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Blood-feeding in the young adult filarial worms Litomosoides sigmodontis

Published online by Cambridge University Press:  01 November 2004

T. ATTOUT ,
S. BABAYAN ,
A. HOERAUF ,
D. W. TAYLOR ,
W. J. KOZEK ,
C. MARTIN  and
O. BAIN
T. ATTOUT
Affiliation:
Parasitologie Comparée et Modèles expérimentaux, associé à l'INSERM (U567), Muséum National d'Histoire Naturelle et Ecole Pratique des Hautes Etudes, 61 rue Buffon, 75231 Paris cedex 05, France
S. BABAYAN
Affiliation:
Parasitologie Comparée et Modèles expérimentaux, associé à l'INSERM (U567), Muséum National d'Histoire Naturelle et Ecole Pratique des Hautes Etudes, 61 rue Buffon, 75231 Paris cedex 05, France Present address: ICAPB, Ashworth Laboratories, University of Edinburgh, West Main Road, Edinburgh EH9 3JT UK.
A. HOERAUF
Affiliation:
Institute of Medical Parasitology, University Clinic Bonn, Sigmund-Freud Strasse 25, 53105 Bonn, Germany
D. W. TAYLOR
Affiliation:
Centre for Infectious Diseases, Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Roslin Midlothian, Scotland, UK
W. J. KOZEK
Affiliation:
Department of Microbiology and Medical Zoology, Medical Sciences Campus, University of Puerto Rico, San Juan, Puerto Rico, 00936-5067, USA
C. MARTIN
Affiliation:
Parasitologie Comparée et Modèles expérimentaux, associé à l'INSERM (U567), Muséum National d'Histoire Naturelle et Ecole Pratique des Hautes Etudes, 61 rue Buffon, 75231 Paris cedex 05, France Present address: Leukocyte Biology/Biochemical Sciences Division, Imperial College School of Medicine, Sir Alexander Fleming Bdg, South Kensington, SW7 2AZ London, UK.
O. BAIN
Affiliation:
Parasitologie Comparée et Modèles expérimentaux, associé à l'INSERM (U567), Muséum National d'Histoire Naturelle et Ecole Pratique des Hautes Etudes, 61 rue Buffon, 75231 Paris cedex 05, France
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Abstract

In this study with the filarial model Litomosoides sigmodontis, we demonstrate that the worms ingest host red blood cells at a precise moment of their life-cycle, immediately after the fourth moult. The red blood cells (RBC) were identified microscopically in live worms immobilized in PBS at 4 °C, and their density assessed. Two hosts were used: Mongolian gerbils, where microfilaraemia is high, and susceptible BALB/c mice with lower microfilaraemia. Gerbils were studied at 12 time-points, between day 9 post-inoculation (the worms were young 4th stage larvae) and day 330 p.i. (worms were old adults). Only the very young adult filarial worms had red blood cells in their gut. Haematophagy was observed between days 25 and 56 p.i. and peaked between day 28 and day 30 p.i. in female worms. In males, haematophagy was less frequent and intense. Similar kinetics of haematophagy were found in BALB/c mice, but frequency and intensity tended to be lower. Haematophagy seems useful to optimize adult maturation. These observations suggest that haematophagy is an important step in the life-cycle of L. sigmodontis. This hitherto undescribed phenomenon might be characteristic of other filarial species including human parasites.

Keywords

filariaLitomosoides sigmodontishaematophagy
Type
Research Article
Information
Parasitology , Volume 130 , Issue 4 , April 2005 , pp. 421 - 428
Copyright
2005 Cambridge University Press

