Evidence for an apical Na–Cl cotransporter involved in ion uptake in a teleost fish

Hiroi, Junya; Yasumasu, Shigeki; McCormick, Stephen D.; Hwang, Pung‐Pung; Kaneko, Toyoji

doi:10.1242/jeb.018663

Cited by 245 publications

(239 citation statements)

References 55 publications

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“…05). Investigations of the role of NKCC1b in the gill are scarce, and we can only note that the higher level of NKCC1b in SW-acclimated tilapia compared with FWacclimated tilapia in this study is inconsistent with the studies of Hiroi et al (2008), where NKCC1b levels were the same or lower in SW compared with FW. -ATPase a subunit and isoform transcripts, protein and activity levels in vivo and in vitro is well established in salmonids (see Mommsen et al (1999), McCormick et al (2008) and ).…”

Section: Kcontrasting

confidence: 99%

Differential effects of cortisol and 11-deoxycorticosterone on ion transport protein mRNA levels in gills of two euryhaline teleosts, Mozambique tilapia (Oreochromis mossambicus) and striped bass (Morone saxatilis)

Kiilerich¹,

Tipsmark²,

Borski³

et al. 2011

Journal of Endocrinology

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The role of cortisol as the only corticosteroid in fish osmoregulation has recently been challenged with the discovery of a mineralocorticoid-like hormone, 11-deoxycorticosterone (DOC), and necessitates new studies of the endocrinology of osmoregulation in fish. Using an in vitro gill explant incubation approach, DOC-mediated regulation of selected osmoregulatory target genes in the gill was investigated and compared with that of cortisol in two euryhaline teleosts, Mozambique tilapia (Oreochromis mossambicus) and striped bass (Morone saxatilis). The effects were tested in gills from both fresh water (FW)-and seawater (SW)-acclimated fish. Both cortisol and DOC caused an up-regulation of the Na C ,K C -ATPase a1 subunit in SW-acclimated tilapia but had no effect in FW-acclimated fish. Cortisol conferred an increase in NaK cotransporter (NKCC) isoform 1a transcript levels in FW-and SW-acclimated tilapia, whereas DOC had a stimulatory effect only in SW-acclimated fish. Cortisol had no effect on NKCC isoform 1b mRNA levels at both salinities, while DOC stimulated this isoform in SW-acclimated fish. In striped bass, cortisol conferred an up-regulation of Na C ,K C -ATPase a1 and NKCC transcript levels in FW-and SW-acclimated fish, whereas DOC resulted in down-regulation of these transcripts in FW-acclimated fish. It was also found that both corticosteroids may rapidly (30 min) alter the mitogen-activated protein kinase signalling pathway in gill, inducing phosphorylation of extracellular signalregulated kinase 1 (ERK1) and ERK2 in a salinity-dependent manner. The study shows a disparate organisation of corticosteroid signalling mechanisms involved in ion regulation in the two species and adds new evidence to a role of DOC as a mineralocorticoid hormone in teleosts.

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Section: Kcontrasting

confidence: 99%

Differential effects of cortisol and 11-deoxycorticosterone on ion transport protein mRNA levels in gills of two euryhaline teleosts, Mozambique tilapia (Oreochromis mossambicus) and striped bass (Morone saxatilis)

Kiilerich¹,

Tipsmark²,

Borski³

et al. 2011

Journal of Endocrinology

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“…In addition, a duplicated pair of NKCC2 isoforms (NKCC2α and NKCC2β) has been identified in several teleosts, and they are expressed in different tissues and organs (Cutler and Cramb, 2008;Hiroi et al, 2008;Watanabe et al, 2011). For example, NKCC2α mRNA is expressed only in the renal tissue of European eel, whereas NKCC2β expression is detected in the intestine and urinary bladder.…”

Section: Fish and Samplingmentioning

confidence: 99%

Molecular Characterization and Expression Pattern of Na+-K+-2Cl- Cotransporter 2 (NKCC2) in the Intestine of Starry Flounder Platichthys stellatus after Bacterial Challenge

