Hormonal regulation of the fish gastrointestinal tract

Comparative Biochemistry and Physiology, Part A 139 (2004) 261 – 271 www.elsevier.com/locate/cbpa

Review

Hormonal regulation of the fish gastrointestinal tractB Randal K. Buddingtona,*, 2shild Krogdahlb a

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Department of Biological Sciences, Mississippi State University, Mississippi State, MS 39762, USA Aquaculture Protein Centre, Institute of Basic Sciences and Aquatic Medicine, Norwegian School of Veterinary Science, P.O. Box 8146 Dep., N-0033 Oslo, Norway Received 3 March 2004; received in revised form 18 August 2004; accepted 6 September 2004

Abstract The gastrointestinal tracts (GIT) of fish and other vertebrates are challenged with a diversity of functional demands caused by changes and differences in dietary inputs and environmental conditions. This contribution reviews how hormonal regulation plays an essential role in modulating the GIT functions of fish to match changes in functional demands. Exemplary is how hormones produced by the GIT, the associated organs (e.g., pancreas), and other sources (e.g., hypothalamus, adrenal cortex, thyroid, gonads) modulate the digestive processes (motility, secretion, and nutrient absorption) in response to dietary inputs. Hormones regulate the other GIT functions of osmoregulation (secretion and absorption of electrolytes and water), immunity, endocrine secretions, metabolism, and the elimination of toxic metabolites and environmental contaminants to match changes in environmental conditions and physiological states. Although the regulatory molecules and associated signaling pathways have been conserved during evolution of the vertebrate GIT, the specific responses often vary among fish with different feeding habits and from different environments, and can differ from those described for mammals. D 2004 Elsevier Inc. All rights reserved. Keywords: Digestion; Immune; Osmoregulation; Intestine; Endocrine

Contents 1. 2. 3. 4.

Introduction. . . . . . . . . . . . . . . . . . GIT signaling networks. . . . . . . . . . . . Signaling molecules that influence the GIT . Endocrine functions of the GIT . . . . . . . 4.1. Endocrine cells of the GIT . . . . . . 4.2. Regulation of GIT endocrine functions Hormonal regulation of digestion . . . . . . 5.1. Secretion . . . . . . . . . . . . . . . 5.2. Absorption . . . . . . . . . . . . . . 5.3. Motility . . . . . . . . . . . . . . . . 5.4. Circulation . . . . . . . . . . . . . . 5.5. Metabolism of nutrients and toxins . . Osmoregulation. . . . . . . . . . . . . . . .

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From the symposium Hormones and Metabolism—A Fishy Perspective presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2003, at Toronto, Ontario, Canada. * Corresponding author. Tel.: +1 662 325 7580; fax: +1 662 325 7939. E-mail address: [email protected] (R.K. Buddington). 1095-6433/$ - see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.cbpb.2004.09.007

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7. Defense functions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8. Perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction The gastrointestinal tract (GIT) is basically a tube that courses through the body. However, the structure and functional characteristics of the GIT vary widely among species (Suyehiro, 1941) and are established by genetic determinants such that they are matched to the wide diversity of feeding habits and environmental conditions exploited by fish. The variation is obvious by comparing the GIT characteristics of carnivorous and herbivorous fish and those from fresh and sea water. The mucosa lining the GIT represents an interface between the external and internal environments, and in conjunction with the associated organs (e.g., pancreas, liver, and gall bladder) provides the functions of digestion, osmoregulation, immunity, endocrine regulation of GIT and systemic functions, and elimination of environmental contaminants and toxic metabolites. The abilities of fish to rapidly and reversibly adapt GIT characteristics to match the changes in functional demands that occur during the life history (e.g., metamorphosis, anadromous or catadromous migrations) or more frequently (day-to-day or seasonal shifts in diet or environmental conditions) are dependent on endocrine signaling pathways, which are augmented by the enteric nervous system (Karila

