Nagashima A et al. (2025), Retention and pseudogenization of aquaporin-10 ...

XB-ART-61298

Biochem Biophys Res Commun 2025 Mar 05;756:151608. doi: 10.1016/j.bbrc.2025.151608.

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Retention and pseudogenization of aquaporin-10 in Rodentia.

Nagashima A , Nagai N , Ota C , Ushio K , Kato A .

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Vertebrates exhibit diversity in the presence and number of aquaporin (Aqp)-10 genes. In Rodentia, mice possess an Aqp10 pseudogene, whereas guinea pigs possess an intact Aqp10. However, Aqp10 retention and pseudogenization history in various rodent lineages remains unclear. Therefore, in this study, we aimed to investigate the molecular evolution of Aqp10 using the recent increasingly decoded rodent genome sequences. We analyzed Aqp10 in the genomes of 43 rodent species belonging to 14 families and found that Aqp10 was pseudogenized in 13 species of three families in the Myomorpha suborder. In contrast, a single intact Aqp10 was retained in the other 30 rodent species, with no Aqp10 pseudogene found in the Castorimorpha, Hystricomorpha, and Sciuromorpha suborders. Additionally, we investigated the tissue expression levels of aquaglyceroporin genes in guinea pigs and rats via reverse transcription-polymerase chain reaction and detected Aqp10 expression in the guinea pig intestines. Notably, none of the examined rat organs expressed Aqp10; however, Aqp7 was expressed in the rat intestines. In situ hybridization showed that guinea pig Aqp10 was expressed in the intestinal epithelial cells. Moreover, AQP10 was permeable to water, glycerol, urea, and boric acid in Xenopus oocytes. Overall, these results clarify the Aqp10 pseudogenization history in Rodentia and suggest guinea pigs as excellent small animal models to analyze the intestinal AQP10 functions.

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Species referenced: Xenopus laevis
Genes referenced: actb aqp1 aqp10 aqp11 aqp12a aqp2 aqp3 aqp4 aqp5 aqp7 aqp8 aqp9

