Thymic negative selection is functional in NOD mice

Journal of Experimental Medicine

Volumn 209, Issue 3, 2012, Pages 623-637

  Mingueneau, Michael ^a   Jiang, Wenyu ^a   Feuerer, Markus ^a,b   Mathis, Diane ^a   Benoist, Christophe ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HETERODIMER; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOCHEMISTRY; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CELL CLONE; CELL ISOLATION; CELL SELECTION; CHIMERA; CONTROLLED STUDY; ENZYME ACTIVATION; GENE DELETION; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; IMMUNOLOGICAL TOLERANCE; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PRIORITY JOURNAL; THYMOCYTE;

ANIMALS; AUTOIMMUNITY; CELL DIFFERENTIATION; CLONAL DELETION; CLONAL SELECTION, ANTIGEN-MEDIATED; DIABETES MELLITUS, TYPE 1; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, IMMUNOLOGICAL; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; SELF TOLERANCE; T-LYMPHOCYTES;

EID: 84860387854     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20112593     Document Type: Article

References (60)

1. Adachi, K., and M.M. Davis. 2011. T-cell receptor ligation induces distinct signaling pathways in naive vs. antigen-experienced T cells. Proc. Natl. Acad. Sci. USA. 108:1549-1554. http://dx.doi.org/10.1073/pnas.1017340108
2. Baldwin, T.A., K.A. Hogquist, and S.C. Jameson. 2004. The fourth way? Harnessing aggressive tendencies in the thymus. J. Immunol. 173: 6515-6520.
3. Barnden, M.J., J. Allison, W.R. Heath, and F.R. Carbone. 1998. Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol. Cell Biol. 76:34-40. http://dx.doi.org/10.1046/j.1440-1711.1998.00709.x
4. Bruno, L., H.J. Fehling, and H. von Boehmer. 1996. The alpha beta T cell receptor can replace the gamma delta receptor in the development of gamma delta lineage cells. Immunity. 5:343-352. http://dx.doi.org/10.1016/S1074-7613(00)80260-5
5. Buch, T., F. Rieux-Laucat, I. Förster, and K. Rajewsky. 2002. Failure of HYspecific thymocytes to escape negative selection by receptor editing. Immunity. 16:707-718. http://dx.doi.org/10.1016/S1074-7613(02)00312-6
6. Choisy-Rossi, C.M., T.M. Holl, M.A. Pierce, H.D. Chapman, and D.V. Serreze. 2004. Enhanced pathogenicity of diabetogenic T cells escaping a non-MHC gene-controlled near death experience. J. Immunol. 173: 3791-3800.
7. Ciofani, M., and J.C. Zúñiga-Pflücker. 2010. Determining γδ versus αβ T cell development. Nat. Rev. Immunol. 10:657-663.
8. Clarke, S.R., M. Barnden, C. Kurts, F.R. Carbone, J.F. Miller, and W.R. Heath. 2000. Characterization of the ovalbumin-specific TCR transgenic line OT-I: MHC elements for positive and negative selection. Immunol. Cell Biol. 78:110-117. http://dx.doi.org/10.1046/j.1440-1711.2000.00889.x
9. D'Alise, A.M., V. Auyeung, M. Feuerer, J. Nishio, J. Fontenot, C. Benoist, and D. Mathis. 2008. The defect in T-cell regulation in NOD mice is an effect on the T-cell effectors. Proc. Natl. Acad. Sci. USA. 105:19857-19862. http://dx.doi.org/10.1073/pnas.0810713105
10. D'Souza, W.N., C.F. Chang, A.M. Fischer, M. Li, and S.M. Hedrick. 2008. The Erk2 MAPK regulates CD8 T cell proliferation and survival. J. Immunol. 181:7617-7629.
