Lrp13 is a novel vertebrate lipoprotein receptor that binds vitellogenins in teleost fishes

Reading, Benjamin J.; Hiramatsu, Naoshi; Schilling, Justin; Molloy, Katelyn T.; Glassbrook, Norm; Mizuta, Hiroyuki; Luo, Wenshu; Baltzegar, David A.; Williams, Valerie N.; Todo, Takashi; Hara, Akihiko; Sullivan, Craig V.

doi:10.1194/jlr.m050286

Cited by 51 publications

(63 citation statements)

References 58 publications

(64 reference statements)

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“…Relative transcript copy number of apoe in the ovary increased as did that of lpl, quite possibly as a mechanism to supply more lipoprotein-harnessed energy (i.e., lipids) to the tissue. Relative transcript copy number of the vtgr also increased, corresponding well with the assumed onset of vitellogenin uptake and expression patterns seen in other species of fish (11,20,27,50,56,58). Relative transcript copy number of the ldlr increased from the perinucleolar stage to the oil droplet stage.…”

Section: R939mentioning

confidence: 55%

Triacylglyceride physiology in the short-finned eel,Anguilla australis—changes throughout early oogenesis

Damsteegt

Falahatimarvast

McCormick

et al. 2015

American Journal of Physiology-Regulatory, Integrative and Comp

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During certain stages in an animal's life cycle, energy requirements may exceed energy intake from the diet. The spawning migration of temperate eels is a textbook example of negative energy balance, forcing these fish to rely on stored fats (triacylglycerides) to provide their muscles with energy for swimming and their growing oocytes with the nutrients needed to develop and support healthy offspring. We predicted broad implications of this great need for endogenous triacylglycerides in terms of their packaging, transport, and ovarian uptake. To test this, serum lipid concentrations and transcript abundances of intestinal and hepatic triacylglyceride packagers and ovarian triacylglyceride modifiers and receivers were investigated throughout previtellogenesis (feeding phase) and into early vitellogenesis (fasting phase) in short-finned eels. A switch from exogenous to endogenous triacylglyceride packaging was seen as the liver upregulated transcript levels of apolipoprotein B and microsomal triacylglyceride transport protein and downregulated those of apolipoprotein E and lipoprotein lipase. In the intestine, the reverse response was observed. Furthermore, ovarian transcript abundances of triacylglyceride modifiers and receivers increased (apolipoprotein E, lipoprotein lipase, and vitellogenin receptor), indicative of increased triacylglyceride uptake during previtellogenesis. We propose that increased hepatic apolipoprotein B production is a conserved vertebrate response to prolonged periods of negative energy balance.

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Section: R939mentioning

confidence: 55%

Triacylglyceride physiology in the short-finned eel,Anguilla australis—changes throughout early oogenesis

Damsteegt

Falahatimarvast

McCormick

et al. 2015

American Journal of Physiology-Regulatory, Integrative and Comp

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“…Additional insights on the fish Lr8-type Vtg receptor have been accumulating; however, when considering the 'multiple Vtg model', almost no information is available regarding the binding of different Vtg subtypes with the Lr8-type Vtg receptor. In an experiment with white perch, Reading et al [123,124] confirmed the possibility that VtgAa and VtgAb may bind to different receptors and indicated that in addition to the Lr8-type Vtg receptor, a novel lipoprotein receptor (low-density lipoprotein receptor-related protein 13, Lrp13) may be involved in Vtg binding. Many unidentified lipoprotein receptors exist in fish, and the affinity of these receptors for Vtg will likely be revealed in the future.…”

Section: Future Concernsmentioning

confidence: 74%

Vitellogenesis and choriogenesis in fishes

2016

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“…Binding of Vtg to the translated products of these receptors, however, has only been verified for salmonid LR8‐type Vtgr. On the other hand, distinct binding of two major VtgA subtypes (VtgAa and VtgAb) to ovarian membrane proteins of Morone species has been confirmed by ligand and Western blotting and by receptor‐binding assays, wherein the classic LR8‐type Vtgr appears to bind VtgAb while a membrane protein with a large molecular mass (>212 kDa) predominantly binds VtgAa (Reading et al, , ). The latter VtgAa binding protein was identified as a novel receptor belonging to the LDLR superfamily, and designated as Lrp13 (Reading et al, ).…”

