Na+ −K+ −Cl− co-transport in the intestine of a marine teleost

Musch, Mark W.; Orellana, Stephanie A.; Kimberg, Leigh; Field, Michael; Halm, Dan R.; Krasny, Edward J.; Frizzell, Raymond A.

doi:10.1038/300351a0

Cited by 207 publications

(75 citation statements)

References 13 publications

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“…The electrochemical Na + gradient established by the basolateral NKA provides the energy necessary for the thermodynamic uphill transport of K + and Cl -from the intestinal lumen across the apical membrane via two parallel cotransport systems: Na + :Cl -(NC) and Na Frizzell et al, 1979;Halm et al, 1985;Musch et al, 1982) (Fig.·1). As for NKA, the NKCC gene exhibits increased expression in euryhaline fish intestine when transferred from freshwater to seawater (Cutler and Cramb, 2002), illustrating the importance of NKCC for seawater osmoregulation.…”

Section: Apical Co-transportersmentioning

confidence: 99%

Intestinal anion exchange in marine fish osmoregulation

Grosell

2006

Journal of Experimental Biology

231

211

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Osmoregulation in marine fishThree distinct strategies for maintaining salt and water balance have evolved in fishes inhabiting the marine environments. (1) Osmoconformity/ionoconformity is found in the strictly marine agnathan hagfishes, which do not appear to regulate osmotic pressure and concentrations of main osmolytes to a great extent in seawater (Morris, 1958). (2) Osmoconformity and ionoregulation are seen in marine elasmobranchs (Hazon et al., 2003) and in the lobe-finned coelacanth (Griffith et al., 1974), which maintains plasma osmolality at or slightly above that of the surrounding seawater but NaCl concentrations at approximately d of ambient levels. (3) The most common strategy is osmoregulation, found in all teleosts (Marshall and Grosell, 2005) and marine lampreys (Morris, 1958), achieved by the regulation of the main extracellular electrolyte (Na + and Cl -) levels at approximately d of full strength seawater. Under steady state conditions at constant salinities, hagfish, elasmobranchs and coelacanths presumably do not need to drink to maintain water balance. It was shown, however, that the unavoidable renal and extra-renal fluid loss to the hypertonic marine environment in hypo-osmoregulating fish was compensated for by ingestion of seawater with subsequent water absorption across the gastro-intestinal tract (Smith, 1930). More recently, it was demonstrated that even the osmoconforming elasmobranchs display transient drinking when exposed to elevated ambient salinity, and evidence for components of the rennin-angiotensin system (RAS), even in the elasmobranchs (Anderson et al., 2002;Hazon et al., 2003) and hagfish (Cobb et al., 2004) as well as in lamprey (Brown et al., 2005), continues to accumulate. The drinking reflex is at least in part controlled by RAS and it thus appears that the ability to regulate ingestion of seawater and thereby the magnitude of intestinal fluid absorption is an ancestral osmoregulatory trait among fishes.The ingestion and processing of the imbibed seawater for osmoregulatory purposes have, at least in teleost fish, received much attention for three quarters of a century since the first classic studies by Smith published in 1930(Smith, 1930. It is now well established that an initial desalinization of the ingested seawater occurs in the esophagus, which absorbs Na + and Cl -through both passive and active transport pathways, Despite early reports, dating back three quarters of a century, of high total CO 2 concentrations in the intestinal fluids of marine teleost fishes, only the past decade has provided some insight into the functional significance of this phenomenon. It is now being recognized that intestinal anion exchange is responsible for high luminal HCO 3 -and CO 3 2-concentrations while at the same time contributing substantially to intestinal Cl -and thereby water absorption, which is vital for marine fish osmoregulation. In species examined to date, the majority of HCO 3 -secreted by the apical anion exchange process is derived from hydration of metabolic ...

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Section: Apical Co-transportersmentioning

confidence: 99%

Intestinal anion exchange in marine fish osmoregulation

Grosell

2006

Journal of Experimental Biology

231

211

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“…In mammals, NaCl in the luminal fluid is absorbed into the enterocytes via concerted action of Cl -/ HCO3 -exchanger (SLC26A6) and Na + /H + exchanger (NHE3 or SLC9A3) on the apical membrane (Kato and Romero, 2011), but it is mostly via Na + -K + -2Cl -co-transporter (NKCC2 or SLC12A1) in the marine teleost intestine (Ando, 1980;Musch et al, 1982;Takei and Loretz, 2011). In parallel with the ion absorption, water moves through a water channel (AQP1) into the cell.…”

Section: Fig 3 Differences In Regulatory Mechanisms Of Drinking In mentioning

confidence: 99%

Regulation of Ion Transport in Eel Intestine by the Homologous Guanylin Family of Peptides

