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

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

Research output: Contribution to journalArticle

27 Citations (Scopus)

Abstract

Sulfate (SO4 2-) is the second most abundant anion in seawater (SW), and excretion of excess SO4 2- from ingested SW is essential for marine fish to survive. Marine teleosts excrete SO 4 2- via the urine produced in the kidney. The SO 4 2- transporter that secretes and concentrates SO 4 2- in the urine has not previously been identified. Here, we have identified and characterized candidates for the long-sought transporters. Using sequences from the fugu database, we have cloned cDNA fragments of all transporters belonging to the Slc13 and Slc26 families from mefugu (Takifugu obscurus). We compared Slc13 and Slc26 mRNA expression in the kidney between freshwater (FW) and SW mefugu. Among 14 clones examined, the expression of a Slc26a6 paralog (mfSlc26a6A) was the most upregulated (30-fold) in the kidney of SW mefugu. Electrophysiological analyses of Xenopus oocytes expressing mfSlc26a6A, mfSlc26a6B, and mouse Slc26a6 (mSlc26a6) demonstrated that all transporters mediate electrogenic Cl-/SO4 2-, Cl-/oxalate2-, and Cl-/nHCO 3 - exchanges and electroneutral Cl-/ formate- exchange. Two-electrode voltage-clamp experiments demonstrated that the SO4 2--elicited currents of mfSlc26a6A is quite large (∼35 μA at +60 mV) and 50- to 200-fold higher than those of mfSlc26a6B and mSlc26a6. Conversely, the currents elicited by oxalate and HCO3 - are almost identical among mfSlc26a6A, mfSlc26a6B, and mSlc26a6. Kinetic analysis revealed that mfSlc26a6A has the highest SO4 2- affinity as well as capacity. Immunohistochemical analyses demonstrated that mfSlc26a6A localizes to the apical (brush-border) region of the proximal tubules. Together, these findings suggest that mfSlc26a6A is the most likely candidate for the major apical SO4 2- transporter that mediates SO4 2- secretion in the kidney of marine teleosts.

Original languageEnglish
JournalAmerican Journal of Physiology - Regulatory Integrative and Comparative Physiology
Volume297
Issue number6
DOIs
Publication statusPublished - Dec 2009
Externally publishedYes

Fingerprint

Seawater
Sulfates
Fishes
Takifugu
Kidney
formic acid
Urine
Oxalates
Microvilli
Xenopus
Fresh Water
Oocytes
Anions
Electrodes
Complementary DNA
Clone Cells
Databases
Messenger RNA

Keywords

  • Mefugu
  • Oxalate
  • Proximal tubule
  • Slc13
  • Slc26
  • Sulfate homeostasis

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

Cite this

Identification of renal transporters involved in sulfate excretion in marine teleost fish. / Kato, Akira; Chang, Min Hwang; Kurita, Yukihiro; Nakada, Tsutomu; Ogoshi, Maho; Nakazato, Takeru; Doi, Hiroyuki; Hirose, Shigehisa; Romero, Michael F.

In: American Journal of Physiology - Regulatory Integrative and Comparative Physiology, Vol. 297, No. 6, 12.2009.

Research output: Contribution to journalArticle

Kato, Akira ; Chang, Min Hwang ; Kurita, Yukihiro ; Nakada, Tsutomu ; Ogoshi, Maho ; Nakazato, Takeru ; Doi, Hiroyuki ; Hirose, Shigehisa ; Romero, Michael F. / Identification of renal transporters involved in sulfate excretion in marine teleost fish. In: American Journal of Physiology - Regulatory Integrative and Comparative Physiology. 2009 ; Vol. 297, No. 6.
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AU - Ogoshi, Maho

AU - Nakazato, Takeru

AU - Doi, Hiroyuki

AU - Hirose, Shigehisa

AU - Romero, Michael F.

