Analysis of APC types involved in CD4 tolerance and regulatory T cell generation using reaggregated thymic organ cultures

Journal of Immunology

Volumn 190, Issue 5, 2013, Pages 2102-2110

  Guerri, Lucia ^a,c   Peguillet, Isabelle ^b   Geraldo, Yvette ^a   Nabti, Sabrina ^a   Premel, Virginie ^a   Lantz, Olivier ^a,b  

^a PSL RESEARCH UNIVERSITY   (France)

^b INSTITUT CURIE   (France)

^c MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL AGGREGATION; CELL SUBPOPULATION; CONTROLLED STUDY; CONVENTIONAL DENDRITIC CELL; EOSINOPHIL; FEMALE; IMMUNOLOGICAL TOLERANCE; IMMUNOREACTIVITY; LYMPHOCYTE DIFFERENTIATION; MACROPHAGE; MOUSE; NONHUMAN; ORGAN CULTURE; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; STROMA CELL; THYMOCYTE; THYMUS; THYMUS HEMATOPOIETIC STROMAL CELL;

ANIMALS; ANTIGENS, CD; B-LYMPHOCYTES; CELL CULTURE TECHNIQUES; DENDRITIC CELLS; EOSINOPHILS; EPITHELIUM; FEMALE; FETUS; MACROPHAGES; MICE; SELF TOLERANCE; STROMAL CELLS; T-LYMPHOCYTES, REGULATORY; THYMOCYTES; THYMUS GLAND;

EID: 84874240567     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202883     Document Type: Article

References (55)

