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Blood, 15 February 2005, Vol. 105, No. 4, pp. 1815-1822.
Prepublished online as a Blood First Edition Paper on October 19, 2004; DOI 10.1182/blood-2004-04-1559.
Previous Article | Table of Contents | Next Article 
TRANSPLANTATION
Human mesenchymal stem cells modulate allogeneic immune cell responses
Sudeepta Aggarwal, and
Mark F. Pittenger
From Osiris Therapeutics, Baltimore, MD.
Mesenchymal stem cells (MSCs) are multipotent cells found in several adult tissues. Transplanted allogeneic MSCs can be detected in recipients at extended time points, indicating a lack of immune recognition and clearance. As well, a role for bone marrow-derived MSCs in reducing the incidence and severity of graft-versus-host disease (GVHD) during allogeneic transplantation has recently been reported; however, the mechanisms remain to be investigated. We examined the immunomodulatory functions of human MSCs (hMSCs) by coculturing them with purified subpopulations of immune cells and report here that hMSCs altered the cytokine secretion profile of dendritic cells (DCs), naive and effector T cells (T helper 1 [TH1] and TH2), and natural killer (NK) cells to induce a more anti-inflammatory or tolerant phenotype. Specifically, the hMSCs caused mature DCs type 1 (DC1) to decrease tumor necrosis factor (TNF- ) secretion and mature DC2 to increase interleukin-10 (IL-10) secretion; hMSCs caused TH1 cells to decrease interferon (IFN- ) and caused the TH2 cells to increase secretion of IL-4; hMSCs caused an increase in the proportion of regulatory T cells (TRegs) present; and hMSCs decreased secretion of IFN- from the NK cells. Mechanistically, the hMSCs produced elevated prostaglandin E2 (PGE2) in co-cultures, and inhibitors of PGE2 production mitigated hMSC-mediated immune modulation. These data offer insight into the interactions between allogeneic MSCs and immune cells and provide mechanisms likely involved with the in vivo MSC-mediated induction of tolerance that could be therapeutic for reduction of GVHD, rejection, and modulation of inflammation. (Blood. 2005;105:1815-1822)

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[Abstract]
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Q. Lian, E. Lye, K. Suan Yeo, E. Khia Way Tan, M. Salto-Tellez, T. M. Liu, N. Palanisamy, R. M. El Oakley, E. H. Lee, B. Lim, et al.
Derivation of Clinically Compliant MSCs from CD105+, CD24- Differentiated Human ESCs
Stem Cells,
February 1, 2007;
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425 - 436.
[Abstract]
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X. Chen, A. McClurg, G.-Q. Zhou, M. McCaigue, M. A. Armstrong, and G. Li
Chondrogenic Differentiation Alters the Immunosuppressive Property of Bone Marrow-Derived Mesenchymal Stem Cells, and the Effect Is Partially due to the Upregulated Expression of B7 Molecules
Stem Cells,
February 1, 2007;
25(2):
364 - 370.
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A. K.S. Chong, A. D. Ang, J. C.H. Goh, J. H.P. Hui, A. Y.T. Lim, E. H. Lee, and B. H. Lim
Bone Marrow-Derived Mesenchymal Stem Cells Influence Early Tendon-Healing in a Rabbit Achilles Tendon Model
J. Bone Joint Surg. Am.,
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S. Jomura, M. Uy, K. Mitchell, R. Dallasen, C. J. Bode, and Y. Xu
Potential Treatment of Cerebral Global Ischemia with Oct-4+ Umbilical Cord Matrix Cells
Stem Cells,
January 1, 2007;
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K. Sato, K. Ozaki, I. Oh, A. Meguro, K. Hatanaka, T. Nagai, K. Muroi, and K. Ozawa
Nitric oxide plays a critical role in suppression of T-cell proliferation by mesenchymal stem cells
Blood,
January 1, 2007;
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228 - 234.
[Abstract]
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[PDF]
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B. Dekel, L. Zangi, E. Shezen, S. Reich-Zeliger, S. Eventov-Friedman, H. Katchman, J. Jacob-Hirsch, N. Amariglio, G. Rechavi, R. Margalit, et al.
