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

Journal of Immunology

Volumn 163, Issue 6, 1999, Pages 3176-3184

  Toomey, Jennifer A ^a   Salcedo, Margarita ^b   Cotterill, Lisa A ^c   Millrain, Margaret M ^c   Chrzanowska Lightowlers, Zosia ^a   Lawry, John ^d   Fraser, Karen ^a   Gays, Frances ^a   Robinson, John H ^a   Shrestha, Sunil ^a   Dyson, P Julian ^c   Brooks, Colin G ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b INSERM   (France)

^c MRC CLINICAL SCIENCES CENTRE   (United Kingdom)

^d UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD94 ANTIGEN; CYTOKINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MESSENGER RNA;

ANIMAL CELL; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY TEST; FETUS; FETUS CELL; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STOCHASTIC MODEL;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD94; CELL ADHESION; CELL DIFFERENTIATION; CELLS, CULTURED; CLONE CELLS; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; EMBRYONIC AND FETAL DEVELOPMENT; H-2 ANTIGENS; HISTOCOMPATIBILITY ANTIGENS CLASS I; KILLER CELLS, NATURAL; LECTINS, C-TYPE; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; RECEPTORS, IMMUNOLOGIC; RNA, MESSENGER; SOLUBILITY; STEM CELLS; STOCHASTIC PROCESSES; THYMUS GLAND; TIME FACTORS;

EID: 0033567959     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (45)

