Endocrine Control of Osmoregulation in Teleost Fish 1

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AMER. ZOOL., 41: (2001) Endocrine Control of Osmoregulation in Teleost Fish 1 STEPHEN D. MCCORMICK 2 Conte Anadromous Fish Research Center, USGS, Biological Resources Division, Turners Falls, Massachusetts
AMER. ZOOL., 41: (2001) Endocrine Control of Osmoregulation in Teleost Fish 1 STEPHEN D. MCCORMICK 2 Conte Anadromous Fish Research Center, USGS, Biological Resources Division, Turners Falls, Massachusetts SYNOPSIS. As the primary link between environmental change and physiological response, the neuroendocrine system is a critical part of osmoregulatory adaptations. Cortisol has been viewed as the seawater-adapting hormone in fish and prolactin as the fresh water adapting hormone. Recent evidence indicates that the growth hormone/insulin-like growth factor I axis is also important in seawater adaptation in several teleosts of widely differing evolutionary lineages. In salmonids, growth hormone acts in synergy with cortisol to increase seawater tolerance, at least partly through the upregulation of gill cortisol receptors. Cortisol under some conditions may promote ion uptake and interacts with prolactin during acclimation to fresh water. The osmoregulatory actions of growth hormone and prolactin are antagonistic. In some species, thyroid hormones support the action of growth hormone and cortisol in promoting seawater acclimation. Although a broad generalization that holds for all teleosts is unlikely, our current understanding indicates that growth hormone promotes acclimation to seawater, prolactin promotes acclimation to fresh water, and cortisol interacts with both of these hormones thus having a dual osmoregulatory function. The capacity to regulate plasma ions in the face of changing external salinity is an obvious necessity for fish that live in estuaries or that move between fresh water and seawater as part of their normal life cycle. The need to respond to salinity change may be rapid, such as during tidal cycles or rapid movements through estuaries, or slow, such as in the seasonal or ontogenetic acquisition of salinity tolerance in anadromous fish. The former requires the rapid activation of existing mechanisms (transport proteins and epithelia), whereas the second requires the differentiation of transport epithelia and synthesis of new transport proteins. As the primary link between environmental change and physiological response, the neuroendocrine system is a critical part of these osmoregulatory adaptations. In this paper I will review recent evidence for the hormones involved in development and differentiation of transport epithelia that control the ability of teleost fish to move between fresh water and seawater. Our previous 1 From the Symposium Osmoregulation: An Integrated Approach presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4 8 January 2000, at Atlanta, Georgia. 2 textbook view of the endocrinology of osmoregulation has been that cortisol is the seawater-adapting hormone and prolactin is the fresh water-adapting hormone, clearly defined for the first time by Utida et al. (1972). Evidence collected in the last 15 yr indicates that the growth hormone/insulin-like growth factor I (GH/IGF- I) axis is also important in the seawater acclimation process of teleosts. Recent findings on the importance of cortisol in ion uptake will also be presented, and these indicate that cortisol has a dual osmoregulatory function in many teleosts. THE PHYSIOLOGY OF EURYHALINITY Irrespective of the salinity of their external environments, teleost fishes maintain their plasma osmotic concentration about one-third that of seawater. In fresh water this requires counteracting the passive gain of water and loss of ions by producing a copious dilute urine and actively taking up ions across the gills. In seawater, teleosts must counteract the passive gain of ions and loss of water. This is accomplished by drinking seawater, absorbing water and salts across the gut, and secreting excess monovalent ions across the gills and divalent ions 781 782 STEPHEN D. MCCORMICK through the kidney. Evans (1984) has estimated that 95% of teleost species are stenohaline, living wholly in either fresh water or seawater. The remaining 5% are euryhaline, having the capacity to withstand large changes in environmental salinity, a trait that is widespread among teleost lineages and has apparently evolved many times. This capacity to evolve euryhalinity may be one reason that teleosts can be found in almost all aquatic habitats. The mechanisms of ion transport in teleost fish have been the subject of several recent reviews (Evans et al., 1999; Marshall and Bryson, 1998). As outlined above, the gills are the primary site of net sodium and chloride transport, actively taking up salts in fresh water and secreting them in seawater. Most of the recent work on the endocrine control of ion transport in fish has focused on the gill, so this review will