Identification of embryonic precursor cells that differentiate into thymic epithelial cells expressing autoimmune regulator

Journal of Experimental Medicine

Volumn 213, Issue 8, 2016, Pages 1441-1458

  Akiyama, Nobuko ^a   Takizawa, Nobukazu ^a   Miyauchi, Maki ^a   Yanai, Hiromi ^a   Tateishi, Ryosuke ^a   Shinzawa, Miho ^a   Yoshinaga, Riko ^a   Kurihara, Masaaki ^b   Demizu, Yosuke ^b   Yasuda, Hisataka ^c   Yagi, Shintaro ^a   Wu, Guoying ^a   Matsumoto, Mitsuru ^d   Sakamoto, Reiko ^a   Yoshida, Nobuaki ^a   Penninger, Josef M ^e   Kobayashi, Yasuhiro ^f   Inoue, Jun Ichiro ^a   Akiyama, Taishin ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

^c Oriental Yeast Co Ltd   (Japan)

^d UNIVERSITY OF TOKUSHIMA   (Japan)

^e Institute of Molecular Biotechnology of the Austrian Academy of Sciences   (Japan)

^f MATSUMOTO DENTAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOIMMUNE REGULATOR PROTEIN; CD24 ANTIGEN; LYMPHOTOXIN BETA RECEPTOR; OSTEOCLAST DIFFERENTIATION FACTOR; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; PLANT LECTIN; TRANSCRIPTION FACTOR; ULEX EUROPAEUS LECTINS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOIMMUNITY; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; EPITHELIUM CELL; FEMALE; FLOW CYTOMETRY; IMMUNOLOGICAL TOLERANCE; MOUSE; NONHUMAN; ORGAN CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; THYMIC EPITHELIAL CELL; UPREGULATION; ANIMAL; BAGG ALBINO MOUSE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; MOUSE EMBRYONIC STEM CELL; THYMUS;

ANIMALS; CELL DIFFERENTIATION; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MOUSE EMBRYONIC STEM CELLS; PLANT LECTINS; THYMUS GLAND; TRANSCRIPTION FACTORS;

EID: 84982965083     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20151780     Document Type: Article

References (53)

