Influence of Interleukin IL-2 and IL-12 + IL-18 on Surface Expression of Immunoglobulin-Like Receptors KIR2DL1, KIR2DL2, and KIR3DL2 in Natural Killer Cells

Chrul, Slawomir; Polakowska, Ewa; Szadkowska, Agnieszka; Bodalski, Jerzy

doi:https://doi.org/10.1155/MI/2006/46957

Mediators of Inflammation

On this page

Abstract References Copyright Related Articles

Research Communication | Open Access

Volume 2006 | Article ID 046957 | https://doi.org/10.1155/MI/2006/46957

Influence of Interleukin IL-2 and IL-12 + IL-18 on Surface Expression of Immunoglobulin-Like Receptors KIR2DL1, KIR2DL2, and KIR3DL2 in Natural Killer Cells

Slawomir Chrul,¹Ewa Polakowska,¹Agnieszka Szadkowska,¹and Jerzy Bodalski¹

Received05 Dec 2005

Revised22 Mar 2006

Accepted25 Apr 2006

Published12 Jun 2006

Abstract

Natural killer (NK) cells express killer cell inhibitory receptors (KIRs) that recognize polymorphic class I MHC molecules. In the present study, we analyze the modulatory effect of IL-2 alone or a combination of IL-12 with IL-18 on surface expression of killer cell immunoglobulin-like receptors KIR2DL1, KIR2DL2, and KIR3DL2 in NK cells. Thus, it was found that IL-2 causes a significant increase in the proportion of cells with given studied receptors. Stimulation by a mixture of IL-12 and IL-18 caused significant increase in the fraction of cells with the KIR2DL1 and KIR2DL2, however no significant change in the percentage of cells with KIR3DL2 receptor on their surface was observed. The results of the study show the presence of KIRs on both resting and activated NK cells, this may suggest that KIRs have also an important role in the regulatory processes after activation of this subpopulation of cells.

