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

Abstract

The tapeworm Ligula intestinalis commonly infests roach (Rutilus rutilus) 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.

Nemrut Krater (Turkey) Gölü’nde Yaşayan Barbus ercisianus (Cypriniformes: Cyprinidae) Balık Türünde Ligula intestinalis (Cestoda: Pseudophyllidea)‘in İlk Bildirimi

“…It can be argued that the parasites both cause stress in the body and excessively stimulate the body's immune system. In another study, changes in the expression levels of genes in brain and liver tissues were investigated in L. intestinalis-infected roaches (Rutilus rutilus) (Boulange-Lecomte et al, 2011). The researchers reported an increase in the IGF genes associated with immunity, especially in females, by about 190%, whereas only a partial increase was observed in males compared to the uninfected samples.…”

Challenges in assigning endocrine-specific modes of action: Recommendations for researchers and regulators

“…It has been well established that roach or bream infested by the tapeworm Ligula intestinalis can experience an inhibition of gonad development and maturation, as well as reduction in the expression of secondary sex characteristics in males. This is probably due to an increase in Cyp19a expression in the gonads and a decrease in the plasma sex steroids 17β‐estradiol and 11‐ketotestosterone, as well as decreases in plasma VTG concentrations and gene expression of VTG in liver, and an increase in Cyp19b expression in the brain observed in infected fish (Hecker and Karbe ; Boulange‐Lecomte et al ; Trubiroha et al ). Some infective agents, such as mycobacteria, microsporidia, or parasites, such as helminths, can be present in fish without any overt signs of illness, external lesions, and/or abnormal behavior.…”

Mass Death of Predatory Carp, <i>Chanodichthys erythropterus</i>, Induced by Plerocercoid Larvae of <i>Ligula intestinalis</i> (Cestoda: Diphyllobothriidae)

“…After that, a local news paper reported that more than 80% of pale chubs, Zacco platypus , in Hoengseong-dam were highly infected with these tapeworm larvae in December 2003. On the other hand, it has been known that the plerocercoid larvae of L. intestinalis induce endocrine disruption, in particular, parasitic castration [ 10 - 14 ], growth suppression, morphological modification [ 15 , 16 ], and mortality increase in the fish [ 17 , 18 ] as well as modified behavioral responses [ 4 , 19 - 22 ]. Recently, we observed a mass death of predatory carp, Chanodichthys erythropterus , infected with the plerocercoid larvae of L. intestinalis in the 4 sites of Nakdong-gang (‘gang’ means river).…”

“…As an interesting example, mice infected with Toxoplasma gondii are easily eaten by the definitive host, the cat, because they become lack of phobia response against the predator [ 24 ]. In case of L. intestinalis , it has been known that the plerocercoid larvae induce endocrine disruption that can lead to parasitic castration [ 10 - 14 ], growth suppression, morphological modification [ 15 , 16 ], mortality increase in the host fish [ 17 , 18 ], and modified behavioral responses [ 4 , 19 - 22 ]. Therefore, the preference for the river-edge in L. intestinalis -infected fish during winter season is suggested to be a modified behavioral response similar to host manipulation by ligulid larvae.…”

“…Among these effects, the physiological function related to reproduction was frequently studied using the fish-ligulid parasite model. The decrease of pituitary gonadotropins, sex steroids, and brain aromatase expressions, as well as the inhibition of gonad maturation and development were mainly revealed as the results of these studies [ 10 - 14 , 27 ]. In the present study, although we did not approach functionally, we were able to know the infertility of infected carp viewing from absence of their reproductive organs at necropsy of the fish, probably because of degeneration.…”