Kupffer cells express a unique combination of phenotypic and functional characteristics compared with splenic and peritoneal macrophages

Journal of Leukocyte Biology

Volumn 92, Issue 4, 2012, Pages 723-733

  Movita, Dowty ^a   Kreefft, Kim ^a   Biesta, Paula ^a   van Oudenaren, Adri ^a   Leenen, Pieter J M ^a   Janssen, Harry L A ^a   Boonstra, Andre ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Endocytosis; IL 10; Immunoregulation; Liver

Indexed keywords

ADAPTOR PROTEIN; CD11 ANTIGEN; CD40 ANTIGEN; DEXTRAN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 3; INTERLEUKIN 10; INTERLEUKIN 12P40; MEMBRANE PROTEIN; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; TOLL INTERACTING PROTEIN; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TRANSMEMBRANE EMP24 PROTEIN TRANSPORT DOMAIN CONTAINING 1; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CELL POPULATION; CONTROLLED STUDY; ENDOSOME; KUPFFER CELL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERITONEUM MACROPHAGE; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN CELL; STEADY STATE; UPREGULATION;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD11B; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; CELLS, CULTURED; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; INTERLEUKIN-10; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KUPFFER CELLS; MACROPHAGES; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; PHENOTYPE; REACTIVE OXYGEN SPECIES; SPLEEN; TOLL-LIKE RECEPTORS;

MUS;

EID: 84868115814     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.1111566     Document Type: Article

References (43)