necessarily be biased in this direction (see Utida et al., [1972] for a review of the endocrine control of the gut and urinary bladder). It has been known for some time that the mitochondrion-rich chloride cell is the site of salt secretion (Foskett and Scheffey, 1982b). There is substantial evidence indicating that the major transporters involved in salt secretion in the gill includes basolaterally located Na,K -ATPase (the sodium pump) and Na, K, 2Cl cotransporter (NKCC), and an apical Cl channel that appears to be homologous with the cystic fibrosis transmembrane conductance regulator (see Fig. 1). The site and mechanims involved in ion uptake in fresh water are less certain. Both chloride cells and pavement cells may be involved in sodium and chloride uptake. Chloride is exchanged for HCO 3 at the apical surface and leaves at the basolateral membrane moving downhill on an electrical gradient (the chloride cell being more negative than the blood). Sodium may enter the gill epithelia by exchange with H, or through an apical Na channel coupled to an apical H -ATPase, and then leave at the basolateral surface through Na,K ATPase. Recent evidence suggests that H -ATPase and the apical sodium channel are located on the apical surface of pavement cells in Mozambique tilapia (Oreochromis mossambicus), but in both pavement cells and chloride cells in the rainbow trout (Oncorhynchus mykiss) (Hiroi et al., 1998; Wilson et al., 2000). Most of our knowledge of the transporters involved in ion uptake and secretion in fish comes from ion substitution and phamacological studies. With the exception of the sodium pump and the apical chloride channel, the sequence and physical structure of transporters involved in ion transport in fish have not been characterized (see Evans et al., 1999). More direct evidence is needed to establish the roles and location of these transporters in teleosts. THE ROLE OF THE GH/IGF-I AXIS IN ACCLIMATION TO SEAWATER Evidence for the importance of the GH/ IGF-I axis in seawater acclimation comes primarily from studies on exogenous hormone treatment, changes in circulating levels, metabolic clearance rate, localization of receptors and production of IGF-I by osmoregulatory tissues (Sakamoto et al., 1993; Mancera and McCormick, 1998a). Komourdjian et al. (1976) found that long term GH treatment increased both the size and salinity tolerance of Atlantic salmon (Salmo salar). Recent studies of growth hormone transgenic salmon also show that these larger fish have increased salinity tolerance (Saunders et al., 1998; Devlin et al., 2000). Because larger salmonids have inherently greater salinity tolerance, it was not clear whether these effects of GH were specific to osmoregulation or were indirect through the growth effects of GH. Bolton et al. (1987) found that a single injection of GH in rainbow trout (Oncorhynchus mykiss) followed two days later by exposure to seawater resulted in increased salinity tolerance. This time course was too rapid to be explained by changes in body size, thus indicating that GH has osmoregulatory actions independent of its effect on growth. Subsequent research found that GH could increase salinity tolerance in many salmonid species (Sakamoto et al., 1993). At least some of the osmoregulatory actions of GH are carried out by IGF-I. Using a protocol similar to that of Bolton et al. (1987), Mc- Cormick et al. (1991b) found that IGF-I increased salinity tolerance in rainbow trout, HORMONES AND OSMOREGULATION IN FISH 783 FIG. 1. Morphology and transport mechanisms of gill chloride cells in seawater and fresh water. See text for details of transport mechanisms. Chloride cells are characterized by numerous mitochondria and an extensive tubular system that is continuous with the basolateral membrane. In seawater, chloride cells are generally larger and contain a deep apical cyrpt, whereas in freshwater the apical surface is broad and contains numerous microvilli. In some species, such as tilapia the H -ATPase and apical sodium channel may be present in pavement cells rather than chloride cells. Recent evidence suggests that individual chloride cells can move between these two mophological states (Hiroi et al., 1999), and also arise from undifferentiated stem cells (Wong and Chan, 1999). 