The Multifunctional Fish Gill: Dominant Site of Gas Exchange, Osmoregulation, Acid-Base Regulation, and Excretion of Nitrogenous Waste

Evans, David H.; Piermarini, Peter M.; Choe, Keith P.

doi:10.1152/physrev.00050.2003

Cited by 2,235 publications

(1,856 citation statements)

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“…The teleost fish gill epithelium is comprised of at least five types of cells, including respiratory pavement cells, ion transporting ionocytes (also termed 'chloride cells'), mucous cells, and neural epithelial cells [36]. These are mounted on a cartilage scaffold forming the gill filaments and secondary lamellae where gas and ion exchange with water takes place [36].…”

Section: Discussionmentioning

confidence: 99%

Dynamic transcriptomic profiles of zebrafish gills in response to zinc depletion

et al. 2010

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BackgroundZinc deficiency is detrimental to organisms, highlighting its role as an essential micronutrient contributing to numerous biological processes. To investigate the underlying molecular events invoked by zinc depletion we performed a temporal analysis of transcriptome changes observed within the zebrafish gill. This tissue represents a model system for studying ion absorption across polarised epithelial cells as it provides a major pathway for fish to acquire zinc directly from water whilst sharing a conserved zinc transporting system with mammals.ResultsZebrafish were treated with either zinc-depleted (water = 2.61 μg L-1; diet = 26 mg kg-1) or zinc-adequate (water = 16.3 μg L-1; diet = 233 mg kg-1) conditions for two weeks. Gill samples were collected at five time points and transcriptome changes analysed in quintuplicate using a 16K oligonucleotide array. Of the genes represented the expression of a total of 333 transcripts showed differential regulation by zinc depletion (having a fold-change greater than 1.8 and an adjusted P-value less than 0.1, controlling for a 10% False Discovery Rate). Down-regulation was dominant at most time points and distinct sets of genes were regulated at different stages. Annotation enrichment analysis revealed that 'Developmental Process' was the most significantly overrepresented Biological Process GO term (P = 0.0006), involving 26% of all regulated genes. There was also significant bias for annotations relating to development, cell cycle, cell differentiation, gene regulation, butanoate metabolism, lysine degradation, protein tyrosin phosphatases, nucleobase, nucleoside and nucleotide metabolism, and cellular metabolic processes. Within these groupings genes associated with diabetes, bone/cartilage development, and ionocyte proliferation were especially notable. Network analysis of the temporal expression profile indicated that transcription factors foxl1, wt1, nr5a1, nr6a1, and especially, hnf4a may be key coordinators of the homeostatic response to zinc depletion.ConclusionsThe study revealed the complex regulatory pathways that allow the organism to subtly respond to the low-zinc condition. Many of the processes affected reflected a fundamental restructuring of the gill epithelium through reactivation of developmental programs leading to stem cell differentiation. The specific regulation of genes known to be involved in development of diabetes provides new molecular links between zinc deficiency and this disease. The present study demonstrates the importance of including the time-dimension in microarray studies.

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Section: Discussionmentioning

confidence: 99%

Dynamic transcriptomic profiles of zebrafish gills in response to zinc depletion

et al. 2010

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“…So far, at least two pathways have been proposed for the apical transport of Na + in fish gill cells (Hirose et al, 2003;Perry et al, 2003;Evans et al, 2005): (1) an apical V-type H + -ATPase electrically linked to Na + absorption via the epithelial Na + channel (ENaC) and (2) an electroneutral exchange of Na + and H + via an apical Na + /H + exchanger (NHE). As the uptake of Na + via passive exchange with H + has been questioned on thermodynamic grounds (Kirschner, 1983;Avella and Bornancin, 1989), most of the latter studies favoured the major role of H + -ATPase in acid-secretion and Na + -uptake mechanisms.…”

Section: H + -Atpase Rich (Hr) Cellsmentioning

confidence: 99%

“…Accordingly, immunocytochemistry (ICC) with heterologous or homologous antibodies and in situ hybridization (ISH) with RNA probes were used to identify the existence of V-type H + -ATPase in fish gills. The distribution of the enzyme in ionocytes and/or pavement cells has been debated, and this has been ascribed to antibody specificities, and/or differences in species, populations or acclimation conditions [see detailed discussion by Evans and colleagues (Evans et al, 2005)]. Under such controversy, we raised the question of whether there is any in vivo evidence to demonstrate the acid-secretion function in cells expressing V-type H + -ATPase.…”

Section: H + -Atpase Rich (Hr) Cellsmentioning

confidence: 99%

“…As discussed above, NCC cells may be one of the possible ionocytes responsible for Cl -uptake via the apical NCC and basolateral ClC and NKA. On the other hand, it was proposed that the apical Cl -/HCO 3 -exchanger is the major player in the mechanism of Cl -uptake linked with basal secretion in fish gills, and anion exchanger (AE) 1 was one of the candidates proposed (Evans et al, 2005;Hwang and Lee, 2007;Evans, 2008). However, ISH and ICC data for the existence of AE1 in teleost gills (Sullivan et al, 1996;Wilson et al, 2000) were controversial when considering the specificity of the antibody or probe used and the absence of evidence for AE1 on the apical membrane of other acid/base-secreting epithelia Tresguerres et al, 2006).…”

