Central pathways integrating metabolism and reproduction in teleosts

Abstract

Energy balance plays an important role in the control of reproduction. However, the cellular and molecular mechanisms connecting the two systems are not well understood especially in teleosts. The hypothalamus plays a crucial role in the regulation of both energy balance and reproduction, and contains a number of neuropeptides, including gonadotropin-releasing hormone (GnRH), orexin, neuropeptide-Y, ghrelin, pituitary adenylate cyclase-activating polypeptide, α-melanocyte stimulating hormone, melanin-concentrating hormone, cholecystokinin, 26RFamide, nesfatin, kisspeptin, and gonadotropin-inhibitory hormone. These neuropeptides are involved in the control of energy balance and reproduction either directly or indirectly. On the other hand, synthesis and release of these hypothalamic neuropeptides are regulated by metabolic signals from the gut and the adipose tissue. Furthermore, neurons producing these neuropeptides interact with each other, providing neuronal basis of the link between energy balance and reproduction. This review summarizes the advances made in our understanding of the physiological roles of the hypothalamic neuropeptides in energy balance and reproduction in teleosts, and discusses how they interact with GnRH, kisspeptin, and pituitary gonadotropins to control reproduction in teleosts.

Keywords: energy balance; fish; metabolism; neuropeptide; reproduction.

Figure 1

Effects of central and peripheral metabolic hormones on the reproductive system. The hypothalamus–pituitary axis receives many stimulatory and inhibitory inputs from central metabolic neuropeptide neurons and peripheral metabolic signals to control the reproductive system according to the energy status. The hormones indicated with blue circles are orexigenic hormones, while those with orange squares are anorexigenic ones. Red lines indicate stimulatory action and blue lines indicate inhibitory action. Most anorexigenic hormones stimulate gonadotropin secretion at the pituitary level. In the goldfish, NPY and ghrelin, which act as orexigenic hormones, also stimulate the reproductive system at the brain and pituitary levels. It should be noted that this figure is drew primarily based on the information obtained from the goldfish. Function of each metabolic hormone might differ in different species [e.g., Ghrelin functions as an anorexigenic factor in the rainbow trout (147) and GnIH stimulates GTH subunit mRNA expression in the puffer fish (97) and the sockeye salmon (92).]. CCK, cholecystokinin; GnIH, gonadotropin-inhibitory hormone; GnRH, gonadotropin-releasing hormone; MCH, melanin-concentrating hormone; NPY, neuropeptide-Y; PACAP, pituitary adenylate cyclase-activating polypeptide.

Figure 2

Interaction between the orexigenic circuit and anorexigenic circuit and among neurons in each circuit in the goldfish. Hormones in the orexigenic circuit are shown in blue and those in the anorexigenic circuit are shown in orange. The orexigenic and anorexigenic circuits are connected each other via inhibitory neuronal fiber projections to form an on-off switch. Reciprocal interaction is observed especially between neurons in the orexigenic circuit. Arrows with dotted lines indicate the interactions that have not been confirmed whether direct or indirect. The complex interaction among metabolic neuropeptides suggests that a change in one metabolic signal can affect the reproductive system through the action via other metabolic neuropeptides. Note that in the goldfish ghrelin secreted in the brain also function as an orexigenic signal. α-MSH, alpha-melanocyte stimulating hormone; CRH, corticotropin-releasing hormone; GAL, galanin; GnRH, gonadotropin-releasing hormone; MCH, melanin-concentrating hormone; NPY, neuropeptide-Y; OXA, orexin A; PACAP, pituitary adenylate cyclase-activating polypeptide.