IFN-γ and TNF-α differentially regulate immunomodulation by murine mesenchymal stem cells

Immunology Letters

Volumn 110, Issue 2, 2007, Pages 91-100

  English, Karen ^a   Barry, Frank P ^b   Field Corbett, Ciara P ^a   Mahon, Bernard P ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

IDO; IFN ; Immunosuppression; Mesenchymal stem cell; Prostaglandin; TNF

Indexed keywords

CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; CYTOKINE; GAMMA INTERFERON; INDOMETACIN; INTERLEUKIN 10; PROSTAGLANDIN E2; SCATTER FACTOR; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; MESENCHYMAL STEM CELL; MIXED LYMPHOCYTE REACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; ANTIGENS, CD80; BONE MARROW CELLS; CELLS, CULTURED; CYCLOOXYGENASE 2; CYCLOOXYGENASE INHIBITORS; CYTOKINES; DINOPROSTONE; FEMALE; IMMUNOLOGIC FACTORS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INDOMETHACIN; INTERFERON TYPE II; LYMPHOCYTE CULTURE TEST, MIXED; MEMBRANE GLYCOPROTEINS; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; PEPTIDES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 34249662219     PISSN: 01652478     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imlet.2007.04.001     Document Type: Article

References (53)

1. Barry F.P. Biology and clinical applications of mesenchymal stem cells. Birth Defects Res C Embryo Today 69 (2003) 250-256
2. Barry F.P., and Murphy J.M. Mesenchymal stem cells: clinical applications and biological characterization. Int J Biochem Cell Biol 36 (2004) 568-584
3. Murphy J.M., Fink D.J., Hunziker E.B., and Barry F.P. Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum 48 (2003) 3464-3474
4. da Silva Meirelles L., Chagastelles P.C., and Nardi N.B. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 119 (2006) 2204-2213
5. Horwitz E.M., Gordon P.L., Koo W.K., Marx J.C., Neel M.D., McNall R.Y., et al. Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: Implications for cell therapy of bone. Proc Natl Acad Sci USA 99 (2002) 8932-8937
6. Koc O.N., Day J., Nieder M., Gerson S.L., Lazarus H.M., and Krivit W. Allogeneic mesenchymal stem cell infusion for treatment of metachromatic leukodystrophy (MLD) and Hurler syndrome (MPS-IH). Bone Marrow Transplant 30 (2002) 215-222
7. Fouillard L., Bensidhoum M., Bories D., Bonte H., Lopez M., Moseley A.M., et al. Engraftment of allogeneic mesenchymal stem cells in the bone marrow of a patient with severe idiopathic aplastic anemia improves stroma. Leukemia 17 (2003) 474-476
8. Zappia E., Casazza S., Pedemonte E., Benvenuto F., Bonanni I., Gerdoni E., et al. Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood 106 (2005) 1755-1761
9. Ortiz L.A., Gambelli F., McBride C., Gaupp D., Baddoo M., Kaminski N., et al. Mesenchymal stem cell engraftment in lung is enhanced in response to bleomycin exposure and ameliorates its fibrotic effects. Proc Natl Acad Sci USA 100 (2003) 8407-8411
10. Khakoo A.Y., Pati S., Anderson S.A., Reid W., Elshal M.F., Rovira I.I., et al. Human mesenchymal stem cells exert potent antitumorigenic effects in a model of Kaposi's sarcoma. J Exp Med 203 (2006) 1235-1247
11. 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 (2002) 42-48
12. Reyes M., and Verfaillie C.M. Characterization of multipotent adult progenitor cells, a subpopulation of mesenchymal stem cells. Ann N Y Acad Sci 938 (2001) 231-233 (discussion 233-235)
13. Aggarwal S., and Pittenger M.F. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105 (2005) 1815-1822
14. Djouad F., Plence P., Bony C., Tropel P., Apparailly F., Sany J., et al. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 102 (2003) 3837-3844
15. Deng W., Han Q., Liao L., Li C., Ge W., Zhao Z., et al. Allogeneic bone marrow-derived flk-1+ Sca-1-mesenchymal stem cells leads to stable mixed chimerism and donor-specific tolerance. Exp Hematol 32 (2004) 861-867
16. Potian J.A., Aviv H., Ponzio N.M., Harrison J.S., and Rameshwar P. Veto-like activity of mesenchymal stem cells: functional discrimination between cellular responses to alloantigens and recall antigens. J Immunol 171 (2003) 3426-3434
17. Zhang W., Ge W., Li C., You S., Liao L., Han Q., et al. Effects of mesenchymal stem cells on differentiation, maturation, and function of human monocyte-derived dendritic cells. Stem Cells Dev 13 (2004) 263-271
18. 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 101 (2003) 3722-3729
19. Augello A., Tasso R., Negrini S.M., 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 35 (2005) 1482-1490
20. Di Nicola 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 (2002) 3838-3843
21. 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 (2006) 2080-2087
22. Groh M.E., Maitra B., Szekely E., and Koc O.N. Human mesenchymal stem cells require monocyte-mediated activation to suppress alloreactive T cells. Exp Hematol 33 (2005) 928-934
23. 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 (2005) 516-525