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 fresh water chloride cells. Cortisol also promotes acclimation to fresh water by maintaining ion transporters and chloride cells, and by interacting to some degree with prolactin. PVC pavement cell. and this effect was later confirmed in other salmonids (McCormick, 1996; Seidelin et al., 1999). For some time it was thought that the osmoregulatory actions of GH and IGF-I were related to the spring migration and growth cycle of anadromous salmon and perhaps restricted to salmonids. Recent evidence, however, indicates that GH/IGF-I effects on salinity acclimation may be widespread among teleosts. GH injection increases hypo-osmoregulatory ability in two cichlid species, the Nile and Mozambique tilapia (Oreochromis niloticus and O. mossambicus) (Xu et al., 1997; Sakamoto et al., 1997). Mancera and McCormick (1998b) found that both GH and IGF-I injections increased salinity tolerance in the intertidal mummichug, Fundulus heteroclitus (Family Cyprinodontidae). Although these represent a small number of the euryhaline species, they are widely separated in the evolution of teleosts, suggesting that the osmoregulatory action of GH and IGF- I may also be widespread among teleosts. Examination of the mechanisms of action of GH and IGF-I to promote salinity tolerance indicates that the gill is an important 784 STEPHEN D. MCCORMICK target tissue. GH and IGF-I stimulate the number and/or size of gill chloride cells in salmonids and tilapia (Sakamoto et al., 1993; Xu et al., 1997). Prunet et al. (1994) found that GH increased the number of chloride cells and accessory cells (both thought to be involved in salt secretion), and decreased the number of -cells (putative ion uptake cells) in juvenile Atlantic salmon. GH and IGF-I increase gill Na, K ATPase activity and/or mrna levels in salmonids, tilapia and mummichog (Madsen et al., 1995; Mancera and McCormick, 1998b; Xuet al., 1997; Sakamoto et al., 1997), and immunocytochemical studies indicate that hormone induced increases in Na, K ATPase are localized to chloride cells (Seidelin et al., 1999). It has recently been shown that GH also upregulates the Na :K :2Cl cotransporter in gill chloride cells of Atlantic salmon (Pelis and McCormick, 2001). To date, regulation of other gill transporters has not been examined. Although the number of studies are limited, there is no evidence that GH can directly (in vitro) increase gill Na, K ATPase activity (McCormick and Bern, 1989). The ability of IGF-I to increase gill Na,K ATPase activity and the ability of GH to regulate in vitro responsiveness of gill tissue to IGF-I further suggests an indirect action of GH on gill tissue, and a direct action of IGF-I (Madsen and Bern, 1993). Levels of IGF-I mrna in gill and kidney increases following GH injection and exposure to seawater, indicating that local production of IGF-I may act in a paracrine fashion to influence transport capacity of gill and renal epithelia (Sakamoto and Hirano, 1993). Whether IGF-I acts primarily in an endocrine or paracrine fashion is unknown. In vivo studies indicate that IGF- I by itself does not carry out all of the osmoregulatory actions of GH, and that other endocrine factors and/or binding proteins may also be involved (McCormick, 1996). To date, investigations on the mechanisms of action of the GH/IGF-I axis have almost exclusively focused on the gill, though it is likely that the gut and kidney are also responsive. Fuentes and Eddy (1997) found that GH treatment increased drinking rate after exposure of Atlantic salmon to seawater, suggesting that GH may affect gut function. In brown trout, IGF-I treatment increased gill but not intestinal Na,K ATPase, whereas cortisol increased both (Seidelin et al., 1999). In addition to the effects of exogenous hormone treatments, changes in the endocrine response to SW also provides evidence for the osmoregulatory actions of GH and IGF-I. This evidence comes primarily from studies on salmonids where the gene sequences of these hormones are known and assays for quantitation of gene expression, circulating levels and receptors have been developed. Plasma levels of GH increase following seawater exposure of coho, chum and Atlantic salmon and rainbow trout (Sakamoto et al., 1993). Metabolic clearance rate of GH in trout is also increased following seawater acclimation (Sakamoto et al., 1990). In Atlantic salmon, plasma IGF-I remains elevated for 2 14 days following seawater exposure (S. D. McCormick, T. Bj. Bjornsson, and S. Moriyama, unpublished results). Hepatic, branchial and renal levels of IGF-I mrna increase during smolting of coho salmon and following seawater transfer (Sakamoto et al., 1995). In Mozambique tilapia, high concentrations of IGF-I have been found specifically in chloride cells and in epithelial cells of the proximal tubule (Reinecke et al., 1997). GH receptors have been found in the gill and kidney (but not intestine) of coho salmon (Fryer and Bern, 1979; Gray et al., 1990), and this GH binding was decreased in stunted juveniles that experience seawater-induced growth retardation. Sakamoto and Hirano (1991) found that the occupancy of hepatic, but not branchial and renal, growth hormone receptors increased following exposure to seawater. A partial sequence and characterization of the IGF-I receptors in fish has been documented (Drakenberg et al., 1993; Elies et al., 1996; Chan et al., 1997; Funkenstein et al., 1997), but there is currently no information on its distribution in transport epithelia. To date, effects of GH and/or IGF-I on osmoregulation outlined above have been demonstrated in six teleost species distributed among three families (salmonidae, cyprinodontidae and cichladae). Although HORMONES