Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-09T20:22:54.703Z Has data issue: false hasContentIssue false

Ligulaintestinalis infection is associated with alterations of both brain and gonad aromatase expression in roach (Rutilusrutilus)

Published online by Cambridge University Press:  10 November 2010

C. Boulange-Lecomte*
Affiliation:
Laboratory of Ecotoxicology, University of Le Havre, BP 540, 76058Le Havre, France
P. Geraudie
Affiliation:
Laboratory of Ecotoxicology, University of Le Havre, BP 540, 76058Le Havre, France
J. Forget-Leray
Affiliation:
Laboratory of Ecotoxicology, University of Le Havre, BP 540, 76058Le Havre, France
M. Gerbron
Affiliation:
Laboratory of Ecotoxicology, University of Le Havre, BP 540, 76058Le Havre, France
C. Minier
Affiliation:
Laboratory of Ecotoxicology, University of Le Havre, BP 540, 76058Le Havre, France
*
*Fax: +33 2 32 74 43 14 E-mail: [email protected]

Abstract

The tapeworm Ligulaintestinalis commonly infests roach (Rutilusrutilus) and is responsible for the inhibition of gonad development. In order to better understand the effect of the plerocercoid on fish physiology, and to discriminate parasitization effects from those of endocrine-disrupting compounds (EDC), Cyp19b and Cyp19a aromatase expression was investigated by real-time quantitative polymerase chain reaction (PCR) in brain and gonads of ligulosed roach, caught from a reference site. Data were compared to reproductive and endocrine endpoints previously reported in a larger cohort study (including the sampled population of the present one), such as gonadosomatic index, Fulton index, gonadal histology, plasma sex steroid levels and brain aromatase activity. A decrease in Cyp19b expression in the brain of infected fish was demonstrated, in agreement with the reduction of aromatase activity previously described. In contrast, Cyp19a expression in the gonads appeared to be enhanced in ligulosed fish, in accordance with the presence of immature but differentiated sexual tissues. Together these results show that: (1) L. intestinalis infestation results in an alteration of aromatase expression which, in particular, may have profound effects on the fish brain; and (2) L. intestinalis infection must be considered as a major confounding factor in ecotoxicological studies using aromatase expression as an EDC biomarker. Moreover, the concordance between activity and expression – investigated for the first time in the same population – gives a functional relevance to the transcript aromatase dosage in the brain. Finally, quantitative PCR was confirmed as a sensitive approach, enabling aromatase status to be defined in the poorly developed gonads of ligulosed individuals.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2010

