Serotonin induced changes in the expression of ovarian gene network in the Indian white shrimp, Penaeus indicus

Tomy, Sherly; Saikrithi, P.; James, Nithoon; Balasubramanian, C.; Panigrahi, A.; Otta, Subhendu Kumar; Subramoniam, T.; Ponniah, A. G.

doi:10.1016/j.aquaculture.2015.11.003

Cited by 33 publications

(27 citation statements)

References 46 publications

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“…In order to refine the induced maturation procedure and to manage reproduction under captivity more effectively, it is imperative to use hormones of 'gonadotropic' nature. In crustaceans, so far several hormones have been reported to have stimulating effect; for example, methyl farnesoate 13 , neurotransmitters 14 and vertebrate-type sex steroids [15][16][17] . Our recent study suggests the role of 17--estradiol and 17--hydroxyprogesterone on vitellogenesis and reproductive maturation of P. monodon 17 .…”

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confidence: 99%

Vertebrate-Type Steroid Profile in Different Tissues of Wild and Endocrinologically Manipulated Female Brood Stocks of <i>Penaeus monodon</i>

et al. 2016

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The endocrine mechanism regulating reproduction of tiger shrimp, Penaeus monodon, is a field of topical interest, which is to be addressed in detail as control of reproduction in captivity is conditional for domestication. In this study, the titres of estradiol and progesterone in hemolymph, ovary and hepatopancreas during various reproductive phases of females were quantified using ELISA. Circulating concentration of hemolymph estradiol and progesterone in the endocrinologically induced (eyestalk ablated) females was also quantified. Additionally, the evidence for estradiol and progesterone receptors was provided using immunohistochemistry. Levels of progesterone in hemolymph and ovary were highest in the vitellogenic and ripe phases (P > 0.05). Conversely, in hepatopancreas significantly higher progesterone level was detected at immature phase (184.3  2.3 pg/ml). Estradiol was highest in hemolymph (65.97  0.8 pg/ml) and ovary (58.47  0.7 pg/ml) at the early vitellogenic phase. In hepatopancreas, however, lowest level of estradiol was detected at the early vitellogenic phase (121  0.38 pg/ml). Progesterone and estradiol receptor protein signals were predominantly found in the previtellogenic oocytes. These results suggest the possible involvement of vertebrate-type steroid in the reproductive maturation of P. monodon.

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Vertebrate-Type Steroid Profile in Different Tissues of Wild and Endocrinologically Manipulated Female Brood Stocks of <i>Penaeus monodon</i>

et al. 2016

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“…MPF controls eukaryotic cell division cycles at the checkpoint from G2 to M phase, and activation of MPF leads to M phase entry and progression of oocytes to meiosis maturation; thus, Cyclin B and Cdc2 are known as possible marker genes of competence of oocyte development (Han et al., ; Kishimoto, ; Ledan, Polanski, Terret & Maro, ; Voronina, Marzluff & Wessel, ). High expression levels of Cyclin B and Cdc2 often correlated with resumption of meiosis and oocyte maturation at the final stage of ovarian maturation (Phinyo et al., ; Tomy et al., ; Visudtiphole, Klinbunga & Kirtikara, ). In the present study, Cyclin B and Cdc2 exhibited upregulated expressions after Mnnm23 RNAi treatment in comparison with those in VC (Figure d,e); these findings suggest that phosphorylation and downregulation of Cyclin B and Cdc2 by Mnnm23 were negated by Mnnm23 knockdown.…”

Section: Discussionmentioning

confidence: 99%

Molecular and functional characterization of nucleoside diphosphate kinase (nm23 ) gene in oriental river prawn Macrobrachium nipponense during ovarian development

