Neutrophils prime a long-lived effector macrophage phenotype that mediates accelerated helminth expulsion

Nature Immunology

Volumn 15, Issue 10, 2014, Pages 938-946

  Chen, Fei ^a,b   Wu, Wenhui ^a,b   Millman, Ariel ^a,b   Craft, Joshua F ^c   Chen, Eunice ^c   Patel, Nirav ^a,b   Boucher, Jean L ^d   Urban, Joseph F ^e   Kim, Charles C ^c   Gause, William C ^a,b  

^a The State University of New Jersey   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e BELTSVILLE HUMAN NUTRITION RESEARCH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 13; CYTOKINE; INTERLEUKIN 4 RECEPTOR ALPHA; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EFFECTOR CELL; FEMALE; GENETIC TRANSCRIPTION; HELMINTH; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; LARVA; MACROPHAGE; MOUSE; NEUTROPHIL; NIPPOSTRONGYLUS BRASILIENSIS; NONHUMAN; PARASITE CLEARANCE; PHENOTYPE; PRIORITY JOURNAL; ADAPTIVE IMMUNITY; ANIMAL; BAGG ALBINO MOUSE; CELL ADHESION; CELL CULTURE; DISEASE RESISTANCE; DNA MICROARRAY; FLOW CYTOMETRY; GENETICS; HOST PARASITE INTERACTION; IMMUNOLOGY; KNOCKOUT MOUSE; LUNG; METABOLISM; NIPPOSTRONGYLUS; PARASITOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRONGYLE INFECTION;

ADAPTIVE IMMUNITY; ANIMALS; CELL ADHESION; CELLS, CULTURED; CYTOKINES; DISEASE RESISTANCE; FEMALE; FLOW CYTOMETRY; HOST-PARASITE INTERACTIONS; INTERLEUKIN-13; INTERLEUKIN-4 RECEPTOR ALPHA SUBUNIT; LARVA; LUNG; MACROPHAGES; MICE, INBRED BALB C; MICE, KNOCKOUT; NEUTROPHILS; NIPPOSTRONGYLUS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STRONGYLIDA INFECTIONS; TRANSCRIPTOME;

EID: 84911102298     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2984     Document Type: Article

References (54)

