Ly49D-mediated ITAM signaling in immature thymocytes impairs development by bypassing the pre-TCR checkpoint

Journal of Immunology

Volumn 187, Issue 1, 2011, Pages 110-117

  Merck, Estelle ^a   Lees, Rosemary K ^a   Voyle, Roger B ^a   Held, Werner ^a   MacDonald, H Robson ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CD24 ANTIGEN; CD5 ANTIGEN; CELL PROTEIN; KILLER CELL ACTIVATING RECEPTOR ASSOCIATED PROTEIN; MEMBRANE RECEPTOR; NATURAL KILLER CELL RECEPTOR; PROTEIN ITAM; PROTEIN ITIM; PROTEIN LY49D; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR BETA CHAIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL MATURATION; CONTROLLED STUDY; GENE EXPRESSION; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; THYMOCYTE; TRANSGENE; TRANSGENIC MOUSE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; H-2 ANTIGENS; HUMANS; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY A; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS; TYROSINE;

EID: 79960400853     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002755     Document Type: Article

References (41)

1. Hayday, A. C., and D. J. Pennington. 2007. Key factors in the organized chaos of early T cell development. Nat. Immunol. 8: 137-144.
2. von Boehmer, H. 2004. Selection of the T-cell repertoire: receptor-controlled checkpoints in T-cell development. Adv. Immunol. 84: 201-238.
3. Mandelboim, O., D. M. Davis, H. T. Reyburn, M. Valés-Gómez, E. G. Sheu, L. Pazmany, and J. L. Strominger. 1996. Enhancement of class II-restricted T cell responses by costimulatory NK receptors for class I MHC proteins. Science 274: 2097-2100.
4. Phillips, J. H., J. E. Gumperz, P. Parham, and L. L. Lanier. 1995. Superantigen-dependent, cell-mediated cytotoxicity inhibited by MHC class I receptors on T lymphocytes. Science 268: 403-405.
5. Remtoula, N., A. Bensussan, and A. Marie-Cardine. 2008. Cutting edge: selective expression of inhibitory or activating killer cell Ig-like receptors in circulating CD4+ T lymphocytes. J. Immunol. 180: 2767-2771.
6. Merck, E., R. B. Voyle, and H. R. MacDonald. 2009. Ly49D engagement on T lymphocytes induces TCR-independent activation and CD8 effector functions that control tumor growth. J. Immunol. 182: 183-192.
7. Isakov, N. 1998. Role of immunoreceptor tyrosine-based activation motif in signal transduction from antigen and Fc receptors. Adv. Immunol. 69: 183-247.
8. Ravetch, J. V., and L. L. Lanier. 2000. Immune inhibitory receptors. Science 290: 84-89.
9. Lanier, L. L. 2005. NK cell recognition. Annu. Rev. Immunol. 23: 225-274.
10. Pauza, M., K. M. Smith, H. Neal, C. Reilly, L. L. Lanier, and D. Lo. 2000. Transgenic expression of Ly-49A in thymocytes alters repertoire selection. J. Immunol. 164: 884-892. (Pubitemid 30043714)
11. Fahlén, L., L. Oberg, T. Brännström, N. K. Khoo, U. Lendahl, and C. L. Sentman. 2000. Ly49A expression on T cells alters T cell selection. Int. Immunol. 12: 215-222.
12. Robson MacDonald, H., R. K. Lees, and W. Held. 1998. Developmentally regulated extinction of Ly-49 receptor expression permits maturation and selection of NK1.1+ T cells. J. Exp. Med. 187: 2109-2114.
13. Voyle, R. B., F. Beermann, R. K. Lees, J. Schümann, J. Zimmer, W. Held, and H. R. MacDonald. 2003. Ligand-dependent inhibition of CD1d-restricted NKT cell development in mice transgenic for the activating receptor Ly49D. J. Exp. Med. 197: 919-925.
14. Held, W., D. Cado, and D. H. Raulet. 1996. Transgenic expression of the Ly49A natural killer cell receptor confers class I major histocompatibility complex (MHC)-specific inhibition and prevents bone marrow allograft rejection. J. Exp. Med. 184: 2037-2041.
15. Ioannidis, V., J. Zimmer, F. Beermann, and W. Held. 2001. Cre recombinase-mediated inactivation of H-2Dd transgene expression: evidence for partial missing self-recognition by Ly49A NK cells. J. Immunol. 167: 6256-6262. (Pubitemid 33081555)
16. Pircher, H., T. W. Mak, R. Lang, W. Ballhausen, E. Rüedi, H. Hengartner, R. M. Zinkernagel, and K. Bürki. 1989. T cell tolerance to Mlsa encoded antigens in T cell receptor V beta 8.1 chain transgenic mice. EMBO J. 8: 719-727. (Pubitemid 19273242)
17. Wilson, A., and H. R. MacDonald. 1998. A limited role for beta-selection during gamma delta T cell development. J. Immunol. 161: 5851-5854.
18. Aoki, N., S. Kimura, Y. Takiyama, Y. Atsuta, A. Abe, K. Sato, and M. Katagiri. 2000. The role of the DAP12 signal in mouse myeloid differentiation. J. Immunol. 165: 3790-3796.
19. Ortaldo, J. R., R. Winkler-Pickett, A. T. Mason, and L. H. Mason. 1998. The Ly-49 family: regulation of cytotoxicity and cytokine production in murine CD3+ cells. J. Immunol. 160: 1158-1165.
