Comparing the Immunoregulatory Effects of Stem Cells from Human Exfoliated Deciduous Teeth and Bone Marrow-derived Mesenchymal Stem Cells
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Abstract
Stem cells from human exfoliated deciduous teeth (SHED) have been introduced recently and possess characteristics similar to mesenchymal stem cells (MSCs). Because of their convenient accessibility and safety of harvest, SHED can be a preferable source for the ever- increasing MSCs’ applications. While they are new, their immunoproperties have not been adequately studied. In this study, we aimed to explore the effect of SHED on T lymphocytes and compare it to conventional MSCs (BMMSCs).
At first the isolated T lymphocytes were activated specifically/nonspecifically in vitro and cocultured with SHED or BMMSCs under the same conditions, subsequently their proliferation and cytokine secretion (IL-2 and IFN-γ) were measured.
In our experiment, BMMSCs and SHED inhibit the proliferation and cytokine production of both PHA and alloantigen stimulated T lymphocytes in a dose-dependent manner. In direct and indirect contact to T lymphocytes, the inhibition of BMMSCs (but not of SHED) was significantly different The cytokine production from activated T cells was affected differently by two types of MSCs. The inhibition decreased by the separation of lymphocytes and MSCs by a semipermeable membrane, but it was not abolished.
This study showed that SHED suppress the activation of human T lymphocytes in vitro like other MSCs. Compared to BMMSCs, this suppression was alleviated. In the equal conditions, the pattern of immune-modulation of BMMSCs and SHED was different, suggesting that SHED do not exert the exact mechanisms of BMMSCs' immunosuppression. This finding should be verified by further studies focused on the detailed mechanisms of the immunomodulation of SHED and also BMMSCs.
1. Cai J, Rao MS. Stem cell and precursor cell therapy. Neuromolecular Med 2002; 2(3):233-49.
2. Yang XF. Immunology of stem cells and cancer stem cells. Cell Mol Immunol 2007; 4(3):161-71.
3. Tasso R, Pennesi G. When stem cells meet immunoregulation. Int Immunopharmacol 2009; 9(5):596-8.
4. Castillo AB, Jacobs CR. Mesenchymal stem cell mechanobiology. Curr Osteoporos Rep 2010; 8(2):98-104.
5. Heng TS, Dudakov JA, Khong DM, Chidgey AP, Boyd RL. Stem cells--meet immunity. J Mol Med 2009;87(11):1061-9.
6. Dazzi F, Horwood NJ. Potential of mesenchymal stem cell therapy. Curr Opin Oncol 2007; 19(6):650-5.
7. Charbord P. Bone marrow mesenchymal stem cells: historical overview and concepts. Hum Gene Ther 2010;21(9):1045-56.
8. Chen Y, Shao JZ, Xiang LX, Dong XJ, Zhang GR.Mesenchymal stem cells: a promising candidate in regenerative medicine. Int J Biochem Cell Biol 2008;40(5):815-20.
9. Hanson S, Thibeault SL, Hematti P. Clinical applications of mesenchymal stem cells in laryngotracheal reconstruction. Curr Stem Cell Res Ther 2010; 5(3):268-72.
10. Newman RE, Yoo D, LeRoux MA, Danilkovitch- Miagkova A. Treatment of inflammatory diseases with mesenchymal stem cells. Inflamm Allergy Drug Targets 2009; 8(2):110-23.
11. Kode JA, Mukherjee S, Joglekar MV, Hardikar AA.Mesenchymal stem cells: immunobiology and role in immunomodulation and tissue regeneration. Cytotherapy 2009; 11(4):377-91.
12. Bernardo ME, Locatelli F, Fibbe WE. Mesenchymal stromal cells. Ann N Y Acad Sci 2009; 1176:101-17.
13. Hoogduijn MJ, Popp F, Verbeek R, Masoodi M, Nicolaou A, Baan C, et al. The immunomodulatory properties of mesenchymal stem cells and their use for immunotherapy. Int Immunopharmacol 2010;10(12):1496-500.
14. Nauta AJ, Fibbe WE. Immunomodulatory properties of mesenchymal stromal cells. Blood 2007; 110(10):3499-506.
15. Jones BJ, McTaggart SJ. Immunosuppression by mesenchymal stromal cells: from culture to clinic. Exp Hematol 2008; 36(6):733-41.
16. Brooke G, Rossetti T, Pelekanos R, Ilic N, Murray P, Hancock S, et al. Manufacturing of human placenta- derived mesenchymal stem cells for clinical trials. Br J Haematol 2009; 144(4):571-9.
