Evolution of oogenesis: the receptor for vitellogenin from the rainbow trout

Abstract

Receptors that transport vitellogenin (VTG) into oocytes are of vital importance to egg-laying species because they mediate a key step in oocyte development. Here we describe the cloning of the first piscine oocyte-specific receptor cDNA, i.e., that encoding the VTG receptor from the rainbow trout ( Oncorhynchus mykiss ). The receptor, a 826-residue type-I membrane protein, is a member of the low density lipoprotein receptor (LDLR) superfamily. It closely resembles the mammalian so-called very low density lipoprotein receptors, in that its aminoterminal ligand binding domain consists of a cluster of 8 cysteine-rich repeats. The short intracellular portion contains the internalization signal typical for the LDLR superfamily, Phe-Glu-Asn-Pro-Val-Tyr. Notably, the receptor lacks a domain with a high density of potential O-glycosylation sites often found in somatic cell-specific members of the LDLR family. A specific transcript of 3.9 kb is abundant in ovary, but undetectable in muscle and heart, which are the major sites of expression of very low density lipoprotein receptors in mammals. In vitro translation of the full-length cDNA produced a 97-kDa protein, and transient expression in COS-1 cells showed that the cDNA encodes a protein of the same size that binds vitellogenin in ligand blots. As revealed by in situ hybridization, transcripts are present in previtellogenic oocytes, indicating that production of receptor protein precedes the phase of yolk deposition. Our results in fish, together with those in birds (Bujo, H., et al. 1994. EMBO J. 13: 5165-5175) suggest that vitellogenesis provides a prime model for the study of ligand/receptor systems designed to sustain reproduction.-Davail, B.

An insect homolog of the vertebrate very low density lipoprotein receptor mediates endocytosis of lipophorins

“…This also indicates that the cell surface localization observed in fat body tissue of older adults is not due to a redistribution of this endocytic receptor, as we previously postulated ( 1), but rather to the appearance of a different cell surface binding site. Moreover, the downregulation observed in the oocytes is very similar to the reported developmental down-regulation of the avian and piscine vitellogenin receptors (7,8). We consider this novel member of the LDL receptor family a likely candidate for the receptor that mediates HDLp endocytosis by fat body cells and oocytes.…”

“…In vertebrates, many different LDL receptor family members have been identified. These can be divided in receptors with a single ligand-binding domain and EGFprecursor domain, such as the classic LDL receptor (3), the apoE receptor 2 (6), and the VLDL receptor (5,7,8), and receptors containing multiple clusters of these two domains, such as the LDL receptor-related protein (4). Until now, only the latter receptor type had been found in invertebrates: a nematode homolog of the LDL receptorrelated protein containing five clusters (9) and two insect vitellogenin receptors containing two clusters (10,11).…”

“…Receptor-mediated endocytosis of lipoproteins has been studied in detail in vertebrate cells (2). Cloning of different receptors that accomplish lipoprotein uptake has re-sulted in the identification of the low density lipoprotein (LDL) receptor family, the members of which share structural and functional features (3)(4)(5)(6)(7)(8). These receptors appear to originate from an ancient receptor in view of the identification of a similarly composed cell surface molecule in Caenorhabditis elegans (9) and two insect vitellogenin receptors belonging to this gene superfamily (10,11).…”

Vitellogenin receptor and fatty acid profiles of individual lipid classes of oocytes from wild and captive-reared greater amberjack (Seriola dumerili) during the reproductive cycle

“…These receptors have been given different names: VLDLR, Vtg Receptors (Vtgr) or Lr8- [21,59]. The structural characteristics of these receptors have been described in several teleosts [21,46,[60][61][62], showing that they are produced from a highly conserved gene among teleost. Recently, Lrp13, a novel vertebrate lipoprotein receptor that binds Vtgs was sequenced from striped bass, white perch, zebrafish (Danio rerio) and cutthroat trout ovaries [20].…”

Are Cell Junctions Implicated in the Regulation of Vitellogenin Uptake? Insights from an RNAseq-Based Study in Eel, Anguilla australis

“…The deduced proteins from both genes clustered into distinct groups corresponding to Lr8 and Lrp13 members from the LDLR family. Both members have been confirmed to bind Vtg in perciform and salmonid species, i.e., white perch, Morone americana [3], rainbow trout, O. mykiss [82] and cutthroat trout, O. clarki [83]. Therefore, they were both considered in this study as putative Vtgrs.…”