A novel regulatory macrophage induced by a helminth molecule instructs IL-10 in CD4+ T cells and protects against mucosal inflammation

Journal of Immunology

Volumn 194, Issue 4, 2015, Pages 1555-1564

  Ziegler, Thomas ^a   Rausch, Sebastian ^a   Steinfelder, Svenja ^a   Klotz, Christian ^b   Hepworth, Matthew R ^a,e   Kühl, Anja A ^c   Burda, Paul Christian ^d,f   Lucius, Richard ^d   Hartmann, Susanne ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b ROBERT KOCH INSTITUTE   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d HUMBOLDT UNIVERSITY   (Germany)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

^f UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ACANTHOCHEILONEMA VITEAE CYSTATIN; ANTIINFLAMMATORY AGENT; ARGINASE 1; CCL1 CHEMOKINE; CD32 ANTIGEN; CYSTATIN; IMMUNOGLOBULIN E; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 LIGAND 2; SPHINGOSINE KINASE 1; UNCLASSIFIED DRUG; IL10 PROTEIN, MOUSE; IMMUNOSUPPRESSIVE AGENT; PARASITE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARGINASE 1 GENE; ARTICLE; BRONCHUS MUCUS; CCL1 GENE; CD4+ T LYMPHOCYTE; COLITIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; EOSINOPHIL; FEMALE; LIGHT GENE; MACROPHAGE; MOUSE; MUCOSA INFLAMMATION; NONHUMAN; PHENOTYPE; RESPIRATORY TRACT INFLAMMATION; SPHINGOSINE KINASE 1 GENE; TH2 CELL; ACANTHOCHEILONEMA; ADOPTIVE TRANSFER; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; DISEASE MODEL; IMMUNOLOGY; INFLAMMATION; MUCOSAL IMMUNITY; PNEUMONIA;

ACANTHOCHEILONEMA; ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, HELMINTH; CD4-POSITIVE T-LYMPHOCYTES; COLITIS; DISEASE MODELS, ANIMAL; FEMALE; IMMUNITY, MUCOSAL; IMMUNOSUPPRESSIVE AGENTS; INFLAMMATION; INTERLEUKIN-10; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PNEUMONIA;

EID: 84922511732     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401217     Document Type: Article

References (42)

