From finch to fish to man: Role of aquaporins in body fluid and brain water regulation

doi:10.1016/j.neuroscience.2004.06.043

Neuroscience

Volume 129, Issue 4, 2004, Pages 897-904

https://doi.org/10.1016/j.neuroscience.2004.06.043 Get rights and content

Abstract

Charles Darwin, in his Origin of the Species, noted that different species of finches on the Galapagos Islands had adapted their beak size based on where they sought their food. Homer Smith, in his book From Fish to Philosopher, discussed the evolution of the nephron from a single conduit in salt water vertebrates, to nephrons with large glomerular capillaries and proximal and distal tubules in fresh water vertebrates, to smaller glomerular capillaries in amphibians, to nephrons with loops of Henle to allow for urinary concentration and dilution in mammals. The kidney with its million nephrons has emerged as the vital organ for regulating body fluid composition and volume. With the recent discovery of aquaporin water channels, our understanding of volume regulation has been greatly enhanced. This article reviews current knowledge regarding: 1) the unifying hypothesis of body fluid volume regulation; 2) brain aquaporins and their role in pathophysiologic states; and 3) function and regulation of renal aquaporins in the syndrome of inappropriate antidiuretic hormone secretion (SIADH).

Section snippets

Unifying hypothesis of body fluid volume regulation

Body fluid volume regulation by the kidney relies on the complex interaction of numerous factors (Table 1). Clinically maladaptive responses can occur when extrarenal factors override the “innate wisdom” of the kidney (Starling, 1909). For example, in patients with cardiac failure or liver disease and in pregnant women, the normal kidney continues to retain sodium and water despite expanded blood, plasma, and extracellular fluid (ECF) volumes. Such fluid retention may ultimately lead to

Acknowledgments

This work was supported by the National Institute of Health (DK19928). Yung-Chang Chen was supported by a grant from the Chang Gung Memorial Hospital (Taipei, Taiwan).

References (74)

G. Fujisawa et al.
Therapeutic efficacy of nonpeptide ADH antagonist OPC-31260 in SIADH rats
Kidney Int
(1993)
K. Fushimi et al.
Phosphorylation of serine 256 is required for cAMP-dependent regulatory exocytosis of aquaporin-2 water channel
J Biol Chem
(1997)
D.E. Griesdale et al.
Aquaporins and brain edema
Surg Neurol
(2004)
H. Kannan et al.
Supraoptic neurosecretory neurons: evidence for the existence of converging inputs both from carotid baroreceptors and osmoreceptors
Brain Res
(1978)
J.K. Kim et al.
Arginine vasopressin gene expression in chronic cardiac failure in rats
Kidney Int
(1990)
T. Ma et al.
Severely impaired urinary concentrating ability in transgenic mice lacking aquaporin-1 water channels
J Biol Chem
(1998)
R.S. Pedersen et al.
Urinary aquaporin-2 in healthy humans and patients with liver cirrhosis and chronic heart failure during baseline conditions and after acute water load
Kidney Int
(2003)
H. Tsukaguchi et al.
Molecular characterization of a broad selectivity neutral solute channel
J Biol Chem
(1998)
F. Umenishi et al.
Comparison of three methods to quantify urinary aquaporin-2 protein
Kidney Int
(2002)
J.L. Venero et al.
Aquaporins in the central nervous system
Prog Neurobiol
(2001)

M. Amiry-Moghaddam et al.

An alpha-syntrophin-dependent pool of AQP4 in astroglial end-feet confers bidirectional water flow between blood and brain

Proc Natl Acad Sci USA

(2003)

M. Amiry-Moghaddam et al.

The molecular basis of water transport in the brain

Nat Rev Neurosci

(2003)

M. Amiry-Moghaddam et al.

Delayed K⁺ clearance associated with aquaporin-4 mislocalization: phenotypic defects in brains of alpha-syntrophin-null mice

Proc Natl Acad Sci USA

(2003)

R.J. Anderson et al.

