Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages

Infection and Immunity

Volumn 73, Issue 1, 2005, Pages 166-173

  Donnelly, Sheila ^a,e   O'Neill, Sandra M ^b   Sekiya, Mary ^c,d   Mulcahy, Grace ^c,d   Dalton, John P ^a,c,d,e  

^a School of Biotechnology   (Ireland)

^b School of Nursing   (Ireland)

^c DUBLIN CITY UNIVERSITY   (Ireland)

^d UNIVERSITY COLLEGE DUBLIN   (Ireland)

^e UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; ARGINASE; BETA ACTIN; CYTOKINE; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 4; INTERLEUKIN 5; NITRIC OXIDE; PHORBOL 13 ACETATE 12 MYRISTATE; PROSTAGLANDIN E2; RECOMBINANT ENZYME; THIOREDOXIN PEROXIDASE;

ANIMAL CELL; ANIMAL MODEL; ANIMAL PARASITOSIS; ARTICLE; ENZYME LINKED IMMUNOSORBENT ASSAY; FASCIOLA HEPATICA; HELMINTHIASIS; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN SECRETION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; CELLS, CULTURED; FASCIOLA HEPATICA; FASCIOLIASIS; FEMALE; INTERFERON TYPE II; INTERLEUKIN-12; INTERLEUKIN-4; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, INBRED BALB C; PEROXIDASES; PHENOTYPE; TH2 CELLS;

EID: 11144316758     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.1.166-173.2005     Document Type: Article

References (63)