Section: Other Pathways Anion Exchangermentioning

confidence: 99%

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Ion uptake and acid secretion in zebrafish (Danio rerio)

Hwang

2009

Journal of Experimental Biology

164

165

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SummaryTransepithelial transport is one of the major processes involved in the mechanism of homeostasis of body fluids in vertebrates including fish. The current models of ion regulation in fish gill ionocytes have been proposed mainly based on studies in traditional model species like salmon, trout, tilapia, eel and killifish, but the mechanisms are still being debated due to the lack of convincing molecular physiological evidence. Taking advantage of plentiful genetic databases for zebrafish, we studied the molecular/cellular mechanisms of ion regulation in fish skin/gills. In our recently proposed model, there are at least three subtypes of ionocytes in zebrafish skin/gills: Na + -K + -ATPase-rich (NaR), Na + -Cl -cotransporter (NCC) and H + -ATPase-rich (HR) cells. Specific isoforms of transporters and enzymes have been identified as being expressed by these ionocytes: zECaC, zPMCA2 and zNCX1b by NaR cells; zNCC gill form by NCC cells; and zH + -ATPase, zNHE3b, zCA2-like a and zCA15a by HR cells. Serial molecular physiological experiments demonstrated the distinct roles of these ionocytes in the transport of various ions: HR, NaR and NCC cells are respectively responsible for acid secretion/Na + uptake, Ca 2+ uptake and Cl -uptake. The expression, regulation and function of transporters in HR and NaR cells are much better understood than those in NCC cells. The basolateral transport pathways in HR and NCC cells are still unclear, and the driving forces for the operations of apical NHE and NCC are another unresolved issue. Studies on zebrafish skin/gill ionocytes are providing new insights into fish ion-regulatory mechanisms, but the zebrafish model cannot simply be applied to other species because of species differences and a lack of sufficient molecular physiological evidence in other species.

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“…2). Gills play a central role in the physiology of fishes, including respiration, acid base balance, nitrogenous waste excretion, and ionoregulation (Evans et al 2005). Therefore, gills are an ideal tissue to use when examining the transcriptomic responses to water chemistry in fish (Oleksiak 2011;Xu et al 2013b;Lam et al 2014).…”

mentioning

confidence: 99%

Genomics of Adaptation to Multiple Concurrent Stresses: Insights from Comparative Transcriptomics of a Cichlid Fish from One of Earth’s Most Extreme Environments, the Hypersaline Soda Lake Magadi in Kenya, East Africa

et al. 2015

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The Magadi tilapia (Alcolapia grahami) is a cichlid fish that inhabits one of the Earth's most extreme aquatic environments, with high pH ( -10), salinity (-60 % of seawater), high temperatures ( -40 °C), and fluctuating oxygen regimes. The Magadi tilapia evolved several unique behavioral, physiological, and anatomical adaptations, some of which are constituent and thus retained in freshwater conditions. We conducted a transcriptomic analysis on A. grahami to study the evolutionary basis of tolerance to multiple stressors. To identify the adaptive regulatory changes associated with stress responses, we massively sequenced gill transcriptomes (RNAseq) from wild and freshwater-acclimated specimens of A. grahami. As a control, corresponding transcriptome data from Oreochromis leucostictus, a closely related freshwater species, were generated. We found expression differences in a large number of genes with known functions related to osmoregulation, energy metabolism, ion transport, and chemical detoxification. Over-representation of metabolism-related gene ontology terms in wild individuals compared to laboratory-acclimated specimens suggested that freshwater conditions greatly decrease the metabolic requirements of this species. Twenty-five genes with diverse physiological functions related to responses to water stress showed signs of divergent natural selection between the Magadi tilapia and its freshwater relative, which shared a most recent common ancestor only about four million years ago. The complete set of genes responsible for urea excretion was identified in the gill transcriptome of A. grahami, making it the only fish species to have a functional ornithine-urea cycle pathway in the gills a major innovation for increasing nitrogenous waste efficiency.

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The Multifunctional Fish Gill: Dominant Site of Gas Exchange, Osmoregulation, Acid-Base Regulation, and Excretion of Nitrogenous Waste

Cited by 2,235 publications

References 773 publications

Dynamic transcriptomic profiles of zebrafish gills in response to zinc depletion

Dynamic transcriptomic profiles of zebrafish gills in response to zinc depletion

Ion uptake and acid secretion in zebrafish (Danio rerio)

Genomics of Adaptation to Multiple Concurrent Stresses: Insights from Comparative Transcriptomics of a Cichlid Fish from One of Earth’s Most Extreme Environments, the Hypersaline Soda Lake Magadi in Kenya, East Africa

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