NKG2C zygosity influences CD94/NKG2C receptor function and the NK-cell compartment redistribution in response to human cytomegalovirus

European Journal of Immunology

Volumn 43, Issue 12, 2013, Pages 3268-3278

  Muntasell, Aura ^a   López Montañés, María ^b   Vera, Andrea ^a   Heredia, Gemma ^b   Romo, Neus ^b   Peñafiel, Judith ^a   Moraru, Manuela ^c   Vila, Joan ^a   Vilches, Carlos ^c   López Botet, Miguel ^a,b  

^a HOSPITAL DEL MAR   (Spain)

^b UNIVERSITAT POMPEU FABRA   (Spain)

^c HOSPITAL UNIVERSITARIO PUERTA DE HIERRO   (Spain)

Author keywords

CD94 NKG2C; Cytomegalovirus; Human; NK cells; NKG2C genotype

Indexed keywords

CD94 ANTIGEN; HLA E ANTIGEN; INTERLEUKIN 15; NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2C; UNCLASSIFIED DRUG; HLA ANTIGEN CLASS 1; HLA-E ANTIGEN; IL15 PROTEIN, HUMAN; KLRC2 PROTEIN, HUMAN; KLRD1 PROTEIN, HUMAN; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY C; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY D;

ADULT; ARTICLE; CELL COMPARTMENTALIZATION; CELL PROLIFERATION; CHILD; DEGRANULATION; GENOTYPE; HEMIZYGOSITY; HUMAN; HUMAN CYTOMEGALOVIRUS; MAJOR CLINICAL STUDY; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; YOUNG ADULT; ZYGOSITY; ADOLESCENT; CALCIUM SIGNALING; CD94/NKG2C; CLINICAL TRIAL; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; FEMALE; GENE DOSAGE; GENETICS; IMMUNOLOGY; MALE; NK CELLS; NKG2C GENOTYPE; PRESCHOOL CHILD;

CD94/NKG2C; CYTOMEGALOVIRUS; HUMAN; NK CELLS; NKG2C GENOTYPE;

ADOLESCENT; ADULT; CALCIUM SIGNALING; CELL DEGRANULATION; CHILD; CHILD, PRESCHOOL; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; FEMALE; GENE DOSAGE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; INTERLEUKIN-15; KILLER CELLS, NATURAL; MALE; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY C; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY D;

EID: 84890386947     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343773     Document Type: Article

References (42)