1. King, C.H. Health metrics for helminthic infections. Adv. Parasitol. 73, 51-69 (2010).
2. Salgame, P., Yap, G.S. & Gause, W.C. Effect of helminth-induced immunity on infections with microbial pathogens. Nat. Immunol. 14, 1118-1126 (2013).
3. Gaze, S. et al. Characterising the mucosal and systemic immune responses to experimental human hookworm infection. PLoS Pathog. 8, e1002520 (2012).
4. Anthony, R.M., Rutitzky, L.I., Urban, J.F. Jr., Stadecker, M.J. & Gause, W.C. Protective immune mechanisms in helminth infection. Nat. Rev. Immunol. 7, 975-987 (2007).
5. Gause, W.C., Wynn, T.A. & Allen, J.E. Type 2 immunity and wound healing: evolutionary refnement of adaptive immunity by helminths. Nat. Rev. Immunol. 13, 607-614 (2013).
6. Harvie, M. et al. The lung is an important site for priming CD4 T-cell-mediated protective immunity against gastrointestinal helminth parasites. Infect. Immun. 78, 3753-3762 (2010).
7. Maizels, R.M. et al. Immune modulation and modulators in Heligmosomoides polygyrus infection. Exp. Parasitol. 132, 76-89 (2012).
8. Zhao, A. et al. 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 (2003).
9. Harris, N. & Gause, W.C. To B or not to B: B cells and the Th2-type immune response to helminths. Trends Immunol. 32, 80-88 (2011).
10. Finkelman, F.D. et al. Interleukin-4-and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol. Rev. 201, 139-155 (2004).
11. Herbert, D.R. et al. Intestinal epithelial cell secretion of RELM-β protects against gastrointestinal worm infection. J. Exp. Med. 206, 2947-2957 (2009).
12. Knott, M.L. et al. Impaired resistance in early secondary Nippostrongylus brasiliensis infections in mice with defective eosinophilopoeisis. Int. J. Parasitol. 37, 1367-1378 (2007).
13. H2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat. Med. 12, 955-960 (2006).
14. Yang, Z. et al. Macrophages as IL-25/IL-33-responsive cells play an important role in the induction of type 2 immunity. PLoS ONE 8, e59441 (2013).
15. Morimoto, M. et al. Peripheral CD4 T cells rapidly accumulate at the host: parasite interface during an infammatory Th2 memory response. J. Immunol. 172, 2424-2430 (2004).
16. Bonne-Année, S. et al. Human and mouse macrophages collaborate with neutrophils to kill larval Strongyloides stercoralis. Infect. Immun. 81, 3346-3355 (2013).
17. Harvie, M., Camberis, M. & Le Gros, G. Development of CD4 T cell dependent immunity against N. brasiliensis infection. Frontiers Immunol. 4, 74 (2013).
18. Katona, I.M., Urban, J.F. Jr. & Finkelman, F.D. The role of L3T4+ and Lyt-2+ T cells in the IgE response and immunity to Nippostrongylus brasiliensis. J. Immunol. 140, 3206-3211 (1988).
19. Liu, Q. et al. B cells have distinct roles in host protection against different nematode parasites. J. Immunol. 184, 5213-5223 (2010).
20. Patel, N., Kreider, T., Urban, J.F. Jr. & Gause, W.C. Characterisation of effector mechanisms at the host:parasite interface during the immune response to tissue-dwelling intestinal nematode parasites. Int. J. Parasitol. 39, 13-21 (2009).
21. H2-type responses in limiting acute tissue damage during experimental helminth infection. Nat. Med. 18, 260-266 (2012).
22. Smith, K.A. et al. Type 2 innate immunity in helminth infection is induced redundantly and acts autonomously following CD11c+ cell depletion. Infect. Immun. 80, 3481-3489 (2012).
23. Obata-Ninomiya, K. et al. The skin is an important bulwark of acquired immunity against intestinal helminths. J. Exp. Med. 210, 2583-2589 (2013).
24. Kreider, T., Anthony, R.M., Urban, J.F. Jr. & Gause, W.C. Alternatively activated macrophages in helminth infections. Curr. Opin. Immunol. 19, 448-453 (2007).
25. Dobrovolskaia, M.A. & Vogel, S.N. Toll receptors, CD14, and macrophage activation and deactivation by LPS. Microbes Infect. 4, 903-914 (2002).
26. Murray, P.J. & Wynn, T.A. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11, 723-737 (2011).
27. Morris, S.M. Jr. Recent advances in arginine metabolism: roles and regulation of the arginases. Br. J. Pharmacol. 157, 922-930 (2009).
28. Ckless, K. et al. Inhibition of arginase activity enhances infammation in mice with allergic airway disease, in association with increases in protein S-nitrosylation and tyrosine nitration. J. Immunol. 181, 4255-4264 (2008).
