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

European Journal of Immunology

Volumn 28, Issue 8, 1998, Pages 2407-2416

  Held, Werner ^a,b   Kunz, Béatrice ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b LUDWIG INSTITUTE FOR CANCER RESEARCH   (Switzerland)

Author keywords

Allele; Ly49; MHC class I; NK cell; Receptor repertoire

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE; GENE CLUSTER; GENE EXPRESSION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; MULTIGENE FAMILY; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROCESS CONTROL; STATISTICS;

ALLELES; ANIMALS; ANTIGENS, LY; BASE SEQUENCE; CLONE CELLS; DNA PRIMERS; GENE EXPRESSION; HISTOCOMPATIBILITY ANTIGENS CLASS I; KILLER CELLS, NATURAL; LECTINS, C-TYPE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MULTIGENE FAMILY; POLYMERASE CHAIN REACTION; RECEPTORS, IMMUNOLOGIC; STOCHASTIC PROCESSES;

EID: 0031879243     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1521-4141(199808)28:08<2407::AID-IMMU2407>3.0.CO;2-D     Document Type: Article

References (45)

1. Höglund, P., Sundbäck, J., Olsson-Alheim, M. Y., Johanson, M., Ohlen, C., Ljunggren, H.-G., Sentman, C. L. and Kärre, K., Host MHC class I gene control of NK cell specificity in the mouse. Immunol. Rev. 1997. 155: 11-28.
2. Raulet, D. H., Held, W., Correa, I., Dorfman, J., Wu, M.-F. and Corral, L., Specificity, tolerance and developmental regulation of natural killer cells defined by expression of class I specific Ly49 receptors. Immunol. Rev. 1997. 155: 41-52.
3. Moretta, A., Biassoni, R., Bottino, C., Pende, D., Vitale, M., Poggi, A., Mingari, M. C. and Moretta, L., Major histocompatibility complex class I-specific receptors on human natural killer and T lymphocytes. Immunol. Rev. 1997. 155: 105-118.
4. Long, E. O., Burshtyn, D. N., Clark, W. P., Peruzzi, M., Rajagopalan, S., Rojo, S., Wagtmann, N. and Winter, C. C., Killer cell inhibitory receptors: diversity, specificity and function. Immunol. Rev. 1997. 155: 135-144.
5. Lanier, L. L., Corliss, B. and Philips, J. H., Arousal and inhibition of human NK cells. Immunol. Rev. 1997. 155: 145-154.
6. Yokoyama, W. M. and Seaman, W. E., The Ly-49 and NKR-P1 gene families encoding lectin-like receptors on natural killer cells: the NK gene complex. Annu. Rev. Immunol. 1993. 11: 613-635.
7. Karlhofer, F. M., Ribaudo, R. K. and Yokoyama, W. M., MHC class I alloantigen specificity of Ly-49 + IL-2 activated natural killer cells. Nature 1992. 358: 66-70.
8. Karlhofer, F. M., Hunziker, R., Reichlin, A., Margulies, D. H. and Yokoyama, W. M., Host MHC class I molecules modulate in vivo expression of a NK cell receptor. J. Immunol. 1994. 153: 2407-2416.
9. Mason, L. H., Ortaldo, J. R., Young, H. A., Kumar, V., Bennett, M. and Anderson, S. K., Cloning and functional characteristics of murine LGL-1: a member of the Ly-49 gene family (Ly-49G2). J. Exp. Med. 1995. 182: 293-303.
10. Yu, Y. Y., George, T., Dorfman, J., Roland, J., Kumar, V. and Bennett, M., The role of Ly49A and 5E6 (Ly49C) molecules in hybrid resistance mediated by murine natural killer cells against normal T cell blasts. Immunity 1996. 4: 67-76.
11. Stoneman, E. R., Bennett, M., An, J., Chesnut, K. A., Wakeland, E. K., Scheerer, J. B., Siciliano, M. J., Kumar, V. and Mathew, P. A., Cloning and characterization of 5E6 (Ly49C), a receptor molecule expressed on a subset of murine natural killer cells. J. Exp. Med. 1995. 182:305-313.
