Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-27T08:05:24.243Z Has data issue: false hasContentIssue false
  • English
  • Français

Neutrophil granule proteins: evidence for the participation in the host reaction to skin microfilariae of Onchocerca volvulus after diethylcarbamazine administration

Published online by Cambridge University Press:  06 April 2009

E. J. Gutiérrez-Peña ,
J. Knab  and
D. W. Büttner
E. J. Gutiérrez-Peña*
Affiliation:
Bernhard Nocht Institute for Tropical Medicine, Bernhard-Nocht-Strasse 74, D-20359 Hamburg, Germany
J. Knab
Affiliation:
Bernhard Nocht Institute for Tropical Medicine, Bernhard-Nocht-Strasse 74, D-20359 Hamburg, Germany
D. W. Büttner
Affiliation:
Bernhard Nocht Institute for Tropical Medicine, Bernhard-Nocht-Strasse 74, D-20359 Hamburg, Germany
*
*Corresponding author. Tel: +49 40 31182 410. Fax: + 49 40 31182 400 or 309.
Get access Rights & Permissions [Opens in a new window]

Summary

The participation of neutrophil granulocytes in the cellular reaction to skin microfilariae of Onchocerca volvulus was studied by immunohistochemistry. Skin biopsies were obtained from adult Liberian and Ugandan patients with generalized onchocerciasis after exposure to topically applied diethylcarbamazine (DEC) and from untreated patients. After DEC many damaged microfilariae were observed either in dermal infiltrates or in epidermal microabscesses consisting both of neutrophils and eosinophils. Infiltrates and microabscesses contained some intact granulocytes and many neutrophils releasing myeloperoxidase, elastase, lactoferrin, defensin, lysozyme, α1-antitrypsin and α1-antichymotrypsin. Eosinophils discharged peroxidase and cationic proteins. Released granule proteins and remnants of disrupted granulocytes were found on the surface and in close proximity of damaged microfilariae in dermal infiltrates and epidermal microabscesses. In larger microabscesses neutrophils were predominant. These observations show that neutrophils and not only eosinophils recruit, accumulate, localize around and release their helminthotoxic granule proteins such as myeloperoxidase onto or closely around skin microfilariae of O. volvulus after topical DEC administration. The association between these processes and the damage of the microfilariae indicated that neutrophils together with eosinophils attack and damage microfilariae of O. volvulus after DEC treatment in the skin.