11. Dugas, V., C. Beauchamp, G. Chabot-Roy, E.E. Hillhouse, and S. Lesage. 2010. Implication of the CD47 pathway in autoimmune diabetes. J. Autoimmun. 35:23-32. http://dx.doi.org/10.1016/j.jaut.2010.01.002
12. Egawa, T., T. Kreslavsky, D.R. Littman, and H. von Boehmer. 2008. Lineage diversion of T cell receptor transgenic thymocytes revealed by lineage fate mapping. PLoS ONE. 3:e1512. http://dx.doi.org/10.1371/journal.pone.0001512
13. Feng, N., P. Vegh, E.V. Rothenberg, and M.A. Yui. 2011. Lineage divergence at the first TCR-dependent checkpoint: preferential γδ and impaired αβ T cell development in nonobese diabetic mice. J. Immunol. 186:826-837. http://dx.doi.org/10.4049/jimmunol.1002630
14. Ferreira, C., Y. Singh, A.L. Furmanski, F.S. Wong, O.A. Garden, and J. Dyson. 2009. Non-obese diabetic mice select a low-diversity repertoire of natural regulatory T cells. Proc. Natl. Acad. Sci. USA. 106:8320-8325. http://dx.doi.org/10.1073/pnas.0808493106
15. Fischer, A.M., C.D. Katayama, G. Pagès, J. Pouysségur, and S.M. Hedrick. 2005. The role of erk1 and erk2 in multiple stages of T cell development. Immunity. 23:431-443. http://dx.doi.org/10.1016/j.immuni.2005.08.013
16. +-like thymocytes in the NOD mouse. Eur. J. Immunol. 26:2989-2998. http://dx.doi.org/10.1002/eji.1830261226
17. Gonzalez, A., I. Andre-Schmutz, C. Carnaud, D. Mathis, and C. Benoist. 2001. Damage control, rather than unresponsiveness, effected by protective DX5+ T cells in autoimmune diabetes. Nat. Immunol. 2:1117-1125. http://dx.doi.org/10.1038/ni738
18. Gorelik, G., and B. Richardson. 2010. Key role of ERK pathway signaling in lupus. Autoimmunity. 43:17-22. http://dx.doi.org/10.3109/08916930903374832
19. Grusby, M.J., H. Auchincloss Jr., R. Lee, R.S. Johnson, J.P. Spencer, M. Zijlstra, R. Jaenisch, V.E. Papaioannou, and L.H. Glimcher. 1993. Mice lacking major histocompatibility complex class I and class II molecules. Proc. Natl. Acad. Sci. USA. 90:3913-3917. http://dx.doi.org/10.1073/pnas.90.9.3913
20. Haks, M.C., J.M. Lefebvre, J.P. Lauritsen, M. Carleton, M. Rhodes, T. Miyazaki, D.J. Kappes, and D.L. Wiest. 2005. Attenuation of gammadeltaTCR signaling efficiently diverts thymocytes to the alphabeta lineage. Immunity. 22:595-606. http://dx.doi.org/10.1016/j.immuni.2005.04.003
21. Hayes, S.M., and P.E. Love. 2002. Distinct structure and signaling potential of the gamma delta TCR complex. Immunity. 16:827-838. http://dx.doi.org/10.1016/S1074-7613(02)00320-5
22. Hayes, S.M., L. Li, and P.E. Love. 2005. TCR signal strength influences alphabeta/gammadelta lineage fate. Immunity. 22:583-593. http://dx.doi.org/10.1016/j.immuni.2005.03.014
23. Holler, P.D., T. Yamagata, W. Jiang, M. Feuerer, C. Benoist, and D. Mathis. 2007. The same genomic region conditions clonal deletion and clonal deviation to the CD8alphaalpha and regulatory T cell lineages in NOD versus C57BL/6 mice. Proc. Natl. Acad. Sci. USA. 104:7187-7192. http://dx.doi.org/10.1073/pnas.0701777104
24. Hu, T., I. Gimferrer, A. Simmons, D. Wiest, and J. Alberola-Ila. 2011. The Ras/MAPK pathway is required for generation of iNKT cells. PLoS ONE. 6:e19890. http://dx.doi.org/10.1371/journal.pone.0019890
25. Huesmann, M., B. Scott, P. Kisielow, and H. von Boehmer. 1991. Kinetics and efficacy of positive selection in the thymus of normal and T cell receptor transgenic mice. Cell. 66:533-540. http://dx.doi.org/10.1016/0092-8674(81)90016-7
26. Judkowski, V., C. Pinilla, K. Schroder, L. Tucker, N. Sarvetnick, and D.B. Wilson. 2001. Identification of MHC class II-restricted peptide ligands, including a glutamic acid decarboxylase 65 sequence, that stimulate diabetogenic T cells from transgenic BDC2.5 nonobese diabetic mice. J. Immunol. 166:908-917.
