Abstract
Red pigment concentrating hormone (RPCH) and pigment dispersing hormone (PDH) are crustacean neuropeptides involved in broad physiological processes including body color changes, circadian rhythm, and ovarian growth. In this study, the full-length cDNA of RPCH and PDH were identified from the brain of the Chinese mitten crab Eriocheir sinensis. The deduced RPCH and PDH mature peptides shared identical sequence to the adipokinetic hormone/RPCH peptides family and the β-PDH isoforms and were designated as Es-RPCH and Es-β-PDH, respectively. Es-RPCH and Es-β-PDH transcripts were distributed in the brain and eyestalks. The positive signals of Es-RPCH and Es-β-PDH were localized in the neuronal clusters 6, 8, 9, 10, and 17 of the brain as revealed by in situ hybridization. The expression level of Es-RPCH and Es-β-PDH mRNA in nervous tissues were all significantly increased at vitellogenic stage, and then decreased at the final meiotic maturation stage. The administrated with synthesized Es-RPCH peptide results in germinal vesicles shift toward the plasma membrane in vitellogenic oocyte, and significant decrease of the gonad-somatic index (GSI) and mean oocyte diameter as well as the expression of vitellogenin mRNA at 30 days post injection in vivo. Similar results were also found when injection of the Es-β-PDH peptide. In vitro culture demonstrated that Es-RPCH and Es-β-PDH induced germinal vesicle breakdown of the late vitellogenic oocytes. Comparative ovarian transcriptome analysis indicated that some reproduction/meiosis-related genes such as cdc2 kinase, cyclin B, 5-HT-R and retinoid-X receptor were significantly upregulated in response to Es-RPCH and Es-β-PDH treatments. Taken together, these results provided the evidence for the inductive effect of Es-RPCH and Es-β-PDH on the oocyte meiotic maturation in E. sinensis.
Highlights
In most animals, ovarian maturation contains two major cellular events: vitellogenesis and the final meiotic maturation of oocytes, which were precisely regulated by elaborate endocrine system [1,2,3]
Phylogenetic analysis showed that Es-Red pigment concentrating hormone (RPCH) is more closely related to crustacean RPCHs and clustered with insects adipokinetic hormone (AKH), grouped into one GnRH superfamily, which is consistent with traditional classification (Figure S2A)
Phylogenetic analysis showed that Es-b-pigment dispersing hormone (PDH) is more closely related to crustacean b-PDHs than a-PDH, followed by pigment dispersing factor, which is consistent with traditional classification (Figure S2B)
Summary
Ovarian maturation contains two major cellular events: vitellogenesis and the final meiotic maturation of oocytes, which were precisely regulated by elaborate endocrine system [1,2,3]. Crustacean neuropeptides are important neuroendocrine factors generally synthesized and secreted from the central nerve system (CNS) such as the brain and the X-organ/sinus gland complex in eyestalks, transported to the target tissue through hemolymph to govern a variety of critical physiological processes including metabolism, molting, growth, and reproduction [4,5,6,7]. Many crustacean neuropeptides have attracted wide attention in the regulation of ovarian development [1, 4, 8]. The neuropeptide F inhibits vitellogenesis and oocyte maturation in the mud crab Scylla paramamosain [5]. Vitellogenesisinhibiting hormone (VIH) suppresses vitellogenin production directly in the target tissues and inhibits the ovarian maturation in the white shrimp Litopenaeus vannamei [10]. The removal of eyestalk has become an alternative method for promoting the ovarian maturation in the artificial reproduction of decapod crustaceans [11]
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