Kim¹,

Nam²

2015

Fisheries and aquatic sciences

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We identified the Na− cotransporter 2 (NKCC2) cDNA isoform from starry flounder, Platichthys stellate. The NKCC2 cDNA encoded a polypeptide of 1,043 amino acids representing 12 putative transmembrane domains based on the bioinformatic topology prediction. In addition, starry flounder NKCC2 possessed highly conserved residues within transmembrane domain 4, known as an essential site for its function. End-point reverse transcription-polymerase chain reaction analysis revealed that the NKCC2 transcript was moderately expressed only in the anterior and posterior intestines and the rectum. The NKCC2 mRNA level in the rectum, but not in other segments, was significantly induced 3 days post Streptococcus parauberis challenge, indicating that excess salt may be transported into the rectum. Taken together, our data indicate that an S. parauberis infection could tip the intestinal fluid balance in favor of fluid accumulation, indicating that bacterial pathogens can interfere with intestinal osmotic balance and normal mucosal immune homeostasis.

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“…The tree shows a single torafugu gene encoding a conventional NCC (Slc12a3), which has been characterized in flounder and mammals (16,31). Moreover, torafugu lack the fish-specific NCC (Slc12a10) that has recently been found in eel, tilapia, and zebrafish and shown to be specifically expressed in the yolk sac membrane and gills (11,21,23). Torafugu also have a single NKCC2 gene, whereas two NKCC1 genes were identified.…”

Section: Identification Of Torafugu Ncc and Nkcc2 Genesmentioning

confidence: 99%

“…The relationships among conventional NCC (Slc12a3), fish-specific NCC (Slc12a10), NKCC1 (Slc12a2), and NKCC2 (Slc12a1) are shown. The fugu genome contains only one NCC gene and lacks the fish-specific NCC gene, which is specifically expressed in the yolk sac membrane and gill (21). Mefugu NCC and NKCC2 are shown in bold.…”

Section: Identification Of Torafugu Ncc and Nkcc2 Genesmentioning

confidence: 99%

“…The gill is another important osmoregulatory tissue in teleosts. Recently, a fish-specific isoform of NCC was identified that is specifically expressed in the mitochondrion-rich cells of the gill epithelium and appears to be involved in Na ϩ and Cl Ϫ uptake in certain freshwater fish species (21,24,54). No gene encoding this fish-specific NCC was identified in the mefugu genome (Fig.…”

Section: Perspectives and Significancementioning

confidence: 99%

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Differential expression of Na⁺-Cl⁻cotransporter and Na⁺-K⁺-Cl⁻cotransporter 2 in the distal nephrons of euryhaline and seawater pufferfishes

