Macrophages as IL-25/IL-33-Responsive Cells Play an Important Role in the Induction of Type 2 Immunity

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Yang, Zhonghan ^a,b   Grinchuk, Viktoriya ^a   Urban, Joseph F ^c   Bohl, Jennifer ^a   Sun, Rex ^a   Notari, Luigi ^a   Yan, Shu ^a   Ramalingam, Thirumalai ^d   Keegan, Achsah D ^a   Wynn, Thomas A ^d   Shea Donohue, Terez ^a   Zhao, Aiping ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b SUN YAT SEN UNIVERSITY   (China)

^c BELTSVILLE HUMAN NUTRITION RESEARCH CENTER   (United States)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 13; INTERLEUKIN 25; INTERLEUKIN 33; INTERLEUKIN 4 RECEPTOR ALPHA; INTERLEUKIN 5; STAT6 PROTEIN;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOCRINE EFFECT; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; HELIGMOSOMOIDES; HELIGMOSOMOIDES BAKERI; IMMUNOCOMPETENT CELL; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; MACROPHAGE; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PROTEIN INDUCTION; STRONGYLOIDIASIS; WORM EXPULSION;

HELIGMOSOMOIDES; MUS;

EID: 84875409549     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059441     Document Type: Article

References (44)

1. Zhao A, Urban JF, Sun R, Stiltz J, Morimoto M, et al. (2010) Critical Role of IL-25 in Nematode Infection-Induced Alterations in Intestinal Function. J Immunol 185: 6921-6929.
2. Humphreys NE, Xu D, Hepworth MR, Liew FY, Grencis RK, (2008) IL-33, a Potent Inducer of Adaptive Immunity to Intestinal Nematodes. The Journal of Immunology 180: 2443-2449.
3. Fort MM, Cheung J, Yen D, Li J, Zurawski SM, et al. (2001) IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity. 15: 985-995.
4. Saenz SA, Siracusa MC, Perrigoue JG, Spencer SP, Urban Jr JF, et al. (2010) IL25 elicits a multipotent progenitor cell population that promotes TH2 cytokine responses. Nature 464: 1362-1366.
5. Moro K, Yamada T, Tanabe M, Takeuchi T, Ikawa T, Kawamoto H, et al. (2010) Innate production of TH2 cytokines by adipose tissue-associated c-Kit+Sca-1+ lymphoid cells. Nature 463: 540-544.
6. Neill DR, Wong SH, Bellosi A, Flynn RJ, Daly M, et al. (2010) Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464: 1367-1370.
7. Price AE, Liang HE, Sullivan BM, Reinhardt RL, Eisley CJ, et al. (2010) Systemically dispersed innate IL-13ΓÇôexpressing cells in type 2 immunity. Proceedings of the National Academy of Sciences 107: 11489-11494.
8. Lee SH, Starkey PM, Gordon S, (1985) Quantitative analysis of total macrophage content in adult mouse tissues. Immunochemical studies with monoclonal antibody F4/80. J. Exp. Med. 161: 475-489.
9. Platt AM, Mowat AM, (2008) Mucosal macrophages and the regulation of immune responses in the intestine. Immunology Letters 119: 22-31.
10. Abraham C, Medzhitov R (2011) Interactions Between the Host Innate Immune System and Microbes in Inflammatory Bowel Disease. Gastroenterology 1729-1737.
11. Anderson GP (2008) Endotyping asthma: new insights into key pathogenic mechanisms in a complex, heterogeneous disease. Lancet 1107-1119.
12. Anthony RM, Urban Jr JF, Alem F, Hamed HA, Rozo CT, et al. (2006) Memory T(H)2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat. Med. 12: 955-960.
13. Zhao A, Urban Jr JF, Anthony RM, Sun R, Stiltz J, et al. (2008) Th2 Cytokine-Induced Alterations in Intestinal Smooth Muscle Function Depend on Alternatively Activated Macrophages. Gastroenterology 135: 217-225.
14. Chang YJ, Kim HY, Albacker LA, Baumgarth N, McKenzie ANJ, et al. (2011) Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat Immunol 12: 631-638.
15. Kim EY, Battaile JT, Patel AC, You Y, Agapov E, et al. (2008) Persistent activation of an innate immune response translates respiratory viral infection into chronic lung disease. Nat Med 14: 633-640.
16. Shirey KA, Pletneva LM, Puche AC, Keegan AD, Prince GA, et al. (2010) Control of RSV-induced lung injury by alternatively activated macrophages is IL-4R[alpha]-, TLR4-, and IFN-[beta]-dependent. Mucosal Immunol 3: 291-300.
17. Shirey KA, Cole LE, Keegan AD, Vogel SN, (2008) Francisella tularensis Live Vaccine Strain Induces Macrophage Alternative Activation as a Survival Mechanism. The Journal of Immunology 181: 4159-4167.
18. Kang Z, Swaidani S, Yin W, Wang C, Barlow J, et al. (2012) Epithelial Cell-Specific Act1 Adaptor Mediates Interleukin-25-Dependent Helminth Expulsion through Expansion of Lin−c-Kit+ Innate Cell Population. Immunity 36: 821-833.
19. Zhang X, Goncalves R, Mosser DM, (2001) The Isolation and Characterization of Murine Macrophages. John Wiley & Sons, Inc. 14: 14.
20. Zhao A, McDermott J, Urban JF Jr, Gause W, Madden KB, et al. (2003) Dependence of IL-4, IL-13, and nematode-induced alterations in murine small intestinal smooth muscle contractility on Stat6 and enteric nerves. J. Immunol. 171: 948-954.
