A facilitative urea transporter is localized in the renal collecting tubule of the dogfish<i>Triakis scyllia</i>

Hyodo, Susumu; Katoh, Fumi; Kaneko, Toyoji; Takei, Yoshiyuki

doi:10.1242/jeb.00773

Cited by 61 publications

(52 citation statements)

References 26 publications

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“…These mechanisms involve passive reabsorption of urea down localized concentration gradients via facilitated urea transporters, and/or active reabsorption via Na ϩ /urea cotransporters (2,26,47). The recent cloning of cDNAs encoding phloretin-sensitive, facilitated urea transporters from the kidneys of a number of elasmobranchs (30,33,34,49) suggests a molecular mechanism for the passive movement of urea across the tubular epithelia. We have identified five transcripts that encode two urea transporter isoforms (strUT-1 and strUT-2) from the kidneys of Atlantic stingrays (33,34).…”

Section: Discussionmentioning

confidence: 99%

Effect of low environmental salinity on plasma composition and renal function of the Atlantic stingray, a euryhaline elasmobranch

Janech¹,

Fitzgibbon²,

Ploth³

et al. 2006

American Journal of Physiology-Renal Physiology

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. Effect of low environmental salinity on plasma composition and renal function of the Atlantic stingray, a euryhaline elasmobranch. Am J Physiol Renal Physiol 291: F770 -F780, 2006. First published April 11, 2006 doi:10.1152/ajprenal.00026.2006.-Marine elasmobranchs maintain internal osmolality higher than their external environment, resulting in an osmotic gradient for branchial water uptake. This gradient is markedly increased in low-salinity habitats. The subsequent increase in water uptake presents a challenge to volume homeostasis. The Atlantic stingray is a marine elasmobranch that inhabits a remarkable range of environmental salinities. We hypothesized that the ability of these stingrays to regulate fluid volume in low-salinity environments is due primarily to a renal glomerular and tubular functional reserve. We tested this hypothesis by measuring renal excretory function after a rapid and sustained 50% reduction in the osmolality of the external medium. Atlantic stingrays were maintained in harbor water [control salinity (CS) ϳ850 mosmol/kgH 2O] for 1 wk. Rays were then either transferred to diluted harbor water [low salinity (LS) ϳ440 mosmol/kgH 2O] or maintained in CS for a further 24 h. Renal excretory function was markedly higher in the rays subjected to low salinity. Glomerular filtration rate was threefold higher and urine flow rate ninefold higher in the LS group. The clearance of solute-free water was greater, and solute-free water comprised a significantly larger proportion of the urine output for the stingrays transferred to dilute harbor water. We conclude that 1) the kidneys of Atlantic stingrays have a remarkable glomerular and tubular functional reserve, and 2) the marked increase in renal function attenuates the increase in fluid volume when these fish move into low-salinity habitats. free water clearance; glomerular filtration rate; tubular urea reabsorption IN GENERAL, MARINE ELASMOBRANCH fishes (sharks, skates, and rays) maintain body fluids hyperosmotic to the ambient environment as part of their osmo-and volume-regulatory strategies. In the ocean, for example, plasma osmolality is 2-10% higher than the osmolality of the surrounding seawater (for review, see Ref. 28), this being due to their ability to maintain high Na ϩ , Cl Ϫ , and urea concentrations in the extracellular fluid (for review, see Refs. 28 and 51).Most species of marine elasmobranchs are confined to marine habitats (9) and only encounter relatively small variations in environmental salinity. However, some species are found in estuaries, as well as marine environments, and therefore can be considered marginally euryhaline (9). Furthermore, a small number of species are euryhaline; i.e., they are able to reside in marine, estuarine, riverine, and even freshwater habitats for extended periods of time. Although, these euryhaline elasmobranchs appear to migrate between habitats on a seasonal basis (48, 54), at least one species, the Atlantic stingray, Dasyatis sabina, can reproduce and complete its life cycle in freshwat...

