The lectin Siglec-G inhibits dendritic cell cross-presentation by impairing MHC class I-peptide complex formation

Nature Immunology

Volumn 17, Issue 10, 2016, Pages 1167-1175

  Ding, Yuanyuan ^a,b,c   Guo, Zhenhong ^b   Liu, Yiqi ^a   Li, Xia ^c   Zhang, Qian ^b   Xu, Xiongfei ^b   Gu, Yan ^b   Zhang, Yi ^b   Zhao, Dezhi ^c   Cao, Xuetao ^a,b,c  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c PEKING UNION MEDICAL COLLEGE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD8ALPHA ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEIN TYROSINE PHOSPHATASE SHP 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SIALIC ACID BINDING IMMUNOGLOBULIN LIKE LECTIN; SIALIC ACID BINDING IMMUNOGLOBULIN LIKE LECTIN G; UNCLASSIFIED DRUG; ANTIGEN; CD8 ANTIGEN; CD8 ANTIGEN, ALPHA CHAIN; HLA ANTIGEN CLASS 1; LECTIN; LYMPHOCYTE ANTIGEN RECEPTOR; NEUTROPHIL CYTOSOLIC FACTOR 1; PEPTIDE FRAGMENT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SIGLECG PROTEIN, MOUSE;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL LOAD; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; COMPLEX FORMATION; CONTROLLED STUDY; CROSS PRESENTATION; CYTOTOXIC T LYMPHOCYTE; DENDRITIC CELL; ENZYME ACTIVATION; HYDROLYSIS; IMMUNOREGULATION; LISTERIA MONOCYTOGENES; LISTERIOSIS; MACROPHAGE; MELANOMA B16; MOUSE; MYCOBACTERIOSIS; MYCOBACTERIUM BOVIS BCG; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; EXPERIMENTAL MELANOMA; EXPERIMENTAL NEOPLASM; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; METABOLISM; PHAGOCYTOSIS; SIGNAL TRANSDUCTION; TUMOR VOLUME;

ANIMALS; ANTIGENS; ANTIGENS, CD8; CROSS-PRIMING; DENDRITIC CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS I; LECTINS; LISTERIA MONOCYTOGENES; LISTERIOSIS; LYMPHOCYTE ACTIVATION; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NADPH OXIDASE; NEOPLASMS, EXPERIMENTAL; PEPTIDE FRAGMENTS; PHAGOCYTOSIS; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 6; RECEPTORS, ANTIGEN, B-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, CYTOTOXIC; TUMOR BURDEN;

EID: 84983490114     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3535     Document Type: Article

References (43)

