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Blood, 15 May 2002, Vol. 99, No. 10, pp. 3838-3843

TRANSPLANTATION

Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli

Massimo Di Nicola, Carmelo Carlo-Stella, Michele Magni, Marco Milanesi, Paolo D. Longoni, Paola Matteucci, Salvatore Grisanti, and Alessandro M. Gianni

From the "Cristina Gandini" Bone Marrow Transplantation Unit, Istituto Nazionale Tumori, Milano, Italy; and Chair of Oncology, University of Milano, Milano, Italy.

CD2+ T lymphocytes obtained from either the donor of bone marrow stromal cells (BMSCs) or a third party were cultured in mixed lymphocyte reactions (MLRs) with either allogeneic dendritic cells (DCs) or peripheral blood lymphocytes (PBLs). When autologous or allogeneic BMSCs were added back to T cells stimulated by DCs or PBLs, a significant and dose-dependent reduction of T-cell proliferation, ranging from 60% ± 5% to 98% ± 1%, was evident. Similarly, addition of BMSCs to T cells stimulated by polyclonal activators resulted in a 65% ± 5% (P = .0001) suppression of proliferation. BMSC- induced T-cell suppression was still evident when BMSCs were added in culture as late as 5 days after starting of MLRs. BMSC-inhibited T lymphocytes were not apoptotic and efficiently proliferated on restimulation. BMSCs significantly suppressed both CD4+ and CD8+ T cells (65% ± 5%, [P = .0005] and 75% ± 15% [P = .0005], respectively). Transwell experiments, in which cell-cell contact between BMSCs and effector cells was prevented, resulted in a significant inhibition of T-lymphocyte proliferation, suggesting that soluble factors were involved in this phenomenon. By using neutralizing monoclonal antibodies, transforming growth factor beta 1 and hepatocyte growth factor were identified as the mediators of BMSC effects. In conclusion, our data demonstrate that (1) autologous or allogeneic BMSCs strongly suppress T-lymphocyte proliferation, (2) this phenomenon that is triggered by both cellular as well as nonspecific mitogenic stimuli has no immunologic restriction, and (3) T-cell inhibition is not due to induction of apoptosis and is likely due to the production of soluble factors.

© 2002 by The American Society of Hematology.
 

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JEMHome page
A.-M. Rodriguez, D. Pisani, C. A. Dechesne, C. Turc-Carel, J.-Y. Kurzenne, B. Wdziekonski, A. Villageois, C. Bagnis, J.-P. Breittmayer, H. Groux, et al.
Transplantation of a multipotent cell population from human adipose tissue induces dystrophin expression in the immunocompetent mdx mouse
J. Exp. Med., May 2, 2005; 201(9): 1397 - 1405.
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S. Glennie, I. Soeiro, P. J. Dyson, E. W.-F. Lam, and F. Dazzi
Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells
Blood, April 1, 2005; 105(7): 2821 - 2827.
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BloodHome page
P. Terness, J.-J. Chuang, T. Bauer, L. Jiga, and G. Opelz
Regulation of human auto- and alloreactive T cells by indoleamine 2,3-dioxygenase (IDO)-producing dendritic cells: too much ado about IDO?
Blood, March 15, 2005; 105(6): 2480 - 2486.
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BloodHome page
S. Aggarwal and M. F. Pittenger
Human mesenchymal stem cells modulate allogeneic immune cell responses
Blood, February 15, 2005; 105(4): 1815 - 1822.
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JRSMHome page
H T Hassan and M El-Sheemy
Adult bone-marrow stem cells and their potential in medicine
J R Soc Med, October 1, 2004; 97(10): 465 - 471.
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Circ. Res.Home page
M. F. Pittenger and B. J. Martin
Mesenchymal Stem Cells and Their Potential as Cardiac Therapeutics
Circ. Res., July 9, 2004; 95(1): 9 - 20.
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BloodHome page
R. Meisel, A. Zibert, M. Laryea, U. Gobel, W. Daubener, and D. Dilloo
Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation
Blood, June 15, 2004; 103(12): 4619 - 4621.
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J. Thorac. Cardiovasc. Surg.Home page
K.H. Grinnemo, A. Mansson, G. Dellgren, D. Klingberg, E. Wardell, V. Drvota, C. Tammik, J. Holgersson, O. Ringden, C. Sylven, et al.
Xenoreactivity and engraftment of human mesenchymal stem cells transplanted into infarcted rat myocardium
J. Thorac. Cardiovasc. Surg., May 1, 2004; 127(5): 1293 - 1300.
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D.-W. Kim, Y.-J. Chung, T.-G. Kim, Y.-L. Kim, and I.-H. Oh
Cotransplantation of third-party mesenchymal stromal cells can alleviate single-donor predominance and increase engraftment from double cord transplantation
Blood, March 1, 2004; 103(5): 1941 - 1948.
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JDRHome page
P.R. Kramer, S. Nares, S.F. Kramer, D. Grogan, and M. Kaiser
Mesenchymal Stem Cells Acquire Characteristics of Cells in the Periodontal Ligament in vitro
Journal of Dental Research, January 1, 2004; 83(1): 27 - 34.
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BloodHome page
F. Djouad, P. Plence, C. Bony, P. Tropel, F. Apparailly, J. Sany, D. Noel, and C. Jorgensen
Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals
Blood, November 15, 2003; 102(10): 3837 - 3844.
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JBJSHome page
T. L. Arinzeh, S. J. Peter, M. P. Archambault, C. van den Bos, S. Gordon, K. Kraus, A. Smith, and S. Kadiyala
Allogeneic Mesenchymal Stem Cells Regenerate Bone in a Critical-Sized Canine Segmental Defect
J. Bone Joint Surg. Am., October 1, 2003; 85(10): 1927 - 1935.
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J. Immunol.Home page
J. A. Potian, H. Aviv, N. M. Ponzio, J. S. Harrison, and P. Rameshwar
Veto-Like Activity of Mesenchymal Stem Cells: Functional Discrimination Between Cellular Responses to Alloantigens and Recall Antigens
J. Immunol., October 1, 2003; 171(7): 3426 - 3434.
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BloodHome page
M. Krampera, S. Glennie, J. Dyson, D. Scott, R. Laylor, E. Simpson, and F. Dazzi
Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide
Blood, May 1, 2003; 101(9): 3722 - 3729.
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BloodHome page
S. M. Devine, C. Cobbs, M. Jennings, A. Bartholomew, and R. Hoffman
Mesenchymal stem cells distribute to a wide range of tissues following systemic infusion into nonhuman primates
Blood, April 15, 2003; 101(8): 2999 - 3001.
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Circ. Res.Home page
D. Orlic, J. M. Hill, and A. E. Arai
Stem Cells for Myocardial Regeneration
Circ. Res., December 13, 2002; 91(12): 1092 - 1102.
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