Limitation of immune tolerance-inducing thymic epithelial cell development by Spi-B-mediated negative feedback regulation

Journal of Experimental Medicine

Volumn 211, Issue 12, 2014, Pages 2425-2438

  Akiyama, Nobuko ^a   Shinzawa, Miho ^a   Miyauchi, Maki ^a   Yanai, Hiromi ^a   Tateishi, Ryosuke ^a   Shimo, Yusuke ^a   Ohshima, Daisuke ^a   Matsuo, Koichi ^b   Sasaki, Izumi ^c   Hoshino, Katsuaki ^c,d,e   Wu, Guoying ^f   Yagi, Shintaro ^f   Inoue, Jun ichiro ^a   Kaisho, Tsuneyasu ^c,d   Akiyama, Taishin ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b KEIO UNIVERSITY   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d RIKEN Center for Integrative Medical Sciences   (Japan)

^e KAGAWA UNIVERSITY   (Japan)

^f UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; OSTEOPROTEGERIN; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SPI B; UNCLASSIFIED DRUG; B7 ANTIGEN; NF-KAPPA B KINASE; OSTEOCLAST DIFFERENTIATION FACTOR; PROTEIN SERINE THREONINE KINASE; SPI-B PROTEIN, MOUSE; TRANSCRIPTION FACTOR ETS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; EMBRYO; EPITHELIUM CELL; IMMUNOLOGICAL TOLERANCE; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; THYMOCYTE; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; CELL CULTURE; EXPERIMENTAL NEOPLASM; FEEDBACK SYSTEM; FEMALE; GENE EXPRESSION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; MALE; METABOLISM; NEWBORN; NUDE MOUSE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THYMUS; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; ANTIGENS, CD80; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; EPITHELIAL CELLS; FEEDBACK, PHYSIOLOGICAL; FEMALE; GENE EXPRESSION; IMMUNE TOLERANCE; MALE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, NUDE; NEOPLASMS, EXPERIMENTAL; OSTEOPROTEGERIN; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-ETS; RANK LIGAND; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR-KAPPA B; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; THYMUS GLAND;

EID: 84911890115     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20141207     Document Type: Article

References (46)

