Triazole pesticides exposure impaired steroidogenesis associated to an increase in AHR and CAR expression in testis and altered sperm parameters in chicken

Loïse Serra; Guillaume Bourdon; Anthony Estienne; Mathias Fréville; Christelle Ramé; Claire Chevaleyre; Philippe Didier; Marine Chahnamian; Patrice Ganier; Florine Pinault; Pascal Froment; Joëlle Dupont

doi:10.1016/j.toxrep.2023.03.005

Triazole pesticides exposure impaired steroidogenesis associated to an increase in AHR and CAR expression in testis and altered sperm parameters in chicken

Toxicol Rep. 2023 Mar 21:10:409-427. doi: 10.1016/j.toxrep.2023.03.005. eCollection 2023.

Affiliations

¹ CNRS, IFCE, INRAE, Université de Tours, PRC, F-37380 Nouzilly, France.
² INRAE - Unité Expérimentale du Pôle d'Expérimentation Avicole de Tours UEPEAT 1295, F-37380 Nouzilly, France.

Abstract

Since several decades, we observe the decline of various bird populations that could be partly linked to the agricultural intensification and the use of large amount of pesticides. Even if triazoles compounds are the most widely used fungicides, their effects on the reproductive parameters in birds are not clearly known. In the present study, we investigated the in vitro effects of 8 triazoles compounds alone (propiconazole (PP, from 0 to 10 µM), prothioconazole (PT), epoxiconazole (Epox), tetraconazole (TT), tebuconazole (TB), difenoconazole (Dif), cyproconazole (Cypro), metconazole (MC) (from 0 to 1 mM)) on the male chicken reproductive functions by using testis explants, primary Sertoli cells and sperm samples. In testis, all triazoles at the higher concentrations for 48 h inhibited lactate and testosterone secretion mostly in association with reduced expression of HSD3B and/or STAR mRNA levels. These data were also associated with increased expression of the nuclear receptors Aryl Hydrocarbon Receptor (AHR) and Constitutive Androstane Receptor (CAR) mRNA levels in testis and for all triazoles except for PP a reduction in Sertoli cell viability. When focusing on the sperm parameters, we demonstrated that most of the triazoles (MC, Epox, Dif, TB, TT and Cypro) at 0.1 or 1 mM for either 2, 12 or 24 min of exposure decreased sperm motility and velocity and increased the percentage of spermatozoa abnormal morphology. At the opposite, PP increased sperm motility in a dose dependent manner after 2 min of exposure whereas no significant effect was observed in response to PT whatever the dose and the time of exposure. Moreover, these effects were associated with an increase in the production of reactive oxygen species in spermatozoa. Taken together, most of the triazoles compounds impair testis steroidogenesis and semen parameters potentially through an increase in AHR and CAR expression and in oxidative stress, respectively.

Data availability statement: All the data will be available.

Keywords: AHR; CAR; Chicken; Rooster; Sperm; Steroidogenesis; Triazole.