Eotaxin-1-regulated eosinophils have a critical role in innate immunity against experimental Brugia malayi infection

European Journal of Immunology

Volumn 35, Issue 1, 2005, Pages 189-197

  Simons, Jonathan E ^a   Rothenberg, Marc E ^b   Lawrence, Rachel A ^a,c  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c ROYAL VETERINARY COLLEGE   (United Kingdom)

Author keywords

Chemokines; Eosinophils; Eotaxin; Nematode; Transgenic knockout

Indexed keywords

EOSINOPHIL PEROXIDASE; EOTAXIN; INTERLEUKIN 5; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRUGIA MALAYI; CELL INFILTRATION; CELL MIGRATION; CONTROLLED STUDY; DEGRANULATION; EOSINOPHIL; EOSINOPHILIA; IMMUNIZATION; INNATE IMMUNITY; LEUKOCYTE FUNCTION; MALE; MOUSE; NEMATODIASIS; NONHUMAN; PERITONEAL CAVITY; PRIORITY JOURNAL; REGULATORY MECHANISM; WILD TYPE;

ANIMALS; BRUGIA MALAYI; CHEMOKINES, CC; EOSINOPHIL PEROXIDASE; EOSINOPHILIA; EOSINOPHILS; FILARIASIS; IMMUNITY, NATURAL; INTERLEUKIN-5; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICROFILARIA;

EID: 12344297508     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200425541     Document Type: Article

References (39)

