Mice lacking Ly49E show normal NK cell development and provide evidence for probabilistic expression of Ly49E in NK cells and T cells

Journal of Immunology

Volumn 186, Issue 4, 2011, Pages 2013-2023

  Aust, Jonathan G ^a   Gays, Frances ^a   Hussain, Farhana ^a   Butcher, Geoffrey W ^b   Kist, Ralf ^b,c   Peters, Heiko ^d   Brooks, Colin G ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b BABRAHAM INSTITUTE   (United Kingdom)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 2; LY49E PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY A; NATURAL KILLER CELL RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL GROWTH; CELL MATURATION; CONTROLLED STUDY; EPITHELIUM CELL; GENE DISRUPTION; GENE LOCUS; HETEROZYGOTE; INTERFERON PRODUCTION; LYMPHOCYTE SUBPOPULATION; MALE; MOUSE; MULTIGENE FAMILY; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROBABILITY; PROTEIN EXPRESSION; SPLEEN CELL; T LYMPHOCYTE; TRANSGENE;

ANIMALS; CELL AGING; CELL DIFFERENTIATION; CELLS, CULTURED; GENE EXPRESSION REGULATION; GENE KNOCK-IN TECHNIQUES; KILLER CELLS, NATURAL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY A; T-LYMPHOCYTES;

EID: 79951826878     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003698     Document Type: Article

References (44)

