The Ly49 gene family. A brief guide to the nomenclature, genetics, and role in intracellular infection

Frontiers in Immunology

Volumn 4, Issue APR, 2013, Pages

  Schenkel, Alan Rowe ^a   Kingry, Luke C ^a,b   Slayden, Richard A ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

Author keywords

Klra; Ly49; Myeloid cells; Natural killer lymphocytes

Indexed keywords

CD11B ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY A;

GENE; GENE CLUSTER; GENE EXPRESSION; GENOME ANALYSIS; HUMAN; IMMUNE RESPONSE; INFECTION; MICROARRAY ANALYSIS; MULTIGENE FAMILY; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY A GENE; NONHUMAN; PSEUDOGENE; REVIEW; SEQUENCE HOMOLOGY; T LYMPHOCYTE; VIRUS RESISTANCE;

EID: 84883733059     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00090     Document Type: Review

References (62)

1. Arase, H., Mocarski, E. S., Campbell, A. E., Hill, A. B., and Lanier, L. L. (2002). Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 296, 1323-1326.
2. Aust, J. G., Gays, F., Hussain, F., Butcher, G. W., Kist, R., Peters, H., et al. (2011). Mice lacking Ly49E show normal NK cell development and provide evidence for probabilistic expression of Ly49E in NK cells and T cells. J. Immunol. 186, 2013-2023.
3. Back, J., Angelov, G. S., Mariuzza, R. A., and Held, W. (2011). The interaction with H-2Dd in cis is associated with a conformational change in the Ly49A NK cell receptor. Front. Immunol. 2:55. doi:10.3389/fimmu.2011.00055
4. Back, J, Malchiodi, E. L., Cho, S., Scarpellino, L., Schneider, P., Kerzic, M. C., et al. (2009). Distinct conformations of Ly49 natural killer cell receptors mediate MHC class I recognition in trans and cis. Immunity 31, 598-608.
5. Barao, I., Alvarez, M., Ames, E., Orr, M. T., Stefanski, H. E., Blazar, B. R., et al. (2011). Mouse Ly49G2+ NK cells dominate early responses during both immune reconstitution and activation independently of MHC. Blood 117, 7032-7041.
6. Belanger, S., Tai, L. H., Anderson, S. K., and Makrigiannis, A. P. (2008). Ly49 cluster sequence analysis in a mouse model of diabetes: an expanded repertoire of activating receptors in the NOD genome. Genes Immun. 9, 509-521.
7. Bosio, C. M. (2011). The subversion of the immune system by Francisella tularensis. Front. Microbiol. 2:9. doi:10.3389/fmicb.2011.00009
8. Brodin, P, Lakshmikanth, T., Karre, K., and Hoglund, P. (2012). Skewing of the NK cell repertoire by MHC class I via quantitatively controlled enrichment and contraction of specific Ly49 subsets. J. Immunol. 188, 2218-2226.
9. Bryceson, Y. T., and Long, E. O. (2008). Line of attack: NK cell specificity and integration of signals. Curr. Opin. Immunol. 20, 344-352.
10. Chan, P. Y., and Takei, F. (1989). Molecular cloning and characterization of a novel murine T cell surface antigen, YE1/48. J. Immunol. 142, 1727-1736.
11. Cheng, T. P., French, A. R., Plougastel, B. F., Pingel, J. T., Orihuela, M. M., Buller, M. L., et al. (2008). Ly49h is necessary for genetic resistance to murine cytomegalovirus. Immunogenetics 60, 565-573.
12. Corbett, A. J., Coudert, J. D., Forbes, C. A., and Scalzo, A. A. (2011). Functional consequences of natural sequence variation of murine cytomegalovirus m157 for Ly49 receptor specificity and NK cell activation. J. Immunol. 186, 1713-1722.
