Regulation of branchial V-H+-ATPase,Na+/K+-ATPase and NHE2 in response to acid and base infusions in the Pacific spiny dogfish (<i>Squalus acanthias</i>)

Tresguerres, Martín; Katoh, Fumi; Fenton, Heather; Jasinska, Edyta J.; Goss, Greg G.

doi:10.1242/jeb.01382

Cited by 100 publications

(87 citation statements)

References 29 publications

(23 reference statements)

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“…2) located, in contrast to teleosts. Instead, all current models for the elasmobranch gill indicate that H + -ATPase functions basolaterally in those ionocytes, which excrete base (Piermarini and Evans, 2001;Piermarini et al, 2002;Tresguerres et al, 2005;Reilly et al, 2011), so that H + ions are returned to the blood when HCO 3 -is excreted apically at times of blood alkalosis (Tresguerres et al, 2005;Tresguerres et al, 2006;Tresguerres et al, 2007;Roa et al, 2014). In the present study, there was a slight tendency towards alkalosis during HEA exposure, with a significant rise in plasma [HCO 3 -] (Fig.…”

Section: Molecular Responses To Heamentioning

confidence: 46%

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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Section: Molecular Responses To Heamentioning

confidence: 46%

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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“…Additional evidence was obtained from studies on marine dogfish, which utilize branchial Na + /H + and Cl -/HCO 3 -exchanges for acid-base regulation, although not ionic regulation (e.g. Tresguerres et al, 2005; see reviews by Perry and Laurent, 1990;Claiborne et al, 2002;Evans et al, 2005). The branchial clearance of an infused HCO 3 -load was impaired in dogfish treated with benzolamide to selectively inhibit gill CA activity (Swenson and Maren, 1987).…”

Section: Discussionmentioning

confidence: 99%

The role of branchial carbonic anhydrase in acid-base regulation in rainbow trout (Oncorhynchus mykiss)

Georgalis

Perry

Gilmour

2006

Journal of Experimental Biology

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SUMMARY The objective of the present study was to examine the branchial distribution of the recently identified rainbow trout cytoplasmic carbonic anhydrase isoform (tCAc) and to investigate its role in the regulation of acid-base disturbances in rainbow trout (Oncorhynchus mykiss). In situ hybridization using an oligonucleotide probe specific to tCAc revealed tCAc mRNA expression in both pavement cells and mitochondria-rich cells (chloride cells). Similarly, using a homologous polyclonal antibody,tCAc immunoreactivity was localized to pavement cells and mitochondria-rich cells in the interlamellar region and along the lamellae of the gills. Exposure of rainbow trout to hypercarbia (∼0.8% CO2) for 24 h resulted in significant increases in tCAc mRNA expression (∼20-fold;quantified by real-time PCR) and protein levels (∼1.3-fold; quantified by western analysis) but not enzyme activity (assessed on crude gill homogenates using the delta-pH CA assay). Inhibition of branchial CA activity in vivo using acetazolamide reduced branchial net acid excretion significantly by 20%. This effect was enhanced to a 36% reduction in branchial net acid excretion by subjecting the trout to hypercarbia (∼0.8%CO2) for 10 h prior to acetazolamide injection, an exposure that significantly increased branchial net acid excretion. The results of the present study support the widely held premise that branchial intracellular CA activity (tCAc) plays a key role in regulating acid-base balance in freshwater teleost fish.

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“…-secreting, H þ -absorbing cells such as gill cells from hagfish [31,32], shark [26,[33][34][35] and trout [36], and b-intercalated cells from mammalian kidney [21,37,38].…”

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confidence: 99%

How to get into bones: proton pump and carbonic anhydrase inOsedaxboneworms

2013

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Osedax are gutless siboglinid worms that thrive on vertebrate bones lying on the ocean floor, mainly those of whales. The posterior body of female Osedax penetrates into the bone forming extensions known as 'roots', which host heterotrophic symbiotic bacteria in bacteriocytes beneath the epidermis. The Osedax root epithelium presumably absorbs bone collagen and/or lipids, which are metabolized by the symbiotic bacteria that in turn serve for Osedax's nutrition. Here, we show that Osedax roots express extremely high amounts of vacuolar-H þ -ATPase (VHA), which is located in the apical membrane and in cytoplasmic vesicles of root and ovisac epithelial cells. The enzyme carbonic anhydrase (CA), which catalyses the hydration of CO 2 into H þ and HCO 3 2 , is also expressed in roots and throughoutOsedax body. These results suggest Osedax roots have massive acid-secreting capacity via VHA, fuelled by H þ derived from the CA-catalysed hydration of CO 2 produced by aerobic metabolism. We propose the secreted acid dissolves the bone carbonate matrix to then allow the absorption of bonederived nutrients across the skin. In an exciting example of convergent evolution, this model for acid secretion is remarkably similar to mammalian osteoclast cells. However, while osteoclasts dissolve bone for repairing and remodelling, the Osedax root epithelium secretes acid to dissolve foreign bone to access nutrients.

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Regulation of branchial V-H+-ATPase,Na+/K+-ATPase and NHE2 in response to acid and base infusions in the Pacific spiny dogfish (Squalus acanthias)

Cited by 100 publications

References 29 publications

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

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

The role of branchial carbonic anhydrase in acid-base regulation in rainbow trout (Oncorhynchus mykiss)

How to get into bones: proton pump and carbonic anhydrase inOsedaxboneworms

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