Genes associated with alternatively activated macrophages discretely regulate helminth infection and pathogenesis in experimental mouse models

Immunobiology

Volumn 215, Issue 9-10, 2010, Pages 704-708

  Horsnell, William G C ^a,b   Brombacher, Frank ^a,b  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

Alternatively activated macrophages; Helminthes

Indexed keywords

ARGINASE 1; CD11B ANTIGEN; CD68 ANTIGEN; CYTOKINE; DECTIN 1; GENE PRODUCT; INTERLEUKIN 13; INTERLEUKIN 4 RECEPTOR ALPHA; MANNOSE RECEPTOR; MEBENDAZOLE; PROTEIN FIZZ1; PROTEIN MR; PROTEIN YM1; SCAVENGER RECEPTOR A; UNCLASSIFIED DRUG;

ARTICLE; BRUGIA MALAYI; CELLULAR IMMUNITY; COMPLEX FORMATION; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENETIC ASSOCIATION; GRANULOMA; HELIGMOSOMOIDES POLYGYRUS; HELMINTHIASIS; HOST PARASITE INTERACTION; MACROPHAGE ACTIVATION; NIPPOSTRONGYLUS BRASILIENSIS; NONHUMAN; PARASITE IDENTIFICATION; PATHOGENESIS; PRIORITY JOURNAL; SCHISTOSOMA MANSONI; STRONGYLOIDIASIS; TH1 CELL; TH2 CELL; UPREGULATION;

ANIMALS; COMPLEMENT PATHWAY, ALTERNATIVE; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HELMINTHIASIS; HUMANS; INTESTINAL DISEASES, PARASITIC; MACROPHAGES; MICE; SCHISTOSOMA MANSONI;

EID: 77955423687     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imbio.2010.05.011     Document Type: Article

References (48)

