Environmental factors responsible for switching on the SO₄²⁻excretory system in the kidney of seawater eels

Abstract

2Ϫ regulation between FW and SW. We previously showed that the expression of renal SO 4 2Ϫ transporter genes, FW-specific Slc13a1 and SW-specific Slc26a6a, changes profoundly after transfer of FW eels to SW, which results in the decrease in plasma SO 4 2Ϫ concentration after 3 days in SW. In this study, we attempted to identify the environmental factor(s) that trigger the switching of SO 4 2Ϫ regulation using changes in plasma and urine SO 4 2Ϫ concentrations and expression of the transporter genes as markers. Transfer of FW eels to 30 mM SO 4 2Ϫ or transfer of SW eels to SO 4 2Ϫ -free SW did not change the SO 4 2Ϫ regulation. Major divalent cations in SW, Mg 2ϩ (50 mM) and Ca 2ϩ (10 mM), were also ineffective, but 50 mM NaCl was effective for switching the SO 4 2Ϫ regulation. Further analyses using choline-Cl and Na-gluconate showed that Cl Ϫ is a primary factor and Na ϩ is permissive for the Cl Ϫ effect. Since plasma SO 4 2Ϫ and Cl Ϫ concentrations were inversely correlated, we injected various solutions into the blood and found that Cl Ϫ alone triggered the switching from FW to SW-type regulation. Furthermore, the inhibitor of Na-Cl cotransporter (NCC) added to media significantly impaired the expression of SW-specific Slc26a6a in 150 mM NaCl. In summary, it appears that Cl Ϫ ions in SW are taken up into the circulation via the NCC together with Na ϩ , and the resultant increase in plasma Cl Ϫ concentration enhances SO 4 2Ϫ excretion by the kidney through downregulation of absorptive Slc13a1 and upregulation of excretory Slc26a6a, resulting in low plasma SO 4 2Ϫ concentration in SW. 2Ϫ regulation when they move between FW and SW. It has been suggested that the gills and intestine are almost impermeable to SO 4 2Ϫ (6, 21), but obligatory influx of SO 4 2Ϫ was nullified by excretion via the kidney in marine teleosts (3,7,8,28). We recently showed that the eel is unique in SO 4 2Ϫ regulation compared with other euryhaline teleosts because it has much higher plasma SO 4 2Ϫ in FW (ϳ6 mM) than in SW (ϳ1 mM) (35) as reported previously (23). We also showed that 85% of the SO 4 2Ϫ in SW is taken up by the gills and 97% of SO 4 2Ϫ that enter the circulation is excreted by the kidney in SW eels (Watanabe T, Takei Y, unpublished data).Among members of the solute carrier (Slc) superfamily of transporters, Slc4a1 (AE1), Slc13a1 (NaS-1), Slc26a1 (Sat-1), Slc26a2 (DTDST), Slc26a3 (DRA), Slc26a6 (CFEX, PAT1), Slc26a7, Slc26a8, Slc26a9, and Slc26a11 have been implicated in SO 4 2Ϫ transport in mammals (20). In teleost fish, Slc13a1, Slc26a1, Slc26a3, and Slc26a6a,b,c have been cloned in the eel (23), Slc26a1 in the rainbow trout (14), Slc13a1 in the zebrafish (19), and Slc26a6a,b,c in the pufferfish Takifugu obscurus (13). Among them, Slc13a1 and Slc26a1 play key roles in SO 4 2Ϫ reabsorption at the renal proximal tubule of mammals (5) and FW eels (23). On the other hand, Slc26a6 and Slc26a1 are suggested to be involved in renal SO 4 2Ϫ secretion in mammals (16,20). In fishes, Slc26a1 seems to be involved in renal SO 4 2Ϫ sec...

Vigorous SO42– influxviathe gills is balanced by enhanced SO42– excretion by the kidney in eels after seawater adaptation

“…In fact, the total negative charge of Cl -and SO 4 2-was almost the same in three euryhaline fishes in freshwater and seawater in the present study (data not shown), and plasma Cl -was inversely correlated with plasma SO 4 2-concentration (Watanabe and Takei, 2011b). Thus, freshwater eels appear to have an unusually high tolerance to hypersulfatemia or a unique mechanism to neutralize the toxic effects of excess SO 4 2-.…”

“…Concerning the transcellular pathway, little is known about SO 4 2-transporters and channels in the gills. In the intestine, solute carrier (Slc) 26a6 family members, anion exchangers that potentially transport SO 4 2-, have been identified in the eel (Watanabe and Takei, 2011b) and pufferfish (Kurita et al, 2008). However, Slc26a6 localized on the apical membrane of epithelia may secrete SO 4 2-into the lumen in exchange for Cl -, as has been shown in the proximal tubule of seawater eel kidney (Watanabe and Takei, 2011a).…”

“…It was also shown that Slc26a6 in the seawater fish intestine is involved in the secretion of HCO 3 -into the lumen for CaCO 3 precipitation to decrease luminal fluid osmolality (Grosell, 2011). Slc26a1, which also , was localized abundantly in the basolateral membrane of proximal tubule of eel kidney (Nakada et al, 2005;Watanabe and Takei, 2011b) and in the kidney of other teleost fish (Katoh et al, 2006;Kato et al, 2009), but its gene transcripts were detectable only in the rectum of seawater eels (Watanabe and Takei, 2011b). Judging from the fact that the gills and intestine of seawater eels take up SO 4 2-, unknown SO 4 2-transporters are likely to be present in these tissues.…”

Toxicological perspective on the osmoregulation and ionoregulation physiology of major ions by freshwater animals: Teleost fish, crustacea, aquatic insects, and Mollusca

“…Then, the SO 4 2− is moved across the basolateral membrane by an SO 4 2− /2HCO 3 − -exchanger (SLC26a1), which is energized by an SO 4 2− gradient across the basolateral membrane [ 316 ]. In Japanese eels, SO 4 2− may play a role in osmoregulation in freshwater because serum SO 4 2− is elevated in freshwater (~19 mM vs ~1 mM in saltwater), whereas Cl − is reduced compared with the Japanese eels in saltwater or other fish in freshwater [ 316 , 318 ].…”

Identification and apical membrane localization of an electrogenic Na+/Ca2+exchanger NCX2a likely to be involved in renal Ca2+excretion by seawater fish

“…Therefore, the SW fish kidney is a good model of renal secretion of divalent ions. Recently, Cl Ϫ /SO 4 2Ϫ exchangers Slc26a6A and Slc26a6B were identified as mediating renal SO 4 2Ϫ secretion in seawater (22,(52)(53). However, ion transporters that are involved in renal Mg 2ϩ or Ca 2ϩ secretion have not yet been identified.…”