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et al., 1998). Efforts to distinguish between regulation by endocrine cells and neurons can be confounded by the sharing of signaling molecules (Beorlegui et al., 1992a; Bjenning and Holmgren, 1988; Dockray, 1979; Jensen and Holmgren, 1985; Kiliaan et al., 1997). The objective of this review is to provide readers with insights into the endocrine regulation of the fish GIT. Although the focus is on digestion, endocrine regulation of the other GIT functions of osmoregulation, immunity, endocrine regulation, and the elimination of toxins is briefly mentioned. Instead of providing an exhaustive review of the literature and a blaundry listQ of known and putative regulatory molecules and their associated influences, we have selected papers that exemplify how hormones and other signaling molecules influence GIT characteristics. Our goal was to provide readers with information to guide them in pursuing more in-depth evaluations. Even though only a small number of fish species and characteristics have been examined, it is evident hormones and regulatory peptides play important roles in modulating the fish GIT. It is also obvious the specific influences and responses vary among species and stages of development. Moreover, despite sharing some similarities with other vertebrates, the patterns and mechanisms of hormonal regulation in fish have some

Fig. 1. GIT functions are regulated by three hormonal signaling networks. Paracrine signals (top panel) from endocrine cells (EC-1 and EC-2) regulate the functions of nearby cells, as well as each other, such that specific functions are matched with local conditions. For intra-GIT signaling networks (middle panel), hormones from one region modulate the functions in other GIT regions and associated organs (as indicated by arrows). Inter-organ signaling networks (bottom panel) involve axes between the GIT and other sources of hormones and signaling molecules (central nervous system, CNS; cardiovascular system, CV) and the GIT.

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unique features that probably reflect the different functional demands placed on the GIT.

2. GIT signaling networks Regulatory peptides and hormones and their associated receptors have been detected along the length of the GIT of various fish species, and form regulatory networks that operate over three distances (Fig. 1). Local signaling networks operate in a paracrine manner with regulatory molecules from one population of cells modulating the activities of nearby cells. Such networks serve to regulate GIT functions to match local conditions and needs. Another set of signaling networks operate between different GIT regions and the associated organs. These intra-GIT signaling networks modulate and optimize GIT characteristics to match changes in the functional demands placed on the various regions, and are best known for digestion. Exemplary are how lumenal conditions (e.g., nutrients and pH) in the proximal small intestine trigger the secretion of regulatory peptides that modulate gastric, pancreatic, and gall bladder secretion. Signaling networks also exist between the GIT and other organ systems and serve to modulate GIT characteristics to match the needs of the entire organism. This is evident from the presence of GIT receptors and responses to growth hormone (Ng et al., 1993), prolactin (Prunet et al., 2000), gonadal steroids (Socorro et al., 2000), glucocorticoids (Ducouret et al., 1995), and oxytocin (Baldisserotto and Mimura, 1997). Some inter-organ networks can adversely affect the GIT, as exemplified by the intestinal dysfunction caused by the higher circulating concentrations of glucocorticoids in response to stress (Meddings and Swain, 2000).

3. Signaling molecules that influence the GIT The number of signaling molecules known to modulate one or more GIT characteristics continues to increase and includes hormones, neurotransmitters, and neuromodulators (Table 1). The majority are peptides with 15–60 amino acid residues, and most are shared with mammals and other vertebrates (El-Salhy, 1984; Holmgren et al., 1982). Although the molecules have been conserved during evolution (Irwin et al., 1999; Wang et al., 1999), there are phylogenetic differences among fish and other vertebrates for the glucagon family of peptides (Irwin, 2001; Irwin et al., 1999), the closely related peptides CCK and gastrin (Johnsen, 1998) and the associated receptors (Dimaline and Dockray, 1994). The elicited responses also vary among species (Uesaka et al., 1996, 1994; Vigna et al., 1985), and with variants of signaling molecules (e.g., CCK; Jensen et al., 2001). Several of the regulatory peptides influence feeding behavior of fish (Le Bail and Bœuf, 1997), hence the

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Table 1 The different classes of signaling molecules that modulate GIT functions of fish, with selected representatives for each class Class

Representatives

Peptides (b~60 AA)

Families of related peptides Gastrin-Cholecystokinin Vasoactive intestinal polypeptide (VIP, secretin, glucagon and related peptides, gastric inhibitory polypeptide) Somatostatin Tachykinins (Substance P) Opioids (enkephalins) Pancreatic Polypeptide (PP, neuropeptide Y, peptide YY) Others (atrial natriuretic peptide, angiotensins, gastrin releasing peptide) growth hormone, prolactin thyroxine, tri-iodothyronine cortisol, estrogen, progesterone, testosterone prostaglandin F and prostaglandin E Interleukin 1 (IL-1) serotonin (5-HT), histamine