1. Anthony R.M., Rutitzky L.I., Urban J.F., Stadecker M.J., Gause W.C. Protective immune mechanisms in helminth infection. Nat. Rev. Immunol. 2007, 7:975-987.
2. Anthony R.M., Urban J.F., Alem F., Hamed H.A., Rozo C.T., Boucher J.L., Van Rooijen N., Gause W.C. Memory TH2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat. Med. 2006, 12:955-960.
3. Babu S., Bhat S.Q., Kumar N.P., Jayantasri S., Rukmani S., Kumaran P., Gopi P.G., Kolappan C., Kumaraswami V., Nutman T.B. Human type 1 and 17 responses in latent tuberculosis are modulated by coincident filarial infection through cytotoxic T lymphocyte antigen-4 and programmed death-1. J. Infect. Dis. 2009, 200:288-298.
4. Barner M., Mohrs M., Brombacher F., Kopf M. Differences between IL-4R alpha-deficient and IL-4-deficient mice reveal a role for IL-13 in the regulation of TH2 responses. Curr. Biol. 1998, 8:669-672.
5. Brombacher F., Arendse B., Peterson R., Holscher A., Holscher C. Analyzing classical and alternative macrophage activation in macrophage/neutrophil-specific IL-4 receptor-alpha-deficient mice. Methods Mol. Biol. 2009, 531:225-252.
6. Cao Y., Brombacher F., Tunyogi-Csapo M., Glant T.T., Finnegan A. Interleukin-4 regulates proteoglycan-induced arthritis by specifically suppressing the innate immune response. Arthritis Rheum. 2007, 56:861-870.
7. Dewals, B., Marillier, R., Hoving, J.C., Leeto, M., Schwegmann, A., Brombacher, F. IL-4Rα-independent expression of mannose receptor and Ym1 by macrophages depends on their IL-10 responsiveness. PLoS Neglected Trop. Dis., in press.
8. Finkelman F.D., Shea-Donohue T., Morris S.C., Gildea L., Strait R., Madden K.B., Schopf L., Urban J.F. Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunol. Rev. 2004, 201:139-155.
9. Fitzpatrick A.M., Holguin F., Teague W.G., Brown L.A. Alveolar macrophage phagocytosis is impaired in children with poorly controlled asthma. J. Allergy Clin. Immunol. 2008, 121(1372-1378):e1371-e1373. 1378.
10. Gallina G., Dolcetti L., Serafini P., De Santo C., Marigo I., Colombo M.P., Basso G., Brombacher F., Borrello I., Zanovello P., et al. Tumors induce a subset of inflammatory monocytes with immunosuppressive activity on CD8+ T cells. J. Clin. Invest. 2006, 116:2777-2790.
11. Goerdt S., Bhardwaj R., Sorg C. Inducible expression of MS-1 high-molecular-weight protein by endothelial cells of continuous origin and by dendritic cells/macrophages in vivo and in vitro. Am. J. Pathol. 1993, 142:1409-1422.
12. Gordon S. Alternative activation of macrophages. Nat. Rev. Immunol. 2003, 3:23-35.
13. Grunig G., Warnock M., Wakil A.E., Venkayya R., Brombacher F., Rennick D.M., Sheppard D., Mohrs M., Donaldson D.D., Locksley R.M., Corry D.B. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 1998, 282:2261-2263.
14. Herbert D.R., Holscher C., Mohrs M., Arendse B., Schwegmann A., Radwanska M., Leeto M., Kirsch R., Hall P., Mossmann H., et al. Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 2004, 20:623-635.
15. Hesse M., Modolell M., La Flamme A.C., Schito M., Fuentes J.M., Cheever A.W., Pearce E.J., Wynn T.A. Differential regulation of nitric oxide synthase-2 and arginase-1 by type 1/type 2 cytokines in vivo: granulomatous pathology is shaped by the pattern of L-arginine metabolism. J. Immunol. 2001, 167:6533-6544.
16. Huang J.T., Welch J.S., Ricote M., Binder C.J., Willson T.M., Kelly C., Witztum J.L., Funk C.D., Conrad D., Glass C.K. Interleukin-4-dependent production of PPAR-gamma ligands in macrophages by 12/15-lipoxygenase. Nature 1999, 400:378-382.
17. Kodelja V., Muller C., Tenorio S., Schebesch C., Orfanos C.E., Goerdt S. Differences in angiogenic potential of classically vs alternatively activated macrophages. Immunobiology 1997, 197:478-493.
18. Kreider T., Anthony R.M., Urban J.F., Gause W.C. Alternatively activated macrophages in helminth infections. Curr. Opin. Immunol. 2007, 19:448-453.
19. Linehan S.A. The mannose receptor is expressed by subsets of APC in non-lymphoid organs. BMC Immunol. 2005, 6:4.
20. Linehan S.A., Weber R., McKercher S., Ripley R.M., Gordon S., Martin P. Enhanced expression of the mannose receptor by endothelial cells of the liver and spleen microvascular beds in the macrophage-deficient PU.1 null mouse. Histochem. Cell Biol. 2005, 123:365-376.
21. Loke P., Gallagher I., Nair M.G., Zang X., Brombacher F., Mohrs M., Allison J.P., Allen J.E. Alternative activation is an innate response to injury that requires CD4+ T cells to be sustained during chronic infection. J. Immunol. 2007, 179:3926-3936.
22. Loke P., MacDonald A.S., Robb A., Maizels R.M., Allen J.E. Alternatively activated macrophages induced by nematode infection inhibit proliferation via cell-to-cell contact. Eur. J. Immunol. 2000, 30:2669-2678.
23. Maizels R.M., Pearce E.J., Artis D., Yazdanbakhsh M., Wynn T.A. Regulation of pathogenesis and immunity in helminth infections. J. Exp. Med. 2009, 206:2059-2066.
24. 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. 2008, 38:479-488.
25. Martinez F.O., Helming L., Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu. Rev. Immunol. 2009, 27:451-483.