Kato

Muro

Kimura

et al. 2011

American Journal of Physiology-Regulatory, Integrative and Comp

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in the distal nephrons of euryhaline and seawater pufferfishes. Am J Physiol Regul Integr Comp Physiol 300: R284 -R297, 2011. First published November 17, 2010 doi:10.1152/ajpregu.00725.2009.-The process of NaCl reabsorption in the distal nephron allows freshwater fishes to excrete hypotonic urine and seawater fishes to excrete urine containing high concentrations of divalent ions; the relevant transporters, however, have not yet been identified. In the mammalian distal nephron, NaCl absorption is mediated by Na ϩ -K ϩ -Cl Ϫ cotransporter 2 (NKCC2, Slc12a1) in the thick ascending limb, Na ϩ -Cl Ϫ cotransporter (NCC, Slc12a3) in the distal convoluted tubule, and epithelial sodium channel (ENaC) in the collecting duct. In this study, we compared the expression profiles of these proteins in the kidneys of euryhaline and seawater pufferfishes. Mining the fugu genome identified one NKCC2 gene and one NCC gene, but no ENaC gene. RT-PCR and in situ hybridization analyses demonstrated that NKCC2 was highly expressed in the distal tubules and NCC was highly expressed in the collecting ducts of euryhaline pufferfish (mefugu, Takifugu obscurus). On the other hand, the kidney of seawater pufferfish (torafugu, Takifugu rubripes), which lacked distal tubules, expressed very low levels of NCC, and, in the collecting ducts, high levels of NKCC2. Acclimation of mefugu to seawater resulted in a 2.7ϫ decrease in NCC expression, whereas NKCC2 expression was not markedly affected. Additionally, internalization of NCC from the apical surface of the collecting ducts was observed. These results suggest that NaCl reabsorption in the distal nephron of the fish kidney is mediated by NCC and NKCC2 in freshwater and by NKCC2 in seawater. distal tubule; collecting duct; NKCC2; NCC; fish kidney; dilute urine FRESHWATER FISHES LIVE IN hypo-osmotic environments, resulting in significant influx of water into the body, mainly across the gills. To maintain body fluid homeostasis, freshwater fishes import ions from surrounding water through the gills (13,22) or from the diet, and excrete excess water in hypotonic urine (ϳ10 mM Na ϩ and Cl Ϫ ) through the kidneys (30). To increase urine volume (i.e., water excretion), freshwater fishes secrete NaCl in the proximal tubule and draw interstitial water into the tubular lumen (9); this proximally introduced NaCl should be reabsorbed in the distal nephron. Reabsorption of Na ϩ and Cl Ϫ ions from urine under water-impermeable conditions is, therefore, essential for net water excretion and the survival of fishes in freshwater. Na ϩ and Cl Ϫ reabsorption is also important for seawater fishes. Unlike freshwater fishes, however, seawater fishes experience passive water efflux. To balance water loss, seawater fishes absorb water and ions through the intestine by drinking large amounts of seawater (17). Surplus ions are excreted mainly through the gills (13, 22), although divalent ions (Mg 2ϩ and SO 4 2Ϫ ) are excreted through isotonic urine (4, 30). To produce urine with high concentrations of Mg 2ϩ (ϳ140 mM) ...

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Evidence for an apical Na–Cl cotransporter involved in ion uptake in a teleost fish

Abstract: SUMMARYCation-chloride cotransporters, such as the Na

Cited by 245 publications

References 55 publications

Differential effects of cortisol and 11-deoxycorticosterone on ion transport protein mRNA levels in gills of two euryhaline teleosts, Mozambique tilapia (Oreochromis mossambicus) and striped bass (Morone saxatilis)

Differential effects of cortisol and 11-deoxycorticosterone on ion transport protein mRNA levels in gills of two euryhaline teleosts, Mozambique tilapia (Oreochromis mossambicus) and striped bass (Morone saxatilis)

Molecular Characterization and Expression Pattern of Na<sup>+</sup>-K<sup>+</sup>-2Cl<sup>-</sup> Cotransporter 2 (NKCC2) in the Intestine of Starry Flounder Platichthys stellatus after Bacterial Challenge

Differential expression of Na⁺-Cl⁻cotransporter and Na⁺-K⁺-Cl⁻cotransporter 2 in the distal nephrons of euryhaline and seawater pufferfishes

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Evidence for an apical Na–Cl cotransporter involved in ion uptake in a teleost fish

Abstract: SUMMARYCation-chloride cotransporters, such as the Na

Cited by 245 publications

References 55 publications

Differential effects of cortisol and 11-deoxycorticosterone on ion transport protein mRNA levels in gills of two euryhaline teleosts, Mozambique tilapia (Oreochromis mossambicus) and striped bass (Morone saxatilis)

Differential effects of cortisol and 11-deoxycorticosterone on ion transport protein mRNA levels in gills of two euryhaline teleosts, Mozambique tilapia (Oreochromis mossambicus) and striped bass (Morone saxatilis)

Molecular Characterization and Expression Pattern of Na<sup>+</sup>-K<sup>+</sup>-2Cl<sup>-</sup> Cotransporter 2 (NKCC2) in the Intestine of Starry Flounder Platichthys stellatus after Bacterial Challenge

Differential expression of Na+-Cl−cotransporter and Na+-K+-Cl−cotransporter 2 in the distal nephrons of euryhaline and seawater pufferfishes

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Differential expression of Na⁺-Cl⁻cotransporter and Na⁺-K⁺-Cl⁻cotransporter 2 in the distal nephrons of euryhaline and seawater pufferfishes