13. Corral, L., Takizawa, H., Hanke, T., Jamieson, A. M., and Raulet, D. H. (1999). A new monoclonal antibody reactive with several Ly49 NK cell receptors mediates redirected lysis of target cells. Hybridoma 18, 359-366.
14. Dam, J., Guan, R., Natarajan, K., Dimasi, N., Chlewicki, L. K., Kranz, D. M., et al. (2003). Variable MHC class I engagement by Ly49 natural killer cell receptors demonstrated by the crystal structure of Ly49C bound to H-2K(b). Nat. Immunol. 4, 1213-1222.
15. Dimasi, N., and Biassoni, R. (2005). Structural and functional aspects of the Ly49 natural killer cell receptors. Immunol. Cell Biol. 83, 1-8.
16. Dissen, E., Fossum, S., Hoelsbrekken, S. E., and Saether, P. C. (2008). NK cell receptors in rodents and cattle. Semin. Immunol. 20, 369-375.
17. Gays, F., Aust, J. G., Reid, D. M., Falconer, J., Toyama-Sorimachi, N., Taylor, P. R., et al. (2006). Ly49B is expressed on multiple subpopulations of myeloid cells. J. Immunol. 177, 5840-5851.
18. Hajjar, A. M., Harvey, M. D., Shaffer, S. A., Goodlett, D. R., Sjostedt, A., Edebro, H., et al. (2006). Lack of in vitro and in vivo recognition of Francisella tularensis subspecies lipopolysaccharide by Toll-like receptors. Infect. Immun. 74, 6730-6738.
19. Hara, T., Nishimura, H., Hasegawa, Y., and Yoshikai, Y. (2001). Thymus-dependent modulation of Ly49 inhibitory receptor expression on NK1.1+gamma/delta T cells. Immunology 102, 24-30.
20. Hayashi, M., Nakashima, T., Kodama, T., Makrigiannis, A. P., Toyama-Sorimachi, N., and Takayanagi, H. (2010). Ly49Q, an ITIM-bearing NK receptor, positively regulates osteoclast differentiation. Biochem. Biophys. Res. Commun. 393, 432-438.
21. Held, W., and Mariuzza, R. A. (2008). Cis interactions of immunoreceptors with MHC and non-MHC ligands. Nat. Rev. Immunol. 8, 269-278.
22. Held, W., Roland, J., and Raulet, D. H. (1995). Allelic exclusion of Ly49-family genes encoding class I MHC-specific receptors on NK cells. Nature 376, 355-358.
23. Johansson, S., Salmon-Divon, M., Johansson, M. H., Pickman, Y., Brodin, P., Karre, K., et al. (2009). Probing natural killer cell education by Ly49 receptor expression analysis and computational modelling in single MHC class I mice. PLoS ONE 4:e6046. doi:10.1371/journal.pone.0006046
24. Jonsson, A H., Yang, L., Kim, S., Taffner, S. M., and Yokoyama, W. M. (2010). Effects of MHC class I alleles on licensing of Ly49A+ NK cells. J. Immunol. 184, 3424-3432.
25. Kamogawa-Schifter, Y., Ohkawa, J., Namiki, S., Arai, N., Arai, K., and Liu, Y. (2005). Ly49Q defines 2 pDC subsets in mice. Blood 105, 2787-2792.
26. Kielczewska, A., Kim, H. S., Lanier, L. L., Dimasi, N., and Vidal, S. M. (2007). Critical residues at the Ly49 natural killer receptor's homodimer interface determine functional recognition of m157, a mouse cytomegalovirus MHC class I-like protein. J. Immunol. 178, 369-377.
27. Kielczewska, A., Pyzik, M., Sun, T., Krmpotic, A., Lodoen, M. B., Munks, M. W., et al. (2009). Ly49P recognition of cytomegalovirus-infected cells expressing H2-Dk and CMV-encoded m04 correlates with the NK cell antiviral response. J. Exp. Med. 206, 515-523.
28. Kim, H. J., Wang, X., Radfar, S., Sproule, T. J., Roopenian, D. C., and Cantor, H. (2011). CD8+ T regulatory cells express the Ly49 Class I MHC receptor and are defective in autoimmune prone B6-Yaa mice. Proc. Natl. Acad. Sci. U.S.A. 108, 2010-2015.
