Ly49Q positively regulates type I IFN production by plasmacytoid dendritic cells in an immunoreceptor tyrosine-based inhibitory motif-dependent manner

Journal of Immunology

Volumn 190, Issue 8, 2013, Pages 3994-4004

  Rahim, Mir Munir A ^a   Tai, Lee Hwa ^b   Troke, Angela D ^a   Mahmoud, Ahmad Bakur ^a,c   Abou Samra, Elias ^a   Roy, Justin G ^a   Mottashed, Amelia ^a   Ault, Nicholas ^a   Corbeil, Chloe ^a   Goulet, Marie Line ^a   Zein, Haggag S ^a,d   Hamilton Valensky, Melisa ^e   Krystal, Gerald ^e   Kerr, William G ^f,g   Toyama Sorimachi, Noriko ^h   Makrigiannis, Andrew P ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

^b OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^c TAIBAH UNIVERSITY   (Saudi Arabia)

^d CAIRO UNIVERSITY   (Egypt)

^e BRITISH COLUMBIA CANCER AGENCY   (Canada)

^f State University of New York Upstate Medical University: College of Medicine   (United States)

^g SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

^h NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CELL PROTEIN; CPG OLIGODEOXYNUCLEOTIDE; INTERFERON; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 12; LY49Q RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PHOSPHATASE; PROTEIN ITIM; PROTEIN SHIP; PROTEIN TYROSINE PHOSPHATASE SHP 1; PROTEIN TYROSINE PHOSPHATASE SHP 2; RECEPTOR; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR AGONIST; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; CD4+ T LYMPHOCYTE; CELL NUCLEUS; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOPLASM; ENZYME ACTIVITY; IMMUNE RESPONSE; INTRACELLULAR TRANSPORT; LYMPHOCYTE PROLIFERATION; MOUSE; MYELOID DENDRITIC CELL; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN SYNTHESIS REGULATION; PROTEIN TRANSPORT; RECEPTOR DOWN REGULATION; T LYMPHOCYTE ACTIVATION;

ANIMALS; DENDRITIC CELLS; GENETIC COMPLEMENTATION TEST; INTERFERON-ALPHA; MACROPHAGES, PERITONEAL; MELANOMA, EXPERIMENTAL; MICE; MICE, 129 STRAIN; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MICE, TRANSGENIC; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY A; OLIGODEOXYRIBONUCLEOTIDES; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT;

EID: 84875977877     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200873     Document Type: Article

References (51)

