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Review
. 2019 Aug 21;10:1067.
doi: 10.3389/fphys.2019.01067. eCollection 2019.

Vitellogenins - Yolk Gene Function and Regulation in Caenorhabditis elegans

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Free PMC article
Review

Vitellogenins - Yolk Gene Function and Regulation in Caenorhabditis elegans

Marcos Francisco Perez et al. Front Physiol. .
Free PMC article

Abstract

Vitellogenins are a family of yolk proteins that are by far the most abundant among oviparous animals. In the model nematode Caenorhabditis elegans, the 6 vitellogenins are among the most highly expressed genes in the adult hermaphrodite intestine, which produces copious yolk to provision eggs. In this article we review what is known about the vitellogenin genes and proteins in C. elegans, in comparison with vitellogenins in other taxa. We argue that the primary purpose of abundant vitellogenesis in C. elegans is to support post-embryonic development and fertility, rather than embryogenesis, especially in harsh environments. Increasing vitellogenin provisioning underlies several post-embryonic phenotypic alterations associated with advancing maternal age, demonstrating that vitellogenins can act as an intergenerational signal mediating the influence of parental physiology on progeny. We also review what is known about vitellogenin regulation - how tissue-, sex- and stage-specificity of expression is achieved, how vitellogenins are regulated by major signaling pathways, how vitellogenin expression is affected by extra-intestinal tissues and how environmental experience affects vitellogenesis. Lastly, we speculate whether C. elegans vitellogenins may play other roles in worm physiology.

Keywords: elegans; embryogenesis; gene; nematode; regulation; roundworm; vitellogenin; yolk.

Figures

FIGURE 1
FIGURE 1
The vitellogenin family in C. elegans is comprised of 6 genes. The outgroup is the vit-6 gene from the African social velvet spider, Stegodyphus mimosarum. Arachnid vitellogenins are the sister group to nematode vitellogenins (Tufail et al., 2014). Scale bar represents nucleotide substitutions per site. Adapted from Perez (2018).
FIGURE 2
FIGURE 2
Vitellogenins are taken up by receptor-mediated endocytosis. C. elegans oocytes pass through the spermatheca for fertilization, after which the embryos begin development in the maternal uterus. Here a VIT-2:GFP translational fusion protein is shown being taken up by proximal oocytes prior to fertilization. As the oocyte nears the spermatheca, VIT-2:GFP taken up by receptor-mediated endocytosis at the cell membrane gradually extends throughout the cytoplasm and can be seen in the embryos in utero after fertilization. Scale bar, 50 μm. Reprinted from Perez (2018).
FIGURE 3
FIGURE 3
Yolk accumulates to pathological levels in post-reproductive hermaphrodites. Brightfield and fluorescence images are shown of hermaphrodites on adult day 1 or adult day 8 carrying a VIT-2:GFP translational fusion. Scale bar, 50 μm. Reprinted from Perez (2018).
FIGURE 4
FIGURE 4
Substantial levels of vitellogenin remain after embryogenesis. Vitellogenin visualized by immunofluorescence in an early embryo and in an embryo immediately prior to hatching. Scale bar, 5 μm. Adapted from Sharrock (1983).
FIGURE 5
FIGURE 5
Vitellogenin underlies the small size and susceptibility to L1 starvation of the progeny of young mothers. Vitellogenin provisioning to embryos increases during the self-fertile reproductive period, possibly due to an increase in biosynthetic capacity in older, larger worms. As a result of their higher embryonic vitellogenin titer, progeny of older mothers are larger at hatching, are more resistant to L1 starvation and reach adulthood sooner, even if the absence of starvation. Conversely the early progeny coming from younger mothers, with the least embryonic vitellogenin, are impaired for these same traits.
FIGURE 6
FIGURE 6
Autofluorescent gut granules are grossly enlarged upon hatching in larvae mutant for the single yolk receptor, rme-2. (A) Blue autofluorescence from lysosome-related organelles in newly hatched wildtype L1 larva. (B) Newly hatched L1 larvae of rme-2(b1008) mutants, which lack any detectable embryonic yolk, have very large lysosome-related organelles. This may be due to the abrogation of phospholipid import by vitellogenin lipoprotein complexes. The physiological consequences of this enlargement are unknown. Scale bars main images 10 μm, insets 5 μm. Reprinted from Perez (2018).
FIGURE 7
FIGURE 7
The regulation of vitellogenin genes is affected by various physiological and environmental conditions upstream of a multitude of signaling pathways. In the figure, physiological or environmental factors known to influence vitellogenin expression are seen in the outermost blue circle. In the intermediate orange circle are shown the various described genetic regulators or signaling pathways (bold), many of which have been shown to mediate physiological or environmental effects. Together these regulators tightly control the abundant and metabolically costly expression of the vitellogenin genes (represented by the central red circle).
FIGURE 8
FIGURE 8
Age-dependent somatic depletion of fat in skn-1 gain of function mutants. Fixed post-reproductive worms are stained with Oil Red O, a lipid stain. Arrows indicate soma and arrowheads indicate germline. (A,B), wildtype worms. (C,D), skn-1 gain of function mutant. Scale bars, 100 μm. Reprinted from Lynn et al. (2015).

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