IL-10 limits production of pathogenic TNF by M1 myeloid cells through induction of nuclear NF-κB p50 member in Trypanosoma congolense infection-resistant C57BL/6 mice

European Journal of Immunology

Volumn 41, Issue 11, 2011, Pages 3270-3280

  Bosschaerts, Tom ^a,b   Morias, Yannick ^a,b   Stijlemans, Benoît ^a,b   Hérin, Michel ^c   Porta, Chiara ^d   Sica, Antonio ^d,e   Mantovani, Alberto ^e   De Baetselier, Patrick ^a,b   Beschin, Alain ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c UNIVERSITY OF NAMUR   (Belgium)

^d UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^e HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

Author keywords

Inflammation; Inflammatory monocytes; Liver

Indexed keywords

CD11B ANTIGEN; CXCL11 CHEMOKINE; CXCL9 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR; INTERLEUKIN 12P40; MONOCYTE CHEMOTACTIC PROTEIN 1; TUMOR NECROSIS FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; INFLAMMATION; LIVER; LIVER INJURY; MOUSE; NAGANA; NONHUMAN; PRIORITY JOURNAL; TRYPANOSOMA CONGOLENSE;

ANIMALS; BLOTTING, WESTERN; CELL SEPARATION; FLOW CYTOMETRY; INTERLEUKIN-10; LIVER; MICE; MICE, INBRED C57BL; MYELOID CELLS; NF-KAPPA B P50 SUBUNIT; SIGNAL TRANSDUCTION; TRYPANOSOMA CONGOLENSE; TRYPANOSOMIASIS, AFRICAN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 80054930244     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201041307     Document Type: Article

References (47)