1. Liu, Y. J. 2005. IPC: professional type 1 interferon-producing cells and plas-macytoid dendritic cell precursors. Annu. Rev. Immunol. 23: 275-306.
2. Asselin-Paturel, C., G. Brizard, J. J. Pin, F. Brière, and G. Trinchieri. 2003. Mouse strain differences in plasmacytoid dendritic cell frequency and function revealed by a novel monoclonal antibody. J. Immunol. 171: 6466-6477.
3. Siegal, F. P., N. Kadowaki, M. Shodell, P. A. Fitzgerald-Bocarsly, K. Shah, S. Ho, S. Antonenko, and Y. J. Liu. 1999. The nature of the principal type 1 interferon-producing cells in human blood. Science 284: 1835-1837.
4. Zucchini, N., G. Bessou, S. H. Robbins, L. Chasson, A. Raper, P. R. Crocker, and M. Dalod. 2008. Individual plasmacytoid dendritic cells are major contributors to the production of multiple innate cytokines in an organ-specific manner during viral infection. Int. Immunol. 20: 45-56.
5. Swiecki, M., S. Gilfillan, W. Vermi, Y. Wang, and M. Colonna. 2010. Plasma-cytoid dendritic cell ablation impacts early interferon responses and antiviral NK and CD8(+) T cell accrual. Immunity 33: 955-966.
6. Kadowaki, N., S. Ho, S. Antonenko, R. W. Malefyt, R. A. Kastelein, F. Bazan, and Y. J. Liu. 2001. Subsets of human dendritic cell precursors express different Toll-like receptors and respond to different microbial antigens. J. Exp. Med. 194: 863-869.
7. Toyama-Sorimachi, N., Y. Tsujimura, M. Maruya, A. Onoda, T. Kubota, S. Koyasu, K. Inaba, and H. Karasuyama. 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. USA 101: 1016-1021.
8. Carlyle, J. R., A. Mesci, J. H. Fine, P. Chen, S. Bélanger, L. H. Tai, and A. P. Makrigiannis. 2008. Evolution of the Ly49 and Nkrp1 recognition systems. Semin. Immunol. 20: 321-330.
9. Gays, F., J. G. Aust, D. M. Reid, J. Falconer, N. Toyama-Sorimachi, P. R. Taylor, and C. G. Brooks. 2006. Ly49B is expressed on multiple subpopulations of myeloid cells. J. Immunol. 177: 5840-5851.
10. Van Beneden, K., A. De Creus, F. Stevenaert, V. Debacker, J. Plum, and G. Leclercq. 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.
11. Toyama-Sorimachi, N., Y. Omatsu, A. Onoda, Y. Tsujimura, T. Iyoda, A. Kikuchi-Maki, H. Sorimachi, T. Dohi, S. Taki, K. Inaba, and H. Karasuyama. 2005. Inhibitory NK receptor Ly49Q is expressed on subsets of dendritic cells in a cellular maturation- and cytokine stimulation-dependent manner. J. Immunol. 174: 4621-4629.
12. Kamogawa-Schifter, Y., J. Ohkawa, S. Namiki, N. Arai, K. Arai, and Y. Liu. 2005. Ly49Q defines 2 pDC subsets in mice. Blood 105: 2787-2792.
13. Omatsu, Y., T. Iyoda, Y. Kimura, A. Maki, M. Ishimori, N. Toyama-Sorimachi, and K. Inaba. 2005. Development of murine plasmacytoid dendritic cells defined by increased expression of an inhibitory NK receptor, Ly49Q. J. Immunol. 174: 6657-6662.
14. Sasawatari, S., M. Yoshizaki, C. Taya, A. Tazawa, K. Furuyama-Tanaka, H. Yonekawa, T. Dohi, A. P. Makrigiannis, T. Sasazuki, K. Inaba, and N. Toyama-Sorimachi. 2010. The Ly49Q receptor plays a crucial role in neu-trophil polarization and migration by regulating raft trafficking. Immunity 32: 200-213.
15. Hayashi, M., T. Nakashima, T. Kodama, A. P. Makrigiannis, N. Toyama-Sorimachi, and H. Takayanagi. 2010. Ly49Q, an ITIM-bearing NK receptor, positively regulates osteoclast differentiation. Biochem. Biophys. Res. Commun. 393: 432-438.
16. Tai, L. H., M. L. Goulet, S. Belanger, A. D. Troke, A. G. St-Laurent, A. Mesci, N. Toyama-Sorimachi, J. R. Carlyle, and A. P. Makrigiannis. 2007. Recognition of H-2K(b) by Ly49Q suggests a role for class Ia MHC regulation of plasma-cytoid dendritic cell function. Mol. Immunol. 44: 2638-2646.
17. Tai, L. H., M. L. Goulet, S. Belanger, N. Toyama-Sorimachi, N. Fodil-Cornu, S. M. Vidal, A. D. Troke, D. W. McVicar, and A. P. Makrigiannis. 2008. Positive regulation of plasmacytoid dendritic cell function via Ly49Q recognition of class I MHC. J. Exp. Med. 205: 3187-3199.