1. Abramson, J., M. Giraud, C. Benoist, and D. Mathis. 2010. Aire's partners in the molecular control of immunological tolerance. Cell. 140:123-135. http://dx.doi.org/10.1016/j.cell.2009.12.030
2. Aichinger, M., M. Hinterberger, and L. Klein. 2012. Probing gene function in thymic epithelial cells. Eur. J. Cell Biol. 91:24-30. http://dx.doi.org/10.1016/j.ejcb.2011.01.005
3. Akiyama, T., S. Maeda, S. Yamane, K. Ogino, M. Kasai, F. Kajiura, M. Matsumoto, and J. Inoue. 2005. Dependence of self-tolerance on TRAF6-directed development of thymic stroma. Science. 308:248-251. http://dx.doi.org/10.1126/science.1105677
4. Akiyama, T., Y. Shimo, H. Yanai, J. Qin, D. Ohshima, Y. Maruyama, Y. Asaumi, J. Kitazawa, H. Takayanagi, J.M. Penninger, et al. 2008. The tumor necrosis factor family receptors RANK and CD40 cooperatively establish the thymic medullary microenvironment and selftolerance. Immunity. 29:423-437. http://dx.doi.org/10.1016/j.immuni.2008.06.015
5. Akiyama, T., M. Shinzawa, and N. Akiyama. 2012a. RANKL-RANK interaction in immune regulatory systems. World J. Orthop. 3:142-150. http://dx.doi.org/10.5312/wjo.v3.i9.142
6. Akiyama, T., M. Shinzawa, and N. Akiyama. 2012b. TNF receptor family signaling in the development and functions of medullary thymic epithelial cells. Front. Immunol. 3:278. http://dx.doi.org/10.3389/fimmu.2012.00278
7. Anderson, G., and Y. Takahama. 2012. Thymic epithelial cells: working class heroes for T cell development and repertoire selection. Trends Immunol. 33:256-263. http://dx.doi.org/10.1016/j.it.2012.03.005
8. Anderson, G., E.J. Jenkinson, and H.R. Rodewald. 2009. A roadmap for thymic epithelial cell development. Eur. J. Immunol. 39:1694-1699. http://dx.doi.org/10.1002/eji.200939379
9. Bartholdy, B., C. Du Roure, A. Bordon, D. Emslie, L.M. Corcoran, and P. Matthias. 2006. The Ets factor Spi-B is a direct critical target of the coactivator OBF-1. Proc. Natl. Acad. Sci. USA. 103:11665-11670. http://dx.doi.org/10.1073/pnas.0509430103
10. Bouneaud, C., P. Kourilsky, and P. Bousso. 2000. Impact of negative selection on the T cell repertoire reactive to a self-peptide: a large fraction of T cell clones escapes clonal deletion. Immunity. 13:829-840. http://dx.doi.org/10.1016/S1074-7613(00)00080-7
11. Burkly, L., C. Hession, L. Ogata, C. Reilly, L.A. Marconi, D. Olson, R. Tizard, R. Cate, and D. Lo. 1995. Expression of relB is required for the development of thymic medulla and dendritic cells. Nature. 373:531-536. http://dx.doi.org/10.1038/373531a0
12. Chen, H.M., D.A. Gonzalez, H.S. Radomska, M.T. Voso, Z. Sun, P. Zhang, D.E. Zhang, and D.G. Tenen. 1998. Two promoters direct expression of the murine Spi-B gene, an Ets family transcription factor. Gene. 207:209-218. http://dx.doi.org/10.1016/S0378-1119(97)00629-X
13. Cowan, J.E., S.M. Parnell, K. Nakamura, J.H. Caamano, P.J. Lane, E.J. Jenkinson, W.E. Jenkinson, and G. Anderson. 2013. The thymic medulla is required for Foxp3+ regulatory but not conventional CD4+ thymocyte development. J. Exp. Med. 210:675-681. http://dx.doi.org/10.1084/jem.20122070
14. Dontje, W., R. Schotte, T. Cupedo, M. Nagasawa, F. Scheeren, R. Gimeno, H. Spits, and B. Blom. 2006. Delta-like1-induced Notch1 signaling regulates the human plasmacytoid dendritic cell versus T-cell lineage decision through control of GATA-3 and Spi-B. Blood. 107:2446-2452. http://dx.doi.org/10.1182/blood-2005-05-2090
15. Garrett-Sinha, L.A., G.H. Su, S. Rao, S. Kabak, Z. Hao, M.R. Clark, and M.C. Simon. 1999. PU.1 and Spi-B are required for normal B cell receptor-mediated signal transduction. Immunity. 10:399-408. http://dx.doi.org/10.1016/S1074-7613(00)80040-0
16. Gray, D., J. Abramson, C. Benoist, and D. Mathis. 2007. Proliferative arrest and rapid turnover of thymic epithelial cells expressing Aire. J. Exp. Med. 204:2521-2528. http://dx.doi.org/10.1084/jem.20070795
