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

Abstract

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.

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

“…To monitor autophagy, we followed the generation and accumulation of LC3, the hallmark of autophagosomes and autolysosomes ( Klionsky et al, 2016 ). The cross-reactivity and specificity of the anti-human LC3B toward the prawn LC3 have been previously tested ( Kankuan et al, 2017 ). The antibody recognizes both the cytosolic precursor (isoform LC3-I) and the vacuolar-associated mature isoform (LC3-II).…”

“…The autophagy machinery is ubiquitous in all living species, and it has been recently well characterized at genome level in crustaceans as well ( Suwansa-Ard et al, 2016 ). We have recently described the autophagy response to starvation in the ovary of the female giant freshwater prawn M. rosenbergii ( Kankuan et al, 2017 ). Interestingly, in this metabolic condition autophagy upregulation paralleled the development and maturation of the oocytes ( Suwansa-Ard et al, 2016 ; Kankuan et al, 2017 ).…”

“…We have recently described the autophagy response to starvation in the ovary of the female giant freshwater prawn M. rosenbergii ( Kankuan et al, 2017 ). Interestingly, in this metabolic condition autophagy upregulation paralleled the development and maturation of the oocytes ( Suwansa-Ard et al, 2016 ; Kankuan et al, 2017 ). Autophagy process is the mechanism for cell recovery in response to a variety of stresses, particularly in response to nutrient depletion (starvation) and caloric restriction ( Kroemer et al, 2010 ; Ferraresi et al, 2017 ).…”

“…Recently, our group reported the presence of several autophagy gene mRNAs in the transcriptome and the expression of the corresponding proteins in various tissues of the giant freshwater prawn M. rosenbergii ( Suwansa-Ard et al, 2016 ). More recently, we showed that starvation could induce oocyte maturation in association with up-regulation of autophagy markers in the ovary tissue of the female prawns ( Kankuan et al, 2017 ). Here, we investigated the effect of NPF on the modulation of autophagy in the hepatopancreas and muscle of the male giant freshwater prawn M. rosenbergii under feeding and starving conditions.…”

Reproductive and growth performances in female giant freshwater prawn following inhibition of gonadal maturation using dopamine and medroxyprogesterone hormone

“…The control treatment presented bigger oocyte in the vitellogenic phase and ovarium was full of matured oocyte. The particular character was considered as matured individual (Soonklang et al, 2012;Kankuan et al, 2017).…”