18. Dzionek, A., Y. Sohma, J. Nagafune, M. Cella, M. Colonna, F. Facchetti, G. Günther, I. Johnston, A. Lanzavecchia, T. Nagasaka, et al. 2001. BDCA-2, a novel plasmacytoid dendritic cell-specific type II C-type lectin, mediates antigen capture and is a potent inhibitor of interferon alpha/beta induction. J. Exp. Med. 194: 1823-1834.
19. Fuchs, A., M. Cella, T. Kondo, and M. Colonna. 2005. Paradoxic inhibition of human natural interferon-producing cells by the activating receptor NKp44. Blood 106: 2076-2082.
20. Blasius, A. L., M. Cella, J. Maldonado, T. Takai, and M. Colonna. 2006. Siglec-H is an IPC-specific receptor that modulates type I IFN secretion through DAP12. Blood 107: 2474-2476.
21. Sjölin, H., S. H. Robbins, G. Bessou, A. Hidmark, E. Tomasello, M. Johansson, H. Hall, F. Charifi, G. B. Karlsson Hedestam, C. A. Biron, et al. 2006. DAP12 signaling regulates plasmacytoid dendritic cell homeostasis and down-modulates their function during viral infection. J. Immunol. 177: 2908-2916.
22. Watarai, H., E. Sekine, S. Inoue, R. Nakagawa, T. Kaisho, and M. Taniguchi. 2008. PDC-TREM, a plasmacytoid dendritic cell-specific receptor, is responsible for augmented production of type I interferon. Proc. Natl. Acad. Sci. USA 105: 2993-2998.
23. Yoshizaki, M., A. Tazawa, E. Kasumi, S. Sasawatari, K. Itoh, T. Dohi, T. Sasazuki, K. Inaba, A. P. Makrigiannis, and N. Toyama-Sorimachi. 2009. Spatiotemporal regulation of intracellular trafficking of Toll-like receptor 9 by an inhibitory receptor, Ly49Q. Blood 114: 1518-1527.
24. Mustelin, T., T. Vang, and N. Bottini. 2005. Protein tyrosine phosphatases and the immune response. Nat. Rev. Immunol. 5: 43-57.
25. Vivier, E., and M. Daëron. 1997. Immunoreceptor tyrosine-based inhibition motifs. Immunol. Today 18: 286-291.
26. Olcese, L., P. Lang, F. Vély, A. Cambiaggi, D. Marguet, M. Bléry, K. L. Hippen, R. Biassoni, A. Moretta, L. Moretta, et al. 1996. Human and mouse killer-cell inhibitory receptors recruit PTP1C and PTP1D protein tyrosine phosphatases. J. Immunol. 156: 4531-4534.
27. Bruhns, P., P. Marchetti, W. H. Fridman, E. Vivier, and M. Daëron. 1999. Differential roles of N- and C-terminal immunoreceptor tyrosine-based inhibition motifs during inhibition of cell activation by killer cell inhibitory receptors. J. Immunol. 162: 3168-3175.
28. Nakamura, M. C., E. C. Niemi, M. J. Fisher, L. D. Shultz, W. E. Seaman, and J. C. Ryan. 1997. Mouse Ly-49A interrupts early signaling events in natural killer cell cytotoxicity and functionally associates with the SHP-1 tyrosine phosphatase. J. Exp. Med. 185: 673-684.
29. Wang, J. W., J. M. Howson, T. Ghansah, C. Desponts, J. M. Ninos, S. L. May, K. H. Nguyen, N. Toyama-Sorimachi, and W. G. Kerr. 2002. Influence of SHIP on the NK repertoire and allogeneic bone marrow transplantation. Science 295: 2094-2097.
30. An, H., J. Hou, J. Zhou, W. Zhao, H. Xu, Y. Zheng, Y. Yu, S. Liu, and X. Cao. 2008. Phosphatase SHP-1 promotes TLR- and RIG-I-activated production of type I interferon by inhibiting the kinase IRAK1. Nat. Immunol. 9: 542-550.
31. Honda, K., and T. Taniguchi. 2006. IRFs: master regulators of signalling by Tolllike receptors and cytosolic pattern-recognition receptors. Nat. Rev. Immunol. 6: 644-658.
32. Schafer, S. L., R. Lin, P. A. Moore, J. Hiscott, and P. M. Pitha. 1998. Regulation of type I interferon gene expression by interferon regulatory factor-3. J. Biol. Chem. 273: 2714-2720.
33. Marié, I., J. E. Durbin, and D. E. Levy. 1998. Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J. 17: 6660-6669.
34. Sato, M., N. Hata, M. Asagiri, T. Nakaya, T. Taniguchi, and N. Tanaka. 1998. Positive feedback regulation of type I IFN genes by the IFN-inducible transcription factor IRF-7. FEBS Lett. 441: 106-110.