1. Lanier, L. L. 1997. Natural killer cells: from no receptors to too many. Immunity 6:371.
2. Lanier, L. L. 1998. NK cell receptors. Annu. Rev. Immunol. 16:359.
3. Kärre, K., H. G. Ljunggren, G. Piontek, and R. Kiessling. 1986. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 319:675.
4. Ljunggren, H. G., and K. Kärre. 1990. In search of the "missing self": MHC molecules and NK cell recognition. Immunol. Today 11:237.
5. Moretta, A., R. Biassoni, C. Bottino, D. Pende, M. Vitale, A. Poggi, M. C. Mingari, and L. Moretta. 1997. Major histocompatibility complex class I-specific receptors on human natural killer and T lymphocytes. Immunol. Rev. 155:105.
6. Lopez-Botet, M., J. J. Perez-Villar, M. Carretero, A. Rodriguez, I. Melero, T. Bellon, M. Llano, and F. Navarro. 1997. Structure and function of the CD94 C-type lectin receptor complex involved in recognition of HLA class I molecules. Immunol. Rev. 155:165.
7. Braud, V. M., D. S. Allan, C. A. O'Callaghan, K. Soderstrom, A. D'Andrea, G. S. Ogg, S. Lazetic, N. T. Young, J. I. Bell, J. H. Phillips, et al. 1998. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391:795.
8. Borrego, F., M. Ulbrecht, E. H. Weiss, J. E. Coligan, and A. G. Brooks. 1998. Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis. J. Exp. Med. 187:813.
9. Lee, N., M. Llano, M. Carretero, A. Ishitani, F. Navarro, M. Lopez-Botet, and D. E. Geraghty. 1998. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc. Natl. Acad. Sci. USA 95:5199.
10. Brown, M. G., A. A. Scalzo, K. Matsumoto, and W. M. Yokoyama. 1997. The natural killer gene complex: a genetic basis for understanding natural killer cell function and innate immunity. Immunol. Rev. 155:53.
11. Takei, F., J. Brennan, and D. L. Mager. 1997. The Ly-49 family: genes, proteins and recognition of class I MHC. Immunol. Rev. 155:67.
12. Salcedo. M., A. D. Diehl, M. Y. Olsson-Alheim, J. Sundbäck, L. Van Kaer, K. Kärre, and H. G. Ljunggren. 1997. Altered expression of Ly49 inhibitory receptors on natural killer cells from MHC class I-deficient mice. J. Immunol. 158:3174.
13. 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.
14. Vance, R. E., and D. H. Raulet. 1998. Toward a quantitative analysis of the repertoire of class I MHC-specific inhibitory receptors on natural killer cells. Curr. Top. Microbiol. Immunol. 230:135.
15. 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.
16. Manoussaka, M., A. Georgiou, B. Rossiter, S. Shrestha, J. A. Toomey, P. V. Sivakumar, M. Bennett, V. Kumar, and C. G. Brooks. 1997. Phenotypic and functional characterization of long-lived NK cell lines of different maturational status obtained from mouse fetal liver. J. Immunol. 158:112.
17. 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.
18. Salcedo, M., P. Bousso, H. G. Ljunggren, P. Kourilsky, and J. P. Abastado. 1998. The Qa-1b molecule binds to a large subpopulation of murine NK cells. Eur. J. Immunol. 28:4356.
19. Vance, R. E., J. R. Kraft, J. D. Altman, P. E. Jensen, and D. H. Raulet. 1998. Mouse CD94/NKG2A is a natural killer cell receptor for the nonclassical major histocompatibility complex (MHC) class I molecule Qa-1(b). J. Exp. Med. 188:1841.
20. Karasuyama, H., and F. Melchers. 1988. Establishment of mouse cell lines which constitutively secrete large quantities of interleukin 2, 3, 4 or 5, using modified cDNA expression vectors. Eur. J. Immunol. 18:97.
21. Brooks, C. G. 1999. Cloning and culturing of mouse NK cells. Methods Mol. Biol., In press.
22. Cotterill, L. A., H. J. Stauss, M. M. Millrain, D. J. Pappin, D. Rahman, B. Canas, P. Chandler, A. Stackpoole, E. Simpson, P. J. Robinson, and P. J. Dyson. 1997. Qa-1 interaction and T cell recognition of the Qa-1 determinant modifier peptide. Eur. J. Immunol. 27:2123.
23. King, T. R., G. J. Christianson, M. J. Mitchell, C. E. Bishop, D. Scott, I. Ehrmann, E. Simpson, E. M. Eicher, and D. C. Roopenian. 1994. Deletion mapping by immunoselection against the H-Y histocompatibility antigen further resolves the Sxra region of the mouse Y chromosome and reveals complexity of the Hya locus. Genomics 24:159.
24. Vance, R. E., D. M. Tanamachi, T. Hanke, and D. H. Raulet. 1997. Cloning of a mouse homolog of CD94 extends the family of C-type lectins on murine natural killer cells. Eur. J. Immunol. 27:3236.
25. Lohwasser, S., P. Hande, D. L. Mager, and F. Takei. 1999. Cloning of murine NKG2A, B and C: second family of C type lectin receptors on murine NK cells. Eur. J. Immunol. 29:755.
26. Sturmhofel, K., and G. J. Hammerling. 1990. Reconstitution of H-2 class I expression by gene transfection decreases susceptibility to natural killer cells of an EL4 class I loss variant. Eur. J. Immunol. 20:171.
27. Teitell, M., H. R. Holcombe, L. Brossay, A. Hagenbaugh, M. J. Jackson, L. Pond, S. P. Balk, C. Terhorst, P. A. Peterson, and M. Kronenberg. 1997. Nonclassical behavior of the mouse CD1 class I-like molecule. J. Immunol. 158:2143.
28. Brossay, L., D. Jullien, S. Cardell, B. C. Sydora, N. Burdin, R. L. Modlin, and M. Kronenberg. 1997. Mouse CD1 is mainly expressed on hemopoietic-derived cells. J. Immunol. 159:1216.
29. Imani, F., and M. J. Soloski. 1991. Heat shock proteins can regulate expression of the TIa region-encoded class Ib molecule Qa-1. Proc. Natl. Acad. Sci. USA 88:10475.
30. Chang, C. S., L. Brossay, M. Kronenberg, and K. P. Kane. 1999. The murine nonclassical class I major histocompatibility complex-like CD1.1 molecule protects target cells from lymphokine-activated killer cell cytolysis. J. Exp. Med. 189:483.
31. Manoussaka, M. S., R. J. Smith, V. Conlin, J. A. Toomey, and C. G. Brooks. 1998. Fetal mouse NK cell clones are deficient in Ly49 expression, share a common broad lytic specificity, and undergo continuous and extensive diversification in vitro. J. Immunol. 160:2197.
32. 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.
33. - thymic or mature γδ T cell clones. Eur. J. Immunol. 28:3399.
34. Lanier, L. L., B. Corliss, J. Wu, and J. H. Phillips. 1998. Association of DAP12 with activating CD94/NKG2C NK cell receptors, Immunity 8:693.
35. Cantoni, C., R. Biassoni, D. Pende, S. Sivori, L. Accame, L. Pareti, G. Semenzato, L. Moretta, A. Moretta, and C. Bottino. 1998. The activating form of CD94 receptor complex: CD94 covalently associates with the Kp39 protein that represents the product of the NKG2-C gene. Eur. J. Immunol. 28:327.
36. Llano, M., N. Lee, F. Navarro, P. Garcia, J. P. Albar, D. E. Geraghty, and M. Lopez-Botet. 1998. HLA-E-bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G-derived nonamer. Eur. J. Immunol. 28:2854.
37. - cells from multipotential murine bone marrow progenitors in a stroma-free culture: definition of cytokine requirements and developmental intermediates. J. Exp. Med. 186:1609.
38. lo target cells: evidence for a Ly-49-independent negative signaling receptor. Eur. J. Immunol. 27:3100.
39. 2-microglobulin-dependent surface expression of functional mouse CD1. 1. J. Exp. Med. 182:1913.
40. Castano, A. R., S. Tangri, J. E. Miller, H. R. Holcombe, M. R. Jackson, W. D. Huse, M. Kronenberg, and P. A. Peterson. 1995. Peptide binding and presentation by mouse CD1. Science 269:223.
41. Lee, D. J., A. Abeyratne, D. A. Carson, and M. Corr. 1998. Induction of an antigen-specific, CD1-restricted cytotoxic T lymphocyte response In vivo. J. Exp. Med 187:433.
42. Ulbrecht, M., S. Modrow, R. Srivastava, P. A. Peterson, and E. H. Weiss. 1998. Interaction of HLA-E with peptides and the peptide transporter in vitro: implications for its function in antigen presentation. J. Immunol. 160:4375.
43. d and a novel 50-kD glycoprotein encoded centromeric to 1-E β. J. Exp. Med. 181:657.
44. 2-microglobulin but is TAP independent. J. Immunol. 160:3217.
45. 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.