12. Gosslin, P., Lusignana, Y., Brennan, J., Takei, F. and Lemieux, S., The NK2.1 receptor is encoded by Ly49C and its expression is regulated by MHC class I alleles. Int. Immunol. 1997. 9: 533-540.
13. Sentman, C. L., Hackett, J., Jr., Kumar, V. and Bennett, M., Identifaction of a subset of murine natural killer cells that mediates rejection of Hh-1d but not Hh-1b bone marrow grafts. J. Exp. Med. 1989. 170: 191-202.
14. Mason, L., Mathieson, B. and Ortaldo, J., Natural killer cell subsets in the mouse. J. Immunol. 1990. 145: 751-759.
15. Brennan, J., Mager, D., Jefferies, W. and Takei, F., Expression of different members of the Ly-49 gene family defines distinct natural killer cell subsets and cell adhesion properties. J. Exp. Med. 1994. 180: 2287-2295.
16. Yu, Y. Y. L., Kumar, V. and Bennett, M., Murine natural killer cells and marrow graft rejection. Annu. Rev. Immunol. 1992. 10: 189-213.
17. Held, W., Cado, D. and Raulet, D. H., Transgenic expression of the Ly49A natural killer cell receptor confers class I MHC-specific inhibition and prevents bone marrow allograft rejection. J. Exp. Mod. 1996. 184: 2037-2041.
18. Trinchieri, G., Biology of natural killer cells. Adv. Immunol. 1989. 47: 187-376.
19. Held, W., Roland, J. and Raulet, D. H., Allelic exclusion of Ly49 family genes encoding class I-MHC-specific receptors on NK cells. Nature 1995. 376: 355-358.
20. Held, W. and Raulet, D. H., Expression of the Ly49A gene in murine natural killer cell clones is predominantly but not exclusively mono-allelic. Eur. J. Immunol. 1997. 27: 2876-2884.
21. Held, W. and Raulet, D. H., Ly49A transgenic mice provide evidence for a major histocompatibility complex-dependent education process in natural killer cell development. J. Exp. Med. 1997. 185: 2079-2088.
22. Yokoyama, W. M., Recognition structures on natural killer cells. Curr. Opin. Immunol. 1993. 5: 67-73.
23. Smith, H. R. C., Karlhofer, F. M. and Yokoyama, W. M., Ly-49 multigene family expressed by IL-2-activated NK cells. J. Immunol. 1994. 153: 1068-1079.
24. Ohlen, C., Kling, G., Höglund, P., Hansson, M., Scangos, G., Bieberich, C., Jay, G. and Karre, K., Prevention of allogeneic bone marrow graft rejection by H-2 transgene in donor mice. Science 1989. 246: 666-668.
25. Bix, M., Liao, N.-S., Zijlstra, M., Loring, J., Jaenisch, R. and Raulet, D., Rejection of class I MHC-deficient hemopoietic cells by irradiated MHC-matched mice. Nature 1991. 349: 329-331.
26. Liao, N., Bix, M., Zijlstra, M., Jaenisch, R. and Raulet, D., MHC class I deficiency: susceptibility to natural killer (NK) cells and impaired NK activity. Science 1991. 253: 199-202.
27. Hoglund, P., Ohlen, C., Carbone, E., Franksson, L., Ljunggren, H., Latour, A., Koller, B. and Karre, K., Recognition of β2-microglobulin-negative (β2m-) T-cell blasts by natural killer cells from normal but not from β2m-mice: nonresponsiveness controlled by β2m-bone marrow in chimeric mice. Proc. Natl. Acad. Sci. USA 1991. 88: 10332-10336.
28. ante, N. M., Uhrberg, M., Shilling, H. G., Lienert-Weidenbach, K., Arnett, K. L., D'Andrea, A., Phillips, J. H., Lanier, L. L. and Parham, P., Functionally and structurally distinct NK cell receptor repertoires in the peripheral blood of two human donors. Immunity 1998. 7: 739-751.
29. Held, W., Dorfman, J. R., Wu, M.-F. and Raulet, D. H., Major histocompatibility complex class I dependent skewing of the natural killer cell Ly49 receptor repertoire. Eur. J. Immunol. 1996. 26: 2286-2292.
