Impaired spermatogenesis and associated endocrine effects of azole fungicides in peripubertal Xenopus tropicalis
Early life exposure to endocrine disrupting chemicals (EDCs) has been suggested to adversely affect reproductive health in humans and wildlife. Here, we characterize endocrine and adverse effects on the reproductive system after juvenile exposure to propiconazole (PROP) or imazalil (IMZ), two common...
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| Format: | Article |
| Language: | English |
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Elsevier
2024-01-01
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| Series: | Ecotoxicology and Environmental Safety |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S0147651323013805 |
| _version_ | 1797350580175241216 |
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| author | Sofie Svanholm Vanessa Brouard Mauricio Roza Daniele Marini Oskar Karlsson Cecilia Berg |
| author_facet | Sofie Svanholm Vanessa Brouard Mauricio Roza Daniele Marini Oskar Karlsson Cecilia Berg |
| author_sort | Sofie Svanholm |
| collection | DOAJ |
| description | Early life exposure to endocrine disrupting chemicals (EDCs) has been suggested to adversely affect reproductive health in humans and wildlife. Here, we characterize endocrine and adverse effects on the reproductive system after juvenile exposure to propiconazole (PROP) or imazalil (IMZ), two common azole fungicides with complex endocrine modes of action. Using the frog Xenopus tropicalis, two short-term (2-weeks) studies were conducted. I: Juveniles (2 weeks post metamorphosis (PM)) were exposed to 0, 17 or 178 µg PROP/L. II: Juveniles (6 weeks PM) were exposed to 0, 1, 12 or 154 µg IMZ/L. Histological analysis of the gonads revealed an increase in the number of dark spermatogonial stem cells (SSCs)/testis area, and in the ratio secondary spermatogonia: dark SSCs were increased in all IMZ groups compared to control. Key genes in gametogenesis, retinoic acid and sex steroid pathways were also analysed in the gonads. Testicular levels of 3β-hsd, ddx4 were increased and cyp19 and id4 levels were decreased in the IMZ groups. In PROP exposed males, increased testicular aldh1a2 levels were detected, but no histological effects observed. Although no effects on ovarian histology were detected, ovarian levels of esr1, rsbn1 were increased in PROP groups, and esr1 levels were decreased in IMZ groups. In conclusion, juvenile azole exposure disrupted testicular expression of key genes in retinoic acid (PROP) and sex steroid pathways and in gametogenesis (IMZ). Our results further show that exposure to environmental concentrations of IMZ disrupted spermatogenesis in the juvenile testis, which is a cause for concern as it may lead to impaired fertility. Testicular levels of id4, ddx4 and the id4:ddx4 ratio were associated with the number of dark SSCs and secondary spermatogonia suggesting that they may serve as a molecular markers for disrupted spermatogenesis. |
| first_indexed | 2024-03-08T12:47:00Z |
| format | Article |
| id | doaj.art-0f6d276a656f4d138124b628dc25295a |
| institution | Directory Open Access Journal |
| issn | 0147-6513 |
| language | English |
| last_indexed | 2024-03-08T12:47:00Z |
| publishDate | 2024-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Ecotoxicology and Environmental Safety |
| spelling | doaj.art-0f6d276a656f4d138124b628dc25295a2024-01-21T05:05:14ZengElsevierEcotoxicology and Environmental Safety0147-65132024-01-01270115876Impaired spermatogenesis and associated endocrine effects of azole fungicides in peripubertal Xenopus tropicalisSofie Svanholm0Vanessa Brouard1Mauricio Roza2Daniele Marini3Oskar Karlsson4Cecilia Berg5Department of Environmental Toxicology, Uppsala University, SE-754 36 Uppsala, Sweden; Corresponding author.Department of Environmental Toxicology, Uppsala University, SE-754 36 Uppsala, SwedenScience for Life Laboratory, Department of Environmental Science, Stockholm University, Stockholm 114 18, SwedenDepartment of Environmental Toxicology, Uppsala University, SE-754 36 Uppsala, Sweden; Department of Veterinary Medicine, University of Perugia, 06126 Perugia, ItalyScience for Life Laboratory, Department of Environmental Science, Stockholm University, Stockholm 114 18, SwedenDepartment of Environmental Toxicology, Uppsala University, SE-754 36 Uppsala, SwedenEarly life exposure to endocrine disrupting chemicals (EDCs) has been suggested to adversely affect reproductive health in humans and wildlife. Here, we characterize endocrine and adverse effects on the reproductive system after juvenile exposure to propiconazole (PROP) or imazalil (IMZ), two common azole fungicides with complex endocrine modes of action. Using the frog Xenopus tropicalis, two short-term (2-weeks) studies were conducted. I: Juveniles (2 weeks post metamorphosis (PM)) were exposed to 0, 17 or 178 µg PROP/L. II: Juveniles (6 weeks PM) were exposed to 0, 1, 12 or 154 µg IMZ/L. Histological analysis of the gonads revealed an increase in the number of dark spermatogonial stem cells (SSCs)/testis area, and in the ratio secondary spermatogonia: dark SSCs were increased in all IMZ groups compared to control. Key genes in gametogenesis, retinoic acid and sex steroid pathways were also analysed in the gonads. Testicular levels of 3β-hsd, ddx4 were increased and cyp19 and id4 levels were decreased in the IMZ groups. In PROP exposed males, increased testicular aldh1a2 levels were detected, but no histological effects observed. Although no effects on ovarian histology were detected, ovarian levels of esr1, rsbn1 were increased in PROP groups, and esr1 levels were decreased in IMZ groups. In conclusion, juvenile azole exposure disrupted testicular expression of key genes in retinoic acid (PROP) and sex steroid pathways and in gametogenesis (IMZ). Our results further show that exposure to environmental concentrations of IMZ disrupted spermatogenesis in the juvenile testis, which is a cause for concern as it may lead to impaired fertility. Testicular levels of id4, ddx4 and the id4:ddx4 ratio were associated with the number of dark SSCs and secondary spermatogonia suggesting that they may serve as a molecular markers for disrupted spermatogenesis.http://www.sciencedirect.com/science/article/pii/S0147651323013805Endocrine disruptionSpermatogenesisPeripubertalAzolesAmphibians |
| spellingShingle | Sofie Svanholm Vanessa Brouard Mauricio Roza Daniele Marini Oskar Karlsson Cecilia Berg Impaired spermatogenesis and associated endocrine effects of azole fungicides in peripubertal Xenopus tropicalis Ecotoxicology and Environmental Safety Endocrine disruption Spermatogenesis Peripubertal Azoles Amphibians |
| title | Impaired spermatogenesis and associated endocrine effects of azole fungicides in peripubertal Xenopus tropicalis |
| title_full | Impaired spermatogenesis and associated endocrine effects of azole fungicides in peripubertal Xenopus tropicalis |
| title_fullStr | Impaired spermatogenesis and associated endocrine effects of azole fungicides in peripubertal Xenopus tropicalis |
| title_full_unstemmed | Impaired spermatogenesis and associated endocrine effects of azole fungicides in peripubertal Xenopus tropicalis |
| title_short | Impaired spermatogenesis and associated endocrine effects of azole fungicides in peripubertal Xenopus tropicalis |
| title_sort | impaired spermatogenesis and associated endocrine effects of azole fungicides in peripubertal xenopus tropicalis |
| topic | Endocrine disruption Spermatogenesis Peripubertal Azoles Amphibians |
| url | http://www.sciencedirect.com/science/article/pii/S0147651323013805 |
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