Over expression of IL-10 by macrophages overcomes resistance to murine filariasis

Experimental Parasitology

Volumn 132, Issue 1, 2012, Pages 90-96

  Specht, Sabine ^a   Taylor, Matthew D ^b   Hoeve, Marieke A ^b   Allen, Judith E ^b   Lang, Roland ^c   Hoerauf, Achim ^a  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY HOSPITAL ERLANGEN   (Germany)

Author keywords

IL 10; Immunosuppression; Microfilaria; Murine filariasis; Patency

Indexed keywords

ARGINASE 1; CYTOKINE; INTERLEUKIN 10; MESSENGER RNA; PROTEIN FIZZ1; PROTEIN YM1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FILARIASIS; GENE IDENTIFICATION; GENE OVEREXPRESSION; HOST PARASITE INTERACTION; HOST RESISTANCE; IMMUNOSTIMULATION; INFECTION RESISTANCE; INFECTION SENSITIVITY; LITOMOSOIDES SIGMODONTIS; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PARASITE LOAD; PARASITE SURVIVAL; PRIORITY JOURNAL; PROTEIN FUNCTION; TH2 CELL;

ANIMALS; CYTOKINES; DISEASE RESISTANCE; DISEASE SUSCEPTIBILITY; FEMALE; FILARIASIS; FILARIOIDEA; INTERLEUKIN-10; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHENOTYPE; SIGMODONTINAE; SPECIFIC PATHOGEN-FREE ORGANISMS;

LITOMOSOIDES SIGMODONTIS; MURINAE; MUS; VERMES;

EID: 84865548173     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2011.09.003     Document Type: Article

References (41)