17. Kong QF, Sun B, Bai SS, Zhai DX, Wang GY, Liu YM, et al. Administration of bone marrow stromal cells ameliorates experimental autoimmune myasthenia gravis by altering the balance of Th1/Th2/Th17/Treg cell subsets through the secretion of TGF-beta. J Neuroimmunol 2009; 207(1-2):83-91.
18. Yen BL, Huang HI, Chien CC, Jui HY, Ko BS, Yao M, et al. Isolation of multipotent cells from human term placenta. Stem Cells 2005; 23(1):3-9.
19. Miao Z, Jin J, Chen L, Zhu J, Huang W, Zhao J, et al.Isolation of mesenchymal stem cells from human placenta: comparison with human bone marrow mesenchymal stem cells. Cell Biol Int 2006; 30(9):681-7.
20. Nakamura S, Yamada Y, Katagiri W, Sugito T, Ito K,Ueda M. Stem cell proliferation pathways comparison between human exfoliated deciduous teeth and dental pulp stem cells by gene expression profile from promising dental pulp. J Endod 2009; 35(11):1536-42.
21. Lee OK, Kuo TK, Chen WM, Lee KD, Hsieh SL, Chen TH. Isolation of multipotent mesenchymal stem cells from umbilical cord blood. Blood 2004; 103(5):1669-75.
22. Kerkis I, Kerkis A, Dozortsev D, Stukart-Parsons GC, Gomes Massironi SM, Pereira LV, et al. Isolation and characterization of a population of immature dental pulp stem cells expressing OCT-4 and other embryonic stem cell markers. Cells Tissues Organs 2006; 184(3-4):105-16.
23. Feng B, Chen L. Review of mesenchymal stem cells and tumors: executioner or coconspirator? Cancer Biother Radiopharm 2009; 24(6):717-21.
24. Brandau S, Jakob M, Hemeda H, Bruderek K, Janeschik S, Bootz F, et al. Tissue-resident mesenchymal stem cells attract peripheral blood neutrophils and enhance their inflammatory activity in response to microbial challenge.J Leukoc Biol 2010; 88(5):1005-15.
25. Koyama N, Okubo Y, Nakao K, Bessho K. Evaluation of pluripotency in human dental pulp cells. J Oral Maxillofac Surg 2009; 67(3):501-6.
26. Arora V, Arora P, Munshi AK. Banking stem cells from human exfoliated deciduous teeth (SHED): saving for the future. J Clin Pediatr Dent 2009; 33(4):289-94.
27. Telles PD, Machado MA, Sakai VT, Nor JE. Pulp tissue from primary teeth: new source of stem cells. J Appl Oral Sci 2011; 19(3):189-94.
28. Huang AH, Chen YK, Lin LM, Shieh TY, Chan AW.Isolation and characterization of dental pulp stem cells from a supernumerary tooth. J Oral Pathol 2008; 37(9):571-4.
29. Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, et al. SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci U S A 2003;100(10):5807-12.
30. Petrovic V, Stefanovic V. Dental tissue--new source for stem cells. ScientificWorldJournal 2009; 9:1167-77.
31. Morsczeck C, Vollner F, Saugspier M, Brandl C, Reichert TE, Driemel O, et al. Comparison of human dental follicle cells (DFCs) and stem cells from human exfoliated deciduous teeth (SHED) after neural differentiation in vitro. Clin Oral Investig 2010;14(4):433-40.
32. Nishino Y, Yamada Y, Ebisawa K, Nakamura S, Okabe K, Umemura E, et al. Stem cells from human exfoliated deciduous teeth (SHED) enhance wound healing and the possibility of novel cell therapy. Cytotherapy 2011;13(5):598-605.
33. Li C, Zhang W, Jiang X, Mao N. Human-placenta- derived mesenchymal stem cells inhibit proliferation and function of allogeneic immune cells. Cell Tissue Res 2007; 330(3):437-46.
34. Tse WT, Pendleton JD, Beyer WM, Egalka MC, Guinan EC. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 2003; 75(3):389-97.
35. Stagg J, Pommey S, Eliopoulos N, Galipeau J. Interferon- gamma-stimulated marrow stromal cells: a new type of nonhematopoietic antigen-presenting cell. Blood 2006;107(6):2570-7.
36. Hematti P. Role of mesenchymal stromal cells in solid organ transplantation. Transplant Rev (Orlando) 2008;22(4):262-73.