References

A R French and W M Yokoyama, “Natural killer cells and viral infections,” Current Opinion in Immunology, vol. 15, no. 1, pp. 45–51, 2003.
View at: Google Scholar
J B VanDeusen and M A Caligiuri, “New developments in anti-tumor efficacy and malignant transformation of human natural killer cells,” Current Opinion in Hematology, vol. 10, no. 1, pp. 55–59, 2003.
View at: Google Scholar
A G Baxter and M J Smyth, “The role of NK cells in autoimmune disease,” Autoimmunity, vol. 35, no. 1, pp. 1–14, 2002.
View at: Google Scholar
G Trinchieri, “Biology of natural killer cells,” Advances in Immunology, vol. 47, pp. 187–376, 1989.
View at: Google Scholar
R B Herberman and J R Ortaldo, “Natural killer cells: their role in defenses against disease,” Science, vol. 214, no. 4516, pp. 24–30, 1981.
View at: Google Scholar
C A Biron, K B Nguyen, G C Pien, L P Cousens, and T P Salazar-Mather, “Natural killer cells in antiviral defense: function and regulation by innate cytokines,” Annual Review of Immunology, vol. 17, pp. 189–220, 1999.
View at: Google Scholar
A A Maghazachi, “Chemokines, G proteins and natural killer cells,” Archivum Immunologiae et Therapiae Experimentalis, vol. 48, no. 2, pp. 65–72, 2000.
View at: Google Scholar
A M Martin, E M Freitas, C S Witt, and F T Christiansen, “The genomic organization and evolution of the natural killer immunoglobulin-like receptor (KIR) gene cluster,” Immunogenetics, vol. 51, no. 4-5, pp. 268–280, 2000.
View at: Google Scholar
U Steffens, Y Vyas, B Dupont, and A Selvakumar, “Nucleotide and amino acid sequence alignment for human killer cell inhibitory receptors (KIR), 1998,” Tissue Antigens, vol. 51, no. 4 pt 1, pp. 398–413, 1998.
View at: Google Scholar
H G Shilling, L A Guethlein, N W Cheng et al., “Allelic polymorphism synergizes with variable gene content to individualize human KIR genotype,” Journal of Immunology, vol. 168, no. 5, pp. 2307–2315, 2002.
View at: Google Scholar
D Pende, R Biassoni, C Cantoni et al., “The natural killer cell receptor specific for HLA-A allotypes: a novel member of the p58/p70 family of inhibitory receptors that is characterized by three immunoglobulin-like domains and is expressed as a 140-kD disulphide- linked dimer,” Journal of Experimental Medicine, vol. 184, no. 2, pp. 505–518, 1996.
View at: Google Scholar
P Hansasuta, T Dong, H Thananchai et al., “Recognition of HLA-A3 and HLA-A11 by KIR3DL2 is peptide-specific,” European Journal of Immunology, vol. 34, no. 6, pp. 1673–1679, 2004.
View at: Google Scholar
M Toneva, V Lepage, G Lafay et al., “Genomic diversity of natural killer cell receptor genes in three populations,” Tissue Antigens, vol. 57, no. 4, pp. 358–362, 2001.
View at: Google Scholar
M A Cook, P AH Moss, and D C Briggs, “The distribution of 13 killer-cell immunoglobulin-like receptor loci in UK blood donors from three ethnic groups,” European Journal of Immunogenetics, vol. 30, no. 3, pp. 213–221, 2003.
View at: Google Scholar
O Mandelboim, S Kent, D M Davis et al., “Natural killer activating receptors trigger interferon $\gamma$ secretion from T cells and natural killer cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 7, pp. 3798–3803, 1998.
View at: Google Scholar
M H Johansson, C Bieberich, G Jay, K Kärre, and P Höglund, “Natural killer cell tolerance in mice with mosaic expression of major histocompatibility complex class I transgene,” Journal of Experimental Medicine, vol. 186, no. 3, pp. 353–364, 1997.
View at: Google Scholar
S KP Kung and R G Miller, “Mouse natural killer subsets defined by their target specificity and their ability to be separately rendered unresponsive in vivo,” Journal of Immunology, vol. 158, no. 6, pp. 2616–2626, 1997.
View at: Google Scholar
M Salcedo, M Andersson, S Lemieux, L Van Kaer, B J Chambers, and H Ljunggren, “Fine tuning of natural killer cell specificity and maintenance of self tolerance in MHC class I-deficient mice,” European Journal of Immunology, vol. 28, no. 4, pp. 1315–1321, 1998.