27. Kanagawa, O., A. Militech, and B.A. Vaupel. 2002. Regulation of diabetes development by regulatory T cells in pancreatic islet antigen-specific TCR transgenic nonobese diabetic mice. J. Immunol. 168:6159-6164.
28. Katz, J.D., B. Wang, K. Haskins, C. Benoist, and D. Mathis. 1993. Following a diabetogenic T cell from genesis through pathogenesis. Cell. 74:1089-1100. http://dx.doi.org/10.1016/0092-8674(93)90730-E
29. Kishimoto, H., and J. Sprent. 2001. A defect in central tolerance in NOD mice. Nat. Immunol. 2:1025-1031. http://dx.doi.org/10.1038/ni726
30. Laurent, J., N. Bosco, P.N. Marche, and R. Ceredig. 2004. New insights into the proliferation and differentiation of early mouse thymocytes. Int. Immunol. 16:1069-1080. http://dx.doi.org/10.1093/intimm/dxh108
31. Lesage, S., S.B. Hartley, S. Akkaraju, J. Wilson, M. Townsend, and C.C. Goodnow. 2002. Failure to censor forbidden clones of CD4 T cells in autoimmune diabetes. J. Exp. Med. 196:1175-1188. http://dx.doi.org/10.1084/jem.20020735
32. Lewandoski, M. 2001. Conditional control of gene expression in the mouse. Nat. Rev. Genet. 2:743-755. http://dx.doi.org/10.1038/35093537
33. Liston, A., S. Lesage, D.H. Gray, L.A. O'Reilly, A. Strasser, A.M. Fahrer, R.L. Boyd, J. Wilson, A.G. Baxter, E.M. Gallo, et al. 2004. Generalized resistance to thymic deletion in the NOD mouse; a polygenic trait characterized by defective induction of Bim. Immunity. 21:817-830.