37. Crop M, Baan C, Weimar W, Hoogduijn M. Potential of mesenchymal stem cells as immune therapy in solid- organ transplantation. Transpl Int 2009; 22(4):365-76.
38. Puissant B, Barreau C, Bourin P, Clavel C, Corre J, Bousquet C, et al. Immunomodulatory effect of human adipose tissue-derived adult stem cells: comparison with bone marrow mesenchymal stem cells. Br J Haematol 2005; 129(1):118-29.
39. Chang CJ, Yen ML, Chen YC, Chien CC, Huang HI, Bai CH, et al. Placenta-derived multipotent cells exhibit immunosuppressive properties that are enhanced in the presence of interferon-gamma. Stem Cells 2006;24(11):2466-77.
40. Le Blanc K, Tammik C, Rosendahl K, Zetterberg E, Ringden O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Hematol 2003; 31(10):890-6.
41. 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(9):3722-9.
42. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood2005; 105(4):1815-22.
43. Ramasamy R, Tong CK, Seow HF, Vidyadaran S, Dazzi F. The immunosuppressive effects of human bone marrow-derived mesenchymal stem cells target T cell proliferation but not its effector function. Cell Immunol 2008; 251(2):131-6.
44. Wada N, Menicanin D, Shi S, Bartold PM, Gronthos S.Immunomodulatory properties of human periodontal ligament stem cells. J Cell Physiol 2009; 219(3):667-76.
45. Yanez R, Lamana ML, Garcia-Castro J, Colmenero I, Ramirez M, Bueren JA. Adipose tissue-derived mesenchymal stem cells have in vivo immunosuppressive properties applicable for the control of the graft-versus- host disease. Stem Cells 2006; 24(11):2582-91.
46. Wang L, Lu XF, Lu YR, Liu J, Gao K, Zeng YZ, et al.Immunogenicity and immune modulation of osteogenic differentiated mesenchymal stem cells from Banna minipig inbred line. Transplant Proc 2006; 38(7):2267-9.
47. Meirelles Lda S, Fontes AM, Covas DT, Caplan AI.Mechanisms involved in the therapeutic properties of mesenchymal stem cells. Cytokine Growth Factor Rev 2009; 20(5-6):419-27.
48. Le Blanc K, Tammik L, Sundberg B, Haynesworth SE, Ringden O. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol 2003; 57(1):11-20.
49. Potian JA, Aviv H, Ponzio NM, Harrison JS, Rameshwar P. Veto-like activity of mesenchymal stem cells: functional discrimination between cellular responses to alloantigens and recall antigens. J Immunol 2003; 171(7):3426-34.
50. Prasanna SJ, Gopalakrishnan D, Shankar SR, Vasandan AB. Pro-inflammatory cytokines, IFNgamma and TNFalpha, influence immune properties of human bone marrow and Wharton jelly mesenchymal stem cells differentially. PLoS One 2010; 5(2):e9016.
51. Chan JL, Tang KC, Patel AP, Bonilla LM, Pierobon N, Ponzio NM, et al. Antigen-presenting property of mesenchymal stem cells occurs during a narrow window at low levels of interferon-gamma. Blood 2006; 107(12):4817-24.
52. Schurgers E, Kelchtermans H, Mitera T, Geboes L, Matthys P. Discrepancy between the in vitro and in vivo effects of murine mesenchymal stem cells on T-cell proliferation and collagen-induced arthritis. Arthritis Res Ther 2010; 12(1):R31.
53. Opitz CA, Litzenburger UM, Lutz C, Lanz TV, Tritschler I, Koppel A, et al. Toll-like receptor engagement enhances the immunosuppressive properties of human bone marrow-derived mesenchymal stem cells by inducing indoleamine-2,3-dioxygenase-1 via interferon- beta and protein kinase R. Stem Cells 2009; 27(4):909-19.
54. Liotta F, Angeli R, Cosmi L, Fili L, Manuelli C, Frosali F, et al. Toll-like receptors 3 and 4 are expressed by human bone marrow-derived mesenchymal stem cells and can inhibit their T-cell modulatory activity by impairing Notch signaling. Stem Cells 2008; 26(1):279-89.
55. Romieu-Mourez R, Francois M, Boivin MN, Bouchentouf M, Spaner DE, Galipeau J. Cytokine modulation of TLR expression and activation in mesenchymal stromal cells leads to a proinflammatory phenotype. J Immunol 2009; 182(12):7963-73.
