Facilitated NaCl Uptake in the Highly Developed Bundle of the Nephron in Japanese Red Stingray Hemitrygon akajei Revealed by Comparative Anatomy and Molecular Mapping

Aburatani, Naotaka; Takagi, Wataru; Wong, Marty Kwok Sing; Kadota, Mitsutaka; Kuraku, Shigehiro; Tokunaga, Kotaro; Kofuji, Kazuya; Saito, Kazuhiro; Godo, Waichiro; Sakamoto, Tatsuya; Hyodo, Susumu

doi:10.2108/zs200038

Cited by 5 publications

(9 citation statements)

References 38 publications

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“…Recently, we reported that the kidney of Japanese red stingray Hemitrygon akajei has a higher capacity to reabsorb NaCl and urea than that of cloudy catshark Scyliorhinus torazame in SW. The difference in osmolyte compositions of the plasma and urine between stingray and catshark was supported by previous data obtained in little skate Leucoraja erinacea ( Stolte et al, 1977 ), whitespotted bamboo shark Chiloscyllium plagiosum ( Wong and Chan, 1977 ), spiny dogfish Squalus acanthias ( Thurau et al, 1969 ), and bull shark ( Imaseki et al, 2019 ), suggesting that the kidneys of batoids (rays and skates) have higher capacity to reabsorb NaCl and urea than those of selachians (sharks) ( Aburatani et al, 2020 ). The enhanced renal reabsorption is likely related to the anatomical characteristics of the batoid nephrons, where the early distal tubule (EDT) is highly convoluted and coiled around the proximal and collecting tubules ( Aburatani et al, 2020 ).…”

Section: Introductionsupporting

confidence: 78%

“… Expression levels were shown in Transcripts Per Kilobase Million (TPM). *Previously cloned sequence ( Aburatani et al, 2020 ). **Orthology was checked by ORTHOSCOPE ( Inoue and Satoh, 2019 ).…”

Section: Resultsmentioning

confidence: 99%

“…Using qPCR, we subsequently investigated the expression levels of nkcc2 , nkaα1 , urea transporter ( ut ), and ncc that have been reported to be important for NaCl and urea reabsorption of the kidney in cartilaginous fishes ( Hyodo et al, 2014 ; Imaseki et al, 2019 ; Aburatani et al, 2020 ). The expression levels of nkcc2 and nkaα1 mRNAs in the kidney of FW-acclimated stingray were significantly higher than those of SW control individuals (1.7- and 2.6-fold, respectively; Figures 2A, B ).…”

Section: Resultsmentioning

confidence: 99%

“…We previously found that the red stingray possesses a highly convoluted and elongated EDT segment, where NKCC2 and NKA are coexpressed for reabsorbing NaCl from the glomerular filtrate ( Aburatani et al, 2020 ). In the present study, in situ hybridization data demonstrated that nkaα1 and nkcc2 mRNA levels were upregulated in the EDT of the stingray nephron following the acclimation to FW.…”

Section: Discussionmentioning

confidence: 99%

“…A polyethylene cannula (SP-45 or SP-55, Natsume Seisakusyo, Tokyo, Japan) was inserted into the protruded opening of urinary tract and was tied to the surrounding tissue by surgical suture. The other side of cannula was connected and secured to a 2-ml sampling tube where excreted urine was collected into (see also Aburatani et al, 2020 ). Stingrays were recovered from anesthesia by irrigating the gills with aerated holding water and then returned to a 100L-container tank (700 cm × 500 cm × 410 cm) for urine collection.…”

Section: Methodsmentioning

confidence: 99%

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Molecular and morphological investigations on the renal mechanisms enabling euryhalinity of red stingray Hemitrygon akajei

et al. 2022

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Most cartilaginous fishes live in seawater (SW), but a few exceptional elasmobranchs (sharks and rays) are euryhaline and can acclimate to freshwater (FW) environments. The plasma of elasmobranchs is high in NaCl and urea concentrations, which constrains osmotic water loss. However, these euryhaline elasmobranchs maintain high levels of plasma NaCl and urea even when acclimating to low salinity, resulting in a strong osmotic gradient from external environment to body fluid. The kidney consequently produces a large volume of dilute urine to cope with the water influx. In the present study, we investigated the molecular mechanisms of dilute urine production in the kidney of Japanese red stingray, Hemitrygon akajei, transferred from SW to low-salinity environments. We showed that red stingray maintained high plasma NaCl and urea levels by reabsorbing more osmolytes in the kidney when transferred to low salinity. RNA-seq and qPCR analyses were conducted to identify genes involved in NaCl and urea reabsorption under the low-salinity conditions, and the upregulated gene expressions of Na+-K+-Cl- cotransporter 2 (nkcc2) and Na+/K+-ATPase (nka) were found in the FW-acclimated individuals. These upregulations occurred in the early distal tubule (EDT) in the bundle zone of the kidney, which coils around the proximal and collecting tubules to form the highly convoluted structure of batoid nephron. Considering the previously proposed model for urea reabsorption, the upregulation of nkcc2 and nka not only causes the reabsorption of NaCl in the EDT, but potentially also supports enhanced urea reabsorption and eventually the production of dilute urine in FW-acclimated individuals. We propose advantageous characteristics of the batoid-type nephron that facilitate acclimation to a wide range of salinities, which might have allowed the batoids to expand their habitats.

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