1. Yokoyama, W. M., and W. E. Seaman. 1993. The Ly-49 and NKR-P1 gene families encoding lectin-like receptors on natural killer cells: the NK gene complex. Annu. Rev. Immunol. 11: 613-635.
2. Yokoyama, W. M., and B. F. Plougastel. 2003. Immune functions encoded by the natural killer gene complex. Nat. Rev. Immunol. 3: 304-316.
3. Carlyle, J. R., A. Mesci, J. H. Fine, P. Chen, S. Bélanger, L. H. Tai, and A. P. Makrigiannis. 2008. Evolution of the Ly49 and Nkrp1 recognition systems. Semin. Immunol. 20: 321-330.
4. Toyama-Sorimachi, N., Y. Tsujimura, M. Maruya, A. Onoda, T. Kubota, S. Koyasu, K. Inaba, and H. Karasuyama. 2004. Ly49Q, a member of the Ly49 family that is selectively expressed on myeloid lineage cells and involved in regulation of cytoskeletal architecture. Proc. Natl. Acad. Sci. USA 101: 1016-1021.
5. Gays, F., J. G. Aust, D. M. Reid, J. Falconer, N. Toyama-Sorimachi, P. R. Taylor, and C. G. Brooks. 2006. Ly49B is expressed on multiple subpopulations of myeloid cells. J. Immunol. 177: 5840-5851.
6. Raulet, D. H., W. Held, I. Correa, J. R. Dorfman, M. F. Wu, and L. Corral. 1997. Specificity, tolerance and developmental regulation of natural killer cells defined by expression of class I-specific Ly49 receptors. Immunol. Rev. 155: 41-52.
7. Takei, F., K. L. McQueen, M. Maeda, B. T. Wilhelm, S. Lohwasser, R. H. Lian, and D. L. Mager. 2001. Ly49 and CD94/NKG2: developmentally regulated expression and evolution. Immunol. Rev. 181: 90-103.
8. Kärre, K. 2002. NK cells, MHC class I molecules and the missing self. Scand. J. Immunol. 55: 221-228.
9. Kane, K. P., E. T. Silver, and B. Hazes. 2001. Specificity and function of activating Ly-49 receptors. Immunol. Rev. 181: 104-114.
10. Toomey, J. A., S. Shrestha, S. A. de la Rue, F. Gays, J. H. Robinson, Z. M. Chrzanowska-Lightowlers, and C. G. Brooks. 1998. MHC class I expression protects target cells from lysis by Ly49-deficient fetal NK cells. Eur. J. Immunol. 28: 47-56.
11. Van Beneden, K., A. De Creus, V. Debacker, J. De Boever, J. Plum, and G. Leclercq. 1999. Murine fetal natural killer cells are functionally and structurally distinct from adult natural killer cells. J. Leukoc. Biol. 66: 625-633.
12. Fraser, K. P., F. Gays, J. H. Robinson, K. van Beneden, G. Leclercq, R. E. Vance, D. H. Raulet, and C. G. Brooks. 2002. NK cells developing in vitro from fetal mouse progenitors express at least one member of the Ly49 family that is acquired in a time-dependent and stochastic manner independently of CD94 and NKG2. Eur. J. Immunol. 32: 868-878.
13. Stevenaert, F., K. Van Beneden, A. De Creus, V. Debacker, J. Plum, and G. Leclercq. 2003. Ly49E expression points toward overlapping, but distinct, natural killer (NK) cell differentiation kinetics and potential of fetal versus adult lymphoid progenitors. J. Leukoc. Biol. 73: 731-738.
14. Gays, F., K. Martin, R. Kenefeck, J. G. Aust, and C. G. Brooks. 2005. Multiple cytokines regulate the NK gene complex-encoded receptor repertoire of mature NK cells and T cells. J. Immunol. 175: 2938-2947.
15. Van Beneden, K., A. De Creus, F. Stevenaert, V. Debacker, J. Plum, and G. Leclercq. 2002. Expression of inhibitory receptors Ly49E and CD94/NKG2 on fetal thymic and adult epidermal TCR V gamma 3 lymphocytes. J. Immunol. 168: 3295-3302. (Pubitemid 34250391)
16. Hanke, T., H. Takizawa, C. W. McMahon, D. H. Busch, E. G. Pamer, J. D. Miller, J. D. Altman, Y. Liu, D. Cado, F. A. Lemonnier, et al. 1999. Direct assessment of MHC class I binding by seven Ly49 inhibitory NK cell receptors. Immunity 11: 67-77. (Pubitemid 29359958)
17. 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)
18. Van Den Broeck, T., F. Stevenaert, S. Taveirne, V. Debacker, C. Vangestel, B. Vandekerckhove, T. Taghon, P. Matthys, J. Plum, W. Held, et al. 2008. Ly49E-dependent inhibition of natural killer cells by urokinase plasminogen activator. Blood 112: 5046-5051.
19. Brodin, P., K. Kärre, and P. Höglund. 2009. NK cell education: not an on-off switch but a tunable rheostat. Trends Immunol. 30: 143-149.
20. Jonsson, A. H., and W. M. Yokoyama. 2009. Natural killer cell tolerance licensing and other mechanisms. Adv. Immunol. 101: 27-79.
21. Orr, M. T., and L. L. Lanier. 2010. Natural killer cell education and tolerance. Cell 142: 847-856.
22. Friedrich, G., and P. Soriano. 1991. Promoter traps in embryonic stem cells: a genetic screen to identify and mutate developmental genes in mice. Genes Dev. 5: 1513-1523. (Pubitemid 21906058)
23. Conrad, M., M. Brielmeier, W. Wurst, and G. W. Bornkamm. 2003. Optimized vector for conditional gene targeting in mouse embryonic stem cells. Biotechniques 34: 1136-1138, 1140.