1. Al-Qaoud K.M., Pearlman E., Hartung T., Klukowski J., Fleischer B., Hoerauf A. A new mechanism for IL-5-dependent helminth control: neutrophil accumulation and neutrophil-mediated worm encapsulation in murine filariasis are abolished in the absence of IL-5. Int. Immunol. 2000, 12:899-908.
2. Allen J.E., Adjei O., Bain O., Hoerauf A., Hoffmann W.H., Makepeace B.L., Schulz-Key H., Tanya V.N., Trees A.J., Wanji S., Taylor D.W. Of mice, cattle, and humans: the immunology and treatment of river blindness. PLoS Negl. Trop. Dis. 2008, 2:e217.
3. Babayan S., Attout T., Specht S., Hoerauf A., Snounou G., Renia L., Korenaga M., Bain O., Martin C. Increased early local immune responses and altered worm development in high-dose infections of mice susceptible to the filaria Litomosoides sigmodontis. Med. Microbiol. Immunol. 2004, 194:151-162.
4. Brattig N.W., Tenner-Racz K., Korten S., Hoerauf A., Büttner D.W. Immunohistology of ectopic secondary lymph follicles in subcutaneous nodules from patients with hyperreactive onchocerciasis (sowda). Parasitol. Res. 2010, 107:657-666.
5. Chakravarti B., Lagoo-Deenadayalan S., Parker J.S., Whitfield D.R., Lagoo A., Chakravarti D.N. In vivo molecular analysis of cytokines in a murine model of ocular onchocerciasis. I. Up-regulation of IL-4 and IL-5 mRNAs and not IL-2 and IFN gamma mRNAs in the cornea due to experimental interstitial keratitis. Immunol. Lett. 1996, 54:59-64.
6. Dewals B.G., Marillier R.G., Hoving J.C., Leeto M., Schwegmann A., Brombacher F. IL-4Ralpha-independent expression of mannose receptor and Ym1 by macrophages depends on their IL-10 responsiveness. PLoS Negl. Trop. Dis. 2010, 4:e689.
7. Hagenbaugh A., Sharma S., Dubinett S.M., Wei S.H., Aranda R., Cheroutre H., Fowell D.J., Binder S., Tsao B., Locksley R.M., Moore K.W., Kronenberg M. Altered immune responses in interleukin 10 transgenic mice. J. Exp. Med. 1997, 185:2101-2110.
8. Harnett W., Harnett M.M. Helminth-derived immunomodulators: can understanding the worm produce the pill?. Nat. Rev. Immunol. 2010, 10:278-284.
9. Hawrylowicz C.M., O'Garra A. Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma. Nat. Rev. Immunol. 2005, 5:271-283.
10. Hoerauf A., Specht S., Satoguina J., Saeftel M. Immunmodulation by filarial nematodes. Parasite Immunol. 2005, 27:417-429.
11. Hoffmann W.H., Pfaff A.W., Schulz-Key H., Soboslay P.T. Determinants for resistance and susceptibility to microfilaraemia in Litomosoides sigmodontis filariasis. Parasitology 2001, 122:641-649.
12. Jenkins S.J., Allen J.E. Similarity and diversity in macrophage activation by nematodes, trematodes, and cestodes. J. Biomed. Biotechnol. 2010, 262609.
13. Klotz C., Ziegler T., Figueiredo A.S., Rausch S., Hepworth M.R., Obsivac N., Sers C., Lang R., Hammerstein P., Lucius R., Hartmann S. A helminth immunomodulator exploits host signaling events to regulate cytokine production in macrophages. PLoS Pathog. 2011, 7:e1001248.
14. Korten S., Hoerauf A., Kaifi J.T., Büttner D.W. Low levels of transforming growth factor-beta (TGF-beta) and reduced suppression of Th2-mediated inflammation in hyperreactive human onchocerciasis. Parasitology 2011, 138:35-45.
15. Kropf P., Fuentes J.M., Fahnrich E., Arpa L., Herath S., Weber V., Soler G., Celada A., Modolell M., Muller I. Arginase and polyamine synthesis are key factors in the regulation of experimental leishmaniasis in vivo. FASEB J. 2005, 19:1000-1002.
16. Lang R., Rutschman R.L., Greaves D.R., Murray P.J. Autocrine deactivation of macrophages in transgenic mice constitutively overexpressing IL-10 under control of the human CD68 promoter. J. Immunol. 2002, 168:3402-3411.
17. Le Goff L., Lamb T.J., Graham A.L., Harcus Y., Allen J.E. IL-4 is required to prevent filarial nematode development in resistant but not susceptible strains of mice. Int. J. Parasitol. 2002, 32:1277-1284.
18. Loke P., Nair M.G., Parkinson J., Guiliano D., Blaxter M., Allen J.E. IL-4 dependent alternatively-activated macrophages have a distinctive in vivo gene expression phenotype. BMC Immunol. 2002, 3:7.
19. Maizels R.M., Yazdanbakhsh M. T-cell regulation in helminth parasite infections: implications for inflammatory diseases. Chem. Immunol. Allergy 2008, 94:112-123.
20. Meghari S., Bechah Y., Capo C., Lepidi H., Raoult D., Murray P.J., Mege J.L. Persistent Coxiella burnetii Infection in Mice Overexpressing IL-10: An Efficient Model for Chronic Q Fever Pathogenesis. PloS Pathog. 2008, 4:e23.