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Section: Discussionmentioning

confidence: 99%

Effect of low environmental salinity on plasma composition and renal function of the Atlantic stingray, a euryhaline elasmobranch

Janech¹,

Fitzgibbon²,

Ploth³

et al. 2006

American Journal of Physiology-Renal Physiology

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“…UT-A is differentially expressed along the nephron (Shayakul et al, 1996), whereas UT-B is expressed in blood vessel of the descending vasa recta (Xu et al, 1997). In non-mammalian vertebrates, several UT cDNAs, including a novel UT-C, have been isolated from kidneys, urinary bladder and gills (Couriaud et al, 1999;Smith and Wright, 1999;Mistry et al, 2001;Mistry et al, 2005;Hyodo et al, 2004;Konno et al, 2006). Here, we report for the first time the full-length cDNA sequence of a putative UT, whose deduced amino acid sequence shared 70% similarity with UT-A2 from the kidneys of human and mouse, from the buccopharyngeal epithelium of P. sinensis.…”

Section: The Buccopharyngeal Epithelium Is Capable Of Active Urea Excmentioning

confidence: 99%

The Chinese soft-shelled turtle,Pelodiscus sinensis, excretes urea mainly through the mouth instead of the kidney

Loong

Lee

et al. 2012

Journal of Experimental Biology

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SUMMARY The Chinese soft-shelled turtle, Pelodiscus sinensis, is well adapted to aquatic environments, including brackish swamps and marshes. It is ureotelic, and occasionally submerges its head into puddles of water during emersion, presumably for buccopharyngeal respiration. This study was undertaken to test the hypothesis that the buccophyaryngeal cavity constitutes an important excretory route for urea in P. sinensis. Results indicate that a major portion of urea was excreted through the mouth instead of the kidney during immersion. When restrained on land, P. sinensis occasionally submerged their head into water (20–100 min), during which urea excretion and oxygen extraction occurred simultaneously. These results indicate for the first time that buccopharyngeal villiform processes (BVP) and rhythmic pharyngeal movements were involved in urea excretion in P. sinensis. Urea excretion through the mouth was sensitive to phloretin inhibition, indicating the involvement of urea transporters (UTs). In addition, saliva samples collected from the buccopharyngeal surfaces of P. sinensis injected intraperitoneally with saline contained ~36 mmol N l−1 urea, significantly higher than that (~2.4 mmol N l−1) in the plasma. After intraperitoneal injection with 20 μmol urea g−1 turtle, the concentration of urea in the saliva collected from the BVP increased to an extraordinarily high level of ~614 μmol N ml−1, but the urea concentration (~45 μmol N ml−1) in the plasma was much lower, indicating that the buccopharyngeal epithelium of P. sinensis was capable of active urea transport. Subsequently, we obtained from the buccopharyngeal epithelium of P. sinensis the full cDNA sequence of a putative UT, whose deduced amino acid sequence had ~70% similarity with human and mouse UT-A2. This UT was not expressed in the kidney, corroborating the proposition that the kidney had only a minor role in urea excretion in P. sinensis. As UT-A2 is known to be a facilitative urea transporter, it is logical to deduce that it was localized in the basolateral membrane of the buccopharyngeal epithelium, and that another type of primary or secondary active urea transporter yet to be identified was present in the apical membrane. The ability to excrete urea through the mouth instead of the kidney might have facilitated the ability of P. sinensis and other soft-shelled turtles to successfully invade the brackish and/or marine environment.

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“…Hybridization was conducted in ULTRAhyb (Ambion) overnight at 68°C. A second kidney RNA blot was run in parallel and probed using a [␣-32 P]UTP-labeled riboprobe common to the openreading frame of both strUT-1 and strUT-2 (nts 154 to 436), as previously described (16). Hybridized probe was visualized by autoradiography after exposing to film (Kodak-OMAT) for 96 h at Ϫ80°C.…”