1. Mocarski, E. S. and Courcelle, C. T., Cytomegaloviruses and their replication. In Knipe, D. M., Howley, P. M., Griffin, D. E. and Lamb, R. A. (Eds.) Fields virology. Lippincott, Williams & Wilkins, Philadelphia, 2001, pp. 2629-2673.
2. Pass, R. F., Cytomegalovirus. In Knipe, D. M., Howley, P. M., Griffin, D. E. and Lamb, R. A. (Eds.), Fields virology. Lippincott, Williams & Wilkins, Philadelphia, 2001, pp. 2675-2705.
3. Gumá, M., Angulo, A., Vilches, C., Gómez-Lozano, N., Malats, N. and López-Botet, M., Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 2004. 104: 3664-3671.
4. Monsivais-Urenda, A., Noyola-Cherpitel, D., Hernández-Salinas, A., García-Sepúlveda, C., Romo, N., Baranda, L., López-Botet, M. et al., Influence of human cytomegalovirus infection on the NK cell receptor repertoire in children. Eur. J. Immunol. 2010. 40: 1418-1427.
5. Noyola, D. E., Fortuny, C., Muntasell, A., Noguera-Julian, A., Muñoz-Almagro, C., Alarcón, A., Juncosa, T. et al., Influence of congenital human cytomegalovirus infection and the NKG2C genotype on NK-cell subset distribution in children. Eur. J. Immunol. 2012. 42: 3256-3266.
6. Béziat, V., Liu, L., Malmberg, J. A., Ivarsson, M. A., Sohlberg, E., Björklund, A. T., Retière, C. et al., NK cell responses to cytomegalovirus infection lead to stable imprints in the human KIR repertoire and involve activating KIRs. Blood 2013. 121: 4703-477.
7. Lopez-Vergès, S., Milush, J. M., Schwartz, B. S., Pando, M. J., Jarjoura, J., York, V. A., Houchins, J. P. et al., Expansion of a unique CD57(+)NKG2Chi natural killer cell subset during acute human cytomegalovirus infection. Proc. Natl. Acad. Sci. USA 2011. 108: 14725-14732.
8. Kuijpers, T. W., Baars, P. A., Dantin, C., van den Burg, M., van Lier, R. A. and Roosnek, E., Human NK cells can control CMV infection in the absence of T cells. Blood 2008. 112: 914-915.
9. Della Chiesa, M., Falco, M., Podesta, M., Locatelli, F., Moretta, L., Frassoni, F. and Moretta, A., Phenotypic and functional heterogeneity of human NK cells developing after umbilical cord blood transplantation: a role for human cytomegalovirus? Blood 2012. 119: 399-410.
10. Foley, B., Cooley, S., Verneris, M. R., Curtsinger, J., Luo, X., Waller, E. K., Anasetti, C. et al., Human cytomegalovirus (CMV)-induced memory-like NKG2C(+) NK cells are transplantable and expand in vivo in response to recipient CMV antigen. J. Immunol. 2012. 189: 5082-5088.
11. Foley, B., Cooley, S., Verneris, M. R., Pitt, M., Curtsinger, J., Luo, X., Lopez-Vergès, S. et al., Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function. Blood 2012. 119: 2665-2674.
12. Arase, H., Mocarski, E. S., Campbell, A. E., Hill, A. B. and Lanier, L. L., Direct recognition of cytomegalovirus by activating and inhibitory NK cell receptors. Science 2002. 296: 1323-1326.
13. Brown, M. G., Dokun, A. O., Heusel, J. W., Smith, H. R., Beckman, D. L., Blattenberger, E. A., Dubbelde, C. E. et al., Vital involvement of a natural killer cell activation receptor in resistance to viral infection. Science 2001. 292: 934-937.
14. Smith, H. R., Heusel, J. W., Mehta, I. K., Kim, S., Dorner, B. G., Naidenko, O. V., Iizuka, K. et al., Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc. Natl. Acad. Sci. USA 2002. 99: 8826-8831.
15. Sun, J. C., Beilke, J. N. and Lanier, L. L., Adaptive immune features of natural killer cells. Nature 2009. 457: 557-561.
16. Vivier, E., Raulet, D. H., Moretta, A., Caligiuri, M. A., Zitvogel, L., Lanier, L. L., Yokoyama, W. M. et al., Innate or adaptive immunity? The example of natural killer cells. Science 2011. 331: 44-49.
17. Sun, J. C., Lopez-Vergès, S., Kim, C. C., DeRisi, J. L. and Lanier, L. L., NK cells and immune "memory" J. Immunol. 2011. 186: 1891-1897.
18. Béziat, V., Dalgard, O., Asselah, T., Halfon, P., Bedossa, P., Boudifa, A., Hervier, B. et al., CMV drives clonal expansion of NKG2C+ NK cells expressing self-specific KIRs in chronic hepatitis patients. Eur. J. Immunol. 2012. 42: 447-457.
19. Björkstrom, N. K., Lindgren, T., Stoltz, M., Fauriat, C., Braun, M., Evander, M., Michaëlsson, J. et al., Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J. Exp. Med. 2011. 208: 13-21.
20. Gumá, M., Cabrera, C., Erkizia, I., Bofill, M., Clotet, B., Ruiz, L. and López-Botet, M., Human cytomegalovirus infection is associated with increased proportions of NK cells that express the CD94/NKG2C receptor in aviremic HIV-1-positive patients. J. Infect. Dis. 2006. 194: 38-41.
21. Mela, C. M. and Goodier, M. R., The contribution of cytomegalovirus to changes in NK cell receptor expression in HIV-1-infected individuals. J. Infect. Dis. 2007. 195: 158-159.