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N2 - Sulfate (SO4 2-) is the second most abundant anion in seawater (SW), and excretion of excess SO4 2- from ingested SW is essential for marine fish to survive. Marine teleosts excrete SO 4 2- via the urine produced in the kidney. The SO 4 2- transporter that secretes and concentrates SO 4 2- in the urine has not previously been identified. Here, we have identified and characterized candidates for the long-sought transporters. Using sequences from the fugu database, we have cloned cDNA fragments of all transporters belonging to the Slc13 and Slc26 families from mefugu (Takifugu obscurus). We compared Slc13 and Slc26 mRNA expression in the kidney between freshwater (FW) and SW mefugu. Among 14 clones examined, the expression of a Slc26a6 paralog (mfSlc26a6A) was the most upregulated (30-fold) in the kidney of SW mefugu. Electrophysiological analyses of Xenopus oocytes expressing mfSlc26a6A, mfSlc26a6B, and mouse Slc26a6 (mSlc26a6) demonstrated that all transporters mediate electrogenic Cl-/SO4 2-, Cl-/oxalate2-, and Cl-/nHCO 3 - exchanges and electroneutral Cl-/ formate- exchange. Two-electrode voltage-clamp experiments demonstrated that the SO4 2--elicited currents of mfSlc26a6A is quite large (∼35 μA at +60 mV) and 50- to 200-fold higher than those of mfSlc26a6B and mSlc26a6. Conversely, the currents elicited by oxalate and HCO3 - are almost identical among mfSlc26a6A, mfSlc26a6B, and mSlc26a6. Kinetic analysis revealed that mfSlc26a6A has the highest SO4 2- affinity as well as capacity. Immunohistochemical analyses demonstrated that mfSlc26a6A localizes to the apical (brush-border) region of the proximal tubules. Together, these findings suggest that mfSlc26a6A is the most likely candidate for the major apical SO4 2- transporter that mediates SO4 2- secretion in the kidney of marine teleosts.

AB - Sulfate (SO4 2-) is the second most abundant anion in seawater (SW), and excretion of excess SO4 2- from ingested SW is essential for marine fish to survive. Marine teleosts excrete SO 4 2- via the urine produced in the kidney. The SO 4 2- transporter that secretes and concentrates SO 4 2- in the urine has not previously been identified. Here, we have identified and characterized candidates for the long-sought transporters. Using sequences from the fugu database, we have cloned cDNA fragments of all transporters belonging to the Slc13 and Slc26 families from mefugu (Takifugu obscurus). We compared Slc13 and Slc26 mRNA expression in the kidney between freshwater (FW) and SW mefugu. Among 14 clones examined, the expression of a Slc26a6 paralog (mfSlc26a6A) was the most upregulated (30-fold) in the kidney of SW mefugu. Electrophysiological analyses of Xenopus oocytes expressing mfSlc26a6A, mfSlc26a6B, and mouse Slc26a6 (mSlc26a6) demonstrated that all transporters mediate electrogenic Cl-/SO4 2-, Cl-/oxalate2-, and Cl-/nHCO 3 - exchanges and electroneutral Cl-/ formate- exchange. Two-electrode voltage-clamp experiments demonstrated that the SO4 2--elicited currents of mfSlc26a6A is quite large (∼35 μA at +60 mV) and 50- to 200-fold higher than those of mfSlc26a6B and mSlc26a6. Conversely, the currents elicited by oxalate and HCO3 - are almost identical among mfSlc26a6A, mfSlc26a6B, and mSlc26a6. Kinetic analysis revealed that mfSlc26a6A has the highest SO4 2- affinity as well as capacity. Immunohistochemical analyses demonstrated that mfSlc26a6A localizes to the apical (brush-border) region of the proximal tubules. Together, these findings suggest that mfSlc26a6A is the most likely candidate for the major apical SO4 2- transporter that mediates SO4 2- secretion in the kidney of marine teleosts.

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KW - Slc26

KW - Sulfate homeostasis

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