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Gce 06 Hormonal Control Vert Review Article Proof.Pdf YGCEN 9576 No. of Pages 6;4C:2; Model 5+ ARTICLE IN PRESS 7 January 2006 Disk Used Jaya (CE) / Prabakaran (TE) General and Comparative Endocrinology xxx (2006) xxx–xxx www.elsevier.com/locate/ygcen 1 Minireview 2 Hormonal control of salt and water balance in vertebrates ¤ 3 Stephen D. McCormick a,b, , Don Bradshaw c 4 a USGS, Conte Anadromous Fish Research Center, Turners Falls, MA, USA 5 b Organismic and Evolutionary Biology Program, University of Massachusetts, Amherst, MA, USA 6 c School of Animal Biology, The University of Western Australia, Perth, WA 6009, Australia 7 Received 23 August 2005; revised 3 December 2005; accepted 13 December 2005 8 9 Abstract 10 The endocrine system mediates many of the physiological responses to the homeostatic and acclimation demands of salt and water 11 transport. Many of the hormones involved in the control of salt and water transport are commonROOF to all vertebrates, although their precise 12 function and target tissues have changed during evolution. Arginine vasopressin (vasotocin), angiotensin II, natriuretic peptides, vasoac- 13 tive intestinal peptide, urotensin II, insulin and non-genomic actions of corticosteroids are involved in acute (minutes and hours) altera- 14 tions in ion and water transport. This rapid alteration in transport is primarily the result changes in behavior, blood Xow to 15 osmoregulatory organs, and membrane insertion or activation (e.g., phosphorylation) of existing transport proteins, ion and water chan- 16 nels, contransporters and pumps. Corticosteroids (through genomic actions), prolactin,D growth P hormone, and insulin-like growth factor I 17 primarily control long-term (several hours to days) changes in transport capacity that are the result of synthesis of new transport proteins, 18 cell proliferation, and diVerentiation. In addition to the important task of establishing broad evolutionary patterns in hormones involved 19 in ion regulation, comparative endocrinology can determine species and population level diVerences in signaling pathways that may be 20 critical for adaptation to extreme or rapidly changing environments. 21 2006 Published by Elsevier Inc. CTE 22 Keywords: Osmoregulation; Vertebrates; Ion transport; AVP; AVT;E ANP; Angiotensin; Aldosterone; Cortisol; Growth hormone; Prolactin; IGF-I 23 1. Physiological requirements for salt and water transport conserve water. The demands for ion and water transport 36 can vary greatly, depending on both internal factors such as 37 24 Maintenance of constant intracellular and extracellular metabolic rate, and external factors such as salinity or 38 25 ionic and osmotic environment (Bernard’s constancy of ‘le water availability. 39 26 milieu intérieur’) is critical for theORR normal functioning of Hormones play a critical role in signaling and control- 40 27 cells. With several notable exceptions, such as hagWsh, ling the homeostatic and acclimation demands of salt and 41 28 sharks and ureotelic marine frogs, the majority of verte- water transport (Bentley, 1998). In spite of the diVerences in 42 29 brates maintain a remarkably similar salt content of their transport needs and capabilities among vertebrates (and 43 30 extracellular Xuid, approximately one-third that of seawa- even the organs responsible for ion transport) many of the 44 31 ter. This basic strategy results in diVerent transport hormones involved are remarkably similar. In addition to 45 32 demands for vertebratesUNC depending on their external envi- acting on the basic mechanisms of ion transport, natural 46 33 ronment. In fresh water environments vertebrates must selection will act on the underlying neuroendocrine con- 47 34 actively take up salts, whereas in seawater they must secrete trols. Our understanding of large evolutionary trends (e.g., 48 35 excess salts. In terrestrial environments vertebrates must evolution of terrestriality) and adaptation of species to new 49 or severe environments requires knowledge of the underly- 50 ing control mechanisms for salt and water regulation. The 51 * Corresponding author. Fax: +1 413 863 9810. purpose of this overview is to provide a general framework 52 E-mail address: [email protected] (S.D. McCormick). for the hormonal control of osmoregulation in vertebrates 53 0016-6480/$ - see front matter 2006 Published by Elsevier Inc. doi:10.1016/j.ygcen.2005.12.009 YGCEN 9576 No. of Pages 6;4C:2; Model 5+ ARTICLE IN PRESS 7 January 2006 Disk Used Jaya (CE) / Prabakaran (TE) 2 S.D. McCormick, D. Bradshaw / General and Comparative Endocrinology xxx (2006) xxx–xxx 54 and to highlight the contributed papers to a symposium on classic example of an acute regulatory response is signaling 70 55 “Hormonal Control of Water and Salt Balance in Verte- by arginine vasotocin (AVT; or arginine vasopressin, AVP 71 56 brates” held in Boston in May 2005 as part of the Fifteenth in the case of mammals) to induce antidiuresis and thus 72 57 International Congress of Comparative Endocrinology. conserve water. Increased plasma