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The Hormonal Control of Osmoregulation in Teleost Fish

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Provided for non-commercial research and educational use. Not for reproduction, distribution or commercial use. This article was originally published in Encyclopedia of Fish Physiology: From Genome to Environment, published by Elsevier, and the attached copy is provided by Elsevier for the author’s benefit and for the benefit of the author’s institution, for non-commercial research and educational use including without limitation use in instruction at your institution, sending it to specific colleagues who you know, and providing a copy to your institution’s administrator. All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institution’s website or repository, are prohibited. For exceptions, permission may be sought for such use through Elsevier’s permissions site at: http://www.elsevier.com/locate/permissionusematerial McCormick S.D. (2011) The Hormonal Control of Osmoregulation in Teleost Fish. In: Farrell A.P., (ed.), Encyclopedia of Fish Physiology: From Genome to Environment, volume 2, pp. 1466–1473. San Diego: Academic Press. ª 2011 Elsevier Inc. All rights reserved. Author's personal copy HORMONAL CONTROLS Hormonal Control of Metabolism and Ionic Regulation Contents The Hormonal Control of Osmoregulation in Teleost Fish Corticosteroids The Hormonal Control of Osmoregulation in Teleost Fish S D McCormick, USGS, Conte Anadromous Fish Research Center, Turners Falls, MA, USA Published by Elsevier Inc. Introduction: Salt and Water Balance in Fish Thyroid Hormones Cortisol The Special Case of Anadromy Prolactin Summary Growth Hormone and IGF-I Further Reading Glossary Insulin-like growth factor-I (IGF-I) A protein Adrenocorticotrophic hormone (ACTH) A protein hormone produced in the liver in response to growth hormone produced in the pituitary that causes release of hormone and acting on growth and ion regulation. cortisol from the interregnal. Na+,K+-ATPase (NKA, the sodium pump) Amajor Anadromy Life-history strategy entailing reproduction ATP-consuming ion pump that, directly or indirectly, drives and early rearing in freshwater followed by a significant many ion-regulatory processes, including maintaining growth phase in seawater. sodium and ion gradients across cell plasma membranes Apoptosis The process of programmed cell death. and being present at high levels in ionocytes. Cortisol The major corticosteroid of teleosts, produced Na+,K+,2Cl� cotransporter (NKCC) An ion- in the interrenal and acting on metabolism and ion translocating enzyme that utilizes a sodium gradient to regulation. transport Na+,K+, and Cl� into the cell. Cystic fibrosis transmembrane conductance Prolactin A protein hormone produced in the pituitary regulator (CFTR) An apical chloride channel involved acting on ion balance and reproduction. in chloride secretion. Receptor A signal transduction molecule that is Euryhaline Animals that physiologically adjust to a activated by a hormone. wide range of water salinity are considered euryhaline Stenohaline Describes an organism that cannot live in (eury ‘broad’; haline ‘salt’), in contrast to stenohaline environments that undergo large changes in salinity animals. (steno ‘narrow’). Growth hormone (GH) A pituitary protein hormone Thyroid hormones Thyroxine and triiodothyronine, controlling growth, metabolism, and ion regulation. produced in the thyroid gland and acting on Hormone Signaling molecule released by a cell that development and metabolism. either stimulates the cell of origin (autocrine), nearby Transactivation Binding of a transcription factor, such cells (paracrine), or travels via the bloodstream to as a receptor–ligand complex, to DNA resulting in distant cells (endocrine). increased gene transcription. 1466 Encyclopedia of Fish Physiology: From Genome to Environment, 2011, Vol. 2, 1466-1473, DOI: 10.1016/B978-0-1237-4553-8.00212-4 Author's personal copy Hormonal Control of Metabolism and Ionic Regulation | Osmoregulation in Teleost Fish 1467 Introduction: Salt and Water Balance As outlined above, the gills are the primary site of in Fish sodium and chloride transport, actively taking up salts in freshwater and excreting them in seawater. Most of Whether in freshwater or seawater, teleost fish maintain the recent work on the endocrine control of ion transport their plasma osmotic concentration at about one-third that in fish has focused on the gill, so this review will necessa­ of seawater (see also Osmotic, Ionic and Nitrogenous- rily be biased in this direction. It has been known for some Waste Balance: Osmoregulation in Fishes: An time that the mitochondrion-rich cell (also known as Introduction). In freshwater, this requires counteracting the chloride