17. Guerau-de-Arellano, M., M. Martinic, C. Benoist, and D. Mathis. 2009. Neonatal tolerance revisited: a perinatal window for Aire control of autoimmunity. J. Exp. Med. 206:1245-1252. http://dx.doi.org/10.1084/jem.20090300
18. Hauri-Hohl, M., S. Zuklys, G.A. Holländer, and S.F. Ziegler. 2014. A regulatory role for TGF-ß signaling in the establishment and function of the thymic medulla. Nat. Immunol. 15:554-561. http://dx.doi.org/10.1038/ni.2869
19. Heinz, S., C. Benner, N. Spann, E. Bertolino, Y.C. Lin, P. Laslo, J.X. Cheng, C. Murre, H. Singh, and C.K. Glass. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell. 38:576-589. http://dx.doi.org/10.1016/j.molcel.2010.05.004
20. Hikosaka, Y., T. Nitta, I. Ohigashi, K. Yano, N. Ishimaru, Y. Hayashi, M. Matsumoto, K. Matsuo, J.M. Penninger, H. Takayanagi, et al. 2008. The cytokine RANKL produced by positively selected thymocytes fosters medullary thymic epithelial cells that express autoimmune regulator. Immunity. 29:438-450. http://dx.doi.org/10.1016/j.immuni.2008.06.018
21. Hinterberger, M., M. Aichinger, O. Prazeres da Costa, D. Voehringer, R. Hoffmann, and L. Klein. 2010. Autonomous role of medullary thymic epithelial cells in central CD4+ T cell tolerance. Nat. Immunol. 11:512-519. http://dx.doi.org/10.1038/ni.1874
22. Jones, P.A., and S.B. Baylin. 2007. The epigenomics of cancer. Cell. 128:683-692. http://dx.doi.org/10.1016/j.cell.2007.01.029
23. Kajiura, F., S. Sun, T. Nomura, K. Izumi, T. Ueno, Y. Bando, N. Kuroda, H. Han, Y. Li, A. Matsushima, et al. 2004. NF-κB-inducing kinase establishes self-tolerance in a thymic stroma-dependent manner. J. Immunol. 172:2067-2075. http://dx.doi.org/10.4049/jimmunol.172.4.2067
24. Kanaya, T., K. Hase, D. Takahashi, S. Fukuda, K. Hoshino, I. Sasaki, H. Hemmi, K.A. Knoop, N. Kumar, M. Sato, et al. 2012. The Ets transcription factor Spi-B is essential for the differentiation of intestinal microfold cells. Nat. Immunol. 13:729-736. http://dx.doi.org/10.1038/ni.2352
25. Khan, I.S., M.L. Mouchess, M.L. Zhu, B. Conley, K.J. Fasano, Y. Hou, L. Fong, M.A. Su, and M.S. Anderson. 2014. Enhancement of an antitumor immune response by transient blockade of central T cell tolerance. J. Exp. Med. 211:761-768. http://dx.doi.org/10.1084/jem.20131889
26. Klein, L., M. Hinterberger, G. Wirnsberger, and B. Kyewski. 2009. Antigen presentation in the thymus for positive selection and central tolerance induction. Nat. Rev. Immunol. 9:833-844. http://dx.doi.org/10.1038/nri2669
27. Kyewski, B., and L. Klein. 2006. A central role for central tolerance. Annu. Rev. Immunol. 24:571-606. http://dx.doi.org/10.1146/annurev.immunol.23.021704.115601
28. Lei, Y., A.M. Ripen, N. Ishimaru, I. Ohigashi, T. Nagasawa, L.T. Jeker, M.R. Bösl, G.A. Holländer, Y. Hayashi, R.W. Malefyt, et al. 2011. Airedependent production of XCL1 mediates medullary accumulation of thymic dendritic cells and contributes to regulatory T cell development. J. Exp. Med. 208:383-394. http://dx.doi.org/10.1084/jem.20102327
29. Leibbrandt, A., and J.M. Penninger. 2008. RANK/RANKL: regulators of immune responses and bone physiology. Ann. N. Y. Acad. Sci. 1143:123-150. http://dx.doi.org/10.1196/annals.1443.016
30. Lio, C.W., and C.S. Hsieh. 2008. A two-step process for thymic regulatory T cell development. Immunity. 28:100-111. http://dx.doi.org/10.1016/j.immuni.2007.11.021
31. Liu, X., P. Invernizzi, Y. Lu, R. Kosoy, Y. Lu, I. Bianchi, M. Podda, C. Xu, G. Xie, F. Macciardi, et al. 2010. Genome-wide meta-analyses identify three loci associated with primary biliary cirrhosis. Nat. Genet. 42:658-660. http://dx.doi.org/10.1038/ng.627