Mechanism of effect of thoracic inferior vena cava constriction on renal water excretion

J Clin Invest

(1974)

J. Badaut et al.

Aquaporins in brain: distribution, physiology, and pathophysiology

J Cereb Blood Flow Metab

(2002)

T. Berl et al.

Disorders of water metabolism

C. Bernard

Lecons sur lex phenomenes de la vie communs aux animaux et auz vegetaux

(1885)

D. Bichet et al.

Role of vasopressin in abnormal water excretion in cirrhotic patients

Ann Intern Med

(1982)

D.K. Binder et al.

Increased seizure threshold in mice lacking aquaporin-4 water channels

Neuroreport

(2004)

M. Buemi et al.

Urinary excretion of aquaporin-2 water channel during pregnancy

Cell Physiol Biochem

(2001)

Chen, YC, Cadnapaphornchai, MA, Schrier, RW (2004) Clinical update on renal aquaporins. Biol Cell, in...

R.J. Cody et al.

Sodium and water balance in chronic congestive heart failure

J Clin Invest

(1986)

J.N. Cohn et al.

Plasma norepinephrine as a guide to prognosis in patients with chronic congestive heart failure

N Engl J Med

(1984)

Darwin C (1839) The voyage of the H.M.S. Beagle. London, UK: Penguin...

S.R. DiGiovanni et al.

Regulation of collecting duct water channel expression by vasopressin in Brattleboro rat

Proc Natl Acad Sci USA

(1994)

C.A. Ecelbarger et al.

Escape from vasopressin-induced antidiuresis: role of vasopressin resistance of the collecting duct

Am J Physiol Renal Physiol

(1998)

C.A. Ecelbarger et al.

Increased abundance of distal sodium transporters in rat kidney during vasopressin escape

J Am Soc Nephrol

(2001)

C.A. Ecelbarger et al.

Role of renal aquaporins in escape from vasopressin-induced antidiuresis in rat

J Clin Invest

(1997)

A. Frigeri et al.

Localization of MIWC and GLIP water channel homologs in neuromuscular, epithelial and glandular tissues

J Cell Sci

(1995)

N. Fujita et al.

Role of water channel AQP-CD in water retention in SIADH and cirrhotic rats

Am J Physiol

(1995)

T. Fukuma et al.

Role of renal water channel (aquaporin-2) in ascites formation in patients with liver cirrhosis: urinary aquaporin-2 excretion and response to vasopressin infusion

Gastroenterology

(1996)

K. Fushimi et al.

Cloning and expression of apical membrane water channel of rat kidney collecting tubule

Nature

(1993)

J. Hensen et al.

Aldosterone in congestive heart failure: analysis of determinants and role in sodium retention

Am J Nephrol

(1991)

P. Ivarsen et al.

Increased urinary excretion of aquaporin 2 in patients with liver cirrhosis

Gut

(2003)

J.S. Jung et al.

Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance

Proc Natl Acad Sci USA

(1994)

J.K. Kim et al.

Vasopressin gene expression in rats with experimental cirrhosis

Hepatology

(1993)

L.S. King et al.

Defective urinary-concentrating ability due to a complete deficiency of aquaporin-1

N Engl J Med

(2001)

Cited by (25)

