Role of Hedgehog signalling at the transition from double-positive to single-positive thymocyte

European Journal of Immunology

Volumn 42, Issue 2, 2012, Pages 489-499

  Furmanski, Anna L ^a   Saldana, Jose Ignacio ^a   Rowbotham, Nicola J ^a   Ross, Susan E ^a   Crompton, Tessa ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Gli2; Hh signalling; T cells; Thymus

Indexed keywords

SONIC HEDGEHOG PROTEIN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR GATA 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELL TRANSFORMATION; CONTROLLED STUDY; GENETIC TRANSCRIPTION; LYMPHOCYTOPOIESIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE SUBPOPULATION; THYMOCYTE; THYMUS; UPREGULATION; WILD TYPE;

ANIMALS; ANTIGENS, CD4; ANTIGENS, CD8; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; EMBRYO, MAMMALIAN; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HEDGEHOG PROTEINS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; THYMOCYTES; THYMUS GLAND; TRANSCRIPTIONAL ACTIVATION;

EID: 84856050034     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201141758     Document Type: Article

References (45)

1. Wells, F. B., Gahm, S. J., Hedrick, S. M., Bluestone, J. A., Dent, A. and Matis, L. A., Requirement for positive selection of gamma delta receptor-bearing T cells. Science 1991. 253: 903-905.
2. - lineage choice. Nat. Rev. Immunol. 2008. 8: 788-801.
3. Takahama, Y., Journey through the thymus: stromal guides for T-cell development and selection. Nat. Rev. Immunol. 2006. 6: 127-135.
4. Alves, N. L., Richard-Le Goff, O., Huntington, N. D., Sousa, A. P., Ribeiro, V. S., Bordack, A. et al., Characterization of the thymic IL-7 niche in vivo. Proc. Natl. Acad. Sci. USA 2009. 106: 1512-1517.
5. Park, J. H., Adoro, S., Guinter, T., Erman, B., Alag, A. S., Catalfamo, M., Kimura, M. Y. et al., signalling by intrathymic cytokines, not T cell antigen receptors, specifies CD8 lineage choice and promotes the differentiation of cytotoxic-lineage T cells. Nat. Immunol. 2010. 11: 257-264.
6. Crompton, T., Outram, S. V. and Hager-Theodorides, A. L., Sonic hedgehog signalling in T-cell development and activation. Nat. Rev. Immunol. 2007. 7: 726-735.
7. Laky, K. and Fowlkes, B. J., Notch signalling in CD4 and CD8 T cell development. Curr. Opin. Immunol. 2008. 20: 197-202.
8. Carpenter, A. C. and Bosselut, R., Decision checkpoints in the thymus. Nat. Immunol. 2010. 11: 666-673.
9. Hernandez-Hoyos, G., Anderson, M. K., Wang, C., Rothenberg, E. V. and Alberola-Ila, J., GATA-3 expression is controlled by TCR signals and regulates CD4/CD8 differentiation. Immunity 2003. 19: 83-94.
10. Matechak, E. O., Killeen, N., Hedrick, S. M. and Fowlkes, B. J., MHC class II-specific T cells can develop in the CD8 lineage when CD4 is absent. Immunity 1996. 4: 337-347.
11. Ling, K. W., van Hamburg, J. P., de Bruijn, M. J., Kurek, D., Dingjan, G. M. and Hendriks, R. W., GATA3 controls the expression of CD5 and the T cell receptor during CD4T cell lineage development. Eur. J. Immunol. 2007. 37: 1043-1052.
12. Outram, S. V., Varas, A., Pepicelli, C. V. and Crompton, T., Hedgehog signalling regulates differentiation from double-negative to double-positive thymocyte. Immunity 2000. 13: 187-197.