21. Melendez A.J., Harnett M.M., Pushparaj P.N., Wong W.S., Tay H.K., McSharry C.P., Harnett W. Inhibition of Fc epsilon RI-mediated mast cell responses by ES-62, a product of parasitic filarial nematodes. Nat. Med. 2007, 13:1375-1381.
22. 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., Karow M., Stevens S., Pearce E.J., Artis D. Alternatively activated macrophage-derived RELM-{alpha} is a negative regulator of type 2 inflammation in the lung. J. Exp. Med. 2009, 206:937-952.
23. Nair M.G., Gallagher I.J., Taylor M.D., Loke P., Coulson P.S., Wilson R.A., Maizels R.M., Allen J.E. Chitinase and Fizz family members are a generalized feature of nematode infection with selective upregulation of Ym1 and Fizz1 by antigen-presenting cells. Infect. Immun. 2005, 73:385-394.
24. 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.
25. Petit G., Diagne M., Marechal P., Owen D., Taylor D., Bain O. Maturation of the filaria Litomosoides sigmodontis in BALB/c mice; comparative susceptibility of nine other inbred strains. Ann. Parasitol. Hum. Comp. 1992, 67:144-150.
26. Pfaff A.W., Schulz-Key H., Soboslay P.T., Geiger S.M., Hoffmann W.H. The role of nitric oxide in the innate resistance to microfilariae of Litomosoides sigmodontis in mice. Parasite Immunol. 2000, 22:397-405.
27. Pfarr K.M., Debrah A.Y., Specht S., Hoerauf A. Filariasis and lymphoedema. Parasite Immunol. 2009, 31:664-672.
28. Saeftel M., Specht S., Volkmann L., Hoerauf A. Synergism between IFN-γ and IL-5, antagonism between IL-4 and IL-10: What a worm infection can tell us beyond the Th1, Th2 paradigm. Immunobiol. 2002, 206:195.
29. Saeftel M., Volkmann L., Korten S., Brattig N., Al-Qaoud K.M., Fleischer B., Hoerauf A. Lack of IFN-γ confers impaired neutrophil granulocyte function and imparts prolonged survival of adult filarial worms in murine filariasis. Microbes Infect. 2001, 3:203-213.
30. Sartono E., Kruize Y.C., Kurniawan A., Maizels R.M., Yazdanbakhsh M. Depression of antigen-specific interleukin-5 and interferon-gamma responses in human lymphatic filariasis as a function of clinical status and age. J. Infect. Dis. 1997, 175:1276-1280.
31. Satoguina J., Mempel M., Larbi J., Badusche M., Loliger C., Adjei O., Gachelin G., Fleischer B., Hoerauf A. Antigen-specific T regulatory-1 cells are associated with immunosuppression in a chronic helminth infection (onchocerciasis). Microbes Infect. 2002, 4:1291-1300.
32. Schreiber T., Ehlers S., Heitmann L., Rausch A., Mages J., Murray P.J., Lang R., Holscher C. Autocrine IL-10 induces hallmarks of alternative activation in macrophages and suppresses antituberculosis effector mechanisms without compromising T cell immunity. J. Immunol. 2009, 183:1301-1312.
33. Simons J.E., Gray C.A., Lawrence R.A. Absence of regulatory IL-10 enhances innate protection against filarial parasites by a neutrophil-independent mechanism. Parasite Immunol 2010, 32:473-478.
34. Specht S., Volkmann L., Wynn T., Hoerauf A. Interleukin-10 (IL-10) counterregulates IL-4-dependent effector mechanisms in Murine Filariasis. Infect. Immun. 2004, 72:6287-6293.
35. Taubert A., Zahner H. Cellular immune responses of filaria (Litomosoides sigmodontis) infected BALB/c mice detected on the level of cytokine transcription. Parasite Immunol. 2001, 23:453-462.
36. Taylor M.D., Harris A., Babayan S.A., Bain O., Culshaw A., Allen J.E., Maizels R.M. CTLA-4 and CD4+CD25+ Regulatory T Cells Inhibit Protective Immunity to Filarial Parasites In Vivo. J. Immunol. 2007, 179:4626-4634.
37. Taylor M.D., Harris A., Nair M.G., Maizels R.M., Allen J.E. F4/80+ alternatively activated macrophages control CD4+ T cell hyporesponsiveness at sites peripheral to filarial infection. J. Immunol. 2006, 176:6918-6927.
38. Taylor M.D., LeGoff L., Harris A., Malone E., Allen J.E., Maizels R.M. Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J. Immunol. 2005, 174:4924-4933.
39. Taylor M.D., van der Werf N., Harris A., Graham A.L., Bain O., Allen J.E., Maizels R.M. Early recruitment of natural CD4+ Foxp3+ Treg cells by infective larvae determines the outcome of filarial infection. Eur. J. Immunol. 2009, 39:192-206.
40. Volkmann L., Bain O., Saeftel M., Specht S., Fischer K., Brombacher F., Matthaei K.I., Hoerauf A. Murine filariasis: interleukin 4 and interleukin 5 lead to containment of different worm developmental stages. Med. Microbiol. Immunol. 2003, 192:23-31.
41. Volkmann L., Saeftel M., Fleischer B., Hoerauf A. IL-4 is essential for the control of microfilariae in murine infection with the filaria Litomosoides sigmodontis. Infect. Immun. 2001, 69:2950-2956.