Regulation of a renal urea transporter with reduced salinity in a marine elasmobranch,<i>Raja erinacea</i>

Morgan, Robyn L.; Ballantyne, James S.; Wright, Patricia A.

doi:10.1242/jeb.00554

Cited by 52 publications

(34 citation statements)

References 33 publications

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“…Our finding that the expression of only one of the strUT-2 transcripts was lower after exposure to low salinity contrasts to the finding that the expression of all three transcripts homologous to a skate urea transporter were lower in the kidneys of little skates exposed to 50% seawater compared with those in 100% seawater (24). Interestingly, renal urea transporter expression was not different between spiny dogfish sharks exposed to 75% seawater or maintained in 100% seawater (27).…”

Section: Discussioncontrasting

confidence: 83%

“…Although, this increase in the filtered load is to a large extent balanced by increased tubular reabsorption, fractional reabsorption of urea is lower in elasmobranchs exposed to low salinity (66 -84%). The finding that kidney urea transporter RNA abundance was lower in marginally euryhaline skates, Raja erinacea exposed to low salinity for 5 days than that in the kidneys of skates at high salinity, has led to the proposal that decreased expression of facilitated urea transporter gene expression contributes at least in part, to the decrease in fractional urea reabsorption (24). We have previously observed that the euryhaline, Atlantic stingrays exposed to a 50% reduction in salinity for 24 h have lower fractional urea reabsorption (84%) compared with rays maintained at high salinity (96%).…”

Section: Discussionmentioning

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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Section: Discussioncontrasting

confidence: 83%

Section: Discussionmentioning

confidence: 99%

mentioning

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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“…These fish appear to be nitrogen limited (Haywood, 1973;Wood et al, 2005;Kajimura et al, 2006;Kajimura et al, 2008), exhibiting elaborate urea-retention mechanisms at the gills (Boylan, 1967;Pärt et al, 1998;Fines et al, 2001;Wood et al, 2013a) and kidney (Schmidt-Nielsen et al, 1972;Morgan et al, 2003a;Morgan et al, 2003b). Nevertheless, there is still substantial urea leakage across the gills, so elasmobranchs are predominantly ureotelic, excreting very little ammonia.…”

Section: Introductionmentioning

confidence: 99%

Physiological and molecular responses of the spiny dogfish shark (Squalus acanthias) to high environmental ammonia: scavenging for nitrogen

Walsh

Wood

2015

Journal of Experimental Biology

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In teleosts, a branchial metabolon links ammonia excretion to Na + uptake via Rh glycoproteins and other transporters. Ureotelic elasmobranchs are thought to have low branchial ammonia permeability, and little is known about Rh function in this ancient group. We cloned Rh cDNAs (Rhag, Rhbg and Rhp2) and evaluated gill ammonia handling in Squalus acanthias. Control ammonia excretion was <5% of urea-N excretion. Sharks exposed to high environmental ammonia (HEA; 1 mmol −1 NH 4 HCO 3 ) for 48 h exhibited active ammonia uptake against partial pressure and electrochemical gradients for 36 h before net excretion was reestablished. Plasma total ammonia rose to seawater levels by 2 h, but dropped significantly below them by 24-48 h. Control ΔP NH3 (the partial pressure gradient of NH 3 ) across the gills became even more negative (outwardly directed) during HEA. Transepithelial potential increased by 30 mV, negating a parallel rise in the Nernst potential, such that the outwardly directed NH 4 + electrochemical gradient remained unchanged. Urea-N excretion was enhanced by 90% from 12 to 48 h, more than compensating for ammonia-N uptake. Expression of Rhp2 (gills, kidney) and Rhbg (kidney) did not change, but branchial Rhbg and erythrocytic Rhag declined during HEA. mRNA expression of branchial Na + /K + -ATPase (NKA) increased at 24 h and that of H + -ATPase decreased at 48 h, while expression of the potential metabolon components Na + /H + exchanger2 (NHE2) and carbonic anhydrase IV (CA-IV) remained unchanged. We propose that the gill of this nitrogen-limited predator is poised not only to minimize nitrogen loss by low efflux permeability to urea and ammonia but also to scavenge ammonia-N from the environment during HEA to enhance urea-N synthesis.KEY WORDS: Elasmobranchs, Rh glycoproteins, Gene expression, Urea, Gills, Ornithine-urea cycle, Transepithelial potential, P NH3 gradient INTRODUCTIONThe discovery that Rhesus (Rh) glycoproteins are expressed in the gills (Nakada et al., 2007;Nawata et al., 2007) has created a new understanding of the mechanisms of ammonia excretion in teleosts RESEARCH ARTICLE 1 Bamfield Marine Sciences Centre, 100 Pachena Road, Bamfield, BC, Canada V0R 1B0. (reviewed by Wright and Wood, 2009;Wright and Wood, 2012;Weihrauch et al., 2009). These channel proteins appear to facilitate the diffusion of NH 3 along P NH 3 (partial pressure of NH 3 ) gradients (Nawata et al., 2010b) and in the gills they function as part of a metabolon which flexibly couples ammonia excretion to Na + uptake (Tsui et al., 2009;Ito et al., 2013). The theory proposes that the deprotonation of NH 4 + as NH 3 enters the apical Rh channel creates a source of protons to fuel Na + uptake via Na + /H + exchangers (NHEs) and/or via a coupled Na + channel/V-type H + -ATPase system, while at the same time the NH 3 leaving the Rh channel traps protons, thereby creating an external microenvironment in which [H + ] is less concentrated. This mechanism becomes particularly prominent during chronic exposure to high enviro...

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“…Active urea transport processes have been described in a variety of tissues, which include: (1) Na + -linked active urea transport in the renal tubule (Schmidt-Nielsen et al, 1972;Morgan et al, 2003a;Morgan et al, 2003b) and gills (Fines et al, 2001) of the spiny dogfish, Squalus acanthias; (2) phloretin-inhibitable active urea secretion in rabbit proximal straight tubules (Kawamura and Kokko, 1976); (3) H + -dependent and/or phloretin-inhibitable active urea transport in the skins of Bufo bufo, Bufo marinus, Bufo viridis and Rana esculenta (Ussing and Johansen, 1969;GarciaRomeu et al, 1981;Rapoport et al, 1988;Lacoste et al, 1991;Dytko et al, 1993); (4) active urea transport in kidney tubules from dogs (Goldberg et al, 1967;Beyer and Gelarden, 1988) and frogs (Forster, 1954;Schmidt-Nielsen and Shrauger, 1963); (5) active urea transport in the yeast Saccharomyces cerevisiae (Pateman et al, 1982;ElBerry et al, 1993); and (6) active urea transport in bacteria (Jahns et al, 1988). However, to date, molecular characterizations of these active UTs have not been performed and therefore a molecular understanding of these transporters in comparison of UT-A, UT-B and UT-C is not possible at present.…”

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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Regulation of a renal urea transporter with reduced salinity in a marine elasmobranch,Raja erinacea

Cited by 52 publications

References 33 publications

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

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

Physiological and molecular responses of the spiny dogfish shark (Squalus acanthias) to high environmental ammonia: scavenging for nitrogen

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

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