Functional dynamics of claudin expression in Japanese medaka (Oryzias latipes): Response to environmental salinity

Abstract

Salinity regulation of 13 claudin paralogs was investigated in osmoregulatory organs of euryhaline Japanese medaka. They were identified by blast-search in the medaka genome database based on representation in osmoregulatory organs of other teleosts. Our hypothesis was that, because of their sequence similarities to mammalian orthologs previously characterized as barrier- and ion-selective channel-forming proteins, these paralogs would respond to salinity according to expected modulation of osmoregulatory function. Cldn10c, -10d, -10e, -10f, -27a, -28a, -28b and -30c had 4- to 100-fold higher expression in gill than other examined organs. Two splice variants of cldn10b were predominantly expressed in kidney, while cldn15a, -15b and -25 were found mainly in intestine. In gills, cldn27a, -28a, -28b and -30c did not change between fresh water (FW) and seawater (SW)-acclimated fish, while cldn10c, -10d, -10e, and -10f were most abundant in SW. Short-term SW transfer induced up-regulation of cldn10 gill paralogs after 1 day, decrease in cldn28b and no difference for cldn27a, -28a and -30c. The reverse pattern was observed after FW transfer of SW medaka. Intestinal cldn15a and -25 did not differ between FW and SW fish. However, cldn15b was 10-fold higher in FW than SW, suggesting a role in functional modulation of the intestine related to water and salt transport. In kidney, cldn10bs were elevated in SW fish, suggesting a role in paracellular ion transport in the marine nephron. Based on in silico analysis, most gill Cldn10s were predicted to form cation pores, whereas Cldn27a, 28a, 28b and 30c may increase epithelial resistance.

Drinking and Water Handling in the Medaka Intestine: A Possible Role of Claudin-15 in Paracellular Absorption?

“…The time-course experiment showed that cldn15b was not significant affected by SW before 24 h and 168 h while the inhibitory effect on the two aqps was apparent at the 6 h and 24 h mark but not significant at the 168 h time point. Thus, while the dynamics of regulation are not straightforward, the overall inhibitory effect of SW on cldn15b, aqp1a, and aqp8ab observed previously was confirmed [8,34].…”

“…Based on similarities to the mammalian CLDN15 shown in Figure 11, we hypothesized that the two medaka orthologs, cldn15a and cldn15b, may share functional properties in terms of forming cation and water pores and therefore may contribute to paracellular water absorption in SW medaka. In fishes (medaka [34]; salmon [31,32]; zebrafish [33]) and mammals [12], CLDN15 orthologs are expressed especially, but not exclusively, in the GI tract. In Atlantic salmon, SW acclimation was shown to induce elevated intestinal cldn15a mRNA expression [32], and a different study in the same species documented higher transepithelial resistance in SW than FW intestine measured ex vivo [48].…”

“…In mice, CLDN15-mediated Na + back-flux into the intestinal lumen is essential for active glucose absorption through the Na + /glucose cotransporter, safeguarding monosaccharide uptake [30]. In fishes, Cldn15a paralogs have been found to be expressed specifically in the gastrointestinal (GI) tract (salmon [31,32], zebrafish [33], medaka [34]). In medaka, we previously identified an additional new paralog, Cldn15b, which is also primarily expressed in the intestine at levels several orders of magnitude higher than any other examined organs [34].…”

Genetic basis for variation in salinity tolerance between stickleback ecotypes

“…Another candidate gene cldn10 encodes a component of tight junctions. Seawater transfer induced elevation of cldn10 expression in the gills of medaka (Bossus et al 2015). It is likely that differential expression of cldn10 can contribute to divergence in salinity tolerance between ecotypes.…”

Optimal dietary protein level improved growth, disease resistance, intestinal immune and physical barrier function of young grass carp (Ctenopharyngodon idella)

“…Tipsmark et al [81] indicated that claudin 15 could regulate paracellular Na þ movement in the intestines of Atlantic salmon (Salmo salar). In Japanese medaka (Oryzias latipes) intestine, the mRNA levels of claudin 15a were significantly higher than the claudin 15b mRNA level in response to a salinity change, leading to a claudin 15b net transport of sodium that was negligible [82]. Meanwhile, Kaplan [83] reported that Na þ , K þ -ATPase carries out the uptake of Na þ in most higher eukaryotes.…”