34. Liston, A., K. Hardy, Y. Pittelkow, S.R. Wilson, L.E. Makaroff, A.M. Fahrer, and C.C. Goodnow. 2007. Impairment of organ-specific T cell negative selection by diabetes susceptibility genes: genomic analysis by mRNA profiling. Genome Biol. 8:R12. http://dx.doi.org/10.1186/gb-2007-8-1-r12
35. Mathis, D., and C. Benoist. 2009. Aire. Annu. Rev. Immunol. 27:287-312. http://dx.doi.org/10.1146/annurev.immunol.25.022106.141532
36. McGargill, M.A., I.L. Ch'en, C.D. Katayama, G. Pagès, J. Pouysségur, and S.M. Hedrick. 2009. Cutting edge: Extracellular signal-related kinase is not required for negative selection of developing T cells. J. Immunol. 183:4838-4842. http://dx.doi.org/10.4049/jimmunol.0902208
37. Philpott, K.L., J.L. Viney, G. Kay, S. Rastan, E.M. Gardiner, S. Chae, A.C. Hayday, and M.J. Owen. 1992. Lymphoid development in mice congenitally lacking T cell receptor αβ-expressing cells. Science. 256:1448-1452. http://dx.doi.org/10.1126/science.1604321
38. Pugliese, A., M. Zeller, A. Fernandez Jr., L.J. Zalcberg, R.J. Bartlett, C. Ricordi, M. Pietropaolo, G.S. Eisenbarth, S.T. Bennett, and D.D. Patel. 1997. The insulin gene is transcribed in the human thymus and transcription levels correlated with allelic variation at the INS VNTR-IDDM2 susceptibility locus for type 1 diabetes. Nat. Genet. 15:293-297. http://dx.doi.org/10.1038/ng0397-293
39. Rapoport, M.J., A.H. Lazarus, A. Jaramillo, E. Speck, and T.L. Delovitch. 1993. Thymic T cell anergy in autoimmune nonobese diabetic mice is mediated by deficient T cell receptor regulation of the pathway of p21ras activation. J. Exp. Med. 177:1221-1226. http://dx.doi.org/10.1084/jem.177.4.1221
40. Rapoport, M.J., A. Mor, P. Vardi, Y. Ramot, O. Levi, and T. Bistritzer. 1999. Defective activation of p21ras in peripheral blood mononuclear cells from patients with insulin dependent diabetes mellitus. Autoimmunity. 29:147-154. http://dx.doi.org/10.3109/08916939908995385
41. Reich, M., T. Liefeld, J. Gould, J. Lerner, P. Tamayo, and J.P. Mesirov. 2006. GenePattern 2.0. Nat. Genet. 38:500-501. http://dx.doi.org/10.1038/ng0506-500
42. Salojin, K., J. Zhang, M. Cameron, B. Gill, G. Arreaza, A. Ochi, and T.L. Delovitch. 1997. Impaired plasma membrane targeting of Grb2-murine son of sevenless (mSOS) complex and differential activation of the Fyn-T cell receptor (TCR)-ζ-Cbl pathway mediate T cell hyporesponsiveness in autoimmune nonobese diabetic mice. J. Exp. Med. 186:887-897. http://dx.doi.org/10.1084/jem.186.6.887
43. Sato, T., K. Hozumi, K. Kishihara, Y. Kametani, C. Sato, Y. Kumagai, T.W. Mak, and S. Habu. 1996. Evidence for down-regulation of highly expressed TCR by CD4 and CD45 on non-selected CD4+CD8+ thymocytes. Int. Immunol. 8:1529-1535. http://dx.doi.org/10.1093/intimm/8.10.1529
44. Serreze, D.V., C.M. Choisy-Rossi, A.E. Grier, T.M. Holl, H.D. Chapman, J.R. Gahagan, M.A. Osborne, W. Zhang, B.L. King, A. Brown, et al. 2008. Through regulation of TCR expression levels, an Idd7 region gene(s) interactively contributes to the impaired thymic deletion of autoreactive diabetogenic CD8+ T cells in nonobese diabetic mice. J. Immunol. 180:3250-3259.