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References

REFERENCES

AL-QAOUD, K. M., TAUBERT, A., ZAHNER, H., FLEISCHER, B. & HOERAUF, A. ( 1997). Infection of BALB/c mice with the filarial nematode Litomosoides sigmodontis: role of CD4+ T cells in controlling larval development. Infection and Immunity 65, 2457–2461.Google Scholar
ALLEN, J. E., DAUB, J., GUILIANO, D., McDONNELL, A., LIZOTTE-WANIEWSKI, M., TAYLOR, D. W. & BLAXTER, M. ( 2000). Analysis of genes expressed at the infective larval stage validates utility of Litomosoides sigmodontis as a murine model for filarial vaccine development. Infection and Immunity 68, 5454–5458.CrossRefGoogle Scholar
ARASU, P. ( 2001). In vitro reactivation of Ancylostoma caninum tissue-arrested third-stage larvae by transforming growth factor-beta. Journal of Parasitology 87, 733–738.Google Scholar
BABAYAN, S., UNGEHEUER, M. N., MARTIN, C., ATTOUT, T., BELNOUE, E., SNOUNOU, G., RENIA, L., KORENAGA, M. & BAIN, O. ( 2003). Resistance and susceptibility to filarial infection with Litomosoides sigmodontis are associated with early differences in parasite development and in localized immune reactions. Infection and Immunity 71, 6820–6829.CrossRefGoogle Scholar
BABAYAN, S., ATTOUT, T., SPECHT, S., HOERAUF, A., SNOUNOU, G., RÉNIA, L., KORENAGA, M., BAIN, O. & MARTIN, C. ( 2004). Increased early local immune responses and altered worm development in high dose infections of mice susceptible to the filaria Litomosoides sigmodontis. Medical Microbiology and Immunology (in the Press).Google Scholar
BAIN, O. ( 2002). Evolutionary relationships among filarial nematodes. In The Filaria, World Class Parasites (ed. Klei, T. R. & Rajan, T. V.), Vol. 5, pp. 21–30. Kluwer Academic Publishers, Boston, USA.CrossRef
BAIN, O. & BABAYAN, S. ( 2003). Behaviour of filariae: morphological and anatomical signatures of their life style within the arthropod and vertebrate hosts. Filaria Journal 2, 1–12.Google Scholar
BAIN, O. & GUERRERO, R. ( 2003). Bisbalia vossi n. g., n. sp. (Nematoda: Onchocercidae), a filarial worm from a geomyoid rodent, Heteromys anomalus, in Venezuela. Systematic Parasitology 54, 145–151.Google Scholar
BAIN, O., PETIT, G. & DIAGNE, M. ( 1989). Etude de quelques Litomosoides parasites de rongueur; conséquences taxonomiques. Annales de Parasitologie Humaine et Comparée 64, 268–289.CrossRefGoogle Scholar
BEG, M. A., FISTEIN, J. L. & STOREY, D. M. ( 1995). The host-parasite relationships in pyridoxine (vitamin B6) deficient cotton rats infected with Litomosoides carinii (Nematoda: Filaroidea). Parasitology 111, 111–118.CrossRefGoogle Scholar
BRINKWORTH, R. I., PROCIV, P., LOUKAS, A. & BRINDLEY, P. J. ( 2001). Hemoglobin-degrading, aspartic proteases of blood-feeding parasites: substrate specificity revealed by homology models. Journal of Biological Chemistry 276, 38844–38851.CrossRefGoogle Scholar
CHEN, S. N. & HOWELLS, R. E. ( 1981). Brugia pahangi: uptake and incorporation of nucleic acid precursors by microfilariae and macrofilariae in vitro. Experimental Parasitology 51, 296–306.CrossRefGoogle Scholar
CLAESSON-WELSH, L. ( 1994 a). Platelet-derived growth factor receptor signals. Journal of Biological Chemistry 269, 32023–32026.Google Scholar
CLAESSON-WELSH, L. ( 1994 b). Signal transduction by the PDGF receptors. Progress in Growth Factor Research 5, 37–54.Google Scholar
CROSS, J. B. & SCOTT, J. A. ( 1947). The developmental anatomy of the fourth stage larvae and adults of Litomosoides carinii, a filarial worm of the cotton rat. Transactions of the American Microscopical Society 66, 1–21.CrossRefGoogle Scholar
DIAGNE, M., PETIT, G., LIOT, P., CABARET, J. & BAIN, O. ( 1990). The filaria Litomosoides galizai in mites; microfilarial distribution in the host and regulation of the transmission. Annales de Parasitologie Humaine et Comparée 65, 193–199.CrossRefGoogle Scholar
FRANZ, M. & BUTTNER, D. W. ( 1983). The fine structure of adult Onchocerca volvulus. V. The digestive tract and the reproductive system of the female worm. Tropenmedizin und Parasitologie 34, 155–161.Google Scholar
GOMEZ-ESCOBAR, N.GREGORY, W. F. & MAIZELS, R. M. ( 2000). Identification of tgh-2, a filarial nematode homolog of Caenorhabditis elegans daf-7 and human transforming growth factor beta, expressed in microfilarial and adult stages of Brugia malayi. Infection and Immunity 68, 6402–6410.CrossRefGoogle Scholar
GOMEZ-ESCOBAR, N.LEWIS, E. & MAIZELS, R. M. ( 1998). A novel member of the transforming growth factor-beta (TGF-beta) superfamily from the filarial nematodes Brugia malayi and B. pahangi. Experimental Parasitology 88, 200–209.CrossRefGoogle Scholar
