Insights on Molecular Mechanisms of Ovarian Development in Decapod Crustacea: Focus on Vitellogenesis-Stimulating Factors and Pathways

Abstract

Vitellogenesis in crustaceans is an energy-consuming process. Though the underlying mechanisms of ovarian maturation in decapod Crustacea are still unclear, evidence indicates the process to be regulated by antagonistically-acting inhibitory and stimulating factors specifically originating from X-organ/sinus gland (XO/SG) complex. Among the reported neuromediators, neuropeptides belonging to the crustacean hyperglycemic hormone (CHH)-family have been studied extensively. The structure and dynamics of inhibitory action of vitellogenesis-inhibiting hormone (VIH) on vitellogenesis have been demonstrated in several species. Similarly, the stimulatory effects of other neuropeptides of the CHH-family on crustacean vitellogenesis have also been validated. Advancement in transcriptomic sequencing and comparative genome analysis has led to the discovery of a large number of neuromediators, peptides, and putative peptide receptors having pleiotropic and novel functions in decapod reproduction. Furthermore, differing research strategies have indicated that neurotransmitters and steroid hormones play an integrative role by stimulating neuropeptide secretion, thus demonstrating the complex intertwining of regulatory factors in reproduction. However, the molecular mechanisms by which the combinatorial effect of eyestalk hormones, neuromediators and other factors coordinate to regulate ovarian maturation remain elusive. These multifunctional substances are speculated to control ovarian maturation possibly via the autocrine/paracrine pathway by acting directly on the gonads or by indirectly exerting their stimulatory effects by triggering the release of a putative gonad stimulating factor from the thoracic ganglion. Acting through receptors, they possibly affect levels of cyclic nucleotides (cAMP and cGMP) and Ca 2+ in target tissues leading to the regulation of vitellogenesis. The “stimulatory paradox” effect of eyestalk ablation on ovarian maturation continues to be exploited in commercial aquaculture operations, and is outweighed by the detrimental physiological effects of this procedure. In this regard, the development of efficient alternatives to eyestalk ablation based on scientific knowledge is a necessity. In this article, we focus principally on the signaling pathways of positive neuromediators and other factors regulating crustacean reproduction, providing an overview of their proposed receptor-mediated stimulatory mechanisms, intracellular signaling, and probable interaction with other hormonal signals. Finally, we provide insight into future research directions on crustacean reproduction as well as potential applications of such research to aquaculture technology development.

Signaling Pathways That Regulate the Crustacean Molting Gland

“…Much of the research of biogenic amines functioning as neurohormones has been focused on their roles in regulating decapod reproduction. For example, serotonin stimulates ovarian maturation, whereas octopamine delays gonadal development and inhibits ovarian maturation (93)(94)(95). Serotonin stimulates YO ecdysteroid production in vitro in mud crab (Scylla serrata) (96).…”

Identification of Low Molecular Weight Proteins and Peptides from Schistosoma mekongi Worm, Egg and Infected Mouse Sera

“…Eleven precursor sequences of S. mekongi arthropod CHH/MIH/GIH/VIH hormone peptides were detected using the transcriptome mining approach. In crustaceans, the crustacean hyperglycemic hormone (CHH)-family, vitellogenesis-inhibiting hormone (VIH), also known as gonad-inhibiting hormone (GIH), play roles in vitellogenesis [ 39 ]. Moreover, MIH is a key endocrine regulator that regulates Callinectes sapidus molting and reproduction [ 40 ].…”

Suppression of a Novel Vitellogenesis-Inhibiting Hormone Significantly Increases Ovarian Vitellogenesis in the Black Tiger Shrimp, Penaeus monodon

“…Moreover, the putative surface representations of PemVIH and PemGIH showed certain similar surface area properties (see Supplement 3 ), suggesting they interact with very similar receptors. It has been shown that CHH peptide hormones commonly bind with G protein-coupled receptors (GPCRs) on target cells ( 43 , 44 ). In L. vannamei and C. sapidus , LivMIH2 and CasMIH have been shown to regulate vitellogenesis in addition to their role in ecdysis ( 28 , 37 ).…”