56. Tomchuck SL, Zwezdaryk KJ, Coffelt SB, Waterman RS, Danka ES, Scandurro AB. Toll-like receptors on human mesenchymal stem cells drive their migration and immunomodulating responses. Stem Cells 2008;26(1):99-107.
57. DelaRosa O, Lombardo E. Modulation of adult mesenchymal stem cells activity by toll-like receptors: implications on therapeutic potential. Mediators Inflamm 2010; 2010:865601.
58. Nasef A, Mathieu N, Chapel A, Frick J, Francois S, Mazurier C, et al. Immunosuppressive effects of mesenchymal stem cells: involvement of HLA-G. Transplantation 2007; 84(2):231-7.
59. Augello A, Tasso R, Negrini SM, Amateis A, Indiveri F, Cancedda R, et al. Bone marrow mesenchymal progenitor cells inhibit lymphocyte proliferation by activation of the programmed death 1 pathway. Eur J Immunol 2005;35(5):1482-90.
60. Kang JW, Kang KS, Koo HC, Park JR, Choi EW, Park YH. Soluble factors-mediated immunomodulatory effects of canine adipose tissue-derived mesenchymal stem cells. Stem Cells Dev 2008; 17(4):681-93.
61. Sato K, Ozaki K, Oh I, Meguro A, Hatanaka K, Nagai T, et al. Nitric oxide plays a critical role in suppression of T- cell proliferation by mesenchymal stem cells. Blood 2007; 109(1):228-34.
62. 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(5):2214-9.
63. Krampera M, Cosmi L, Angeli R, Pasini A, Liotta F, Andreini A, et al. Role for interferon-gamma in the immunomodulatory activity of human bone marrow mesenchymal stem cells. Stem Cells 2006; 24(2):386-98.
64. Yang SH, Park MJ, Yoon IH, Kim SY, Hong SH, Shin JY, et al. Soluble mediators from mesenchymal stem cells suppress T cell proliferation by inducing IL-10. Exp Mol Med 2009; 41(5):315-24.
65. Roelen DL, van der Mast BJ, in't Anker PS, Kleijburg C, Eikmans M, van Beelen E, et al. Differential immunomodulatory effects of fetal versus maternal multipotent stromal cells. Hum Immunol 2009; 70(1):16-23.
66. Yamaza T, Kentaro A, Chen C, Liu Y, Shi Y, Gronthos S, et al. Immunomodulatory properties of stem cells from human exfoliated deciduous teeth. Stem Cell Res Ther 2010; 1(1):5.
67. Nasef A, Zhang YZ, Mazurier C, Bouchet S, Bensidhoum M, Francois S, et al. Selected Stro-1-enriched bone marrow stromal cells display a major suppressive effect on lymphocyte proliferation. Int J Lab Hematol 2009;31(1):9-19.
68. Abul K. Abbas, Andrew H. Lichtman, Shiv Pillai.Cellular and Molecular Immunology. 6th edition, Saunders Elsevier; 2010.
69. Rasmusson I. Immune modulation by mesenchymal stem cells. Exp Cell Res 2006; 312(12):2169-79.
70. Darlington PJ, Boivin MN, Renoux C, Francois M, Galipeau J, Freedman MS, et al. Reciprocal Th1 and Th17 regulation by mesenchymal stem cells: Implication for multiple sclerosis. Ann Neurol 2010; 68(4):540-5.
71. Sioud M, Mobergslien A, Boudabous A, Floisand Y.Mesenchymal stem cell-mediated T cell suppression occurs through secreted galectins. Int J Oncol 2010;38(2):385-90.
72. Sarugaser R, Ennis J, Stanford WL, Davies JE. Isolation, propagation, and characterization of human umbilical cord perivascular cells (HUCPVCs). Methods Mol Biol 2009; 482:269-79.
73. DelaRosa O, Lombardo E, Beraza A, Mancheno-Corvo P, Ramirez C, Menta R, et al. Requirement of IFN-gamma- mediated indoleamine 2,3-dioxygenase expression in the modulation of lymphocyte proliferation by human adipose-derived stem cells. Tissue Eng Part A 2009;15(10):2795-806.
74. 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(7):2821-7.
75. Huang GT, Gronthos S, Shi S. Mesenchymal stem cells derived from dental tissues vs. those from other sources: their biology and role in regenerative medicine. J Dent Res 2009; 88(9):792-806.
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| Issue | Vol 12, No 4 (2013) | |
| Section | Articles | |
| Keywords | ||
| Cytokine Immunoregulatory Mesenchymal stem cells Stem cells from human exfoliated deciduous teeth (SHED) T lymphocyte | ||
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