Isolation and Characterization of Nontubular Sca-1+Lin- Multipotent Stem/Progenitor Cells from Adult Mouse Kidney
J. Am. Soc. Nephrol.,
December 1, 2006;
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C.-J. Chang, M.-L. Yen, Y.-C. Chen, C.-C. Chien, H.-I. Huang, C.-H. Bai, and B. L. Yen
Placenta-Derived Multipotent Cells Exhibit Immunosuppressive Properties That Are Enhanced in the Presence of Interferon-{gamma}
Stem Cells,
November 1, 2006;
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2466 - 2477.
[Abstract]
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Y. Miura, Z. Gao, M. Miura, B.-M. Seo, W. Sonoyama, W. Chen, S. Gronthos, L. Zhang, and S. Shi
Mesenchymal Stem Cell-Organized Bone Marrow Elements: An Alternative Hematopoietic Progenitor Resource
Stem Cells,
November 1, 2006;
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2428 - 2436.
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R. Yanez, M. L. Lamana, J. Garcia-Castro, I. Colmenero, M. Ramirez, and J. A. Bueren
Adipose Tissue-Derived Mesenchymal Stem Cells Have In Vivo Immunosuppressive Properties Applicable for the Control of the Graft-Versus-Host Disease
Stem Cells,
November 1, 2006;
24(11):
2582 - 2591.
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M. R. Rosen
Are Stem Cells Drugs?: The Regulation of Stem Cell Research and Development
Circulation,
October 31, 2006;
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M. Tomita, T. Mori, K. Maruyama, T. Zahir, M. Ward, A. Umezawa, and M. J. Young
A Comparison of Neural Differentiation and Retinal Transplantation with Bone Marrow-Derived Cells and Retinal Progenitor Cells
Stem Cells,
October 1, 2006;
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2270 - 2278.
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J. M. van Laar and A. Tyndall
Adult stem cells in the treatment of autoimmune diseases
Rheumatology,
October 1, 2006;
45(10):
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[Abstract]
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A. J. Nauta, G. Westerhuis, A. B. Kruisselbrink, E. G. A. Lurvink, R. Willemze, and W. E. Fibbe
Donor-derived mesenchymal stem cells are immunogenic in an allogeneic host and stimulate donor graft rejection in a nonmyeloablative setting
Blood,
September 15, 2006;
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S. Arnhold, P. Heiduschka, H. Klein, Y. Absenger, S. Basnaoglu, F. Kreppel, S. Henke-Fahle, S. Kochanek, K.-U. Bartz-Schmidt, K. Addicks, et al.
Adenovirally Transduced Bone Marrow Stromal Cells Differentiate into Pigment Epithelial Cells and Induce Rescue Effects in RCS Rats.
Invest. Ophthalmol. Vis. Sci.,
September 1, 2006;
47(9):
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[Abstract]
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A. J. Nauta, A. B. Kruisselbrink, E. Lurvink, R. Willemze, and W. E. Fibbe
Mesenchymal Stem Cells Inhibit Generation and Function of Both CD34+-Derived and Monocyte-Derived Dendritic Cells
J. Immunol.,
August 15, 2006;
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2080 - 2087.
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T. P. Martens, M. Argenziano, and M. C. Oz
New Technology for Surgical Coronary Revascularization
Circulation,
August 8, 2006;
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606 - 614.
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T. J. Rabelink and C. van Kooten
Stem Cell Therapy for Glomerular Disease
J. Am. Soc. Nephrol.,
August 1, 2006;
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K. McIntosh, S. Zvonic, S. Garrett, J. B. Mitchell, Z. E. Floyd, L. Hammill, A. Kloster, Y. Di Halvorsen, J. P. Ting, R. W. Storms, et al.
The Immunogenicity of Human Adipose-Derived Cells: Temporal Changes In Vitro
Stem Cells,
May 1, 2006;
24(5):
1246 - 1253.
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Z. Guo, H. Li, X. Li, X. Yu, H. Wang, P. Tang, and N. Mao
In Vitro Characteristics and In Vivo Immunosuppressive Activity of Compact Bone-Derived Murine Mesenchymal Progenitor Cells
Stem Cells,
April 1, 2006;
24(4):
992 - 1000.
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J. Stagg, S. Pommey, N. Eliopoulos, and J. Galipeau
Interferon-{gamma}-stimulated marrow stromal cells: a new type of nonhematopoietic antigen-presenting cell
Blood,
March 15, 2006;
107(6):
2570 - 2577.