cell) is the site of salt secretion (see also the passive gain of water and loss of ions, and is accom- Role of the Gills: Morphology of Branchial Ionocytes plished through the production of large volumes of dilute and Osmotic, Ionic and Nitrogenous-Waste Balance: urine and active uptake of ions across the gills. In seawater, Mechanisms of Gill Salt Secretion in Marine Teleosts). teleosts must counteract the passive gain of ions and loss of There is substantial evidence indicating that the major water. This is accomplished by drinking seawater, absorb- transporters involved in salt secretion in the gill include ing water and salts across the gut, and excreting basolaterally located Na+,K+-ATPase (NKA, the sodium monovalent ions across the gills and divalent ions through pump) and Na+,K+,2Cl� cotransporter (NKCC), and an the kidney. It has been estimated that 95% of teleost apical Cl� channel that is homologous with the cystic species are stenohaline, living wholly in either freshwater fibrosis transmembrane conductance regulator (CFTR) or seawater. The remaining 5% are euryhaline, having the (Figure 1). capacity to tolerate a wide range of salinities. This trait is The site and mechanisms involved in ion uptake by the widespread among teleost lineages and has apparently gill in freshwater are less certain. Both mitochondrion - rich evolved many times, and may be one reason that teleosts cells and pavement cells may be involved in sodium and can be found in almost all aquatic habitats. chloride uptake (see also Osmotic, Ionic and Growth hormone/IGF-I Prolactin Cortisol Cortisol + H + Na PVC + − H − HCO3 Cl PVC + Na l l e PVC c y − r Cl o s Stem cell + s e Na c c A + + K + + + K + K K K K + K − Cl + − Na Cl + + + − + Na + Na Na + Cl Na + + Na Na + Na Na Na Seawater Freshwater (ion secretion) (ion uptake) Figure 1 Morphology, transport mechanisms, and hormonal control of gill chloride cells in freshwater and seawater. Chloride cells are characterized by numerous mitochondria and an extensive tubular system that is continuous with the basolateral membrane. In seawater, mitochondrion-rich cells are generally larger and contain a deep apical crypt, whereas in freshwater, there is a broad apical surface containing numerous microvilli. Growth hormone and cortisol can individually promote the differentiation of the seawater chloride cell, and also interact positively to control epithelial transport capacity. Prolactin inhibits the formation of seawater chloride cells and promotes the development of freshwater chloride cells. Cortisol also promotes acclimation to freshwater by maintaining ion transporters and chloride cells, and by interacting to some degree with prolactin PVC, pavement cell. Reproduced from McCormick SD (2001) Endocrine control of osmoregulation in teleost fish. American Zoologist 41: 781–794. Author's personal copy 1468 Hormonal Control of Metabolism and Ionic Regulation | Osmoregulation in Teleost Fish Nitrogenous-Waste Balance:MechanismsofIon in vitro. Cortisol has also been shown to increase the Transport in Freshwater Fishes). Chloride is exchanged transcription and abundance of the major transport pro­ � for HCO3 at the apical surface and leaves at the basolateral teins involved in salt secretion by the gill: NKA, NKCC, membrane moving downhill on an electrical gradient (the and CFTR. The effect of exogenous cortisol generally chloride cell being more negative than the blood). Sodium requires several days to reach its peak, suggesting that cell may enter the gill epithelia by exchange with H+,or proliferation and differentiation are required for its com­ throughanapicalNa+ channel coupled to an apical H+­ plete action. In the intestine, exogenous cortisol ATPase, and pass into the bloodstream at the basolateral gill stimulates NKA activity, together with ion and water surface through NKA. Recent work suggests that in some absorption, thus improving acclimation to high environ­ species there is also a Na+/Cl� co-transporter on the apical mental salinity. An increased drinking response after surface that is involved in ion uptake. More direct evidence transfer to seawater has been observed in salmonids trea­ is needed to be certain of the roles and location of these ted with cortisol. transporters involved in ionuptakeinteleosts. Changes in circulating cortisol in response to There are three primary lines of evidence for the increased environmental salinity are reported for many involvement of hormones in ion regulation. The first teleost species. The clearance rate (the inverse of the involves the treatment of animals (in vivo) or isolated amount of time a compound remains in circulation) of tissues (in vitro) with hormones and examining ion reg­ cortisol also increases in seawater, suggesting
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