AND OSMOREGULATION IN FISH 785 these represent a small number of the total number of teleosts, they are widely spread within the teleost lineage: salmonids appeared early in teleost evolution, while Fundulus and tilapia belong in the two most recently evolved teleost clades (Atherinomorpha and Percomorpha; Helfman et al., 1997). Since the effects of the GH/IGF-I axis in osmoregulation has only recently been found for these species, it seems likely that more research will establish that these effects are widespread among euryhaline teleosts. INTERACTION OF THE GH/IGF-I AXIS WITH CORTISOL The recent evidence for a role of the GH/ IGF-I axis does not diminish the importance of cortisol in salt secretion in fish. Several lines of evidence provide substantial support for a role of cortisol in seawater acclimation, including increased circulating levels and metabolic clearance after exposure to seawater, the effects of interrenalectomy, and the effects of cortisol treatment on ion regulation and salinity tolerance in intact, hypophysectomized and interrenalectomized fish (see reviews by Bern and Madsen, 1992; Foskett et al., 1983; Mc- Cormick, 1995). Recent evidence indicates that the GH/IGF-I and cortisol axes work together to regulate salt secretion in teleosts. It has been shown for several salmonid species that injection of GH and cortisol together increases gill Na,K ATPase activity and salinity tolerance to a greater extent than either hormone alone (Madsen, 1990b; Madsen and Korsgaard, 1991; McCormick, 1996). This effect can be seen in both hypophysectomized and intact fish (Björnsson et al., 1987; Madsen, 1990a). Stimulation of gill Na,K ATPase activity appears to involve a synergistic action of the two hormones (Madsen, 1990b; McCormick, 1996). Similar to the effects reported for salmonids, Mancera and McCormick (1999) found that GH and cortisol together increase hypo-osmoregulatory ability of mummichog to a greater extent than either hormone alone. It is less clear whether IGF-I and cortisol have a similar capacity to interact. McCormick (1996) found that in Atlantic salmon, IGF-I and cortisol together stimulated gill Na,K ATPase activity to a greater extent than either hormone alone, but that this interaction was weaker than that for GH and cortisol. In brown trout (Salmo trutta), Seidelin et al., (1999) have recently found an additive effect of IGF-I and cortisol on gill Na,K ATPase activity and mrna levels, and a significant interaction between the two hormones in increasing the number of Na, K ATPase immunoreactive cells (chloride cells) in the gill. One mechanism by which the GH/IGF-I and cortisol axes may interact is through the regulation of cortisol receptors. The cortisol receptor from rainbow trout has recently been cloned (Ducouret et al., 1995), and in situ hybridization and immunocytochemical approaches have shown that cortisol receptors are preferentially located in chloride cells and undifferentiated cells (stem cells) in the primary filament of chum salmon (Uchida et al., 1998). GH treatment causes increased numbers of gill cortisol receptors in coho and Atlantic salmon (Shrimpton et al., 1995; Shrimpton and McCormick, 1998). The number of gill cortisol receptors is strongly correlated with the capacity of cortisol to stimulate gill Na,K ATPase in vitro and in vivo (McCormick et al., 1991a; Shrimpton et al., 1994; Shrimpton and Mc- Cormick, 1999), indicating that the regulation of cortisol receptors is physiologically relevant. Laurent et al. (1994) found that growth hormone increased mitotic activity (bromodeoxyuridine labelling) in several cell types in the gill of rainbow trout. Cortisol had no effect or decreased mitotic activity, but increased the number of chloride cells, suggesting that cortisol acts primarily on differentiation of chloride cells. These findings indicate that cortisol and growth hormone may interact, with GH causing general cell proliferation in the gill, creating more stem cells that can then be acted on by cortisol. It would be of interest to examine whether GH increases the number of stem cells with high levels of cortisol receptors as described above. In addition to the interaction of the GH/ IGF-I axis and cortisol at the gill tissue, these endocrine axes may also interact at 786 STEPHEN D. MCCORMICK higher regulatory pathways, such as the hypothalamus and pituitary. In vivo and in vitro exposure to GH increases the sensitivity of interrenal tissue to ACTH (adrenocorticotrophic hormone) in coho salmon, causing increased release of cortisol (Young, 1988). Rousseau et al. (1999) found that corticotropin releasing hormone is a potent stimulator of in vitro growth hormone release in European eel (Anguilla anguilla). Although there is conflicting evidence regarding the role of thyroid hormones in osmoregulation, most studies have found that thyroid hormones by themselves cannot increase ion uptake or secretory capacity (Ayson et al., 1995
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