Differential response patterns of kisspeptin and RFamide‐related peptide to photoperiod and sex steroid feedback in the Djungarian hamster (Phodopus sungorus)

Abstract

Many animals synchronise their reproductive activity with the seasons to optimise the survival of their offspring. This synchronisation involves switching on and off their gonadotrophic axis. Ever since their discovery as key regulators of gonadotrophin-releasing hormone (GnRH) neurones, the hypothalamic RF-amide peptides kisspeptin and RFamide-related peptide (RFRP) have been a major focus of research on the seasonal regulation of the gonadotrophic axis. In the present study, we investigated the regulation of both neuropeptides in the Djungarian hamster, a major animal model for the study of seasonal reproduction. During the long-day breeding period, kisspeptin neurones in the anteroventral periventricular area are solely controlled by a positive sex steroid feedback and, in the arcuate nucleus, they are subject to a very strong negative sex steroid feedback associated with a minor photoperiodic effect. During short-day sexual quiescence, the disappearance of this hormonal feedback leads to high levels of kisspeptin in arcuate neurones. Notably, chronic central administration of kisspeptin is able to over-ride the photoperiodic inhibition of the gonadotrophic axis and reactivate the reproductive function. Therefore, our data suggest that kisspeptin secretion by arcuate neurones during sexual quiescence is inhibited by mechanisms upstream of kisspeptin neurones. RFRP expression is solely controlled by photoperiod, being strongly reduced in short days independently of the sex steroid feedback. Thus, kisspeptin and RFRP display contrasting patterns of expression and regulation. Upstream mechanisms controlling these neurones should be the focus of further studies on the roles of these RFamide neuropeptides in the seasonal control of reproduction.

Dynamic expressions of hypothalamic genes regulate seasonal breeding in a natural rodent population

“…Prominent kp neurons locate in the Arc nucleus of male mice, rats and hamsters (Kauffman et al, ; Revel et al, ; Smith et al, ); our data which sampled the entire hypothalamus likely represented the changes in Kiss‐1 mainly from the Arc nucleus in voles. One explanation of stable Kiss‐1 expression from summer to autumn is that SP decreased testosterone levels and weakened its negative feedback on Kiss‐1 neurons in the Arc (Ansel et al, ; Rasri‐Klosen et al, ; Sáenz de Miera et al, ; Smith et al, ). Because limitation of food availability can suppress Kiss‐1 expression in rat and mouse, our second explanation is that more abundant food availability from summer to autumn possibly helped maintain the high expression of Kiss‐1 for metabolic processes rather than reproductive processes (Castellano et al, ; Luque, Kineman, & Tena‐Sempere, ).…”

“…The Kiss‐1 expression in the Arc is regulated by both melatonin and testosterone feedback, depending on which force is stronger, and thus, the photoperiodic response varied among species. Kiss‐1 in the AVPV is upregulated by testosterone, but not affected by melatonin in both male Syrian and Siberian hamsters (Ansel et al, ; Rasri‐Klosen, Simonneaux, & Klosen, ). Rfrp‐3 is always inhibited by SP exposure and melatonin (Rasri‐Klosen et al, ; Revel, Saboureau, Pevet, Simonneaux, & Mikkelsen, ; Ubuka et al, ).…”

“…Kiss‐1 in the AVPV is upregulated by testosterone, but not affected by melatonin in both male Syrian and Siberian hamsters (Ansel et al, ; Rasri‐Klosen, Simonneaux, & Klosen, ). Rfrp‐3 is always inhibited by SP exposure and melatonin (Rasri‐Klosen et al, ; Revel, Saboureau, Pevet, Simonneaux, & Mikkelsen, ; Ubuka et al, ). Administration of exogenous T 3 or TSH reverses the expression of both genes from the SP to LP response pattern in hamsters (Henson, Carter, & Freeman, ; Klosen et al, ).…”

An integrative view of mammalian seasonal neuroendocrinology

“…Kiss1 and Npvf display large opposite seasonal variation in expression, modulated in a sex and species‐specific manner. Although Kiss1 expression is generally, but not always, higher in the breeding season, there is a conserved down‐regulation of Npvf expression in short days, in all long‐ and short‐day breeders studied . The role of these neuropeptides in seasonal breeding has been extensively reviewed over the last years …”

“…The sex steroid sensitivity of Npvf ‐expressing neurones has comparatively received little attention and available data are discordant . However, gonadectomy does not appear to affect Npvf expression in Syrian, Siberian or European hamsters, although it affects the expression of Kiss1 . This suggests that Npvf ‐expressing neurones are not bona fide targets of sex steroids and also weakens the hypothesis that the two subpopulations are synaptically connected, at least in hamsters.…”