Tricellulin, occludin and claudin-3 expression in salmon intestine and kidney during salinity adaptation (original) (raw)
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Journal of Comparative Physiology B-biochemical Systemic and Environmental Physiology, 2011
In water of varying ion content, the gills and kidney of fishes contribute significantly to the maintenance of salt and water balance. However, little is known about the molecular architecture of the tight junction (TJ) complex and the regulation of paracellular permeability characteristics in these tissues. In the current studies, puffer fish (Tetraodon biocellatus) were acclimated to freshwater (FW), seawater (SW) or ion-poor freshwater (IPW) conditions. Following acclimation, alterations in systemic endpoints of hydromineral status were examined in conjunction with changes in gill and kidney epithelia morphology/morphometrics, as well as claudin TJ protein mRNA abundance. T. biocellatus were able to maintain endpoints of hydromineral status within relatively tight limits across the broad range of water ion content examined. Both gill and kidney tissue exhibited substantial alterations in morphology as well as claudin TJ protein mRNA abundance. These responses were particularly pronounced when comparing fish acclimated to SW versus those acclimated to IPW. TEM observations of IPW-acclimated fish gills revealed the presence of cells that exhibited the typical characteristics of gill mitochondria-rich cells (e.g. voluminous, Na+-K+-ATPase-immunoreactive, exposed to the external environment at the apical surface), but were not mitochondria-rich. To our knowledge, this type of cell has not previously been described in hyperosmoregulating fish gills. Furthermore, modifications in the morphometrics and claudin mRNA abundance of kidney tissue support the notion that spatial alterations in claudin TJ proteins along the nephron of fishes will likely play an important role in the regulation of salt and water balance in these organisms.
AJP: Regulatory, Integrative and Comparative Physiology, 2008
In euryhaline teleosts, permeability changes in gill epithelia are essential during acclimation to changed salinity. This study examined expression patterns of branchial tight junction proteins called claudins, which are important determinants of ion selectivity and general permeability in epithelia. We identified Atlantic salmon genes belonging to the claudin family by screening expressed sequence tag libraries available at NCBI, and classification was performed with the aid of maximum likelihood analysis. In gill libraries, five isoforms (10e, 27a, 28a, 28b, and 30) were present, and quantitative PCR analysis confirmed tissue-specific expression in gill when compared with kidney, intestine, heart, muscle, brain, and liver. Expression patterns during acclimation of freshwater salmon to seawater (SW) and during the smoltification process were examined. Acclimation to SW reduced the expression of claudin 27a and claudin 30 but had no overall effect on claudin 28a and claudin 28b. In ...
Journal of Experimental Biology, 2010
SUMMARY Osmotic balance in fish is maintained through the coordinated regulation of water and ion transport performed by epithelia in intestine, kidney and gill. In the current study, six aquaporin (AQP) isoforms found in Atlantic salmon (Salmo salar) were classified and their tissue specificity and mRNA expression in response to a hyperosmotic challenge and during smoltification were examined. While AQP-1a was generic, AQP-1b had highest expression in kidney and AQP-3 was predominantly found in oesophagus, gill and muscle. Two novel teleost isoforms, AQP-8a and -8b, were expressed specifically in liver and intestinal segments, respectively. AQP-10 was predominantly expressed in intestinal segments, albeit at very low levels. Transfer from freshwater (FW) to seawater (SW) induced elevated levels of intestinal AQP-1a, -1b and -8b mRNA, whereas only AQP-8b was stimulated during smoltification. In kidney, AQP-1a, -3 and -10 were elevated in SW whereas AQP-1b was reduced compared with F...