24. Rodríguez, C. I., F. Buchholz, J. Galloway, R. Sequerra, J. Kasper, R. Ayala, A. F. Stewart, and S. M. Dymecki. 2000. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat. Genet. 25: 139-140.
25. Aust, J. G., F. Gays, K. M. Mickiewicz, E. Buchanan, and C. G. Brooks. 2009. The expression and function of the NKRP1 receptor family in C57BL/6 mice. J. Immunol. 183: 106-116.
26. Toomey, J. A., M. Salcedo, L. A. Cotterill, M. M. Millrain, Z. Chrzanowska-Lightowlers, J. Lawry, K. Fraser, F. Gays, J. H. Robinson, S. Shrestha, et al. 1999. Stochastic acquisition of Qa1 receptors during the development of fetal NK cells in vitro accounts in part but not in whole for the ability of these cells to distinguish between class I-sufficient and class I-deficient targets. J. Immunol. 163: 3176-3184. (Pubitemid 29431817)
27. Brooks, C. G., A. Georgiou, and R. K. Jordan. 1993. The majority of immature fetal thymocytes can be induced to proliferate to IL-2 and differentiate into cells indistinguishable from mature natural killer cells. J. Immunol. 151: 6645-6656.
28. Brooks, C. G. 2000. Cloning and culturing of fetal mouse natural killer cells. Methods Mol. Biol. 121: 13-24.
29. Truett, G. E., P. Heeger, R. L. Mynatt, A. A. Truett, J. A. Walker, and M. L. Warman. 2000. Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotechniques 29: 52, 54.
30. Brown, M. G., A. O. Dokun, J. W. Heusel, H. R. Smith, D. L. Beckman, E. A. Blattenberger, C. E. Dubbelde, L. R. Stone, A. A. Scalzo, and W. M. Yokoyama. 2001. Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 292: 934-937.
31. Lee, S. H., S. Girard, D. Macina, M. Busa, A. Zafer, A. Belouchi, P. Gros, and S. M. Vidal. 2001. Susceptibility to mouse cytomegalovirus is associated with deletion of an activating natural killer cell receptor of the C-type lectin superfamily. Nat. Genet. 28: 42-45.
32. Tai, L. H., M. L. Goulet, S. Belanger, N. Toyama-Sorimachi, N. Fodil-Cornu, S. M. Vidal, A. D. Troke, D. W. McVicar, and A. P. Makrigiannis. 2008. Positive regulation of plasmacytoid dendritic cell function via Ly49Q recognition of class I MHC. J. Exp. Med. 205: 3187-3199.
33. Sasawatari, S., M. Yoshizaki, C. Taya, A. Tazawa, K. Furuyama-Tanaka, H. Yonekawa, T. Dohi, A. P. Makrigiannis, T. Sasazuki, K. Inaba, and N. Toyama-Sorimachi. 2010. The Ly49Q receptor plays a crucial role in neutrophil polarization and migration by regulating raft trafficking. Immunity 32:200-213.
34. Hayashi, M., T. Nakashima, T. Kodama, A. P. Makrigiannis, N. Toyama-Sorimachi, and H. Takayanagi. 2010. Ly49Q, an ITIM-bearing NK receptor, positively regulates osteoclast differentiation. Biochem. Biophys. Res. Commun. 393: 432-438.
35. Fodil-Cornu, N., S. H. Lee, S. Belanger, A. P. Makrigiannis, C. A. Biron, R. M. Buller, and S. M. Vidal. 2008. Ly49h-deficient C57BL/6 mice: a new mouse cytomegalovirus-susceptible model remains resistant to unrelated pathogens controlled by the NK gene complex. J. Immunol. 181: 6394-6405.
36. 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.
37. Held, W., and D. H. Raulet. 1997. Expression of the Ly49A gene in murine natural killer cell clones is predominantly but not exclusively mono-allelic. Eur. J. Immunol. 27: 2876-2884.
38. Held, W., and B. Kunz. 1998. An allele-specific, stochastic gene expression process controls the expression of multiple Ly49 family genes and generates a diverse, MHC-specific NK cell receptor repertoire. Eur. J. Immunol. 28: 2407-2416.
39. Tanamachi, D. M., T. Hanke, H. Takizawa, A. M. Jamieson, and D. R. Raulet. 2001. Expression of natural killer receptor alleles at different Ly49 loci occurs independently and is regulated by major histocompatibility complex class I molecules. J. Exp. Med. 193: 307-315.
40. Makrigiannis, A. P., E. Rousselle, and S. K. Anderson. 2004. Independent control of Ly49g alleles: implications for NK cell repertoire selection and tumor cell killing. J. Immunol. 172: 1414-1425.
41. Rouhi, A., C. B. Lai, T. P. Cheng, F. Takei, W. M. Yokoyama, and D. L. Mager. 2009. Evidence for high bi-allelic expression of activating Ly49 receptors. Nucleic Acids Res. 37: 5331-5342.
42. Le Hir, H., A. Nott, and M. J. Moore. 2003. How introns influence and enhance eukaryotic gene expression. Trends Biochem. Sci. 28: 215-220.
43. Wilhelm, B. T., K. L. McQueen, J. D. Freeman, F. Takei, and D. L. Mager. 2001. Comparative analysis of the promoter regions and transcriptional start sites of mouse Ly49 genes. Immunogenetics 53: 215-224.
44. Saleh, A., G. E. Davies, V. Pascal, P. W. Wright, D. L. Hodge, E. H. Cho, S. J. Lockett, M. Abshari, and S. K. Anderson. 2004. Identification of probabilistic transcriptional switches in the Ly49 gene cluster: a eukaryotic mechanism for selective gene activation. Immunity 21: 55-66.