View at: Google Scholar
W E Carson, J G Giri, M J Lindemann et al., “Interleukin (IL) 15 is a novel cytokine that activates human natural killer cells via components of the IL-2 receptor,” Journal of Experimental Medicine, vol. 180, no. 4, pp. 1395–1403, 1994.
View at: Google Scholar
L L Lanier, D W Buck, L Rhodes et al., “Interleukin 2 activation of natural killer cells rapidly induces the expression and phosphorylation of the Leu-23 activation antigen,” Journal of Experimental Medicine, vol. 167, no. 5, pp. 1572–1585, 1988.
View at: Google Scholar
H Okamura, H Tsutsui, T Komatsu et al., “Cloning of a new cytokine that induces IFN- $\gamma$ production by T cells,” Nature, vol. 378, no. 6552, pp. 88–91, 1995.
View at: Google Scholar
Y Hyodo, K Matsui, N Hayashi et al., “IL-18 up-regulates perforin-mediated NK activity without increasing perforin messenger RNA expression by binding to constitutively expressed IL-18 receptor,” Journal of Immunology, vol. 162, no. 3, pp. 1662–1668, 1999.
View at: Google Scholar
D L Hodge, W B Schill, J M Wang et al., “IL-2 and IL-12 alter NK cell responsiveness to IFN- $\gamma$ -inducible protein 10 by down-regulating CXCR3 expression,” Journal of Immunology, vol. 168, no. 12, pp. 6090–6098, 2002.
View at: Google Scholar
B R Lauwerys, N Garot, J C Renauld, and F A Houssiau, “Cytokine production and killer activity of NK/T-NK cells derived with IL-2, IL-15, or the combination of IL-12 and IL-18,” Journal of Immunology, vol. 165, no. 4, pp. 1847–1853, 2000.
View at: Google Scholar
T Fukao, S Matsuda, and S Koyasu, “Synergistic effects of IL-4 and IL-18 on IL-12-dependent IFN- $\gamma$ production by dendritic cells,” Journal of Immunology, vol. 164, no. 1, pp. 64–71, 2000.
View at: Google Scholar
C L Hofstra, I Van Ark, G Hofman, M Kool, F P Nijkamp, and A JM Van Oosterhout, “Prevention of Th2-like cell responses by coadministration of IL-12 and IL-18 is associated with inhibition of antigen-induced airway hyperresponsiveness, eosinophilia, and serum IgE levels,” Journal of Immunology, vol. 161, no. 9, pp. 5054–5060, 1998.
View at: Google Scholar
B R Lauwerys, J C Renauld, and F A Houssiau, “Synergistic proliferation and activation of natural killer cells by interleukin 12 and interleukin 18,” Cytokine, vol. 11, no. 11, pp. 822–830, 1999.
View at: Google Scholar
M Tomura, X Y Zhou, S Maruo et al., “A critical role for IL-18 in the proliferation and activation of ${\mathrm{NK}}1.1^ + {\mathrm{CD}}3^ -$ cells,” Journal of Immunology, vol. 160, no. 10, pp. 4738–4746, 1998.
View at: Google Scholar
K Yamanaka, I Hara, H Nagai et al., “Synergistic antitumor effects of interleukin-12 gene transfer and systemic administration of interleukin-18 in a mouse bladder cancer model,” Cancer Immunology Immunotherapy, vol. 48, no. 6, pp. 297–302, 1999.
View at: Google Scholar
E Aktas, M Akdis, S Bilgic et al., “Different natural killer (NK) receptor expression and immunoglobulin E (IgE) regulation by NK1 and NK2 cells,” Clinical and Experimental Immunology, vol. 140, no. 2, pp. 301–309, 2005.
View at: Google Scholar
M Draghi, N Yawata, M Gleimer, M Yawata, N M Valiante, and P Parham, “Single-cell analysis of the human NK cell response to missing self and its inhibition by HLA class I,” Blood, vol. 105, no. 5, pp. 2028–2035, 2005.
View at: Google Scholar
G Ferlazzo, D Thomas, S L Lin et al., “The abundant NK cells in human secondary lymphoid tissues require activation to express killer cell Ig-like receptors and become cytolytic,” Journal of Immunology, vol. 172, no. 3, pp. 1455–1462, 2004.
View at: Google Scholar
R Gazit, B Z Garty, Y Monselise et al., “Expression of KIR2DL1 on the entire NK cell population: a possible novel immunodeficiency syndrome,” Blood, vol. 103, no. 5, pp. 1965–1966, 2004.