1. Capron, M., Eosinophils and parasites. Ann. Parasitol. Hum. Comp. 1991. 66 Suppl 1: 41-45.
2. Allen, J. E. and Maizels, R. M., Th1/Th2: reliable paradigm or dangerous dogma? Immunol. Today 1997. 18: 387-392.
3. Urban, J. F., Madden, K. B., Svetic, A., Cheever, A., Trotta, P. P., Gause, W. C., Katona, I. M. and Finkelman, F. D., The importance of Th2 cytokines in protective immunity to nematodes. Immunol. Rev. 1992. 127: 205-220.
4. Foster, P. S., Mould, A. W., Yang, M., Mackenzie, J., Mattes, J., Hogan, S. P., Mahalingam, S., McKenzie, A. N., Rothenberg, M. E., Young, I. G. et al, Elemental signals regulating eosinophil accumulation in the lung. Immunol. Rev. 2001. 179: 173-181.
5. Rothenberg, M. E., Luster, A. D. and Leder, P., Murine eotaxin: an eosinophil chemoattractant inducible in endothelial cells and in interleukin 4-induced tumor suppression. Proc. Natl. Acad. Sci. USA 1995. 92: 8960-8964.
6. Zimmermann, N., Hogan, S. P., Mishra, A., Brandt, E. B., Bodette, T. R., Pope, S. M., Finkelman, F. D. and Rothenberg, M. E., Murine eotaxin-2: a constitutive eosinophil chemokine induced by allergen challenge and IL-4 overexpression. J. Immunol. 2000. 165: 5839-5846.
7. Hogarth, P. J., Taylor, M. J. and Bianco, A. E., IL-5-dependent immunity to microfilariae is independent of IL-4 in a mouse model of onchocerciasis. J. Immunol. 1998. 160: 5436-5440.
8. Al-Qaoud, K. M., Pearlman, E., Hartung, T., Klukowski, J., Fleischer, B. and 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.
9. Le Goff, L., Loke, P., Ali, H. F., Taylor, D. W. and Allen, J. E., Interleukin-5 is essential for vaccine-mediated immunity but not innate resistance to a filarial parasite. Infect. Immun. 2000. 68: 2513-2517.
10. Lange, A. M., Yutanawiboonchai, W., Scott, P. and Abraham, D., IL-4- and IL-5-dependent protective immunity to Onchocerca volvulus infective larvae in BALB/cBYJ mice. J. Immunol. 1994. 153: 205-211.
11. Martin, C., Le Goff, L., Ungeheuer, M. N., Vuong, P. N. and Bain, O., Drastic reduction of a filarial infection in eosinophilic interleukin-5 transgenic mice. Infect. Immun. 2000. 68: 3651-3656.
12. Ramalingam, T., Ganley-Leal, L., Porte, P. and Rajan, T. V., Impaired clearance of primary but not secondary Brugia infections in IL-5 deficient mice. Exp. Parasitol. 2003. 105: 131-139.
13. Pearlman, E., Garhart, C. A., Grand, D. J., Diaconu, E., Strine, E. R. and Hall, L. R., Temporal recruitment of neutrophils and eosinophils to the skin in a murine model for onchocercal dermatitis. Am. J. Trop. Med. Hyg. 1999. 61: 14-18.
14. Cooper, P. J., Beck, L. A., Espinel, I, Deyampert, N. M., Hartnell, A., Jose, P. J., Paredes, W., Guderian, R. H. and Nutman, T. B., Eotaxin and RANTES expression by the dermal endothelium is associated with eosinophil infiltration after ivermectin treatment of onchocerciasis. Clin. Immunol. 2000. 95: 51-61.
15. Cheng, S. S., Lukacs, N. W. and Kunkel, S. L., Eotaxin/CCL11 is a negative regulator of neutrophil recruitment in a murine model of endotoxemia. Exp. Mol. Pathol. 2002. 73: 1-8.
16. Gray, C. A. and Lawrence, R. A., A role for antibody and Fc receptor in the clearance of Brugia malayi microfilariae. Eur. J. Immunol. 2002. 32: 1114-1120.
17. Grove, D. I., Davis, R. S. and Warren, K. S., Brugia malayi microfilaraemia in mice: a model for the study of the host response to microfilariae. Parasitology 1979. 79: 303-316.
18. Kazura, J. W. and Davis, R. S., Soluble Brugia malayi microfilarial antigens protect mice against challenge by an antibody-dependent mechanism. J. Immunol. 1982. 128: 1792-1796.
19. Pearlman, E., Kroeze, W. K., Hazlett, F. E., Jr., Chen, S.-S. A., Mawhorter, S. D., Boom, W. H. and Kazura, J. W., Brugia malayi: acquired resistance to microfilariae in BALB/c mice correlates with local Th2 responses. Exp. Parasitol. 1993. 76: 200-208.
20. Sabin, E. A., Kopf, M. A. and Pearce, E. J., Schistosoma mansoni egg induced early IL-4 production is dependent upon IL-5 and eosinophils. J. Exp. Med. 1996. 184: 1871-1878.
21. Hamann, K. J., Gleich, G. J., Checkel, J. L., Loegering, D. A., McCall, J. W. and Barker, R. L., In vitro killing of microfilariae of Brugia pahangi and Brugia malayi by eosinophil granule proteins. J. Immunol. 1990. 144: 3166-3173.
