Lunatic Fringe enhances competition for Delta-like Notch ligands but does not overcome defective pre-TCR signaling during thymocyte β-selection in vivo

Journal of Immunology

Volumn 185, Issue 8, 2010, Pages 4609-4617

  Visan, Ioana ^a,b   Yuan, Julie S ^a,b   Liu, Ying ^c   Stanley, Pamela ^c   Guidos, Cynthia J ^a,b  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUCOSE; LIGAND; NOTCH1 RECEPTOR; PROTEIN PRECURSOR; T LYMPHOCYTE RECEPTOR; GLYCOSYLTRANSFERASE; LFNG PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR; NOTCH1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; BINDING COMPETITION; CELL SELECTION; CONTROLLED STUDY; GENE OVEREXPRESSION; IN VIVO CULTURE; LIGAND BINDING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; THYMOCYTE; ADOPTIVE TRANSFER; ANIMAL; CELL DIFFERENTIATION; CELL LINEAGE; CELL SEPARATION; CYTOLOGY; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELL; IMMUNOLOGY; METABOLISM; T LYMPHOCYTE; THYMUS; TRANSGENIC MOUSE;

ADOPTIVE TRANSFER; ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL SEPARATION; FLOW CYTOMETRY; GLYCOSYLTRANSFERASES; HEMATOPOIETIC STEM CELLS; LIGANDS; MICE; MICE, TRANSGENIC; RECEPTOR, NOTCH1; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; THYMUS GLAND;

EID: 78049517631     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002008     Document Type: Article

References (39)

