Mechanisms of Cl− uptake in rainbow trout: Cloning and expression of slc26a6, a prospective Cl−/HCO3− exchanger

Boyle, David; Clifford, Alexander M.; Orr, Elizabeth C.; Chamot, Danuta; Goss, Greg G.

doi:10.1016/j.cbpa.2014.11.001

Cited by 29 publications

(19 citation statements)

References 39 publications

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“…However, mucosal DNDS/DIDS failed to decrease HCO 3 - secretion in this study, which suggests that eel Pat-1 and DRA are not involved in HCO 3 - secretion in SW eel intestine, or these AEs of eels are insensitive to these stilbene inhibitors. It is important to note that DNDS/DIDS effectively blocked Pat-1 in mammals (Stewart et al, 2009) and teleosts (Boyle et al, 2015), but DIDS was ineffective to block DRA in the rat (Barmeyer et al, 2007) and mouse (Whittamore and Hatch, 2017). There are no studies on DIDS/DNDS sensitivity to teleost DRA, but it is possible that they are ineffective to block eel DRAs.…”

Section: Discussionmentioning

confidence: 99%

Molecular mechanisms for intestinal HCO₃^-secretion and its regulation by guanylin in seawater-acclimated eels

Takei

Wong

Ando

2019

Preprint

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The intestine of marine teleosts secretes HCO 3 into the lumen and precipitates Ca 2+ and Mg 2+ in the imbibed seawater as carbonates to decrease luminal fluid osmolality and facilitate water absorption. However, reports on studies on the hormonal regulation of HCO 3 secretion are just emerging. Here, we showed that guanylin (GN) applied to the mucosal side of intestinal epithelia increased HCO 3 secretion in seawater-acclimated eels. The effect of GN on HCO 3 secretion was slower than that on the short-circuit current, and the time-course of the GN effect was similar to that of bumetanide. Mucosal bumetanide and serosal 4,4'-dinitrostilbene-2,2'-disulfonic acid (DNDS) inhibited the GN effect, suggesting an involvement of apical Na + -K + -2Clcotransporter (NKCC2) and basolateral Cl -/HCO 3 exchanger (AE)/Na + -HCO 3 cotransporter (NBC) in the GN effect. However, mucosal DNDS and diphenylamine-2-carboxylic acid (DPC) failed to inhibit the GN effect, showing that apical AE and Clchannel are not involved. To identify molecular species of possible transporters involved in the GN effect, we performed RNA-seq analyses followed by quantitative real-time PCR after transfer of eels to seawater. Among the genes upregulated after seawater transfer, those of Slc26a3a, b (DRAa, b) and Slc26a6a, c (Pat-1a, c) on the apical membrane of the intestinal epithelial cells, and those of Sls4a4a (NBCe1a), Slc4a7 (NBCn1), Slc4a10a (NBCn2a) and Slc26a1 (Sat-1) on the basolateral membrane were candidate transporters involved in HCO 3 secretion. Judging from the slow effect of GN, we suggest that GN inhibits NKCC2b on the apical membrane and decreases cytosolic Cland Na + , which then activates apical DNDS-insensitive DRAa, b and basolateral DNDS-sensitive NBCela, n1, n2a to enhance transcellular HCO 3 flux across the intestinal epithelia of seawater-acclimated eels. Alper, S. L. and Sharma, A. K. (2013). The SLC26 gene family of anion transporters and channels. Mol. Aspects Med. 34, 494-515. Ando, M., and Subramanyam, M. V. V. (1990). Bicarbonate transport systems in the intestine of the seawater eel. J. Exp. Biol. 150, 381-394. Ando, M. and Takei, Y. (2015). Guanylin activates Clsecretion into the lumen of seawater eel intestine via apical Clchannel under simulated in vivo condition. Am. J. Physiol. 308, R400-R410. Ando, M., Wong, M. K. S. and Takei, Y. (2014). Mechanisms of guanylin action on water and ion absorption at different regions of seawater eel intestine. Am. J. Physiol. 307, R653-R663. Barmeyer, C., Ye, J. H., Sidani, S., Geibel, J., Binder, H. J. and Rajendran V. M. (2007).Characteristics of rat downregulated in adenoma (rDRA) expressed in HEK 293 cells. Pflü.Arch. 454, 441-450.

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Section: Discussionmentioning

confidence: 99%

Molecular mechanisms for intestinal HCO₃^-secretion and its regulation by guanylin in seawater-acclimated eels

Takei

Wong

Ando

2019

Preprint

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“…nos2 and nos1 primers were designed using O. mykiss nos2, and nos1 nucleotide sequences. slc26a6 Primers were developed from an O. mykiss cloned sequence (4). nka ␣1a, nka ␣1b, nkcc1, cftr1, and ef1␣ primers were identical to those previously described (42).…”

Section: Methodsmentioning

confidence: 99%

“…There is an overall shift from an ion-absorptive mode in freshwater (FW) to an ion-secretory mode in seawater (SW), which among other details (see Ref. 29,49) includes an important differential regulation of branchial ion transport proteins, including Na ϩ -K ϩ -ATPase (Nka) isoforms, Na ϩ -K ϩ -2Cl Ϫ cotransporter (Nkcc), cystic fibrosis transmembrane conductance regulator (Cftr), H ϩ -ATPase, and Cl Ϫ /HCO 3 Ϫ exchanger (Slc26a6) (4,27,45,63,66,70). This regulation is controlled by multiple signaling events, including long-term endocrine transcriptional effectors (e.g., cortisol, growth hormone and prolactin) and rapid but short-term neurotransmitters of the adrenergic system (e.g., catecholamines) (15,44,50,52).…”

