References
Dominici, M., Mueller, I., Slaper-Cortenbach, I., Marini, F., Krause, D., Deans, R., Keating, A., Prockop, D. J., & Horwitz, E. (2006). Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy, 8(4), 315–317.
Jazedje, T., Perin, P., Czeresnia, C. E., Maluf, M., Halpern, S., Secco, M., Bueno, D. F., Vieira, N. M., Zucconi, E., & Zatz, M. (2009). Human fallopian tube: a new source of multipotent adult mesenchymal stem cells discarded in surgical procedures. Journal of Translational Medicine, 7, 46.
Garjett, C. E. (2007). Review article: stem cells in human reproduction. Reproductive Sciences, 14(5), 405–424.
Rodriguez, M. (2007). Effectors of demyelination and remyelination in the CNS: implications for multiple sclerosis. Brain Pathology, 17, 219–229.
Oksenberg, J. R., & Hauser, S. L. (2005). Genetics of multiple sclerosis. Neurologic Clinics, 1(23), 61–75.
Friese, M. A., Montalban, X., Willcox, N., Bell, J. I., Martin, R., & Fuger, L. (2006). The value of animal models for drug development in multiple sclerosis. Brain, 129(8), 1940–1952.
Tennakoon, D. K., Mehta, R. S., Ortega, S. B., Bhoj, V., Racke, M. K., & Karandikar, N. J. (2006). Therapeutic induction of regulatory cytotoxic CD8+ T cells in multiple sclerosis. Journal of Immunology, 176, 7119–7129.
Weiner, H. L., Mackin, G. A., Matsui, M., Orav, E. J., Khoury, S. J., Dawson, D. M., & Hafler, D. A. (1993). Double-blind pilot trial of oral tolerization with myelin antigens in multiple sclerosis. Science, 259(5099), 1321–1324.
Baxter, A. G. (2007). The origin and application of experimental autoimmune encephalomyelitis. Nature Medicine, 7(11), 904.
Dardalhon, V., Korn, T., Kuchroo, V. K., & Anderson, A. C. (2008). Role of Th1 and Th17 cells in organ-specific autoimmunity. Journal of Autoimmunity, 31(3), 252–256.
Jäger, A., Dardalhon, V., Sobel, R. A., Bettelli, E., & Kuchroo, V. K. (2009). Th1, Th17, and Th9 effector cells induce experimental autoimmune encephalomyelitis with different pathological phenotypes. Journal of Immunology, 183(11), 7169–7177.
Kroenke, M. A., & Segal, B. M. (2007). Th17 and Th1 responses directed against the immunizing epitope, as opposed to secondary epitopes, dominate the autoimmune repertoire during relapses of experimental autoimmune encephalomyelitis. Journal of Neuroscience Research, 85, 1685–1693.
Nakae, S., Matsuki, T., Nambu, A., Ishigame, H., Kakuta, S., Sudo, K., & Iwakura, Y. (2006). IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. Journal of Immunology, 177(1), 566–573.
Ivanov, I., Mackenzie, B. S., Zhou, B., Tadokoro, C. E., Leppeley, A., Lafaille, J. J., Cua, D. J., & Littman, D. R. (2006). The orphan nuclear receptor RORgt directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell, 126, 1121–1133.
Kreimborg, K., Etzensperger, R., Dumoutier, L., Haak, L., Rebollo, A., Buch, T., Heppner, F. L., Renauld, J. C., & Becher, B. (2007). IL-22 is expressed by Th17 cells in an IL-23-dependent fashion, but not required for the development of autoimmune encephalomyelitis. Journal of Immunology, 179, 8098–8104.
Zhou, L., Ivanov, I., Spolski, R., Sherendoz, K., Egawa, T., Levy, D. E., Leonard, W. J., & Littmann, D. R. (2007). IL-6 programs Th17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nature Immunology, 8(9), 1–8.
Yang, K., Vega, J., Hadzipasic, M., Schatzmann Peron, J. P., Zhu, B., Carrier, Y., Masli, S., Rizzo, L. V., & Weiner, H. L. (2009). Deficiency of thrombospondin-1 reduces Th17 differentiation and attenuates experimental autoimmune encephalomyelitis. Journal of Autoimmunity, 32(2), 94–103.
Matusevicius, D., Kivisäkk, P., He, B., Kostulas, N., Ozenci, V., Fredrikson, S., & Link, H. (1999). Interleukin-17 mRNA expression in blood and CSF mononuclear cells is augmented in multiple sclerosis. Multiple Sclerosis, 5, 101–104.