21. Urban JF Jr, Noben-Trauth N, Donaldson DD, Madden KB, Morris SC, et al. (1998) IL-13, IL-4Ralpha, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity. 8: 255-264.
22. Zhao A, Bossone C, Pineiro-Carrero V, Shea-Donohue T, (2001) Colitis-induced alterations in adrenergic control of circular smooth muscle in vitro in rats 8. J. Pharmacol. Exp. Ther. 299: 768-774.
23. Shea-Donohue T, Sullivan C, Finkelman FD, Madden KB, Morris SC, et al. (2001) The role of IL-4 in Heligmosomoides polygyrus-induced alterations in murine intestinal epithelial cell function. J. Immunol. 167: 2234-2239.
24. El Asmar R, Panigrahi P, Bamford P, Berti I, Not T, et al. (2002) Host-dependent zonulin secretion causes the impairment of the small intestine barrier function after bacterial exposure. Gastroenterology 123: 1607-1615.
25. Morimoto M, Zhao A, Sun R, Stiltz J, Madden KB, et al. (2009) IL-13 Receptor {alpha}2 Regulates the Immune and Functional Response to Nippostrongylus brasiliensis Infection. J Immunol 183: 1934-1939.
26. Shea-Donohue T, Fasano A, Smith A, Zhao A, (2010) Enteric pathogens and gut function: Role of cytokines and STATs. Gut Microbes 1: 316-324.
27. Gordon S, Martinez FO, (2010) Alternative Activation of Macrophages: Mechanism and Functions. Immunity 32: 593-604.
28. Zhao A, Urban JF Jr, Morimoto M, Elfrey JE, Madden KB, et al. (2006) Contribution of 5-HT2A receptor in nematode infection-induced murine intestinal smooth muscle hypercontractility. Gastroenterology 131: 568-578.
29. Madden KB, Whitman L, Sullivan C, Gause WC, Urban JF Jr, et al. (2002) Role of STAT6 and mast cells in IL-4- and IL-13-induced alterations in murine intestinal epithelial cell function. J. Immunol. 169: 4417-4422.
30. Madden KB, Yeung KA, Zhao A, Gause WC, Finkelman FD, et al. (2004) Enteric nematodes induce stereotypic STAT6-dependent alterations in intestinal epithelial cell function. J. Immunol. 172: 5616-5621.
31. Owyang AM, Zaph C, Wilson EH, Guild KJ, McClanahan T, et al. (2006) Interleukin 25 regulates type 2 cytokine-dependent immunity and limits chronic inflammation in the gastrointestinal tract. J. Exp. Med. 203: 843-849.
32. Finkelman FD, Shea-Donohue T, Goldhill J, Sullivan CA, Morris SC, et al. (1997) Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models. Annu. Rev. Immunol. 15: 505-533.
33. Zaph C, Du Y, Saenz SA, Nair MG, Perrigoue JG, et al. (2008) Commensal-dependent expression of IL-25 regulates the IL-23-IL-17 axis in the intestine. The Journal of Experimental Medicine 205: 2191-2198.
34. Liew FY, Pitman NI, McInnes IB, (2010) Disease-associated functions of IL-33: the new kid in the IL-1 family. Nat Rev Immunol 10: 103-110.
35. Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, et al. (2005) IL-33, an Interleukin-1-like Cytokine that Signals via the IL-1 Receptor-Related Protein ST2 and Induces T Helper Type 2-Associated Cytokines. Immunity 23: 479-490.
36. Wang YH, Angkasekwinai P, Lu N, Voo KS, Arima K, et al. (2007) IL-25 augments type 2 immune responses by enhancing the expansion and functions of TSLP-DC-activated Th2 memory cells. J. Exp. Med. 204: 1837-1847.
37. Caruso R, Sarra M, Stolfi C, Rizzo A, Fina D, et al. (2009) Interleukin-25 inhibits interleukin-12 production and Th1 cell-driven inflammation in the gut. Gastroenterology 136: 2270-2279.
38. Espinassous Q, (2009) IL-33 enhances lipopolysaccharide-induced inflammatory cytokine production from mouse macrophages by regulating lipopolysaccharide receptor complex. J. Immunol. 183: 1446-1455.
39. Rizzo A, Monteleone I, Fina D, Stolfi C, Caruso R, et al. (2011) Inhibition of colitis by IL-25 associates with induction of alternatively activated macrophages. Inflammatory Bowel Diseases. 18: 449-459.
40. Joshi A, Oak S, Hartigan A, Finn W, Kunkel S, et al. (2010) Interleukin-33 contributes to both M1 and M2 chemokine marker expression in human macrophages. BMC Immunology 11: 52.
41. Zhao A, Morimoto M, Dawson H, Elfrey JE, Madden KB, et al. (2005) Immune Regulation of Protease-Activated Receptor-1 Expression in Murine Small Intestine during Nippostrongylus brasiliensis Infection. J Immunol 175: 2563-2569.
42. Voehringer D, Reese TA, Huang X, Shinkai K, Locksley RM, (2006) Type 2 immunity is controlled by IL-4/IL-13 expression in hematopoietic non-eosinophil cells of the innate immune system. The Journal of Experimental Medicine 203: 1435-1446.
43. Siracusa MC, Comeau MR, Artis D, (2011) New insights into basophil biology: initiators, regulators, and effectors of type 2 inflammation. Annals of the New York Academy of Sciences 1217: 166-177.
44. Sullivan BM, Liang HE, Bando JK, Wu D, Cheng LE, et al. (2011) Genetic analysis of basophil function in vivo. Nat Immunol 12: 527-535.