1. McSorley, H. J., J. P. Hewitson, and R. M. Maizels. 2013. Immunomodulation by helminth parasites: defining mechanisms and mediators. Int. J. Parasitol. 43: 301-310.
2. Summers, R. W., D. E. Elliott, J. F. Urban, Jr., R. A. Thompson, and J. V. Weinstock. 2005. Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128: 825-832.
3. Broadhurst, M. J., J. M. Leung, V. Kashyap, J. M. McCune, U. Mahadevan, J. H. McKerrow, and P. Loke. 2010. IL-22+ CD4+ T cells are associated with therapeutic trichuris trichiura infection in an ulcerative colitis patient. Sci. Transl. Med. 2: 60ra88.
4. Pineda, M. A., F. Lumb, M. M. Harnett, and W. Harnett. 2014. ES-62, a therapeutic anti-inflammatory agent evolved by the filarial nematode Acanthochei-lonema viteae. Mol. Biochem. Parasitol. 194: 1-8.
5. Schierack, P., R. Lucius, B. Sonnenburg, K. Schilling, and S. Hartmann. 2003. Parasite-specific immunomodulatory functions of filarial cystatin. Infect. Immun. 71: 2422-2429.
6. Hartmann, S., and R. Lucius. 2003. Modulation of host immune responses by nematode cystatins. Int. J. Parasitol. 33: 1291-1302.
7. Schnoeller, C., S. Rausch, S. Pillai, A. Avagyan, B. M. Wittig, C. Loddenkemper, A. Hamann, E. Hamelmann, R. Lucius, and S. Hartmann. 2008. A helminth immunomodulator reduces allergic and inflammatory responses by induction of IL-10-producing macrophages. J. Immunol. 180: 4265-4272.
8. Klotz, C., T. Ziegler, A. S. Figueiredo, S. Rausch, M. R. Hepworth, N. Obsivac, C. Sers, R. Lang, P. Hammerstein, R. Lucius, and S. Hartmann. 2011. A helminth immunomodulator exploits host signaling events to regulate cytokine production in macrophages. PLoS Pathog. 7: e1001248.
9. Mantovani, A., A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati. 2004. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25: 677-686.
10. Martinez, F. O., A. Sica, A. Mantovani, and M. Locati. 2008. Macrophage activation and polarization. Front. Biosci. 13: 453-461.
11. Wang, W., M. H. Graeler, and E. J. Goetzl. 2005. Type 4 sphingosine 1-phos-phate G protein-coupled receptor (S1P4) transduces S1P effects on T cell proliferation and cytokine secretion without signaling migration. FASEB J. 19: 1731-1733.
12. Pesce, J. T., T. R. Ramalingam, M. M. Mentink-Kane, M. S. Wilson, K. C. El Kasmi, A. M. Smith, R. W. Thompson, A. W. Cheever, P. J. Murray, and T. A. Wynn. 2009. Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog. 5: e1000371.
13. Francisco, L. M., V. H. Salinas, K. E. Brown, V. K. Vanguri, G. J. Freeman, V. K. Kuchroo, and A. H. Sharpe. 2009. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J. Exp. Med. 206: 3015-3029.
14. Hang, L., T. Setiawan, A. M. Blum, J. Urban, K. Stoyanoff, S. Arihiro, H. C. Reinecker, and J. V. Weinstock. 2010. Heligmosomoides polygyrus infection can inhibit colitis through direct interaction with innate immunity. J. Immunol. 185: 3184-3189.
15. Chen, F., Z. Liu, W. Wu, C. Rozo, S. Bowdridge, A. Millman, N. Van Rooijen, J. F. Urban, Jr., T. A. Wynn, and W. C. Gause. 2012. An essential role for TH2-type responses in limiting acute tissue damage during experimental helminth infection. Nat. Med. 18: 260-266.
16. Esser-von Bieren, J., I. Mosconi, R. Guiet, A. Piersgilli, B. Volpe, F. Chen, W. C. Gause, A. Seitz, J. S. Verbeek, and N. L. Harris. 2013. Antibodies trap tissue migrating helminth larvae and prevent tissue damage by driving IL-4Ra-independent alternative differentiation of macrophages. PLoS Pathog. 9: e1003771.
17. Daniłowicz-Luebert, E., S. Steinfelder, A. A. Kühl, G. Drozdenko, R. Lucius, M. Worm, E. Hamelmann, and S. Hartmann. 2013. A nematode immunomodulator suppresses grass pollen-specific allergic responses by controlling excessive Th2 inflammation. Int. J. Parasitol. 43: 201-210.
18. Brem-Exner, B. G., C. Sattler, J. A. Hutchinson, G. E. Koehl, K. Kronenberg, S. Farkas, S. Inoue, C. Blank, S. J. Knechtle, H. J. Schlitt, et al. 2008. Macrophages driven to a novel state of activation have anti-inflammatory properties in mice. J. Immunol. 180: 335-349.
19. Hunter, M. M., A. Wang, K. S. Parhar, M. J. Johnston, N. Van Rooijen, P. L. Beck, and D. M. McKay. 2010. In vitro-derived alternatively activated macrophages reduce colonic inflammation in mice. Gastroenterology 138: 1395-1405.
20. Tierney, J. B., M. Kharkrang, and A. C. La Flamme. 2009. Type II-activated macrophages suppress the development of experimental autoimmune encepha-lomyelitis. Immunol. Cell Biol. 87: 235-240.
21. Nishida, M., Y. Okumura, S. Fujimoto, I. Shiraishi, T. Itoi, and K. Hamaoka. 2005. Adoptive transfer of macrophages ameliorates renal fibrosis in mice. Biochem. Biophys. Res. Commun. 332: 11-16.