1. Yuan, J. S., P. C. Kousis, S. Suliman, I. Visan, and C. J. Guidos. 2010. Functions of notch signaling in the immune system: consensus and controversies. Annu. Rev. Immunol. 28:343-365.
2. Koch, U., T. A. Lacombe, D. Holland, J. L. Bowman, B. L. Cohen, S. E. Egan, and C. J. Guidos. 2001. Subversion of the T/B lineage decision in the thymus by lunatic fringe-mediated inhibition of Notch-1. Immunity 15:225-236.
3. Wilson, A., H. R. MacDonald, and F. Radtke. 2001. Notch 1-deficient common lymphoid precursors adopt a B cell fate in the thymus. J. Exp. Med. 194:1003-1012.
4. Sambandam, A., I. Maillard, V. P. Zediak, L. Xu, R. M. Gerstein, J. C. Aster, W. S. Pear, and A. Bhandoola. 2005. Notch signaling controls the generation and differentiation of early T lineage progenitors. Nat. Immunol. 6:663-670.
5. Tan, J. B., I. Visan, J. S. Yuan, and C. J. Guidos. 2005. Requirement for Notch1 signals at sequential early stages of intrathymic T cell development. Nat. Immunol. 6:671-679.
6. Balciunaite, G., R. Ceredig, and A. G. Rolink. 2005. The earliest subpopulation of mouse thymocytes contains potent T, significant macrophage, and natural killer cell but no B-lymphocyte potential. Blood 105:1930-1936.
7. Benz, C., and C. C. Bleul. 2005. A multipotent precursor in the thymus maps to the branching point of the T versus B lineage decision. J. Exp. Med. 202:21-31.
8. Taghon, T., M. A. Yui, and E. V. Rothenberg. 2007. Mast cell lineage diversion of T lineage precursors by the essential T cell transcription factor GATA-3. Nat. Immunol. 8:845-855.
9. Bell, J. J., and A. Bhandoola. 2008. The earliest thymic progenitors for T cells possess myeloid lineage potential. Nature 452:764-767.
10. Wada, H., K. Masuda, R. Satoh, K. Kakugawa, T. Ikawa, Y. Katsura, and H. Kawamoto. 2008. Adult T-cell progenitors retain myeloid potential. Nature 452:768-772.
11. Feyerabend, T. B., G. Terszowski, A. Tietz, C. Blum, H. Luche, A. Gossler, N. W. Gale, F. Radtke, H. J. Fehling, and H. R. Rodewald. 2009. Deletion of Notch1 converts pro-T cells to dendritic cells and promotes thymic B cells by cell-extrinsic and cell-intrinsic mechanisms. Immunity 30:67-79.
12. Wolfer, A., A. Wilson, M. Nemir, H. R. MacDonald, and F. Radtke. 2002. Inactivation of Notch1 impairs VDJbeta rearrangement and allows pre-TCR-independent survival of early alpha beta Lineage Thymocytes. Immunity 16:869-879.
13. Maillard, I., L. Tu, A. Sambandam, Y. Yashiro-Ohtani, J. Millholland, K. Keeshan, O. Shestova, L. Xu, A. Bhandoola, and W. S. Pear. 2006. The requirement for Notch signaling at the beta-selection checkpoint in vivo is absolute and independent of the pre-T cell receptor. J. Exp. Med. 203:2239-2245.
14. von Boehmer, H. 2005. Unique features of the pre-T-cell receptor alpha-chain: not just a surrogate. Nat. Rev. Immunol. 5:571-577.
15. Yamasaki, S., E. Ishikawa, M. Sakuma, K. Ogata, K. Sakata-Sogawa, M. Hiroshima, D. L. Wiest, M. Tokunaga, and T. Saito. 2006. Mechanistic basis of pre-T cell receptor-mediated autonomous signaling critical for thymocyte development. Nat. Immunol. 7:67-75.
16. Groves, T., P. Smiley, M. P. Cooke, K. Forbush, R. M. Perlmutter, and C. J. Guidos. 1996. Fyn can partially substitute for Lck in T lymphocyte development. Immunity 5:417-428.
17. van Oers, N. S., B. Lowin-Kropf, D. Finlay, K. Connolly, and A. Weiss. 1996. alpha beta T cell development is abolished in mice lacking both Lck and Fyn protein tyrosine kinases. Immunity 5:429-436.
18. Hoffman, E. S., L. Passoni, T. Crompton, T. M. Leu, D. G. Schatz, A. Koff, M. J. Owen, and A. C. Hayday. 1996. Productive T-cell receptor beta-chain gene rearrangement: coincident regulation of cell cycle and clonality during development in vivo. Genes Dev. 10:948-962.
19. Taghon, T., M. A. Yui, R. Pant, R. A. Diamond, and E. V. Rothenberg. 2006. Developmental and molecular characterization of emerging beta-and gammadelta-selected pre-T cells in the adult mouse thymus. Immunity 24:53-64.
