The mechanism of sodium chloride uptake in hyperregulating aquatic animals

Kirschner, Leonard B.

doi:10.1242/jeb.00907

Cited by 182 publications

(162 citation statements)

References 127 publications

(103 reference statements)

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“…More specifically, the gill Na + , K + ATPase, located mainly in chloride cells, requires energy input and plays an important role in osmoregulation in both hyperosmotic (Jobling, 1995;Evans et al, 2005) and hyposmotic (Evans, 2008;Parks et al, 2008) environments. The activity of this ATPase spends at least half of the energy consumed during Na + /H + exchange in ionocytes (Kirschner, 2004). For this reason, Na + , K + ATPase is considered to be a good biomarker of osmoregulation in teleosts.…”

Section: Introductionmentioning

confidence: 99%

The effect of salinity on osmoregulation and development of the juvenile fat snook, Centropomus parallelus (POEY)

et al. 2013

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Eurihaline fish support waters with different salt concentration. However, numerous studies have shown that salinity can affect fish development. Thus, the effect of salinity change from 20 to 5 and 35 on survival, weight, length, gill chloride cell ultrastructure and gill Na + , K + ATPase activity was evaluated in Centropomus parallelus following short-term (6, 24 and 96 hours) and long-term exposure (30 and 60 days). Salinity did not affect C. parallelus survival, final weight and length. The quantity of chloride cells increased visibly at salinities of 5 and 35, with the cells exhibiting the typical features of uptake and secretory cells, respectively. Na + , K + ATPase activity in the gill of the C. parallelus was significantly greater at a salinity of 5 than at a salinity of 20 or 35 after 96 hours, but not after 30 or 60 days. These results indicate that salinity change from high to low salt water induces gill chloride cell and Na + , K + ATPase activity adaptations after short-term exposure. However, after long-term exposure at salinity 5, gill Na + , K + ATPase activity is no more necessary at high levels. The increase in salinity to 35 does not induce significant change in gills. Juveniles of C. parallelus may thus be capable of acclimating to salinities of 5 to 35 for 60 days without significant effects on development.Keywords: Centropomus parallelus, chloride cell, osmoregulation, Na + , K + ATPase. O efeito da salinidade sobre a osmoregulação e o desenvolvimento do juvenil de robalo-peva, Centropomus parallelus (POEY) ResumoPeixes eurihalinos suportam águas com diferentes concentrações de sal. Contudo, muitos estudos têm mostrado que a salinidade pode afetar o desenvolvimento do peixe. Portanto, o efeito da mudança de salinidade de 20 para 5 e 35 na taxa de sobrevivência, peso, comprimento, morfologia das células de cloreto branquiais e atividade da Na + , K + ATPase foram avaliadas no Centropomus parallelus após curto (6, 24 e 96 horas) e longo tempo de exposição (30 e 60 dias). A salinidade não afetou a sobrevivência, o peso e comprimento final do robalo-peva. A quantidade de células de cloreto aumentou visivelmente nas salinidades 5 e 35, exibindo morfologias típicas de células que absorvem e secretam sal, respectivamente. A atividade da Na + , K + ATPase nas brânquias do C. parallelus foi significativamente maior na salinidade 5 do que nas salinidades 20 ou 35 após 96 horas, mas não após 30 e 60 dias. Esses resultados indicam que a mudança de alta para baixa salinidade provoca adaptações nas células de cloreto e na atividade da Na + , K + ATPase branquial em curto prazo. Contudo, após longa exposição na salinidade 5, a alta atividade da Na + , K + ATPase branquial não é mais necessária. O aumento de salinidade para 35 não induz mudanças significativas nas brânquias. Portanto, juvenis de C. parallelus possuem a capacidade de aclimatação nas salinidades de 5 a 35 sem efeitos significativos no desenvolvimento após 60 dias.Palavras-chave: Centropomus parallelus, célula de cloreto, osmoregula...

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Section: Introductionmentioning

confidence: 99%

The effect of salinity on osmoregulation and development of the juvenile fat snook, Centropomus parallelus (POEY)

et al. 2013

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“…To determine whether any of these systems was utilized to maintain Na + homeostasis or for recovery, we assessed the possible use of these pathways under basal and recovery conditions. Previous studies have determined that Na + uptake can occur in the absence of ambient Cl -availability (Krogh, 1938;Krogh, 1939;Kirschner, 2004), although the rate may be reduced relative to conditions that provide Cl - (de With et al, 1987). Considering this evidence that Na + uptake can occur in Cl --free conditions, we were not surprised to find a lack of dependency on Cl -.…”

Section: Discussionmentioning

confidence: 50%

“…One possible characteristic of pathways involved in Na + recovery could be dependency on availability of extracellular anions (de With, 1980;de With et al, 1987). Uptake of Na + in many freshwater organisms requires Cl - (Kirschner, 2004) and the possibility of HCO 3 --dependent Na + uptake via a Na + /HCO 3 --dependent carrier system exists (Perry et al, 2003). The observed stimulated Na + uptake associated with recovery from ECF release was attributed to both increased transport capacity and affinity.…”