Comparative Biochemistry and Physiology A-molecular & Integrative Physiology, 2010
In fishes, variation in paracellular permeability is important for regulating salt and water balance. Paracellular permeability is maintained by TJs in vertebrate epithelia. This study examined the spatial distribution and effects of salinity on claudin-3 isoform mRNA expression and abundance along the gastrointestinal (GI) tract of the euryhaline puffer fish (Tetraodon nigroviridis) and related these to morphological heterogeneity of the TJ complex. The puffer fish GI tract was divided into three regions (anterior, middle and posterior) and four isoforms of claudin-3 (Tncldn3a, Tncldn3b, Tncldn3c and Tncldn3d) were found to be expressed in each section. The effect of freshwater (FW) or seawater (SW) acclimation on regional 1) Tncldn3 isoform mRNA abundance, 2) TJ complex morphology and 3) Na + -K + -ATPase (NKA) activity was examined. In situ hybridization indicated that all Tncldn3 isoforms localized to the mucosal epithelium in the intestine. The mRNA abundance of Tncldn3 isoforms varied spatially along the GI tract. Furthermore, region as well as isoform specific alterations in mRNA abundance could be observed along the GI tract in response to salinity change. Qualitative TEM observations suggested that the depth of TJ complexes increased from anterior to posterior along the GI tract and that TJ complexes in the GI tract of FW fish were deeper than those in SW. NKA activity increased from anterior to posterior in fish acclimated to FW, whereas activity in fish acclimated to SW was uniformly high along the length of the intestine. Taken together data; (1) suggest a progressive decrease in epithelial permeability from anterior to posterior along the longitudinal axis of the puffer fish GI tract, (2) indicate that claudin-3 protein isoforms may play a role in regulating paracellular movement of solutes across this epithelium, and (3) provide further evidence that claudin-3 proteins are involved in the homeostatic control of salt and water balance in fishes.
The Journal of experimental biology, 2014
Expression profiles of claudin-6, -10d and -10e in the euryhaline teleost fish Tetraodon nigroviridis revealed claudin-6 in brain, eye, gill and skin tissue, while claudin-10d and -10e were found in brain, gill and skin only. In fishes, the gill and skin are important tissue barriers that interface directly with surrounding water, but these organs generally function differently in osmoregulation. Therefore, roles for gill and skin claudin-6, -10d and -10e in the osmoregulatory strategies of T. nigroviridis were investigated. In the gill epithelium, claudin-6, -10d and -10e co-localized with Na(+)-K(+)-ATPase immunoreactive (NKA-ir) ionocytes, and differences in sub-cellular localization could be observed in hypoosmotic (freshwater, FW) versus hyperosmotic (seawater, SW) environments. Claudin-10d and -10e abundance increased in the gills of fish acclimated to SW versus FW, while claudin-6 abundance decreased in the gills of fish acclimated to SW. Taken together with our knowledge of ...
Gene, 2020
Acclimation to low salinities is a vital physiological challenge for euryhaline fish as the European sea bass Dicentrarchus labrax. This species undertakes seasonal migrations towards lagoons and estuaries where a wide range of salinity variations occur along the year. We have previously reported intraspecific differences in freshwater tolerance, with an average 30% mortality rate. In this study, we bring new evidence of mechanisms underlying freshwater tolerance in sea bass at gill and kidney levels. In fresh water (FW), intraspecific differences in mRNA expression levels of several ion transporters and prolactin receptors were measured. We showed that the branchial Cl-/HCO3-anion transporter (slc26a6c) was over-expressed in freshwater intolerant fish, probably as a compensatory response to low blood chloride levels and potential metabolic alkalosis. Moreover, prolactin receptor a (prlra) and Na+/Cl-cotransporter (ncc1) but not ncc-2a expression seemed to be slightly increased and highly variable between individuals in freshwater intolerant fish. In the posterior kidney, freshwater intolerant fish exhibited differential expression levels of slc26 anion transporters and Na+/K+/2Cl-cotransporter 1b (nkcc1b). Lower expression levels of prolactin receptors (prlra, prlrb) were measured in posterior kidney which probably contributes to the failure in ion reuptake at the kidney level. Freshwater intolerance seems to be a consequence of renal failure of ion reabsorption, which is not sufficiently compensated at the branchial level. Highlights ► Freshwater intolerance is not due to an altered ion uptake at the gills. ► Cl − uptake-related genes are less expressed in the kidney of freshwater (FW) intolerant fish vs FW tolerant fish. ► Branchial and renal prolactin receptors are differentially expressed between freshwater tolerance phenotypes.