Larger proteins Iodinated proteins Steroids Prostaglandins Cytokines Neurotransmitters

Assembled from several sources.

functional demands placed on the GIT. Exemplary is how some of the CCK forms inhibit feeding (Himick and Peter, 1994; Peyon et al., 1999). Feeding responses to regulatory peptides can be expected to vary among species due to differences in phylogeny, feeding habits, and environmental conditions (Murat et al., 1981). A limited number of larger proteins influence the GIT via inter-organ signaling networks. Receptors for the iodinated proteins, thyroxine and tri-iodothyronine, have been detected in the intestines of fish (Nowell et al., 2001), as have receptors for prolactin (Prunet et al., 2000; Sandra et al., 2001). Although thyroid hormones mediate GIT development (Nowell et al., 2001), the presence of receptors in the intestines of adults is suggestive of other influences. GIT characteristics are responsive to several steroid-based molecules, including estrogen, testosterone, and the mineralcorticoids and glucocorticoids (see below), and to prostaglandins (Kagstrom and Holmgren, 1997). The various regulatory molecules modulate cell and tissue functions by signal transduction pathways that are shared with other vertebrates (Mommsen and Mojsov, 1998). These include intracellular receptors and extracellular receptors linked to channels, intracellular enzymes, and G-proteins. The cellular responses include different patterns of gene expression and protein synthesis (genomic) and changes in the activities of existing proteins (non-genomic; Sutter-Dub, 2002).

4. Endocrine functions of the GIT The GIT is the largest endocrine organ in the vertebrate body (Holst et al., 1996). The wide diversity and amounts of secreted hormones and signaling molecules secreted by the

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numerous types of endocrine cells rapidly and reversibly alter characteristics of the GIT and other organ systems, and allow fish to adapt to changes in dietary inputs (quantitative and qualitative) and environmental conditions.

less is known about neural regulation of the endocrine cells associated with the GIT of fish.

5. Hormonal regulation of digestion 4.1. Endocrine cells of the GIT Numerous types of endocrine cells are present along the entire length of the GIT of fish (Abad et al., 1987; Beorlegui et al., 1992a,b; Elbal and Agulleiro, 1986; Holmgren et al., 1982;Yoshida et al., 1983). Although the types of endocrine cells and regional patterns of distribution along the length of the GIT are similar to those described for other vertebrates (Stevens and Hume, 1995), variation exists among fish with different feeding habits and GIT designs and from different environments (Andreozzi et al., 1997; Noaillac-Depeyre and Hollande, 1981). The regulatory peptides associated with the pancreatic tissue of fish are similar to those known for mammals (Nozaki et al., 1988; Tagliafierro et al., 1996), but the specific types of endocrine cells can vary among species (Cheung et al., 1991; Youson and Al-Mahrouki, 1999). Moreover, because of the diffuse nature of the pancreas in many species of fish, endocrine cells can be detected in other tissues, such as the pyloric ceca of salmonids (Beorlegui et al., 1992a,b; Nozaki et al., 1988) and the intestine of other species (Tagliafierro et al., 1996). 4.2. Regulation of GIT endocrine functions The types and amounts of hormones released from the endocrine cells of the GIT and pancreas are partly determined by the composition of the lumenal conditions (nutrients, pH, ionic composition) and distension of the GIT. Notable is the secretion of CCK, secretin, gastrin, and the more recently detected calcitonin (Okuda et al., 1999). Endocrine functions of the fish GIT are also affected by environmental contaminants (Pederzoli et al., 1996). The three signaling networks influence the GIT endocrine cells. A notable example of a local (paracrine) network is the secretion of somatostatin from D cells in the gastric mucosa to inhibit secretion of histamine and gastrin from nearby enterochromafin and G cells (Sachs et al., 1997). Intra-GIT signaling is exemplified by regulation of pancreatic insulin secretion by intestinal secretion of GLP-1 and somatostatin (Skoglund et al., 2000; Stewart et al., 1978). Inter-organ system signaling networks modulate GIT endocrine functions and include the influences of steroid hormones (estrogen, testosterone, glucocorticoids) on pancreatic endocrine secretions of mammals (Morimoto et al., 2001; Sutter-Dub, 2002) and salmonids (Holloway et al., 2000). Neural inputs also modulate endocrine functions of the GIT. This has been established for the endocrine cells of the mammalian pancreas (Ahren, 1999) and gastrin secretion by the G-cells in the gastric mucosa (Sachs et al., 1997). Much

