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Body Water Homeostasis: Clinical Disorders of Urinary Dilution and Concentration

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Body Water Homeostasis: Clinical Disorders of Urinary Dilution and Concentration Review Body Water Homeostasis: Clinical Disorders of Urinary Dilution and Concentration Robert W. Schrier Department of Medicine, University of Colorado School of Medicine, Denver, Colorado J Am Soc Nephrol 17: 1820–1832, 2006. doi: 10.1681/ASN.2006030240 he discovery of the aquaporin-1 (AQP1) water channel AQP deletion/mutation are of importance not only for kidney by Agre and colleagues (1,2), which led to the Nobel function but also for other epithelia (14). T Prize in 2003, has revolutionized the understanding of AVP regulates AQP2 in both an acute (short term) (15) and body fluid water regulation by the kidney. Moreover, the iden- chronic (long term) manner (16,17). The short-term regulation tification of other water channels in the kidney, namely AQP2, by AVP involves trafficking of vesicles that contain AQP2 to the 3, and 4, along with urea and ion transporters, has allowed a apical membrane with resultant increased water permeability. much improved understanding of urinary dilution and concen- Suppression of plasma AVP reverses this exocytosis of AQP2, tration in health and disease at the cellular and molecular levels and the vesicles are retrieved from the membrane (endocytosis) (3–8). into the cytoplasm. Both the short- and long-term regulation of The AQP have provided a pathway for water movement AQP2 by AVP is initiated by activation of the V2 receptor on across cellular membranes that could not be explained by sim- the basolateral membrane of the collecting duct. The binding of ple diffusion through the lipid bilayers of cell membranes. AVP to the V2 receptor, which is coupled to a guanine-nucle- AQP1 has been found to be expressed constitutively on both otide–binding protein Gs, results in activation of adenylyl cy- the apical and the basolateral membranes of the proximal tu- clase. This results in an increase in intracellular cAMP concen- bule and descending limb of Henle’s loop. This water channel tration that mediates the activation of protein kinase A (PKA). is not under control of vasopressin but is important in urinary Activated PKA phosphorylates the serine 256 residue at the concentration. Water efflux through these channels in the de- C-terminus of AQP2 protein (18,19). The phosphorylated AQP2 scending limb is an important factor in the countercurrent then is translocated to the collecting duct apical membrane, concentrating mechanism, and diminished maximal urinary thus constituting short-term regulation of AQP2. The long-term osmolality has been shown in AQP1 knockout mice (9) and regulation of AQP2 is mediated by the cAMP response element humans without the AQP1 gene (10). in the 5Ј flanking region of the AQP2 gene in response to AVP AQP2, 3, and 4 are expressed in the cortical and medullary stimulation (20,21). The AQP2 transcription and protein expres- collecting duct (Figure 1) (11). AQP2 is found exclusively in the sion involves the phosphorylation of the cAMP response el- principal cells of the collecting tubule and collecting duct and is ement–binding protein. In contrast to the involvement of PKA known to be regulated by arginine vasopressin (AVP). AQP3 activation in the short-term regulation of AQP2, there is some and 4 are located on the basolateral membrane of the principal in vivo evidence for PKA-independent long-term regulation of cells in the collecting duct. AQP3 knockout mice exhibit sub- AQP2 expression by AVP (22). There also is recent in vitro (23) stantial polyuria secondary to vasopressin-resistant nephro- and in vivo (24) evidence for AQP2 regulation by hyperosmo- genic diabetes insipidus (NDI) (12). AQP3 is regulated by AVP. lality independent of AVP. The in vivo experiments were per- AQP4 predominates on the basolateral membrane of the inner formed in Brattleboro rats, which have no detectable circulatory medulla and is not regulated by AVP. AQP4 knockout mice AVP. also exhibit an NDI that is less severe than that observed in the Disorders of water balance can lead to either clinically rele- AQP3 knockout mice (13). Whereas AQP3 and AQP4 constitute vant hyponatremia or hypernatremia. Hyponatremia is much the exit channels for water movement across the basolateral more common and is the most frequent fluid and electrolyte membrane of the collecting duct, AQP2 is the water channel for disturbance in hospitalized patients. When defined as plasma Ͻ water reabsorption across the apical membrane of the principal sodium concentration 135 mEq/L, the prevalence of hypona- cells of the collecting duct. These transgenic mouse models of tremia in hospitalized patients may be as high as 15 to 30%. Studies indicate that 40 to 75% of these cases are hospital acquired (25,26). It is clear that hyponatremia may occur in the presence of an increase in total body sodium, a decrease in total Published online ahead of print. Publication date available at www.jasn.org. body sodium, or a near-normal total body sodium (Figure 2). In Address correspondence to: Dr. Robert W. Schrier, Department of Medicine, any of these three circumstances, hyponatremia has occurred University of Colorado School of Medicine, 4200 East Ninth Avenue B-173, Denver, CO 80262. Phone: 303-315-8059; Fax: 303-315-2685; E-mail: because of a relatively greater amount of total body water as [email protected] compared with total body solute. Recent advances of the mech- Copyright © 2006 by the American Society of Nephrology ISSN: 1046-6673/1707-1820 J Am Soc Nephrol 17: 1820–1832, 2006 Body Water Homeostasis 1821 water excretion. However, these defects generally are not of sufficient magnitude to lead to hyponatremia in association with a normal fluid intake. With normal fluid intake, hypona- tremia generally results from the inability to decrease urine osmolality below plasma rather than a defect in maximal sol- ute-free water excretion. The failure to dilute the urine below plasma generally is due to a failure to suppress maximally the antidiuretic hormone AVP (27). The failure of some hypothy- roid patients to suppress plasma AVP during an acute water load was reported initially by Skowsky et al. (28). Recently, experimental studies in rats with advanced hypo- thyroidism (serum total T4 0.6 Ϯ 0.02 ng/dl) further examined urinary dilution and maximal solute-free water excretion (29). There was a significant decrease in cardiac index and heart rate in these hypothyroid animals that was normalized with l- thyroxine replacement. During an acute water load, these hy- pothyroid animals exhibited a significantly lower urine flow Figure 1. Nephron sites of aquaporin (AQP) water channels and higher urinary osmolality than either control animals or (blue), ion transporters (black), and urea transporters (green). hypothyroid animals that were treated with l-thyroxine. The ROMK, renal outer medullary potassium channel; UT, urea hypothyroid animals also had significantly higher plasma AVP transporter. concentrations despite a lower plasma osmolality that normal- ized with l-thyroxine treatment. The impaired water excretion anisms of impaired urinary diluting capacity that lead to these also was associated with an upregulation of AVP-mediated hyponatremic disorders are discussed. AQP2 expression and membrane trafficking in the inner me- dulla (Figure 3). Taken together, these results suggested a major Hypothyroidism role of nonosmotic AVP release in the hyponatremia associated Advanced primary hypothyroidism can lead to hyponatre- with advanced hypothyroidism. Studies therefore were under- mia, most frequently associated with myxedema. Milder forms taken with a vasopressin V2 receptor antagonist (OPC-31260) in of hypothyroidism can lead to a decrease in renal blood flow, these animals with advanced hypothyroidism. Minimal urinary glomerular filtration, and a decrease in maximal solute-free osmolality in hypothyroid rats that were treated with the V2 Figure 2. Diagnostic and therapeutic approach to the hypovolemic, euvolemic, and hypervolemic hyponatremic patient. 1822 Journal of the American Society of Nephrology J Am Soc Nephrol 17: 1820–1832, 2006 Figure 3. Effects in control (CTL) and hypothyroid (HT) and thyroid (T) replaced rats on urine flow (A), urine osmolality (B), plasma vasopressin (AVP; C), and inner medullary AQP2 plasma membrane (PM)/intracellular vesical (ICV) densitometry ratio (D). Reprinted from reference (27), with permission. receptor antagonist was normalized as compared with un- fect in hypothyroidism would be of clinical relevance only in Ͻ treated hypothyroid rats (97 versus 430 mOsm/kg H2O; P patients who were undergoing excessive extrarenal fluid losses 0.0001). Maximal solute-free water excretion in the hypothyroid (e.g., diarrhea). rats significantly increased but did not reach euthyroid values. These experimental results therefore support the pivotal role of Addison’s Disease and Hypopituitarism the baroreceptor-mediated nonosmotic AVP release in the hy- Primary adrenal insufficiency (Addison’s disease) involves ponatremia associated with advanced hypothyroidism. The deficiency of glucocorticoid and mineralocorticoid hormones, submaximal solute-free water excretion would not be of clinical both of which can be associated with hyponatremia. Hypopi- significance unless other factors, such as diuretics or large fluid tuitarism is associated with only glucocorticoid deficiency, be- intakes, intervene. cause the renin-angiotensin-aldosterone system is intact. Al- Of interest, a defect in maximal urinary concentration was though secondary hypothyroidism is associated with observed at a somewhat less prolonged
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