SIGNR1 Ligation on Murine Peritoneal Macrophages Induces IL-12 Production Through NFkappaB Activation

Overview

Journal Glycoconj J

Publisher Springer

Specialties Biochemistry
Endocrinology

Date 2010 Jul 1

PMID 20589530

Citations 3

Authors

Chiaki Kato

Naoya Kojima

Affiliations

Soon will be listed here.

Abstract

We have previously shown that murine resident peritoneal macrophages (PEMs) are activated in response to uptake of oligomannose-coated liposomes (OMLs), leading to production of interleukin (IL)-12. To understand the mechanism of activation of PEMs by OMLs, in the present study we investigated the role of a mannose-binding C-type lectin receptor, SIGNR1, in production of proinflammatory cytokines by PEMs, in which SIGNR1 acts as a physiological receptor for OMLs. Engagement of SIGNR1 on PEMs with an anti-SIGNR1-specific rat IgM antibody, ERTR9, induced production of IL-12 and tumor necrosis factor (TNF)-alpha from PEMs, while secretion of IL-6 and IL-1beta was not detected with the same treatment. The level of phosphorylated IkappaB kinase in PEMs also increased in response to ERTR9 treatment of the cells. Treatment of PEMs with a specific nuclear factor kappa-B (NFkappaB) inhibitor, BAY11-7082, reduced ERTR9-dependent IL-12 production. Intraperitoneal treatment with BAY11-7082 also led to reduction of subsequent OML-induced IL-12 production from PEMs. These results indicate that SIGNR1-mediated intercellular signaling may induce production of cytokines such as IL-12 through NFkappaB activation.

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References

Nagaoka K, Takahara K, Tanaka K, Yoshida H, Steinman R, Saitoh S . Association of SIGNR1 with TLR4-MD-2 enhances signal transduction by recognition of LPS in gram-negative bacteria. Int Immunol. 2005; 17(7):827-36. PMC: 1343522. DOI: 10.1093/intimm/dxh264. View

Kawai T, Akira S . Pathogen recognition with Toll-like receptors. Curr Opin Immunol. 2005; 17(4):338-44. DOI: 10.1016/j.coi.2005.02.007. View

Avrameas A, McIlroy D, Hosmalin A, Autran B, Debre P, Monsigny M . Expression of a mannose/fucose membrane lectin on human dendritic cells. Eur J Immunol. 1996; 26(2):394-400. DOI: 10.1002/eji.1830260219. View

Geijtenbeek T, Torensma R, van Vliet S, van Duijnhoven G, Adema G, van Kooyk Y . Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell. 2000; 100(5):575-85. DOI: 10.1016/s0092-8674(00)80693-5. View

Ishii M, Kojima N . Mucosal adjuvant activity of oligomannose-coated liposomes for nasal immunization. Glycoconj J. 2009; 27(1):115-23. DOI: 10.1007/s10719-009-9263-8. View

Delhase M, Hayakawa M, Chen Y, Karin M . Positive and negative regulation of IkappaB kinase activity through IKKbeta subunit phosphorylation. Science. 1999; 284(5412):309-13. DOI: 10.1126/science.284.5412.309. View

Hoshino K, Sugiyama T, Matsumoto M, Tanaka T, Saito M, Hemmi H . IkappaB kinase-alpha is critical for interferon-alpha production induced by Toll-like receptors 7 and 9. Nature. 2006; 440(7086):949-53. DOI: 10.1038/nature04641. View

Takahara K, Yashima Y, Omatsu Y, Yoshida H, Kimura Y, Kang Y . Functional comparison of the mouse DC-SIGN, SIGNR1, SIGNR3 and Langerin, C-type lectins. Int Immunol. 2004; 16(6):819-29. DOI: 10.1093/intimm/dxh084. View

Shimizu Y, Takagi H, Nakayama T, Yamakami K, Tadakuma T, Yokoyama N . Intraperitoneal immunization with oligomannose-coated liposome-entrapped soluble leishmanial antigen induces antigen-specific T-helper type immune response in BALB/c mice through uptake by peritoneal macrophages. Parasite Immunol. 2007; 29(5):229-39. DOI: 10.1111/j.1365-3024.2007.00937.x. View

10.

PIERCE J, Schoenleber R, Jesmok G, Best J, Moore S, Collins T . Novel inhibitors of cytokine-induced IkappaBalpha phosphorylation and endothelial cell adhesion molecule expression show anti-inflammatory effects in vivo. J Biol Chem. 1997; 272(34):21096-103. DOI: 10.1074/jbc.272.34.21096. View

11.

May M, Ghosh S . Signal transduction through NF-kappa B. Immunol Today. 1998; 19(2):80-8. DOI: 10.1016/s0167-5699(97)01197-3. View

12.

Caparros E, Munoz P, Sierra-Filardi E, Serrano-Gomez D, Puig-Kroger A, Rodriguez-Fernandez J . DC-SIGN ligation on dendritic cells results in ERK and PI3K activation and modulates cytokine production. Blood. 2006; 107(10):3950-8. DOI: 10.1182/blood-2005-03-1252. View

13.

Kojima N, Biao L, Nakayama T, Ishii M, Ikehara Y, Tsujimura K . Oligomannose-coated liposomes as a therapeutic antigen-delivery and an adjuvant vehicle for induction of in vivo tumor immunity. J Control Release. 2008; 129(1):26-32. DOI: 10.1016/j.jconrel.2008.03.023. View

14.

Geijtenbeek T, van Vliet S, Koppel E, Sanchez-Hernandez M, Appelmelk B, van Kooyk Y . Mycobacteria target DC-SIGN to suppress dendritic cell function. J Exp Med. 2003; 197(1):7-17. PMC: 2193797. DOI: 10.1084/jem.20021229. View

15.

Trinchieri G . Immunobiology of interleukin-12. Immunol Res. 1998; 17(1-2):269-78. DOI: 10.1007/BF02786451. View

16.

Takagi H, Furuya N, Kojima N . Preferential production of IL-12 by peritoneal macrophages activated by liposomes prepared from neoglycolipids containing oligomannose residues. Cytokine. 2007; 40(3):241-50. DOI: 10.1016/j.cyto.2007.10.005. View

17.

Robinson M, Sancho D, Slack E, LeibundGut-Landmann S, Reis e Sousa C . Myeloid C-type lectins in innate immunity. Nat Immunol. 2006; 7(12):1258-65. DOI: 10.1038/ni1417. View

18.

Numazaki M, Kato C, Kawauchi Y, Kajiwara T, Ishii M, Kojima N . Cross-linking of SIGNR1 activates JNK and induces TNF-alpha production in RAW264.7 cells that express SIGNR1. Biochem Biophys Res Commun. 2009; 386(1):202-6. DOI: 10.1016/j.bbrc.2009.06.011. View

19.

Park C, Takahara K, Umemoto E, Yashima Y, Matsubara K, Matsuda Y . Five mouse homologues of the human dendritic cell C-type lectin, DC-SIGN. Int Immunol. 2001; 13(10):1283-90. DOI: 10.1093/intimm/13.10.1283. View

20.

Tailor P, Tamura T, Ozato K . IRF family proteins and type I interferon induction in dendritic cells. Cell Res. 2006; 16(2):134-40. DOI: 10.1038/sj.cr.7310018. View