Section: Introductionmentioning

confidence: 97%

“…A member of the low‐density lipoprotein receptor (LDLR) gene family, which contains a single ligand‐binding domain consisting of eight ligand‐binding repeats (termed LR8 or VLDLR by Bujo et al, ), was previously identified and designated as the Vtgr in teleosts (Davail et al, ; Prat et al, ; Hiramatsu et al, ). Several biochemical studies, however, have revealed multiple ovarian membrane proteins that specifically bind Vtg in salmonids (Tyler and Lubberink, ) and in perciforms (Reading et al, , ).…”

Section: Introductionmentioning

confidence: 99%

“…Thus far, teleost Vtgs appear to be incorporated into the yolk not only via the classical LR8‐type Vtgr—an ortholog of mammalian VLDLR—but also via other oocyte membrane receptors, including candidates such as LR7‐type receptor—an ortholog of mammalian LDLR—and LDLR‐related proteins (LRPs) (Hiramatsu et al, ; Reading et al, ). Five Vtg‐binding proteins were detected by ligand blotting ovarian follicle membrane preparations from rainbow trout ( Oncorhynchus mykiss ) (Tyler and Lubberink, ), and transcripts encoding three distinct lipoprotein receptors—LR8‐type Vtgr (Mizuta et al, ), Ldlr (Luo et al, ), and a novel, unclassified receptor termed LR13+1 (Hiramatsu et al, )—were cloned as cDNA orthologs from the ovaries of cutthroat trout, O. clarki .…”

Section: Introductionmentioning

confidence: 99%

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Molecular cloning and partial characterization of a low‐density lipoprotein receptor‐related protein 13 (Lrp13) involved in vitellogenin uptake in the cutthroat trout (Oncorhynchus clarki)

Mushirobira

Mizuta

Luo

et al. 2015

Molecular Reproduction Devel

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Multiple ovarian membrane proteins that bind vitellogenin (Vtg) have been detected in teleosts. One of these Vtg receptors was recently identified as low-density lipoprotein receptor-related protein 13 (lrp13/Lrp13) in perciform species, but little is known about this Vtg receptor in salmonid fish. In this study, a cDNA encoding a putative Vtg receptor with 13+1 ligand binding repeats (lr13+1) was cloned from the ovary, and identified as an lrp13 ortholog for cutthroat trout (Oncorhynchus clarki). This lrp13 was predominantly expressed in the pre-vitellogenic stage ovary, and its expression decreased during vitellogenesis. Ovarian localization of Lrp13 was observed by immunohistochemistry using specific antiserum against recombinant Lrp13. Lrp13 immunoreactivity was observed at the oolemma, throughout the zona radiata, and within the perivitelline space between the zona radiata and granulosa cells in ovarian follicles at both the lipid-droplet and vitellogenic stages of growth-an expression pattern that mimics that of a lr8/LR8-type Vtg receptor in this species and of lrp13/Lrp13 in Morone species. Six discrete Vtg-binding proteins were detected in cutthroat trout ovarian membrane proteins when probing with a digoxygenin-labeled salmonid A-type Vtg (VtgAs) followed by chemiluminescent ligand detection. Western blotting using the anti-Lrp13 serum revealed a broad signal consisting of two proteins with masses ranging from ∼190 to ∼210 kDa, which corresponded with some of the VtgA-binding proteins. These findings suggest that, in addition to lr8/LR8, lrp13/Lrp13 acts as a VtgA receptor in trout.

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Lrp13 is a novel vertebrate lipoprotein receptor that binds vitellogenins in teleost fishes

Cited by 51 publications

References 58 publications

Triacylglyceride physiology in the short-finned eel,Anguilla australis—changes throughout early oogenesis

Triacylglyceride physiology in the short-finned eel,Anguilla australis—changes throughout early oogenesis

Vitellogenesis and choriogenesis in fishes

Molecular cloning and partial characterization of a low‐density lipoprotein receptor‐related protein 13 (Lrp13) involved in vitellogenin uptake in the cutthroat trout (Oncorhynchus clarki)

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