29. Herbert, D.R. et al. Arginase I suppresses IL-12/IL-23p40-driven intestinal infammation during acute schistosomiasis. J. Immunol. 184, 6438-6446 (2010).
30. Bonne-Année, S., Hess, J.A. & Abraham, D. Innate and adaptive immunity to the nematode Strongyloides stercoralis in a mouse model. Immunol. Res. 51, 205-214 (2011).
31. Gong, D. et al. TGFβ signaling plays a critical role in promoting alternative macrophage activation. BMC Immunol. 13, 31 (2012).
32. Oo-puthinan, S. et al. The amino acids involved in the distinct carbohydrate specifcities between macrophage galactose-type C-type lectins 1 and 2 (CD301a and b) of mice. Biochim. Biophys. Acta 1780, 89-100 (2008).
33. Staples, K.J. et al. Phenotypic characterization of lung macrophages in asthmatic patients: overexpression of CCL17. J. Allergy Clin. Immunol. 130, 1404.e7-1412.e7 (2012).
34. Becker, H.M. et al. α1β1 integrin-mediated adhesion inhibits macrophage exit from a peripheral infammatory lesion. J. Immunol. 190, 4305-4314 (2013).
35. Huang, D.W., Sherman, B.T. & Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).
36. Durrant, W.E. & Dong, X. Systemic acquired resistance. Annu. Rev. Phytopathol. 42, 185-209 (2004).
37. Kurtz, J. Specifc memory within innate immune systems. Trends Immunol. 26, 186-192 (2005).
38. Netea, M.G., Quintin, J. & van der Meer, J.W. Trained immunity: a memory for innate host defense. Cell Host Microbe 9, 355-361 (2011).
39. Didierlaurent, A. et al. Sustained desensitization to bacterial Toll-like receptor ligands after resolution of respiratory infuenza infection. J. Exp. Med. 205, 323-329 (2008).
40. Reece, J.J., Siracusa, M.C. & Scott, A.L. Innate immune responses to lung-stage helminth infection induce alternatively activated alveolar macrophages. Infect. Immun. 74, 4970-4981 (2006).
41. Marsland, B.J., Kurrer, M., Reissmann, R., Harris, N.L. & Kopf, M. Nippostrongylus brasiliensis infection leads to the development of emphysema associated with the induction of alternatively activated macrophages. Eur. J. Immunol. 38, 479-488 (2008).
42. Satoh, T. et al. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat. Immunol. 11, 936-944 (2010).
43. Monticelli, S. & Natoli, G. Short-term memory of danger signals and environmental stimuli in immune cells. Nat. Immunol. 14, 777-784 (2013).
44. Mantovani, A., Cassatella, M.A., Costantini, C. & Jaillon, S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11, 519-531 (2011).
45. Galioto, A.M. et al. Role of eosinophils and neutrophils in innate and adaptive protective immunity to larval strongyloides stercoralis in mice. Infect. Immun. 74, 5730-5738 (2006).
46. Tsuda, Y. et al. Three different neutrophil subsets exhibited in mice with different susceptibilities to infection by methicillin-resistant Staphylococcus aureus. Immunity 21, 215-226 (2004).
47. Soehnlein, O., Weber, C. & Lindbom, L. Neutrophil granule proteins tune monocytic cell function. Trends Immunol. 30, 538-546 (2009).
48. Rosenthal, L.A., Sutterwala, F.S., Kehrli, M.E. & Mosser, D.M. Leishmania major-human macrophage interactions: cooperation between Mac-1 (CD11b/CD18) and complement receptor type 1 (CD35) in promastigote adhesion. Infect. Immun. 64, 2206-2215 (1996).
49. Dent, L.A. et al. Interleukin-5 transgenic mice show enhanced resistance to primary infections with Nippostrongylus brasiliensis but not primary infections with Toxocara canis. Infect. Immun. 67, 989-993 (1999).
50. Voehringer, D. Protective and pathological roles of mast cells and basophils. Nat. Rev. Immunol. 13, 362-375 (2013).
51. Pesce, J.T. et al. Neutrophils clear bacteria associated with parasitic nematodes augmenting the development of an effective Th2-type response. J. Immunol. 180, 464-474 (2008).
52. Tusher, V.G., Tibshirani, R. & Chu, G. Signifcance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA 98, 5116-5121 (2001).
53. Liu, Z. et al. IL-2 and autocrine IL-4 drive the in vivo development of antigen-specifc Th2 T cells elicited by nematode parasites. J. Immunol. 174, 2242-2249 (2005).
54. Gause, W.C. & Adamovicz, J. The use of the PCR to quantitate gene expression. PCR Methods Appl. 3, S123-S135 (1994).