Parasitology Research

, Volume 91, Issue 2, pp 144–150 | Cite as

Preliminary study on sex-related inflammatory reactions in mice infected with Schistosoma mansoni

  • J. Boissier
  • K. Chlichlia
  • Y. Digon
  • A. Ruppel
  • H. Moné
Original Paper
First Online:
Received:
Accepted:

Abstract

The aim of this study was to investigate the contribution of the sex of both the parasite and the host to the inflammatory response induced in unisexual infections of Schistosoma mansoni in mice. Organ weight, cell count and the delayed type hypersensitivity reaction were used as tools in this comparative study. The inflammatory reactions differed as a function of the sex of both the host and the parasite. Female mice showed a stronger inflammatory reaction to schistosome infection than males, while male schistosomes induced a stronger inflammatory response compared to females. The host-related differences in the inflammatory reaction may reflect differences in the factors affecting the immune defence of male and female mice. The differences in the inflammatory response induced by the parasite are discussed in terms of the quantity and quality of antigens among male and female worms.

Keywords

Male Parasite Parasite Antigen Schistosome Infection Female Parasite Strong Inflammatory Response 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
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Notes

Acknowledgements

This work was supported financially by the UNDP World Bank WHO Special Program for Research and Training in Tropical Diseases, the French Ministère de l'Enseignement Supérieur et de la Recherche, the Centre National de la Recherche Scientifique and the Conseil Régional du Languedoc-Roussillon. The experiments comply with the current laws of France and Germany.