1. Akiyama, N., M. Shinzawa, M. Miyauchi, H. Yanai, R. Tateishi, Y. Shimo, D. Ohshima, K. Matsuo, I. Sasaki, K. Hoshino, et al. 2014. Limitation of immune tolerance-inducing thymic epithelial cell development by SpiB-mediated negative feedback regulation. J. Exp. Med. 211:2425-2438. http://dx.doi.org/10.1084/jem.20141207
2. 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
3. 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 self-tolerance. Immunity. 29:423-437. http://dx.doi.org/10.1016/j.immuni.2008.06.015
4. Akiyama, T., M. Shinzawa, and N. Akiyama. 2012. 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
5. Akiyama, T., M. Shinzawa, J. Qin, and N. Akiyama. 2013. Regulations of gene expression in medullary thymic epithelial cells required for preventing the onset of autoimmune diseases. Front. Immunol. 4:249. http://dx.doi.org/10.3389/fimmu.2013.00249
6. + progenitors. Eur. J. Immunol. 43:589-594. http://dx.doi.org/10.1002/eji.201243209
7. + medullary epithelial progenitors. Eur. J. Immunol. 46:857-862. http://dx.doi.org/10.1002/eji.201546253
8. Bennett, A.R., A. Farley, N.F. Blair, J. Gordon, L. Sharp, and C.C. Blackburn. 2002. Identification and characterization of thymic epithelial progenitor cells. Immunity. 16:803-814. http://dx.doi.org/10.1016/S1074-7613(02)00321-7
9. Bleul, C.C., T. Corbeaux, A. Reuter, P. Fisch, J.S. Mönting, and T. Boehm. 2006. Formation of a functional thymus initiated by a postnatal epithelial progenitor cell. Nature. 441:992-996. http://dx.doi.org/10.1038/nature04850
10. Boehm, T., S. Scheu, K. Pfeffer, and C.C. Bleul. 2003. Thymic medullary epithelial cell differentiation, thymocyte emigration, and the control of autoimmunity require lympho-epithelial cross talk via LTβR. J. Exp. Med. 198:757-769. http://dx.doi.org/10.1084/jem.20030794
11. Chin, R.K., J.C. Lo, O. Kim, S.E. Blink, P.A. Christiansen, P. Peterson, Y. Wang, C. Ware, and Y.X. Fu. 2003. Lymphotoxin pathway directs thymic Aire expression. Nat. Immunol. 4:1121-1127. http://dx.doi.org/10.1038/ni982
12. Danzl, N.M., S. Jeong, Y. Choi, and K. Alexandropoulos. 2014. Identification of novel thymic epithelial cell subsets whose differentiation is regulated by RAN KL and Traf6. PLoS One. 9:e86129. http://dx.doi.org/10.1371/journal.pone.0086129
13. Furuya, Y., K. Mori, T. Ninomiya, Y. Tomimori, S. Tanaka, N. Takahashi, N. Udagawa, K. Uchida, and H. Yasuda. 2011. Increased bone mass in mice after single injection of anti-receptor activator of nuclear factor-κB ligand-neutralizing antibody: evidence for bone anabolic effect of parathyroid hormone in mice with few osteoclasts. J. Biol. Chem. 286:37023-37031. http://dx.doi.org/10.1074/jbc.M111.246280
14. Gäbler, J., J. Arnold, and B. Kyewski. 2007. Promiscuous gene expression and the developmental dynamics of medullary thymic epithelial cells. Eur. J. Immunol. 37:3363-3372. http://dx.doi.org/10.1002/eji.200737131
15. + thymic epithelial cells. Nat. Immunol. 3:635-642. http://dx.doi.org/10.1038/ni812
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. 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 RAN KL 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
19. Hsieh, C.S., H.M. Lee, and C.W. Lio. 2012. Selection of regulatory T cells in the thymus. Nat. Rev. Immunol. 12:157-167. http://dx.doi.org/10.1038/nri3155
20. + thymocytes control mature medullary thymic epithelial cell cellularity. Immunity. 29:451-463. http://dx.doi.org/10.1016/j.immuni.2008.08.007
21. Kajiura, F., S. Sun, T. Nomura, K. Izumi, T. Ueno, Y. Bando, N. Kuroda, H. Han, Y. Li, A. Matsushima, et al. 2004. NF-κ B-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
22. 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 anti-tumor immune response by transient blockade of central T cell tolerance. J. Exp. Med. 211:761-768. http://dx.doi.org/10.1084/jem.20131889
