sundberg, J Arvidson, P Ljungman, H Lonnies, S Nava and O Ringden. (2007). Transplantation of mesenchymal stem cells to enhance engraftment of hematopoietic stem cells. Leukemia 21:1733-1738. (Pubitemid 47086763)
11. Le Blanc K, F Frassoni, L Ball, F Locatelli, H Roelofs, I Lewis, E Lanino, B Sundberg, ME Bernardo, et al. (2008). Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 371:1579-1586. (Pubitemid 351626841)
12. Ringden O, M Uzunel, I Rasmusson, M Remberger, B Sundberg, H Lonnies, HU Marschall, A Dlugosz, A Szakos, et al. (2006). Mesenchymal stem cells for treatment of therapy- resistant graft-versus-host disease. Transplantation 81:1390-1397. (Pubitemid 43847148)
13. Weng JY, X Du, SX Geng, YW Peng, Z Wang, ZS Lu, SJ Wu, CW Luo, R Guo, et al. (2010). Mesenchymal stem cell as salvage treatment for refractory chronic GVHD. Bone Marrow Transplant 45:1732-1740.
14. Ringden O and A Keating. (2011). Mesenchymal stromal cells as treatment for chronic GVHD. Bone Marrow Transplant 46:163-164.
15. Kern S, H Eichler, J Stoeve, H Kluter and K Bieback. (2006). Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24:1294-1301. (Pubitemid 44464698)
16. Stenderup K, J Justesen, C Clausen and M Kassem. (2003). Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 33:919-926. (Pubitemid 37543568)
17. Stephens P, KJ Davies, T al-Khateeb, JP Shepherd and DW Thomas. (1996). A comparison of the ability of intra-oral and extra-oral fibroblasts to stimulate extracellular matrix reorganization in a model of wound contraction. J Dent Res 75:1358-1364. (Pubitemid 32774104)
18. Ringden O and B Berg. (1977). Correlation between magnitude of MLC and kidney graft survival in intrafamilial transplantation. Tissue Antigens 10:364-372. (Pubitemid 8252969)
19. Mahanonda R, N Sa-Ard-Iam, P Montreekachon, A Pimkhaokham, K Yongvanichit, MM Fukuda and S Pichyangkul. (2007). IL-8 and IDO expression by human gingival fibroblasts via TLRs. J Immunol 178:1151-1157. (Pubitemid 46095188)
20. Muller AJ and GC Prendergast. (2007). Indoleamine 2,3- dioxygenase in immune suppression and cancer. Curr Cancer Drug Targets 7:31-40. (Pubitemid 46345506)
21. Munn DH and AL Mellor. (2004). IDO and tolerance to tumors. Trends Mol Med 10:15-18. (Pubitemid 38165324)
22. Le Blanc K, C Tammik, K Rosendahl, E Zetterberg and O Ringden. (2003). HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol 31:890-896. (Pubitemid 37211373)
23. Aggarwal S and MF Pittenger. (2005). Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105:1815-1822. (Pubitemid 40223708)
24. Nauta AJ and WE Fibbe. (2007). Immunomodulatory properties of mesenchymal stromal cells. Blood 110:3499-3506. (Pubitemid 350159613)
25. Selmani Z, A Naji, I Zidi, B Favier, E Gaiffe, L Obert, C Borg, P Saas, P Tiberghien, et al. (2008). 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.
26. Frassoni F, M Labopin and A Bacigalupo. (2002). Expanded mesenchymal stem cells (MSC) co-infused with HLA identical hematopoietic stem cell transplants, reduce acute and chronic graft-versus-host disease: a matched pair analysis. Bone Marrow Transplant 29:S2.
27. Rubinstein P, RE Rosenfield, JW Adamson and CE Stevens. (1993). Stored placental blood for unrelated bone marrow reconstitution. Blood 81:1679-1690. (Pubitemid 23101579)
28. Klyushnenkova E, JD Mosca, V Zernetkina, MK Majumdar, KJ Beggs, DW Simonetti, RJ Deans and KR McIntosh. (2005). T cell responses to allogeneic human mesenchymal stem cells: immunogenicity, tolerance, and suppression. J Biomed Sci 12:47-57. (Pubitemid 40576763)
29. Trivedi P and P Hematti. (2008). Derivation and immunological characterization of mesenchymal stromal cells from human embryonic stem cells. Exp Hematol 36:350-359.
30. Gotherstrom C, O Ringden, C Tammik, E Zetterberg, M Westgren and K Le Blanc. (2004). Immunologic properties of human fetal mesenchymal stem cells. Am J Obstet Gynecol 190:239-245. (Pubitemid 38156354)
31. Ryan JM, F Barry, JM Murphy and BP Mahon. (2007). Interferon- gamma does not break, but promotes the immunosuppressive capacity of adult human mesenchymal stem cells. Clin Exp Immunol 149:353-363. (Pubitemid 47063057)
32. Le Blanc K, L Tammik, B Sundberg, SE Haynesworth and O Ringden. (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. (Pubitemid 38019084)
33. Najar M, R Rouas, G Raicevic, HI Boufker, P Lewalle, N Meuleman, D Bron, M Toungouz, P Martiat and L Lagneaux. (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.
34. Krampera M, S Glennie, J Dyson, D Scott, R Laylor, E Simpson and F Dazzi. (2003). Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide. Blood 101:3722-3729. (Pubitemid 36857965)
35. Ren G, L Zhang, X Zhao, G Xu, Y Zhang, AI Roberts, RC Zhao and Y Shi. (2008). Mesenchymal stem cell-mediated immunosuppression occurs via concerted action of chemokines and nitric oxide. Cell Stem Cell 2:141-150. (Pubitemid 351181031)
36. Forouzandeh F, RB Jalili, M Germain, V Duronio and A Ghahary. (2008). Differential immunosuppressive effect of indoleamine 2,3-dioxygenase (IDO) on primary human CD4 + and CD8 + T cells. Mol Cell Biochem 309:1-7.
37. Munn DH, MD Sharma, B Baban, HP Harding, Y Zhang, D Ron and AL Mellor. (2005). GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity 22:633-642. (Pubitemid 40719198)