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The nematode parasite Onchocerca volvulus generates the transforming growth factor-beta (TGF-beta)

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Abstract

Transforming growth factor-beta (TGF-β) is a highly conserved cytokine that has a well-known regulatory role in immunity, but also in organ development of most animal species including helminths. Homologous tgf-b genes and mRNA have been detected in the filaria Brugia malayi. The in situ protein expression is unknown for filariae. Therefore, we examined several filariae for the expression and localization of latent (stable) TGF-β in adult and larval stages. A specific goat anti-human latency associated protein (LAP, TGF-β 1) antibody, purified by affinity chromatography, was used for light and electron microscopic immunohistochemistry. Adult Onchocerca volvulus, Onchocerca gibsoni, Onchocerca ochengi, Onchocerca armillata, Onchocerca fasciata, Onchocerca flexuosa, Wuchereria bancrofti, Dirofilaria sp., B. malayi, and infective larvae of W. bancrofti reacted with the antibody. Labeling of worm tissues varied between negative and all degrees of positive reactions. Latent TGF-β was strongly expressed adjacent to the cell membranes of the hypodermis, epithelia, and muscles and adjacent to many nuclei in all organs. TGF-β was well expressed in worms without Wolbachia endobacteria eliminated by doxycycline treatment. Pleomorphic neoplasms in O. volvulus were also labeled. We conclude that latent TGF-β protein is expressed by filariae independently of Wolbachia, possibly regulating worm tissue homeostasis.

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Abbreviations

IVM:

ivermectin

LM, EM:

light microscopy, electron microscopy

LTBP:

latent TGF-β binding protein

LAP:

latency associated peptide/protein

L3:

infective larva (e)

mf:

microfilaria (e)

OvAST1:

onchoastacin

RER:

rough endoplasmatic reticulum

TGF-β:

transforming growth factor-beta

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Acknowledgements

We thank Frank Geisinger and Ingeborg Albrecht for their technical assistance. We are obliged to Prof. D. B. Copeman (James Cook University of North Queensland, Townsville, Australia) for the O. gibsoni; to Prof. Rolf Garms (Bernhard Nocht Institute) for the W. bancrofti larvae; Priv.-Doz. Alfons Renz (University of Hohenheim, Germany) for O. ochengi and O. armillata; and Prof. Mohammed Omar (Hamburg, previously Abha, Saudi Arabia) for the O. fasciata.

Nodulectomies for research purposes had been approved by the Ethics Commission of the Medical Board in Hamburg and by the local authorities and the doxycycline studies by the Ethics Committee of the School of Medical Sciences of the Kwame Nkrumah University of Science, Kumasi, Ghana. The procedures used were in accordance with the Declaration of Helsinki (1975 and its revisions in 1983 and 2000).

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Authors and Affiliations

  1. Bernhard Nocht Institute for Tropical Medicine, Bernhard-Nocht-Str. 74, 20359, Hamburg, Germany

    Simone Korten, Dietrich W. Büttner, Christel Schmetz & Norbert Brattig

  2. Institute for Medical Microbiology, Immunology and Parasitology, University of Bonn, Sigmund-Freud-Str. 25, 53105, Bonn, Germany

    Simone Korten, Achim Hoerauf & Sabine Mand

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  1. Simone Korten
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  2. Dietrich W. Büttner
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  3. Christel Schmetz
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  5. Sabine Mand
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  6. Norbert Brattig
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Correspondence to Simone Korten.

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Korten, S., Büttner, D.W., Schmetz, C. et al. The nematode parasite Onchocerca volvulus generates the transforming growth factor-beta (TGF-beta). Parasitol Res 105, 731–741 (2009). https://doi.org/10.1007/s00436-009-1450-9

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  • DOI: https://doi.org/10.1007/s00436-009-1450-9

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