1. Abdallahi, O. M., H. Bensalem, R. Augier, M. Diagana, M. De Reggi, and B. Gharib. 2001. Arginase expression in peritoneal macrophages and increase circulating polyamine levels in mice infected with Schistosoma mansoni. Cell Mol. Life Sci. 58:1350-1357.
2. + cytotoxic T-cell and Th2 cytokine responses as well as delayed virus clearance. Proc. Natl. Acad. Sci. USA 90:948-952.
3. Aderem, A., and R. J. Ultevitch. 2000. Toll-like receptors in the induction of the innate immune response. Nature 406:782-787.
4. Alleva, D. G., C. J. Burger, and K. D. Elgert. 1994. Tumour-induced regulation of suppressor macrophage nitric oxide and TNF-alpha production: role of tumour-derived IL-10, TGF-β, and prostaglandin E2. J. Immunol. 153:1674-1686.
5. Baeuerle, P. A., and T. Henkel. 1994. Function and activation of NF-κB in the immune system. Annu. Rev. Immunol. 12:141-279.
6. Behm, C. A., and N. C. Sangster. 1999. Pathology, pathophysiology, and clinical aspects, p. 185-201. In J. P. Dalton (ed.), Fasciolosis. CAB International, Wallingford, United Kingdom.
7. Bertini, R., O. M. Howard, H. F. Dong, J. J. Oppenheim, C. Bizzarri, R. Sergi, G. Caselli, S. Pagliel, B. Romines, J. A. Wilshire, M. Mengozzi, H. Nakamura, J. Yodoi, K. Pekkari, R. Gurunath, A. Holmgren, L. A. Herzenberg, L. A. Herzenberg, and P. Ghezzi. 1999. Thioredoxin, a redox enzyme released in infection and inflammation, is a unique chemoattractant for neutrophils, monocytes, and T cells. J. Exp. Med. 189:1783-1789.
8. Bird, J. J., D. R. Brown, A. C. Mullen, N. H. Moskowitz, M. A. Mahowald, J. R. Sider, T. F. Gajewski, C. R. Wang, and S. L. Reiner. 1998. Helper T-cell differentiation is controlled by the cell cycle. Immunity 9:229-237.
9. Bogdan, C. 1997. Of microbes, macrophages, and nitric oxide. Behring. Inst. Mitt. 99:58-64.
10. Brady, M. T., S. M. O'Neill, J. P. Dalton, and K. H. G. Mills. 1999. Fasciola hepatica suppresses a protective Th1 response against Bordetella pertussis. Infect. Immun. 67:5372-5378.
11. Crabtree, J. E., and R. A. Wilson. 1986. The role of pulmonary cellular reactions in the resistance of vaccinated mice to Schistosoma mansoni. Parasite Immunol. 8:265-285.
12. Dalton, D. K., S. Pitts-Meek, S. Keshav, I. S. Figari, A. Bradley, and T. A. Stewart. 1993. Multiple defects of immune-cell function in mice with disrupted interferon-γ genes. Science 259:1739-1742.
13. Dalton, J. P., S. McGonigle, T. P. Rolph, and S. J. Andrews. 1996. Induction of protective immunity in cattle against infection with Fasciola hepatica by vaccination with cathepsin L proteinase and with hemoglobin. Infect. Immun. 64:5066-5074.
14. Doyle, A. G., G. Herbein, L. J. Montaner, A. J. Minty, D. Caput, P. Ferrara, and S. Gordon. 1994. Interleukin-13 alters the activation state of murine macrophages in vitro: comparison with interleukin 4 and interferon-gamma. Eur. J. Immunol. 24:1441-1445.
15. Dunn, M. A., M. Roijkind, P. K. Hait, and K. S. Warren. 1978. Conversion of arginine to proline in murine schistosomiasis. Gastroenterology 75:1010-1015.
16. Dunn, M. A., S. Seifter, and P. K. Hait. 1981. Proline trapping in granulomas, the site of collagen biosynthesis in murine schistosomiasis. Hepatology 1: 28-32.
17. Falcone, F. H., P. Loke, X. Zang, A. S. MacDonald, R. M. Maizels, J. E. Allen. 2001. A Brugia malayi homolog of macrophage migration inhibitory factor reveals an important link between macrophages and eosinophil recruitment during nematode infection. J. Immunol. 167:5348-5354.
18. Frangioni, J. V., and B. G. Neel. 1993. Solubilization and purification of enzymatically active glutathione-S-transferase (pGEX) fusion proteins. Anal. Biochem. 210:179-187.
19. Gett, A. V., and P. D. Hodgkin. 1998. Cell division regulates the T-cell cytokine repertoire, revealing a mechanism underlying class regulation. Proc. Natl. Acad. Sci. USA 95:9488-9493.
20. Goerdt, S., and C. E. Orfanos. 1999. Other functions, other genes: alternative activation of antigen-presenting cells. Immunity 10:137-142.