23. 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
24. 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
25. Lkhagvasuren, E., M. Sakata, I. Ohigashi, and Y. Takahama. 2013. Lymphotoxin β receptor regulates the development of CCL21-expressing subset of postnatal medullary thymic epithelial cells. J. Immunol. 190:5110-5117. http://dx.doi.org/10.4049/jimmunol.1203203
26. Maeda, K., Y. Kobayashi, N. Udagawa, S. Uehara, A. Ishihara, T. Mizoguchi, Y. Kikuchi, I. Takada, S. Kato, S. Kani, et al. 2012. Wnt5a-Ror2 signaling between osteoblast-lineage cells and osteoclast precursors enhances osteoclastogenesis. Nat. Med. 18:405-412. http://dx.doi.org/10.1038/nm.2653
27. Mathis, D., and C. Benoist. 2009. Aire. Annu. Rev. Immunol. 27:287-312. http://dx.doi.org/10.1146/annurev.immunol.25.022106.141532
28. Mayer, C.E., S. Žuklys, S. Zhanybekova, I. Ohigashi, H.Y. Teh, S.N. Sansom, N. Shikama-Dorn, K. Hafen, I.C. Macaulay, M.E. Deadman, et al. 2016. Dynamic spatio-temporal contribution of single β5t+ cortical epithelial precursors to the thymus medulla. Eur. J. Immunol. 46:846-856. http://dx.doi.org/10.1002/eji.201545995
29. Mouri, Y., M. Yano, M. Shinzawa, Y. Shimo, F. Hirota, Y. Nishikawa, T. Nii, H. Kiyonari, T. Abe, H. Uehara, et al. 2011. Lymphotoxin signal promotes thymic organogenesis by eliciting RANK expression in the embryonic thymic stroma. J. Immunol. 186:5047-5057. http://dx.doi.org/10.4049/jimmunol.1003533
30. Ohigashi, I., S. Zuklys, M. Sakata, C.E. Mayer, S. Zhanybekova, S. Murata, K. Tanaka, G.A. Holländer, and Y. Takahama. 2013. Aire-expressing thymic medullary epithelial cells originate from β5t-expressing progenitor cells. Proc. Natl. Acad. Sci. USA. 110:9885-9890. http://dx.doi.org/10.1073/pnas.1301799110
31. Ohigashi, I., S. Zuklys, M. Sakata, C.E. Mayer, Y. Hamazaki, N. Minato, G.A. Hollander, and Y. Takahama. 2015. Adult thymic medullary epithelium is maintained and regenerated by lineage-restricted cells rather than bipotent progenitors. Cell Reports. 13:1432-1443. http://dx.doi.org/10.1016/j.celrep.2015.10.012
32. Onder, L., V. Nindl, E. Scandella, Q. Chai, H.W. Cheng, S. Caviezel-Firner, M. Novkovic, D. Bomze, R. Maier, F. Mair, et al. 2015. Alternative NF-κB signaling regulates mTEC differentiation from podoplanin-expressing presursors in the cortico-medullary junction. Eur. J. Immunol. 45:2218-2231. http://dx.doi.org/10.1002/eji.201545677
33. Ribeiro, A.R., P.M. Rodrigues, C. Meireles, J.P. Di Santo, and N.L. Alves. 2013. Thymocyte selection regulates the homeostasis of IL-7-expressing thymic cortical epithelial cells in vivo. J. Immunol. 191:1200-1209. http://dx.doi.org/10.4049/jimmunol.1203042
34. Rietze, R.L., H. Valcanis, G.F. Brooker, T. Thomas, A.K. Voss, and P.F. Bartlett. 2001. Purification of a pluripotent neural stem cell from the adult mouse brain. Nature. 412:736-739. http://dx.doi.org/10.1038/35089085
35. Roberts, N.A., A.J. White, W.E. Jenkinson, G. Turchinovich, K. Nakamura, D.R. Withers, F.M. McConnell, G.E. Desanti, C. Benezech, S.M. Parnell, et al. 2012. Rank signaling links the development of invariant γδ T cell progenitors and Aire(+) medullary epithelium. Immunity. 36:427-437. http://dx.doi.org/10.1016/j.immuni.2012.01.016
36. Rossi, S.W., W.E. Jenkinson, G. Anderson, and E.J. Jenkinson. 2006. Clonal analysis reveals a common progenitor for thymic cortical and medullary epithelium. Nature. 441:988-991. http://dx.doi.org/10.1038/nature04813
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. Seach, N., T. Ueno, A.L. Fletcher, T. Lowen, M. Mattesich, C.R. Engwerda, H.S. Scott, C.F. Ware, A.P. Chidgey, D.H. Gray, and R.L. Boyd. 2008. The lymphotoxin pathway regulates Aire-independent expression of ectopic genes and chemokines in thymic stromal cells. J. Immunol. 180:5384-5392. http://dx.doi.org/10.4049/jimmunol.180.8.5384
