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      Osmoregulation in zebrafish: ion transport mechanisms and functional regulation

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          Abstract

          Fish, like mammals, have to maintain their body fluid ionic and osmotic homeostasis through sophisticated iono-/osmoregulation mechanisms, which are conducted mainly by ionocytes of the gill (the skin in embryonic stages), instead of the renal tubular cells in mammals. Given the advantages in terms of genetic database availability and manipulation, zebrafish is an emerging model for research into regulatory and integrative physiology. At least five types of ionocytes, HR, NaR, NCC, SLC26, and KS cells, have been identified to carry out Na + uptake/H + secretion/NH 4 + excretion, Ca 2+ uptake, Na +/Cl - uptake, K + secretion, and Cl - uptake/HCO 3 - secretion, respectively, through distinct sets of transporters. Several hormones, namely isotocin, prolactin, cortisol, stanniocalcin-1, calcitonin, endothelin-1, vitamin D, parathyorid hormone 1, catecholamines, and the renin-angiotensin-system, have been demonstrated to positively or negatively regulate ion transport through specific receptors at different ionocytes stages, at either the transcriptional/translational or posttranslational level. The knowledge obtained using zebrafish answered many long-term contentious or unknown issues in the field of fish iono-/osmoregulation. The homology of ion transport pathways and hormone systems also means that the zebrafish model informs studies on mammals or other animal species, thereby providing insights into related fields.

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          Most cited references202

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          The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste.

          The fish gill is a multipurpose organ that, in addition to providing for aquatic gas exchange, plays dominant roles in osmotic and ionic regulation, acid-base regulation, and excretion of nitrogenous wastes. Thus, despite the fact that all fish groups have functional kidneys, the gill epithelium is the site of many processes that are mediated by renal epithelia in terrestrial vertebrates. Indeed, many of the pathways that mediate these processes in mammalian renal epithelial are expressed in the gill, and many of the extrinsic and intrinsic modulators of these processes are also found in fish endocrine tissues and the gill itself. The basic patterns of gill physiology were outlined over a half century ago, but modern immunological and molecular techniques are bringing new insights into this complicated system. Nevertheless, substantial questions about the evolution of these mechanisms and control remain.
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            Calcium absorption across epithelia.

            Ca(2+) is an essential ion in all organisms, where it plays a crucial role in processes ranging from the formation and maintenance of the skeleton to the temporal and spatial regulation of neuronal function. The Ca(2+) balance is maintained by the concerted action of three organ systems, including the gastrointestinal tract, bone, and kidney. An adult ingests on average 1 g Ca(2+) daily from which 0.35 g is absorbed in the small intestine by a mechanism that is controlled primarily by the calciotropic hormones. To maintain the Ca(2+) balance, the kidney must excrete the same amount of Ca(2+) that the small intestine absorbs. This is accomplished by a combination of filtration of Ca(2+) across the glomeruli and subsequent reabsorption of the filtered Ca(2+) along the renal tubules. Bone turnover is a continuous process involving both resorption of existing bone and deposition of new bone. The above-mentioned Ca(2+) fluxes are stimulated by the synergistic actions of active vitamin D (1,25-dihydroxyvitamin D(3)) and parathyroid hormone. Until recently, the mechanism by which Ca(2+) enter the absorptive epithelia was unknown. A major breakthrough in completing the molecular details of these pathways was the identification of the epithelial Ca(2+) channel family consisting of two members: TRPV5 and TRPV6. Functional analysis indicated that these Ca(2+) channels constitute the rate-limiting step in Ca(2+)-transporting epithelia. They form the prime target for hormonal control of the active Ca(2+) flux from the intestinal lumen or urine space to the blood compartment. This review describes the characteristics of epithelial Ca(2+) transport in general and highlights in particular the distinctive features and the physiological relevance of the new epithelial Ca(2+) channels accumulating in a comprehensive model for epithelial Ca(2+) absorption.
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              Ion regulation in fish gills: recent progress in the cellular and molecular mechanisms.

              Fish encounter harsh ionic/osmotic gradients on their aquatic environments, and the mechanisms through which they maintain internal homeostasis are more challenging compared with those of terrestrial vertebrates. Gills are one of the major organs conducting the internal ionic and acid-base regulation, with specialized ionocytes as the major cells carrying out active transport of ions. Exploring the iono/osmoregulatory mechanisms in fish gills, extensive literature proposed several models, with many conflicting or unsolved issues. Recent studies emerged, shedding light on these issues with new opened windows on other aspects, on account of available advanced molecular/cellular physiological approaches and animal models. Respective types of ionocytes and ion transporters, and the relevant regulators for the mechanisms of NaCl secretion, Na(+) uptake/acid secretion/NH(4)(+) excretion, Ca(2+) uptake, and Cl(-) uptake/base secretion, were identified and functionally characterized. These new ideas broadened our understanding of the molecular/cellular mechanisms behind the functional modification/regulation of fish gill ion transport during acute and long-term acclimation to environmental challenges. Moreover, a model for the systematic and local carbohydrate energy supply to gill ionocytes during these acclimation processes was also proposed. These provide powerful platforms to precisely study transport pathways and functional regulation of specific ions, transporters, and ionocytes; however, very few model species were established so far, whereas more efforts are needed in other species.
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                Author and article information

                Journal
                EXCLI J
                EXCLI J
                EXCLI J
                EXCLI Journal
                Leibniz Research Centre for Working Environment and Human Factors
                1611-2156
                11 May 2015
                2015
                : 14
                : 627-659
                Affiliations
                [1 ]Institute of Cellular and Organismic Biology, Academia Sinica, Nakang, Taipei, Taiwan
                [2 ]Institute of Biological Chemistry, Academia Sinica, Nakang, Taipei, Taiwan
                [3 ]National Institute for Basic Biology, Myodaiji-cho, Okazaki, 444-8787, Japan
                Author notes
                *To whom correspondence should be addressed: Pung-Pung Hwang, Institute of Cellular and Organismic Biology, Academia Sinica, Nakang, Taipei, Taiwan, E-mail: pphwang@ 123456gate.sinica.edu.tw
                Article
                2015-246 Doc627
                10.17179/excli2015-246
                4650948
                26600749
                c0c2fb5d-74be-4981-b5e8-447cf07dc0e8
                Copyright © 2015 Guh et al.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Licence ( http://creativecommons.org/licenses/by/4.0/) You are free to copy, distribute and transmit the work, provided the original author and source are credited.

                History
                : 30 March 2015
                : 21 April 2015
                Categories
                Review Article

                osmoregulation,ion regulation,ionocyte,hormone,zebrafish
                osmoregulation, ion regulation, ionocyte, hormone, zebrafish

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