Das Sarma, J., Ciric, B., Marek, R., Sadhukhan, S., Caruso, M. L., Shafagh, J., Fitzgerald, D. C., Shindler, K. S., & Rostami, A. (2009). Functional interleukin-17 receptor A is expressed in central nervous system glia and upregulated in experimental autoimmune encephalomyelitis. Journal of Neuroinflammation, 28(6).
Kawanokuchi, J., Shimizu, K., Nitta, A., Yamada, K., Mizuno, T., Takeuchi, H., & Suzumura, A. (2008). Production and functions of IL-17 in microglia. Journal of Neuroimmunology, 194, 54–61.
Kang, Z., Altuntas, C. Z., Gulen, M. F., Liu, C., Giltiay, N., Qin, H., Liu, L., Qian, W., Ransohoff, R. M., Bergmann, C., Stohlman, S., Tuohy, V. K., & Li, X. (2010). Astrocyte-restricted ablation of Interleukin-17-induced act1-mediated signaling ameliorates autoimmune encephalomyelitis. Immunity, 32, 415–422.
Peron, J. P., Ligeiro-de-Oliveira, A. P., & Rizzo, L. V. (2009). It takes guts for tolerance: the phenomenon of oral tolerance and the regulation of autoimmune response. Autoimmunity Reviews, 9(1), 1–4.
Peron, J. P., Yang, K., Chen, M. L., Brandao, W. N., Basso, A. S., Commodaro, A. G., Weiner, H. L., & Rizzo, L. V. (2010). Oral tolerance reduces Th17 cells as well as the overall inflammation in the central nervous system of EAE mice. Journal of Neuroimmunology, 227(1–2), 10–17.
Kelly, C., Flatt, C., & McClenaghan, N. H. (2011). Stem cell-based approaches for the treatment of diabetes. Stem Cells International, 424986, 1–8.
Yang, J., Jiang, Z., Fitzgerald, D. C., Ma, C., Yu, S., Li, H., Zhao, Z., Li, Y., Ciric, B., Curtis, M., Rostami, A., & Zhang, G. X. (2009). Adult neural stem cells expressing IL-10 confer potent immunomodulation and remyelination in experimental autoimmune encephalitis. The Journal of Clinical Investigation, 119(12), 3678–3691.
Pluchino, S., Cusimano, M., Bacigaluppi, M., & Martino, G. (2010). Remodelling the injured CNS through the establishment of atypical ectopic perivascular neural stem cell niches. Archives Italiennes de Biologie, 148, 173–183.
Macdonald, G. I., Augello, A., & De Bari, C. (2011). Mesenchymal stem cells: re-establishing immunological tolerance in autoimmune rheumatic diseases. Arthritis and Rheumatism. doi:10.1002/art.30474.
Vieira, N. M., Zuconni, E., Bueno, C. R., Jr., Secco, M., Suzuki, M. F., Bartolini, P., Vainzof, M., & Zatz, M. (2010). Human multipotent mesenchymal stromal cells from distinct sources show different in vivo potential to differentiate into muscle cells when injected in dystrophic mice. Stem Cell Reviews, 6(4), 560–566.
Chen, Y., Inobe, J., & Weiner, H. L. (1995). Induction of oral tolerance to myelin basic protein in CD8 depleted mice: both CD4 and CD8 cells mediate suppression. Journal of Immunology, 155, 910–916.
Bassi, E. J., Aita, C. A., & Câmara, N. O. (2011). Immune regulatory properties of multipotent mesenchymal stromal cells: where do we stand? World Journal of Stem Cells, 3(1), 1–8.
Matysiak, M., Orlowski, W., Fortak-Michalska, M., Jurewicz, A., & Selmaj, K. (2011). Immunoregulatory function of bone marrow mesenchymal stem cells in EAE depends on their differentiation state and secretion of PGE2. Journal of Neuroimmunology, 233(1–2), 106–111.
Almolda, B., Gonzalez, B., & Castellano, B. (2011). Antigen presentation in EAE: role of microglia, macrophages and dendritic cells. Frontiers in Bioscience, 16, 1157–1171.
Park, M. J., Park, H. S., Cho, M. L., Oh, H. J., Cho, Y. G., Min, S. Y., Chung, B. H., Lee, J. W., Kim, H. Y., & Cho, S. G. (2011). Transforming growth factor β-transduced mesenchymal stem cells ameliorate experimental autoimmune arthritis through reciprocal regulation of Treg/Th17 cells and osteoclastogenesis. Arthritis and Rheumatism, 63(6), 1668–1680.
Pluchino, S., Quattrini, A., Brambilla, E., Gritti, A., Salani, G., Dina, G., Galli, R., Del Carro, U., Amadio, S., Bergami, A., Furlan, R., Comi, G., Vescovi, A. L., & Martino, G. (2003). Injection of adult neurospheres induces recovery in a chronic model of multiple sclerosis. Nature, 422(6933), 688–694.