21. Gordon, S. 2003. Alternative activation of macrophages. Nat. Rev. Immunol. 3:23-35.
22. Hesse, M., M. Modolel, A. C. La Flamme, M. Schito, J. M. Fuentes, A. W. Cheever, E. J. Pearce, and T. A. Wynn. 2001. 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. 167:6533-6544.
23. Hofmann, B., H. J. Hecht, and L. Flohe. 2002. Peroxiredoxins. Biol. Chem. 383:347-364.
24. Holcomb, I. N., R. C. Kabakoff, B. Chan, T. W. Baker, A. Gurney, W. Henzel, C. Nelson, H. B. Lowman, B. D. Wright, N. J. Skelton, G. D. Frantz, D. B. Tumas, F. V. Peale, D. L. Shelton, and C. C. Hebert. 2000. FIZZ1, a novel cysteine-rich secreted protein associated with pulmonary inflammation, defines a new gene family. EMBO J. 19:4046-4055.
25. Holland, M. J., Y. M. Harcus, P. L. Riches, and R. M. Maizels. 2000. Proteins secreted by the parasite nematode Nippostrongylus brasiliensis act as adjuvants for Th2 responses. Eur. J. Immunol. 30:1977-1987.
26. Jin, D., H. Chae, S. Rhee, and K. Jeang. 1997. Regulatory role for a novel human thioredoxin peroxidase in NF-κB activation J. Biol. Chem. 272: 30952-30961.
27. Kullberg, M. C., E. J. Pearce, S. E. Hieny, A. Sher, and J. A. Berzofsky. 1992. Infection with Schistosoma mansoni alters Th1/Th2 cytokine responses to a non-parasite antigen. J. Immunol. 148:3264-3270.
28. 2 amongst mouse strains: a possible mechanism to polarize Th2 response in BALB/c mice. J. Immunol. 164:2386-2395.
29. Lee, S. C., Z. H. Jaffar, K. Wan, S. T. Hogate, and K. Roberts. 1999. Regulation of pulmonary T-cell responses to inhaled antigen: role of Th1- and Th2-mediated inflammation. J. Immunol. 162:6867-6879.
30. + T cells. Eur. J. Immunol. 30:1127-1135.
31. Loke, P., A. S. MacDonald, A. Robb, R. M. Maizels, and J. E. Allen. 2000. Alternatively activated macrophages induced by nematode infection inhibit proliferation via cell-to-cell contact. Eur. J. Immunol. 30:2669-2678.
32. Loke, P., M. G. Nair, J. Parkinson, D. Guiliano, M. Blaxter, and J. E. Allen. 2002. IL-4-dependent alternatively activated macrophages have a distinctive in vivo gene expression phenotype. BMC Immunol. 3:7-18.
33. Maizels, R. M., and M. Yazdanbakhsh. 2003. Immuneregulation by helminth parasites: cellular and molecular mechanisms. Nat. Rev. Immunol. 3:733-744.
34. McGonigle, S., J. P. Dalton, and E. R. James. 1998. Peroxiredoxins: a new antioxidant family. Parasitol. Today 14:139-145.
35. McGonigle, S., P. Curley, and J. P. Dalton. 1997. Cloning of peroxiredoxin, a novel antioxidant enzyme, from the helminth parasite Fasciola hepatica. Parasitology 115:101-104.
36. Mills, C. D., K. Kincaid, J. M. Alt, M. J. Heilman, and A. M. Hill. 2000. M-1/M-2 macrophages and the Th1/Th2 paradigm. J. Immunol. 164:6166-6173.
37. Mulcahy, G., P. Joyce, and J. P. Dalton. 1999. Immunology of Fasciola hepatica infection, p. 341-376. In J. P. Dalton (ed.), Fasciolosis. CAB International, Wallingford, United Kingdom.
38. + T cells correlates with Th1/Th2 phenotype. J. Immunol. 160:5347-5354.
39. Munder, M., K. Eichmann, J. M. Moran, F. Centeno, G. Soler, and M. Modolell. 1999. Th1/Th2-Regulated expression of arginase isoforms in murine macrophages and dendritic cells. J. Immunol. 163:3771-3777.
40. Murata, Y., M. Amao, J. Yoneda, and J. Hamuro. 2002. Intracellular thiol redox status of macrophages directs the Th1 skewing in thioredoxin transgenic mice during aging. Mol. Immunol. 38:747-757.
41. Murata, Y., T. Ohteki, S. Koyasu, and J. Hamuro. 2002. IFN-gamma and pro-inflammatory cytokine production by antigen-presenting cells is dictated by intracellular thiol redox status regulated by oxygen tension. Eur. J. Immunol. 32:2866-2873.
42. Murata, Y., T. Shimamura, and J. Hamuro. 2002. The polarization of T(h)1/ T(h)2 balance is dependent on the intracellular thiol redox status of macrophages due to the distinctive cytokine production. Int. Immunol. 14:201-212.
43. Nair, M. G., D. W. Cochrane, and J. E. Allen. 2003. 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. 85:173-180.