1. Burnet, M. 1959. The Clonal Selection Theory of Acquired Immunity. Vanderbilt University Press, Nashville, TN.
2. Sprent, J. 2005. Proving negative selection in the thymus. J. Immunol. 174: 3841-3842.
3. Yamaguchi, T., J. B. Wing, and S. Sakaguchi. 2011. Two modes of immune suppression by Foxp3(+) regulatory T cells under inflammatory or noninflammatory conditions. Semin. Immunol. 23: 424-430.
4. Wirnsberger, G., M. Hinterberger, and L. Klein. 2011. Regulatory T-cell differentiation versus clonal deletion of autoreactive thymocytes. Immunol. Cell Biol. 89: 45-53.
5. Singer, A., S. Adoro, and J. H. Park. 2008. Lineage fate and intense debate: myths, models and mechanisms of CD4- versus CD8-lineage choice. Nat. Rev. Immunol. 8: 788-801.
6. Anderson, G., E. J. Jenkinson, N. C. Moore, and J. J. Owen. 1993. MHC class IIpositive epithelium and mesenchyme cells are both required for T-cell development in the thymus. Nature 362: 70-73.
7. 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.
8. Gallegos, A. M., and M. J. Bevan. 2004. Central tolerance to tissue-specific antigens mediated by direct and indirect antigen presentation. J. Exp. Med. 200: 1039-1049.
9. Lei, Y., A. M. Ripen, N. Ishimaru, I. Ohigashi, T. Nagasawa, L. T. Jeker, M. R. Bösl, G. A. Holländer, Y. Hayashi, Rde. 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.
10. Chen, Y., E. Ladi, P. Herzmark, E. Robey, and B. Roysam. 2009. Automated 5-D analysis of cell migration and interaction in the thymic cortex from time-lapse sequences of 3-D multi-channel multi-photon images. J. Immunol. Methods 340: 65-80.
11. Ladi, E., T. A. Schwickert, T. Chtanova, Y. Chen, P. Herzmark, X. Yin, H. Aaron, S. W. Chan, M. Lipp, B. Roysam, and E. A. Robey. 2008. Thymocyte-dendritic cell interactions near sources of CCR7 ligands in the thymic cortex. J. Immunol. 181: 7014-7023.
12. Jenkinson, E. J., G. Anderson, and J. J. Owen. 1992. Studies on T cell maturation on defined thymic stromal cell populations in vitro. J. Exp. Med. 176: 845-853.
13. van Meerwijk, J. P., S. Marguerat, R. K. Lees, R. N. Germain, B. J. Fowlkes, and H. R. MacDonald. 1997. Quantitative impact of thymic clonal deletion on the T cell repertoire. J. Exp. Med. 185: 377-383.
14. Proietto, A. I., S. van Dommelen, and L. Wu. 2009. The impact of circulating dendritic cells on the development and differentiation of thymocytes. Immunol. Cell Biol. 87: 39-45.
15. Proietto, A. I., S. van Dommelen, P. Zhou, A. Rizzitelli, A. D'Amico, R. J. Steptoe, S. H. Naik, M. H. Lahoud, Y. Liu, P. Zheng, et al. 2008. Dendritic cells in the thymus contribute to T-regulatory cell induction. Proc. Natl. Acad. Sci. USA 105: 19869-19874.
16. Wu, L., and K. Shortman. 2005. Heterogeneity of thymic dendritic cells. Semin. Immunol. 17: 304-312.
17. Li, J., J. Park, D. Foss, and I. Goldschneider. 2009. Thymus-homing peripheral dendritic cells constitute two of the three major subsets of dendritic cells in the steady-state thymus. J. Exp. Med. 206: 607-622.
18. Martín-Gayo, E., E. Sierra-Filardi, A. L. Corbí, and M. L. Toribio. 2010. Plasmacytoid dendritic cells resident in human thymus drive natural Treg cell development. Blood 115: 5366-5375.
19. Hanabuchi, S., T. Ito, W. R. Park, N. Watanabe, J. L. Shaw, E. Roman, K. Arima, Y. H. Wang, K. S. Voo, W. Cao, and Y. J. Liu. 2010. Thymic stromal lymphopoietin-activated plasmacytoid dendritic cells induce the generation of FOXP3+ regulatory T cells in human thymus. J. Immunol. 184: 2999-3007.
20. Baba, T., Y. Nakamoto, and N. Mukaida. 2009. Crucial contribution of thymic Sirp alpha+ conventional dendritic cells to central tolerance against blood-borne antigens in a CCR2-dependent manner. J. Immunol. 183: 3053-3063.
21. 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.
22. Ardavin, C., L. Wu, C. L. Li, and K. Shortman. 1993. Thymic dendritic cells and T cells develop simultaneously in the thymus from a common precursor population. Nature 362: 761-763.
23. Surh, C. D., and J. Sprent. 1994. T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 372: 100-103.
24. Esashi, E., T. Sekiguchi, H. Ito, S. Koyasu, and A. Miyajima. 2003. Cutting Edge: A possible role for CD4+ thymic macrophages as professional scavengers of apoptotic thymocytes. J. Immunol. 171: 2773-2777.
25. Throsby, M., A. Herbelin, J. M. Pléau, and M. Dardenne. 2000. CD11c+ eosinophils in the murine thymus: developmental regulation and recruitment upon MHC class I-restricted thymocyte deletion. J. Immunol. 165: 1965-1975.
26. Kim, H. J., E. S. Alonzo, G. Dorothee, J. W. Pollard, and D. B. Sant'Angelo. 2010. Selective depletion of eosinophils or neutrophils in mice impacts the efficiency of apoptotic cell clearance in the thymus. PLoS ONE 5: e11439.
27. Frommer, F., and A. Waisman. 2010. B cells participate in thymic negative selection of murine auto-reactive CD4+ T cells. PLoS ONE 5: e15372.
28. Webb, S. R., and J. Sprent. 1990. Tolerogenicity of thymic epithelium. Eur. J. Immunol. 20: 2525-2528.
29. Boehmer, H., J. Sprent, and M. Nabholz. 1975. Tolerance to histocompatibility determinants in tetraparental bone marrow chimeras. J. Exp. Med. 141: 322-334.
