Claudin-3 tight junction proteins in<i>Tetraodon nigroviridis</i>: cloning, tissue-specific expression, and a role in hydromineral balance

Bagherie-Lachidan, Mazdak; Wright, Stephen I.; Kelly, Scott P.

doi:10.1152/ajpregu.00039.2008

Cited by 60 publications

(44 citation statements)

References 41 publications

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“…Scott et al (21) proposed that reducing the paracellular loss of chloride was a probable mechanism contributing to population variation in FW tolerance in F. heteroclitus. The strong coordinated regulation of these genes in the gill is consistent with the immediate challenge of regulating paracellular ion loss when challenged with a hypoosmotic environment (22,23).…”

Section: Resultssupporting

confidence: 53%

Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient

Whitehead

Roach

Zhang

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

195

224

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Adaptive variation tends to emerge clinally along environmental gradients or discretely among habitats with limited connectivity. However, in Atlantic killifish (Fundulus heteroclitus), a population genetic discontinuity appears in the absence of obvious barriers to gene flow along parallel salinity clines and coincides with a physiologically stressful salinity. We show that populations resident on either side of this discontinuity differ in their abilities to compensate for osmotic shock and illustrate the physiological and functional genomic basis of population variation in hypoosmotic tolerance. A population native to a freshwater habitat, upstream of the genetic discontinuity, exhibits tolerance to extreme hypoosmotic challenge, whereas populations native to brackish or marine habitats downstream of the discontinuity lose osmotic homeostasis more severely and take longer to recover. Comparative transcriptomics reveals a core transcriptional response associated with acute and acclimatory responses to hypoosmotic shock and posits unique mechanisms that enable extreme osmotic tolerance. Of the genes that vary in expression among populations, those that are putatively involved in physiological acclimation are more likely to exhibit nonneutral patterns of divergence between freshwater and brackish populations. It is not the well-known effectors of osmotic acclimation, but rather the lesser-known immediateearly responses, that appear important in contributing to population differences.adaptive acclimation | ecological genomics | microarray A tlantic killifish (Fundulus heteroclitus) occupy an extremely wide osmotic niche from freshwater to marine, and populations are distributed along steep salinity gradients in Atlantic coast estuaries. In the Chesapeake Bay, salinity gradients are distributed across hundreds of kilometers, although no obvious barriers to gene flow exist across this continuum of osmotic habitats. Because salinity is arguably the most important single physical environmental variable that delimits aquatic species distributions in nature (including Fundulus species; ref. 1), we exploit F. heteroclitus distributed along Chesapeake Bay salinity gradients as a model to discover genes and pathways that enable extreme physiological plasticity and to explore the physiological and functional genomic basis of adaptive microevolution in alternative osmotic environments.Results and Discussion Population Genetic Divergence. We characterized the genetic structure of killifish distributed along two parallel salinity gradients in Chesapeake Bay: one along the Potomac River and the other along the James River (Fig. 1A). Steep clines in allele frequency for both mitochondrial and nuclear markers were centered at nearly identical salinities along the parallel gradients (Fig. 1B). Genotype frequency clines bounded the tidal freshwater transition region (<0.5 ppt) of both rivers, where sites upstream are freshwater year-round according to 20 y of data logged from fixed monitoring stations (www.chesapeakebay.net/ data_...

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Section: Resultssupporting

confidence: 53%

Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient

Whitehead

Roach

Zhang

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

195

224

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“…In line S. P. Kelly and H. Chasiotis with this contention, both claudin-3 and -8 are considered to be barrier-promoting (or 'tightening') tight junction components in mammalian systems (Milatz et al, 2010;Yu et al, 2003). Furthermore, both claudins have previously been linked to epithelial tightening in the gills and kidney of fish (Bagherie-Lachidan et al, 2008;Bagherie-Lachidan et al, 2009;Duffy et al, 2011). However, in contrast to these observations, a primary cultured epithelium generated using puffer fish gill cells did not exhibit any alteration in claudin-8d mRNA abundance in response to cortisol treatment and, in the same preparation, claudin-3a transcript abundance decreased in response to cortisol (Bui et al, 2010).…”

Section: S P Kelly and H Chasiotismentioning

confidence: 81%

Glucocorticoid and mineralocorticoid receptors regulate paracellular permeability in a primary cultured gill epithelium

Kelly

Chasiotis

2011

Journal of Experimental Biology

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SUMMARYThe role of corticosteroid receptors (CRs) in the regulation of gill permeability was examined using a primary cultured trout gill epithelium. The epithelium expressed both glucocorticoid receptors (GR1 and GR2) and a mineralocorticoid receptor (MR), and cortisol treatment significantly increased transepithelial resistance (TER) and decreased paracellular [ 3 H]PEG-4000 flux. Epithelial permeability was unaffected by deoxycorticosterone or aldosterone. The GR antagonist RU486 as well as MR antagonists spironolactone and RU26752 significantly reduced, but did not completely block, the effects of cortisol. The MR antagonist eplerenone was without effect. Only RU486 + spironolactone or RU486 + RU26752 treatment completely suppressed the effects of cortisol. On its own, RU486 had cortisol-like effects which could be blocked by spironolactone, suggesting that although RU486 is a GR antagonist, in this system it may also have agonistic properties that are mediated through the MR. The GR agonist dexamethasone increased TER and reduced [ 3 H]PEG-4000 flux across cultured epithelia and was unaffected by MR antagonists. Therefore, alterations in transcript abundance of select tight junction (TJ) proteins were examined in response to cortisol, dexamethasone (a GR agonist) and RU486 (as a MR agonist). Occludin and claudin-7, -8d, -12 and -31 mRNA were significantly elevated in response to cortisol, dexamethasone or RU486 treatment. Claudin-3a mRNA was significantly elevated in response to cortisol or dexamethasone only, and claudin-28b and -30 mRNA were significantly altered following cortisol or RU486 treatment only. The data support a role for the GRs and MR in regulating gill permeability and suggest that TJ proteins are responsive to cortisol through both or individual CR types.

