Seasonal changes in gene expression of steroidogenic enzymes, androgen and estrogen receptors in frog testis

Abstract

The anuran amphibian Pelophylax esculentus shows an annual cycle of sexual steroid production and spermatogenesis. To more thoroughly comprehend the steroidogenic pathways that govern the seasonal reproductive cycle, we investigated the mRNA expression of key enzymes involved in the androgenic and oestrogenic biosynthesis pathways in the testis of frogs taken in the reproductive and postreproductive period. Furthermore, we also analysed androgen and oestrogen levels and their own receptor gene expressions. Our findings showed that during the reproductive period, 3β‐hydroxysteroid dehydrogenase, 17β‐hydroxysteroid dehydrogenase and 5α‐reductase mRNA levels were higher than those during the postreproductive period. High testosterone and 5α‐dihydrotestosterone titres as well as the expression levels of androgen receptors in the reproductive testis strongly confirmed that the androgenic pathway is necessary for spermatogenesis activation. Conversely, during the postreproductive period, the highest P450 aromatase, estrogen receptor α and β mRNA levels, paralleling with oestradiol titres, indicated that the oestrogenic pathway is essential for the interruption of the reproductive processes. Our findings demonstrated, for the first time in amphibians, that testicular endocrine cyclic activity could be modulated by the up‐regulation of key steroidogenic enzyme gene expressions. This in turn determines the activation of the androgenic pathway in reproductive phase and the oestrogenic one in postreproductive phase.

Seasonal expression and cellular distribution of star and steroidogenic enzymes in quail testis

“…This means that the steroidogenesis in the testis of Coturnix coturnix could occur both in somatic and germinal cells in agreement with what has already been highlighted in other animal models, as bivalvia mollusk (Prisco et al, ), amphibians (Santillo et al, ), reptiles (Rosati, Agnese, et al, ; Rosati, Andreuccetti, et al, ), and mammals (Bilińska, Schmalz‐Frączek, Kotula, & Carreau, ; Carreau et al, ). In particular, in Coturnix testis, as well as showed in Podarcis testis (Rosati, Andreuccetti, et al, ), the steroidogenic process could be quite relevant during the spermiogenesis, that is, in spermatids and testicular spermatozoa.…”

“…Mature males show synchronized cycles of testicular growth and involution between the breeding and nonbreeding periods (Bronson, ). Seasonal changes of steroidogenesis and spermatogenesis in wild animals have been reported in different species, including the amphibian Pelophylax esculentus (Burrone, Raucci, & Di Fiore, ; Santillo, Falvo, Chieffi Baccari, & Di Fiore, ; Santillo et al, ), the reptilian Podarcis sicula (Rosati, Agnese, Di Fiore, Andreuccetti, & Prisco, ; Rosati, Santillo, Di Fiore, Andreuccetti, & Prisco, ), the birds such as Junco hyemalis (Rosvall, Bergeon Burns, Jayaratna, & Ketterson, ) and Tachycineta bicolor (Bentz, Dossey, & Rosvall, ), and mammalian Japanese raccoon dog (Qiang, Murase, & Tsubota, ), American black bears (Tsubota et al, ), Japanese black bears (Komatsu, Tsubota, Yamamoto, Atoji, & Suzuki, ) and Bank vole (Kotula‐Balak et al, ).…”

“…In contrast, few investigations are available concerning gene expression and/or localization of steroid‐synthesizing enzymes in no mammalian testes. In the amphibian Pelophylax esculentus has been shown that cyclic endocrine activity in the testis could be regulated by the upregulation of the steroidogenic enzyme gene expression (Santillo et al, ). In particular, during the reproductive period, 3β‐HSD, 17β‐HSD, and 5αred mRNA levels as well as T and DHT titers are higher than those during the nonreproductive period, suggesting that the androgenic pathway is necessary for spermatogenesis activation.…”

“…In particular, during the reproductive period, 3β‐HSD, 17β‐HSD, and 5αred mRNA levels as well as T and DHT titers are higher than those during the nonreproductive period, suggesting that the androgenic pathway is necessary for spermatogenesis activation. Conversely, during the nonreproductive period, the highest P450 arom, paralleling with E2 titers, indicates that an estrogenic pathway is essential for the interruption of the reproductive processes (Santillo et al, ). In addition, in Pelophylax esculentus testis it is known that StAR, P450 arom, and 5α‐Red expression could be regulated by the d ‐Aspartate (Burrone et al, ; Di Fiore, Santillo, & Chieffi Baccari, ; Di Fiore, Santillo, Falvo, Longobardi, & Chieffi baccari, ).…”

Effects of chemical pollutants on reproductive and developmental processes in Italian amphibians

“…Most temperate amphibian species breed annually with their reproduction being controlled by both hormones and the environment (Burrone, Raucci, & Di Fiore, ; Jadhao, Pinelli, D'Aniello, & Tsutsui, ; Rastogi, Pinelli, Polese, D'Aniello, & Chieffi Baccari, ; Santillo, Burrone, Minucci, Di Giovanni, & Chieffi Baccari, ; Santillo, Falvo, Chieffi Baccari, & Di Fiore, ; Santillo, Pinelli, Burrone, Chieffi Baccari, & Di Fiore, ). For most species, reproductive and larval development periods coincide with the usage of pesticides and fertilizers in agricultural areas in the spring and summer (Rastogi et al, ).…”