Education of murine NK cells requires both cis and trans recognition of MHC class I molecules

Journal of Immunology

Volumn 191, Issue 10, 2013, Pages 5044-5051

  Bessoles, Stéphanie ^a,d   Angelov, Georgi S ^a   Back, Jonathan ^a,e   Leclercq, Georges ^b   Vivier, Eric ^c   Held, Werner ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b GHENT UNIVERSITY   (Belgium)

^c CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^d PSL RESEARCH UNIVERSITY   (France)

^e Glenmark Pharmaceuticals   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL RECEPTOR; H2 ANTIGEN; HLA ANTIGEN CLASS 1; KLRA1 PROTEIN, MOUSE; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ARTICLE; CELL INTERACTION; CELL TRANSFER; CIS ISOMER; CONTROLLED STUDY; IN VIVO STUDY; LYMPHOCYTE FUNCTION; MOLECULAR RECOGNITION; MOUSE; NATURAL KILLER CELL; NATURAL KILLER CELL EDUCATION; NONHUMAN; PRIORITY JOURNAL; STEADY STATE; T LYMPHOCYTE; TRANS ISOMER; ADOPTIVE TRANSFER; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; GENETICS; IMMUNOLOGY; METABOLISM; TRANSGENIC MOUSE;

ADOPTIVE TRANSFER; ANIMALS; CELL LINE; H-2 ANTIGENS; HISTOCOMPATIBILITY ANTIGENS CLASS I; KILLER CELLS, NATURAL; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY A;

EID: 84887463670     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301971     Document Type: Article

References (39)

