Season affects the estrogen system and the immune response of common carp

Fish Physiol Biochem. 2024 Apr;50(2):797-812. doi: 10.1007/s10695-023-01286-2. Epub 2023 Dec 29.

Abstract

The physiology of ectothermic animals, including fish, is strictly regulated by season-related external factors such as temperature or photoperiod. The immune response and the production of hormones, such as estrogens, are therefore also subject to seasonal changes. This study in common carp aimed to determine how the season affects the estrogen system and the immune response, including the antibacterial response during Aeromonas salmonicida infection. We compared the immune reaction in spring and autumn in the head kidney and liver and found that carp have higher levels of blood 17β-estradiol in autumn, while in the liver of these fish there is a higher constitutive expression of genes encoding vitellogenin, estrogen receptors and Cyp19 aromatase than in spring. Fish sampled in autumn also exhibited higher expression of immune-related genes in the liver. In contrast, in the head kidney from fish sampled in the autumn, the expression of genes encoding estrogen receptors and aromatase was lower than in spring, and a similar profile of expression was also measured in the head kidney for inos, arginases and il-10. In turn, during bacterial infection, we observed higher upregulation of the expression of inos, il-12p35, ifnγ-2, arginase 2 and il-10 in the liver of carp sampled in spring. In the liver of carp infected in spring a higher upregulation of the expression of the genes encoding CRPs was observed compared to fish infected during autumn. The opposite trend occurred in the head kidney, where the upregulation of the expression of the genes involved in the immune response was higher in fish infected in autumn than in those infected in spring. During the infection, also season-dependent changes occurred in the estrogen system. In conclusion, we demonstrated that season differentially affects the estrogenic and immune activity of the head kidney and liver. These results reinforce our previous findings that the endocrine and immune systems cooperate in maintaining homeostasis and fighting infection.

Keywords: Common carp; Estrogen system; Head kidney; Immune response; Liver; Seasonality.

MeSH terms

  • Animals
  • Aromatase / genetics
  • Aromatase / metabolism
  • Carps* / genetics
  • Carps* / metabolism
  • Estrogens / metabolism
  • Fish Diseases*
  • Gram-Negative Bacterial Infections*
  • Immunity, Innate
  • Interleukin-10
  • Receptors, Estrogen / genetics
  • Receptors, Estrogen / metabolism
  • Seasons

Substances

  • Interleukin-10
  • Aromatase
  • Estrogens
  • Receptors, Estrogen