Functional characterization and localization of a gill-specific claudin isoform in Atlantic salmon
American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 2011
Claudins are the major determinants of paracellular epithelial permeability in multicellular organisms. In Atlantic salmon ( Salmo salar L.), we previously found that mRNA expression of the abundant gill-specific claudin 30 decreases during seawater (SW) acclimation, suggesting that this claudin is associated with remodeling of the epithelium during salinity change. This study investigated localization, protein expression, and function of claudin 30. Confocal microscopy showed that claudin 30 protein was located at cell-cell interfaces in the gill filament in SW- and fresh water (FW)-acclimated salmon, with the same distribution, overall, as the tight junction protein ZO-1. Claudin 30 was located at the apical tight junction interface and in cell membranes deeper in the epithelia. Colocalization with the α-subunit of the Na+-K+-ATPase was negligible, suggesting limited association with mitochondria-rich cells. Immunoblotting of gill samples showed lower claudin 30 protein expression...
Occludin immunolocalization and protein expression in goldfish
Journal of Experimental Biology, 2008
Tight junctions (TJs) are an integral component of models illustrating ion transport mechanisms across fish epithelia; however, little is known about TJ proteins in fishes. Using immunohistochemical methods and Western blot analysis, we examined the localization and expression of occludin, a transmembrane TJ protein, in goldfish tissues. In goldfish gills, discontinuous occludin immunostaining was detected along the edges of secondary gill lamellae and within parts of the interlamellar region that line the lateral walls of the central venous sinus. In the goldfish intestine, occludin immunolocalized in a TJ-specific distribution pattern to apical regions of columnar epithelial cells lining the intestinal lumen. In the goldfish kidney, occludin was differentially expressed in discrete regions of the nephron. Occludin immunostaining was strongest in the distal segment of the nephron, moderate in the collecting duct and absent in the proximal segment. To investigate a potential role for occludin in the maintenance of the hydromineral balance of fishes, we subjected goldfish to 1, 2 and 4 weeks of food deprivation, and then examined the endpoints of hydromineral status, Na + ,K + -ATPase activity and occludin protein expression in the gills, intestine and kidney. Occludin expression altered in response to hydromineral imbalance in a tissue-specific manner suggesting a dynamic role for this TJ protein in the regulation of epithelial permeability in fishes.
The role of aquaporin 3 in teleost fish
Comparative Biochemistry and Physiology A-molecular & Integrative Physiology, 2007
The aquaporin isoform, AQP3 has now been identified in a number of different teleost fish species, with additional DNA sequence information on AQP3 genes in further fish species available in genome databases. In zebrafish (Danio rerio), the AQP3 gene is present as two duplicate isoforms resulting from a teleostean fish genome-wide duplication. A further splicoform/isoform has also been identified in rainbow trout (Oncorhynchus mykiss). The identification of these AQP3 isoforms in other fish species is consequently explored. The role of AQP3 in physiological/osmoregulatory processes, in various teleost organs is then described. In teleost gill, AQP3 is expressed in 'chloride' cells, and in some species, in other epithelial cell types, where it may have a number of different functions including the prevention of dehydration. In eel esophagus, immunohistochemistry shows that AQP3 is expressed in surface epithelial cells in the anterior esophagus, but in mucus cells within the epithelium of the posterior esophagus. In eel intestine, AQP3 is found in macrophage-like cells and probably plays no part in osmoregulatory processes. In the rectum, as in the posterior esophagus AQP3 is expressed in mucus cells. In eel kidney, AQP3 is expressed in a subset of renal tubules, and localizes to the apical pole of tubule cells. There is no apparent change in the location or protein abundance of renal AQP3 following the acclimation of eels from freshwater to seawater. Comparative Biochemistry and Physiology, Part A xx (2006) xxxxxx + MODEL CBA-07981; No of Pages 10 www.elsevier.com/locate/cbpa