Cytokine modulation of TLR expression and activation in mesenchymal stromal cells leads to a proinflammatory phenotype

Journal of Immunology

Volumn 182, Issue 12, 2009, Pages 7963-7973

  Romieu Mourez, Raphaëlle ^a   François, Moïra ^a   Boivin, Marie Noëlle ^a   Bouchentouf, Manaf ^a   Spaner, David E ^b   Galipeau, Jacques ^a  

^a MCGILL UNIVERSITY   (Canada)

^b Sunnybrook Health Sciences Centre   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ANTIGEN; CYTOKINE; DEATH RECEPTOR; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; RANTES; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; GUANOSINE 3',5' POLYPHOSPHATE SYNTHETASES; GUANOSINE 3',5'-POLYPHOSPHATE SYNTHETASES; INTERFERON REGULATORY FACTOR 1; LIGAND; LIGASE; TRANSCRIPTION FACTOR REL;

ADULT; AGED; ANIMAL CELL; ANTIGEN PRESENTING CELL; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOREGULATION; INFLAMMATORY CELL; INNATE IMMUNITY; MACROPHAGE; MALE; MESENCHYME CELL; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; STROMA CELL; UPREGULATION; ANIMAL; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INFLAMMATION; METABOLISM;

ADULT; ANIMALS; CELLS, CULTURED; CYTOKINES; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INTERFERON REGULATORY FACTOR-1; LIGANDS; LIGASES; MALE; MICE; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-REL; STROMAL CELLS; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 4;

EID: 67649209791     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0803864     Document Type: Article

References (39)