Section: Animalsmentioning

confidence: 99%

“…This proposal is supported by the presence of phloretin-sensitive, but not ouabain-sensitive, urea flux across nephron segments located within the peritubular sheath (10). The recent cloning of cDNAs encoding phloretin-sensitive, facilitated urea transporters from the kidneys of a number elasmobranch species has provided a molecular mechanism for the passive movement of urea across the tubular epithelia (13,16,18,36).…”

mentioning

confidence: 99%

“…Although only single cDNAs encoding unique urea transporters have been cloned from the kidneys of elasmobranchs, a number of unidentified transcripts homologous to the cloned urea transporters are expressed in the kidneys and extra-renal tissues of these fish (13,16,18,24,36). These findings indicate that multiple urea transporters isoforms could be expressed in the elasmobranch kidney.…”

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confidence: 99%

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Cloning and functional characterization of a second urea transporter from the kidney of the Atlantic stingray,Dasyatis sabina

Janech¹,

Fitzgibbon²,

Nowak³

et al. 2006

American Journal of Physiology-Regulatory, Integrative and Comp

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. Cloning and functional characterization of a second urea transporter from the kidney of the Atlantic stingray, Dasyatis sabina. Am J Physiol Regul Integr Comp Physiol 291: R844 -R853, 2006. First published April 13, 2006; doi:10.1152/ajpregu.00739.2005.-The cloning of cDNAs encoding facilitated urea transporters (UTs) from the kidneys of the elasmobranchs indicates that in these fish renal urea reabsorption occurs, at least in part, by passive processes. The previously described elasmobranch urea transporter clones from shark (shUT) and stingray (strUT-1) differ from each other primarily because of the COOHterminus of the predicted strUT-1 translation product being extended by 51-amino acid residues compared with shUT. Previously, we noted multiple UT transcripts were present in stingray kidney. We hypothesized that a COOH terminally abbreviated UT isoform, homologous to shUT, would also be present in stingray kidney. Therefore, we used 5Ј/3Ј rapid amplification of cDNA ends to identify a 3ЈUTR-variant (strUT-1a) of the cDNA that encodes (strUT-1), as well as three, 3ЈUTR-variant cDNAs (strUT-2a,b,c) that encode a second phloretinsensitive, urea transporter (strUT-2). The 5ЈUTR and the first 1,132 nucleotides of the predicted coding region of the strUT-2 cDNAs are identical to the strUT-1 cDNAs. The remainder of the coding region contains only five novel nucleotides. The strUT-2 cDNAs putatively encode a 379-amino acid protein, the first 377 amino acids identical to strUT-1 plus 2 additional amino acids. We conclude that 1) a second UT isoform is expressed in the Atlantic stingray and that this isoform is similar in size to the UT previously cloned from the kidney of the dogfish shark, and 2) at least five transcripts encoding the 2 stingray UTs are derived from a single gene product through alternative splicing and polyadenylation. elasmobranch; euryhaline; alternative splicing; osmoregulation MARINE ELASMOBRANCHS (sharks, skates, and rays) use a unique volume-and osmoregulatory strategy; in general, they maintain their body fluids hyperosmotic to the ambient environment (for a review, see Ref. 15; see also 29,42). The high body fluid osmolality is achieved, in large part, by the retention of urea. At ocean salinities, plasma urea concentrations average 350 mmol/l, and urea contributes 30 -50% of the plasma osmolality (for a review, see Ref. 15). The use of this strategy for body fluid volume regulation necessitates the efficient reabsorption of most of the filtered load of urea by the kidneys. For marine elasmobranchs maintained at ocean salinities, fractional urea reabsorption is 90 -98% (9, 14, 34).

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A facilitative urea transporter is localized in the renal collecting tubule of the dogfishTriakis scyllia

Cited by 61 publications

References 26 publications

Effect of low environmental salinity on plasma composition and renal function of the Atlantic stingray, a euryhaline elasmobranch

Effect of low environmental salinity on plasma composition and renal function of the Atlantic stingray, a euryhaline elasmobranch

The Chinese soft-shelled turtle,Pelodiscus sinensis, excretes urea mainly through the mouth instead of the kidney

Cloning and functional characterization of a second urea transporter from the kidney of the Atlantic stingray,Dasyatis sabina

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