The energy and nutrients contained in feedstuffs are made available by a sequential process. The complex polymers (e.g., proteins, starches, lipids) are hydrolyzed into smaller molecules (amino acids and peptides, monosaccharides, fatty acids and monoglycerides), which are absorbed across the apical membrane of epithelial cells and transferred across the basolateral membrane into the systemic circulation. The digestive processes and maintenance of the GIT are costly. Processing of meals increases energy costs and oxygen consumption by the GIT by up to 70% (Alsop and Wood, 1997; Owen, 2001) and 20–25% of total body protein synthesis of mammals is dedicated to the GIT. The costs are higher when the associated organs (e.g., liver, pancreas) are included (Gill et al., 1989). The high costs make it imperative that the GIT be efficiently regulated. This is accomplished by a wide diversity of regulatory molecules that act in local, intra-GIT, inter-organ system signaling networks. 5.1. Secretion The fluids, electrolytes, enzymes, mucous, and other molecules secreted by the gastrointestinal tract (stomach, small and large intestine) and associated organs (e.g., pancreas and gall bladder) are critical for digestion. The secretions originate from distinct cell populations that are responsive to peptides, hormones, and neurotransmitters (Wapnir and Teichberg, 2002) in multiple, interacting signaling pathways. The complexity of regulation and the involvement of multiple, interacting signaling molecules and networks is well known for gastric secretion (Holstein and Cederberg, 1986). Fish with true stomachs secrete hydrochloric acid and pepsin from a single cell type, the oxyntopeptic cell. The magnitude of secretion and the relative proportions of acid and pepsin are determined by interactions among numerous excitatory and inhibitory signals that directly influence the secretory activity of oxyntopeptic cells, or indirectly by modulating the secretion of other regulatory molecules (Holstein and Humphrey, 1980). Briefly, G cells and enterochromaffin cells in the gastric mucosa function as breceptorsQ and respond to the presence of food, particularly amino acids, peptides and proteins, by secreting gastrin and histamine, respectively, which increase secretion of acid and enzymes by nearby oxyntopeptic cells and stimulate gastric motility. Somatostatin from nearby D cells provides a paracrine negative feedback mechanism that reduces acid and pepsin secretion, and prostaglandins secreted by the gastric mucosa stimulate production of alkaline mucous to protect the mucosa against acid damage (Faggio et al.,