26. Mearns H., Horsnell W.G., Hoving J.C., Dewals B., Cutler A.J., Kirstein F., Myburgh E., Arendse B., Brombacher F. Interleukin-4-promoted T helper 2 responses enhance Nippostrongylus brasiliensis-induced pulmonary pathology. Infect. Immun. 2008, 76:5535-5542.
27. Mohrs M., Ledermann B., Kohler G., Dorfmuller A., Gessner A., Brombacher F. Differences between IL-4- and IL-4 receptor alpha-deficient mice in chronic leishmaniasis reveal a protective role for IL-13 receptor signaling. J. Immunol. 1999, 162:7302-7308.
28. Munder M., Eichmann K., Moran J.M., Centeno F., Soler G., Modolell M. TH1/TH2-regulated expression of arginase isoforms in murine macrophages and dendritic cells. J. Immunol. 1999, 163:3771-3777.
29. Mylonas K.J., Nair M.G., Prieto-Lafuente L., Paape D., Allen J.E. Alternatively activated macrophages elicited by helminth infection can be reprogrammed to enable microbial killing. J. Immunol. 2009, 182:3084-3094.
30. Nair M.G., Cochrane D.W., Allen J.E. Macrophages in chronic type 2 inflammation have a novel phenotype characterized by the abundant expression of Ym1 and Fizz1 that can be partly replicated in vitro. Immunol. Lett. 2003, 85:173-180.
31. Nair M.G., Du Y., Perrigoue J.G., Zaph C., Taylor J.J., Goldschmidt M., Swain G.P., Yancopoulos G.D., Valenzuela D.M., Murphy A., et al. Alternatively activated macrophage-derived RELM-{alpha} is a negative regulator of type 2 inflammation in the lung. J. Exp. Med. 2009, 206:937-952.
32. Odegaard J.I., Ricardo-Gonzalez R.R., Goforth M.H., Morel C.R., Subramanian V., Mukundan L., Eagle A.R., Vats D., Brombacher F., Ferrante A.W., Chawla A. Macrophage-specific PPARgamma controls alternative activation and improves insulin resistance. Nature 2007, 447:1116-1120.
33. Pearce E.J., MacDonald A.S. The immunobiology of schistosomiasis. Nat. Rev. Immunol. 2002, 2:499-511.
34. Pesce J.T., Ramalingam T.R., Mentink-Kane M.M., Wilson M.S., El Kasmi K.C., Smith A.M., Thompson R.W., Cheever A.W., Murray P.J., Wynn T.A. Arginase-1-expressing macrophages suppress TH2 cytokine-driven inflammation and fibrosis. PLoS Pathog. 2009, 5:e1000371.
35. Pesce J.T., Ramalingam T.R., Wilson M.S., Mentink-Kane M.M., Thompson R.W., Cheever A.W., Urban J.F., Wynn T.A. Retnla (relmalpha/fizz1) suppresses helminth-induced TH2-type immunity. PLoS Pathog. 2009, 5:e1000393.
36. Ponomarev E.D., Maresz K., Tan Y., Dittel B.N. CNS-derived interleukin-4 is essential for the regulation of autoimmune inflammation and induces a state of alternative activation in microglial cells. J. Neurosci. 2007, 27:10714-10721.
37. Reece J.J., Siracusa M.C., Southard T.L., Brayton C.F., Urban J.F., Scott A.L. Hookworm-induced persistent changes to the immunological environment of the lung. Infect. Immun. 2008, 76:3511-3524.
38. Ricote M., Huang J.T., Welch J.S., Glass C.K. The peroxisome proliferator-activated receptor(PPARgamma) as a regulator of monocyte/macrophage function. J. Leukoc. Biol. 1999, 66:733-739.
39. Sadick M.D., Heinzel F.P., Holaday B.J., Pu R.T., Dawkins R.S., Locksley R.M. Cure of murine leishmaniasis with anti-interleukin 4 monoclonal antibody. Evidence for a T cell-dependent, interferon gamma-independent mechanism. J. Exp. Med. 1990, 171:115-127.
40. Sandler N.G., Mentink-Kane M.M., Cheever A.W., Wynn T.A. Global gene expression profiles during acute pathogen-induced pulmonary inflammation reveal divergent roles for TH1 and TH2 responses in tissue repair. J. Immunol. 2003, 171:3655-3667.
41. Siracusa M.C., Reece J.J., Urban J.F., Scott A.L. Dynamics of lung macrophage activation in response to helminth infection. J. Leukoc. Biol. 2008, 84:1422-1433.
42. Stein M., Keshav S., Harris N., Gordon S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J. Exp. Med. 1992, 176:287-292.
43. Stenger S., Solbach W., Rollinghoff M., Bogdan C. Cytokine interactions in experimental cutaneous leishmaniasis. II. Endogenous tumor necrosis factor-alpha production by macrophages is induced by the synergistic action of interferon (IFN)-gamma and interleukin (IL) 4 and accounts for the antiparasitic effect mediated by IFN-gamma and IL 4. Eur. J. Immunol. 1991, 21:1669-1675.
44. Varin, A., Gordon, S. 2009. Alternative activation of macrophages: immune function and cellular biology. Immunobiology.
45. Varin, A., Mukhopadhyay, S., Herbein, G., Gordon, S., 2010. Alternative activation of macrophages by IL-4 impairs phagocytosis of pathogens but potentiates microbial-induced signalling and cytokine secretion. Blood 115, 353-362.
46. Weng M., Huntley D., Huang I.F., Foye-Jackson O., Wang L., Sarkissian A., Zhou Q., Walker W.A., Cherayil B.J., Shi H.N. Alternatively activated macrophages in intestinal helminth infection: effects on concurrent bacterial colitis. J. Immunol. 2007, 179:4721-4731.
47. Zhao A., McDermott J., Urban J.F., Gause W., Madden K.B., Yeung K.A., Morris S.C., Finkelman F.D., Shea-Donohue T. Dependence of IL-4, IL-13, and nematode-induced alterations in murine small intestinal smooth muscle contractility on Stat6 and enteric nerves. J. Immunol. 2003, 171:948-954.
48. Zhao, A., Urban, J.F., Anthony, R.M., Sun, R., Stiltz, J., van Rooijen, N., Wynn, T.A., Gause, W.C., Shea-Donohue, T., 2008. TH2 cytokine-induced alterations in intestinal smooth muscle function depend on alternatively activated macrophages. Gastroenterology 135, 217-225 e211.