1. Ljunggren, H. G., and K. Kärre. 1990. In search of the 'missing self': MHC molecules and NK cell recognition. Immunol. Today 11:237-244.
2. Lanier, L. L. 2005. NK cell recognition. Annu. Rev. Immunol. 23:225-274.
3. Held, W., J. R. Dorfman, M.-F. Wu, and D. H. Raulet. 1996. Major histocompatibility complex class I-dependent skewing of the natural killer cell Ly49 receptor repertoire. Eur. J. Immunol. 26:2286-2292.
4. Held, W., and D. H. Raulet. 1997. Ly49A transgenic mice provide evidence for a major histocompatibility complex-dependent education process in natural killer cell development. J. Exp. Med. 185:2079-2088.
5. Guia, S., B. N. Jaeger, S. Piatek, S. Mailfert, T. Trombik, A. Fenis, N. Chevrier, T. Walzer, Y. M. Kerdiles, D. Marguet, et al. 2011. Confinement of activating receptors at the plasma membrane controls natural killer cell tolerance. Sci. Signal. 4:ra21.
6. Fernandez, N. C., E. Treiner, R. E. Vance, A. M. Jamieson, S. Lemieux, and D. H. Raulet. 2005. A subset of natural killer cells achieves self-tolerance without expressing inhibitory receptors specific for self-MHC molecules. Blood 105:4416-4423.
7. Kim, S., J. Poursine-Laurent, S. M. Truscott, L. Lybarger, Y. J. Song, L. Yang, A. R. French, J. B. Sunwoo, S. Lemieux, T. H. Hansen, and W. M. Yokoyama. 2005. Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 436:709-713.
8. Anfossi, N., P. André, S. Guia, C. S. Falk, S. Roetynck, C. A. Stewart, V. Breso, C. Frassati, D. Reviron, D. Middleton, et al. 2006. Human NK cell education by inhibitory receptors for MHC class I. Immunity 25:331-342.
9. Chalifour, A., L. Scarpellino, J. Back, P. Brodin, E. Devèvre, F. Gros, F. Lévy, G. Leclercq, P. Höglund, F. Beermann, and W. Held. 2009. A Role for cis interaction between the Inhibitory Ly49A receptor and MHC class I for natural killer cell education. Immunity 30:337-347.
10. Elliott, J. M., and W. M. Yokoyama. 2011. Unifying concepts of MHC-dependent natural killer cell education. Trends Immunol. 32:364-372.
11. Raulet, D. H. 2006. Missing self recognition and self tolerance of natural killer (NK) cells. Semin. Immunol. 18:145-150.
12. Höglund, P., and P. Brodin. 2010. Current perspectives of natural killer cell education by MHC class I molecules. Nat. Rev. Immunol. 10:724-734.
13. Raulet, D. H., and R. E. Vance. 2006. Self-tolerance of natural killer cells. Nat. Rev. Immunol. 6:520-531.
14. Doucey, M. A., L. Scarpellino, J. Zimmer, P. Guillaume, I. F. Luescher, C. Bron, and W. Held. 2004. Cis association of Ly49A with MHC class I restricts natural killer cell inhibition. Nat. Immunol. 5:328-336.
15. 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.
16. Masuda, A., A. Nakamura, T. Maeda, Y. Sakamoto, and T. Takai. 2007. Cis binding between inhibitory receptors and MHC class I can regulate mast cell activation. J. Exp. Med. 204:907-920.
17. Li, N. L., L. Fu, H. Uchtenhagen, A. Achour, and D. N. Burshtyn. 2013. Cis association of leukocyte Ig-like receptor 1 with MHC class I modulates accessibility to antibodies and HCMV UL18. Eur. J. Immunol. 43:1042-1052.
18. Joncker, N. T., N. Shifrin, F. Delebecque, and D. H. Raulet. 2010. Mature natural killer cells reset their responsiveness when exposed to an altered MHC environment. J. Exp. Med. 207:2065-2072.
19. Elliott, J. M., J. A. Wahle, and W. M. Yokoyama. 2010. MHC class I-deficient natural killer cells acquire a licensed phenotype after transfer into an MHC class I-sufficient environment. J. Exp. Med. 207:2073-2079.
20. Ioannidis, V., J. Zimmer, F. Beermann, and W. Held. 2001. Cre recombinasemediated inactivation of H-2Dd transgene expression: evidence for partial missing self-recognition by Ly49A NK cells. J. Immunol. 167:6256-6262.
21. Lee, P. P., D. R. Fitzpatrick, C. Beard, H. K. Jessup, S. Lehar, K. W. Makar, M. Pérez-Melgosa, M. T. Sweetser, M. S. Schlissel, S. Nguyen, et al. 2001. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15:763-774.
22. Narni-Mancinelli, E., J. Chaix, A. Fenis, Y. M. Kerdiles, N. Yessaad, A. Reynders, C. Gregoire, H. Luche, S. Ugolini, E. Tomasello, et al. 2011. Fate mapping analysis of lymphoid cells expressing the NKp46 cell surface receptor. Proc. Natl. Acad. Sci. USA 108:18324-18329.
23. Held, W., J. Roland, and D. H. Raulet. 1995. Allelic exclusion of Ly49-family genes encoding class I MHC-specific receptors on NK cells. Nature 376:355-358.
24. 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 Vb8.1 chain transgenic mice. EMBO J. 8:719-727.
25. Van Beneden, K., F. Stevenaert, A. De Creus, V. Debacker, J. De Boever, J. Plum, and G. Leclercq. 2001. Expression of Ly49E and CD94/NKG2 on fetal and adult NK cells. J. Immunol. 166:4302-4311.
26. Soderquest, K., T. Walzer, B. Zafirova, L. S. Klavinskis, B. Polić, E. Vivier, G. M. Lord, and A. Martín-Fontecha. 2011. Cutting edge: CD8+ T cell priming in the absence of NK cells leads to enhanced memory responses. J. Immunol. 186:3304-3308.
27. Waggoner, S. N., R. T. Taniguchi, P. A. Mathew, V. Kumar, and R. M. Welsh. 2010. Absence of mouse 2B4 promotes NK cell-mediated killing of activated CD8+ T cells, leading to prolonged viral persistence and altered pathogenesis. J. Clin. Invest. 120:1925-1938.
28. Zimmer, J., V. Ioannidis, and W. Held. 2001. H-2D ligand expression by Ly49A+ natural killer (NK) cells precludes ligand uptake from environmental cells: implications for NK cell function. J. Exp. Med. 194:1531-1539.
29. Back, J., E. L. Malchiodi, S. Cho, L. Scarpellino, P. Schneider, M. C. Kerzic, R. A. Mariuzza, and W. Held. 2009. Distinct conformations of Ly49 natural killer cell receptors mediate MHC class I recognition in trans and cis. Immunity 31:598-608.
30. Treanor, B., P. M. Lanigan, S. Kumar, C. Dunsby, I. Munro, E. Auksorius, F. J. Culley, M. A. Purbhoo, D. Phillips, M. A. Neil, et al. 2006. Microclusters of inhibitory killer immunoglobulin-like receptor signaling at natural killer cell immunological synapses. J. Cell Biol. 174:153-161.
31. Choudhuri, K., D. Wiseman, M. H. Brown, K. Gould, and P. A. Van Der Merwe. 2005. T-cell receptor triggering is critically dependent on the dimensions of its peptide-MHC ligand. Nature 436:578-582.
32. Velikovsky, C. A., L. Deng, L. K. Chlewicki, M. M. Fernández, V. Kumar, and R. A. Mariuzza. 2007. Structure of natural killer receptor 2B4 bound to CD48 reveals basis for heterophilic recognition in signaling lymphocyte activation molecule family. Immunity 27:572-584.
33. Joncker, N. T., N. C. Fernandez, E. Treiner, E. Vivier, and D. H. Raulet. 2009. NK cell responsiveness is tuned commensurate with the number of inhibitory receptors for self-MHC class I: the rheostat model. J. Immunol. 182:4572-4580.
34. Wu, M.-F., and D. H. Raulet. 1997. Class I-deficient hemopoietic cells and nonhemopoietic cells dominantly induce unresponsiveness of natural killer cells to class I-deficient bone marrow cell grafts. J. Immunol. 158:1628-1633.
35. Johansson, M. H., C. Bieberich, G. Jay, K. Kärre, and P. Höglund. 1997. Natural killer cell tolerance in mice with mosaic expression of major histocompatibility complex class I transgene. J. Exp. Med. 186:353-364.
36. Sjöström, A., M. Eriksson, C. Cerboni, M. H. Johansson, C. L. Sentman, K. Kärre, and P. Höglund. 2001. Acquisition of external major histocompatibility complex class I molecules by natural killer cells expressing inhibitory Ly49 receptors. J. Exp. Med. 194:1519-1530.
37. Ruggeri, L., M. Capanni, M. Casucci, I. Volpi, A. Tosti, K. Perruccio, E. Urbani, R. S. Negrin, M. F. Martelli, and A. Velardi. 1999. Role of natural killer cell alloreactivity in HLA-mismatched hematopoietic stem cell transplantation. Blood 94:333-339.
38. Ruggeri, L., M. Capanni, E. Urbani, K. Perruccio, W. D. Shlomchik, A. Tosti, S. Posati, D. Rogaia, F. Frassoni, F. Aversa, et al. 2002. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295:2097-2100.
39. Pende, D., S. Marcenaro, M. Falco, S. Martini, M. E. Bernardo, D. Montagna, E. Romeo, C. Cognet, M. Martinetti, R. Maccario, et al. 2009. Anti-leukemia activity of alloreactive NK cells in KIR ligand-mismatched haploidentical HSCT for pediatric patients: evaluation of the functional role of activating KIR and redefinition of inhibitory KIR specificity. Blood 113:3119-3129.