22. Greene, B. M., Taylor, H. R. and Aikawa, M., Cellular killing of microfilariae of Onchocerca volvulus: eosinophil and neutrophil-mediated immune serum-dependent destruction. J. Immunol. 1981. 127: 1611-1618.
23. Folkard, S. G., Hogarth, P. J., Taylor, M. J. and Bianco, A. E., Eosinophils are the major effector cells of immunity to microfilariae in a mouse model of onchocerciasis. Parasitology 1996. 112: 323-329.
24. Yoshida, T., Ikuta, K., Sugaya, H., Maki, K., Takagi, M., Kanazawa, H., Sunaga, S., Kinashi, T., Yoshimura, K., Miyazaki, J. et al., Defective B-1 cell development and impaired immunity against Angiostronglus cantonensis in IL-5R alpha-deficient mice. Immunity 1996. 4: 483-494.
25. Rotman, H. L., Yutanawiboonchai, W., Brigandi, R. A., Leon, O., Gleich, G. J., Nolan, T. J., Schad, G. A. and Abraham, D., Strongyloides stercoralis: eosinophil-dependent immune-mediated killing of third stage larvae in BALB/cByJ mice. Exp. Parasitol. 1996. 82: 267-278.
26. Ovington, K. S., McKie, K., Matthaei, K. I., Young, I. G. and Behm, C. A., Regulation of primary Strongyloides ratti infections in mice: a role for interleukin-5. Immunology 1998. 95: 488-493.
27. Lukacs, N. W., Oliveira, S. H. and Hogaboam, C. M., Chemokines and asthma: redundancy of function or a coordinated effort? J. Clin. Invest. 1999. 104: 995-999.
28. Rothenberg, M. E., Eosinophilia. N. Engl. J. Med. 1998. 338: 1592-1600.
29. Nickel, R., Beck, L. A., Stellato, C. and Schleimer, R. P., Chemokines and allergic disease. J. Allergy Clin. Immunol. 1999. 104: 723-742.
30. Gurish, M. F., Humbles, A., Tao, H., Finkelstein, S., Boyce, J. A., Gerard, C., Friend, D. S. and Austen, K. F., CCR3 is required for tissue eosinophilia and larval cytotoxicity after infection with Trichinella spiralis. J. Immunol. 2002. 168: 5730-5736.
31. Kephart, G. M., Gleich, G. J., Connor, D. H., Gibson, D. W. and Ackerman, S. J., Deposition of eosinophil granule major basic protein onto microfilariae of Onchocerca volvulus in the skin of patients treated with diethylcarbamazine. Lab. Invest. 1984. 50: 51-61.
32. Jones, R. E., Finkelman, F. D., Hester, R. B. and Kayes, S. G., Toxocara canis: failure to find IgE receptors (Fc epsilon R) on eosinophils from infected mice suggests that murine eosinophils do not kill helminth larvae by an IgE-dependent mechanism. Exp. Parasitol. 1994. 78: 64-75.
33. de Andres, B., Rakasz, E., Hagen, M., McCormik, M. L., Mueller, A. L., Elliot, D., Metwali, A., Sandor, M., Britigan, B. E., Weinstock, J. V. et al., Lack of Fc-epsilon receptors on murine eosinophils: implications for the functional significance of elevated IgE and eosinophils in parasitic infections. Blood 1997. 89: 3826-3836.
34. Herbert, D. R., Lee, J. J., Lee, N. A., Nolan, T. J., Schad, G. A. and Abraham, D., Role of IL-5 in innate and adaptive immunity to larval Strongyloides stercoralis in mice. J. Immunol. 2000. 165: 4544-4551.
35. Culley, F. J., Brown, A., Conroy, D. M., Sabroe, I., Pritchard, D. I. and Williams, T. J., Eotaxin is specifically cleaved by hookworm metalloproteases preventing its action in vitro and in vivo. J. Immunol. 2000. 165: 6447-6453.
36. Lawrence, R. A., Allen, J. E., Osborne, J. and Maizels, R. M., Adult and microfilarial stages of the filarial parasite Brugia malayi stimulate contrasting cytokine and Ig isotype responses in BALB/c mice. J. Immunol. 1994. 153: 1216-1224.
37. Maizels, R. M., Blaxter, M. L., Selkirk, M. E. and Robertson, B. D., Parasite antigens, parasite genes. A laboratory manual for molecular parasitology. Cambridge University Press, Cambridge 1991.
38. Pope, S. M., Brandt, E. B., Mishra, A., Hogan, S. P., Zimmermann, N., Matthaei, K. I., Foster, P. S. and Rothenberg, M. E., IL-13 induces eosinophil recruitment into the lung by an IL-5- and eotaxin-dependent mechanism. J. Allergy Clin. Immunol. 2001. 108: 594-601.
39. Varga, S. M., Beckman, N. A., Chu, M. and Braciale, T. J., Sensitive detection and quantitation of mouse eosinophils in tissues using an enzymatic eosinophil peroxidase assay: its use to rapidly measure pulmonary eosinophilia during experimental respiratory syncytial virus infection of mice. J. Immunol. Methods 2002. 262: 111 -120.