30. Dorfman, J. R. and Raulet, D. H., Major histocompatibility complex genes determine natural killer cell tolerance. Eur. J. Immunol. 1996. 26: 151-155.
31. Brennan, J., Lemieux, S., Freeman, J. D., Mager, D. L. and Takei, F., Heterogeneity among Ly-49C natural killer (NK) cells: Characterization of highly related receptors with differeing functions and expression patterns. J. Exp. Med. 1996. 184: 2085-2090.
32. Sundbäck, J., Kärre, K. and Sentman, C. L., Cloning of minimally divergent allelic forms of the natural killer (NK) receptor Ly-49C, differentially controlled by host genes in the MHC and NK gene complex. J. Immunol. 1996. 157: 3936-3942.
33. Malissen, M., Trucy, J., Jouvin-Marche, E., Cazenave, P. A., Scollay, R. and Malissen, B., Regulation of TCR alpha and beta gene allelic exclusion during T-cell development, Immunol. Today 1992. 13: 315-322.
34. Shinkai, Y., Rathbun, G., Lam, K. P., Oltz, E. M., Stewart, V., Mendelsohn, M., Charron, J., Datta, M., Young, F., Stall, A. M. and Alt, F. W., Rag-2-Deficient Mice Lack Mature Lymphocytes Owing To Inability To Initiative V(D)J Rearrangement. Cell 1992. 68: 855-867.
35. Murphy, W., Kumar, V. and Bennett, M., Rejection of bone marrow allografts by mice with severe combined immunodeficiency (SCID). J. Exp. Med. 1987. 165: 1212-1217.
36. Zerrahn, J., Held, W. and Raulet, D. H., The MHC reactivity of the T cell repertoire prior to positive and negative selection. Cell 1997. 88: 627-636.
37. Padovan, E., Giachino, C., Cella, M., Valitutti, S., Acuto, O. and Lanzavecchia, A., Normal T lymphocytes can express two different T cell receptor β chains: Implications for the mechanism of allelic exclusion. J. Exp. Med. 1995. 181: 1587-1591.
38. Casanova, J. L., Romero, P., Widmann, C., Kourilsky, P. and Maryanski, J. L., T cell receptor genes in a series of class I major histocompatibility complex-restricted cytotoxic T lymphocyte clones specific for a Plasmodium berghei nonapeptide: implications for T cell allelic exclusion and antigen-specific repertoire. J. Exp. Med. 1991. 174: 1371-1383.
39. Petire, H. T., Livak, F., Schatz, D. G., Strasser, A., Crispe, I. N. and Shortman, K., Multiple rearrangements in T cell receptor a chain genes maximize the production of useful thymocytes. J. Exp. Med. 1993. 178: 615-622.
40. Unkeless, J. C., Characterization of a monoclonal antibody directed against mouse macrophage and lymphocyte Fc receptors. J. Exp. Med. 1979. 150: 580-596.
41. Koo, G. C. and Peppard, J. R., Establishment of monoclonal anti-NK-1.1 antibody. Hybridoma 1984. 3: 301-303.
42. Roland, J. and Cazenave, P. A., Ly-49 antigen defines an alpha beta TCR population in i-IEL with an extrathymic maturation. Int. Immunol. 1992. 4: 699-706.
43. Mason, L., Giardina, S., Hecht, T., Ortaldo, J. and Mathieson, B., LGL-1: A non polymorphic antigen expressed on a major population of mouse natural killer cells. J. Immunol. 1988. 140: 4403-4412.
44. Held, W., Lowin-Kropf, B. and Raulet, D. H., Generation of short term murine natural killer cell clones to analyze Ly49 gene expression. Methods Mol. Biol. 1998. in press.
45. Wong, S., Freeman, J. D., Kelleher, C., Mager, D. and Takei, F., Ly-49 multigene family. New members of a superfamily of type II membrane proteins with lectin-like domains. J. Immunol. 1991. 147: 1417-1423.