Keywords

diethylcarbamazineOnchocerca volvuluseosinophilsneutrophilsgranule proteinsmyeloperoxidase
Type
Research Article
Information
Parasitology , Volume 113 , Issue 4 , October 1996 , pp. 403 - 414
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ackerman, S. J., Gleich, G. J., Loegering, D. A., Richardson, B. A. & Butterworth, A. E. (1985). Comparative toxicity of Purified human eosinophil granule cationic proteins for schisotsomula of schistosoma mansoni. American journal of Tropical Medicine and Hygiene 34, 735–745.CrossRefGoogle ScholarPubMed
Ackerman, S. J., Kephart, G. M., Francis, H., Awadzi, K., Gleich, G. J. & Ottesen, E. A. (1990). Eosinophil degranulation. An immunologic determinant in the pathogenesis of the Mazzotti reaction in human onchocerciasis. Journal of Immunology 144, 3961–3969.CrossRefGoogle ScholarPubMed
Albiez, E. J., Büttner, D. W. & Duke, B. O. L. (1988). Diagnosis and extirpation of nodules in human onchocerciasis. Tropical Medicine and Parasitology 39, 331–346.Google ScholarPubMed
Albiez, E. J., Newland, H. S., White, A. T., Kaiser, A., Greene, B. M., Taylor, H. R. & Büttner, D. W. (1988). Chemotherapy of onchocerciasis with high doses of diethylcarbamazine or a single dose of ivermectin: microfilaria levels and side effects. Tropical Medicine and Parasitology 39, 19–24.Google ScholarPubMed
Bass, D. A. & Szejda, P. (1979). Eosinophils versus neutrophils in host defense. Killing of newborn larvae of Trichinella spiralis by human granulocytes in vitro. Journal of Clinical Investigation 64, 1415–1422.CrossRefGoogle ScholarPubMed
Bozeman, P. M., Learn, D. B. & Thomas, E. L. (1990). Assay of the human leukocyte enzymes myeloperoxidase and eosinophil peroxidase. Journal of Immunological Methods 126, 125–133.CrossRefGoogle ScholarPubMed
Butterworth, A. E., Sturrock, R. F., Houba, V., Mahmoud, A. A. F., Sher, A. & Rees, P. H. (1975). Eosinophils as mediators of antibody-dependent damage to schistosomula. Nature, London 256, 727–729.CrossRefGoogle ScholarPubMed
Butterworth, A. E., Wassom, D. L., Gleich, G. J., Loegering, D. A. & David, J. R. (1979). Damage to schistosomula of Schistosoma mansoni induced directly by eosinophil major basic protein. Journal of Immunology 122, 221–229.CrossRefGoogle ScholarPubMed
Buys, J., Wever, R. & Ruitenberg, E. J. (1984). Myeloperoxidase is more efficient than eosinophil peroxidase in the in vitro killing of newborn larvae of Trichinella spiralis. Immunology 51, 601–607.Google ScholarPubMed
Connor, D. H., George, G. H. & Gibson, D. W. (1985). Pathologic changes of human onchocerciasis. Implications for future research. Reviews of Infectious Diseases 7, 809–819.CrossRefGoogle ScholarPubMed
Cordell, J. L., Falini, B., Erber, W. N., Ghosh, A. K., Abdulaziz, Z., Macdonald, S., Pulford, K. A. F., Stein, H. & Mason, D. Y. (1984). Immunoenzymatic labelling of monoclonal antibodies using immune complexes of alkaline phosphatase and monoclonal anti-alkaline phosphatase (APAAP complexes). Journal of Histochemistry and Cytochemistry 32, 219–229.CrossRefGoogle ScholarPubMed
Du Bois, R. M., Bernaudin, J. F., Paakko, P., Hubbard, R., Takahashi, H., Ferrans, V. & Crystal, R. G. (1991). Human neutrophils express the α1-antitrypsin gene and produce α1-antitrypsin. Blood 77, 2724–2730.CrossRefGoogle Scholar
Gibson, D. W., Connor, D. H., Brown, H. L., Fuglsang, H., Anderson, J., Duke, B. O. L. & Buck, A. A. (1976). Onchocercal dermatitis: ultrastructural studies of microfilariae and host tissues, before and after treatment with diethylcarbamazine (Hetrazan). American Journal of Tropical Medicine and Hygiene 25, 74–87.CrossRefGoogle ScholarPubMed
Gibson, D. W., Heggie, C. & Connor, D. H. (1980). Clinical and pathologic aspects of onchocerciasis. Pathology Annual 15, 195–240.Google ScholarPubMed
Greene, B. M., Taylor, H. R. & Aikawa, M. (1981). Cellular killing of microfilariae of Onchocerca volvulus: eosinophil and neutrophil-mediated immune serum-dependent destruction. Journal of Immunology 127, 1611–1618.CrossRefGoogle ScholarPubMed
Hamann, K. J., Gleich, G. J., Checkel, J. L., Loegering, D. A., McCall, J. W. & Barker, R. L. (1990). In Vitro killing of microfilariae of Brugia pahangi and Brugia malayi by eosinophil granule proteins. Journal of Immunology 144, 3166–3173.CrossRefGoogle ScholarPubMed
Hawking, F., Sewell, P. & Thurstone, J. P. (1950). The mode of action of hetrazan on filarial worms. British Journal of Pharmacology 5, 217–238.Google ScholarPubMed
Horii, Y., Owhashi, M., Ishii, A., Bandou, K. & Usui, I. (1984). Leukocyte accumulation in sparganosis: demonstration of eosinophil and neutrophil chemotactic factors from the plerocercoid of Spirometra erinacei in vivo and in vitro. American Journal of Tropical Medicine and Hygiene 33, 138–143.CrossRefGoogle ScholarPubMed
Horii, Y., Owhashi, M., Fujita, K., Nakanishi, H. & Ishii, A. (1988). A comparative study on eosinophil and neutrophil chemotactic activities of various helminth parasites. Parasitology Research 75, 76–78.CrossRefGoogle ScholarPubMed
Incani, R. N. & McLaren, D. J. (1981). Neutrophil-mediated cytotoxicity to schistosomula of Schistosoma mansoni in vitro: studies on the kinetics of complement and/or antibody-dependent adherence and killing. Parasite Immunology 3, 107–126.CrossRefGoogle ScholarPubMed