13. Shah, D. K., Hager-Theodorides, A. L., Outram, S. V., Ross, S. E., Varas, A. and Crompton, T., Reduced thymocyte development in sonic hedgehog knockout embryos. J. Immunol. 2004. 172: 2296-2306.
14. + precursor cells. J. Immunol. 2004. 173: 5046-5053.
15. El Andaloussi, A., Graves, S., Meng, F., Mandal, M., Mashayekhi, M. and Aifantis, I., Hedgehog signalling controls thymocyte progenitor homeostasis and differentiation in the thymus. Nat. Immunol. 2006. 7: 418-426.
16. Rowbotham, N. J., Hager-Theodorides, A. L., Cebecauer, M., Shah, D. K., Drakopoulou, E., Dyson, J., Outram, S. V. and Crompton, T., Activation of the Hedgehog signalling pathway in T-lineage cells inhibits TCR repertoire selection in the thymus and peripheral T-cell activation. Blood 2007. 109: 3757-3766.
17. Rowbotham, N. J., Hager-Theodorides, A. L., Furmanski, A. L., Ross, S. E., Outram, S. V., Dessens, J. T. and Crompton, T., Sonic hedgehog negatively regulates pre-TCR-induced differentiation by a Gli2-dependent mechanism. Blood 2009. 113: 5144-5156.
18. Jia, J. and Jiang, J., Decoding the Hedgehog signal in animal development. Cell. Mol. Life Sci. 2006. 63: 1249-1265.
19. Koebernick, K. and Pieler, T., Gli-type zinc finger proteins as bipotential transducers of Hedgehog signalling. Differentiation 2002. 70: 69-76.
20. Sasaki, H., Nishizaki, Y., Hui, C., Nakafuku, M. and Kondoh, H., Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: implication of Gli2 and Gli3 as primary mediators of Shh signalling. Development 1999. 126: 3915-3924.
21. Hager-Theodorides, A. L., Furmanski, A. L., Ross, S. E., Outram, S. V., Rowbotham, N. J. and Crompton, T., The Gli3 transcription factor expressed in the thymus stroma controls thymocyte negative selection via Hedgehog-dependent and -independent mechanisms. J. Immunol. 2009. 183: 3023-3032.
22. Varas, A., Hernandez-Lopez, C., Valencia, J., Mattavelli, S., Martinez, V. G., Hidalgo, L., Gutierrez-Frias, C., Zapata, A. G. et al., Survival and function of human thymic dendritic cells are dependent on autocrine Hedgehog signalling. J. Leukoc. Biol. 2008. 83: 1476-1483.
23. Syn, W. K., Witek, R. P., Curbishley, S. M., Jung, Y., Choi, S. S., Enrich, B., Omenetti, A. et al., Role for hedgehog pathway in regulating growth and function of invariant NKT cells. Eur. J. Immunol. 2009. 39: 1879-1892.
24. Rowbotham, N. J., Furmanski, A. L., Hager-Theodorides, A. L., Ross, S. E., Drakopoulou, E., Koufaris, C., Outram, S. V. and Crompton, T., Repression of hedgehog signal transduction in T-lineage cells increases TCR-induced activation and proliferation. Cell Cycle 2008. 7: 904-908.
25. Sacedon, R., Varas, A., Hernandez-Lopez, C., Gutierrez-deFrias, C., Crompton, T., Zapata, A. G. and Vicente, A., Expression of hedgehog proteins in the human thymus. J. Histochem. Cytochem. 2003. 51: 1557-1566.
26. Kisielow, P., Teh, H. S., Bluthmann, H. and von Boehmer, H., Positive selection of antigen-specific T cells in thymus by restricting MHC molecules. Nature 1988. 335: 730-733.
27. von Boehmer, H., Kirberg, J. and Rocha, B., An unusual lineage of alpha/beta T cells that contains autoreactive cells. J. Exp. Med. 1991. 174: 1001-1008.
28. Baldwin, T. A., Sandau, M. M., Jameson, S. C. and Hogquist, K. A., The timing of TCR alpha expression critically influences T cell development and selection. J. Exp. Med. 2005. 202: 111-121.
