RME-1-associated recycling endosomes participate in vitellogenin secretion in Caenorhabditis elegans

Abstract

Vitellogenins (VITs), the lipoprotein precursors of yolk proteins in Caenorhabditis elegans, are expressed in the intestine, secreted into the pseudocoelom, and ultimately transported into oocytes. However, the mechanism by which VITs are secreted out of the intestine remains unclear. In this study, a candidate RNA interference (RNAi) screen suggested that both the conventional secretion pathway and recycling endosomes (REs) are essential for VIT secretion. In addition to expected conventional secretion, VITs were also found to be synthesized in the intestinal rough endoplasmic reticulum (ER) and then transported to the Golgi apparatus. VIT-2::GFP accumulated in enlarged REs upon depletion of receptor-mediated endocytosis 1 (RME-1), a key protein that facilitates endocytic recycling. Moreover, the number of VIT-2::GFP-containing REs decreased upon inhibition of either ER-to-Golgi trafficking, trans-Golgi-to-endosome trafficking, or endocytosis. These findings suggested that REs are required for intestinal secretion of both newly synthesized VITs and yolk proteins endocytosed from the pseudocoelom. Moreover, RME-1 was found at the periphery of vitellogenin-containing vesicles (VVs), and this required RAB-10, the upstream regulator of RME-1 in endocytic recycling. RAB-10 was additionally required for the trafficking of VV from the apical/luminal side to the basal/pseudocoelomic side of the intestine. Together, these results identify REs as an intermediate compartment for the secretion of VIT/yolk proteins out of the intestine, suggesting a conserved role for endocytic recycling in the secretion of lipoproteins in mammals, particularly those assembled by apolipoprotein B-100 (apoB-100), a mammalian homolog of VITs.

Keywords

vitellogenin / yolk protein / secretion / recycling endosomes / Caenorhabditis elegans / apoB-100

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