1. Tabel, H., Wei, G. and Shi, M., T cells and immunopathogenesis of experimental African trypanosomiasis. Immunol. Rev. 2008. 225: 128-139.
2. Iraqi, F., Sekikawa, K., Rowlands, J. and Teale, A., Susceptibility of tumour necrosis factor-alpha genetically deficient mice to Trypanosoma congolense infection. Parasite Immunol. 2001. 23: 445-451.
3. Magez, S., Radwanska, M., Drennan, M., Fick, L., Baral, T. N., Allie, N., Jacobs, M., et al., Tumor necrosis factor (TNF) receptor-1 (TNFp55) signal transduction and macrophage-derived soluble TNF are crucial for nitric oxide-mediated Trypanosoma congolense parasite killing. J. Infect. Dis. 2007. 196: 954-962.
4. Magez, S., Radwanska, M., Drennan, M., Fick, L., Baral, T. N., Brombacher, F. and De Baetselier, P., Interferon-gamma and nitric oxide in combination with antibodies are key protective host immune factors during Trypanosoma congolense Tc13 Infections. J. Infect. Dis. 2006. 193: 1575-1583.
5. Shi, M., Pan, W. and Tabel, H., Experimental African trypanosomiasis: IFN-gamma mediates early mortality. Eur. J. Immunol. 2003. 33: 108-118.
6. Shi, M., Wei, G., Pan, W. and Tabel, H., Trypanosoma congolense infections: antibody-mediated phagocytosis by Kupffer cells. J. Leukoc. Biol. 2004. 76: 399-405.
7. Naessens, J., Bovine trypanotolerance: a natural ability to prevent severe anaemia and haemophagocytic syndrome? Int. J. Parasitol. 2006. 36: 521-528.
8. Guilliams, M., Oldenhove, G., Noel, W., Herin, M., Brys, L., Loi, P., Flamand, V., et al., African trypanosomiasis: naturally occurring regulatory T cells favor trypanotolerance by limiting pathology associated with sustained type 1 inflammation. J. Immunol. 2007. 179: 2748-2757.
9. Noel, W., Hassanzadeh, G., Raes, G., Namangala, B., Daems, I., Brys, L., Brombacher, F., et al., Infection stage-dependent modulation of macrophage activation in Trypanosoma congolense-resistant and -susceptible mice. Infect. Immun. 2002. 70: 6180-6187.
10. +T cells mediates early mortality in highly susceptible mice. J. Immunol. 2006. 176: 1724-1732.
11. Mou, Z., Jia, P., Kuriakose, S., Khadem, F. and Uzonna, J. E., Interleukin-17-mediated control of parasitemia in experimental Trypanosoma congolense infection in mice. Infect. Immun. 2010. 78: 5271-5279.
12. Uzonna, J. E., Kaushik, R. S., Gordon, J. R. and Tabel, H., Immunoregulation in experimental murine Trypanosoma congolense infection: anti-IL-10 antibodies reverse trypanosome-mediated suppression of lymphocyte proliferation in vitro and moderately prolong the lifespan of genetically susceptible BALB/c mice. Parasite Immunol. 1998. 20: 293-302.
13. Bosschaerts, T., Guilliams, M., Noel, W., Herin, M., Burk, R. F., Hill, K. E., Brys, L., et al., Alternatively activated myeloid cells limit pathogenicity associated with African trypanosomiasis through the IL-10 inducible gene selenoprotein P. J. Immunol. 2008. 180: 6168-6175.
14. Shi, M. Q., Wei, G. J. and Tabel, H., Trypanosoma congolense infections: MHC class II-restricted immune responses mediate either protection or disease, depending on IL-10 function. Parasite Immunol. 2007. 29: 107-111.
15. Cao, S., Zhang, X., Edwards, J. P. and Mosser, D. M., NF-kappaB1 (p50) homodimers differentially regulate pro- and anti-inflammatory cytokines in macrophages. J. Biol. Chem. 2006. 281: 26041-26050.
16. Carmody, R. J., Ruan, Q., Palmer, S., Hilliard, B. and Chen, Y. H., Negative regulation of toll-like receptor signaling by NF-kappaB p50 ubiquitination blockade. Science 2007. 317: 675-678.
17. Driessler, F., Venstrom, K., Sabat, R., Asadullah, K. and Schottelius, A. J., Molecular mechanisms of interleukin-10-mediated inhibition of NF-kappaB activity: a role for p50. Clin. Exp. Immunol. 2004. 135: 64-73.
18. Saccani, A., Schioppa, T., Porta, C., Biswas, S. K., Nebuloni, M., Vago, L., Bottazzi, B., et al., p50 nuclear factor-kappaB overexpression in tumor-associated macrophages inhibits M1 inflammatory responses and antitumor resistance. Cancer Res. 2006. 66: 11432-11440.
19. Smallie, T., Ricchetti, G., Horwood, N. J., Feldmann, M., Clark, A. R. and Williams, L. M., IL-10 inhibits transcription elongation of the human TNF gene in primary macrophages. J. Exp. Med. 2010. 207: 2081-2088.
20. Geissmann, F., Auffray, C., Palframan, R., Wirrig, C., Ciocca, A., Campisi, L., Narni-Mancinelli, E. and Lauvau, G., Blood monocytes: distinct subsets, how they relate to dendritic cells, and their possible roles in the regulation of T-cell responses. Immunol. Cell. Biol. 2008. 86: 398-408.
21. Guilliams, M., Bosschaerts, T., Herin, M., Hunig, T., Loi, P., Flamand, V., De Baetselier, P. and Beschin, A., Experimental expansion of the regulatory T cell population increases resistance to African trypanosomiasis. J. Infect. Dis. 2008. 198: 781-791.
22. Guilliams, M., Movahedi, K., Bosschaerts, T., VandenDriessche, T., Chuah, M. K., Herin, M., Acosta-Sanchez, A., et al., IL-10 dampens TNF/inducible nitric oxide synthase-producing dendritic cell-mediated pathogenicity during parasitic infection. J. Immunol. 2009. 182: 1107-1118.