1. Bevan, M.J. Cross-priming for a secondary cytotoxic response to minor H antigens with H-2 congenic cells which do not cross-react in the cytotoxic assay. J. Exp. Med. 143, 1283-1288 (1976
2. Joffre, O.P., Segura, E., Savina, A., & Amigorena, S. Cross-presentation by dendritic cells. Nat. Rev. Immunol. 12, 557-569 (2012
3. den Haan, J.M., Lehar, S.M., & Bevan, M.J. CD8+but not CD8?dendritic cells cross-prime cytotoxic T cells in vivo. J. Exp. Med. 192, 1685-1696 (2000
4. Merad, M., Sathe, P., Helft, J., Miller, J., & Mortha, A. The dendritic cell lineage: ontogeny and function of dendritic cells and their subsets in the steady state and the inflamed setting. Annu. Rev. Immunol. 31, 563-604 (2013
5. Haniffa, M., et al. Human tissues contain CD141hi cross-presenting dendritic cells with functional homology to mouse CD103+nonlymphoid dendritic cells. Immunity 37, 60-73 (2012
6. Dudziak, D., et al. Differential antigen processing by dendritic cell subsets. in vivo. Science 315, 107-111 (2007
7. Hildner, K., et al. Batf3 deficiency reveals a critical role for CD8α+ dendritic cells in cytotoxic T cell immunity. Science 322, 1097-1100 (2008
8. Basha, G., et al. A CD74-dependent MHC class I endolysosomal cross-presentation pathway. Nat. Immunol. 13, 237-245 (2012
9. Guermonprez, P., & Amigorena, S. Pathways for antigen cross presentation. Springer Semin. Immunopathol. 26, 257-271 (2005
10. Guermonprez, P., et al. ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature 425, 397-402 (2003
11. Savina, A., et al. The small GTPase Rac2 controls phagosomalalkalinization and antigen crosspresentation selectively in CD8+ dendritic cells. Immunity 30, 544-555 (2009
12. Schnorrer, P., et al. The dominant role of CD8+ dendritic cells in cross-presentation is not dictated by antigen capture. Proc. Natl. Acad. Sci. USA 103, 10729-10734 (2006
13. Delamarre, L., Pack, M., Chang, H., Mellman, I., & Trombetta, E.S. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 307, 1630-1634 (2005
14. Hotta, C., Fujimaki, H., Yoshinari, M., Nakazawa, M., & Minami, M. The delivery of an antigen from the endocytic compartment into the cytosol for cross-presentation is restricted to early immature dendritic cells. Immunology 117, 97-107 (2006
15. Samie, M., & Cresswell, P. The transcription factor TFEB acts as a molecular switch that regulates exogenous antigen-presentation pathways. Nat. Immunol. 16, 729-736 (2015
16. Osorio, F., et al. The unfolded-protein-response sensor IRE-1α regulates the function of CD8α+ dendritic cells. Nat. Immunol. 15, 248-257 (2014
17. Geijtenbeek, T.B., van Vliet, S.J., Engering, A., t' Hart, B.A., & van Kooyk, Y. Self-And nonself-recognition by C-Type lectins on dendritic cells. Annu. Rev. Immunol. 22, 33-54 (2004
18. Li, N., et al. Cloning and characterization of Siglec-10, a novel sialic acid binding member of the Ig superfamily, from human dendritic cells. J. Biol. Chem. 276, 28106-28112 (2001
19. Chen, W., et al. Induction of Siglec-G by RNA viruses inhibits the innate immune response by promoting RIG-I degradation. Cell 152, 467-478 (2013
20. Ding, C., et al. Siglecg limits the size of B1a B cell lineage by down-regulating NF?B activation. PLoS One 2, e997 (2007
21. Xu, S., et al. IL-17A-producing γδT cells promote CTL responses against Listeria monocytogenes infection by enhancing dendritic cell cross-presentation. J. Immunol. 185, 5879-5887 (2010
22. Westcott, M.M., Henry, C.J., Amis, J.E., & Hiltbold, E.M. Dendritic cells inhibit the progression of Listeria monocytogenes intracellular infection by retaining bacteria in major histocompatibility complex class II-rich phagosomes and by limiting cytosolic growth. Infect. Immun. 78, 2956-2965 (2010
23. Schnupf, P., & Portnoy, D.A. Listeriolysin O: a phagosome-specific lysin. Microbes Infect. 9, 1176-1187 (2007
24. Baghdadi, M., et al. TIM-4 glycoprotein-mediated degradation of dying tumor cells by autophagy leads to reduced antigen presentation and increased immune tolerance. Immunity 39, 1070-1081 (2013
25. Simmons, D.P., et al. Type I IFN drives a distinctive dendritic cell maturation phenotype that allows continued class II MHC synthesis and antigen processing. J. Immunol. 188, 3116-3126 (2012
26. Rodriguez, A., Regnault, A., Kleijmeer, M., Ricciardi-Castagnoli, P., & Amigorena, S. Selective transport of internalized antigens to the cytosol for MHC class I presentation in dendritic cells. Nat. Cell Biol. 1, 362-368 (1999
27. Segura, E., Durand, M., & Amigorena, S. Similar antigen cross-presentation capacity and phagocytic functions in all freshly isolated human lymphoid organ-resident dendritic cells. J. Exp. Med. 210, 1035-1047 (2013
28. Savina, A., et al. NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 126, 205-218 (2006
29. Lambeth, J.D., & Neish, A.S. Nox enzymes and new thinking on reactive oxygen: a double-edged sword revisited. Annu. Rev. Pathol. 9, 119-145 (2014
30. Crocker, P.R., Paulson, J.C., & Varki, A. Siglecs and their roles in the immune system. Nat. Rev. Immunol. 7, 255-266 (2007
31. Chowdhury, A.K., et al. Src-mediated tyrosine phosphorylation of p47phox in hyperoxia-induced activation of NADPH oxidase and generation of reactive oxygen species in lung endothelial cells. J. Biol. Chem. 280, 20700-20711 (2005
32. Chen, G.Y., Tang, J., Zheng, P., & Liu, Y. CD24 and Siglec-10 selectively repress tissue damage-induced immune responses. Science 323, 1722-1725 (2009
33. Luber, C.A., et al. Quantitative proteomics reveals subset-specific viral recognition in dendritic cells. Immunity 32, 279-289 (2010
34. Cai, Y., et al. Increased complement C1q level marks active disease in human tuberculosis. PLoS One 9, e92340 (2014
35. Manca, C., et al. Host targeted activity of pyrazinamide in Mycobacterium tuberculosis infection. PLoS One 8, e74082 (2013
36. Burgdorf, S., Kautz, A., Böhnert, V., Knolle, P.A., & Kurts, C. Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 316, 612-616 (2007
37. Ackerman, A.L., Kyritsis, C., Tampé, R., & Cresswell, P. Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens. Proc. Natl. Acad. Sci. USA 100, 12889-12894 (2003
38. Jancic, C., et al. Rab27a regulates phagosomal pH and NADPH oxidase recruitment to dendritic cell phagosomes. Nat. Cell Biol. 9, 367-378 (2007
39. Maeda, A., Kurosaki, M., Ono, M., Takai, T., & Kurosaki, T. Requirement of SH2-containing protein tyrosine phosphatases SHP-1 and SHP-2 for paired immunoglobulin-like receptor B (PIR-B)-mediated inhibitory signal. J. Exp. Med. 187, 1355-1360 (1998
40. Kaneko, T., et al. Dendritic cell-specific ablation of the protein tyrosine phosphatase Shp1 promotes Th1 cell differentiation and induces autoimmunity. J. Immunol. 188, 5397-5407 (2012
41. Hoffmann, A., et al. Siglec-G is a B1 cell-inhibitory receptor that controls expansion and calcium signaling of the B1 cell population. Nat. Immunol. 8, 695-704 (2007
42. Hamilton, S.E., Badovinac, V.P., Khanolkar, A., & Harty, J.T. Listeriolysin O-deficient Listeria monocytogenes as a vaccine delivery vehicle: antigen-specific CD8 T cell priming and protective immunity. J. Immunol. 177, 4012-4020 (2006
43. Ma, F., et al. The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-γ. Nat. Immunol. 12, 861-869 (2011