Pluchino, S., Zanotti, L., Brambilla, E., Rovere-Querini, P., Capobianco, A., Alfaro-Cervello, C., Salani, G., Cossetti, C., Borsellino, G., Battistini, L., Ponzoni, M., Doglioni, C., Garcia-Verdugo, J. M., Comi, G., Manfredi, A. A., & Martino, G. (2009). Immune regulatory neural stem/precursor cells protect from central nervous system autoimmunity by restraining dendritic cell function. PLoS One, 4(6), e5959.
Takeda, A., Hamano, S., Yamanaka, A., Hanada, T., Ishibashi, T., Mak, T. W., Yoshimura, A., & Yoshida, H. (2003). Cutting edge: role of IL-27/WSX-1 signaling for induction of T-bet through activation of STAT1 during initial Th1 commitment. Journal of Immunology, 170(4886–90).
Fitzgerald, D. C., Ciric, B., Touil, T., Harle, H., Grammatikopolou, J., Das Sarma, J., Gran, B., Zhang, G., & Rostami, A. (2007). Suppressive Effect of IL-27 on encephalitogenic Th17 cells and the effector phase of experimental autoimmune encephalomyelitis. Journal of Immunology, 179, 3268–3275.
Awasthi, A., Carrier, Y., Peron, J. P. S., Bettelli, E., Kamanaka, M., Flavell, R. A., Kuchroo, V. K., Oukka, M., & Weiner, H. L. (2007). A dominant function for interleukin 27 in generating interleukin 10–producing anti-inflammatory T cells. Nature Immunology, 8(12), 1380–1389.
Croitoru-Lamoury, J., Lamoury, F. M., Caristo, M., Suzuki, K., Walker, D., Takikawa, O., Taylor, R., & Brew, B. J. (2011). Interferon-γ regulates the proliferation and differentiation of mesenchymal stem cells via activation of indoleamine 2,3 dioxygenase (IDO). PLoS One, 16(6), 14698.
Sioud, M. (2011). New insights into mesenchymal stromal cell-mediated T-cell suppression through galectins. Scandinavian Journal of Immunology, 73(2), 79–84.
Mellor, A. L., Chandler, P., Marshall, B., Jhaver, K., Hansen, A., Koni, P. A., Iwashima, M., & Munn, D. H. (2003). Induced Indoleamine −2,3- Dioxygenase expression in dendritic cell subsets suppresses T cell clonal expansion. Journal of Immunology, 171, 1652–1655.
Wang, Y., Lawson, M. A., Dantzer, R., & Kelley, K. W. (2010). LPS-induced indoleamine 2,3-dioxygenase is regulated in an interferon-gamma-independent manner by a JNK signaling pathway in primary murine microglia. Brain, Behavior, and Immunity, 24(2), 201–209.
Huang, L., Baban, B., Johnson, B. A., & Mellor, A. L. (2010). Dendritic cells, indoleamine 2,3 dioxygenase and acquired immune privilege. International Reviews of Immunology, 29(2), 133–155.
Munn, D., Sharma, M. D., Baban, B., Harding, H. P., Zhang, Y., Ron, D., & Mellor, A. L. (2005). GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity, 22(5), 633–642.
Fallarino, F., Gromann, U., Macgrath, B. C., Cavener, D. R., Vacca, C., Orabonna, C., Bianchi, R., Belladonna, M. L., Volpi, C., Santamaria, P., Fioretti, M. C., & Puccetti, P. (2006). The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor zeta-chain and induce a regulatory phenotype in naive T cells. Journal of Immunology, 176, 6752–6761.
Curti, A., Pandolofi, S., Valzasina, B., Aluigi, M., Isidori, A., Ferri, E., Salvestrini, V., Bonanno, G., Rutella, S., Durelli, I., Horestein, A. L., Fiore, F., Massaia, M., Colombo, M. P., Baccaranni, M., & Lemoli, R. M. (2007). Modulation of tryptophan catabolism by human leukemic cells results in the conversion of CD25- into CD25+ reg ulatory cells. Blood, 109(7), 2871–2877.
Acknowledgements
Peron JPS is a recipient of CAPES (PNPD 0188085) and Brandao WN is a recipient of FAPESP fellowship (2009/13109-5).
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Peron, J.P.S., Jazedje, T., Brandão, W.N. et al. Human Endometrial-Derived Mesenchymal Stem Cells Suppress Inflammation in the Central Nervous System of EAE Mice. Stem Cell Rev and Rep 8, 940–952 (2012). https://doi.org/10.1007/s12015-011-9338-3
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DOI: https://doi.org/10.1007/s12015-011-9338-3