Regulation of gill claudin paralogs by salinity, cortisol and prolactin in Mozambique tilapia (Oreochromis mossambicus)

Tipsmark, Christian K.; Breves, Jason P.; Rabeneck, D. Brett; Trubitt, Rebecca T.; Lerner, Darren T.; Grau, E. Gordon

doi:10.1016/j.cbpa.2016.05.014

Cited by 17 publications

(13 citation statements)

References 47 publications

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“…The effects of cortisol appear to be complex and context dependent, and increased cortisol levels are associated with both hyper- and hyposmotic challenge. In Omoss and Onil cortisol has been observed to both enhance, suppress, or act independently of the effects of prolactin or growth hormone on osmoregulatory proteins [47-49]. Consistent with this, cortisol appears to have been an important factor in both of our treatments, because the GO term response to corticosteroid appeared in the DE vs.…”

Section: Discussionsupporting

confidence: 62%

“…The coordinated actions of prolactin, GH/IGF, and cortisol mediate paracellular permeability by regulating tight junction proteins [49,58]. In freshwater, these junctions allow little movement of ions or water (“tight”), whereas in saline conditions paracellular junctions promote the selective escape of ions down transepithelial gradients [“leaky”;, 58].…”

Section: Discussionmentioning

confidence: 99%

“…We observed contrasting DE in 25 of the 37 “cichlid+” genes identified as claudins: 14 up and 11 down (Figure 3; Supplemental Tables 2 and 3). Poor characterization of these proteins in fishes, and unclear homology with human proteins ( Onil have ~58 CLDN genes; humans ~28) precludes us from predicting their effects on permeability [but see, 49]. By contrast, four of seven MARVEL domain-containing paralogs ( OCLN, MARVELD2, MARVELD3 ) were up-regulated, and the others were SE, indicating that tight junctions were becoming ‘tighter’ in the blackwater treatment, and more ‘leaky’ in whitewater.…”

Section: Discussionmentioning

confidence: 99%

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Osmoregulation in freshwaters: Gene expression in the gills of a Neotropical cichlid in contrasting pH and ionic environments

Willis

Saenz

Wang

et al. 2018

Preprint

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22 24 25 Abstract 26 27 Freshwater habitats of the Neotropics exhibit a gradient from relatively neutral, ion-rich 28 whitewater to acidic, ion-poor blackwater. Closely related species often show 29 complementary distributions among ionic habitats, suggesting that adaptation to divergent 30 osmoregulatory environments may be an important driver of Neotropical fish diversity. 31 However, little is known about the evolutionary tradeoffs involved in ionoregulation across 32 distinct freshwater environments. Here, we surveyed gill mRNA expression of Cichla 33 ocellaris var. monoculus, a Neotropical cichlid, to examine cellular and physiological 34 responses to experimental conditions mimicking whitewater and blackwater.35 Gene ontology enrichment of expressed genes indicated that the gills were remodeled 36 during both forms of environmental challenge, with changes biased towards the cellular 37 membrane. We observed expression of signaling pathways from both the acute and 38 extended response phases, including evidence that growth hormone (GH) may mediate 39 osmoregulation in whitewater through paracrine expression of insulin-like growth factor I 40 (IGF-I), but not through the GH receptor, which instead showed correlated up-regulation 41 with the prolactin receptor and insulin-like growth factor II in blackwater.42 Differential expression of genes related to paracellular tight junctions and transcellular ion 43 transport showed responses similar to euryhaline fishes in fresh versus seawater, with 44 some exceptions, suggesting that relaxed ion retention via the gills, possibly mediated by 45 the GH/IGF-I axis, is a strong candidate for evolutionary modification in whitewater and 46 blackwater endemic populations. In each osmoregulatory domain, we saw examples of 3 47 contrasting differential expression of paralogs of genes that are single copy in most 48 terrestrial vertebrates, indicating that adaption by fishes to diverse physicochemcial 49 environments has capitalized on diversification of osmoregulatory gene families. 50 51 53 54 Running title: gene expression across an Amazon ionic gradient 4 55 56 Introduction 57 58Gill surfaces of fishes must be thin in order to facilitate gas exchange, but this also 59 promotes rapid gain or loss of ions and water with the environment -a functional tradeoff 60 called the 'osmo-respiratory compromise' [1]. Management of osmotic and ionic stress is 61 therefore a major biological challenge for fishes and has been estimated to account for 2-62 20% of resting metabolic rate [2]. A great deal has been learned about mechanisms 63 involved in osmoregulation from studies of euryhaline fishes exposed to salinity gradients 64 [3]; however, these fishes represent a small fraction of fish diversity, as the vast majority 65 are stenohaline. Among these, freshwater fishes are challenged to maintain homeostasis in 66 the face of wide variation in solute concentration, pH, and other chemical factors, but are 67 less well-studied than their euryhaline counterparts [4]. Moreover, it is clear...