20. Mason, L. H., S. K. Anderson, W. M. Yokoyama, H. R. Smith, R. Winkler-Pickett, and J. R. Ortaldo. 1996. The Ly-49D receptor activates murine natural killer cells. J. Exp. Med. 184: 2119-2128.
21. Smith, K. M., J. Wu, A. B. Bakker, J. H. Phillips, and L. L. Lanier. 1998. Ly-49D and Ly-49H associate with mouse DAP12 and form activating receptors. J. Immunol. 161: 7-10.
22. Lanier, L. L., B. C. Corliss, J. Wu, C. Leong, and J. H. Phillips. 1998. Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 391: 703-707.
23. Snyder, M. R., M. Lucas, E. Vivier, C. M. Weyand, and J. J. Goronzy. 2003. Selective activation of the c-Jun NH2-terminal protein kinase signaling pathway by stimulatory KIR in the absence of KARAP/DAP12 in CD4+ T cells. J. Exp. Med. 197: 437-449.
24. Nakamura, M. C., P. A. Linnemeyer, E. C. Niemi, L. H. Mason, J. R. Ortaldo, J. C. Ryan, and W. E. Seaman. 1999. Mouse Ly-49D recognizes H-2Dd and activates natural killer cell cytotoxicity. J. Exp. Med. 189: 493-500.
25. Azzam, H. S., A. Grinberg, K. Lui, H. Shen, E. W. Shores, and P. E. Love. 1998. CD5 expression is developmentally regulated by T cell receptor (TCR) signals and TCR avidity. J. Exp. Med. 188: 2301-2311.
26. Kassiotis, G., R. Zamoyska, and B. Stockinger. 2003. Involvement of avidity for major histocompatibility complex in homeostasis of naive and memory T cells. J. Exp. Med. 197: 1007-1016.
27. Ortaldo, J. R., R. Winkler-Pickett, J. Willette-Brown, R. L. Wange, S. K. Anderson, G. J. Palumbo, L. H. Mason, and D. W. McVicar. 1999. Structure/function relationship of activating Ly-49D and inhibitory Ly-49G2 NK receptors. J. Immunol. 163: 5269-5277.
28. Coudert, J. D., L. Scarpellino, F. Gros, E. Vivier, and W. Held. 2008. Sustained NKG2D engagement induces cross-tolerance of multiple distinct NK cell activation pathways. Blood 111: 3571-3578.
29. Orr, M. T., J. C. Sun, D. G. Hesslein, H. Arase, J. H. Phillips, T. Takai, and L. L. Lanier. 2009. Ly49H signaling through DAP10 is essential for optimal natural killer cell responses to mouse cytomegalovirus infection. J. Exp. Med. 206: 807-817.
30. Mehta, I. K., H. R. Smith, J. Wang, D. H. Margulies, and W. M. Yokoyama. 2001. A "chimeric" C57l-derived Ly49 inhibitory receptor resembling the Ly49D activation receptor. Cell. Immunol. 209: 29-41.
31. Scarpellino, L., F. Oeschger, P. Guillaume, J. D. Coudert, F. Lévy, G. Leclercq, and W. Held. 2007. Interactions of Ly49 family receptors with MHC class I ligands in trans and cis. J. Immunol. 178: 1277-1284. (Pubitemid 46154597)
32. Flamand, V., E. W. Shores, T. Tran, K. Huang, E. Lee, A. Grinberg, J. P. Kinet, and P. E. Love. 1996. Delayed maturation of CD4- CD8- Fc gamma RII/III+ T and natural killer cell precursors in Fc epsilon RI gamma transgenic mice. J. Exp. Med. 184: 1725-1735.
33. Lucas, M., L. Daniel, E. Tomasello, S. Guia, N. Horschowski, N. Aoki, D. Figarella-Branger, S. Gomez, and E. Vivier. 2002. Massive inflammatory syndrome and lymphocytic immunodeficiency in KARAP/DAP12-transgenic mice. Eur. J. Immunol. 32: 2653-2663.
34. Levelt, C. N., P. Mombaerts, A. Iglesias, S. Tonegawa, and K. Eichmann. 1993. Restoration of early thymocyte differentiation in T-cell receptor beta-chain-deficient mutant mice by transmembrane signaling through CD3 epsilon. Proc. Natl. Acad. Sci. USA 90: 11401-11405.
35. Shinkai, Y., and F. W. Alt. 1994. CD3 epsilon-mediated signals rescue the development of CD4+CD8+ thymocytes in RAG-2-/- mice in the absence of TCR beta chain expression. Int. Immunol. 6: 995-1001.
36. Mombaerts, P., S. J. Anderson, R. M. Perlmutter, T. W. Mak, and S. Tonegawa. 1994. An activated lck transgene promotes thymocyte development in RAG-1 mutant mice. Immunity 1: 261-267.
37. Fehling, H. J., B. M. Iritani, A. Krotkova, K. A. Forbush, C. Laplace, R. M. Perlmutter, and H. von Boehmer. 1997. Restoration of thymopoiesis in pT alpha-/- mice by anti-CD3epsilon antibody treatment or with transgenes encoding activated Lck or tailless pT alpha. Immunity 6: 703-714. (Pubitemid 27305733)
38. Williams, J. A., K. S. Hathcock, D. Klug, Y. Harada, B. Choudhury, J. P. Allison, R. Abe, and R. J. Hodes. 2005. Regulated costimulation in the thymus is critical for T cell development: dysregulated CD28 costimulation can bypass the pre-TCR checkpoint. J. Immunol. 175: 4199-4207.
39. Aifantis, I., F. Gounari, L. Scorrano, C. Borowski, and H. von Boehmer. 2001. Constitutive pre-TCR signaling promotes differentiation through Ca2+ mobilization and activation of NF-kappaB and NFAT. Nat. Immunol. 2: 403-409.
40. 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.
41. Surh, C. D., and J. Sprent. 2000. Homeostatic T cell proliferation: how far can T cells be activated to self-ligands? J. Exp. Med. 192: F9-F14.