Physiological and immunocytochemical evidence for a putative H-K-ATPase in elasmobranch renal acid secretion

Swenson, Erik R.; Fine, Adrian; Maren, Thomas H.; Reale, E.; Lacy, Eric R.; Smolka, Adam J.

doi:10.1152/ajprenal.1994.267.4.f639

Cited by 7 publications

(6 citation statements)

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“…The acidification in the proximal tubule was also found in the little skate (23). In spiny dogfish, infusion of an inhibitor for mammalian gastric H ϩ -K ϩ -ATPase Sch28080 abolished over 80% of basal acid excretion, implying that H ϩ -K ϩ -ATPasedependent mechanism(s) for urine acidification exist in the elasmobranch kidney (108). These authors conducted immunohistochemistry using an antibody directed against the COOH-terminus of porcine gastric H ϩ -K ϩ -ATPase ␣-subunit and found that the apical and basolateral membranes of many nephron segments were stained with the antibody.…”

Section: Urea Synthesis In the Kidneymentioning

confidence: 89%

Morphological and functional characteristics of the kidney of cartilaginous fishes: with special reference to urea reabsorption

Hyodo

Kakumura

Takagi

et al. 2014

American Journal of Physiology-Regulatory, Integrative and Comp

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functional characteristics of the kidney of cartilaginous fishes: with special reference to urea reabsorption. Am J Physiol Regul Integr Comp Physiol 307: R1381-R1395, 2014. First published October 22, 2014 doi:10.1152/ajpregu.00033.2014.-For adaptation to highsalinity marine environments, cartilaginous fishes (sharks, skates, rays, and chimaeras) adopt a unique urea-based osmoregulation strategy. Their kidneys reabsorb nearly all filtered urea from the primary urine, and this is an essential component of urea retention in their body fluid. Anatomical investigations have revealed the extraordinarily elaborate nephron system in the kidney of cartilaginous fishes, e.g., the four-loop configuration of each nephron, the occurrence of distinct sinus and bundle zones, and the sac-like peritubular sheath in the bundle zone, in which the nephron segments are arranged in a countercurrent fashion. These anatomical and morphological characteristics have been considered to be important for urea reabsorption; however, a mechanism for urea reabsorption is still largely unknown. This review focuses on recent progress in the identification and mapping of various pumps, channels, and transporters on the nephron segments in the kidney of cartilaginous fishes. The molecules include urea transporters, Na, and aquaporins, which most probably all contribute to the urea reabsorption process. Although research is still in progress, a possible model for urea reabsorption in the kidney of cartilaginous fishes is discussed based on the anatomical features of nephron segments and vascular systems and on the results of molecular mapping. The molecular anatomical approach thus provides a powerful tool for understanding the physiological processes that take place in the highly elaborate kidney of cartilaginous fishes. cartilaginous fish; kidney; osmoregulation; transporters; urea BODY FLUID REGULATION is essential for all organisms to survive in their respective habitats, including freshwater (FW), seawater (SW), and terrestrial environments. It is well known that teleost fish regulate their plasma Na ϩ and Cl Ϫ concentrations and osmolality at levels about one-third of SW. Meanwhile, cartilaginous fishes (sharks, skates, rays, and chimaeras) have adopted a unique osmoregulatory strategy for adaptation to the high-salinity marine environment. Cartilaginous fishes control plasma ions to levels approximately one-half of surrounding SW while they store high concentrations of the nitrogenous compound urea as an osmolyte (the so-called "ureosmotic strategy"). As a result, their body fluids are slightly hyperosmotic to surrounding SW (for instance, plasma osmolality of houndshark is 1,000 mosmol/kg H 2 O in SW of 988 mosmol/kg H 2 O; Ref. 53), and thus cartilaginous fishes do not typically suffer dehydration even in the high-osmolality SW environment. To maintain high concentration of urea in the body, urea production by the ornithine urea cycle (OUC) is essential. Investigations on the OUC enzymes have proved that the liver is the primary organ f...

