Mechanisms for type-II vitellogenesis-inhibiting hormone suppression of vitellogenin transcription in shrimp hepatopancreas: Crosstalk of GC/cGMP pathway with different MAPK-dependent cascades

Abstract

Vitellogenesis is the process of yolk formation via accumulating vitellin (Vn) with nutrients in the oocytes. Expression of vitellogenin (Vg), the precursor of Vn, is one of the indicators for the start of vitellogenesis. In Pacific white shrimp (Litopenaeus vannamei), the type-II vitellogenesis-inhibiting hormone (VIH-2) effectively suppresses hepatopancreatic Vg mRNA expression. In this study, we demonstrate the increasing transcript levels of hepatopancreatic Vg during L. vannamei ovarian development, suggesting that the hepatopancreas-derived Vg/Vn may also contribute to vitellogenesis in this species. Using a combination of in vivo injections and in vitro primary cell cultures, we provide evidences that the inhibition of VIH-2 on hepatopancreatic Vg gene expression is mediated through a functional coupling of the GC/cGMP pathway with different MAPK-dependent cascades in female shrimp. In VIH-2 signaling, the NO-independent GC/cGMP/PKG cascades were upstream of the MAPKs. Activations of the MAPK signal by VIH-2 include the phosphorylation of JNK and the mRNA/protein expression of P38MAPK. Additionally, the cAMP/PKA pathway is another positive intracellular signal for hepatopancreatic Vg mRNA expression but is independent of its VIH-2 regulation. Our findings establish a model for the signal transduction mechanism of Vg regulation by VIH and shed light on the biological functions and signaling of the CHH family in crustaceans.

Heat Shock Protein 40 (HSP40) in Pacific White Shrimp (Litopenaeus vannamei): Molecular Cloning, Tissue Distribution and Ontogeny, Response to Temperature, Acidity/Alkalinity and Salinity Stresses, and Potential Role in Ovarian Development

“…et al,2018; Luo et al, 2015). However, neither the hepatopancreatic or ovarian Vg (Figure 7F), nor the ovarian VgR (Figure 7G) transcript levels changed after RNAi of Lv-HSP40 for 24 h. It is speculated that Lv-HSP40 directly acting on the ovary and is irrelevant to the exogenous vitellogenesis occurred in hepatopancreas (Chen T. et al, 2018). Within the ovary, Lv-HSP40 mRNA were majorly expressed in the follicle cells (Figure 4B), which provide nutrients and energy to the developing oocytes for growth and maturation.…”

The Crustacean Hyperglycemic Hormone Superfamily: Progress Made in the Past Decade

“…Recently, a study on the mode of GIH action was carried out in L. vannamei using vg expression in the hepatopancreas as the bioassay. According to Chen et al ( 250 ), in vivo injection and in vitro incubation of hepatopancreatic primary cells with recombinant GIH elevated the levels of intracellular cGMP, but not cAMP or nitric oxide, indicating that GIH exerts a cGMP-mediated inhibitory action. Pharmacological reagents were then tested to characterize the GIH signaling pathway.…”

Transcriptional Regulation of Vih by Oct4 and Sox9 in Scylla paramamosain

“…In the S. olivacea , VIH in the eyestalk is involved in inhibiting the production of VTG ( 34 ). Type II VIH in P. vannamei has the activity of inhibiting its vitellogenesis, and it can effectively inhibit the expression of Vtg mRNA in the hepatopancreas of the shrimp ( 35 ). In order to further explore the influence of Oct4 and Sox9 on SpVtg , we tested the expression level of SpVtg in ovary and hepatopancreas of mud crab after Oct4 and Sox9 interference.…”