30. Good, M. F., K. W. Pyke, and G. J. Nossal. 1983. Functional clonal deletion of cytotoxic T-lymphocyte precursors in chimeric thymus produced in vitro from embryonic Anlagen. Proc. Natl. Acad. Sci. USA 80: 3045-3049.
31. Bonomo, A., and P. Matzinger. 1993. Thymus epithelium induces tissue-specific tolerance. J. Exp. Med. 177: 1153-1164.
32. von Boehmer, H., and K. Hafen. 1986. Minor but not major histocompatibility antigens of thymus epithelium tolerize precursors of cytolytic T cells. Nature 320: 626-628.
33. Hubert, F. X., S. A. Kinkel, G. M. Davey, B. Phipson, S. N. Mueller, A. Liston, A. I. Proietto, P. Z. Cannon, S. Forehan, G. K. Smyth, et al. 2011. Aire regulates the transfer of antigen from mTECs to dendritic cells for induction of thymic tolerance. Blood 118: 2462-2472.
34. Ohnmacht, C., A. Pullner, S. B. King, I. Drexler, S. Meier, T. Brocker, and D. Voehringer. 2009. Constitutive ablation of dendritic cells breaks self-tolerance of CD4 T cells and results in spontaneous fatal autoimmunity. J. Exp. Med. 206: 549-559.
35. McCaughtry, T. M., T. A. Baldwin, M. S. Wilken, and K. A. Hogquist. 2008. Clonal deletion of thymocytes can occur in the cortex with no involvement of the medulla. J. Exp. Med. 205: 2575-2584.
36. Paessens, L. C., D. M. Fluitsma, and Y. van Kooyk. 2008. Haematopoietic antigen-presenting cells in the human thymic cortex: evidence for a role in selection and removal of apoptotic thymocytes. J. Pathol. 214: 96-103.
37. Ohkura, N., and S. Sakaguchi. 2010. Regulatory T cells: roles of T cell receptor for their development and function. Semin. Immunopathol. 32: 95-106.
38. Bettini, M. L., and D. A. Vignali. 2010. Development of thymically derived natural regulatory T cells. Ann. N. Y. Acad. Sci. 1183: 1-12.
39. Liston, A., K. M. Nutsch, A. G. Farr, J. M. Lund, J. P. Rasmussen, P. A. Koni, and A. Y. Rudensky. 2008. Differentiation of regulatory Foxp3+ T cells in the thymic cortex. Proc. Natl. Acad. Sci. USA 105: 11903-11908.
40. Nunes-Cabaço, H., I. Caramalho, N. Sepúlveda, and A. E. Sousa. 2011. Differentiation of human thymic regulatory T cells at the double positive stage. Eur. J. Immunol. 41: 3604-3614.
41. Lee, H. M., and C. S. Hsieh. 2009. Rare development of Foxp3+ thymocytes in the CD4+CD8+ subset. J. Immunol. 183: 2261-2266.
42. Aschenbrenner, K., L. M. D'Cruz, E. H. Vollmann, M. Hinterberger, J. Emmerich, L. K. Swee, A. Rolink, and L. Klein. 2007. Selection of Foxp3+ regulatory T cells specific for self antigen expressed and presented by Aire+ medullary thymic epithelial cells. Nat. Immunol. 8: 351-358.
43. 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.
44. Bensinger, S. J., A. Bandeira, M. S. Jordan, A. J. Caton, and T. M. Laufer. 2001. Major histocompatibility complex class II-positive cortical epithelium mediates the selection of CD4(+)25(+) immunoregulatory T cells. J. Exp. Med. 194: 427-438.
45. Wirnsberger, G., F. Mair, and L. Klein. 2009. Regulatory T cell differentiation of thymocytes does not require a dedicated antigen-presenting cell but is under T cell-intrinsic developmental control. Proc. Natl. Acad. Sci. USA 106: 10278-10283.
46. Anderson, G., and E. J. Jenkinson. 2007. Investigating central tolerance with reaggregate thymus organ cultures. Methods Mol. Biol. 380: 185-196.
47. Robertson, J. M., P. E. Jensen, and B. D. Evavold. 2000. DO11.10 and OT-II T cells recognize a C-terminal ovalbumin 323-339 epitope. J. Immunol. 164: 4706-4712.
48. Gray, D. H., A. L. Fletcher, M. Hammett, N. Seach, T. Ueno, L. F. Young, J. Barbuto, R. L. Boyd, and A. P. Chidgey. 2008. Unbiased analysis, enrichment and purification of thymic stromal cells. J. Immunol. Methods 329: 56-66.
49. Irla, M., S. Hugues, J. Gill, T. Nitta, Y. Hikosaka, I. R. Williams, F. X. Hubert, H. S. Scott, Y. Takahama, G. A. Holländer, and W. Reith. 2008. Autoantigenspecific interactions with CD4+ thymocytes control mature medullary thymic epithelial cell cellularity. Immunity 29: 451-463.
50. Bautista, J. L., C. W. Lio, S. K. Lathrop, K. Forbush, Y. Liang, J. Luo, A. Y. Rudensky, and C. S. Hsieh. 2009. Intraclonal competition limits the fate determination of regulatory T cells in the thymus. Nat. Immunol. 10: 610-617.
51. D'Acquisto, F., and T. Crompton. 2011. CD3+CD42CD82 (double negative) T cells: saviours or villains of the immune response? Biochem. Pharmacol. 82: 333-340.
52. Hillhouse, E. E., and S. Lesage. 2012. A comprehensive review of the phenotype and function of antigen-specific immunoregulatory double negative T cells. J. Autoimmun.
53. Wang, J., A. Ioan-Facsinay, E. I. van der Voort, T. W. Huizinga, and R. E. Toes. 2007. Transient expression of FOXP3 in human activated nonregulatory CD4+ T cells. Eur. J. Immunol. 37: 129-138.
54. Morgan, M. E., J. H. van Bilsen, A. M. Bakker, B. Heemskerk, M. W. Schilham, F. C. Hartgers, B. G. Elferink, L. van der Zanden, R. R. de Vries, T.W. Huizinga, et al. 2005. Expression of FOXP3 mRNA is not confined to CD4+CD25+ T regulatory cells in humans. Hum. Immunol. 66: 13-20.
55. Koble, C., and B. Kyewski. 2009. The thymic medulla: a unique microenvironment for intercellular self-antigen transfer. J. Exp. Med. 206: 1505-1513.