Johnson, E. H., Lustigman, S., Brotman, B., Browne, J. & Prince, A. M. (1991). Onchocerca volvulus: in vitro killing of microfilariae by neutrophils and eosinophils from experimentally infected chimpanzees. Tropical Medicine and Parasitology 42, 351–355.Google ScholarPubMed
Johnson, E. H., Irvine, M., Kass, P. H., Browne, J., Abdullai, M., Prince, A. M. & Lustigman, S. (1994). Onchocerca volvulus: in vitro cytotoxic effects of human neutrophils and serum on third-stage larvae. Tropical Medicine and Parasitology 45, 331–335.Google ScholarPubMed
Johnson, E. H., Lustigman, S., Kass, P. H., Irvine, M., Browne, J. & Prince, A. M. (1995). Onchocerca volvulus: a comparative study of in vitro neutrophil killing of microfilariae and humoral responses in infected and endemic normals. Experimental Parasitology 81, 9–19.CrossRefGoogle ScholarPubMed
Johnson, P., Mackenzie, C. D., Suswillo, R. R. & Denham, D. A. (1981). Serum-mediated adherence of feline granulocytes to microfilariae of Brugia pahangi in vitro: variations with parasite maturation. Parasite Immunology 3, 69–80.CrossRefGoogle ScholarPubMed
Johnson, P., Mackenzie, C. D., Denham, D. A. & Suswillo, R. R. (1988). The effect of diethylcarbamazine on the in vitro serum-mediated adherence of feline granulocytes to microfilariae of Brugia pahangi. Tropical Medicine and Parasitology 39, 291–294.Google ScholarPubMed
Kazura, J. W. & Grove, D. I. (1978). Stage-specific antibody-dependent eosinophil-mediated destruction of Trichinella spiralis. Nature, London 274, 588–589.CrossRefGoogle ScholarPubMed
Kephart, G. M., Gleich, G. J., Connor, D. H., Gibson, D. W. & Ackerman, S. J. (1984). Deposition of eosinophil granule major basic protein onto microfilariae of Onchocerca volvulus in the skin of patients treated with diethylcarbamazine. Laboratory Investigation 50, 51–61.Google ScholarPubMed
King, C. H., Greene, B. M. & Spagnuolo, P. J. (1983). Diethylcarbamazine citrate, an antifilarial drug, stimulates human granulocyte adherence. Antimicrobial Agents and Chemotherapy 24, 453–456.CrossRefGoogle ScholarPubMed
Kobayashi, J., Matsuda, H., Fujita, K., Sakai, T. & Shinoda, K. (1969). Some observations on the mode of action of diethylcarbamazine on the cotton rat filaria (In Japanese.) Japanese Journal of Parasitology 18, 563–574.Google Scholar
Lehrer, R. I. & Ganz, T. (1990). Antimicrobial polypeptides of human neutrophils. Blood 76, 2169–2181.CrossRefGoogle ScholarPubMed
Mackenzie, C. D., Jungery, M., Taylor, P. M. & Ogilve, B. M. (1981). The in vitro interaction of eosinophils, neutrophils, macrophages and mast cells with nematode surfaces in the presence of complement or antibodies. Journal of Pathology 133, 161–175.CrossRefGoogle ScholarPubMed
Maizels, R. M. & Denham, D. A. (1992). Diethylcarbamazine (DEC): immunopharmacological interactions of an anti-filarial drug. Parasitology 105 (Suppl.), S49–S60.CrossRefGoogle ScholarPubMed
Müller, s. & Walter, R. D. (1992). Purification and characterization of polyamine oxidase from Ascaris suum. The Biochemical Journal 283, 75–80.CrossRefGoogle ScholarPubMed
Nathan, C., Srimal, S., Farber, C., Sanchez, E., Kabbash, L., Asch, A., Gailit, J. & Wright, S. D. (1989). Cytokine induced respiratory burst of human neutrophils: dependence on extracellular matrix proteins and CD11/CD18 integrins. Journal of Cell Biology 109, 1341–1349.CrossRefGoogle ScholarPubMed
Njoo, F. L., Hack, C. E., Costing, J., Stilma, J. S. & Kijlstra, A. (1993). Neutrophil activation in ivermectin-treated onchocerciasis patients. Clinical and Experimental Immunology 94, 330–333.CrossRefGoogle ScholarPubMed
Ottesen, E. A. (1995). Immune responsiveness and the pathogenesis of human onchocerciasis. Journal of Infectious Diseases 171, 659–671.CrossRefGoogle ScholarPubMed
Piessens, W. F. & Beldekas, M. (1979). Diethylcarbamazine enhances antibody-mediated cellular adherence to Brugia malayi microfilariae. Nature, London 282, 845–847.CrossRefGoogle ScholarPubMed
Racz, P., Tenner-Racz, K., Büttner, D. W. & Albiez, E. J. (1982). Ultrastructural evidence for eosinophil-parasite adherence (EPA) reaction in human onchocercal lymphadenitis in the early period following diethylcarbamzaine treatment. Tropical Medicine and Parasitology 33, 213–218.Google ScholarPubMed
Ruitenberg, E. J., Buys, J., Teppema, J. S. & Elgersma, A. (1983). Rat mononuclear cells and neutrophils are more effective than eosinophils in antibody-mediated stage-specific killing of Trichinella spiralis in vitro. Zeitschrift für Parasitenkunde 69, 807–815.CrossRefGoogle ScholarPubMed
Spitznagel, J. K. & Shafer, W. M. (1985). Neutrophil killing of bacteria by oxygen-independent mechanisms: a historical summary. Reviews of Infectious Diseases 7, 398–403.CrossRefGoogle ScholarPubMed
Zabucchi, G., Menegazzi, R., Cramer, R., Nardon, E. & Patriarca, P. (1990). Mutual influence between eosinophil peroxidase (EPO) and neutrophils: neutrophils reversibly inhibit EPO enzymatic activity and EPO increases neutrophil adhesiveness. Immunology 69, 580–587.Google ScholarPubMed