Boric acid transport activity of marine teleost aquaporins expressed in Xenopus oocytes

Author:

Kumagai Shiori1,Watanabe Erika1,Hayashi Naoko2,Kimura Yuuri2,Kamiya Takehiro3,Nagashima Ayumi1ORCID,Ushio Kazutaka1ORCID,Imaizumi Genki1,Kim Juhyun1,Munakata Keijiro12,Umezawa Takahiro2,Hirose Shigehisa2,Kasai Koji3,Fujiwara Toru3,Romero Michael F.456ORCID,Kato Akira1247ORCID

Affiliation:

1. School of Life Science and Technology Tokyo Institute of Technology Yokohama Japan

2. Graduate School of Bioscience and Biotechnology Tokyo Institute of Technology Yokohama Japan

3. Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences The University of Tokyo Tokyo Japan

4. Department of Physiology and Biomedical Engineering Mayo Clinic College of Medicine Rochester Minnesota United States

5. Nephrology & Hypertension Mayo Clinic College of Medicine Rochester Minnesota United States

6. O'Brien Urology Research Center Mayo Clinic College of Medicine Rochester Minnesota United States

7. Center for Biological Resources and Informatics Tokyo Institute of Technology Yokohama Japan

Abstract

AbstractMarine teleosts ingest large amounts of seawater containing various ions, including 0.4 mM boric acid, which can accumulate at toxic levels in the body. However, the molecular mechanisms by which marine teleosts absorb and excrete boric acid are not well understood. Aquaporins (Aqps) are homologous to the nodulin‐like intrinsic protein (NIP) family of plant boric acid channels. To investigate the potential roles of Aqps on boric acid transport across the plasma membrane in marine teleosts, we analyzed the function of Aqps of Japanese pufferfish (Takifugu rubripes) expressed in Xenopus laevis oocytes. Takifugu genome database contains 16 genes encoding the aquaporin family members (aqp0a, aqp0b, aqp1aa, aqp1ab, aqp3a, aqp4a, aqp7, aqp8bb, aqp9a, aqp9b, aqp10aa, aqp10bb, aqp11a, aqp11b, aqp12, and aqp14). When T. rubripes Aqps (TrAqps) were expressed in X. laevis oocytes, a swelling assay showed that boric acid permeability was significantly increased in oocytes expressing TrAqp3a, 7, 8bb, 9a, and 9b. The influx of boric acid into these oocytes was also confirmed by elemental quantification. Electrophysiological analysis using a pH microelectrode showed that these TrAqps increase B(OH)3 permeability. These results indicate that TrAqp3a, 7, 8bb, 9a, and 9b act as boric acid transport systems, likely as channels, in marine teleosts.

Funder

Japan Society for the Promotion of Science

National Institutes of Health

Publisher

Wiley

Subject

Physiology (medical),Physiology

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