22. Zhang, T., Scott, J. M., Hwang, I., and Kim, S., Cutting edge: antibody-dependent memory-like NK cells distinguished by FcRgamma deficiency. J. Immunol. 2013. 190: 1402-1406.
23. Lanier, L. L., Corliss, B., Wu, J. and Phillips, J. H., Association of DAP12 with activating CD94/NKG2C NK cell receptors. Immunity 1998. 8: 693-701.
24. Lanier, L. L., Corliss, B. C., Wu, J., Leong, C. and Phillips, J. H., Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 1998. 391: 703-707.
25. Tomasello, E., Olcese, L., Vely, F., Geourgeon, C., Blery, M., Moqrich, A., Gautheret, D. et al., Gene structure, expression pattern, and biological activity of mouse killer cell activating receptor-associated protein (KARAP)/DAP-12. J. Biol. Chem. 1998. 273: 34115-34119.
26. Llano, M., Lee, N., Navarro, F., Garcia, P., Albar, J. P., Geraghty, D. E. and López-Botet, M., HLA-E-bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G-derived nonamer. Eur. J. Immunol. 1998. 28: 2854-2863.
27. Gumá, M., Budt, M., Sáez, A., Brckalo, T., Hengel, H., Angulo, A. and López-Botet, M., Expansion of CD94/NKG2C+ NK cells in response to human cytomegalovirus-infected fibroblasts. Blood 2006. 107: 3624-3631.
28. Brunetta, E., Fogli, M., Varchetta, S., Bozzo, L., Hudspeth, K. L., Marcenaro, E., Moretta, A. et al., Chronic HIV-1 viremia reverses NKG2A/NKG2C ratio on natural killer cells in patients with human cytomegalovirus co-infection. AIDS 2010. 24: 27-34.
29. Miyashita, R., Tsuchiya, N., Hikami, K., Kuroki, K., Fukazawa, T., Bijl, M., Kallenberg, C. G. et al., Molecular genetic analyses of human NKG2C (KLRC2) gene deletion. Int. Immunol. 2004. 16: 163-168.
30. Moraru, M., Cisneros, E., Gómez-Lozano, N., de Pablo, R., Portero, F., Cañizares, M., Vaquero, M. et al., Host genetic factors in susceptibility to herpes simplex type 1 virus infection: contribution of polymorphic genes at the interface of innate and adaptive immunity. J. Immunol. 2012. 188: 4412-4420.
31. Strong, R. K., Holmes, M. A., Li, P., Braun, L., Lee, N. and Geraghty, D. E., HLA-E allelic variants. Correlating differential expression, peptide affinities, crystal structures, and thermal stabilities. J. Biol. Chem. 2003. 278: 5082-5090.
32. Guma, M., Busch, L. K., Salazar-Fontana, L. I., Bellosillo, B., Morte, C., García, P. and López-Botet, M., The CD94/NKG2C killer lectin-like receptor constitutes an alternative activation pathway for a subset of CD8+ T cells. Eur. J. Immunol. 2005. 35: 2071-2080.
33. French, A. R., Sjolin, H., Kim, S., Koka, R., Yang, L., Young, D. A., Cerboni, C. et al., DAP12 signaling directly augments proproliferative cytokine stimulation of NK cells during viral infections. J. Immunol. 2006. 177: 4981-4990.
34. Hikami, K., Tsuchiya, N., Yabe, T. and Tokunaga, K., Variations of human killer cell lectin-like receptors: common occurrence of NKG2-C deletion in the general population. Genes Immun. 2003. 4: 160-167.
35. Béziat, V., Descours, B., Parizot, C., Debré, P. and Vieillard, V., NK cell terminal differentiation: correlated stepwise decrease of NKG2A and acquisition of KIRs. PLoS One 2010. 5: e11966.
36. Björkström, N. K., Riese, P., Heuts, F., Andersson, S., Fauriat, C., Ivarsson, M. A., Björklund, A. T. et al., Expression patterns of NKG2A, KIR, and CD57 define a process of CD56dim NK-cell differentiation uncoupled from NK-cell education. Blood 2010. 116: 3853-3864.
37. Lopez-Vergès, S., Milush, J. M., Pandey, S., York, V. A., Arakawa-Hoyt, J., Pircher, H., Norris, P. J. et al., CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK-cell subset. Blood 2010. 116: 3865-3874.
38. Bournazos, S., Woof, J. M., Hart, S. P. and Dransfield, I., Functional and clinical consequences of Fc receptor polymorphic and copy number variants. Clin. Exp. Immunol. 2009. 157: 244-254.
39. Jiang, W., Johnson, C., Jayaraman, J., Simecek, N., Noble, J., Moffatt, M. F., Cookson, W. O. et al., Copy number variation leads to considerable diversity for B but not A haplotypes of the human KIR genes encoding NK cell receptors. Genome Res. 2012. 22: 1845-1854.
40. Pelak, K., Need, A. C., Fellay, J., Shianna, K. V., Feng, S., Urban, T. J., Ge, D. et al., Copy number variation of KIR genes influences HIV-1 control. PLoS Biol. 2011. 9: e1001208.
41. Moraru, M., Cañizares, M., Muntasell, A., de Pablo, R., López-Botet, M. and Vilches, C., Assessment of copy-number variation in the NKG2C receptor gene in a single-tube and characterization of a reference cell panel, using standard polymerase chain reaction. Tissue Antigens 2012. 80: 184-187.
42. Romo, N., Fitó, M., Guma, M., Sala, J., García, C., Ramos, R., Muntasell, A. et al., Association of atherosclerosis with expression of the LILRB1 receptor by human NK and T-cells supports the infectious burden hypothesis. Arterioscler. Thromb. Vasc. Biol. 2011. 31: 2314-2321.