Protein kinase C mediates juvenile hormone–dependent phosphorylation of Na+/K+-ATPase to induce ovarian follicular patency for yolk protein uptake

Abstract

<p class="first" id="d533318e166">In oviparous animals, vitellogenesis is prerequisite to egg production and embryonic growth after oviposition. For successful insect vitellogenesis and oogenesis, vitellogenin (Vg) synthesized in the fat body (homologue to vertebrate liver and adipose tissue) must pass through the intercellular channels, a condition known as patency in the follicular epithelium, to reach the surface of oocytes. This process is controlled by juvenile hormone (JH) in many insect species, but the underlying mechanisms remain elusive. Previous work has suggested the possible involvement of Na ⁺/K ⁺-ATPase in patency initiation, but again, the regulatory cascade of Na ⁺/K ⁺-ATPase for patency initiation has been lacking. Using the migratory locust <i>Locusta migratoria</i> as a model system, we report here that RNAi-mediated knockdown of gene coding for Na ⁺/K ⁺-ATPase, inhibition of its phosphorylation, or suppression of its activity causes loss of patency, resulting in blocked Vg uptake, arrested oocyte maturation, and impaired ovarian growth. JH triggers G protein–coupled receptor (GPCR), receptor tyrosine kinase (RTK), phospholipase C (PLC), inositol trisphosphate receptor (IP3R), and protein kinase C (PKC) to phosphorylate Na ⁺/K ⁺-ATPase α-subunit at amino acid residue Ser ⁸, consequently activating Na ⁺/K ⁺-ATPase for the induction of patency in vitellogenic follicular epithelium. Our results thus point to a previously unidentified mechanism by which JH induces the phosphorylation and activation of Na ⁺/K ⁺-ATPase via a signaling cascade of GPCR, RTK, PLC, IP3R, and PKC. The findings advance our understanding of JH regulation in insect vitellogenesis and oogenesis. </p>