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Section: Discussionsupporting

confidence: 62%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Osmoregulation in freshwaters: Gene expression in the gills of a Neotropical cichlid in contrasting pH and ionic environments

Willis

Saenz

Wang

et al. 2018

Preprint

View full text Add to dashboard Cite

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“…Claudins play an important regulatory role in the adaptation of fishes to salinity via tight junctions (Tipsmark et al, 2016). Tilapia transferred from freshwater to seawater showed increased transcription levels of claudins, Na + ‐K + ‐ATPase, and Na + ‐K + ‐2Cl ‐ cotransporters with increased plasma osmotic pressure (Tipsmark et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Chromosome‐level genome assembly for the largemouth bass Micropterus salmoides provides insights into adaptation to fresh and brackish water

Sun

Dong

et al. 2020

Molecular Ecology Resources

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Largemouth bass (LMB; Micropterus salmoides) has been an economically important fish in North America, Europe, and China. This study obtained a chromosome‐level genome assembly of LMB using PacBio and Hi‐C sequencing. The final assembled genome is 964 Mb, with contig N50 and scaffold N50 values of 1.23 Mb and 36.48 Mb, respectively. Combining with RNA sequencing data, we annotated a total of 23,701 genes. Chromosomal assembly and syntenic analysis proved that, unlike most Perciformes with the popular haploid chromosome number of 24, LMB has only 23 chromosomes (Chr), among which the Chr1 seems to be resulted from a chromosomal fusion event. LMB is phylogenetically closely related to European seabass and spotted seabass, diverging 64.1 million years ago (mya) from the two seabass species. Eight gene families comprising 294 genes associated with ionic regulation were identified through positive selection, transcriptome and genome comparisons. These genes involved in iron facilitated diffusion (such as claudin, aquaporins, sodium channel protein and so on) and others related to ion active transport (such as sodium/potassium‐transporting ATPase and sodium/calcium exchanger). The claudin gene family, which is critical for regulating cell tight junctions and osmotic homeostasis, showed a significant expansion in LMB with 27 family members and 68 copies for salinity adaptation. In summary, we reported the first high‐quality LMB genome, and provided insights into the molecular mechanisms of LMB adaptation to fresh and brackish water. The chromosome‐level LMB genome will also be a valuable genomic resource for in‐depth biological and evolutionary studies, germplasm conservation and genetic breeding of LMB.

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“…Claudins are tight junction membrane proteins that are expressed in epithelia and endothelia, and form paracellular barriers and pores that determine tight junction permeability (Gunzel & Yu, 2013). Earlier studies indicate that expression variation in claudins is important in permeability changes associated with salinity acclimation and possibly the formation of deeper tight junctions in the gills of freshwater fish (Bagherie‐Lachidan, Wright, & Kelly, 2008; Kolosov, Bui, Chasiotis, & Kelly, 2013; Madsen & Tipsmark, 2008; Marshall et al., 2018; Tipsmark, Baltzegar, Ozden, Grubb, & Borski, 2008; Tipsmark et al., 2016). Our results suggest that both expression changes and genetic variation in CLDND1 might play a key role in the repeated marine‐freshwater divergence in nine‐spined sticklebacks.…”

Section: Discussionmentioning

confidence: 99%

Population transcriptomics reveals weak parallel genetic basis in repeated marine and freshwater divergence in nine‐spined sticklebacks

Wang

Zhang

et al. 2020

Molecular Ecology

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The degree to which adaptation to similar selection pressures is underlain by parallel versus non-parallel genetic changes is a topic of broad interest in contemporary evolutionary biology. Sticklebacks provide opportunities to characterize and compare the genetic underpinnings of repeated marine-freshwater divergences at both intraand interspecific levels. While the degree of genetic parallelism in repeated marinefreshwater divergences has been frequently studied in the three-spined stickleback (Gasterosteus aculeatus), much less is known about this in other stickleback species.Using a population transcriptomic approach, we identified both genetic and gene expression variations associated with marine-freshwater divergence in the nine-spined stickleback (Pungitius pungitius). Specifically, we used a genome-wide association study approach, and found that ~1% of the total 173,491 identified SNPs showed marine-freshwater ecotypic differentiation. A total of 861 genes were identified to have SNPs associated with marine-freshwater divergence, but only 12 of these genes have also been reported as candidates associated with marine-freshwater divergence in the three-spined stickleback. Hence, our results indicate a low degree of interspecific genetic parallelism in marine-freshwater divergence. Moreover, 1,578 genes in the brain and 1,050 genes in the liver were differentially expressed between marine and freshwater nine-spined sticklebacks, ~5% of which have also been identified as candidates associated with marine-freshwater divergence in the three-spined stickleback. However, only few of these (e.g., CLDND1) appear to have been involved in repeated marine-freshwater divergence in nine-spined sticklebacks. Taken together, the results indicate a low degree of genetic parallelism in repeated marine-freshwater divergence both at intra-and interspecific levels. K E Y W O R D S expression divergence, Gasterosteidae, genetic parallelism, RNA-seq, SNP | 1643 WANG et Al.

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Regulation of gill claudin paralogs by salinity, cortisol and prolactin in Mozambique tilapia (Oreochromis mossambicus)

Cited by 17 publications

References 47 publications

Osmoregulation in freshwaters: Gene expression in the gills of a Neotropical cichlid in contrasting pH and ionic environments

Osmoregulation in freshwaters: Gene expression in the gills of a Neotropical cichlid in contrasting pH and ionic environments

Chromosome‐level genome assembly for the largemouth bass Micropterus salmoides provides insights into adaptation to fresh and brackish water

Population transcriptomics reveals weak parallel genetic basis in repeated marine and freshwater divergence in nine‐spined sticklebacks

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