20. Garbe, A. I., A. Krueger, F. Gounari, J. C. Zúñiga- Pflücker, and H. von Boehmer. 2006. Differential synergy of Notch and T cell receptor signaling determines alphabeta versus gammadelta lineage fate. J. Exp. Med. 203:1579-1590.
21. Borowski, C., X. Li, I. Aifantis, F. Gounari, and H. von Boehmer. 2004. Pre-TCRalpha and TCRalpha are not interchangeable partners of TCRbeta during T lymphocyte development. J. Exp. Med. 199:607-615.
22. Prockop, S. E., and H. T. Petrie. 2004. Regulation of thymus size by competition for stromal niches among early T cell progenitors. J. Immunol. 173:1604-1611.
23. Stanley, P. 2007. Regulation of Notch signaling by glycosylation. Curr. Opin. Struct. Biol. 17:530-535.
24. Mohtashami, M., and J. C. Zúñiga-Pflücker. 2006. Three-dimensional architecture of the thymus is required to maintain Delta-like expression necessary for inducing T cell development. J. Immunol. 176:730-734.
25. Lehar, S. M., J. Dooley, A. G. Farr, and M. J. Bevan. 2005. Notch ligands Delta1 and Jagged1 transmit distinct signals to T cell precursors. Blood 105:1440-1447.
26. Ciofani, M., T. M. Schmitt, A. Ciofani, A. M. Michie, N. Cuburu, A. Aublin, J. L. Maryanski, and J. C. Zúñiga-Pflücker. 2004. Obligatory role for cooperative signaling by pre-TCR and Notch during thymocyte differentiation. J. Immunol. 172:5230-5239.
27. Huang, E. Y., A. M. Gallegos, S. M. Richards, S. M. Lehar, and M. J. Bevan. 2003. Surface expression of Notch1 on thymocytes: correlation with the doublenegative to double-positive transition. J. Immunol. 171:2296-2304.
28. Moloney, D. J., L. H. Shair, F. M. Lu, J. Xia, R. Locke, K. L. Matta, and R. S. Haltiwanger. 2000. Mammalian Notch1 is modified with two unusual forms of O-linked glycosylation found on epidermal growth factor-like modules. J. Biol. Chem. 275:9604-9611.
29. Rampal, R., A. S. Li, D. J. Moloney, S. A. Georgiou, K. B. Luther, A. Nita-Lazar, and R. S. Haltiwanger. 2005. Lunatic fringe, manic fringe, and radical fringe recognize similar specificity determinants in O-fucosylated epidermal growth factor-like repeats. J. Biol. Chem. 280:42454-42463.
30. Wang, Y., L. Shao, S. Shi, R. J. Harris, M. W. Spellman, P. Stanley, and R. S. Haltiwanger. 2001. Modification of epidermal growth factor-like repeats with O-fucose: molecular cloning and expression of a novel GDP-fucose protein O-fucosyltransferase. J. Biol. Chem. 276:40338-40345.
31. Panin, V. M., L. Shao, L. Lei, D. J. Moloney, K. D. Irvine, and R. S. Haltiwanger. 2002. Notch ligands are substrates for protein O- fucosyltransferase-1 and Fringe. J. Biol. Chem. 277:29945-29952.
32. Haines, N., and K. D. Irvine. 2003. Glycosylation regulates Notch signalling. Nat. Rev. Mol. Cell Biol. 4:786-797.
33. Ge, C., and P. Stanley. 2008. The O-fucose glycan in the ligand-binding domain of Notch1 regulates embryogenesis and T cell development. Proc. Natl. Acad. Sci. USA 105:1539-1544.
34. Visan, I., J. B. Tan, J. S. Yuan, J. A. Harper, U. Koch, and C. J. Guidos. 2006. Regulation of T lymphopoiesis by Notch1 and Lunatic fringe-mediated competition for intrathymic niches. Nat. Immunol. 7:634-643.
35. Fehling, H. J., A. Krotkova, C. Saint-Ruf, and H. von Boehmer. 1995. Crucial role of the pre-T-cell receptor a gene in development of ab but not gd T cells. Nature 375:795-798.
36. Ciofani, M., and J. C. Zúñiga-Pflücker. 2005. Notch promotes survival of pre-T cells at the b-selection checkpoint by regulating cellular metabolism. Nat. Immunol. 6:881-888.
37. Aifantis, I., M. Mandal, K. Sawai, A. Ferrando, and T. Vilimas. 2006. Regulation of T-cell progenitor survival and cell-cycle entry by the pre-T-cell receptor. Immunol. Rev. 209:159-169.
38. Porritt, H. E., K. Gordon, and H. T. Petrie. 2003. Kinetics of steady-state differentiation and mapping of intrathymic-signaling environments by stem cell transplantation in nonirradiated mice. J. Exp. Med. 198:957-962.
39. Yashiro-Ohtani, Y., Y. He, T. Ohtani, M. E. Jones, O. Shestova, L. Xu, T. C. Fang, M. Y. Chiang, A. M. Intlekofer, S. C. Blacklow, et al. 2009. Pre-TCR signaling inactivates Notch1 transcription by antagonizing E2A. Genes Dev. 23:1665-1676.