32. Malchow, S., D.S. Leventhal, S. Nishi, B.I. Fischer, L. Shen, G.P. Paner, A.S. Amit, C. Kang, J.E. Geddes, J.P. Allison, et al. 2013. Aire-dependent thymic development of tumor-associated regulatory T cells. Science. 339:1219-1224. http://dx.doi.org/10.1126/science.1233913
33. Mells, G.F., J.A. Floyd, K.I. Morley, H.J. Cordell, C.S. Franklin, S.Y. Shin, M.A. Heneghan, J.M. Neuberger, P.T. Donaldson, D.B. Day, et al. Wellcome Trust Case Control Consortium 3. 2011. Genome-wide association study identifies 12 new susceptibility loci for primary biliary cirrhosis. Nat. Genet. 43:329-332. (published erratum appears in Nat. Genet. 2011. 43:1164) http://dx.doi.org/10.1038/ng.789
34. Mizuno, A., N. Amizuka, K. Irie, A. Murakami, N. Fujise, T. Kanno, Y. Sato, N. Nakagawa, H. Yasuda, S. Mochizuki, et al. 1998. Severe osteoporosis in mice lacking osteoclastogenesis inhibitory factor/osteoprotegerin. Biochem. Biophys. Res. Commun. 247:610-615. http://dx.doi.org/10.1006/bbrc.1998.8697
35. Ohshima, D., J. Qin, H. Konno, A. Hirosawa, T. Shiraishi, H. Yanai, Y. Shimo, M. Shinzawa, N. Akiyama, R. Yamashita, et al. 2011. RANK signaling induces interferon-stimulated genes in the fetal thymic stroma. Biochem. Biophys. Res. Commun. 408:530-536. http://dx.doi.org/10.1016/j.bbrc.2011.04.049
36. Ray, D., R. Bosselut, J. Ghysdael, M.G. Mattei, A. Tavitian, and F. Moreau-Gachelin. 1992. Characterization of Spi-B, a transcription factor related to the putative oncoprotein Spi-1/PU.1. Mol. Cell. Biol. 12:4297-4304.
37. - inducer cells regulate development of Aire-expressing epithelial cells in the thymic medulla. J. Exp. Med. 204:1267-1272. http://dx.doi.org/10.1084/jem.20062497
38. Sasaki, I., K. Hoshino, T. Sugiyama, C. Yamazaki, T. Yano, A. Iizuka, H. Hemmi, T. Tanaka, M. Saito, M. Sugiyama, et al. 2012. Spi-B is critical for plasmacytoid dendritic cell function and development. Blood. 120:4733-4743. http://dx.doi.org/10.1182/blood-2012-06-436527
39. Schotte, R., M. Nagasawa, K. Weijer, H. Spits, and B. Blom. 2004. The ETS transcription factor Spi-B is required for human plasmacytoid dendritic cell development. J. Exp. Med. 200:1503-1509. http://dx.doi.org/10.1084/jem.20041231
40. Shinkura, R., K. Kitada, F. Matsuda, K. Tashiro, K. Ikuta, M. Suzuki, K. Kogishi, T. Serikawa, and T. Honjo. 1999. Alymphoplasia is caused by a point mutation in the mouse gene encoding Nf-κb-inducing kinase. Nat. Genet. 22:74-77. http://dx.doi.org/10.1038/8780
41. Sun, S.C. 2012. The noncanonical NF-κB pathway. Immunol. Rev. 246:125-140. http://dx.doi.org/10.1111/j.1600-065X.2011.01088.x
42. Thu, Y.M., and A. Richmond. 2010. NF-κB inducing kinase: a key regulator in the immune system and in cancer. Cytokine Growth Factor Rev. 21:213-226. http://dx.doi.org/10.1016/j.cytogfr.2010.06.002
43. Träger, U., S. Sierro, G. Djordjevic, B. Bouzo, S. Khandwala, A. Meloni, M. Mortensen, and A.K. Simon. 2012. The immune response to melanoma is limited by thymic selection of self-antigens. PLoS ONE. 7:e35005. http://dx.doi.org/10.1371/journal.pone.0035005
44. Weih, F., D. Carrasco, S.K. Durham, D.S. Barton, C.A. Rizzo, R.P. Ryseck, S.A. Lira, and R. Bravo. 1995. Multiorgan inflammation and hematopoietic abnormalities in mice with a targeted disruption of RelB, a member of the NF-κB/Rel family. Cell. 80:331-340. http://dx.doi.org/10.1016/0092-8674(95)90416-6
45. Yagi, S., K. Hirabayashi, S. Sato, W. Li, Y. Takahashi, T. Hirakawa, G. Wu, N. Hattori, N. Hattori, J. Ohgane, et al. 2008. DNA methylation profile of tissue-dependent and differentially methylated regions (T-DMRs) in mouse promoter regions demonstrating tissue-specific gene expression. Genome Res. 18:1969-1978. http://dx.doi.org/10.1101/gr.074070.107
46. Zhu, M.L., A. Nagavalli, and M.A. Su. 2013. Aire deficiency promotes TRP-1-specific immune rejection of melanoma. Cancer Res. 73:2104-2116. http://dx.doi.org/10.1158/0008-5472.CAN-12-3781