Boric acid transport activity of marine teleost aquaporins expressed in <i>Xenopus</i> oocytes

Kumagai, Shiori; Watanabe, Eri; Hayashi, Naoko; Kimura, Yuuri; Kamiya, Takehiro; Nagashima, Ayumi; Ushio, Kazutaka; Imaizumi, Genki; Kim, Ju-Hyun; Munakata, Keijiro; Umezawa, Takahiro; Hirose, Shigehisa; Kasai, Koji; Fujiwara, Toru; Romero, Michael F.; Kato, Akira

doi:10.14814/phy2.15655

Cited by 4 publications

(4 citation statements)

References 55 publications

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“…Furthermore, we previously reported that Japanese pufferfish (Takifugu rubripes) Aqp9a transports water, urea, and boric acid, but little glycerol (11), and that the set of amino acids in ar/R was consistent with the tetrapod Aqp10 mutants examined in this study. Additionally, human…”

Section: Discussionsupporting

confidence: 82%

“…Xenopus laevis oocytes were dissociated with collagenase, as previously described (11,12,23), and injected with 50 nL of water or a solution containing 0.5 ng/nL cRNA (25 ng/oocyte) using the Nanoject-II injector (Drummond Scientific, Broomall, PA, USA). Oocytes were incubated in the OR3 medium at 16 °C and observed for 5 d after injection.…”

Section: Expression Of Aqp10s In Xenopus Oocytesmentioning

confidence: 99%

“…OR3 medium (1 L) consisted of 0.7% w/v powdered Leibovitz L-15 medium with L-glutamine (Thermo Fisher Scientific), 50 mL of 10,000 U penicillin and 10,000 U streptomycin solution in 0.9% NaCl (Nacalai Tesque Inc., Kyoto, Japan), and 5 mM HEPES (pH 7.50). The osmolality was adjusted to 200 mOsmol/kg with NaCl powder (11,12,23). The frogs were handled, and the oocytes were harvested as described in the "Cloning of Aqp10s using the human, African clawed frog, gray bichir, zebrafish, and ancestral sequences" section.…”

Section: Expression Of Aqp10s In Xenopus Oocytesmentioning

confidence: 99%

“…Oocyte swelling was monitored using a stereomicroscope (SZX9; Olympus, Tokyo, Japan) equipped with a charge-coupled device camera (DS-Fi2; Nikon, Tokyo, Japan), as previously described (11,12). The oocyte volume was calculated assuming a spherical geometry.…”

Section: Swelling Assaymentioning

confidence: 99%

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Selectivity and evolution of Aqp10 in solute permeability influenced by pore molecular weight

Nagashima,

Ushio,

Nishihara

et al. 2024

Preprint

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Aqp10 is an aquaglyceroporin that transports not only water but also uncharged low-molecular-weight compounds. We previously demonstrated the evolution of solute permeability in Aqp10 paralogs and showed that the urea and boric acid permeabilities of Aqp10.2 were much weaker than those of Aqp10.1 and plesiomorphic Aqp10s. However, the molecular mechanism responsible for the weak permeability of Aqp10.2 to urea and boric acid remains unclear. Herein, we present a novel hypothesis that explains the solute selectivity of Aqp10. We deduced the ancestral sequences of Aqp10.1 and Aqp10.2 paralogs via molecular phylogenetic analysis. Constructed structural models of these sequences revealed that both the well known amino acid site at position 3 and the sum of molecular weights of the four amino acid sites in the ar/R region were important for the formation of the Aqp10 selectivity filter. Site-directed mutagenesis revealed that a decrease in the sum of the molecular weights of the four amino acid sites enhanced the Aqp10 permeability to urea and boric acid. Based on this, we proposed a model in which the presence of two or more bulky amino acids in the ar/R region, which increases the sum of the molecular weights of amino acids in the ar/R region, was essential for the formation of a filter that limited urea and boric acid transport. Our results outline the molecular mechanism by which Aqp10.2 acquired a selectivity filter during evolution and provide structural insights into the narrowly tuned filter responsible for the solute selectivity of aquaglyceroporins.

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Section: Discussionsupporting

confidence: 82%

Section: Expression Of Aqp10s In Xenopus Oocytesmentioning

confidence: 99%

Section: Expression Of Aqp10s In Xenopus Oocytesmentioning

confidence: 99%

Section: Swelling Assaymentioning

confidence: 99%

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Selectivity and evolution of Aqp10 in solute permeability influenced by pore molecular weight

Nagashima,

Ushio,

Nishihara

et al. 2024

Preprint

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Aquaporin water channels: roles beyond renal water handling

Nejsum

2023

Nat Rev Nephrol

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Functional Divergence in Solute Permeability between Ray-Finned Fish-Specific Paralogs of aqp10

Imaizumi,

Ushio,

Nishihara

et al. 2023

Genome Biology and Evolution

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Aquaporin (Aqp) 10 is a member of the aquaglyceroporin subfamily of water channels, and human Aqp10 is permeable to solutes such as glycerol, urea, and boric acid. Tetrapods have a single aqp10 gene, whereas ray-finned fishes have paralogs of this gene through tandem duplication, whole-genome duplication, and subsequent deletion. A previous study on Aqps in the Japanese pufferfish Takifugu rubripes showed that one pufferfish paralog, Aqp10.2b, was permeable to water and glycerol, but not to urea and boric acid. To understand the functional differences of Aqp10 s between humans and pufferfish from an evolutionary perspective, we analyzed Aqp10 s from an amphibian (Xenopus laevis) and a lobe-finned fish (Protopterus annectens), and Aqp10.1 and Aqp10.2 from several ray-finned fishes (Polypterus senegalus, Lepisosteus oculatus, Danio rerio and Clupea pallasii). The expression of tetrapod and lobe-finned fish Aqp10 s and Aqp10.1-derived Aqps in ray-finned fishes in Xenopus oocytes increased the membrane permeabilities to water, glycerol, urea and boric acid. In contrast, Aqp10.2-derived Aqps in ray-finned fishes increased water and glycerol permeabilities, while those of urea and boric acid were much weaker than those of Aqp10.1-derived Aqps. These results indicate that water, glycerol, urea, and boric acid permeability are plesiomorphic activities of Aqp10 s, and that the ray-finned fish-specific Aqp10.2 paralogs have secondarily reduced or lost urea and boric acid permeability.

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

Cited by 4 publications

References 55 publications

Selectivity and evolution of Aqp10 in solute permeability influenced by pore molecular weight

Selectivity and evolution of Aqp10 in solute permeability influenced by pore molecular weight

Aquaporin water channels: roles beyond renal water handling

Functional Divergence in Solute Permeability between Ray-Finned Fish-Specific Paralogs of aqp10

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