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What Hormones May Regulate Food Intake in Fish?

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What Hormones May Regulate Food Intake in Fish? Ayuut. Living Resour.. 1997, 10, 37 1-379 What hormones may regulate food intake in fish? Pierre-Yves Le Bail (') and Gilles Rteiif2) (') 1,nhoratoir~d~ Phytio1og-i~rkr Poissons, INRA, Campus de Umulieu, 35042 I~L~LP~,Fruncp. 1;-mail: [email protected]./r '2' Laboratoire de PhysiolobIz'e des Poissons, ibI~M;IcK. I'. 70, 29280 l'louz~n6,France. E.:-mail: ghoeu/@ijiremer.j? Received May 2, 1997; acccptcd October 23, 1997. Le Bail P.-Y., G. Bœuf. Aquat. Livin~Resour., 1997, 10,371-379. Abstract This is an ovcmicw of thc hormoncs which may be involved in food intake control in fish, and some hypo- thetical pathways of thcir action arc givcn based on mammalian knowledge. Most of the observed effects of these hormones may result from four types of mechanisms, each hormone acting by one or several as follows: (1) hormones could have a direct effect on central nervous system centres, associated with food intake behaviour or via vagal afferent neurons; (2) an indirect effect may occur via the gut which slows gastrointestinal transit, thus rcsulting in stomach distention which activates vagal afferent neurons; (3) they could have an indirect cffcct, acting dircctly on intermediary metabolism via glucose, free fatty acids or amino acids mohilization or storage; (4) the last possible pathway is an indirect effect by modifying directly or indirectly secretions of other hormones involved in food intake control. Some of thesc hormones (CCK, PYY, glucagon, adrenalin) act as short-term factors which regulate meal ingestion and are generally inhibi- tory factors. On thc othcr hand, other hormones (GH, TH, and leptin) require more time to modify food intake behaviour, and appcar as stored calorie rcgulators. However, the orientation of hormones to short-terin or to long-term action is not always clear as it has been noted for insulin and glucocorticoids, and may depend on the hormonal and metabolite environment. Keywords: Food intake, hormones. Quelles sont les hormones qui semblent impliquées dans la prise alimentaire des poissons ? Résumé Cette synthèse donne un aperçu des hormones pouvant être impliquées dans le contrôle de la prise alimen- taire des poissons et propose des voies d'action hypothétiques en se basant sur les connaissances acquises chez les mammifères. La plupart des effets observés résulteraient de quatre types de mécanismes, chaque hormone agissant par le biais d'un ou de plusieurs d'entre eux : (1) les hormones peuvent agir directement sur les noyaux du système nerveux central associés au comportement alimentaire, ou via les afférents du nerf vague ; (2) elles peuvent agir indirectement via le tube digestif en ralentissant le transit gastro-intestinal, ce qui conduit à une distension de l'estomac activant les afférents du nerf vague ; (3) elles peuvent agir indi- rectement au niveau du métabolisme intermédiaire via la mobilisation ou le stockage du glucose, des acides gras libres ou des acides aminés ; (4) elles peuvent modifier directement ou indirectement sur la sécrétion d'autres hormones impliquées dans le contrôle de la prise alimentaire. Certaines de ces hormones (CCK, PYY, glucagon, adrénaline) agissent à court terme en régulant le niveau d'ingestion et sont généralement inhibitrices. D'autres hormones (GH, TH et leptin) demandent plus de temps pour modifier le comportement de prise alimentaire et apparaissent comme des régulateurs du stockage énergétique. Cependant, les actions à court ou à long terme de ces hormones ne sont pas toujours très claires, comme cela est observé pour les glucocorticoïdes et l'insuline, et semblent dépendre de l'environnement métabolique et hormonal. Mots-clés : Prise alimentaire, hormones. Aquat. Living Resour. 6990-7740/97/06/0 IFKEMER-Elsevier, Paris P.-Y. Le Bail and G. Beuf INTRODUCTION higher vertebrates, hepatic inner ring deiodinating type III activity increases in fasted animals, contributing to In vertebrates, food intakc bchaviour is controlled by the dccreased circulating T, level (Darras et al., 1995). the brain which receives information from differcnt A recent and surprising result has been obtained by sources. Firstly, thcrc are environmental intluences Setkow et cl1 (1996) who demonstrated in starved trout such as social interactions, food quality and effort that 75-8 I % of al1 T3 was secreted by the thyroid, with involvcd in aliment ingestion. Secondly memory, only 19-25 5% resulting from T4 to T3 conversion, an which permits food recognition. Thirdly, pcriphcral opposite situation compared with fed fish (Eales and stimuli, including metabolic molecules such as glucosc Brown, 1993). Howcvcr, the drop in thyroid hormones and hormones, can givc information on the physiologi- normally occurs scveral days after the beginning of the cal status of animals. treatment. Moreover, no rclationship haï bccn found Mcchanisms which control satiety and food intake bctween appetite, time of meal or level of food ration are complex, polyfactorial and are not yct clcarly and T3 