Neuropeptide F stimulates ovarian development and spawning in the female giant freshwater prawn, Macrobrachium rosenbergii, and its expression in the ovary during ovarian maturation cycle

Tinikul, Yotsawan; Engsusophon, Attakorn; Kruangkum, Thanapong; Thongrod, Sirorat; Tinikul, Ruchanok; Sobhon, Prasert

doi:10.1016/j.aquaculture.2016.11.026

Cited by 25 publications

(17 citation statements)

References 42 publications

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“…In contrast, the contig N13763 shows higher similarity with the NPY receptor. Interestingly, the existence of NPY/F in crustacean species has been reported in some transcriptome analyses ( 43 – 49 , 51 , 52 ), and NPF has been suggested to stimulate ovarian development in M. rosenbergii ( 80 ). Therefore, NPF may have a similar function in M. japonicus .…”

Section: Discussionmentioning

confidence: 96%

Transcriptomic Analysis of the Kuruma Prawn Marsupenaeus japonicus Reveals Possible Peripheral Regulation of the Ovary

et al. 2020

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Crustacean reproduction has been hypothesized to be under complex endocrinological regulation by peptide hormones. To further improve our understanding of the mechanisms underlying this complex regulation, knowledge is needed regarding the hormones not only of the central nervous system (CNS) such as the X-organ/sinus gland (XOSG), brain, and thoracic ganglia, but also the peripheral gonadal tissues. For example, in vertebrates, some gonadal peptide hormones including activin, inhibin, follistatin, and relaxin are known to be involved in the reproductive physiology. Therefore, it is highly likely that some peptide factors from the ovary are serving as the signals among peripheral tissues and central nervous tissues in crustaceans. In this work, we sought to find gonadal peptide hormones and peptide hormone receptors by analyzing the transcriptome of the ovary of the kuruma prawn Marsupenaeus japonicus. The generated ovarian transcriptome data led to the identification of five possible peptide hormones, including bursicon-α and-β, the crustacean hyperglycemic hormone (CHH)-like peptide, insulin-like peptide (ILP), and neuroparsin-like peptide (NPLP). Dominant gene expressions for the bursicons were observed in the thoracic ganglia and the ovary, in the CNS for the CHH-like peptide, in the heart for NPLP, and in the ovary for ILP. Since the gene expressions of CHH-like peptide and NPLP were affected by a CHH (Penaeus japonicus sinus gland peptide-I) from XOSG, we produced recombinant peptides for CHH-like peptide and NPLP using Escherichia coli expression system to examine their possible peripheral regulation. As a result, we found that the recombinant NPLP increased vitellogenin gene expression in incubated ovarian tissue fragments. Moreover, contigs encoding putative receptors for insulin-like androgenic gland factor, insulin, neuroparsin, and neuropeptide Y/F, as well as several contigs encoding orphan G-protein coupled receptors and receptor-type guanylyl cyclases were also identified in the ovarian transcriptome. These results suggest that reproductive physiology in crustaceans is regulated by various gonadal peptide hormones, akin to vertebrates.

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Section: Discussionmentioning

confidence: 96%

Transcriptomic Analysis of the Kuruma Prawn Marsupenaeus japonicus Reveals Possible Peripheral Regulation of the Ovary

et al. 2020

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“…To add to the complexity of clearly defining crustacean neuropeptides, many neuropeptides are pleiotropic and novel functions are being described for previously characterized neuropeptides. Recent studies have found that several neuropeptides are now also involved in crustacean reproduction, including the red pigment concentrating hormone (RPCH) ( 32 ), neuroparsin ( 33 ), neuropeptide F ( 34 ), and pigment-dispersing hormone (PDH) ( 35 ). Moreover, the roles of the vast majority of neuropeptides identified in crustaceans have not been clarified yet, highlighting the gap in crustacean neuropeptide research, including those related to reproduction and sexual maturation.…”