KNOX, D. P., SKUCE, P. J., NEWLANDS, G. F. & REDMOND, D. L. ( 2001). Nematode gut peptidases, proteins and vaccination. In Parasitic Nematodes. Molecular Biology, Biochemistry and Immunology (ed. Kennedy, M. W. & Harnett, W.), pp. 247–268. CABI Publishing, Wallingford.CrossRef
LE GOFF, L., LAMB, T., GRAHAM, A., HARCUS, Y. & ALLEN, J. ( 2002). IL-4 is required to prevent filarial nematode development in resistant but not susceptible strains of mice. International Journal for Parasitology 32, 1277–1284.CrossRefGoogle Scholar
MARECHAL, P., LE GOFF, L., PETIT, G., DIAGNE, M., TAYLOR, D. W. & BAIN, O. ( 1996). The fate of the filaria Litomosoides sigmodontis in susceptible and naturally resistant mice. Parasite 3, 25–31.CrossRefGoogle Scholar
MARTIN, C., AL-QAOUD, K. M., UNGEHEUER, M. N., PAEHLE, K., VUONG, P. N., BAIN, O., FLEISCHER, B. & HOERAUF, A. ( 2000 a). IL-5 is essential for vaccine-induced protection and for resolution of primary infection in murine filariasis. Medical Microbiology and Immunology 189, 67–74.Google Scholar
MARTIN, C., LE GOFF, L., UNGEHEUER, M. N., VUONG, P. N. & BAIN, O. ( 2000 b). Drastic reduction of a filarial infection in eosinophilic interleukin-5 transgenic mice. Infection and Immunity 68, 3651–3656.Google Scholar
MARTIN, C., SAEFTEL, M., VUONG, P. N., BABAYAN, S., FISCHER, K., BAIN, O. & HOERAUF, A. ( 2001). B-Cell Deficiency Suppresses Vaccine-induced protection against murine filariasis but does not increase the recovery rate for primary infection. Infection and Immunity 69, 7067–7073.CrossRefGoogle Scholar
MEYER-INGOLD, W. & EICHNER, W. ( 1995). Platelet-derived growth factor. Cell Biology International 19, 389–398.CrossRefGoogle Scholar
NEWTON, S. E. & MUNN, E. A. ( 1999). The development of vaccines against gastrointestinal nematode parasites, particularly Haemonchus contortus. Parasitology Today 15, 116–122.CrossRefGoogle Scholar
PETIT, G., DIAGNE, M., MARECHAL, P., OWEN, D., TAYLOR, D. & BAIN, O. ( 1992). Maturation of the filaria Litomosoides sigmodontis in BALB/c mice: comparative susceptibility of nine other inbred strains. Annales de Parasitologie Humaine et Comparée 67, 144–150.CrossRefGoogle Scholar
PUDNEY, M., LITCHFIELD, T., BIANCO, A. E. & MacKENZIE, C. D. ( 1988). Moulting and exsheathment of the infective larvae of Onchocerca lienalis (Filarioidea) in vitro. Acta Tropica 45, 67–76.Google Scholar
ROBBINS, S. L., COTRAN, R. S. & KUMAR, V. ( 1994). Pathologic Basis of Diseases, 5th Edn. W. B. Saunders, Philadelphia, USA.
SAEFTEL, M., VOLKMANN, L., KORTEN, S., BRATTIG, N., AL-QAOUD, K., FLEISCHER, B. & HOERAUF, A. ( 2001). Lack of interferon-gamma confers impaired neutrophil granulocyte function and imparts prolonged survival of adult filarial worms in murine filariasis. Microbes and Infection 3, 203–213.CrossRefGoogle Scholar
SMITH, W. D., NEWLANDS, G. F., SMITH, S. K., PETTIT, D. & SKUCE, P. J. ( 2003). Metalloendopeptidases from the intestinal brush border of Haemonchus contortus as protective antigens for sheep. Parasite Immunology 25, 313–323.CrossRefGoogle Scholar
STOREY, D. M. ( 1982). The host-parasite relationships in normal and protein-malnourished cotton rats infected with Litomosoides carinii (Nematoda: Filarioidea). Parasitology 85, 543–558.CrossRefGoogle Scholar
STURCHLER, D., HANCK, A., WEISER, H., MANZ, U. & WEISS, N. ( 1985). Retinol deficiency and Dipetalonema viteae infection in the hamster. Journal of Helminthology 59, 201–210.CrossRefGoogle Scholar
TISSENBAUM, H. A., HAWDON, J., PERREGAUX, M., HOTEZ, P., GUARENTE, L. & RUVKUN, G. ( 2000). A common muscarinic pathway for diapause recovery in the distantly related nematode species Caenorhabditis elegans and Ancylostoma caninum. Proceedings of the National Academy of Sciences, USA 97, 460–465.CrossRefGoogle Scholar
URATA, J., SHOJO, H. & KANEKO, Y. ( 2003). Inhibition mechanisms of hematophagous invertebrate compounds acting on the host blood coagulation and platelet aggregation pathways. Biochimie 85, 493–500.CrossRefGoogle Scholar
VOLKMANN, L., BAIN, O., SAEFTEL, M., SPECHT, S., FISCHER, K., BROMBACHER, F., MATTHAEI, K. I. & HOERAUF, A. ( 2003). Murine filariasis: interleukin 4 and interleukin 5 lead to containment of different worm developmental stages. Medical Microbiology and Immunology 192, 23–31.Google Scholar
WILLIAMSON, A. L., BRINDLEY, P. J., KNOX, D. P., HOTEZ, P. J. & LOUKAS, A. ( 2003). Digestive proteases of blood-feeding nematodes. Trends in Parasitology 19, 417–423.CrossRefGoogle Scholar
ZHANG, M., ZOLA, H., READ, L. & PENTILLA, I. ( 2001). Identification of soluble transforming growth factor-beta receptor III (sTbetaIII) in rat milk. Immunology and Cell Biology 79, 291–297.CrossRefGoogle Scholar