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2000). G cells are present in the proximal intestine of fish that lack oxyntopeptic cells, hence true stomachs (e.g., cyprinids; Noaillac-Depeyre and Hollande, 1981; Pan et al., 2000), indicating gastrin regulates more than just acid and pepsin secretion. The presence of digesta and reduced pH in the proximal small intestine stimulate several populations of mucosal cells to secrete regulatory peptides. These include gastric inhibitory peptide (GIP) from K cells, CCK from I cells, somatostatin from D cells, and secretin from S cells. The various regulatory peptides act in combination to regulate acid and enzyme secretion by the oxyntopeptic cells (Holstein and Cederberg, 1988; Holstein and Humphrey, 1980) and digestive processes in the small intestine, and thereby optimize digestive functions of the entire GIT. The proteases, amylases, lipases, and other enzymes secreted by the acinar cells of the exocrine pancreas and the bile from the gall bladder are essential for intestinal hydrolysis of feedstuffs. In some species the secretion of pancreatic enzymes and bile and the activities of brush border membrane hydrolases respond positively to increasing levels of proteins, lipids and carbohydrates (Krogdahl et al., 2004; Nordrum et al., 2000) and to enzyme inhibitors (Olli et al., 1994). In fish, like mammals, the presence of nutrients in the proximal small intestine triggers the secretion of CCK, which stimulates the secretion of the pancreatic enzymes and bile (Aldman and Holmgren, 1995; Einarsson et al., 1997). However, the secretory responses are lower when mammalian forms of CCK are administered (Vigna and Gorbman, 1979, 1977). The exocrine pancreas of mammals is responsive to gonadal steroids (Hilgendorf et al., 2001) and to neural inputs (Chey and Chang, 2001), but comparable data are lacking for fish. The L cells in the distal small intestine provide an interesting example of intra-GIT regulation of secretory functions. The presence of nutrients in the distal small intestine increases expression of genes coding for glucagon and peptide YY. The glucagon gene product is processed to yield two different signaling molecules, glucagon-like peptides (GLP) 1 and 2. GLP-1 and peptide YY inhibit gastric secretion and motility, whereas GLP-2 stimulates growth and digestive capacities of the proximal small intestine. The detection of glucagon-like peptide reactive cells in the mucosa of the salmonid intestine (Nozaki et al., 1988) suggest a similar intra-GIT feedback system operates in fish. Secretion of water and electrolytes by the intestine and associated organs is essential for normal digestion, and in mammals is tightly regulated (Wapnir and Teichberg, 2002). The importance of the regulation is obvious from the detrimental consequences when intestinal secretion is disturbed by pathogenic bacteria and toxins. Although secretin-reactive cells are present in the intestine of fish, there is little known about hormonal regulation of secretion of water, bicarbonate and other electrolytes in fish. However, differences are to be expected for comparisons with

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terrestrial vertebrates and between fish adapted to fresh and seawater. 5.2. Absorption Dietary nutrients are absorbed by transporters in the apical membrane of the enterocytes and are transferred to the systemic circulation by another set of transporters in the basolateral membrane. Similar to other vertebrates, the activities and densities of the nutrient transporters in the GIT of fish are responsive to changes in diet composition (Buddington et al., 1987; Collie and Ferraris, 1995). Although less is known for fish, the solute transporters are responsive to local paracrine networks (calcitonin; Okuda et al., 1999), intra-GIT regulatory signals (e.g., enteroglucagon, somatotropin; Bird et al., 1994; Stumpel et al., 1998) and inter-organ system hormones (e.g., estrogen, testosterone, growth hormone; Collie and Stevens, 1985; Habibi and Ince, 1984; Hazzard and Ahearn, 1992; Reshkin et al., 1989). The responses of the transporters can be rapid and detectable within 30 min of exposure, suggesting the insertion of pre-existing transporters into the apical membrane. Other responses are slower and require days to weeks, and are caused by changes in the densities of transporters per enterocyte and the number of enterocytes with transporters. 5.3. Motility The patterns of motility (frequency and magnitude) are largely determined by interactions among hormones, regulatory peptides, and neurotransmitters that modulate contractility of the smooth muscle layers lining the GIT of fish (Bueno and Fioramonti, 1994; Jensen and Holmgren, 1985; Olsson and Holmgren, 2001; Olsson and Holmgren, 2000). However, attempts to distinguish between neural and hormonal modulation of GIT motility has been complicated by the association of regulatory peptides with GIT neurons (Karila et al., 1998; Venugopalan et al., 1995) and by some hormones modulating the activities of enteric motor neurons (Jensen and Holmgren, 1985). The responses to the regulatory signals also vary among GIT regions (Andrews and Young, 1988; Holmgren and Jonsson, 1988), such as the opposing modulation of gastric and intestinal contractions by gastrin and CCK (Aldman et al., 1989; Jonsson et al., 1987). These characteristics are shared with other vertebrates, but the inability of mammalian peptides to modulate GIT motility in some species of fish indicate there are differences among the signaling peptides or receptors (Aldman et al., 1989). 5.4. Circulation Perfusion of the GIT with blood is increased during digestion. Although several GIT regulatory peptides have been implicated as vasoactive agents or stimulate production

