Identification of renal transporters involved in sulfate excretion in marine teleost fish

Kato, Akira; Chang, Min; Kurita, Yukihiro; Nakada, Tsutomu; Ogoshi, Maho; Nakazato, Takeru; Doi, Hiroyuki; Hirose, Shigehisa; Romero, Michael F.

doi:10.1152/ajpregu.00228.2009

Cited by 38 publications

(105 citation statements)

References 54 publications

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“…As for the transporters, we chose Slc13a1 and Slc26a6a because they are known to be expressed only in FW and SW eels, respectively (23,35). The higher expression of the Slc26a6a gene in SW is also reported very recently in the euryhaline pufferfish, Takifugu obscurus (13). Since intravascular injection of SO 4 2Ϫ downregulates Slc26a1 in trout (14), we expected that SO 4 2Ϫ may be responsible for the change.…”

Section: Environmental Ions Responsible For Switching So 4 2ϫ Regulationmentioning

confidence: 98%

“…Therefore, NCC is the most likely candidate for Cl Ϫ uptake into the circulation in the presence of Na ϩ . Since injection of Cl Ϫ ion into blood changed the renal SO 4 2Ϫ transporter, the increase may be detected by a Cl Ϫ sensor in the kidney, probably in the proximal tubular cells that are involved in the SO 4 2Ϫ excretion (13,33). However, the pathway of information transfer that leads to changes in SO 4 2Ϫ transporter genes has not yet been identified.…”

Section: Ncc Responsible For CL ϫ Uptake From the Environmentmentioning

confidence: 99%

“…After transfer to SW, Cl Ϫ is taken up from SW in parallel with Na ϩ probably via the NCC, resulting in an transient increase in plasma Cl Ϫ concentration. The increase is detected by an unknown sensor in the circulatory system and turns on the switch for SO 4 2Ϫ excretion by the kidney through downregulating Slc13a1 and upregulating Slc26a6a in the proximal tubules (13,23,35), which facilitates SO 4 2Ϫ excretion into the tubular lumen and decreases plasma SO 4 2Ϫ concentration. We showed that Slc26a6a, Slc26a6b, and Slc26a6c are present on the apical membrane and Slc26a1 on the basolateral membrane of the epithelial cells of proximal tubule of SW eel kidney (35).…”

Section: Ncc Responsible For CL ϫ Uptake From the Environmentmentioning

confidence: 99%

“…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.…”

mentioning

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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confidence: 99%

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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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Section: Environmental Ions Responsible For Switching So 4 2ϫ Regulationmentioning

confidence: 98%

Section: Ncc Responsible For CL ϫ Uptake From the Environmentmentioning

confidence: 99%

Section: Ncc Responsible For CL ϫ Uptake From the Environmentmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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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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Osmoregulation and Excretion

Larsen

Deaton

Onken

et al. 2014

Comprehensive Physiology

185

141

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The article discusses advances in osmoregulation and excretion with emphasis on how multicellular animals in different osmotic environments regulate their milieu intérieur. Mechanisms of energy transformations in animal osmoregulation are dealt with in biophysical terms with respect to water and ion exchange across biological membranes and coupling of ion and water fluxes across epithelia. The discussion of functions is based on a comparative approach analyzing mechanisms that have evolved in different taxonomic groups at biochemical, cellular and tissue levels and their integration in maintaining whole body water and ion homeostasis. The focus is on recent studies of adaptations and newly discovered mechanisms of acclimatization during transitions of animals between different osmotic environments. Special attention is paid to hypotheses about the diversity of cellular organization of osmoregulatory and excretory organs such as glomerular kidneys, antennal glands, Malpighian tubules and insect gut, gills, integument and intestine, with accounts on experimental approaches and methods applied in the studies. It is demonstrated how knowledge in these areas of comparative physiology has expanded considerably during the last two decades, bridging seminal classical works with studies based on new approaches at all levels of anatomical and functional organization. A number of as yet partially unanswered questions are emphasized, some of which are about how water and solute exchange mechanisms at lower levels are integrated for regulating whole body extracellular water volume and ion homeostasis of animals in their natural habitats. © 2014 American Physiological Society.

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Bicarbonate Secreted From the Pancreas Contributed to the Formation of Ca Precipitates in Japanese eel, Anguilla japonica

2012

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Marine teleosts produce Ca precipitates in the intestine as a product of osmoregulation. Ca precipitates are formed by a chemical reaction of Mg(2+) and Ca(2+) derived from ingested seawater with bicarbonate (HCO(3)(-)). It has been reported that HCO(3)(-) originates from the intestine; however, the pancreas is predicted to be another organ that may supply HCO(3)(-) to the intestinal tract. In the present study, the pancreas was surgically removed from Japanese eel to confirm its contribution to Ca precipitate formation. Pancreatectomized eel produced significantly less Ca precipitates than control eel in seawater, indicating that HCO(3)(-) from the pancreas contributes substantially to the formation of Ca precipitates. To further examine the molecular mechanisms of HCO(3)(-) secretion, we cloned cDNAs encoding HCO(3)(-) transporters and identified those transporters that elevated their mRNA expression in the intestine and pancreas following seawater transfer. In the intestine, mRNA expression of Slc26a6A was increased shortly after seawater transfer, whereas Slc26a1 mRNA expression increased gradually following seawater transfer. In the pancreas, Slc26a3 mRNA expression was high during the early stage of seawater acclimation, whereas Slc26a1 expression increased gradually after transfer to seawater. In the intestine and pancreas, therefore, both transient and progressively increasing types of HCO(3)(-) transporters are likely to be involved in HCO(3)(-) secretion into the intestinal lumen in a coordinated manner.

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Identification of renal transporters involved in sulfate excretion in marine teleost fish

Cited by 38 publications

References 54 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

Osmoregulation and Excretion

Bicarbonate Secreted From the Pancreas Contributed to the Formation of Ca Precipitates in Japanese eel, Anguilla japonica

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Identification of renal transporters involved in sulfate excretion in marine teleost fish

Cited by 38 publications

References 54 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

Osmoregulation and Excretion

Bicarbonate Secreted From the Pancreas Contributed to the Formation of Ca Precipitates in Japanese eel, Anguilla japonica

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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