References

  1. Attallah AM, Smith AH, Murrell KD, Fleischer A, Woody J, Vannier WE, Scher I, Ahmed A, Sell KW (1979) Characterization of the immunosuppressive state during Schistosoma mansoni infection. J Immunol 122:1413–1420PubMedGoogle Scholar
  2. Baki CA, Guerret S, Grimaud JA, Chevallier M (1998) Liver fibrosis in unisexual murine schistosomiasis: quantitative study and morphological changes in mice with chronic infection. Cell Mol Biol 44:627–633Google Scholar
  3. Bickle Q, Bain J, McGregor A, Doenhoff M (1979) Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse. III. The failure of primary infections with cercariae of one sex to induce resistance to reinfection. Trans R Soc Trop Med Hyg 73:37–41PubMedGoogle Scholar
  4. Blazkovec AA, Orsini MW (1976) Ontogenic aspects of sexual dimorphism and the primary immune response to sheep erythrocytes in hamsters from prepuberty through senescence. Int Arch Allergy Immunol 50:55–67Google Scholar
  5. Boissier J, Moné H (2000) Experimental observations on the sex ratio of adult Schistosoma mansoni, with comments on the natural male bias. Parasitology 121:379–383CrossRefPubMedGoogle Scholar
  6. Boissier J, Morand S, Moné H (1999) A review of performance and pathogenicity of male and female Schistosoma mansoni during the life cycle. Parasitology 119:447–454CrossRefPubMedGoogle Scholar
  7. Davis AH, Blanton R, Kich P (1985) Stage and sex specific differences in actin gene expression in Schistosoma mansoni. Mol Biochem Parasitol 17:289–298CrossRefPubMedGoogle Scholar
  8. Eloi-Santos S, Olsen NJ, Correa-Oliveira R, Colley DG (1992) Schistosoma mansoni: mortality, pathophysiology, and susceptibility differences in male and female mice. Exp Parasitol 75:168–192PubMedGoogle Scholar
  9. Eppert A, Lewis FA, Grzywacz C, Coura-Filho P, Caldas I, Minchella DJ (2002) Distribution of schistosome infections in molluscan hosts at different levels of parasite prevalence. J Parasitol 88:232–236PubMedGoogle Scholar
  10. Fantappie MR, Galina A, Luis de Mendonca R, Furtado DR, Secor WE, Colley DG, Correa-Oliveira R, Freeman GJ, Tempone AJ, Lannes de Camargo L, Rumjanek DF (1999) Molecular characterisation of a NADH ubiquinone oxidoreductase subunit 5 from Schistosoma mansoni and inhibition of mitochondrial respiratory chain function by testosterone. Mol Cell Biochem 202:149–158CrossRefPubMedGoogle Scholar
  11. Harrison RA, Bickle Q, Doenhoff MJ (1982) Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse. Evidence that the mechanisms which mediate resistance during early patent infections may lack immunological specificity. Parasitology 84:93–110PubMedGoogle Scholar
  12. Hoffman KF, Johnston DA, Dunne DW (2002) Identification of Schistosoma mansoni gender-associated gene transcripts by cDNA microarray profiling. Genome Biol 3: research 0041.1–0041.12CrossRefGoogle Scholar
  13. Hsu SYL (1969) Sex of schistosome cercariae as a factor in the immunization of rhesus monkeys. Exp Parasitol 25:202–209PubMedGoogle Scholar
  14. Leptak CL, McKerrow JH (1997) Schistosome egg granulomas and hepatic expression of TNF-α are dependent on immune priming during parasite maturation. J Immunol 158:301–307PubMedGoogle Scholar
  15. Lopes JD, Moreira AAB, Campos R, Kanamura HY, Hoshino-Shimizu S, Gayotto LCC, Da Silva LC (1981). Circulating antigens, antibodies and glomerular immune complexes in mice with unisexual Schistosoma mansoni infection. Rev Inst Med Trop Sao Paulo 23:155–160PubMedGoogle Scholar
  16. Mahmoud AAF, Woodruff AW (1978) The causation of splenomegaly in schistosomiasis in mice. Clin Sci Mol Med 54:397–401PubMedGoogle Scholar
  17. Martin JT (2000) Sexual dimorphism in immune function: the role of prenatal exposure to androgens and estrogens. Eur J Pharmacol 405:251–261CrossRefPubMedGoogle Scholar
  18. Menrath M, Michel A, Kunz W (1995) A female-specific cDNA sequence of Schistosoma mansoni encoding a mucin-like protein that is expressed in the epithelial cells of the reproductive duct. Parasitology 111:477–483PubMedGoogle Scholar
  19. Minchella DJ, Sollenberger KM, Pereira de Souza C (1995) Distribution of schistosome genetic diversity within molluscan intermediate hosts. Parasitology 111:217–220PubMedGoogle Scholar
  20. Moloney NA, Hinchcliffe P, Webbe G (1986) The ability of single sex infections of Schistosoma japonicum to induce resistance to reinfection in mice. J Helminthol 60:250–254PubMedGoogle Scholar
  21. Moné H, Mouahid G, Shaban MA, Al Jabri A, Boissier J, Ruppel A, Idris M (2003) Ecological and molecular studies on emerging schistosomiasis mansoni in Dhofar Governorate, Sultanate of Oman. Trop Med Int Health 8:269–276PubMedGoogle Scholar
  22. Mota-Santos TA, Toledo MIM, Correa MCR, Correa-Oliveira R, Gazzinelli G (1981) Schistosomiasis from S. mansoni in mice: the relationship between acquired immunity and serum levels of lethal antibody. Parasite Immunol 3:319–325PubMedGoogle Scholar
  23. Nakazawa M, Fantappie MR, Freeman GJ, Eloi-Santos S, Olsen NJ, Kovacs WJ, Secor WE, Colley DG (1997) Schistosoma mansoni: susceptibility differences between male and female mice can be mediated by testosterone during early infection. Exp Parasitol 85:233–240CrossRefPubMedGoogle Scholar
  24. Nash TE (1978) Antibody response to a polysaccharide antigen present in the schistosome gut. Am J Trop Med Hyg 27:938–943Google Scholar
  25. Nelson JL, Steinberg AD (1987) Sex steroids, autoimmunity and autoimmune diseases. In: Berczi I, Kovacs K(eds) Hormones and immunity. MTP Press, The HagueGoogle Scholar
  26. Noya O, Alarcon de Noya B, Losada S, Colmenares C, Guzman C, Lorenzo MA, Bermudez H (2002) Laboratory diagnosis of schistosomiasis in areas of low transmission: a review of a line of research. Mem Inst Oswaldo Cruz 97:167–169PubMedGoogle Scholar
  27. Ruppel A, Diesfeld HJ, Rother U (1985a) Immunoblot analysis of Schistosoma mansoni antigens with sera of schistosomiasis patients: diagnostic potential of an adult schistosome polypeptide. Clin Exp Immunol 62:499–506PubMedGoogle Scholar
  28. Ruppel A, Diesfeld HJ, Hempelmann E, Janitschke K, Karam M, Breternitz U, Rother U, Burger R (1985b) Schistosoma mansoni: characterization of a protein with diagnostic potential using monospecific patient sera and monoclonal antibodies. Immunobiology 170:76Google Scholar
  29. Silva CLM, Morel N, Lenzi HL, Noel F (1998) Increased reactivity to 5-hydroxytryptamine of portal veins from mice infected with Schistosoma mansoni. Comp Biochem Physiol Part A 120:417–423CrossRefGoogle Scholar
  30. Sire C, Durand P, Pointier JP, Théron A (1999) Genetic diversity and recruitment pattern of Schistosoma mansoni in a Biomphalaria glabrata snail population: a field study using random-amplifield polymorphic DNA markers. J Parasitol 83:436–441Google Scholar
  31. Smithers SR (1962) Stimulation of acquired resistance to Schistosoma mansoni in monkeys: role of eggs and worms. Exp Parasitol 12:263–273Google Scholar
  32. Vogel H (1941) Infektionsversuche an verschiedenen Bilharzia-Zwischenwirten mit einen einzelnen Mirazidium von Bilharzia mansoni und B. japonica. Zentralbl Bakteriol 1 Abt Orig B Hyg Krankenhaushyg Betriebshyg Praev Med 148:29–35Google Scholar
  33. Vogel H, Minning W (1953) Über die erworbene resistenz von Macacus rhesus gegenüber Schistosoma japonicum. Z Tropenmed Parasitol 4:418–505Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • J. Boissier
    • 1
  • K. Chlichlia
    • 2
  • Y. Digon
    • 1
  • A. Ruppel
    • 2
  • H. Moné
    • 1
  1. 1.UMR 5555 CNRS-UP Parasitologie Fonctionnelle et Evolutive, CBETMUniversité de Perpignan Perpignan France
  2. 2.Department of Tropical HygieneUniversity of HeidelbergHeidelbergGermany

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