osmolality (such as might 73 occur following reduced water intake or exposure to seawa- 74 58 2. Acute endocrine responses ter) signals osmosensors in the hypothalamus to release 75 AVT. Increased circulating AVT binds to membrane 76 59 Most organisms have at least a limited capacity to V2-type AVT receptors in the renal collecting duct, result- 77 60 respond to an osmotic or ionic challenge by rapidly chang- ing in the insertion of stored aquaporin (water channel) 78 61 ing existing transport mechanism. Some of these may be proteins into the plasma membrane. This increases water 79 62 independent of hormones (autoregulatory), such as changes reabsorption by the kidney permitting restoration of 80 63 in ion availability to transporters. Most changes in ion plasma osmolality. 81 64 transport, however, are cued by neuroendocrine or endo- Although it is likely that the AVT/AVP hormone has an 82 65 crine factors. Although there is a continuum of temporal osmoregulatory role in most vertebrates, the AVT–aquapo- 83 66 responses, we can roughly divide transport responses into rin response may have evolved with terrestriality, since it 84 67 those that activate existing transport mechanisms (acute has only been found to date in amphibians (Uchiyama and 85 68 regulatory response), and those that require development Konno, this volume) birds (Goldstein, this volume) and 86 69 of new proteins and cells (acclimation response) (Fig. 1). A mammals (Table 1). AVT functions as a physiological anti- 87 diuretic hormone in the few species of reptiles that have 88 been studied to date and reduces glomerular Wltration rate 89 ACCLIMATION PHASE ACUTE PHASE X and urine ow by acting on both V1-type receptors in the 90 aVerent arteriole and VROOF-type receptors found in the thin 91 2 MC (genomic) PROLACTIN intermediate segment and collecting ducts (Bradshaw and 92 AVT/AVP GH / IGF-I Bradshaw, 1996).P V -type AVT receptors have also been 93 ANG II 2 NAT PEPT localized in the reptilian nephron (Bradshaw and Brad- 94 MC (non-genomic) shaw, 2002). Shane et al. (2006, this volume) have shown 95 that AVT can stimulate amiloride-sensitive (ENaC) sodium 96 reabsorption in the A6 Xenopus kidney cell line. Recent evi- 97 PLASMA HORMONE LEVEL dence summarized by Balment (2006, this volume) indicates 98 that AVT is involved in salt secretion and/or water conser- 99 vation necessary for seawater acclimation of teleost Wsh. 100 CTEDAlthough a V2-type AVT receptor has yet to be described in 101 Wsh, Perrott et al. (1993) have found that AVT can cause 102 E increased cAMP in the trout renal tubules, consistent with a 103 V2-type AVT receptor action in mammals. AVT at very low 104 doses is antidiuretic in Wsh (Balment et al., 1993), but AVT 105 receptors are upregulated in sea water and localized in the 106 gill leaXets, suggesting a direct action of this peptide on the 107 TRANSPORT CAPACITY ( ) CAPACITY TRANSPORT gills (Avella et al., 1999; Guibbolini et al., 1989). Thus, 108 ION / WATER TRANSPORT ( ) ION / WATER AVT’s role in water conservation may have arisen early in 109 MIN HOUR DAY WEEK vertebrates. It should be noted, however, that a wide diver- 110 sity of Wshes has yet to be examined. In particular it will be 111 OSMOTIC CHALLENGE of interest to determine if this response is present in teleosts 112 that are restricted to fresh water where demands for water 113 Fig. 1. Schematic diagram of the hormonal control of ion and water trans- port. Osmotic stimulus (such as alteration in internal osmotic pressure conservation may have placed little selection on develop- 114 caused by dehydrationUNCORR or exposure to seawater) results in release of rapid ment or maintenance of this capacity. Acher (2002) has sug- 115 acting hormones (blue) that activate existing proteins and cells to increase gested that “striking evolutionary stability” of AVT/AVP is 116 ion and/or water transport in the acute phase (seconds to hours) through the result of strong selection pressure on maintaining the 117 stimulation of existing mechanism (e.g., insertion of aquaporins into mem- osmoregulatory function of this hormone. In contrast, the 118 branes or phosphorylation of transporters). Osmotic stimuli and rapid act- W ing hormones will increase long term acting hormones (green) to bring urea-based isosmotic strategy of cartilaginous shes has 119 about increased protein synthesis, cell proliferation, diVerentiation and tis- ‘released’ these Wsh from selective pressure allowing a 120 sue reorganization that will allow increased transport capacity in the accli- greater diversity of structure of AVT-like peptides in this 121 mation phase (several hours to several days). The ability to increase group of vertebrates. 122 maximum transport capacity will be present only in species with phenotypic The natriuretic peptides, as their name implies, have 123 plasticity in response to osmotic challenge. Abbreviations: AVT D arginine vasotocin; AVP D arginine vasopressin; ANG II D angiotensin II; NAT important, acute osmoregulatory actions in vertebrates.
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