The existence of kisspeptin-like peptides and effects on ovarian development and maturation in the giant freshwater prawn Macrobrachium rosenbergii

Thongbuakaew, Tipsuda; Saetan, Jirawat; Suwansa‐ard, Saowaros; Kankoun, Wilairat; Sumpownon, C.; Parhar, Ishwar S.; Meeratana, Prasert; Sobhon, Prasert; Sretarugsa, Prapee

doi:10.1016/j.aquaculture.2016.01.006

Cited by 14 publications

(3 citation statements)

References 78 publications

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“…However, there are three neuropeptides that either have been reported or suggested to be present in decapods that were not found in any of the SRAs from the seven decapod species studied here. These are a pituitary adenylate cyclase activating polypeptide (PACAP) from L. vannamei ( Lugo et al , 2013 ), a GnRH-like peptide from P. clarkii ( Guan et al , 2014 ) and two kisspeptins from M. rosenbergii ( Thongbuakaew et al , 2016 ). None of these peptides could be found in any of the SRAs, neither those from the species from which they were reported, nor from any of the other species.…”

Section: Discussionmentioning

confidence: 99%

Similarities between decapod and insect neuropeptidomes

Veenstra

2016

PeerJ

108

133

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Background. Neuropeptides are important regulators of physiological processes and behavior. Although they tend to be generally well conserved, recent results using trancriptome sequencing on decapod crustaceans give the impression of significant differences between species, raising the question whether such differences are real or artefacts.Methods. The BLAST+ program was used to find short reads coding neuropeptides and neurohormons in publicly available short read archives. Such reads were then used to find similar reads in the same archives, and the DNA assembly program Trinity was employed to construct contigs encoding the neuropeptide precursors as completely as possible.Results. The seven decapod species analyzed in this fashion, the crabs Eriocheir sinensis, Carcinus maenas and Scylla paramamosain, the shrimp Litopenaeus vannamei, the lobster Homarus americanus, the fresh water prawn Macrobrachium rosenbergii and the crayfish Procambarus clarkii had remarkably similar neuropeptidomes. Although some neuropeptide precursors could not be assembled, in many cases individual reads pertaining to the missing precursors show unambiguously that these neuropeptides are present in these species. In other cases, the tissues that express those neuropeptides were not used in the construction of the cDNA libraries. One novel neuropeptide was identified: elongated PDH (pigment dispersing hormone), a variation on PDH that has a two-amino-acid insertion in its core sequence. Hyrg is another peptide that is ubiquitously present in decapods and is likely a novel neuropeptide precursor.Discussion. Many insect species have lost one or more neuropeptide genes, but apart from elongated PDH and hyrg all other decapod neuropeptides are present in at least some insect species, and allatotropin is the only insect neuropeptide missing from decapods. This strong similarity between insect and decapod neuropeptidomes makes it possible to predict the receptors for decapod neuropeptides that have been deorphanized in insects. This includes the androgenic insulin-like peptide that seems to be homologous to drosophila insulin-like peptide 8.

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Section: Discussionmentioning

confidence: 99%

Similarities between decapod and insect neuropeptidomes

Veenstra

2016

PeerJ

108

133

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“…Nowadays, the aquaculture of this crustacean still faces many problems, including diseases and stress during captivity that result in lower fecundity and reproduction. There have been several attempts to increase the reproduction of this prawn by inducing gonad maturation, reducing the gonad development period and spawning using special formula feed (Cavalli et al, 2001 ; Takács-Vellai et al, 2005 ; Ribeiro et al, 2012 ) or through hormone injections (Tinikul et al, 2009 ; Sumpownon et al, 2015 ; Thongbuakaew et al, 2016a ) or by eye-stalk ablation (Okumura and Aida, 2001 ).…”

Section: Introductionmentioning

confidence: 99%

Starvation Promotes Autophagy-Associated Maturation of the Ovary in the Giant Freshwater Prawn, Macrobrachium rosenbergii

et al. 2017

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Limitation of food availability (starvation) is known to influence the reproductive ability of animals. Autophagy is a lysosomal driven degradation process that protects the cell under metabolic stress conditions, such as during nutrient shortage. Whether, and how starvation-induced autophagy impacts on the maturation and function of reproductive organs in animals are still open questions. In this study, we have investigated the effects of starvation on histological and cellular changes that may be associated with autophagy in the ovary of the giant freshwater prawn, Macrobachium rosenbergii. To this end, the female prawns were daily fed (controls) or unfed (starvation condition) for up to 12 days, and the ovary tissue was analyzed at different time-points. Starvation triggered ovarian maturation, and concomitantly increased the expression of autophagy markers in vitellogenic oocytes. The immunoreactivities for autophagy markers, including Beclin1, LC3-II, and Lamp1, were enhanced in the late oocytes within the mature ovaries, especially at the vitellogenic stages. These markers co-localized with vitellin in the yolk granules within the oocytes, suggesting that autophagy induced by starvation could drive vitellin utilization, thus promoting ovarian maturation.

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“…The presence of kisspeptin-like peptides and their receptors was reported in the neural tissues of M. rosenbergii by Thongbuakaew et al ( 174 ); the co-localization of Kiss-I and GnRH signals in the same neurons suggested that locally-synthesized kisspeptin plays a pivotal role in ovarian maturation and spawning by exerting autocrine and paracrine regulation on GnRH secretion from neural and ovarian tissue. Moreover, injection of exogenous kisspeptin was also shown to induce ovarian maturation and spawning in M. rosenbergii perhaps via action on GnRH or stimulation of E2 production in the ovary.…”

Section: Potential Involvement Of Other Factors (Ecdysteroids/vertebrmentioning

confidence: 69%

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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The existence of kisspeptin-like peptides and effects on ovarian development and maturation in the giant freshwater prawn Macrobrachium rosenbergii

Cited by 14 publications

References 78 publications

Similarities between decapod and insect neuropeptidomes

Similarities between decapod and insect neuropeptidomes

Starvation Promotes Autophagy-Associated Maturation of the Ovary in the Giant Freshwater Prawn, Macrobrachium rosenbergii

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

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