Section: Introductionmentioning

confidence: 99%

Dynamic changes in nitric oxide synthase expression are involved in seawater acclimation of rainbow troutOncorhynchus mykiss

Gerber

Frank

Madsen

2018

American Journal of Physiology-Regulatory, Integrative and Comp

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Recent research has shown that nitric oxide (NO) produced by nitric oxide synthases (NOS) is an inhibitor of ion transporter activity and a modulator of epithelial ion transport in fish, but little is known on changes in the NOS/NO system during osmotic stress. We hypothesized that the NOS/NO system responds to salinity changes as an integrated part of the acclimation process. Expression and localization of nos1/Nos1 and nos2/Nos2 were investigated in gill, kidney, and intestine of freshwater (FW)- and seawater (SW)-transferred trout using quantitative PCR, Western blotting, and immunohistochemistry, along with expressional changes of major ion transporters in the gill. The classical branchial ion transporters showed expected expressional changes upon SW transfer, there among a rapid decrease in Slc26a6 mRNA, coding a branchial Cl/[Formula: see text] exchanger. There was a major downregulation of nos1/ nos2/Nos2 expression in the gill during SW acclimation. A significant decrease in plasma nitrite supported an overall decreased Nos activity and NO production. In the middle intestine, Nos1 was upregulated during SW acclimation, whereas no changes in nos/Nos expression were observed in the posterior intestine and the kidney. Nos1 was localized along the longitudinal axis of the gill filament, beneath smooth muscle fibers of the intestine wall and in blood vessel walls of the kidney. Nos2 was localized within the epithelium adjacent to the gill filament axis and in hematopoietic tissues of the kidney. We conclude that downregulation of branchial NOS is integrated to the SW acclimation process likely to avoid the inhibitory effects of NO on active ion extrusion.

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“…For example, the accessory cell signature included highly restricted expression of Slc26a6, an apical membrane Cl -/HCO3 exchanger, associated with gill function but until now misattributed to expression within MRCs 25,26 . We were interested to note that the markers defining the erythrocyte population, including beta-globin, were expressed widely among all cell types.…”

Section: A Single-nuclei Survey Of Atlantic Salmon Gill Cellsmentioning

confidence: 99%

A single nuclei transcriptomic analysis of the Atlantic salmon gill through smoltification and seawater transfer

West

Mizoro

Wood

et al. 2020

Preprint

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Anadromous salmonids begin life adapted to the freshwater environments of their natal streams before a developmental transition, known as smoltification, transforms them into marine-adapted fish. In the wild, the extending photoperiods of spring stimulates smoltification, typified by radical reprogramming of the gill from an ion-absorbing organ to ion-excreting organ. Prior work has highlighted the role of specialized “mitochondrion-rich” cells in delivering this phenotype. However, transcriptomic studies identify thousands of smoltification-driven differentially regulated genes, indicating that smoltification causes a multifaceted, multicellular change; but direct evidence of this is lacking.Here, we use single-nuclei RNAseq to characterize the Atlantic salmon gill during smoltification and seawater transfer. We identify 20 distinct clusters of nuclei, including known, but also novel gill cell types. These data allow us to isolate cluster-specific, smoltification-induced changes in gene expression. We also show how cellular make-up of the gill changes through smoltification. As expected we noted an increase in the proportion of seawater mitochondrion-rich cells, however, we also identify a reduction of several immune-related cells. Overall, our results provide unrivaled detail of the cellular complexity in the gill, and suggest that smoltification triggers unexpected immune reprogramming directly preceding seawater entry.

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Mechanisms of Cl− uptake in rainbow trout: Cloning and expression of slc26a6, a prospective Cl−/HCO3− exchanger

Cited by 29 publications

References 39 publications

Molecular mechanisms for intestinal HCO₃^-secretion and its regulation by guanylin in seawater-acclimated eels

Molecular mechanisms for intestinal HCO₃^-secretion and its regulation by guanylin in seawater-acclimated eels

Dynamic changes in nitric oxide synthase expression are involved in seawater acclimation of rainbow troutOncorhynchus mykiss

A single nuclei transcriptomic analysis of the Atlantic salmon gill through smoltification and seawater transfer

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Mechanisms of Cl− uptake in rainbow trout: Cloning and expression of slc26a6, a prospective Cl−/HCO3− exchanger

Cited by 29 publications

References 39 publications

Molecular mechanisms for intestinal HCO3-secretion and its regulation by guanylin in seawater-acclimated eels

Molecular mechanisms for intestinal HCO3-secretion and its regulation by guanylin in seawater-acclimated eels

Dynamic changes in nitric oxide synthase expression are involved in seawater acclimation of rainbow troutOncorhynchus mykiss

A single nuclei transcriptomic analysis of the Atlantic salmon gill through smoltification and seawater transfer

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Molecular mechanisms for intestinal HCO₃^-secretion and its regulation by guanylin in seawater-acclimated eels

Molecular mechanisms for intestinal HCO₃^-secretion and its regulation by guanylin in seawater-acclimated eels