Oocyte signals derived from polyunsaturated fatty acids control sperm recruitment in vivo

Abstract

A fundamental question in animal development is how motile cells find their correct target destinations. During mating in the nematode Caenorhabditis elegans, males inject sperm through the hermaphrodite vulva into the uterus. Amoeboid sperm crawl around fertilized eggs to the spermatheca--a convoluted tube where fertilization occurs. Here, we show that polyunsaturated fatty acids (PUFAs), the precursors of eicosanoid signalling molecules, function in oocytes to control directional sperm motility within the uterus. PUFAs are transported from the intestine, the site of fat metabolism, to the oocytes yolk, which is a lipoprotein complex. Loss of the RME-2 low-density lipoprotein (LDL) receptor, which mediates yolk endocytosis and fatty acid transport into oocytes, causes severe defects in sperm targeting. We used an RNAi screen to identify lipid regulators required for directional sperm motility. Our results support the hypothesis that PUFAs function in oocytes as precursors of signals that control sperm recruitment to the spermatheca. A common property of PUFAs in mammals and C. elegans is that these fats control local recruitment of motile cells to their target tissues.

Proteomic Study and Marker Protein Identification of Caenorhabditis elegans Lipid Droplets

“…Vit-1, 2, 3, 4, 5, and 6 were also present (Table I). Vit proteins are apolipoprotein homologs believed to transport lipids to growing oocytes during yolk deposition (33). Western blotting analysis showed that Vit-2 was only partially associated with LDs and the main signal was in total membrane fraction (Fig.…”

Identification of two epoxide hydrolases in Caenorhabditis elegans that metabolize mammalian lipid signaling molecules

“…C18 and C20 polyunsaturated fatty acids (PUFAs) have been shown to effect directed sperm movement towards the spermatheca and the formation of synaptic vesicles in neuronal tissues. [18,19] FAT-3 mutants lack the delta6 fatty acid desaturase and so cannot convert linoleic acid into C20 PUFAs because this desaturase activity is a prerequisite to subsequent elongase activity. [20] These mutants show a number of defects which are rescued by dietary supplementation of C20 and C18 PUFAs, including smaller brood size, alterations in the defecation cycle, and defects in chemotaxis.…”

Gamete interactions require transmembranous immunoglobulin-like proteins with conserved roles during evolution

“…Therefore, when genes involved in the synthesis are mutated, spermatozoa become partly defective in their relocation from the uterus into the spermatheca. [18][19][20] These phenotypes seem similar to those of spe-9 and spe-45 mutants, resulting in the incomplete sperm recruitment into the spermatheca. Currently the sperm prostaglandin-receptor(s) is not known, but SPE-9 and/or SPE-45 could function in the prostaglandin binding to spermatozoa and/or subsequent sperm reaction(s).…”