Mesenchymal stem cells can induce long-term acceptance of solid organ allografts in synergy with low-dose mycophenolate

Transplant Immunology

Volumn 20, Issue 1-2, 2008, Pages 55-60

  Popp, F C ^a   Eggenhofer, E ^a   Renner, P ^a   Slowik, P ^a   Lang, S A ^a   Kaspar, H ^a   Geissler, E K ^a   Piso, P ^a   Schlitt, H J ^a   Dahlke, M H ^a,b  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b Department of Microbiology and Infectious Diseases   (Australia)

Author keywords

IDO; Mesenchymal stemcells; Solid organ transplantation

Indexed keywords

INDOLEAMINE 2,3 DIOXYGENASE; MYCOPHENOLIC ACID; TRYPTOPHAN;

ALLOGRAFT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; DENDRITIC CELL; HEART TRANSPLANTATION; MESENCHYMAL STEM CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ANIMALS; DENDRITIC CELLS; GRAFT REJECTION; GRAFT SURVIVAL; HEART TRANSPLANTATION; IMMUNOSUPPRESSION; IMMUNOSUPPRESSIVE AGENTS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MYCOPHENOLIC ACID; RATS; T-LYMPHOCYTES, REGULATORY; TRYPTOPHAN;

EID: 56049100237     PISSN: 09663274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.trim.2008.08.004     Document Type: Article

References (43)