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of vasoactive agents (Holmgren, 1995; Kagstrom and Holmgren, 1997; Preston et al., 1998), perfusion responses can contrast with those described for mammals (Shahbazi et al., 2002). 5.5. Metabolism of nutrients and toxins The metabolic activities of the GIT mucosa and the liver are critical determinants of the concentrations and relative proportions of absorbed nutrients in the systemic circulation. The mucosa has first access to dietary nutrients, and the metabolism of enterocytes is largely dependent on amino acids absorbed from the lumen of the GIT (Reeds and Burrin, 2000). At the present time, there is little known about hormonal regulation of mucosal metabolism in fish. The liver has second access to dietary nutrients, and a diversity of hormones modulate hepatic metabolism in fish. Of particular importance are insulin, glucagon, and somatostatin from the pancreas, and somatostatin, enteroglucagon and its derivatives, and others from the intestine (Harmon et al., 1993; Janssens and Lowrey, 1987; Kao et al., 1998; Mommsen et al., 2001; Mommsen et al., 1992;). Since the pancreatic and intestinal hormones are secreted into the portal blood, the liver is exposed to concentrations that are several-fold higher than in the general circulation (Plisetskaya and Sullivan, 1989). Although the various pancreatic and intestinal hormones play critical roles in regulating hepatic metabolism of fish, the specific responses are likely to vary from those known for mammals (Plisetskaya, 1998). Hepatic metabolism is also responsive to hormones from extra-GIT organs. The relationship between estradiol and vitellogenesis is one example (Mosconi et al., 2002). The GIT mucosa, in conjunction with the liver, detoxifies and eliminates metabolic wastes and lipophilic xenobiotics. Toxic metabolic wastes and environmental contaminants are transformed by cytochrome P-450 enzymes (CYP) and eliminated by solute transporters known as multidrug resistance proteins or P-glycoproteins, with representatives in fish (Cai et al., 2003; Clarke et al., 1992; Doi et al., 2001; Husoy et al., 1994; Kleinow et al., 2000). The CYP and export transporters of fish are induced by substrates (Bard et al., 2002; Jorgensen et al., 2001; Pacheco and Santos, 2001), but the only evidence for hormonal regulation is from the rectal salt gland of sharks (Miller et al., 2002). The metabolic processes also influence circulating concentrations and forms of some hormones (e.g., thyroid hormones; Eales et al., 2000).

organs, such as the rectal salt gland of elasmobranchs (Silva et al., 1997). Although the epithelial cells lining the GIT are capable of absorbing and secreting electrolytes (Masyuk et al., 2002), there are regional differences in the magnitude of electrolyte and water flux due to differences in the densities and proportions of transporters (e.g., Na– K–ATPase, Na–K–2Cl co-transporters), ion channels, and aquaporins, and the permeability of the tight junctions linking the epithelial cells (Bakker et al., 1993). During adaptation to changes in salinity the direction and magnitude of electrolyte and water fluxes are altered by the combined actions of various hormones (Loretz et al., 1983; O’Grady and Wolters, 1990; Seidelin and Madsen, 1999) and enteric neurotransmitters (Brown and O’Grady, 1997). Most of the hormones that influence GIT osmoregulatory functions originate from extra-GIT tissues, and particularly the hypophysis (Nakamura and Hirano, 1986). Pituitary hormones known to directly modulate electrolyte and water balance of fish include oxytocin and vasopressin (Baldisserotto and Mimura, 1997; Bond et al., 2002) and prolactin (Ayson et al., 1994; Eckert et al., 2001; Kelly et al., 1999; Manzon, 2002; Morley et al., 1981; Santos et al., 1999), but those isolated from fish are not identical to mammalian forms (Anderson et al., 1995; Greger et al., 1988; Karnaky et al., 1991; Thorndyke and Shuttleworth, 1985). Osmoregulatory functions are also responsive to estradiol and testosterone (Sunny and Oommen, 2002; Vijayan et al., 2001), atrial natriuretic peptide and other related peptides (Evans, 1990; Karnaky et al., 1991; Loretz, 1996; Loretz and Pollina, 2000; O’Grady and Wolters, 1990; Takei and Hirose, 2002), angiotensin II (Anderson et al., 2001; Marsigliante et al., 2001; Takei and Tsuchida, 2000; Veillette et al., 1995;Vilella et al., 1996), and urotensin (Baldisserotto and Mimura, 1997). Glucocorticoids have been implicated in osmoregulation (Hirano and Utida, 1968; Porthe-Nibelle and Lahlou, 1975; Veillette et al., 1995), and may compensate for the absence of aldosterone and other mineralcorticoids in fish (Sloman et al., 2001). The increase in circulating concentrations of growth hormone and insulin-like growth factor during sea water adaptation (Kelly et al., 1999; Sakamoto and Hirano, 1991) partly explains the increases in feed intake, improved digestion, and enhanced growth rates when some species are raised at intermediate salinities (Boeuf and Payan, 2001; Seidelin and Madsen, 1999). However, the beneficial responses to changes in salinity are not universal and differ among stenohaline (fresh or sea water) and euryhaline fishes (Kelly et al., 1999; Perrott et al., 1991).