[Abstract]
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[PDF]
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H. Liu, D. M. Kemeny, B. C. Heng, H. W. Ouyang, A. J. Melendez, and T. Cao
The immunogenicity and immunomodulatory function of osteogenic cells differentiated from mesenchymal stem cells.
J. Immunol.,
March 1, 2006;
176(5):
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G. M. Spaggiari, A. Capobianco, S. Becchetti, M. C. Mingari, and L. Moretta
Mesenchymal stem cell-natural killer cell interactions: evidence that activated NK cells are capable of killing MSCs, whereas MSCs can inhibit IL-2-induced NK-cell proliferation
Blood,
February 15, 2006;
107(4):
1484 - 1490.
[Abstract]
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M. Aluigi, M. Fogli, A. Curti, A. Isidori, E. Gruppioni, C. Chiodoni, M. P. Colombo, P. Versura, A. D'Errico-Grigioni, E. Ferri, et al.
Nucleofection Is an Efficient Nonviral Transfection Technique for Human Bone Marrow-Derived Mesenchymal Stem Cells
Stem Cells,
February 1, 2006;
24(2):
454 - 461.
[Abstract]
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J. J. Minguell and A. Erices
Mesenchymal Stem Cells and the Treatment of Cardiac Disease
Experimental Biology and Medicine,
January 1, 2006;
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39 - 49.
[Abstract]
[Full Text]
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P. A. Sotiropoulou, S. A. Perez, A. D. Gritzapis, C. N. Baxevanis, and M. Papamichail
Interactions Between Human Mesenchymal Stem Cells and Natural Killer Cells
Stem Cells,
January 1, 2006;
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[Abstract]
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D. G. Phinney, K. Hill, C. Michelson, M. DuTreil, C. Hughes, S. Humphries, R. Wilkinson, M. Baddoo, and E. Bayly
Biological Activities Encoded by the Murine Mesenchymal Stem Cell Transcriptome Provide a Basis for Their Developmental Potential and Broad Therapeutic Efficacy
Stem Cells,
January 1, 2006;
24(1):
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A. Corcione, F. Benvenuto, E. Ferretti, D. Giunti, V. Cappiello, F. Cazzanti, M. Risso, F. Gualandi, G. L. Mancardi, V. Pistoia, et al.
Human mesenchymal stem cells modulate B-cell functions
Blood,
January 1, 2006;
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A. Poggi, C. Prevosto, A.-M. Massaro, S. Negrini, S. Urbani, I. Pierri, R. Saccardi, M. Gobbi, and M. R. Zocchi
Interaction between Human NK Cells and Bone Marrow Stromal Cells Induces NK Cell Triggering: Role of NKp30 and NKG2D Receptors
J. Immunol.,
November 15, 2005;
175(10):
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C. E. Murry, L. J. Field, and P. Menasche
Cell-Based Cardiac Repair: Reflections at the 10-Year Point
Circulation,
November 15, 2005;
112(20):
3174 - 3183.
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A. Shahdadfar, K. Fronsdal, T. Haug, F. P. Reinholt, and J. E. Brinchmann
In Vitro Expansion of Human Mesenchymal Stem Cells: Choice of Serum Is a Determinant of Cell Proliferation, Differentiation, Gene Expression, and Transcriptome Stability
Stem Cells,
September 1, 2005;
23(9):
1357 - 1366.
[Abstract]
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K. C. Wollert and H. Drexler
Mesenchymal Stem Cells for Myocardial Infarction: Promises and Pitfalls
Circulation,
July 12, 2005;
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F. Togel, Z. Hu, K. Weiss, J. Isaac, C. Lange, and C. Westenfelder
Administered mesenchymal stem cells protect against ischemic acute renal failure through differentiation-independent mechanisms
Am J Physiol Renal Physiol,
July 1, 2005;
289(1):
F31 - F42.
[Abstract]
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F. Togel, Z. Hu, K. Weiss, J. Isaac, C. Lange, C. Westenfelder, T. Stasko, M.D. Brown, J.A. Carucci, S. Euvrard, et al.
Amelioration of Acute Renal Failure by Stem Cell Therapy--Paracrine Secretion Versus Transdifferentiation into Resident Cells: Administered Mesenchymal Stem Cells Protect against Ischemic Acute Renal Failure through Differentiation-Independent Mechanisms. Am J Physiol Renal Physiol E-pub February 15, 2005
J. Am. Soc. Nephrol.,
May 1, 2005;
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