22. Cao, Q., Y. Wang, D. Zheng, Y. Sun, Y. Wang, V. W. Lee, G. Zheng, T. K. Tan, J. Ince, S. I. Alexander, and D. C. Harris. 2010. IL-10/TGF-beta-modified macrophages induce regulatory T cells and protect against adriamycin nephro-sis. J. Am. Soc. Nephrol. 21: 933-942.
23. Wang, Y., Y. P. Wang, G. Zheng, V. W. Lee, L. Ouyang, D. H. Chang, D. Mahajan, J. Coombs, Y. M. Wang, S. I. Alexander, and D. C. Harris. 2007. Ex vivo programmed macrophages ameliorate experimental chronic inflammatory renal disease. Kidney Int. 72: 290-299.
24. Leung, G., A. Wang, M. Fernando, V. C. Phan, and D. M. McKay. 2013. Bone marrow-derived alternatively activated macrophages reduce colitis without promoting fibrosis: participation of IL-10. Am. J. Physiol. Gastrointest. Liver Physiol. 304: G781-G792.
25. Hutchinson, J. A., F. Gövert, P. Riquelme, J. H. Bräsen, B. G. Brem-Exner, M. Matthäi, M. Schulze, L. Renders, U. Kunzendorf, E. K. Geissler, and F. Fändrich. 2009. Administration of donor-derived transplant acceptance-inducing cells to the recipients of renal transplants from deceased donors is technically feasible. Clin. Transplant. 23: 140-145.
26. Hutchinson, J. A., P. Riquelme, B. Sawitzki, S. Tomiuk, P. Miqueu, M. Zuhayra, H. H. Oberg, A. Pascher, U. Lützen, U. Janssen, et al. 2011. Cutting edge: im-munological consequences and trafficking of human regulatory macrophages administered to renal transplant recipients. J. Immunol. 187: 2072-2078.
27. Hutchinson, J. A., P. Riquelme, and E. K. Geissler. 2012. Human regulatory macrophages as a cell-based medicinal product. Curr. Opin. Organ Transplant. 17: 48-54.
28. Fleming, B. D., and D. M. Mosser. 2011. Regulatory macrophages: setting the threshold for therapy. Eur. J. Immunol. 41: 2498-2502.
29. Hawrylowicz, C. M., and A. O'Garra. 2005. Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma. Nat. Rev. Immunol. 5: 271-283.
30. Saraiva, M., and A. O'Garra. 2010. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10: 170-181.
31. Vieira, A. T., C. T. Fagundes, A. L. Alessandri, M. G. Castor, R. Guabiraba, V. O. Borges, K. D. Silveira, E. L. Vieira, J. L. Gonçalves, T. A. Silva, et al. 2009. Treatment with a novel chemokine-binding protein or eosinophil lineage-ablation protects mice from experimental colitis. Am. J. Pathol. 175: 2382-2391.
32. Hall, L. J., C. T. Murphy, A. Quinlan, G. Hurley, F. Shanahan, K. Nally, and S. Melgar. 2013. Natural killer cells protect mice from DSS-induced colitis by regulating neutrophil function via the NKG2A receptor. Mucosal Immunol. 6: 1016-1026.
33. Mowat, A. M., and C. C. Bain. 2011. Mucosal macrophages in intestinal ho-meostasis and inflammation. J. Innate Immun. 3: 550-564.
34. Mosser, D. M., and J. P. Edwards. 2008. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 8: 958-969.
35. Bronte, V., and P. Zanovello. 2005. Regulation of immune responses by L-arginine metabolism. Nat. Rev. Immunol. 5: 641-654.
36. van der Werf, N., S. A. Redpath, M. Azuma, H. Yagita, and M. D. Taylor. 2013. Th2 cell-intrinsic hypo-responsiveness determines susceptibility to helminth infection. PLoS Pathog. 9: e1003215.
37. Xue, J., S. V. Schmidt, J. Sander, A. Draffehn, W. Krebs, I. Quester, D. De Nardo, T. D. Gohel, M. Emde, L. Schmidleithner, et al. 2014. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity 40: 274-288.
38. Riquelme, P., S. Tomiuk, A. Kammler, F. Fändrich, H. J. Schlitt, E. K. Geissler, and J. A. Hutchinson. 2013. IFN-γ-induced iNOS expression in mouse regulatory macrophages prolongs allograft survival in fully immunocompetent recipients. Mol. Ther. 21: 409-422.
39. Atochina, O., T. Daly-Engel, D. Piskorska, E. McGuire, and D. A. Harn. 2001. A schistosome-expressed immunomodulatory glycoconjugate expands peritoneal Gr1(+) macrophages that suppress naive CD4(+) T cell proliferation via an IFN-gamma and nitric oxide-dependent mechanism. J. Immunol. 167: 4293-4302.
40. Smith, P., N. E. Mangan, C. M. Walsh, R. E. Fallon, A. N. McKenzie, N. van Rooijen, and P. G. Fallon. 2007. Infection with a helminth parasite prevents experimental colitis via a macrophage-mediated mechanism. J. Immunol. 178: 4557-4566.
41. Murphy, J., R. Summer, A. A. Wilson, D. N. Kotton, and A. Fine. 2008. The prolonged life-span of alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 38: 380-385.
42. Potts, B. E., M. L. Hart, L. L. Snyder, D. Boyle, D. A. Mosier, and S. K. Chapes. 2008. Differentiation of C2D macrophage cells after adoptive transfer. Clin. Vaccine Immunol. 15: 243-252.