View at: Google Scholar
T Momot, S Koch, N Hunzelmann et al., “Association of killer cell immunoglobulin-like receptors with scleroderma,” Arthritis and Rheumatism, vol. 50, no. 5, pp. 1561–1565, 2004.
View at: Google Scholar
P Musette, L Michel, F Jean-Louis, M Bagot, and A Bensussan, “Polymorphic expression of CD158k/p140/KIR3DL2 in Sézary patients,” Blood, vol. 101, no. 3, p. 1203, 2003.
View at: Google Scholar
P K Epling-Burnette, J S Painter, P Chaurasia et al., “Dysregulated NK receptor expression in patients with lymphoproliferative disease of granular lymphocytes,” Blood, vol. 103, no. 9, pp. 3431–3439, 2004.
View at: Google Scholar
R Miyashita, N Tsuchiya, T Yabe et al., “Association of killer cell immunoglobulin-like receptor genotypes with microscopic polyangiitis,” Arthritis and Rheumatism, vol. 54, no. 3, pp. 992–997, 2006.
View at: Google Scholar
G Batoni, S Esin, F Favilli et al., “Human ${\mathrm{CD}}56^{{\mathrm{bright}}}$ and ${\mathrm{CD}}56^{{\mathrm{dim}}}$ natural killer cell subsets respond differentially to direct stimulation with Mycobacterium bovis bacillus Calmette-Guérin,” Scandinavian Journal of Immunology, vol. 62, no. 6, pp. 498–506, 2005.
View at: Google Scholar
Y Jin, B B Damaj, and A A Maghazachi, “Human resting ${\mathrm{CD}}16^ -$ , ${\mathrm{CD}}16^ +$ and IL-2-, IL-12-, IL-15- or IFN- $\alpha$ -activated natural killer cells differentially respond to sphingosylphosphorylcholine, lysophosphatidylcholine and platelet-activating factor,” European Journal of Immunology, vol. 35, no. 9, pp. 2699–2708, 2005.
View at: Google Scholar
M Vitale, M Della Chiesa, S Carlomagno et al., “NK-dependent DC maturation is mediated by TNF $\alpha$ and IFN $\gamma$ released upon engagement of the NKp30 triggering receptor,” Blood, vol. 106, no. 2, pp. 566–571, 2005.
View at: Google Scholar
E Marcenaro, B Ferranti, and A Moretta, “NK-DC interaction: on the usefulness of auto-aggression,” Autoimmunity Reviews, vol. 4, no. 8, pp. 520–525, 2005.
View at: Google Scholar
E C Shin, K S Choi, S J Kim, and J S Shin, “Modulation of the surface expression of CD158 killer cell Ig-like receptor by interleukin-2 and transforming growth factor- $\beta$ ,” Yonsei Medical Journal, vol. 45, no. 3, pp. 510–514, 2004.
View at: Google Scholar
T Kogure, H Fujinaga, A Niizawa et al., “Killer-cell inhibitory receptors, CD158a/b, are upregulated by interleukin-2, but not interferon- $\gamma$ or interleukin-4,” Mediators of Inflammation, vol. 8, no. 6, pp. 313–318, 1999.
View at: Google Scholar
K Matsumoto and K Kanmatsuse, “Interleukin-18 and interleukin-12 synergize to stimulate the production of vascular permeability factor by T lymphocytes in normal subjects and in patients with minimal-change nephrotic syndrome,” Nephron, vol. 85, no. 2, pp. 127–133, 2000.
View at: Google Scholar
M Nakahira, H J Ahn, W R Park et al., “Synergy of IL-12 and IL-18 for IFN- $\gamma$ gene expression: IL-12-induced STAT4 contributes to IFN- $\gamma$ promoter activation by up-regulating the binding activity of IL-18-induced activator protein 1-,” Journal of Immunology, vol. 168, no. 3, pp. 1146–1153, 2002.
View at: Google Scholar
M Okamoto, S Kato, K Oizumi et al., “Interleukin 18 (Il-18) in synergy with Il-2 induces lethal lung injury in mice: a potential role for cytokines, chemokines, and natural killer cells in the pathogenesis of interstitial pneumonia,” Blood, vol. 99, no. 4, pp. 1289–1298, 2002.
View at: Google Scholar
M Tarkowski, S Chrul, and J Bodalski, “The effect of IL-18 on IL-12-induced CD30 expression and IL-4 and IFN- $\gamma$ production by allergen and PPD specific T cells,” Clinical and Experimental Immunology, vol. 127, no. 1, pp. 78–84, 2002.
View at: Google Scholar

Copyright

Copyright © 2006 Slawomir Chrul et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation Order printed copies

Views

269

Downloads

827

Citations