44. Noel, W., G. Hassanzadeh, G. Raes, B. Namangala, I. Daems, L. Brys, F. Brombacher, P. D. Baetselier, and A. Beschin. 2002. Infection stage-dependent modulation of macrophage activation in Trypanosoma congolense-resistant and -susceptible mice. Infect. Immun. 70:6180-6187.
45. Okano, M., A. R. Satoskar, K. Nishizaki, M. Abe, and D. A. Harn. 1999. Induction of Th2 responses and IgE largely due to carbohydrates functioning as adjuvants on Schistosoma mansoni egg antigens. J. Immunol. 163:6712-6717.
46. O'Neill, S. M., K. H. Mills, and J. P. Dalton. 2000. Fasciola hepatica infection downregulates Th1 responses in mice. Parasite Immunol. 22:147-155.
47. Pekkari, K., J. Avila-Carino, A. Bengtsson, R. Gurunath, A. Scheynius, and A. Holmgren. 2001. Truncated thioredoxin (Trx80) induces production of interleukin-12 and enhances CD14 expression in human monocytes. Blood 97:3184-3190.
48. Peterson, J. D., L. A. Herzenberg, K. Vasquez, and C. Waltenbaugh. 1998. Glutathione levels in antigen-presenting cells modulate Th1 versus Th2 response patterns. Proc. Natl. Acad. Sci. USA 95:3071-3076.
49. Raes, G., P. De Baetselier, W. Noel, A. Beschin, F. Brombacher, and G. G. Hassanzadeh. 2002. Differential expression of FIZZ1 and Ym1 in alternatively activated versus classically activated macrophages. J. Leukoc. Biol. 71: 597-602.
50. Rodriguez-Sosa, M., A. R. Satoskar, R. Calderon, L. Gomez-Garcia, R. Saavedra, R. Bojalil, and L. I. Terrazas. 2002. Chronic helminth infection induces alternatively activated macrophages expressing high levels of CCR5 with low interleukin-12 production and Th2 biasing ability. Infect. Immun. 70:3656-3664.
51. Sandler, N. G., M. M. Mentink-Kane, A. W. Cheever, and T. A. Wynn. 2003. Global gene expression profiles during acute pathogen-induced pulmonary inflammation reveal divergent roles for Th1 and Th2 responses in tissue repair. J. Immunol. 171:3655-3667.
52. Sasaki, M., Y. Ohara-Nemoto, S. Tajika, M. Kobayashi, C. Yamaura, and S. Kimura. 2001. Antigenic characterisation of a novel Streptococcus aerginosus antigen that induces nitric oxide synthesis by murine peritoneal exudate cells. J. Med. Microbiol. 50:952-958.
53. Sonoki, T., A. Nagasaki, T. Gotoh, M. Takiguchi, M. Takeya, H. Matsuzaki, and M. Mori. 1997. Coinduction of nitric-oxide synthase and arginase I in cultured rat peritoneal macrophages and rat tissues in vivo by lipopolysaccharide. J. Biol. Chem. 272:3689-3693.
54. Stadecker, M. J. 1999. The regulatory role of the antigen presenting cell in the development of hepatic immunopathology during infection with Schistosoma mansoni. Pathobiology 67:269-272.
55. Stein, M., S. Keshav, N. Harris, and S. Gordon. 1992. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J. Exp. Med. 176:287-292.
56. + cells: a potential mechanism for immune polarization of helminth infections. J. Immunol. 167:5294-5303.
57. Todt, J., J. Sonstein, T. Polak, G. D. Seitzman, B. Hu, and J. L. Curtis. 2000. Repeated intratracheal challenge with particulate antigen modulates murine lung cytokines. J. Immunol. 164:4037-4047.
58. 2 is a potent inhibitor of human interleukin 12 production. J. Exp. Med. 181:775-779.
59. Verity, C. K., D. P. McManus, and P. J. Brindley. 2002. Cellular responses to Schistosoma japonicum cathepsin D aspartic protease. Parasite Immunol. 24:363-367.
60. Welch, J., L. Escoubet-Lozach, D. B. Sykes, K. Liddiard, D. R. Greaves, and C. K. Glass. 2002. Th2 cytokines and allergic challenge induce Ym1 expression in macrophages by a STAT6-dependent mechanism. J. Biol. Chem. 277: 42821-42829.
61. + T helper cell and B-cell responses against novel egg antigen, thioredoxin peroxidase. Infect. Immun. 69:1134-1141.
62. Wood, Z. A., E. Schroder, J. Robin Harris, and L. B. Poole. 2003. Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28:32-40.
63. Yazdanbakhsh, M., A. van der Biggelaar, and R. M. Maizels. 2001. Th2 responses without atopy: immunoregulation in chronic helminth infections and reduces allergic disease. Trends Immunol. 22:372-377.