6. Osmoregulation 7. Defense functions The GIT tract plays an essential role in regulating the water and electrolyte status of fish (Lionetto et al., 2001), acts in conjunction with the gills and kidneys (Foskett et al., 1983), and can include specialized osmoregulatory

The expansive surface area required for efficient digestion of feedstuffs increases the risk of invasion by organisms and absorption of toxins. By necessity, the GIT has become

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the largest immunologic organ in the vertebrate body (Takahashi and Kiyono, 1999). Although the fish GIT includes innate (Douglas et al., 2001) and adaptive immune functions (Matsunaga, 1998; Rombout et al., 1993), several differences exist with mammals (Cain et al., 2002; ; Hebert et al., 2002; Magor and Magor, 2001; Mayer et al., 2002; Sailendri and Muthukkaruppan, 1975). These have been related to the phylogenetic position of fish (Hart et al., 1986; Magor and Magor, 2001). GIT immune functions are regulated by a combination of local, intra-GIT, and inter-organ signaling networks (Klein, 1998; Shanahan, 2000; Wang, 1996) and by inputs from the central nervous system (Ottaway, 1991). For example, high intensity culture and extreme environmental conditions impose stress and the surges in glucorticoids and other stress-associated hormones can compromise immune functions (Bly et al., 1997; Ruane et al., 1999; Yada and Nakanishi, 2002). Although much less is known about hormonal regulation of the defense functions of the fish GIT, there are similarities with mammals, including the involvement of interleukins (Bird et al., 2002) and other cytokines (Yada and Nakanishi, 2002).

8. Perspectives Our understanding of hormonal regulation of the GIT is largely from studies of mammals. Although this has provided valuable insights, because of the different and diverse functional demands placed on the fish GIT, it can be expected, and is increasingly understood, how the patterns, signals, and mechanisms of regulation differ among fish and from those of mammals. The phylogenetic differences among fish and other vertebrates provide opportunities to explore the evolution of hormones and signaling systems. These efforts will benefit from the development of reagents and antisera that are specific for fish and the application of new technologies (e.g., proteomics). GIT regulatory peptides and other hormones are critical for guiding development of the mammalian GIT (Pacha, 2000). Therefore, the ontogenetic changes in the types, densities, and secretory functions of endocrine cells in the GIT of fish (Elliott and Youson, 1991; El-Salhy, 1984; Garcia Hernandez et al., 1994; Kamisaka et al., 2001; KraljKlobucar, 1987; Kurokawa and Suzuki, 2002; L’Hermite et al., 1985; Reinecke et al., 1997; Youson and Potter, 1993) may play important roles in guiding the patterns of development for the GIT. This has been partly verified by the role of thyroid hormones in the parr-smolt transition of salmonids (Schreiber and Specker, 1999) and the metamorphosis of lampreys (Manzon et al., 1998). Whereas the functional activities per unit of tissue are of interest to investigators, the total functional capacities of the GIT are of critical importance to organisms. Therefore, hormones and other regulatory molecules that alter the amount of tissue can have a profound impact on the

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functional capacities of the GIT. For example, administration of growth hormone to striped bass hybrids increases GIT absorptive capacities by increasing rates of nutrient absorption per unit intestine and the amount of absorptive tissue (Sun and Farmanfarmaian, 1992). In contrast, the higher circulating concentrations of estrogen and testosterone during spawning migrations of the river lampey (Lampetra fluviatilis) induce GIT atrophy (Pickering, 1976) decrease absorptive capacities. These findings highlight the need to integrate physiologic responses at different levels of organization.

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