1. Crispe, I. N. (2009) The liver as a lymphoid organ. Annu. Rev. Immunol. 27, 147-163.
2. Parker, G. A., Picut, C. A. (2005) Liver immunobiology. Toxicol. Pathol. 33, 52-62.
3. Cantor, H. M., Dumont, A. E. (1967) Hepatic suppression of sensitization to antigen absorbed into the portal system. Nature 215, 744-745.
4. May, A. G., Bauer, S., Leddy, J. P., Panner, B., Vaughan, J., Russell, P. S. (1969) Survival of allografts after hepatic portal venous administration of specific transplantation antigen. Ann. Surg. 170, 824-832.
5. Gorczynski, R. M. (1992) Immunosuppression induced by hepatic portal venous immunization spares reactivity in IL-4 producing T lymphocytes. Immunol. Lett. 33, 67-77.
6. Knolle, P., Schlaak, J., Uhrig, A., Kempf, P., Meyer zum Buschenfelde, K. H., Gerken, G. (1995) Human Kupffer cells secrete IL-10 in response to lipopolysaccharide (LPS) challenge. J. Hepatol. 22, 226-229.
7. Roth, S., Gong, W., Gressner, A. M. (1998) Expression of different isoforms of TGF-α and the latent TGF-β binding protein (LTBP) by rat Kupffer cells. J. Hepatol. 29, 915-922.
8. Devey, L., Ferenbach, D., Mohr, E., Sangster, K., Bellamy, C. O., Hughes, J., Wigmore, S. J. (2009) Tissue-resident macrophages protect the liver from ischemia reperfusion injury via a heme oxygenase-1-dependent mechanism. Mol. Ther. 17, 65-72.
9. You, Q., Cheng, L., Kedl, R. M., Ju, C. (2008) Mechanism of T cell tolerance induction by murine hepatic Kupffer cells. Hepatology 48, 978-990.
10. Kawai, T., Akira, S. (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11, 373-384.
11. Wu, J., Lu, M., Meng, Z., Trippler, M., Broering, R., Szczeponek, A., Krux, F., Dittmer, U., Roggendorf, M., Gerken, G., Schlaak, J. F. (2007) Toll-like receptor-mediated control of HBV replication by nonparenchymal liver cells in mice. Hepatology 46, 1769-1778.
12. Wu, J., Meng, Z., Jiang, M., Zhang, E., Trippler, M., Broering, R., Bucchi, A., Krux, F., Dittmer, U., Yang, D., Roggendorf, M., Gerken, G., Lu, M., Schlaak, J. F. (2010) Toll-like receptor-induced innate immune responses in non-parenchymal liver cells are cell type-specific. Immunology 129, 363-374.
13. Seki, E., Tsutsui, H., Nakano, H., Tsuji, N., Hoshino, K., Adachi, O., Adachi, K., Futatsugi, S., Kuida, K., Takeuchi, O., Okamura, H., Fujimoto, J., Akira, S., Nakanishi, K. (2001) Lipopolysaccharide-induced IL-18 secretion from murine Kupffer cells independently of myeloid differentiation factor 88 that is critically involved in induction of production of IL-12 and IL-1β. J. Immunol. 166, 2651-2657.
14. Kinoshita, M., Uchida, T., Sato, A., Nakashima, M., Nakashima, H., Shono, S., Habu, Y., Miyazaki, H., Hiroi, S., Seki, S. (2010) Characterization of two F4/80-positive Kupffer cell subsets by their function and phenotype in mice. J. Hepatol. 53, 903-910.
15. Valatas, V., Xidakis, C., Roumpaki, H., Kolios, G., Kouroumalis, E. A. (2003) Isolation of rat Kupffer cells: a combined methodology for highly purified primary cultures. Cell Biol. Int. 27, 67-73.
16. Austyn, J. M., Gordon, S. (1981) F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur. J. Immunol. 11, 805-815.
17. Lloyd, C. M., Phillips, A. R., Cooper, G. J., Dunbar, P. R. (2008) Threecolour fluorescence immunohistochemistry reveals the diversity of cells staining for macrophage markers in murine spleen and liver. J. Immunol. Methods 334, 70-81.
18. Boonstra, A., Rajsbaum, R., Holman, M., Marques, R., Asselin-Paturel, C., Pereira, J. P., Bates, E. E., Akira, S., Vieira, P., Liu, Y. J., Trinchieri, G., O'Garra, A. (2006) Macrophages and myeloid dendritic cells, but not plasmacytoid dendritic cells, produce IL-10 in response to MyD88-and TRIF-dependent TLR signals, and TLR-independent signals. J. Immunol. 177, 7551-7558.
19. Brown, K. L., Poon, G. F., Birkenhead, D., Pena, O. M., Falsafi, R., Dahlgren, C., Karlsson, A., Bylund, J., Hancock, R. E., Johnson, P. (2011) Host defense peptide LL-37 selectively reduces proinflammatory macrophage responses. J. Immunol. 186, 5497-5505.
20. Hume, D. A., Perry, V. H., Gordon, S. (1984) The mononuclear phagocyte system of the mouse defined by immunohistochemical localisation of antigen F4/80: macrophages associated with epithelia. Anat. Rec. 210, 503-512.
21. Knolle, P. A., Gerken, G. (2000) Local control of the immune response in the liver. Immunol. Rev. 174, 21-34.
