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Seawater fish use an electrogenic boric acid transporter, Slc4a11A, for boric acid excretion by the kidney
Boric acid is a vital micronutrient in animals; however, excess amounts are toxic to them. Little is known about whole-body boric acid homeostasis in animals. Seawater (SW) contains 0.4 mM boric acid, and since marine fish drink SW, their urinary system was used here as a model of the boric acid exc...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Biochemistry and Molecular Biology
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9803922/ https://www.ncbi.nlm.nih.gov/pubmed/36435196 http://dx.doi.org/10.1016/j.jbc.2022.102740 |
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author | Kato, Akira Kimura, Yuuri Kurita, Yukihiro Chang, Min-Hwang Kasai, Koji Fujiwara, Toru Hirata, Taku Doi, Hiroyuki Hirose, Shigehisa Romero, Michael F. |
author_facet | Kato, Akira Kimura, Yuuri Kurita, Yukihiro Chang, Min-Hwang Kasai, Koji Fujiwara, Toru Hirata, Taku Doi, Hiroyuki Hirose, Shigehisa Romero, Michael F. |
author_sort | Kato, Akira |
collection | PubMed |
description | Boric acid is a vital micronutrient in animals; however, excess amounts are toxic to them. Little is known about whole-body boric acid homeostasis in animals. Seawater (SW) contains 0.4 mM boric acid, and since marine fish drink SW, their urinary system was used here as a model of the boric acid excretion system. We determined that the bladder urine of a euryhaline pufferfish (river pufferfish, Takifugu obscurus) acclimated to fresh water and SW contained 0.020 and 19 mM of boric acid, respectively (a 950-fold difference), indicating the presence of a powerful excretory renal system for boric acid. Slc4a11 is a potential animal homolog of the plant boron transporter BOR1; however, mammalian Slc4a11 mediates H(+) (OH(−)) conductance but does not transport boric acid. We found that renal expression of the pufferfish paralog of Slc4a11, Slc4a11A, was markedly induced after transfer from fresh water to SW, and Slc4a11A was localized to the apical membrane of kidney tubules. When pufferfish Slc4a11A was expressed in Xenopus oocytes, exposure to media containing boric acid and a voltage clamp elicited whole-cell outward currents, a marked increase in pH(i), and increased boron content. In addition, the activity of Slc4a11A was independent of extracellular Na(+). These results indicate that pufferfish Slc4a11A is an electrogenic boric acid transporter that functions as a B(OH)(4)(−) uniporter, B(OH)(3)-OH(−) cotransporter, or B(OH)(3)/H(+) exchanger. These observations suggest that Slc4a11A is involved in the kidney tubular secretion of boric acid in SW fish, probably induced by the negative membrane potential and low pH of urine. |
format | Online Article Text |
id | pubmed-9803922 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | American Society for Biochemistry and Molecular Biology |
record_format | MEDLINE/PubMed |
spelling | pubmed-98039222023-01-04 Seawater fish use an electrogenic boric acid transporter, Slc4a11A, for boric acid excretion by the kidney Kato, Akira Kimura, Yuuri Kurita, Yukihiro Chang, Min-Hwang Kasai, Koji Fujiwara, Toru Hirata, Taku Doi, Hiroyuki Hirose, Shigehisa Romero, Michael F. J Biol Chem Research Article Boric acid is a vital micronutrient in animals; however, excess amounts are toxic to them. Little is known about whole-body boric acid homeostasis in animals. Seawater (SW) contains 0.4 mM boric acid, and since marine fish drink SW, their urinary system was used here as a model of the boric acid excretion system. We determined that the bladder urine of a euryhaline pufferfish (river pufferfish, Takifugu obscurus) acclimated to fresh water and SW contained 0.020 and 19 mM of boric acid, respectively (a 950-fold difference), indicating the presence of a powerful excretory renal system for boric acid. Slc4a11 is a potential animal homolog of the plant boron transporter BOR1; however, mammalian Slc4a11 mediates H(+) (OH(−)) conductance but does not transport boric acid. We found that renal expression of the pufferfish paralog of Slc4a11, Slc4a11A, was markedly induced after transfer from fresh water to SW, and Slc4a11A was localized to the apical membrane of kidney tubules. When pufferfish Slc4a11A was expressed in Xenopus oocytes, exposure to media containing boric acid and a voltage clamp elicited whole-cell outward currents, a marked increase in pH(i), and increased boron content. In addition, the activity of Slc4a11A was independent of extracellular Na(+). These results indicate that pufferfish Slc4a11A is an electrogenic boric acid transporter that functions as a B(OH)(4)(−) uniporter, B(OH)(3)-OH(−) cotransporter, or B(OH)(3)/H(+) exchanger. These observations suggest that Slc4a11A is involved in the kidney tubular secretion of boric acid in SW fish, probably induced by the negative membrane potential and low pH of urine. American Society for Biochemistry and Molecular Biology 2022-11-23 /pmc/articles/PMC9803922/ /pubmed/36435196 http://dx.doi.org/10.1016/j.jbc.2022.102740 Text en © 2022 The Authors https://creativecommons.org/licenses/by/4.0/This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). |
spellingShingle | Research Article Kato, Akira Kimura, Yuuri Kurita, Yukihiro Chang, Min-Hwang Kasai, Koji Fujiwara, Toru Hirata, Taku Doi, Hiroyuki Hirose, Shigehisa Romero, Michael F. Seawater fish use an electrogenic boric acid transporter, Slc4a11A, for boric acid excretion by the kidney |
title | Seawater fish use an electrogenic boric acid transporter, Slc4a11A, for boric acid excretion by the kidney |
title_full | Seawater fish use an electrogenic boric acid transporter, Slc4a11A, for boric acid excretion by the kidney |
title_fullStr | Seawater fish use an electrogenic boric acid transporter, Slc4a11A, for boric acid excretion by the kidney |
title_full_unstemmed | Seawater fish use an electrogenic boric acid transporter, Slc4a11A, for boric acid excretion by the kidney |
title_short | Seawater fish use an electrogenic boric acid transporter, Slc4a11A, for boric acid excretion by the kidney |
title_sort | seawater fish use an electrogenic boric acid transporter, slc4a11a, for boric acid excretion by the kidney |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9803922/ https://www.ncbi.nlm.nih.gov/pubmed/36435196 http://dx.doi.org/10.1016/j.jbc.2022.102740 |
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