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Section: Urea Synthesis In the Kidneymentioning

confidence: 89%

Morphological and functional characteristics of the kidney of cartilaginous fishes: with special reference to urea reabsorption

Hyodo

Kakumura

Takagi

et al. 2014

American Journal of Physiology-Regulatory, Integrative and Comp

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“…In the light of these observations and additional in situ measurements of renal acidification in the marine skate Raja erinacea, a novel mechanism of HCO 3 -reabsorption was proposed for elasmobranchs involving (Deetjen and Maren, 1974). Years later, Swenson and colleagues (Swenson et al, 1994) proposed a mechanism for CA-independent urinary acidification involving the secretion of H + via a luminal H + ,K + -ATPase. Although these findings led to, or supported, acceptance of the hypothesis that marine fish lack renal CA, this conclusion is no longer believed given the physiological evidence for cytosolic CA activity in proximal tubules of winter flounder (Renfro et al, 1999;Pelis et al, 2003;Pelis and Renfro, 2004) and the finding of membrane-associated CA IV mRNA in dogfish kidney (Gilmour et al, 2007a).…”

Section: Role Of the Kidney In Acid-base Regulationmentioning

confidence: 99%

Carbonic anhydrase and acid–base regulation in fish

Gilmour

Perry

2009

Journal of Experimental Biology

183

131

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SummaryCarbonic anhydrase (CA) is the zinc metalloenzyme that catalyses the reversible reactions of CO 2 with water. CA plays a crucial role in systemic acid-base regulation in fish by providing acid-base equivalents for exchange with the environment. Unlike airbreathing vertebrates, which frequently utilize alterations of breathing (respiratory compensation) to regulate acid-base status, acid-base balance in fish relies almost entirely upon the direct exchange of acid-base equivalents with the environment (metabolic compensation). The gill is the critical site of metabolic compensation, with the kidney playing a supporting role. At the gill, cytosolic CA catalyses the hydration of CO 2 to H + and HCO 3 -for export to the water. In the kidney, cytosolic and membranebound CA isoforms have been implicated in HCO 3 -reabsorption and urine acidification. In this review, the CA isoforms that have been identified to date in fish will be discussed together with their tissue localizations and roles in systemic acid-base regulation.

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“…Meanwhile, molecular anatomy can determine the localization of transport proteins for urea, ions and water in situ, and thus is a powerful tool to overcome the difficulty in studying the elasmobranch kidney. Spatial patterns in the distribution of various pumps (Hentschel et al, 1993;Swenson et al, 1994), channels and transporters (Biemesderfer et al, 1996) in the nephron segments can provide valuable information on the movement of the above molecules across the kidney tubules, and thus on the reabsorption mechanism of urea.…”

mentioning

confidence: 99%

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

Hyodo

Katoh

Kaneko

et al. 2004

Journal of Experimental Biology

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SUMMARYReabsorption of filtered urea by the kidney tubule is essential for retaining high levels of urea in body fluids of marine elasmobranchs. To elucidate the mechanisms of urea reabsorption, we examined the distribution of a facilitative urea transporter (UT) in the kidney of the dogfish Triakis scyllia. We isolated a cDNA encoding a UT that is homologous to the facilitative UT cloned from another dogfish species, Squalus acanthias. The Triakis UT mRNA is abundantly expressed in the kidney, while low levels of expression were detected in the brain and liver. In the dogfish kidney, each nephron makes four turns and traverses repeatedly between bundle zone and sinus zone. In the bundle zone, the resulting five tubular segments are arranged in a countercurrent loop fashion. Immunohistochemistry using specific antibodies raised against the cloned UT revealed that, among the nephron segments, the UT is expressed exclusively in the final segment of the bundle zone, i.e. in the collecting tubule of the Triakis kidney. In contrast to the limited localization of UT, the transport enzyme Na+/K+-ATPase is distributed in the basolateral membrane of numerous tubular segments both in the sinus zone and the bundle zone. However, in the collecting tubule,Na+/K+-ATPase immunoreactivity was not detected. The present study suggests that the collecting tubule is responsible for the reabsorption of urea in the marine elasmobranch kidney. Other countercurrent segments may contribute to production of a driving force for facilitative diffusion of urea through the UT.

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Physiological and immunocytochemical evidence for a putative H-K-ATPase in elasmobranch renal acid secretion

Cited by 7 publications

References 0 publications

Morphological and functional characteristics of the kidney of cartilaginous fishes: with special reference to urea reabsorption

Morphological and functional characteristics of the kidney of cartilaginous fishes: with special reference to urea reabsorption

Carbonic anhydrase and acid–base regulation in fish

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

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