35. Sato, M., H. Suemori, N. Hata, M. Asagiri, K. Ogasawara, K. Nakao, T. Nakaya, M. Katsuki, S. Noguchi, N. Tanaka, and T. Taniguchi. 2000. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 13: 539-548.
36. Honda, K., H. Yanai, H. Negishi, M. Asagiri, M. Sato, T. Mizutani, N. Shimada, Y. Ohba, A. Takaoka, N. Yoshida, and T. Taniguchi. 2005. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434: 772-777.
37. Mach, N., S. Gillessen, S. B. Wilson, C. Sheehan, M. Mihm, and G. Dranoff. 2000. Differences in dendritic cells stimulated in vivo by tumors engineered to secrete granulocyte-macrophage colony-stimulating factor or Flt3-ligand. Cancer Res. 60: 3239-3246.
38. Patel, R., S. Bélanger, L. H. Tai, A. D. Troke, and A. P. Makrigiannis. 2010. Effect of Ly49 haplotype variance on NK cell function and education. J. Immunol. 185: 4783-4792.
39. Kumagai, Y., O. Takeuchi, H. Kato, H. Kumar, K. Matsui, E. Morii, K. Aozasa, T. Kawai, and S. Akira. 2007. Alveolar macrophages are the primary interferonalpha producer in pulmonary infection with RNA viruses. Immunity 27: 240-252.
40. Kerkmann, M., S. Rothenfusser, V. Hornung, A. Towarowski, M. Wagner, A. Sarris, T. Giese, S. Endres, and G. Hartmann. 2003. Activation with CpG-A and CpG-B oligonucleotides reveals two distinct regulatory pathways of type I IFN synthesis in human plasmacytoid dendritic cells. J. Immunol. 170: 4465-4474.
41. Guiducci, C., G. Ott, J. H. Chan, E. Damon, C. Calacsan, T. Matray, K. D. Lee, R. L. Coffman, and F. J. Barrat. 2006. Properties regulating the nature of the plasmacytoid dendritic cell response to Toll-like receptor 9 activation. J. Exp. Med. 203: 1999-2008.
42. Villadangos, J. A., and L. Young. 2008. Antigen-presentation properties of plasmacytoid dendritic cells. Immunity 29: 352-361.
43. Swiecki, M., Y. Wang, W. Vermi, S. Gilfillan, R. D. Schreiber, and M. Colonna. 2011. Type I interferon negatively controls plasmacytoid dendritic cell numbers in vivo. J. Exp. Med. 208: 2367-2374.
44. Tsui, F. W., and H. W. Tsui. 1994. Molecular basis of the motheaten phenotype. Immunol. Rev. 138: 185-206.
45. Pathak, M. K., and T. Yi. 2001. Sodium stibogluconate is a potent inhibitor of protein tyrosine phosphatases and augments cytokine responses in hemopoietic cell lines. J. Immunol. 167: 3391-3397.
46. Dai, J., N. J. Megjugorac, S. B. Amrute, and P. Fitzgerald-Bocarsly. 2004. Regulation of IFN regulatory factor-7 and IFN-alpha production by enveloped virus and lipopolysaccharide in human plasmacytoid dendritic cells. J. Immunol. 173: 1535-1548.
47. Sivori, S., M. Falco, S. Carlomagno, E. Romeo, C. Soldani, A. Bensussan, A. Viola, L. Moretta, and A. Moretta. 2010. A novel KIR-associated function: evidence that CpG DNA uptake and shuttling to early endosomes is mediated by KIR3DL2. Blood 116: 1637-1647.
48. An, H., W. Zhao, J. Hou, Y. Zhang, Y. Xie, Y. Zheng, H. Xu, C. Qian, J. Zhou, Y. Yu, et al. 2006. SHP-2 phosphatase negatively regulates the TRIF adaptor protein-dependent type I interferon and proinflammatory cytokine production. Immunity 25: 919-928.
49. Ju, X., M. Zenke, D. N. Hart, and G. J. Clark. 2008. CD300a/c regulate type I interferon and TNF-alpha secretion by human plasmacytoid dendritic cells stimulated with TLR7 and TLR9 ligands. Blood 112: 1184-1194.
50. Cao, W., and L. Bover. 2010. Signaling and ligand interaction of ILT7: receptor-mediated regulatory mechanisms for plasmacytoid dendritic cells. Immunol. Rev. 234: 163-176.
51. Meyer-Wentrup, F., D. Benitez-Ribas, P. J. Tacken, C. J. Punt, C. G. Figdor, I. J. de Vries, and G. J. Adema. 2008. Targeting DCIR on human plasmacytoid dendritic cells results in antigen presentation and inhibits IFN-alpha production. Blood 111: 4245-4253.