29. Kim, S., Poursine-Laurent, J., Truscott, S. M., Lybarger, L., Song, Y. J., Yang, L., et al. (2005). Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 436, 709-713.
30. Kingry, L. C., Troyer, R. M., Marlenee, N. L., Bielefeldt-Ohmann, H., Bowen, R. A., Schenkel, A. R., et al. (2011). Genetic identification of unique immunological responses in mice infected with virulent and attenuated Francisella tularensis. Microbes Infect. 13, 261-275.
31. Lavender, K. J., and Kane, K. P. (2006). Cross-species dependence of Ly49 recognition on the supertype defining B-pocket of a class I MHC molecule. J. Immunol. 177, 8578-8586.
32. Lee, S. H., Girard, S., Macina, D., Busa, M., Zafer, A., Belouchi, A., et al. (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.
33. Loch, S., and Tampe, R. (2005). Viral evasion of the MHC class I antigen-processing machinery. Pflugers Arch. 451, 409-417.
34. Lowin-Kropf, B., Kunz, B., Beermann, F., and Held, W. (2000). Impaired natural killing of MHC class I-deficient targets by NK cells expressing a catalytically inactive form of SHP-1. J. Immunol. 165, 1314-1321.
35. Makrigiannis, A. P., and Anderson, S. K. (2000). Ly49 gene expression in different inbred mouse strains. Immunol. Res. 21, 39-47.
36. Makrigiannis, A. P., Gosselin, P., Mason, L. H., Taylor, L. S., McVicar, D. W., Ortaldo, J. R., et al. (1999). Cloning and characterization of a novel activating Ly49 closely related to Ly49A. J. Immunol. 163, 4931-4938.
37. Makrigiannis, A. P., Pau, A. T., Saleh, A., Winkler-Pickett, R., Ortaldo, J. R., and Anderson, S. K. (2001). Class I MHC-binding characteristics of the 129/J Ly49 repertoire. J. Immunol. 166, 5034-5043.
38. Makrigiannis, A. P., Pau, A. T., Schwartzberg, P. L., McVicar, D. W., Beck, T. W., and Anderson, S. K. (2002). A BAC contig map of the Ly49 gene cluster in 129 mice reveals extensive differences in gene content relative to C57BL/6 mice. Genomics 79, 437-444.
39. Martin, A. M., Freitas, E. M., Witt, C. S., and Christiansen, F. T. (2000). The genomic organization and evolution of the natural killer immunoglobulin-like receptor (KIR) gene cluster. Immunogenetics 51, 268-280.
40. Mehta, I. K., Smith, H. R., Wang, J., Margulies, D. H., and Yokoyama, W. M. (2001). A "chimeric" C57l-derived Ly49 inhibitory receptor resembling the Ly49D activation receptor. Cell. Immunol. 209, 29-41.
41. Middleton, D., and Gonzelez, F. (2010). The extensive polymorphism of KIR genes. Immunology 129, 8-19.
42. Nylenna, O., Naper, C., Vaage, J. T., Woon, P. Y., Gauguier, D., Dissen, E., et al. (2005). The genes and gene organization of the Ly49 region of the rat natural killer cell gene complex. Eur. J. Immunol. 35, 261-272.
43. Orr, M. T., Edelmann, K. H., Vieira, J., Corey, L., Raulet, D. H., and Wilson, C. B. (2005). Inhibition of MHC class I is a virulence factor in herpes simplex virus infection of mice. PLoS Pathog. 1:e7. doi:10.1371/journal.ppat.0010007
44. Orr, M T., and Lanier, L. L. (2011). Inhibitory Ly49 receptors on mouse natural killer cells. Curr. Top. Microbiol. Immunol. 350, 67-87.
45. Ortaldo, J. R., Winkler-Pickett, R., Mason, A. T., and Mason, L. H. (1998). The Ly-49 family: regulation of cytotoxicity and cytokine production in murine CD3+ cells. J. Immunol. 160, 1158-1165.