22. Raes, G., Noel, W., Beschin, A., Brys, L., de Baetselier, P., Hassanzadeh, G. H. (2002) FIZZ1 and Ym as tools to discriminate between differentially activated macrophages. Dev. Immunol. 9, 151-159.
23. Loke, P. N., Nair, M., Parkinson, J., Guiliano, D., Blaxter, M., Allen, J. (2002) IL-4 dependent alternatively-activated macrophages have a distinctive in vivo gene expression phenotype. BMC Immunol. 3, 7.
24. Davies, J. M., MacSharry, J., Shanahan, F. (2010) Differential regulation of Toll-like receptor signalling in spleen and Peyer's patch dendritic cells. Immunology 131, 438-448.
25. Liu, Z. J., Yan, L. N., Li, X. H., Xu, F. L., Chen, X. F., You, H. B., Gong, J. P. (2008) Up-regulation of IRAK-M is essential for endotoxin tolerance induced by a low dose of lipopolysaccharide in Kupffer cells. J. Surg. Res. 150, 34-39.
26. Gordon, S. (2007) The macrophage: past, present and future. Eur. J. Immunol. 37 (Suppl. 1), S9-S17.
27. Gregory, D. J., Olivier, M. (2005) Subversion of host cell signalling by the protozoan parasite Leishmania. Parasitology 130 (Suppl.), S27-S35.
28. Klein, I., Cornejo, J. C., Polakos, N. K., John, B., Wuensch, S. A., Topham, D. J., Pierce, R. H., Crispe, I. N. (2007) Kupffer cell heterogeneity: functional properties of bone marrow derived and sessile hepatic macrophages. Blood 110, 4077-4085.
29. Mebius, R. E., Kraal, G. (2005) Structure and function of the spleen. Nat. Rev. Immunol. 5, 606-616.
30. Ghosn, E. E., Cassado, A. A., Govoni, G. R., Fukuhara, T., Yang, Y., Monack, D. M., Bortoluci, K. R., Almeida, S. R., Herzenberg, L. A. (2010) Two physically, functionally, and developmentally distinct peritoneal macrophage subsets. Proc. Natl. Acad. Sci. USA 107, 2568-2573.
31. Bouwens, L., Baekeland, M., De Zanger, R., Wisse, E. (1986) Quantitation, tissue distribution and proliferation kinetics of Kupffer cells in normal rat liver. Hepatology 6, 718-722.
32. Salvidio, E., Crosby, W. H. (1960) Thrombocytopenia after intravenous injection of India ink. J. Lab. Clin. Med. 56, 711-716.
33. Cohen, P., Braunwald, J., Gardner, F. H. (1965) Destruction of canine and rabbit platelets following intravenous administration of carbon particles or endotoxin. J. Lab. Clin. Med. 66, 263-271.
34. Ravetch, J. V. (1994) Fc receptors: rubor redux. Cell 78, 553-560.
35. Levier, D. G., Brown, R. D., McCay, J. A., Fuchs, B. A., Harris, L. S., Munson, A. E. (1993) Hepatic and splenic phagocytosis in female B6C3F1 mice implanted with morphine sulfate pellets. J. Pharmacol. Exp. Ther. 267, 357-363.
36. Hardonk, M. J., Dijkhuis, F. W., Hulstaert, C. E., Koudstaal, J. (1992) Heterogeneity of rat liver and spleen macrophages in gadolinium chloride-induced elimination and repopulation. J. Leukoc. Biol. 52, 296-302.
37. Elomaa, O., Kangas, M., Sahlberg, C., Tuukkanen, J., Sormunen, R., Liakka, A., Thesleff, I., Kraal, G., Tryggvason, K. (1995) Cloning of a novel bacteria-binding receptor structurally related to scavenger receptors and expressed in a subset of macrophages. Cell 80, 603-609.
38. Van der Laan, L. J., Dopp, E. A., Haworth, R., Pikkarainen, T., Kangas, M., Elomaa, O., Dijkstra, C. D., Gordon, S., Tryggvason, K., Kraal, G. (1999) Regulation and functional involvement of macrophage scavenger receptor MARCO in clearance of bacteria in vivo. J. Immunol. 162, 939-947.
39. Jones, C., Virji, M., Crocker, P. R. (2003) Recognition of sialylated meningococcal lipopolysaccharide by siglecs expressed on myeloid cells leads to enhanced bacterial uptake. Mol. Microbiol. 49, 1213-1225.
40. Holt, M. P., Cheng, L., Ju, C. (2008) Identification and characterization of infiltrating macrophages in acetaminophen-induced liver injury. J. Leukoc. Biol. 84, 1410-1421.
41. Karlmark, K. R., Weiskirchen, R., Zimmermann, H. W., Gassler, N., Ginhoux, F., Weber, C., Merad, M., Luedde, T., Trautwein, C., Tacke, F. (2009) Hepatic recruitment of the inflammatory Gr1+ monocyte subset upon liver injury promotes hepatic fibrosis. Hepatology 50, 261-274.
42. Kono, H., Fujii, H., Asakawa, M., Yamamoto, M., Maki, A., Matsuda, M., Rusyn, I., Matsumoto, Y. (2002) Functional heterogeneity of the kupffer cell population is involved in the mechanism of gadolinium chloride in rats administered endotoxin. J. Surg. Res. 106, 179-187.
43. He, Y., Sadahiro, T., Noh, S. I., Wang, H., Todo, T., Chai, N. N., Klein, A. S., Wu, G. D. (2009) Flow cytometric isolation and phenotypic characterization of two subsets of ED2(+) (CD163) hepatic macrophages in rats. Hepatol Res. 39, 1208-1218.