23. Stijlemans, B., Baral, T. N., Guilliams, M., Brys, L., Korf, J., Drennan, M., Van Den Abbeele, J., et al., A glycosylphosphatidylinositol-based treatment alleviates trypanosomiasis-associated immunopathology. J. Immunol. 2007. 179: 4003-4014.
24. Siewe, L., Bollati-Fogolin, M., Wickenhauser, C., Krieg, T., Muller, W. and Roers, A., Interleukin-10 derived from macrophages and/or neutrophils regulates the inflammatory response to LPS but not the response to CpG DNA. Eur. J. Immunol. 2006. 36: 3248-3255.
25. Porta, C., Rimoldi, M., Raes, G., Brys, L., Ghezzi, P., Di Liberto, D., Dieli, F., et al., Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor kappaB. Proc. Natl. Acad. Sci. USA 2009. 106: 14978-14983.
26. Benoit, M., Desnues, B. and Mege, J. L., Macrophage polarization in bacterial infections. J. Immunol. 2008. 181: 3733-3739.
27. Serbina, N. V., Jia, T., Hohl, T. M. and Pamer, E. G., Monocyte-mediated defense against microbial pathogens. Annu. Rev. Immunol. 2008. 26: 421-452.
28. Aldridge, J. R., Jr., Moseley, C. E., Boltz, D. A., Negovetich, N. J., Reynolds, C., Franks, J., Brown, S. A., et al., TNF/iNOS-producing dendritic cells are the necessary evil of lethal influenza virus infection. Proc. Natl. Acad. Sci. USA 2009. 106: 5306-5311.
29. De Trez, C., Magez, S., Akira, S., Ryffel, B., Carlier, Y. and Muraille, E., iNOS-producing inflammatory dendritic cells constitute the major infected cell type during the chronic Leishmania major infection phase of C57BL/6 resistant mice. PLoS Pathog. 2009. 5: e1000494.
30. Lykens, J. E., Terrell, C. E., Zoller, E. E., Divanovic, S., Trompette, A., Karp, C. L., Aliberti, J., et al., Mice with a selective impairment of IFN-gamma signaling in macrophage lineage cells demonstrate the critical role of IFN-gamma-activated macrophages for the control of protozoan parasitic infections in vivo. J. Immunol. 2010. 184: 877-885.
31. Herbert, D. R., Orekov, T., Perkins, C. and Finkelman, F. D., IL-10 and TGF-beta redundantly protect against severe liver injury and mortality during acute schistosomiasis. J. Immunol. 2008. 181: 7214-7220.
32. Li, K., Xu, W., Guo, Q., Jiang, Z., Wang, P., Yue, Y. and Xiong, S., Differential macrophage polarization in male and female BALB/c mice infected with coxsackievirus B3 defines susceptibility to viral myocarditis. Circ. Res. 2009. 105: 353-364.
33. Fairweather, D. and Cihakova, D., Alternatively activated macrophages in infection and autoimmunity. J. Autoimmun. 2009. 33: 222-230.
34. Maynard, C. L. and Weaver, C. T., Diversity in the contribution of interleukin-10 to T-cell-mediated immune regulation. Immunol. Rev. 2008. 226: 219-233.
35. Schreiber, T., Ehlers, S., Heitmann, L., Rausch, A., Mages, J., Murray, P. J., Lang, R. and Holscher, C., Autocrine IL-10 induces hallmarks of alternative activation in macrophages and suppresses antituberculosis effector mechanisms without compromising T cell immunity. J. Immunol. 2009. 183: 1301-1312.
36. Saraiva, M. and O'Garra, A., The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 2010. 10: 170-181.
37. Pils, M. C., Pisano, F., Fasnacht, N., Heinrich, J. M., Groebe, L., Schippers, A., Rozell, B., et al., Monocytes/macrophages and/or neutrophils are the target of IL-10 in the LPS endotoxemia model. Eur. J. Immunol. 2010. 40: 443-448.
38. Williams, L. M., Ricchetti, G., Sarma, U., Smallie, T. and Foxwell, B. M., Interleukin-10 suppression of myeloid cell activation - a continuing puzzle. Immunology 2004. 113: 281-292.
39. Mancino, A. and Lawrence, T., Nuclear factor-kappaB and tumor-associated macrophages. Clin. Cancer Res. 2010. 16: 784-789.
40. Ziegler-Heitbrock, L., The p50-homodimer mechanism in tolerance to LPS. J. Endotoxin Res. 2001. 7: 219-222.
41. Bonizzi, G. and Karin, M., The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 2004. 25: 280-288.
42. Bosschaerts, T., Guilliams, M., Stijlemans, B., Morias, Y., Engel, D., Tacke, F., Herin, M., et al., Tip-DC development during parasitic infection is regulated by IL-10 and requires CCL2/CCR2, IFN-gamma and MyD88 signaling. PLoS Pathog. 2010. 6.
43. Holub, M., Cheng, C. W., Mott, S., Wintermeyer, P., van Rooijen, N. and Gregory, S. H., Neutrophils sequestered in the liver suppress the proinflammatory response of Kupffer cells to systemic bacterial infection. J. Immunol. 2009. 183: 3309-3316.
44. Ocuin, L. M., Bamboat, Z. M., Balachandran, V. P., Cavnar, M. J., Obaid, H., Plitas, G. and DeMatteo, R. P., Neutrophil IL-10 suppresses peritoneal inflammatory monocytes during polymicrobial sepsis. J. Leukoc. Biol. 2011. 89: 423-432.
45. Akol, G. W. and Murray, M., Early events following challenge of cattle with tsetse infected with Trypanosoma congolense: development of the local skin reaction. Vet. Rec. 1982. 110: 295-302.
46. Emery, D. L. and Moloo, S. K., The dynamics of the cellular reactions elicited in the skin of goats by Glossina morsitans morsitans infected with Trypanosoma (Nannomonas) congolense or T. (Duttonella) vivax. Acta Trop. 1981. 38: 15-28.
47. Ghassabeh, G. H., De Baetselier, P., Brys, L., Noel, W., Van Ginderachter, J. A., Meerschaut, S., Beschin, A., et al., Identification of a common gene signature for type II cytokine-associated myeloid cells elicited in vivo in different pathologic conditions. Blood 2006. 108: 575-583.