Functional and structural characterization of the zebrafish Na<sup>+</sup>-sulfate cotransporter 1 (NaS1) cDNA and gene (<i>slc13a1</i>)

Markovich, Daniel; Romano, Alessandro; Storelli, Carlo; Verri, Tiziano

doi:10.1152/physiolgenomics.90234.2008

Cited by 13 publications

(12 citation statements)

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“…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).…”

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confidence: 99%

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

Watanabe

Takei

2011

American Journal of Physiology-Regulatory, Integrative and Comp

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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...

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confidence: 99%

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

Watanabe

Takei

2011

American Journal of Physiology-Regulatory, Integrative and Comp

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“…Thus, the involvement of the SLC13 and SLC26 family of anion exchangers in cellular selenite transport is a real possibility, as the members of these transporter families are usually implicated in sulfate and sulfite transport (Labotka et al, 1989). It is important to note here that the expression of a Na + -dependent sulfate transporter (SLC13A1) has been found in multiple tissues including the intestine of zebrafish (Danio rerio), and this transporter has also been suggested to be sensitive to anions like selenate and thiosulfate (Markovich et al, 2008). In addition, the sulfate/anion exchanger SLC26A1 has recently been cloned and characterized in rainbow trout kidney (Katoh et al, 2006), although its expression in other tissues has not yet been examined.…”

Section: Discussionmentioning

confidence: 96%

Transport of selenium across the plasma membrane of primary hepatocytes and enterocytes of rainbow trout

Misra

Kwong

Niyogi

2012

Journal of Experimental Biology

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SUMMARYTransport of essential solutes across biological membranes is one of the fundamental characteristics of living cells. Although selenium is an essential micronutrient, little is known about the cellular mechanisms of chemical species-specific selenium transport in fish. We report here the kinetic and pharmacological transport characteristics of selenite and its thiol (glutathione and L-cysteine) derivatives in primary cultures of hepatocytes and isolated enterocytes of rainbow trout. Findings from the current study suggest an apparent low-affinity linear transport system for selenite in both cell types. However, we recorded high-affinity Hill kinetics (K d 3.61±0.28mmoll -1 ) in enterocytes exposed to selenite in the presence of glutathione. The uptake of selenite in the presence of thiols was severalfold higher than uptake of selenite alone (at equimolar concentration) in both hepatocytes and enterocytes. Cellular accumulation of selenium was found to be energy independent. Interestingly, we observed a decrease in selenite transport with increasing pH, whereas selenite uptake increased with increasing pH in the presence glutathione in both cell types. The cellular uptake of selenite demonstrated a pronounced competitive interaction with a structurally similar compound, sulfite. The uptake of selenite as well as its thiol derivatives was found to be sensitive to the anion transport blocker DIDS, irrespective of the cell type. Inorganic mercury (Hg 2+) elicited an inhibition of selenite transport in both cell types, but augmented the transport of reduced forms of selenite in hepatocytes. Based on the substrate choice and comparable pharmacological properties, we advocate that multiple anion transport systems are probably involved in the cellular transport of selenite in fish. Supplementary material available online at

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“…These slc genes encode various transmembrane transporters of anions and cations (e.g., slc13a1, slc5a8, slc12a2, slc12a4, slc26a2).. The apical membrane Na + -sulfate cotransporter encoded by slc13a1 mediates sulfate reabsorption across the renal proximal tubule and intestinal epithelia, promoting osmoregulation in low-salinity waters [32,33]. Similarly, a considerable number of genes were identified encoding energy-dependent ATP-binding transporters (atp1a3, atp2a2, atp2a3) and voltagegated ion channels (scn1b, kcna2/3/10)..…”

Section: Genome-wide Selective Sweep Analysismentioning

confidence: 99%

Adaptive evolution of low salinity tolerance and hypoosmotic regulation in a euryhaline teleost, Takifugu obscurus

Zhang

Hou

Liu

et al. 2019

Preprint

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Background The mechanism of osmoregulation is crucial for maintaining growth, development, and life activities in teleosts. Takifugu obscurus, the only euryhaline species in the genus Takifugu, is a proper model organism for studying the mechanism of low salt-tolerance and hypoosmotic regulation.Results In this study, whole genome sequencing data were obtained from 90 pufferfish representing five species within this genus, T. rubripes, T. obscurus, T. flavidus, T. niphobles, and T. bimaculatus. Using a phylogeny, PCA, and population structure analyses, we observed similar amounts of population genetic differentiation among species. The five species are closely related to each other and have differentiated within a relatively short period, while T. bimaculatus and T. flavidus shared the most similar genetic backgrounds. We further identified hundreds of genes under selection related to hypoosmotic regulation between T. obscurus and other Takifugu species, including 16 representative genes involving ion transporters ( atp1a3 , atp2a2 , atp2a3 , slc13a1 , slc5a8 , slc12a2 , slc12a4 , slc26a2 , scn1b , and kcna 2/3/10), genes involved in hormone regulation ( fyn , prlr , and grb2 ), and a gene associated with water absorption ( aqp3 ). Conclusions: Our findings provide preliminary insight into the mechanism of osmoregulation and will facilitate follow-up validation of candidate genes related to osmoregulation in T. obscurus .

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Functional and structural characterization of the zebrafish Na⁺-sulfate cotransporter 1 (NaS1) cDNA and gene (slc13a1)

Cited by 13 publications

References 32 publications

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

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

Transport of selenium across the plasma membrane of primary hepatocytes and enterocytes of rainbow trout

Adaptive evolution of low salinity tolerance and hypoosmotic regulation in a euryhaline teleost, Takifugu obscurus

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Functional and structural characterization of the zebrafish Na+-sulfate cotransporter 1 (NaS1) cDNA and gene (slc13a1)

Cited by 13 publications

References 32 publications

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

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

Transport of selenium across the plasma membrane of primary hepatocytes and enterocytes of rainbow trout

Adaptive evolution of low salinity tolerance and hypoosmotic regulation in a euryhaline teleost, Takifugu obscurus

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Functional and structural characterization of the zebrafish Na⁺-sulfate cotransporter 1 (NaS1) cDNA and gene (slc13a1)

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

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