1. Pittenger M.F., Mackay A.M., Beck S.C., Jaiswal R.K., Douglas R., Mosca J.D., et al. Multilineage potential of adult human mesenchymal stem cells. Science 284 5411 (1999) 143-147
2. Aggarwal S., and Pittenger M.F. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105 4 (2005) 1815-1822
3. Di N.M., Carlo-Stella C., Magni M., Milanesi M., Longoni P.D., Matteucci P., et al. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99 10 (2002) 3838-3843
4. Inoue S., Popp F.C., Koehl G.E., Piso P., Schlitt H.J., Geissler E.K., et al. Immunomodulatory effects of mesenchymal stem cells in a rat organ transplant model. Transplantation 81 11 (2006) 1589-1595
5. Maccario R., Podesta M., Moretta A., Cometa A., Comoli P., Montagna D., et al. Interaction of human mesenchymal stem cells with cells involved in alloantigen-specific immune response favors the differentiation of CD4+ T-cell subsets expressing a regulatory/suppressive phenotype. Haematologica 90 4 (2005) 516-525
6. Wood K.J., and Sakaguchi S. Regulatory T cells in transplantation tolerance. Nat Rev Immunol 3 3 (2003) 199-210
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 105 5 (2005) 2214-2219
8. Jiang X.X., Zhang Y., Liu B., Zhang S.X., Wu Y., Yu X.D., et al. Human mesenchymal stem cells inhibit differentiation and function of monocyte-derived dendritic cells. Blood 105 10 (2005) 4120-4126
9. Nauta A.J., Kruisselbrink A.B., Lurvink E., Willemze R., and Fibbe W.E. Mesenchymal stem cells inhibit generation and function of both CD34+-derived and monocyte-derived dendritic cells. J Immunol 177 4 (2006) 2080-2087
10. Meisel R., Zibert A., Gobel U., Daubener W., and Dilloo D. Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood 103 12 (2004) 4619-4621
11. Hwu P., Du M.X., Lapointe R., Do M., Taylor M.W., and Young H.A. Indoleamine 2,3-dioxygenase production by human dendritic cells results in the inhibition of T cell proliferation. J Immunol 164 7 (2000) 3596-3599
12. Munn D.H., Shafizadeh E., Attwood J.T., Bondarev I., Pashine A., and Mellor A.L. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J Exp Med 189 9 (1999) 1363-1372
13. Munn D.H., Sharma M.D., Lee J.R., Jhaver K.G., Johnson T.S., Keskin D.B., et al. Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science 297 5588 (2002) 1867-1870
14. Munn D.H., Zhou M., Attwood J.T., Bondarev I., Conway S.J., Marshall B., et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281 5380 (1998) 1191-1193
15. Bartholomew A., Sturgeon C., Siatskas M., Ferrer K., McIntosh K., Patil S., et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol 30 1 (2002) 42-48
16. Ringden O., Uzunel M., Rasmusson I., Remberger M., Sundberg B., Lonnies H., et al. Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation 81 10 (2006) 1390-1397
17. Allison A.C., and Eugui E.M. Mechanisms of action of mycophenolate mofetil in preventing acute and chronic allograft rejection. Transplantation 80 2 Suppl (2005) S181-190
18. Ono K., and Lindsey E.S. Improved technique of heart transplantation in rats. J Thorac Cardiovasc Surg 57 2 (1969) 225-229
19. Popp F.C., Slowik P., Eggenhofer E., Renner P., Lang S.A., Stoeltzing O., et al. No contribution of multipotent mesenchymal stromal cells to liver regeneration in a rat model of prolonged hepatic injury. Stem Cells (2006)
20. Cavinato R.A., Casiraghi F., Azzollini N., Cassis P., Cugini D., Mister M., et al. Pretransplant donor peripheral blood mononuclear cells infusion induces transplantation tolerance by generating regulatory T cells. Transplantation 79 9 (2005) 1034-1039
21. Oluwole S.F., Fawwaz R.A., Reemtsma K., and Hardy M.A. Induction of donor-specific unresponsiveness to rat cardiac allograft by donor leukocytes and cyclosporine. Transplantation 45 6 (1988) 1131-1135
22. Yang L., Du Temple B., Khan Q., and Zhang L. Mechanisms of long-term donor-specific allograft survival induced by pretransplant infusion of lymphocytes. Blood 91 1 (1998) 324-330
23. Alegre E., Lopez A.S., and Gonzalez A. Tryptophan metabolites interfere with the Ehrlich reaction used for the measurement of kynurenine. Anal Biochem 339 1 (2005) 188-189
24. Guillonneau C., Hill M., Hubert F.X., Chiffoleau E., Herve C., Li X.L., et al. CD40Ig treatment results in allograft acceptance mediated by CD8CD45RC T cells, IFN-gamma, and indoleamine 2,3-dioxygenase. J Clin Invest 117 4 (2007) 1096-1106
25. Djouad F., Charbonnier L.M., Bouffi C., Louis-Plence P., Bony C., Apparailly F., et al. Mesenchymal stem cells inhibit the differentiation of dendritic cells through an Il-6-dependent mechanism. Stem Cells (2007)
26. English K., Barry F.P., and Mahon B.P. Murine mesenchymal stem cells suppress dendritic cell migration, maturation and antigen presentation. Immunol Lett 115 1 (2008) 50-58
27. Zhou H.P., Yi D.H., Yu S.Q., Sun G.C., Cui Q., Zhu H.L., et al. Administration of donor-derived mesenchymal stem cells can prolong the survival of rat cardiac allograft. Transplant Proc 38 9 (2006) 3046-3051
28. Brennan D.C., Mohanakumar T., and Flye M.W. Donor-specific transfusion and donor bone marrow infusion in renal transplantation tolerance: a review of efficacy and mechanisms. Am J Kidney Dis 26 5 (1995) 701-715
29. Le Blanc K., Frassoni F., Ball L., Locatelli F., Roelofs H., Lewis I., et al. Mesenchymal stem cells for treatment of steroid-resistant, severe, acute graft-versus-host disease: a phase II study. Lancet 371 9624 (2008) 1579-1586
30. Kunter U., Rong S., Boor P., Eitner F., Muller-Newen G., Djuric Z., et al. Mesenchymal stem cells prevent progressive experimental renal failure but maldifferentiate into glomerular adipocytes. J Am Soc Nephrol 18 6 (2007) 1754-1764
31. Karnoub A.E., Dash A.B., Vo A.P., Sullivan A., Brooks M.W., Bell G.W., et al. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis. Nature 449 7162 (2007) 557-563
32. Devine S.M., Cobbs C., Jennings M., Bartholomew A., and Hoffman R. Mesenchymal stem cells distribute to a wide range of tissues following systemic infusion into nonhuman primates. Blood 101 8 (2003) 2999-3001
33. Devine S.M., Bartholomew A.M., Mahmud N., Nelson M., Patil S., Hardy W., et al. Mesenchymal stem cells are capable of homing to the bone marrow of non-human primates following systemic infusion. ExpHematol 29 2 (2001) 244-255
34. Eliopoulos N., Stagg J., Lejeune L., Pommey S., and Galipeau J. Allogeneic marrow stromal cells are immune rejected by MHC class I- and class II-mismatched recipient mice. Blood 106 13 (2005) 4057-4065
35. Sudres M., Norol F., Trenado A., Gregoire S., Charlotte F., Levacher B., et al. Bone marrow mesenchymal stem cells suppress lymphocyte proliferation in vitro but fail to prevent graft-versus-host disease in mice. JImmunol 176 12 (2006) 7761-7767
36. Frumento G., Rotondo R., Tonetti M., Damonte G., Benatti U., and Ferrara G.B. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J Exp Med 196 4 (2002) 459-468
37. Bauer T.M., Jiga L.P., Chuang J.J., Randazzo M., Opelz G., and Terness P. Studying the immunosuppressive role of indoleamine 2,3-dioxygenase: tryptophan metabolites suppress rat allogeneic T-cell responses in vitro and in vivo. TransplInt 18 1 (2005) 95-100
38. Chabannes D., Hill M., Merieau E., Rossignol J., Brion R., Soulillou J.P., et al. A role for heme oxygenase-1 in the immunosuppressive effect of adult rat and human mesenchymal stem cells. Blood 110 10 (2007) 3691-3694
39. Mehling A., Grabbe S., Voskort M., Schwarz T., Luger T.A., and Beissert S. Mycophenolate mofetil impairs the maturation and function of murine dendritic cells. J Immunol 165 5 (2000) 2374-2381
40. Stagg J., Pommey S., Eliopoulos N., and Galipeau J. Interferon-gamma-stimulated marrow stromal cells: a new type of nonhematopoietic antigen-presenting cell. Blood 107 6 (2006) 2570-2577
41. Chan J.L., Tang K.C., Patel A.P., Bonilla L.M., Pierobon N., Ponzio N.M., et al. Antigen-presenting property of mesenchymal stem cells occurs during a narrow window at low levels of interferon-gamma. Blood 107 12 (2006) 4817-4824
42. Morelli A.E., and Thomson A.W. Tolerogenic dendritic cells and the quest for transplant tolerance. Nat Rev Immunol 7 8 (2007) 610-621
43. Puccetti P., and Grohmann U. IDO and regulatory T cells: a role for reverse signalling and non-canonical NF-kappaB activation. Nat Rev Immunol 7 10 (2007) 817-823