Mating Increases CHST10 Activity in Rat Oviductal Mucosa to Induce the Synthesis of HNK-1 Glycoproteins: Possible Role in Sperm–Oviduct Interactions

Previously, we reported that mating induces an early transcriptional response in the oviductal mucosa of rats. The functional category 'cell-to-cell signaling and interaction' was overrepresented in this gene list. Therefore, in the present study, we describe the role of one of these genes, <i>carbohydrate sulfotransferase 10</i> (<i>Chst10</i>), in the oviductal mucosa. CHST10 participates in the synthesis of the carbohydrate moiety human natural killer-1 (HNK-1), which mediates cell-to-cell interactions. When using one-dimensional Western blot and sulfotransferase analyses, we found that mating increased the protein level and activity of CHST10 in the oviductal mucosa at 3 h after stimulation. A two-dimensional Western blot analysis and mass spectrometry were used to identify the novel HNK-1 glycoproteins aldehyde dehydrogenase 9 family, member A1 (ALDH9A1), fructose bisphosphate aldolase A (ALDOA), and four and a half LIM domains protein 1 (FHL1) in the oviductal mucosa, and we found that mating induces the synthesis of their acidic variants. Interestingly, in the utero-tubal junction (UTJ), acrosome-reacted sperm apparently were interacting with regions in which ALDH9A1 and HNK-1 signals overlap. Furthermore, vaginocervical stimulation applied to unmated rats increased the mRNA level of <i>Chst10</i> in the oviductal mucosa. In conclusion, mating increases the activity of CHST10 in the oviductal mucosa, which in turn induces the synthesis of acidic variants of ALDH9A1 and FHL1 via HNK-1 glycosylation. ALDH9A1, HNK-1-ALDH9A1, and/or other HNK-1 glycoproteins could participate in the negative selection of sperm in the UTJ, since we detected acrosome-reacted sperm apparently interacting with regions where these proteins are located. Finally, the sensorial component of mating could regulate early events (e.g., sperm transport and selection) occurring in the oviductal mucosa after mating.