46. Roland, J., Soulard, V., Sellier, C., Drapier, A. M., Di Santo, J. P., Cazenave, P. A., et al. (2006). NK cell responses to Plasmodium infection and control of intrahepatic parasite development. J. Immunol. 177, 1229-1239.
47. Scarpellino, L., Oeschger, F., Guillaume, P., Coudert, J. D., Levy, F., Leclercq, G., et al. (2007). Interactions of Ly49 family receptors with MHC class I ligands in trans and cis. J. Immunol. 178, 1277-1284.
48. Shegarfi, H., Sydnes, K., Lovik, M., Inngjerdingen, M., Rolstad, B., and Naper, C. (2009). The role of natural killer cells in resistance to the intracellular bacterium Listeria monocytogenes in rats. Scand. J. Immunol. 70, 238-244.
49. Smith, H. R., Karlhofer, F. M., and Yokoyama, W. M. (1994). Ly-49 multigene family expressed by IL-2-activated NK cells. J. Immunol. 153, 1068-1079.
50. Sun, J. C., Beilke, J. N., and Lanier, L. L. (2009). Adaptive immune features of natural killer cells. Nature 457, 557-561.
51. Tassi, I., Le Friec, G., Gilfillan, S., Takai, T., Yokoyama, W. M., and Colonna, M. (2009). DAP10 associates with Ly49 receptors but contributes minimally to their expression and function in vivo. Eur. J. Immunol. 39, 1129-1135.
52. Tay, C. H., Yu, L. Y., Kumar, V., Mason, L., Ortaldo, J. R., and Welsh, R. M. (1999). The role of LY49 NK cell subsets in the regulation of murine cytomegalovirus infections. J. Immunol. 162, 718-726.
53. Temme, S., Eis-Hubinger, A. M., McLellan, A. D., and Koch, N. (2010). The herpes simplex virus-1 encoded glycoprotein B diverts HLA-DR into the exosome pathway. J. Immunol. 184, 236-243.
54. To, K., Agrotis, A., Besra, G., Bobik, A., and Toh, B. H. (2009). NKT cell subsets mediate differential proatherogenic effects in ApoE-/- mice. Arterioscler. Thromb. Vasc. Biol. 29, 671-677.
55. Toma-Hirano, M., Namiki, S., Shibata, Y., Ishida, K., Arase, H., Miyatake, S., et al. (2009). Ly49Q ligand expressed by activated B cells induces plasmacytoid DC maturation. Eur. J. Immunol. 39, 1344-1352.
56. Toyama-Sorimachi, N., Tsujimura, Y., Maruya, M., Onoda, A., Kubota, T., Koyasu, S., et al. (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. U.S.A. 101, 1016-1021.
57. Van Beneden, K., De Creus, A., Stevenaert, F., Debacker, V., Plum, J., and Leclercq, G. (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.
58. Van Beneden, K., Stevenaert, F., De Creus, A., Debacker, V., De Boever, J., Plum, J., et al. (2001). Expression of Ly49E and CD94/NKG2 on fetal and adult NK cells. J. Immunol. 166, 4302-4311.
59. Van Den Broeck, T., Stevenaert, F., Taveirne, S., Debacker, V., Vangestel, C., Vandekerckhove, B., et al. (2008). Ly49E-dependent inhibition of natural killer cells by urokinase plasminogen activator. Blood 112, 5046-5051.
60. Yokoyama, W. M., Jacobs, L. B., Kanagawa, O., Shevach, E. M., and Cohen, D. I. (1989). A murine T lymphocyte antigen belongs to a supergene family of type II integral membrane proteins. J. Immunol. 143, 1379-1386.
61. Yokoyama, W. M., Kehn, P. J., Cohen, D. I., and Shevach, E. M. (1990). Chromosomal location of the Ly-49 (A1, YE1/48) multigene family. Genetic association with the NK 1.1 antigen. J. Immunol. 145, 2353-2358.
62. Yokoyama, W. M., and Seaman, W. E. (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.