Yuge

Takei

2007

Zoological Science

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It is generally accepted that ancient fishes first experienced freshwater (FW), and then variably by lineage moved onto the land or re-entered the seas during evolution. As both land and sea are desiccating environments, animals must change their strategies for body fluid regulation from protecting against overhydration in FW to coping with dehydration in seawater (SW) or on land. The evolution of the mechanisms for acquisition of water surely must have accompanied these dramatic environmental changes. The major route for water acquisition is by oral drinking in terrestrial tetrapods (represented here by mammals) and in SW fishes (represented by teleosts as they are dehydrated in SW), but the regulation is contrasting between the two groups; mechanisms inducing thirst have developed in mammals, whereas inhibitory mechanisms are dominant in marine teleosts as observed in FW teleosts. Thus, the apparent difference was found not between hydrating and dehydrating habitat, but rather between terrestrial and aquatic habitats. This contrast is also reflected in regulatory hormones; dipsogenic hormones such as angiotensin II play pivotal roles in water homeostasis in mammals, whereas antidipsogenic hormones such as atrial natriuretic peptide are essential in teleosts. Imbibed water becomes body fluid only after absorption by the intestine, and there is a distinct difference in the mechanisms for water absorption between mammals and teleosts. Like regulation of drinking, we found that the inhibitory mechanisms are dominant for intestinal water absorption in teleosts. In the initial part of this short review, interesting differences in the body fluid regulation between mammals and teleosts are introduced, particularly with regard to water acquisition (drinking and intestinal absorption). Then an attempt was made to discuss the evolution of the mechanisms from the two perspectives; transitions from aquatic to terrestrial habitats and from hydrating (FW) to dehydrating (land and SW) habitats.

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“…Previous electrophysiological studies have demonstrated that, as in most epithelial cells, the resting membrane potential of acinar cells is mainly dependent on the transmembrane K+ gradient (Ishikawa & Kanno, 1991), suggesting the presence of a resting K+ efflux. It is well known that, in addition to a Na+-K+ pump, a loop diuretic-sensitive Na+-K+-2Cl-symport operates in a variety of transporting epithelia (Geck, Pietrzyk, Burckhardt, Pfeiffer & Heinz, 1980;Munsch, Orellano, Kimberg, Field, Halm, Krasney & Frizzell, 1982;Ishikawa & Kanno, 1991). Our results showed that 01 mm furosemide, and the replacement of Cl-with NO3-, had no effect on the K+ transport in the unstimulated pieces of pancreas, suggesting that a furosemidesensitive Na+-K+-2Cl-symport is not responsible for the K+ influx in the unstimulated guinea-pig pancreas.…”

Section: Discussionmentioning

confidence: 99%

Acetylcholine‐evoked potassium transport in the isolated guinea‐pig pancreas

Singh²,

Salido³

et al. 1997

Experimental Physiology

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SUMMARYIn this study, K+ concentration was measured in effluent samples from superfused guinea-pig pancreatic pieces in control conditions and during stimulation with ACh, employing the technique of flame photometry. ACh (10-7_10-5 M) evoked a dose-dependent and sustained increase in K+ concentration in the effluent (K+ release). The removal of Ca2+ from the superfusing medium and the addition of 10-4 M EGTA caused a significant (P < 0.05) reduction in the ACh-evoked K+ efflux. Replacement of extracellular Cl-in the superfusing physiological salt solution with NO3-abolished the ACh-induced K+ efflux. In contrast, when Cl-was replaced with Br-, ACh still evoked marked K+ release. Pretreatment of pancreatic segments with the loop diuretic furosemide (10-4 M) resulted in an inhibition of K+ efflux elicited by ACh. Stimulation of pancreatic segments with the Na+-K+-ATPase inhibitor ouabain (10-3 M) caused a large efflux of K+. In the continuous presence of ouabain, ACh application elicited no further change in the K+ release. The results indicate that ACh-evoked K+ release from guinea-pig pancreatic segments is sensitive to ouabain, Cl-, furosemide and extracellular Ca2' and that only the basal efflux is augmented by ouabain. The findings provide further evidence that a diuretic-sensitive coupled Na+-K+-Cl-cotransport system operates in the guinea-pig pancreas, as it does in other similar transporting epithelia, to bring about K+ mobilization.

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Na+ −K+ −Cl− co-transport in the intestine of a marine teleost

Cited by 207 publications

References 13 publications

Intestinal anion exchange in marine fish osmoregulation

Intestinal anion exchange in marine fish osmoregulation

Regulation of Ion Transport in Eel Intestine by the Homologous Guanylin Family of Peptides

Acetylcholine‐evoked potassium transport in the isolated guinea‐pig pancreas

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