Section: Introductionmentioning

confidence: 99%

Insights Into Sexual Maturation and Reproduction in the Norway Lobster (Nephrops norvegicus) via in silico Prediction and Characterization of Neuropeptides and G Protein-coupled Receptors

et al. 2018

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Multiple biological processes across development and reproduction are modulated by neuropeptides that are predominantly produced and secreted from an animal's central nervous system. In the past few years, advancement of next-generation sequencing technologies has enabled large-scale prediction of putative neuropeptide genes in multiple non-model species, including commercially important decapod crustaceans. In contrast, knowledge of the G protein-coupled receptors (GPCRs), through which neuropeptides act on target cells, is still very limited. In the current study, we have used in silico transcriptome analysis to elucidate genes encoding neuropeptides and GPCRs in the Norway lobster (Nephrops norvegicus), which is one of the most valuable crustaceans in Europe. Fifty-seven neuropeptide precursor-encoding transcripts were detected, including phoenixin, a vertebrate neurohormone that has not been detected in any invertebrate species prior to this study. Neuropeptide gene expression analysis of immature and mature female N. norvegicus, revealed that some reproduction-related neuropeptides are almost exclusively expressed in immature females. In addition, a total of 223 GPCR-encoding transcripts were identified, of which 116 encode GPCR-A (Rhodopsin), 44 encode GPCR-B (Secretin) and 63 encode other GPCRs. Our findings increase the molecular toolbox of neural signaling components in N. norvegicus, allowing for further advances in the fisheries/larvae culture of this species.

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“…In crustaceans, feeding with NPF-I-laced pellets increased the growth rate in juvenile L. vannamei ( Christie et al, 2011 ). In addition, the female giant freshwater prawns, M. rosenbergii , injected with various concentrations of NPF showed increasing GSI and shortening of the ovarian maturation cycle ( Tinikul et al, 2017 ). Strikingly, the effects of NPF on the stimulation of ovarian maturation resemble those of starvation that we reported in M. rosenbergii ( Kankuan et al, 2017 ).…”

Section: Discussionmentioning

confidence: 99%

“…Recently, by transcriptomic analysis we identified three isoforms of NPF (MrNPF-I, II, III) and four isoforms of sNPF (sMrNPF) in the central nervous system (CNS) and the ovary of the female giant freshwater prawn Macrobrachium rosenbergii ( Suwansa-Ard et al, 2015 ). More recently, we demonstrated that MrNPF-I expressed in the ovaries of M. rosenbergii could stimulate ovarian maturation by shortening the ovarian cycle ( Tinikul et al, 2017 ). While NPF is known to promote food intake and organ growth, it is unknown how NPF affects tissue homeostasis under fasting conditions.…”

Section: Introductionmentioning

confidence: 99%

Autophagy-Associated Shrinkage of the Hepatopancreas in Fasting Male Macrobrachium rosenbergii Is Rescued by Neuropeptide F

et al. 2018

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Invertebrate neuropeptide F-I (NPF-I), much alike its mammalian homolog neuropeptide Y, influences several physiological processes, including circadian rhythms, cortical excitability, stress response, and food intake behavior. Given the role of autophagy in the metabolic stress response, we investigated the effect of NPF-1 on autophagy during fasting and feeding conditions in the hepatopancreas and muscle tissues of the male giant freshwater prawn Macrobrachium rosenbergii. Starvation up-regulated the expression of the autophagy marker LC3 in both tissues. Yet, based on the relative levels of the autophagosome-associated LC3-II isoform and of its precursor LC3-I, the hepatopancreas was more responsive than the muscle to starvation-induced autophagy. Injection of NPF-I inhibited the autophagosome formation in the hepatopancreas of fasting prawns. Relative to the body weight, the muscle weight was not affected, while that of the hepatopancreas decreased upon starvation and NPF-1 treatment could largely prevent such weight loss. Thus, the hepatopancreas is the reserve organ for the nutrient homeostasis during starvation and NPF-I plays a crucial role in the balancing of energy expenditure and energy intake during starvation by modulating autophagy.

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Neuropeptide F stimulates ovarian development and spawning in the female giant freshwater prawn, Macrobrachium rosenbergii, and its expression in the ovary during ovarian maturation cycle

Cited by 25 publications

References 42 publications

Transcriptomic Analysis of the Kuruma Prawn Marsupenaeus japonicus Reveals Possible Peripheral Regulation of the Ovary

Transcriptomic Analysis of the Kuruma Prawn Marsupenaeus japonicus Reveals Possible Peripheral Regulation of the Ovary

Insights Into Sexual Maturation and Reproduction in the Norway Lobster (Nephrops norvegicus) via in silico Prediction and Characterization of Neuropeptides and G Protein-coupled Receptors

Autophagy-Associated Shrinkage of the Hepatopancreas in Fasting Male Macrobrachium rosenbergii Is Rescued by Neuropeptide F

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