39. Sekai, M., Y. Hamazaki, and N. Minato. 2014. Medullary thymic epithelial stem cells maintain a functional thymus to ensure lifelong central T cell tolerance. Immunity. 41:753-761. http://dx.doi.org/10.1016/j.immuni.2014.10.011
40. Shackleton, M., F. Vaillant, K.J. Simpson, J. Stingl, G.K. Smyth, M.L. Asselin-Labat, L. Wu, G.J. Lindeman, and J.E. Visvader. 2006. Generation of a functional mammary gland from a single stem cell. Nature. 439:84-88. http://dx.doi.org/10.1038/nature04372
41. Shinzawa, M., Y. Maruyama, J. Qin, N. Akiyama, M. Miyauchi, H. Yanai, M. Takami, J. Inoue, and T. Akiyama. 2011. Splenic extramedullary hemopoiesis caused by a dysfunctional mutation in the NF-κB-inducing kinase gene. Biochem. Biophys. Res. Commun. 414:773-778. http://dx.doi.org/10.1016/j.bbrc.2011.10.001
42. Sugiyama, M., G. Nakato, T. Jinnohara, H. Akiba, K. Okumura, H. Ohno, and H. Yoshida. 2012. Expression pattern changes and function of RAN KL during mouse lymph node microarchitecture development. Int. Immunol. 24:369-378. http://dx.doi.org/10.1093/intimm/dxs002
43. Ucar, A., O. Ucar, P. Klug, S. Matt, F. Brunk, T.G. Hofmann, and B. Kyewski. 2014. Adult thymus contains FoxN1(-) epithelial stem cells that are bipotent for medullary and cortical thymic epithelial lineages. Immunity. 41:257-269. http://dx.doi.org/10.1016/j.immuni.2014.07.005
44. Varfolomeev, E., J.W. Blankenship, S.M. Wayson, A.V. Fedorova, N. Kayagaki, P. Garg, K. Zobel, J.N. Dynek, L.O. Elliott, H.J. Wallweber, et al. 2007. IAP antagonists induce autoubiquitination of c-IAPs, NF-κB activation, and TNFα-dependent apoptosis. Cell. 131:669-681. http://dx.doi.org/10.1016/j.cell.2007.10.030
45. Venanzi, E.S., D.H. Gray, C. Benoist, and D. Mathis. 2007. Lymphotoxin pathway and Aire influences on thymic medullary epithelial cells are unconnected. J. Immunol. 179:5693-5700. http://dx.doi.org/10.4049/jimmunol.179.9.5693
46. Weih, F., and J. Caamaño. 2003. Regulation of secondary lymphoid organ development by the nuclear factor-κB signal transduction pathway. Immunol. Rev. 195:91-105. http://dx.doi.org/10.1034/j.1600-065X.2003.00064.x
47. 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
48. White, A.J., K. Nakamura, W.E. Jenkinson, M. Saini, C. Sinclair, B. Seddon, P. Narendran, K. Pfeffer, T. Nitta, Y. Takahama, et al. 2010. Lymphotoxin signals from positively selected thymocytes regulate the terminal differentiation of medullary thymic epithelial cells. J. Immunol. 185:4769-4776. http://dx.doi.org/10.4049/jimmunol.1002151
49. Wong, K., N.L. Lister, M. Barsanti, J.M. Lim, M.V. Hammett, D.M. Khong, C. Siatskas, D.H. Gray, R.L. Boyd, and A.P. Chidgey. 2014. Multilineage potential and self-renewal define an epithelial progenitor cell population in the adult thymus. Cell Reports. 8:1198-1209. http://dx.doi.org/10.1016/j.celrep.2014.07.029
50. Wu, G., K. Hirabayashi, S. Sato, N. Akiyama, T. Akiyama, K. Shiota, and S. Yagi. 2012. DNA methylation profile of Aire-deficient mouse medullary thymic epithelial cells. BMC Immunol. 13:58. http://dx.doi.org/10.1186/1471-2172-13-58
51. 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
52. Yang, S., N. Fujikado, D. Kolodin, C. Benoist, and D. Mathis. 2015. Immune tolerance. Regulatory T cells generated early in life play a distinct role in maintaining self-tolerance. Science. 348:589-594. http://dx.doi.org/10.1126/science.aaa7017
53. Yin, Q., S.C. Lin, B. Lamothe, M. Lu, Y.C. Lo, G. Hura, L. Zheng, R.L. Rich, A.D. Campos, D.G. Myszka, et al. 2009. E2 interaction and dimerization in the crystal structure of TRAF6. Nat. Struct. Mol. Biol. 16:658-666. http://dx.doi.org/10.1038/nsmb.1605