Jiang

Sun

et al. 2018

Aquac Res

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nm23 belongs to nucleoside diphosphate kinase superfamily-a group of multifunctional regulatory proteins. In this study, Macrobrachium nipponense nm23 (Mnnm23) complementary DNA (cDNA) was isolated and characterized. Full-length cDNA of Mnnm23 measured 829 bp, with a 531 bp open reading frame encoding for 177 amino acids (aa). Specific functional sites of Mnnm23 aa sequence were highly conserved with those in other decapod crustaceans. Mnnm23 transcripts were ubiquitously distributed in various tissues. Expression level of Mnnm23 was highest in stage I ovaries and gradually decreased as ovaries developed. After Mnnm23 knockdown by RNA interference, expression levels of Cyclin B and cyclin-dependent kinase 2 in ovaries increased in comparison with that of vehicle control (VC); vitellogenin and vitellogenin receptor transcripts in ovaries and gonadosomatic indexes of prawn reached peak values in advance during ovarian cycle in comparison with VC. In histological observation, more advanced oocyte and ovarian development were observed in prawns after Mnnm23 knockdown in comparison with that of VC. These results suggest that Mnnm23 is involved in ovarian development in M. nipponense and possibly functions in hindering rapid oocyte and ovarian maturation of this prawn species.

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“…It is ubiquitously found in several microorganisms, and throughout the plant and animal world in significant amounts; it functions as a neurotransmitter in the brain and as a neurohormone in the periphery, regulating several important physiological functions both in vertebrates and invertebrates. In invertebrates, serotonin modulates multiple functions including circadian rhythms ( 39 ), neurogenesis ( 40 ), osmotic adjustment ( 41 ), growth ( 42 ), aggression ( 43 ), molting ( 44 ), and reproduction ( 27 ). Several reports have correlated the role of serotonin in the regulation of growth and reproductive development of vertebrates, rather than focusing on invertebrates.…”

Section: Serotoninmentioning

confidence: 99%

“…Emerging evidence suggests serotonin to be the upstream neurotransmitter controlling reproduction by acting at the eyestalks and the central nervous system in crustaceans ( 7 , 30 , 46 , 47 ). Serotonergic neuromodulation of reproductive function resulted in a significant increase in oocyte diameter and enhanced ovarian maturation in P. indicus ( 27 , 48 ), Litopenaeus vannamei ( 49 ), Penaeus monodon ( 50 ), Fenneropenaeus merguiensis ( 51 ), Macrobrachium rosenbergii ( 46 , 52 ), and Procambarus clarkii ( 53 ). Injection of serotonin to the giant freshwater prawn M. rosenbergii , shortened the normal duration required for ovarian maturation in females and brought about a significant increase in the testis-somatic index in males ( 54 ).…”

Section: Serotoninmentioning

confidence: 99%

“…The endocrine pathway where serotonin is considered to stimulate downstream reproductive hormones is hypothesized to be performed mainly by the action of serotonin at the eyestalk and/or the central nervous system level. In more detail, serotonin may function to regulate the synthesis and release of endocrine factors such as VSH and/or VIH, or may also act upon red pigment-concentrating hormone (RPCH) to serve as an intermediary substance, causing its release from eyestalk neural tissue, which may, in turn, stimulate the release of the putative VSH ( 27 , 38 , 46 , 47 ). A faster response in ovarian maturation observed in ablated females of P. indicus and F. merguiensis treated with serotonin suggests that lowering levels of inhibitory hormones is an essential prerequisite for serotonin to effectively induce maturation ( 27 , 62 ).…”

Section: Serotoninmentioning

confidence: 99%

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

2020

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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.

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Serotonin induced changes in the expression of ovarian gene network in the Indian white shrimp, Penaeus indicus

Cited by 33 publications

References 46 publications

Vertebrate-Type Steroid Profile in Different Tissues of Wild and Endocrinologically Manipulated Female Brood Stocks of <i>Penaeus monodon</i>

Vertebrate-Type Steroid Profile in Different Tissues of Wild and Endocrinologically Manipulated Female Brood Stocks of <i>Penaeus monodon</i>

Molecular and functional characterization of nucleoside diphosphate kinase (nm23 ) gene in oriental river prawn Macrobrachium nipponense during ovarian development

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

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