Cloning of rainbow trout SLC26A1: involvement in renal sulfate secretion

Katoh, Fumi; Tresguerres, Martín; Lee, Kyung Mi; Kaneko, Toyoji; Aida, Kô; Goss, Greg G.

doi:10.1152/ajpregu.00482.2005

Cited by 28 publications

(39 citation statements)

References 51 publications

(69 reference statements)

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“…High SO 4 2Ϫ diet induced a decrease in Slc13a1 expression in the renal proximal tubule of mammals (18,26) and injection of Na 2 SO 4 into the circulation increased Slc26a1 transcripts in the kidney of rainbow trout (14), indicating the role of SO 4 2Ϫ in the transporter regulation. It seems that major ions in SW are responsible for changes in the transporter gene expression, but it remains to be determined which ion(s) actually switch the renal SO 4 2Ϫ regulation to a SW type.…”

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confidence: 94%

“…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 secretion in rainbow trout (14), Slc26a6a in pufferfish (13), and Slc26a6a,b,c and Slc26a1 in SW eels (35). However, it is not yet known which factor(s) in SW are responsible for changing the expression of the transporter genes during the course of SW adaptation in euryhaline fishes.…”

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confidence: 99%

“…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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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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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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“…SLC26-related SulP genes are widely distributed among bacterial species (Felce et al 2004;Price et al 2004), in addition to the widespread expression of SLC26 genes among eukaryotic organisms (Mount et al 2004). Vertebrate SLC26 polypeptides transport a wide range of anions, including Cl − , HCO 3 − , iodide, formate, oxalate, and sulfate, and have been implicated in teleost kidney sulfate excretion and osmoregulation (Renfro et al 1999;Nakada et al 2005;Katoh et al 2006). SulP sulfate transporters of plants and yeast have been characterized functionally, and evidence of SulP-mediated HCO 3 − transport has been demonstrated in Synechococcus species (Price et al 2004), but little other functional data on bacterial SulP proteins is available.…”

Section: Introductionmentioning

confidence: 99%

“…Overexpression screening of several bacterial SulP genes revealed inducible, stable accumulation of M. tuberculosis Rv1739c and E. coli ychM. In view of the importance of the SulP gene family in plant (Yoshimoto et al 2007) and yeast (Shibagaki et al 2006), and fish biology (Renfro et al 1999;Nakada et al 2005;Katoh et al 2006), and the significance of the SLC26 gene superfamily in mammalian biology (Mount et al 2004;Markovich et al 2007), and the proposed importance of sulfate in M. tuberculosis pathogenicity (Schelle et al 2006;Fan et al 2007), we investigated further the function of Rv1739c (Fig. 1A) as a candidate sulfate transporter of mycobacteria.…”

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confidence: 99%

Increased sulfate uptake by E. coli overexpressing the SLC26-related SulP protein Rv1739c from Mycobacterium tuberculosis

Zolotarev

Unnikrishnan

Shmukler

et al. 2008

Comparative Biochemistry and Physiology Part A: Molecular &

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Growth and virulence of mycobacteria requires sulfur uptake. The Mycobacterium tuberculosis genome contains, in addition to the ABC sulfate permease cysTWA, three SLC26-related SulP genes of unknown function. We report that induction of Rv1739c expression in E. coli increased bacterial uptake of sulfate, but not Cl − , formate, or oxalate. Uptake was time-dependent, maximal at pH 6.0, and exhibited a K 1/2 for sulfate of 4.0 μM. Na + -independent sulfate uptake was not reduced by bicarbonate, nitrate, or phosphate, but was inhibited by sulfite, selenate, thiosulfate, Nethylmaleimide and carbonyl cyanide 3-chloro-phenylhydrazone. Sulfate uptake was also increased by overexpression of the Rv1739c transmembrane domain, but not of the cytoplasmic C-terminal STAS domain. Mutation to serine of the three cysteine residues of Rv1739c did not affect magnitude, pH-dependence, or pharmacology of sulfate uptake. Expression of Rv1739c in a M. bovis BCG strain lacking the ABC sulfate permease subunit CysA could not complement sulfate auxotrophy. Moreover, inducible expression of Rv1739c in an E. coli strain lacking CysA did not increase sulfate uptake by intact cells. Our data show that facilitation of bacterial sulfate uptake by Rv1739c requires CysA and its associated sulfate permease activity, and suggest that Rv1739c may be a CysTWAdependent sulfate transporter.

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The SoLute Carrier (SLC) Family Series in Teleost Fish

Verri

Terova

Romano

et al. 2012

Functional Genomics in Aquaculture

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Cloning of rainbow trout SLC26A1: involvement in renal sulfate secretion

Abstract: . Cloning of rainbow trout SLC26A1: involvement in renal sulfate secretion.

Cited by 28 publications

References 51 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

Increased sulfate uptake by E. coli overexpressing the SLC26-related SulP protein Rv1739c from Mycobacterium tuberculosis

The SoLute Carrier (SLC) Family Series in Teleost Fish

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Cloning of rainbow trout SLC26A1: involvement in renal sulfate secretion

Abstract: . Cloning of rainbow trout SLC26A1: involvement in renal sulfate secretion.

Cited by 28 publications

References 51 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

Increased sulfate uptake by E. coli overexpressing the SLC26-related SulP protein Rv1739c from Mycobacterium tuberculosis

The SoLute Carrier (SLC) Family Series in Teleost Fish

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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