Testicular Steroidogenesis and Locomotor Activity Are Regulated by Gonadotropin-Inhibitory Hormone in Male European Sea Bass

Abstract

Gonadotropin-inhibitory hormone (GnIH) is a neurohormone that suppresses reproduction by acting at both the brain and pituitary levels. In addition to the brain, GnIH may also be produced in gonads and can regulate steroidogenesis and gametogenesis. However, the function of GnIH in gonadal physiology has received little attention in fish. The main objective of this study was to evaluate the effects of peripheral sbGnih-1 and sbGnih-2 implants on gonadal development and steroidogenesis during the reproductive cycle of male sea bass (Dicentrarchus labrax). Both Gnihs decreased testosterone (T) and 11-ketotestosterone (11-KT) plasma levels in November and December (early- and mid-spermatogenesis) but did not affect plasma levels of the progestin 17,20β-dihydroxy-4-pregnen-3-one (DHP). In February (spermiation), fish treated with sbGnih-1 and sbGnih-2 exhibited testicles with abundant type A spermatogonia and partial spermatogenesis. In addition, we determined the effects of peripheral Gnih implants on plasma follicle-stimulating hormone (Fsh) and luteinizing hormone (Lh) levels, as well as on brain and pituitary expression of the main reproductive hormone genes and their receptors during the spermiation period (February). Treatment with sbGnih-2 increased brain gnrh2, gnih, kiss1r and gnihr transcript levels. Whereas, both Gnihs decreased lhbeta expression and plasma Lh levels, and sbGnih-1 reduced plasmatic Fsh. Finally, through behavioral recording we showed that Gnih implanted animals exhibited a significant increase in diurnal activity from late spermatogenic to early spermiogenic stages. Our results indicate that Gnih may regulate the reproductive axis of sea bass acting not only on brain and pituitary hormones but also on gonadal physiology and behavior.

Gonadotropin‐inhibitory hormone in the flatfish, Solea senegalensis: Molecular cloning, brain localization and physiological effects

“…Abundant studies have reported the inhibitory role of GnIH on GnRH and gonadotropin synthesis and release in birds and mammals (Tsutsui et al, ; Kriegsfeld et al, ; Clarke et al, ) but results in fish are contradictory depending on the sex, the species, the administered peptide, and the physiological stage of the animals (Amano et al, ; Zhang et al, ; Moussavi et al ; Qi et al, ; Biran et al, ; Wang et al, ; Di Yorio et al, ; Paullada‐Salmerón et al, ,). In our study, in vivo treatment of adult sole with ssGnih‐2 did not affect gene expression of the main reproductive hormones, but treatment with ssGnih‐3 provoked a significant reduction in gnrh‐3 and lh transcript levels.…”

“…Similar results were obtained in goldfish, where Gnih‐3 treatment reduced gnrh‐3 transcript levels at 12 hr post‐injection (Qi et al, ). In contrast, Gnih‐3 injection in orange‐spotted grouper stimulated Gnrh‐3 transcription (Wang et al, ) and in sea bass, which only exhibits two putative Gnih peptides, neither Gnih‐1 nor Gnih‐2 affected gnrh‐3 expression (Paullada‐Salmerón et al, 2016b, c). These results would indicate differential responses depending on the species and/or the developmental stage of the fish.…”

“…These results would indicate differential responses depending on the species and/or the developmental stage of the fish. Interestingly, a study performed in sea bass showed that centrally administered Gnih‐1 and Gnih‐2 inhibit Gnrh‐1 and Gnrh‐2 expression, respectively (Paullada‐Salmerón et al, ), while peripherally administered Gnih‐2 stimulated Gnrh‐2 transcript levels (Paullada‐Salmerón et al, ). This evidence suggests that Gnih actions on the different Gnrh forms could depend, not only on the species, but also on the route of administration.…”

“…Before treatment, anesthetized animals were measured, weighed and tagged. The protocol of injection was based on previous information available in fish Gnih studies (Zhang et al, ; Moussavi et al ; Paullada‐Salmerón et al, ). As the size of Gnih‐1 peptide was variable between species, and this peptide appeared to be ineffective in other studies performed in fish, we decided to focus on ssGnih‐2 and ssGnih‐3, which were revealed much more effective in this group of vertebrates.…”

“…These reproductive dysfunctions include inhibition of oocyte maturation and spawning in females, inhibition of spermatogenesis and spermiation in males, inhibition of reproductive behavior and consequently, the absence of fertilized spawning from cultured broodstock (Mañanós, Duncan, & Mylonas, ). Interestingly, recent studies in sea bass showed that Gnih inhibited testicular steroidogenesis, determined marked effects on the progression of gametogenesis and also affected sea bass behavior (Paullada‐Salmerón et al, ). The existence of an inhibitory system over the reproductive axis such as Gnih, potentially involved in the regulation of reproductive, locomotor and behavioral processes, could therefore be underlying the reproductive dysfunctions observed in sole.…”