Insights into the Prostanoid Pathway in the Ovary Development of the Penaeid Shrimp Penaeus monodon

Abstract

The prostanoid pathway converts polyunsaturated fatty acids (PUFAs) into bioactive lipid mediators, including prostaglandins, thromboxanes and prostacyclins, all of which play vital roles in the immune and reproductive systems in most animal phyla. In crustaceans, PUFAs and prostaglandins have been detected and often associated with female reproductive maturation. However, the presence of prostanoid biosynthesis genes remained in question in these species. In this study, we outlined the prostanoid pathway in the black tiger shrimp Penaeus monodon based on the amplification of nine prostanoid biosynthesis genes: cytosolic phospholipase A2, hematopoietic prostaglandin D synthase, glutathione-dependent prostaglandin D synthase, prostaglandin E synthase 1, prostaglandin E synthase 2, prostaglandin E synthase 3, prostaglandin F synthase, thromboxane A synthase and cyclooxygenase. TBLASTX analysis confirmed the identities of these genes with 51-99% sequence identities to their closest homologs. In addition, prostaglandin F2α (PGF2α), which is a product of the prostaglandin F synthase enzyme, was detected for the first time in P. monodon ovaries along with the previously identified PUFAs and prostaglandin E2 (PGE2) using RP-HPLC and mass-spectrometry. The prostaglandin synthase activity was also observed in shrimp ovary homogenates using in vitro activity assay. When prostaglandin biosynthesis was examined in different stages of shrimp ovaries, we found that the amounts of prostaglandin F synthase gene transcripts and PGF2α decreased as the ovaries matured. These findings not only indicate the presence of a functional prostanoid pathway in penaeid shrimp, but also suggest a possible role of the PGF2α biosynthesis in shrimp ovarian development.

Improving the Reproductive Performance of Domesticated Giant Tiger Shrimp, Penaeus monodon

“…Significant up-regulation of PmCOX, PmPGFS, and PmPGES1 gene expression was observed in the HIGH group, whilst PmPGES3 was significantly up-regulated in the LOW group. The up-regulation of PmPGFS in the HIGH group is noteworthy, given its role in regulating the onset of maturation and the previously demonstrated reduction in PmPGFS gene expression in ovaries mature (Wimuttisuk et al, 2013). Within P. monodon ovaries, oocytes migrate radially away from the site of proliferation and therefore it is possible for oogonia, primary oocytes and mature oocytes to be present simultaneously within mature ovaries (Tanfermin and Pudadera, 1989).…”

“…Prostanoids derived from ARA (i.e. series II prostaglandin) have significant roles in the onset of maturation, stimulation and sequestration of egg yolk and development of essential cellular machinery such as cortical rods in P. monodon (Wouters et al, 2001a, Meunpol et al, 2010, Wimuttisuk et al, 2013. It has previously been reported that the ARA:EPA ratio in mature ovaries of wild P. monodon range from 0.3-0.6 (Crocos, 1997, Marsden et al, 1991, D'Souza and Kelly, 2000, Wouters et al, 2001a, Huang et al, 2008, whilst the diet used by Coman et al (2011) contained a ARA:EPA ratio of 0.5 and resulted in a ratio of 0.57 in spawned eggs.…”

“…Interestingly, Wouters (2001a) noted that compound diets contain relative low levels of both ARA and EPA when compared with fresh-frozen feeds, and therefore may require further investigation in relation to spawning. The requirement for ARA is of particular interest given ARA serves as the primary substrate for the synthesis of series II prostaglandins, hormones with significant regulatory control over maturation and oocyte development in P. monodon (Wimuttisuk et al, 2013).…”

“…The prostanoid pathway is characterized by the release of cellular/ intracellular membrane bound ARA by phospholipase A2 (cPLA2), which is subsequently cyclized and reduced to prostaglandin H2 (PGH2) by the cyclooxygenase (COX) (see Figure 7) (Stanley, 2006, Funk, 2001. Class specific synthases then convert PGH2 to various prostaglandins, such as prostaglandin E2 (PGE2), prostaglandin D2 (PGD2) and prostaglandin F2α (PGF2α) (Wimuttisuk et al, 2013). In crustaceans the presence or absence of prostaglandin class varies.…”

“…Predicted Penaeus monodon prostanoid biosynthesis pathway. Modified from Wimuttisuk et al (2013) PGF2α in the Florida crayfish Procambarus paeninsulanus (Spaziani et al, 1995, Spaziani et al, 1993, Kuruma shrimp Marsupenaeus japonicus (Tahara and Yano, 2004), and P. monodon (Wimuttisuk et al, 2013), whilst only PGE2 has been reported in the shore crab Carcinus maenas (Hampson et al, 1992) and acorn barnacle Balanus Amphitrite (Knight et al, 2000). In P. monodon, PGF2 acts as a regulator of maturation (Wimuttisuk et al, 2013), whilst PGE2 promotes the development of yolk globules and cortical rods in P. monodon oocytes during early, and late stage development respectively (Meunpol et al, 2010).…”