45. Siggs, O.M., L.E. Makaroff, and A. Liston. 2006. The why and how of thymocyte negative selection. Curr. Opin. Immunol. 18:175-183. http://dx.doi.org/10.1016/j.coi.2006.01.001
46. Singh, K., P. Deshpande, S. Pryshchep, I. Colmegna, V. Liarski, C.M. Weyand, and J.J. Goronzy. 2009. ERK-dependent T cell receptor threshold calibration in rheumatoid arthritis. J. Immunol. 183:8258-8267. http://dx.doi.org/10.4049/jimmunol.0901784
47. Sohn, S.J., J. Thompson, and A. Winoto. 2007. Apoptosis during negative selection of autoreactive thymocytes. Curr. Opin. Immunol. 19:510-515. http://dx.doi.org/10.1016/j.coi.2007.06.001
48. Starr, T.K., S.C. Jameson, and K.A. Hogquist. 2003. Positive and negative selection of T cells. Annu. Rev. Immunol. 21:139-176. http://dx.doi.org/10.1146/annurev.immunol.21.120601.141107
49. Teixeiro, E., and M.A. Daniels. 2010. ERK and cell death: ERK location and T cell selection. FEBS J. 277:30-38. http://dx.doi.org/10.1111/j.1742-4658.2009.07368.x
50. Terrence, K., C.P. Pavlovich, E.O. Matechak, and B.J. Fowlkes. 2000. Premature expression of T cell receptor (TCR)αβ suppresses TCRγδ gene rearrangement but permits development of γδ lineage T cells. J. Exp. Med. 192:537-548. http://dx.doi.org/10.1084/jem.192.4.537
51. Trop, S., M. Rhodes, D.L. Wiest, P. Hugo, and J.C. Zúñiga-Pflücker. 2000. Competitive displacement of pT alpha by TCR-alpha during TCR assembly prevents surface coexpression of pre-TCR and alpha beta TCR. J. Immunol. 165:5566-5572.
52. van Santen, H.M., C. Benoist, and D. Mathis. 2004. Number of T reg cells that differentiate does not increase upon encounter of agonist ligand on thymic epithelial cells. J. Exp. Med. 200:1221-1230. http://dx.doi.org/10.1084/jem.20041022
53. Villunger, A., V.S. Marsden, and A. Strasser. 2003. Efficient T cell receptormediated apoptosis in nonobese diabetic mouse thymocytes. Nat. Immunol. 4:717-718, author reply:718. http://dx.doi.org/10.1038/ni0803-717
54. Wang, Y., O. Horvath, A. Hamm-Baarke, M. Richelme, C. Grégoire, R. Guinamard, V. Horejsi, P. Angelisova, J. Spicka, B. Schraven, et al. 2005. Single and combined deletions of the NTAL/LAB and LAT adaptors minimally affect B-cell development and function. Mol. Cell. Biol. 25:4455-4465. http://dx.doi.org/10.1128/MCB.25.11.4455-4465.2005
55. Wicker, L.S., M.C. Appel, F. Dotta, A. Pressey, B.J. Miller, N.H. DeLarato, P.A. Fischer, R.C. Boltz Jr., and L.B. Peterson. 1992. Autoimmune syndromes in major histocompatibility complex (MHC) congenic strains of nonobese diabetic (NOD) mice. The NOD MHC is dominant for insulitis and cyclophosphamide-induced diabetes. J. Exp. Med. 176:67-77. http://dx.doi.org/10.1084/jem.176.1.67
56. Willoughby, J.E., P.S. Costello, R.H. Nicolas, N.J. Robinson, G. Stamp, F. Powrie, and R. Treisman. 2007. Raf signaling but not the ERK effector SAP-1 is required for regulatory T cell development. J. Immunol. 179:6836-6844.
57. + T cells: halflife and survival signals in the absence of major histocompatibility complex class II molecules. J. Exp. Med. 191:355-364. http://dx.doi.org/10.1084/jem.191.2.355
58. Yamagata, T., D. Mathis, and C. Benoist. 2004. Self-reactivity in thymic double-positive cells commits cells to a CD8 alpha alpha lineage with characteristics of innate immune cells. Nat. Immunol. 5:597-605. http://dx.doi.org/10.1038/ni1070
59. Zhang, J., K. Salojin, and T.L. Delovitch. 1998. Sequestration of CD4-associated Lck from the TCR complex may elicit T cell hyporesponsiveness in nonobese diabetic mice. J. Immunol. 160:1148-1157.
60. Zucchelli, S., P. Holler, T. Yamagata, M. Roy, C. Benoist, and D. Mathis. 2005. Defective central tolerance induction in NOD mice: genomics and genetics. Immunity. 22:385-396. http://dx.doi.org/10.1016/j.immuni.2005.01.015