24. 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 (2005) 4120-4126
25. Rasmusson I., Ringden O., Sundberg B., and Le Blanc K. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation 76 (2003) 1208-1213
26. 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 (2005) 2214-2219
27. Angoulvant D., Clerc A., Benchalal S., Galambrun C., Farre A., Bertrand Y., et al. Human mesenchymal stem cells suppress induction of cytotoxic response to alloantigens. Biorheology 41 (2004) 469-476
28. Barry F.P., Murphy J.M., English K., and Mahon B.P. Immunogenicity of adult mesenchymal stem cells: lessons from the fetal allograft. Stem Cells Dev 14 (2005) 252-265
29. Meisel R., Zibert A., Laryea M., 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 (2004) 4619-4621
30. Mellor A.L., and Munn D.H. Immunology at the maternal-fetal interface: lessons for T cell tolerance and suppression. Annu Rev Immunol 18 (2000) 367-391
31. Peister A., Mellad J.A., Larson B.L., Hall B.M., Gibson L.F., and Prockop D.J. Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 103 (2004) 1662-1668
32. Jarnicki A.G., Lysaght J., Todryk S., and Mills K.H. Suppression of antitumor immunity by IL-10 and TGF-beta-producing T cells infiltrating the growing tumor: influence of tumor environment on the induction of CD4+ and CD8+ regulatory T cells. J Immunol 177 (2006) 896-904
33. Okunishi K., Dohi M., Nakagome K., Tanaka R., Mizuno S., Matsumoto K., et al. A novel role of hepatocyte growth factor as an immune regulator through suppressing dendritic cell function. J Immunol 175 (2005) 4745-4753
34. Kuroiwa T., Kakishita E., Hamano T., Kataoka Y., Seto Y., Iwata N., et al. Hepatocyte growth factor ameliorates acute graft-versus-host disease and promotes hematopoietic function. J Clin Invest 107 (2001) 1365-1373
35. Harris S.G., Padilla J., Koumas L., Ray D., and Phipps R.P. Prostaglandins as modulators of immunity. Trends Immunol 23 (2002) 144-150
36. Loftin C.D., Trivedi D.B., and Langenbach R. Cyclooxygenase-1-selective inhibition prolongs gestation in mice without adverse effects on the ductus arteriosus. J Clin Invest 110 (2002) 549-557
37. O'Shea J.J., Ma A., Lipsky P., and Cytokines autoimmunity. Nat Rev Immunol 2 (2002) 37-45
38. Latchman Y.E., Liang S.C., Wu Y., Chernova T., Sobel R.A., Klemm M., et al. PD-L1-deficient mice show that PD-L1 on T cells, antigen-presenting cells, and host tissues negatively regulates T cells. Proc Natl Acad Sci USA 101 (2004) 10691-10696
39. Sandner S.E., Clarkson M.R., Salama A.D., Sanchez-Fueyo A., Domenig C., Habicht A., et al. Role of the programmed death-1 pathway in regulation of alloimmune responses in vivo. J Immunol 174 (2005) 3408-3415
40. 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 (1998) 1191-1193
41. Tse W.T., Pendleton J.D., Beyer W.M., Egalka M.C., and Guinan E.C. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 75 (2003) 389-397
42. Rasmusson I., Ringden O., Sundberg B., and Le Blanc K. Mesenchymal stem cells inhibit lymphocyte proliferation by mitogens and alloantigens by different mechanisms. Exp Cell Res 305 (2005) 33-41
43. Keir M.E., Liang S.C., Guleria I., Latchman Y.E., Qipo A., Albacker L.A., et al. Tissue expression of PD-L1 mediates peripheral T cell tolerance. J Exp Med 203 (2006) 883-895
44. Petrovas C., Casazza J.P., Brenchley J.M., Price D.A., Gostick E., Adams W.C., et al. PD- 1 is a regulator of virus-specific CD8+ T cell survival in HIV infection. J Exp Med 203 (2006) 2281-2292
45. Rodig N., Ryan T., Allen J.A., Pang H., Grabie N., Chernova T., et al. Endothelial expression of PD-L1 and PD-L2 down-regulates CD8+ T cell activation and cytolysis. Eur J Immunol 33 (2003) 3117-3126
46. Ozkaynak E., Wang L., Goodearl A., McDonald K., Qin S., O'Keefe T., et al. Programmed death-1 targeting can promote allograft survival. J Immunol 169 (2002) 6546-6553
47. Carter L., Fouser L.A., Jussif J., Fitz L., Deng B., Wood C.R., et al. PD-1:PD-L inhibitory pathway affects both CD4(+) and CD8(+) T cells and is overcome by IL-2. Eur J Immunol 32 (2002) 634-643
48. Glennie S., Soeiro I., Dyson P.J., Lam E.W., and Dazzi F. Bone marrow mesenchymal stem cells induce division arrest anergy of activated T cells. Blood 105 (2005) 2821-2827
49. Terness P., Bauer T.M., Rose L., Dufter C., Watzlik A., Simon H., et al. Inhibition of allogeneic T cell proliferation by indoleamine 2,3-dioxygenase-expressing dendritic cells: mediation of suppression by tryptophan metabolites. J Exp Med 196 (2002) 447-457
50. 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 (2000) 3596-3599
51. 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 24 (2006) 386-398
52. Ryan J.M., Barry F.P., Murphy J.M., and Mahon B.P. Mesenchymal stem cells avoid allogeneic rejection. J Inflamm (London) 2 (2005) 8
53. Plumas J., Chaperot L., Richard M.J., Molens J.P., Bensa J.C., and Favrot M.C. Mesenchymal stem cells induce apoptosis of activated T cells. Leukemia 19 (2005) 1597-1604