during a daily pcriod (Farbridge and Leather- defincd, cvcn in mammals in which thcy havc been land, 1993; Ciome~et al., 1997). None of these obser- studied for several decades. For several biological fac- vations identify 'I'H as having a short-tcrm role in the tors, it is difficult to separate their neuromediator, para- control of food intake. crine and endocrine effects, and for othcrs, their However, in some experiments, thyroid chronic hormonal status was not clearly established. In tïsh, if trcatmcnt incrcascd the voluntary food intake of fish we don't take into account studics on tissue localiza- (Donaldson et al., 1979). No more spccific data are tion of hormones and their plasma concentration availablc in fi\h to aid our understanding of this poten- changes, littlc information is available concerning hor- tial effect of TH. However, in mammals, T3 is well mone effect on food intake, or the mechanisms known to stimulate cell metabolism by increasing ATP i nvol vcd. consumption which nccds more glucose. The decrease The aim of this brief rcview is to givc an ovcrview of of plasma glucose observed after T, injection in carp the hormones which may be involved in food intakc (Murat and Scrfàty, 1971; Donaldson et cil., 1979), control in fish, and to givc somc hypothctical pathways suggests that T, may cxcrt its fccding action via a of their action using mammalian knowledge. This non- lower stimulation of the sympathetic system by the exhaustive and schematic presentation takes its infor- decrease of plasma carbohydratcs. This possible path- mation from numerous rcviews in which the reader way has to be established, taking into account the will find more details. nutritional status of the tish, and the apparent opposite timing of the action on food intakc of T3 and glucose. T3 specific binding sitcs havc bccn recently discov- STIMULATING HORMONES crcd in the olfactory epithelium and the brain (olfac- tory bulb, telencephalon, mid-brain and cerebellum) in migrating wild salmon (Kudo et al., 1994), suggesting, Thyroid hormones (TH) as in mammals, an important role in CNS and func- Thyroid follicles, prcscnt in the conncctive tissue of tional brain. tish pharyngeal region, release essentially tetra-iodot- Lastly, as most aspects of the thyroid hormones hyronine or thyroxine (T4). Thc major source of tri- influcncc intcrmcdiary metabolism, Leatherland iodothyronine (T,) comes from the enzymatic conver- (1994) suggested that T3 could act as a permissive fac- sion of T3 by the removal of outer ring iodine by some tor which would facilitate the direct action of other peripheral tissues, through deiodinase action (rcviews: anabolic hormones involved in food intake control. Ealcs, 1985; Leatherland, 1994). T4 is considered to be the precursor of T, which is the active hormone. Dif- Growth hormone (GH) ferently from mammals, plasma T, and T, are trans- ported by other carrier proteins, mainly corresponding The monomeric mature growth hormone (CH) is a to lipoproteins in salmonids (Babin, 1992) which have 22-kDa protein prcscnt in al1 vertebrates (review: a "buffering" effect on homeostatic control of free thy- Scanes and Campbell, 1995). It contains about 190 roid hormones. Thyroid hormones are involvcd in amino acids, but this number slightly varies betwecn development, metamorphosis, growth and reproductive different GH species. Four cysteine residues are functions, as well as in general metabolism. In fish, present that interact to form two disulfide bridges that they are among the most studied hormones, however link large and small peptide loops. The major sources their direct effects at the molecular level remain of plasma GH (synthesis and secretion) are acidophil unclear. CH-secreting cells (somatotrophs) localized in the Nutritional status has a strong influence on thyroid proximal Pars distulis of the adenohypophysis. Other function in fish. The reduction of food ration, or fast- very secondary sources are the brain and the immune ing, decreases the sensitivity of the thyroid tissue to system but thcse were not yet demonstrated in fish. GH TSH, and hepatic deiodinase activity. Thcsc two phe- receptors are present in almost al1 tissues, from mam- nomena induce a decrease in circulating T, and T4. In mals to fish, which have been studied. Growth hor- Aquat. Living Rewur., Vol. 10, no 6 - 1997 What hormones may regulate food intake in fish? mone is involved in growth, osmoregulation and reproductive functions, as well as in carbohydrate, lipid, and protein metabolism. In fish, a clear relationship exists between nutri- tional status and GH Icvels. Himick and Peter (1995) found that in goldfish plasma CH increased 30 min after the beginning of the meal. However, in our study on rainbow trout, we cannot find any relationship between diurnal GH fluctuations and the level of the food ration or the time of the daily mcal (Gomez et al., 1996). So, the short term relationship between GH and nutrition remains unclear. This discrepancy observed Time (hours) between these experimcnts could be due to difièrence in the agc or in the metabolic status of the fish, and sta- Figure 1.
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