Section: Introductionmentioning

confidence: 99%

“…Furthermore, microtubule-dependent relocation of transport proteins from the cytoplasm to the epithelial membrane (Tresguerres et al, 2006) could also contribute to the rapid activation of the Na + uptake mechanism. Additionally, the enhanced transport may rely on availability of intracellular H + ions (Kirschner, 2004), which are produced by the hydration of CO 2 , and would therefore be dependent upon carbonic anhydrase (CA). Therefore, our two final objectives were to (5) determine whether the amplified Na + uptake was Cl --or HCO 3 --dependent and (6) conduct a pharmacological assessment of transport mechanisms involved in Na + recovery.…”

Section: Introductionmentioning

confidence: 99%

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Fluid and osmolyte recovery in the common pond snailLymnaea stagnalisfollowing full-body withdrawal

Ebanks

Grosell

2008

Journal of Experimental Biology

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SUMMARYThe common pond snail Lymnaea stagnalis sacrifices 40-60% of its extracellular fluid (ECF) including solutes to the surrounding environment to fully retract into its shell. Our objectives were to determine recovery time following such ECF loss and characterize mechanisms involved in recovering Na + , the primary cationic osmolyte in this snail. Pallial fluid was initially collected post-stimulation and again after a second stimulation on sub-groups of those snails 2·h to 10·weeks after initial sampling. Samples were analyzed for pH, osmotic pressure, and individual solute concentrations. Lost volume was recovered within 8·h with no significant changes in pH or total CO 2 . Significant decreases in osmotic pressure, [Na + ] (43% loss), and [Cl -] recovered in 48·h as a result of enhanced uptake from the water. Copper and total extracellular proteins took 5 weeks to recover. Measurements of Na + transport kinetics completed before and immediately after fluid loss revealed a near threefold increase in both affinity and capacity of the Na + uptake system. Sodium uptake was independent of ambient Cl -and HCO 3 -in both control and fluid-depleted snails. Amiloride significantly reduced recovery-phase Na + uptake rates but did not influence baseline Na + flux. Recovery uptake was significantly reduced by amiloride, ethylisopropylamiloride, bafilomycin and ethoxzolamide indicating dependency upon Na + /H + exchange, H + pump activity and H + from carbonic anhydrase-catalyzed CO 2 hydration. Thus enhanced uptake during recovery is likely via electrogenic Na + /H + exchange and/or possibly a cation channel.

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“…In the current study we found that, besides ouabain (normoxic condition), hypoxia reduced 86 Rb + effluxes from the basolateral to the apical side of the gill hemilamella, where 86 Rb (K + ) ions enter the cells by the activity of Na + , K + -ATPase, at the basolateral side. In the hyperosmoregulating Carcinus the Na + /K + -pump actively transports K + into the cytoplasm of the gill epithelial cells from which it passively diffuses out of the cell through K + channels at both sides of the epithelium (Kirschner, 2004).…”

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confidence: 99%

The effects of hypoxia on active ionic transport processes in the gill epithelium of hyperregulating crab, Carcinus maneas

Lucu

Ziegler

2017

Comparative Biochemistry and Physiology Part A: Molecular &

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A B S T R A C TEffects of hypoxia on the osmorespiratory functions of the posterior gills of the shore crab Carcinus maenas acclimated to 12 ppt seawater (DSW) were studied. Short-circuit current (Isc) across the hemilamella (one epithelium layer supported by cuticle) was substantially reduced under exposure to 1.6, 2.0, or 2.5 mg O 2 /L hypoxic saline (both sides of epithelium) and fully recovered after reoxygenation. Isc was reduced equally in the epithelium exposed to 1.6 mg O 2 /L on both sides and when the apical side was oxygenated and the basolateral side solely exposed to hypoxia. Under 1.6 mg O 2 /L, at the level of maximum inhibition of Isc, conductance was decreased from 40.0 mS cm − 2 to 34.7 mS cm − 2 and fully recovered after reoxygenation. Isc inhibition under hypoxia and reduced 86 Rb + (K + ) fluxes across apically located K + channels were caused preferentially by reversible inhibition of basolaterally located and ouabain sensitive Na + ,K + -ATPase mediated electrogenic transport. Reversible inhibition of Isc is discussed as decline in active transport energy supply down regulating metabolic processes and saving energy during oxygen deprivation. In response to a 4 day exposure of Carcinus to 2.0 mg O 2 /L, hemolymph Na + and Cl − concentration decreased, i.e. hyperosmoregulation was weakened. Variations of the oxygen concentration level and exposure time to hypoxia lead to an increase of the surface of mitochondria per epithelium area and might in part compensate for the decrease in oxygen availability under hypoxic conditions.

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The mechanism of sodium chloride uptake in hyperregulating aquatic animals

Abstract: SUMMARYThe emphasis in this review will be on Na+ absorption across the skin and gills of vertebrates and the gills of crustaceans. However, some recent studies of Cl– uptake, especially in crustaceans, will also be described.

Cited by 182 publications

References 127 publications

The effect of salinity on osmoregulation and development of the juvenile fat snook, Centropomus parallelus (POEY)

The effect of salinity on osmoregulation and development of the juvenile fat snook, Centropomus parallelus (POEY)

Fluid and osmolyte recovery in the common pond snailLymnaea stagnalisfollowing full-body withdrawal

The effects of hypoxia on active ionic transport processes in the gill epithelium of hyperregulating crab, Carcinus maneas

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