Identification of Receptor‐Interacting Regions of Vitellogenin within Evolutionarily Conserved β‐Sheet Structures by Using a Peptide Array

Abstract

Vitellogenesis, a key process in oviparous animals, is characterized by enhanced synthesis of the lipoprotein vitellogenin, which serves as the major yolk-protein precursor. In most oviparous animals, and specifically in crustaceans, vitellogenin is mainly synthesized in the hepatopancreas, secreted to the hemolymph, and taken up into the ovary by receptor-mediated endocytosis. In the present study, localization of the vitellogenin receptor and its interaction with vitellogenin were investigated in the freshwater prawn Macrobrachium rosenbergii. The receptor was immuno-histochemically localized to the cell periphery and around yolk vesicles. A receptor blot assay revealed that the vitellogenin receptor interacts with most known vitellogenin subunits, the most prominent being the 79 kDa subunit. The receptor was, moreover, able to interact with trypsin-digested vitellogenin peptides. By combining a novel peptide-array approach with tandem mass spectrometry, eleven vitellogenin-derived peptides that interacted with the receptor were identified. A 3D model of vitellogenin indicated that four of the identified peptides are N-terminally localized. One of the peptides is homologous to the receptor-recognized site of vertebrate vitellogenin, and assumes a conserved β-sheet structure. These findings suggest that this specific β-sheet region in the vitellogenin N-terminal lipoprotein domain is the receptor-interacting site, with the rest of the protein serving to enhance affinity for the receptor. The conservation of the receptor recognition site in invertebrate and vertebrate vitellogenin might have vast implications for oviparous species reproduction, development, immunity, and pest management.

Insect tissue-specific vitellogenin facilitates transmission of plant virus

“…The mature Vg contains an N-terminal domain (Vitellogenin_N [Vit_N)], a middle-region domain of unknown function (DUF1943), and a von Willebrand factor type D (vWD) C-terminal domain [ 5 , 33 , 44 – 46 ]. Domain Vit_N is required for interaction with the Vg receptor (VgR) [ 9 , 47 ], while domains DUF1943 and vWD play roles in pathogen recognition [ 48 ]. An example in vertebrate animals is that of Oreochromis aureus Vg, which interacts with VgR via a polypeptide fragment located in the Vit_N domain [ 9 ].…”

“…An example in vertebrate animals is that of Oreochromis aureus Vg, which interacts with VgR via a polypeptide fragment located in the Vit_N domain [ 9 ]. Arthropoda, Macrobrachium rosenbergii Vg also interacts with its receptor via a specific β -sheet region in the Vit_N lipoprotein domain [ 47 ]. In scallops, both the recombinant DUF1943 and vWD domains of the Patinopecten yessoensis Vg protein can interact with the lipopolysaccharides and lipoteichoic acid expressed on the bacterial cell wall [ 45 ].…”

Transfer of Immunity from Mother to Offspring Is Mediated via Egg-Yolk Protein Vitellogenin

“…Mutation hotspots are found within the honey bee vitellogenin sequence, and the multiple alleles are under ongoing positive selection in Africa, East- and West-Europe. By analogy to vertebrate adaptive immunity [ 15 , 25 , 26 ], certain Vg variants could be more sensitive to specific pathogen recognition. Vitellogenin alleles in at least some insects may thus evolve under local pathogen pressure.…”

Ancient Duplications Have Led to Functional Divergence of Vitellogenin-Like Genes Potentially Involved in Inflammation and Oxidative Stress in Honey Bees

“…The main production site is most likely the fat body, as Vg and most secreted proteins are produced in this tissue ( Arrese and Soulages 2010 ). The presence of the N-sheet domain in all three Vg-like proteins suggests that they could be taken up from the hemolymph by some tissues, given that the N-sheet contains the Vg receptor binding area ( Roth et al 2013 ). The Vg receptor transfers Vg to tissues located in the head, the ovaries, and the hypopharyngeal glands, among others ( Guidugli-Lazzarini et al 2008 ).…”