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	Fig. 1. Retention and pseudogenization of aquaporin (Aqp)-10 in Rodentia. Presence of Aqp10 or pseudogenized Aqp10 (Aqp10p) in 43 rodent species and rabbits are shown. (A) Phylogenetic relationship of 43 rodent species analyzed in this study. Divergence times were retrieved from the TimeTree database (http://www.timetree.org/). Rabbits were analyzed as a related species not included in the Rodentia order. (B) Synteny of Aqp10 and Aqp10p in various rodent species. Synteny conservation of the region surrounding Aqp10 is also shown. Genomic regions used for synteny analyses are listed in Table S2. (C) Aqp10 pseudogenization in several rodent species. Open reading frames divided into six exons are indicated by blue boxes. Deleted regions are indicated by open boxes. Nonsense and frameshift mutations are indicated by red and yellow bars, respectively. Supporting data for dot plot analyses and nucleotide sequence alignment are shown in Figs. S1–2. (D) The nonsynonymous and synonymous nucleotide substitution rates (dN and dS, respectively) among intact Aqp10. The mean distance values within groups for dN, dS, and dN/dS were calculated based on the NG method. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
	Fig. 2. Tissue distribution of Aqps in guinea pigs and rats. (A) Expression profiles of Aqp10 and other Aqp genes in guinea pig tissues were analyzed via semi-quantitative reverse transcription-polymerase chain reaction (RT-PCR). Pseudo-gel images of PCR products were generated using a microchip electrophoresis system. β-actin (Actb) was used as an internal control. Whole images of the gels are shown in Fig. S4. (B) Expression profiles of Aqp10 and related aquaglyceroporin genes in rat tissues were analyzed via semi-quantitative RT-PCR. Actb was used as an internal control. Whole images of the gels are shown in Fig. S5. (C) In situ hybridization of Aqp10 in guinea pig small intestines. Sense probes did not show any labeling. L, lumen. (D) Water and solute (glycerol, urea, and boric acid) permeabilities of guinea pig AQP10 were measured using a swelling assay. Change in volume was compared between the AQP10-expressing and control oocytes. Values are presented as interquartile ranges from the 25th to 75th percentiles (box), ranges (whiskers), outliers (>1.5 × interquartile range above the upper quartile), and medians (line in the box). Mean values, standard deviations, and total number of assayed oocytes are presented in Table S5. Statistical significance was evaluated via an unpaired t-test (∗∗∗∗P < 0.0001).
	Supplementary Fig. S1. Dot plot analyses of Aqp10 pseudogenes in Rodentia The Aqp10 gene and its flanking regions in comparison with the corresponding genome regions of various Rodentia species are shown. Homologous regions were plotted with dotmatcher program (window size: 20; threshold: 70).
	Supplementary Fig. S1. Dot plot analyses of Aqp10 pseudogenes in Rodentia The Aqp10 gene and its flanking regions in comparison with the corresponding genome regions of various Rodentia species are shown. Homologous regions were plotted with dotmatcher program (window size: 20; threshold: 70).
	Supplementary Fig. S1. Dot plot analyses of Aqp10 pseudogenes in Rodentia The Aqp10 gene and its flanking regions in comparison with the corresponding genome regions of various Rodentia species are shown. Homologous regions were plotted with dotmatcher program (window size: 20; threshold: 70).
	Supplementary Fig. S2. Multiple alignment of Aqp10 pseudogenes (Aqp10p). The nucleotide sequences of six exons for Aqp10p were aligned with Chinese hamster Aqp10. Nonsense mutations and frame shifts are indicated by red markers.
	Supplementary Fig. S2. Multiple alignment of Aqp10 pseudogenes (Aqp10p). The nucleotide sequences of six exons for Aqp10p were aligned with Chinese hamster Aqp10. Nonsense mutations and frame shifts are indicated by red markers.
	Supplementary Fig. S2. Multiple alignment of Aqp10 pseudogenes (Aqp10p). The nucleotide sequences of six exons for Aqp10p were aligned with Chinese hamster Aqp10. Nonsense mutations and frame shifts are indicated by red markers.
	Supplementary Fig. S2. Multiple alignment of Aqp10 pseudogenes (Aqp10p). The nucleotide sequences of six exons for Aqp10p were aligned with Chinese hamster Aqp10. Nonsense mutations and frame shifts are indicated by red markers.
	Supplementary Fig. S2. Multiple alignment of Aqp10 pseudogenes (Aqp10p). The nucleotide sequences of six exons for Aqp10p were aligned with Chinese hamster Aqp10. Nonsense mutations and frame shifts are indicated by red markers.
	Supplementary Fig. S2. Multiple alignment of Aqp10 pseudogenes (Aqp10p). The nucleotide sequences of six exons for Aqp10p were aligned with Chinese hamster Aqp10. Nonsense mutations and frame shifts are indicated by red markers.
	Supplementary Fig. S2. Multiple alignment of Aqp10 pseudogenes (Aqp10p). The nucleotide sequences of six exons for Aqp10p were aligned with Chinese hamster Aqp10. Nonsense mutations and frame shifts are indicated by red markers.
	Supplementary Fig. S2. Multiple alignment of Aqp10 pseudogenes (Aqp10p). The nucleotide sequences of six exons for Aqp10p were aligned with Chinese hamster Aqp10. Nonsense mutations and frame shifts are indicated by red markers.
	Supplementary Fig. S2. Multiple alignment of Aqp10 pseudogenes (Aqp10p). The nucleotide sequences of six exons for Aqp10p were aligned with Chinese hamster Aqp10. Nonsense mutations and frame shifts are indicated by red markers.
	Supplementary Fig. S2. Multiple alignment of Aqp10 pseudogenes (Aqp10p). The nucleotide sequences of six exons for Aqp10p were aligned with Chinese hamster Aqp10. Nonsense mutations and frame shifts are indicated by red markers.
	Supplementary Fig. S2. Multiple alignment of Aqp10 pseudogenes (Aqp10p). The nucleotide sequences of six exons for Aqp10p were aligned with Chinese hamster Aqp10. Nonsense mutations and frame shifts are indicated by red markers.
	Supplementary Fig. S2. Multiple alignment of Aqp10 pseudogenes (Aqp10p). The nucleotide sequences of six exons for Aqp10p were aligned with Chinese hamster Aqp10. Nonsense mutations and frame shifts are indicated by red markers.
	Supplementary Fig. S3. Phylogenetic analysis of AQPs in guinea pig, rat, mouse, and human. The amino acid sequences of AQPs were aligned using ClustalW software. A phylogenetic tree was constructed using the maximum-likelihood method and MEGA software. Numbers indicate bootstrap values, and the scale bar represents the genetic distance of amino acid substitutions per site.
	Supplementary Fig. S4. Whole images of a Microchip Electrophoresis system for RT-PCR analysis of guinea pig Aqp. Expression profiles of Aqp10 and the other aquaporin genes in guinea pig tissues were determined using semiquantitative RT-PCR. Pseudo-gel images of the PCR products were generated using a microchip electrophoresis system for DNA/RNA Analysis MCE-202 MultiNA.
	Supplementary Fig. S4. Whole images of a Microchip Electrophoresis system for RT-PCR analysis of guinea pig Aqp. Expression profiles of Aqp10 and the other aquaporin genes in guinea pig tissues were determined using semiquantitative RT-PCR. Pseudo-gel images of the PCR products were generated using a microchip electrophoresis system for DNA/RNA Analysis MCE-202 MultiNA.
	Supplementary Fig. S5. Whole images of a Microchip Electrophoresis system for RT-PCR analysis of rat Aqp. Expression profiles of Aqp10 and the other aquaglyceroporin genes in rat tissues were determined using semiquantitative RT-PCR. Pseudo-gel images of the PCR products were generated using a microchip electrophoresis system for DNA/RNA Analysis MCE-202 MultiNA.