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

Arme, C. (2002) Ligula intestinalis – a tapeworm contraceptive. Biologist (London) 49, 265269.Google ScholarPubMed
Arme, C. & Owen, R.W. (1968) Occurrence and pathology of Ligula intestinalis infections in British fish. Journal of Parasitology 54, 272280.Google Scholar
Callard, G.V., Tchoudakova, A.V., Kishida, M. & Wood, E. (2001) Differential tissue distribution, developmental programming, estrogen regulation and promoter characteristics of cyp19 genes in teleost fish. The Journal of Steroid Biochemistry and Molecular Biology 79, 305314.CrossRefGoogle ScholarPubMed
Carter, V., Pierce, R., Dufour, S., Arme, C. & Hoole, D. (2005) The tapeworm Ligula intestinalis (Cestoda: Pseudophyllidea) inhibits LH expression and puberty in its teleost host, Rutilus rutilus. Reproduction 130, 939945.Google Scholar
Cheshenko, K., Pakdel, F., Segner, H., Kah, O. & Eggen, R.I. (2008) Interference of endocrine disrupting chemicals with aromatase CYP19 expression or activity, and consequences for reproduction of teleost fish. General and Comparative Endocrinology 155, 3162.Google Scholar
Diotel, N., Page, Y.L., Mouriec, K., Tong, S.K., Pellegrini, E., Vaillant, C., Anglade, I., Brion, F., Pakdel, F., Chung, B.C. & Kah, O. (2010) Aromatase in the brain of teleost fish: expression, regulation and putative functions. Frontiers in Neuroendocrinology 31, 172192.CrossRefGoogle ScholarPubMed
Geraudie, P., Boulange-Lecomte, C., Gerbron, M., Hinfray, N., Brion, F. & Minier, C. (2010a) Endocrine effects of the tapeworm Ligula intestinalis in its teleost host, the roach (Rutilus rutilus). Parasitology 137, 697704.Google Scholar
Geraudie, P., Gerbron, M., Hill, E. & Minier, C. (2010b) Roach (Rutilus rutilus) reproductive cycle: a study of biochemical and histological parameters in a low contaminated site. Fish Physiology and Biochemistry 36, 767777.Google Scholar
Guiguen, Y., Fostier, A., Piferrer, F. & Chang, C.F. (2010) Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. General and Comparative Endocrinology 165, 352366.CrossRefGoogle ScholarPubMed
Hall, S.R., Becker, C. & Cáceres, C.E. (2007) Ecology and evolution of disease dynamics: parasitic castration: a perspective from a model of dynamic energy budgets. Integrative and Comparative Biology 47, 295309.Google Scholar
Hecker, M. & Karbe, L. (2005) Parasitism in fish – an endocrine modulator of ecological relevance? Aquatic Toxicology 72, 195207.Google Scholar
Hecker, M., Sanderson, J.T. & Karbe, L. (2007) Suppression of aromatase activity in populations of bream (Abramis brama) from the river Elbe, Germany. Chemosphere 66, 542552.CrossRefGoogle ScholarPubMed
Hellemans, J., Mortier, G., De Paepe, A., Speleman, F. & Vandesompele, J. (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biology 8, R19.Google Scholar
Hoole, D., Carter, V. & Dufour, S. (2010) Ligula intestinalis (Cestoda: Pseudophyllidea): an ideal fish-metazoan parasite model? Parasitology 137, 425438.CrossRefGoogle ScholarPubMed
Jobling, S. & Tyler, C.R. (2003) Endocrine disruption, parasites and pollutants in wild freshwater fish. Parasitology 126, S103S108.CrossRefGoogle ScholarPubMed
Kennedy, C.R., Shears, P.C. & Shears, J.A. (2001) Long-term dynamics of Ligula intestinalis and roach Rutilus rutilus: a study of three epizootic cycles over thirty-one years. Parasitology 123, 257269.CrossRefGoogle ScholarPubMed
Loot, G., Brosse, S., Lek, S. & Guegan, J.F. (2001) Behaviour of roach (Rutilus rutilus) altered by Ligula intestinalis (Cestoda: Pseudophyllidea): a field demonstration. Freshwater Biology 46, 12191227.CrossRefGoogle Scholar
Minier, C., Caltot, G., Leboulenger, F. & Hill, E.M. (2000) An investigation of the incidence of intersex fish in Seine-Maritime and Sussex regions. Analysis 28, 801806.Google Scholar
Munakata, A. & Kobayashi, M. (2010) Endocrine control of sexual behavior in teleost fish. General and Comparative Endocrinology 165, 456468.CrossRefGoogle ScholarPubMed
Orr, T.S.C. (1966) Spawning behaviour of Rudd, Scardinius erythrophthalmus infested with Plerocercoids of Ligula intestinalis. Nature 12, 736.Google Scholar
Sures, B. (2008) Environmental parasitology. Interactions between parasites and pollutants in the aquatic environment. Parasite 15, 434438.CrossRefGoogle ScholarPubMed
Trubiroha, A., Wuertz, S., Frank, S.N., Sures, B. & Kloas, W. (2009) Expression of gonadotropin subunits in roach (Rutilus rutilus, Cyprinidae) infected with plerocercoids of the tapeworm Ligula intestinalis (Cestoda). International Journal for Parasitology 39, 14651473.Google Scholar
Trubiroha, A., Kroupova, H., Wuertz, S., Frank, S.N., Sures, B. & Kloas, W. (2010) Naturally-induced endocrine disruption by the parasite Ligula intestinalis (Cestoda) in roach (Rutilus rutilus). General and Comparative Endocrinology 166, 234240.Google Scholar
Tyler, C.R., Lange, A., Paull, G.C., Katsu, Y. & Iguchi, T. (2007) The roach (Rutilus rutilus) as a sentinel for assessing endocrine disruption. Environmental Sciences 14, 235253.Google Scholar