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“…However, recent studies collectively suggest that the physiology of fish gill TJs is not straightforward (for review, see Chasiotis et al, 2012b), and a small number of reports further suggest that the molecular architecture and physiological properties of TJs in the skin of adult teleosts may also be complex and perhaps more environmentally responsive than might have been expected (Bagherie-Lachidan et al, 2008;Bagherie-Lachidan et al, 2009;Loh et al, 2004). In a comprehensive analysis of the claudin (Cldn) family of TJ proteins in Fugu (=Takifugu) rubripes, Loh et al (Loh et al, 2004) reported the presence of at least 32 cldn genes in gill Claudin-6, -10d and -10e contribute to seawater acclimation in the euryhaline puffer fish Tetraodon nigroviridis Phuong Bui and Scott P. Kelly* tissue, while other TJ proteins such as occludin and ZO-1 have also been described in gills of fishes such as Atlantic salmon (Tipsmark and Madsen, 2012), goldfish (Chasiotis and Kelly, 2008;Chasiotis et al, 2009;Chasiotis and Kelly, 2011a;Chasiotis and Kelly, 2011b), killifish (Whitehead et al, 2011), rainbow trout (Chasiotis et al, 2010;Kelly and Chasiotis, 2011) and zebrafish (Clelland and Kelly, 2010;Kumai et al, 2011).…”

Section: Research Articlementioning

confidence: 99%

“…However, in the initial phase of the study, it was found that cldn-6, -10d and -10e were also selectively present in the skin of T. nigroviridis. Given that the skin, like the gill epithelium, is exposed directly to surrounding water, and that recent evidence suggests that some Cldns may be responsive to salinity change in the integument of fish (Bagherie-Lachidan et al, 2008;Bagherie-Lachidan et al, 2009), it was considered reasonable to also examine the characteristics of epidermal Cldn-6, -10d and -10e in different ionic environments.…”

Section: Research Articlementioning

confidence: 99%

“…Nevertheless, to date, approximately 36 genes encoding TJ proteins (including Cldns, occludin and ZO-1), have been reported in the skin of at least six different teleost species (Bagherie-Lachidan et al, 2008;Bagherie-Lachidan et al, 2009;Chasiotis et al, 2010;Chasiotis and Kelly, 2012;Clelland and Kelly, 2010;Loh et al, 2004;Miyamoto et al, 2009;Syakuri et al, 2013). Furthermore, transcript abundance of several putative 'tightening has been reported to increase in the skin of T. nigroviridis acclimated to a hyperosmotic environment versus those held in FW (Bagherie-Lachidan et al, 2008;BagherieLachidan et al, 2009). Similarly, in the present study, the abundance of putative barrier-forming Cldn-6 was significantly elevated in SW fish versus FW fish (Figs 6, 7).…”

Section: Research Articlementioning

confidence: 99%

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Claudin-6, -10d, and -10e contribute to seawater acclimation in the euryhaline puffer fishTetraodon nigroviridis

Bui

Kelly

2014

Journal of Experimental Biology

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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 claudin-6 and -10 function in other vertebrates, data support the idea that in SW-acclimated T. nigroviridis, these claudins are abundant in gill ionocytes, where they contribute to the formation of a Na + shunt and 'leaky' epithelium, both of which are characteristic of salt-secreting SW fish gills. Skin claudin10d and -10e abundance also increased in fish acclimated to SW versus those in FW, but so did claudin-6. In skin, claudin-6 was found to co-localize with NKA-ir cells, but claudin-10d and -10e did not. This study provides direct evidence that the gill epithelium contains salinity-responsive tight junction proteins that are abundant primarily in ionocytes. These same proteins also appear to play a role in the osmoregulatory physiology of the epidermis.

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Claudin-3 tight junction proteins inTetraodon nigroviridis: cloning, tissue-specific expression, and a role in hydromineral balance

Abstract: Bagherie-Lachidan M, Wright SI, Kelly SP. Claudin-3 tight junction proteins in Tetraodon nigroviridis: cloning, tissue-specific expression, and a role in hydromineral balance.

Cited by 60 publications

References 41 publications

Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient

Genomic mechanisms of evolved physiological plasticity in killifish distributed along an environmental salinity gradient

Glucocorticoid and mineralocorticoid receptors regulate paracellular permeability in a primary cultured gill epithelium

Claudin-6, -10d, and -10e contribute to seawater acclimation in the euryhaline puffer fishTetraodon nigroviridis

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