29. Egawa, T., Kreslavsky, T., Littman, D. R. and von Boehmer, H., Lineage diversion of T cell receptor transgenic thymocytes revealed by lineage fate mapping. PLoS One 2008. 3: e1512.
30. Maione, F., Paschalidis, N., Iqbal, A. J., Crompton, T., Perretti, M. and D'Acquisto, F., Analysis of the inflammatory response in HY-TCR transgenic mice highlights the pathogenic potential of CD4(- )CD8(-) T cells. Autoimmunity 2010. 42: 672-681.
31. Terrence, K., Pavlovich, C. P., Matechak, E. O. and Fowlkes, B. J., Premature expression of T cell receptor (TCR)alphabeta suppresses TCRgammadelta gene rearrangement but permits development of gammadelta lineage T cells. J. Exp. Med. 2000. 192: 537-548.
32. Hayes, S. M., Li, L. and Love, P. E., TCR signal strength influences alphabeta/gammadelta lineage fate. Immunity 2005. 22: 583-593.
33. Simpson, E., Takacs, K. and Altmann, D. M., Thymic repertoire selection by superantigens: presentation by human and mouse MHC molecules. Thymus 1994. 23: 1-13.
34. Backstrom, B. T., Muller, U., Hausmann, B. and Palmer, E., Positive selection through a motif in the alphabeta T cell receptor. Science 1998. 281: 835-838.
35. Outram, S. V., Hager-Theodorides, A. L., Shah, D. K., Rowbotham, N. J., Drakopoulou, E., Ross, S. E., Lanske, B. et al., Indian hedgehog (Ihh) both promotes and restricts thymocyte differentiation. Blood 2009. 113: 2217-2228.
36. Feng, C., Woodside, K. J., Vance, B. A., El-Khoury, D., Canelles, M., Lee, J., Gress, R. et al., A potential role for CD69 in thymocyte emigration. Int. Immunol. 2002. 14: 535-544.
37. Gabor, M. J., Godfrey, D. I. and Scollay, R., Recent thymic emigrants are distinct from most medullary thymocytes. Eur. J. Immunol. 1997. 27: 2010-2015.
38. Drakopoulou, E., Outram, S. V., Rowbotham, N. J., Ross, S. E., Furmanski, A. L., Saldana, J. I., Hager-Theodorides, A. L. and Crompton, T., Non-redundant role for the transcription factor Gli1 at multiple stages of thymocyte development. Cell Cycle 2010. 9: 4144-4152.
39. Pan, Y., Bai, C. B., Joyner, A. L. and Wang, B., Sonic hedgehog signalling regulates Gli2 transcriptional activity by suppressing its processing and degradation. Mol. Cell. Biol. 2006. 26: 3365-3377.
40. Azzam, H. S., Grinberg, A., Lui, K., Shen, H., Shores, E. W. and Love, P. E., CD5 expression is developmentally regulated by T cell receptor (TCR) signals and TCR avidity. J. Exp. Med. 1998. 188: 2301-2311.
41. Xiong, Y. and Bosselut, R., The enigma of CD4-lineage specification. Eur. J. Immunol. 2011. 41: 568-574.
42. Melichar, H. and Kang, J., Integrated morphogen signal inputs in gammadelta versus alphabeta T-cell differentiation. Immunol. Rev. 2007. 215: 32-45.
43. + thymocytes. Nature 1988. 333: 742-746.
44. Philpott, K. L., Viney, J. L., Kay, G., Rastan, S., Gardiner, E. M., Chae, S., Hayday, A. C. and Owen, M. J., Lymphoid development in mice congenitally lacking T cell receptor alpha beta-expressing cells. Science 1992. 256: 1448-1452.
45. Furmanski, A. L., Ferreira, C., Bartok, I., Dimakou, S., Rice, J., Stevenson, F. K., Millrain, M. M. et al., Public T cell receptor beta-chains are not advantaged during positive selection. J. Immunol. 2008. 180: 1029-1039.