1. Uccelli, A., L. Moretta, and V. Pistoia. 2008. Mesenchymal stem cells in health and disease. Nat. Rev. Immunol. 8: 726-736.
2. Stagg, J., and J. Galipeau. 2007. Immune plasticity of bone marrow-derived mesenchymal stromal cells. Handb. Exp. Pharmacol. 45-66.
3. Nasef, A., N. Ashammakhi, and L. Fouillard. 2008. Immunomodulatory effect of mesenchymal stromal cells: possible mechanisms. Regen. Med. 3: 531-546.
4. Le Blanc, K., C. Tammik, K. Rosendahl, E. Zetterberg, and O. Ringden. 2003. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp. Hematol. 31: 890-896.
5. Stagg, J., S. Pommey, N. Eliopoulos, and J. Galipeau. 2006. Interferon-γ-stimulated marrow stromal cells: a new type of nonhematopoietic antigen-presenting cell. Blood 107: 2570-2577.
6. Chan, J. L., K. C. Tang, A. P. Patel, L. M. Bonilla, N. Pierobon, N. M. Ponzio, and P. Rameshwar. 2006. Antigen-presenting property of mesenchymal stem cells occurs during a narrow window at low levels of interferon-γ. Blood 107: 4817-4824.
7. Romieu-Mourez, R., M. Francois, M. N. Boivin, J. Stagg, and J. Galipeau. 2007. Regulation of MHC class II expression and antigen processing in murine and human mesenchymal stromal cells by IFN-γ, TGF-β, and cell density. J. Immunol. 179: 1549-1558.
8. Hawiger, D., K. Inaba, Y. Dorsett, M. Guo, K. Mahnke, M. Rivera, J. V. Ravetch, R. M. Steinman, and M. C. Nussenzweig. 2001. Dendritic cells induce peripheral T cell unresponsiveness under steady state conditions in vivo. J. Exp. Med. 194: 769-779.
9. Trinchieri, G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3: 133-146.
10. D'Andrea, A., M. Rengaraju, N. M. Valiante, J. Chehimi, M. Kubin, M. Aste, S. H. Chan, M. Kobayashi, D. Young, E. Nickbarg, et al. 1992. Production of natural killer cell stimulatory factor (interleukin 12) by peripheral blood mononuclear cells. J. Exp. Med. 176: 1387-1398.
11. Ma, X., J. M. Chow, G. Gri, G. Carra, F. Gerosa, S. F. Wolf, R. Dzialo, and G. Trinchieri. 1996. The interleukin 12 p40 gene promoter is primed by interferon γ in monocytic cells. J. Exp. Med. 183: 147-157.
12. Gautier, G., M. Humbert, F. Deauvieau, M. Scuiller, J. Hiscott, E. E. Bates, G. Trinchieri, C. Caux, and P. Garrone. 2005. A type I interferon autocrine-paracrine loop is involved in Toll-like receptor-induced interleukin-12p70 secretion by dendritic cells. J. Exp. Med. 201: 1435-1446.
13. Edwards, A. D., S. P. Manickasingham, R. Sporri, S. S. Diebold, O. Schulz, A. Sher, T. Kaisho, S. Akira, and C. Reis e Sousa. 2002. Microbial recognition via Toll-like receptor-dependent and -independent pathways determines the cytokine response of murine dendritic cell subsets to CD40 triggering. J. Immunol. 169: 3652-3660.
14. Napolitani, G., A. Rinaldi, F. Bertoni, F. Sallusto, and A. Lanzavecchia. 2005. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat. Immunol. 6: 769-776.
15. Trinchieri, G., and A. Sher. 2007. Cooperation of Toll-like receptor signals in innate immune defence. Nat. Rev. Immunol. 7: 179-190.
16. Siren, J., J. Pirhonen, I. Julkunen, and S. Matikainen. 2005. IFN-α regulates TLR-dependent gene expression of IFN-α, IFN-β, IL-28, and IL-29. J. Immunol. 174: 1932-1937. (Pubitemid 40223933)
17. Tissari, J., J. Siren, S. Meri, I. Julkunen, and S. Matikainen. 2005. IFN-α enhances TLR3-mediated antiviral cytokine expression in human endothelial and epithelial cells by up-regulating TLR3 expression. J. Immunol. 174: 4289-4294. (Pubitemid 40396010)
18. Pevsner-Fischer, M., V. Morad, M. Cohen-Sfady, L. Rousso-Noori, A. Zanin-Zhorov, S. Cohen, I. R. Cohen, and D. Zipori. 2007. Toll-like receptors and their ligands control mesenchymal stem cell functions. Blood 109: 1422-1432.
19. 2-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat. Med. 15: 42-49.
20. Liotta, F., R. Angeli, L. Cosmi, L. Fili, C. Manuelli, F. Frosali, B. Mazzinghi, L. Maggi, A. Pasini, V. Lisi, et al. 2008. 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 26: 279-289.
21. Eliopoulos, N., J. Stagg, L. Lejeune, S. Pommey, and J. Galipeau. 2005. Allogeneic marrow stromal cells are immune rejected by MHC class I- and class II-mismatched recipient mice. Blood 106: 4057-4065.
22. Romieu-Mourez, R., M. Solis, A. Nardin, D. Goubau, V. Baron-Bodo, R. Lin, B. Massie, M. Salcedo, and J. Hiscott. 2006. Distinct roles for IFN regulatory factor (IRF)-3 and IRF-7 in the activation of antitumor properties of human macrophages. Cancer Res. 66: 10576-10585.
23. Matsumoto, M., K. Funami, M. Tanabe, H. Oshiumi, M. Shingai, Y. Seto, A. Yamamoto, and T. Seya. 2003. Subcellular localization of Toll-like receptor 3 in human dendritic cells. J. Immunol. 171: 3154-3162. (Pubitemid 37093540)
24. Yoneyama, M., M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5: 730-737.
25. Kato, H., S. Sato, M. Yoneyama, M. Yamamoto, S. Uematsu, K. Matsui, T. Tsujimura, K. Takeda, T. Fujita, O. Takeuchi, and S. Akira. 2005. Cell type-specific involvement of RIG-I in antiviral response. Immunity 23: 19-28.
26. Venkataraman, T., M. Valdes, R. Elsby, S. Kakuta, G. Caceres, S. Saijo, Y. Iwakura, and G. N. Barber. 2007. Loss of DExD/H box RNA helicase LGP2 manifests disparate antiviral responses. J. Immunol. 178: 6444-6455. (Pubitemid 46717428)
27. Sanjabi, S., A. Hoffmann, H. C. Liou, D. Baltimore, and S. T. Smale. 2000. Selective requirement for c-Rel during IL-12 P40 gene induction in macrophages. Proc. Natl. Acad. Sci. USA 97: 12705-12710.
28. + dendritic cells by specifically inducing p35 gene transcription. J. Exp. Med. 194: 1021-1032.
29. Wang, J., X. Wang, S. Hussain, Y. Zheng, S. Sanjabi, F. Ouaaz, and A. A. Beg. 2007. Distinct roles of different NF-κB subunits in regulating inflammatory and T cell stimulatory gene expression in dendritic cells. J. Immunol. 178: 6777-6788. (Pubitemid 46847402)
30. Liu, J., S. Cao, L. M. Herman, and X. Ma. 2003. Differential regulation of interleukin (IL)-12 p35 and p40 gene expression and interferon (IFN)-γ-primed IL-12 production by IFN regulatory factor 1. J. Exp. Med. 198: 1265-1276.
31. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124: 783-801.
32. Iwasaki, A., and R. Medzhitov. 2004. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5: 987-995.
33. Kawai, T., and S. Akira. 2006. TLR signaling. Cell Death Differ. 13: 816-825.
34. Tsai, E. Y., J. V. Falvo, A. V. Tsytsykova, A. K. Barczak, A. M. Reimold, L. H. Glimcher, M. J. Fenton, D. C. Gordon, I. F. Dunn, and A. E. Goldfeld. 2000. A lipopolysaccharide-specific enhancer complex involving Ets, Elk-1, Sp1, and CREB binding protein and p300 is recruited to the tumor necrosis factor α promoter in vivo. Mol. Cell. Biol. 20: 6084-6094.
35. Zhu, C., K. Rao, H. Xiong, K. Gagnidze, F. Li, C. Horvath, and S. Plevy. 2003. Activation of the murine interleukin-12 p40 promoter by functional interactions between NFAT and ICSBP. J. Biol. Chem. 278: 39372-39382.
36. Zhao, J., H. J. Kong, H. Li, B. Huang, M. Yang, C. Zhu, M. Bogunovic, F. Zheng, L. Mayer, K. Ozato, et al. 2006. IRF-8/interferon (IFN) consensus sequence-binding protein is involved in Toll-like receptor (TLR) signaling and contributes to the cross-talk between TLR and IFN-γ signaling pathways. J. Biol. Chem. 281: 10073-10080.
37. Means, T. K., F. Hayashi, K. D. Smith, A. Aderem, and A. D. Luster. 2003. The Toll-like receptor 5 stimulus bacterial flagellin induces maturation and chemokine production in human dendritic cells. J. Immunol. 170: 5165-5175.
38. Bromley, S. K., T. R. Mempel, and A. D. Luster. 2008. Orchestrating the orchestrators: chemokines in control of T cell traffic. Nat. Immunol. 9: 970-980.
39. Ringden, O., M. Uzunel, B. Sundberg, L. Lonnies, S. Nava, J. Gustafsson, L. Henningsohn, and K. Le Blanc. 2007. Tissue repair using allogeneic mesenchymal stem cells for hemorrhagic cystitis, pneumomediastinum and perforated colon. Leukemia 21: 2271-2276.