Renal osteodystrophy: A historical review of its origins and conceptual evolution
2022, Bone Reports
Citation Excerpt :
Pertinent parallel evolutionary changes as amphibians evolved in the Devonian period were the rudiments of a respiratory system in the lungfish, known in Swahili as Kamongo, that Homer Smith sought, imported, studied, and narrated (Smith, 1932). It was also during this stretch of time when osmoregulation and excretion of nitrogenous products of migrating predatory fish led to the appearance of the beginnings of the vascular tufts of the glomerulus for the excretion of waste products by filtration, followed by increasing refinements in tubular regulatory function and the loop of Henle necessary for water, electrolyte, calcium, and phosphate regulation when life on land necessitated the preservation of water and scarce elements necessary to maintain homeostasis (Bochenbauer and Keita, 2021; Keogh et al., 2021; Koonan, 2012; Natochin, 1996; Schrier et al., 2004). As fundamental for survival as those evolutionary genetic transmutations of bone metabolism were, they went unknown until the past few decades.
Long considered an inert supporting framework, bone studies went neglected until the 17th century when they began as descriptive microscopic studies of structure which over time progressed into that of chemistry and physiology. It was in the mid-19th century that studies evolved into an inquisitive discipline which matured into the experimental investigation of bone in health and disease in the 20th century, and ultimately that of molecular studies now deciphering the genetic language of bone biology. These fundamental studies were catalyzed by increasing clinical interest in bone disease. The first bone disease to be identified was rickets in 1645. Its subsequent connection to albuminuric patients reported in 1883 later became renal osteodystrophy in 1942, launching studies that elucidated the functions of vitamin D and parathyroid hormone and their role in the altered calcium and phosphate metabolism of the disease. Studies in osteoporosis and renal osteodystrophy have driven most recent progress benefitting from technological advances in imaging and the precision of evaluating bone turnover, mineralization, and volume. This review exposes the progress of bone biology from a passive support structure to a dynamically regulated organ with vital homeostatic functions whose understanding has undergone more revisions and paradigm shifts than that of any other organ.
Renal Toxicology/Nephrotoxicity of Cisplatin and Other Chemotherapeutic Agents
2018, Comprehensive Toxicology: Third Edition
Acute kidney injury (AKI) is characterized by a rapid decline in kidney function. AKI can be induced in many ways, and one of the most common causes of AKI is chemical nephrotoxicity. Anticancer chemotherapeutics such as gemcitabine, pemetrexed, bevacizumab, ifosfamide, and cisplatin are considered nephrotoxic. Of these, cisplatin is commonly studied as nephrotoxicity is its major dose-limiting toxicity. This article will outline the mechanisms by which these chemotherapeutics induce AKI. Furthermore, this article will outline previous and current strategies developed to abrogate chemotherapy-induced AKI. Currently, there are no FDA-approved renoprotective agents for the treatment/prevention of chemotherapy-induced AKI. Thus, developing ways to study and understand the molecular mechanisms involved in AKI will aid in the development of future renoprotective agents.
Aquaporin molecular characterization in the sea-bass (Dicentrarchus labrax): The effect of salinity on AQP1 and AQP3 expression
2007, Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology
Euryhaline fish possess the ability to compensate for environmental salinity changes through hydro-mineral regulation. A number of proteins have been studied in order to understand water and ion exchanges, known as fish osmoregulation. Sea-bass (Dicentrarchus labrax) cDNA sequences encoding a homologue of mammalian aquaporin (termed AQP1) and a homologue of mammalian aquaglyceroporin (termed AQP3) have been isolated and sequenced. The aquaporin amino acid sequences share respectively more than 60% and 65% identity with other known aquaporins. We have shown that salinity influences aquaporin expression levels in the gill, kidney and digestive tract, the main osmoregulatory organs. AQP1 may have a major osmoregulatory role in water transport in kidney and gut in SW-acclimated fish, whereas AQP3 could be implicated in gill water transport in FW-acclimated fish.
Hyponatremia: Clinical Diagnosis and Management
2007, American Journal of Medicine
Citation Excerpt :
The mechanisms involved in producing concentrated or dilute urine have been enumerated in great detail elsewhere,17 and we will review these mechanisms only briefly so as to provide a context for the clinical categorization of patients with hyponatremia.
Hyponatremia is a common clinical problem in hospitalized patients and nursing home residents. It also may occur in healthy athletes after endurance exercise. The majority of patients with hyponatremia are asymptomatic and do not require immediate correction of hyponatremia. Symptomatic hyponatremia is a medical emergency requiring rapid correction to prevent the worsening of brain edema. How fast we should increase the serum sodium levels depends on the onset of hyponatremia and still remains controversial. If the serum sodium levels are corrected too rapidly, patients may develop central pontine myelinolysis, but if they are corrected too slowly, patients may die of brain herniation. We review the epidemiology and mechanisms of hyponatremia, the sensitivity of women to hyponatremic injury, the adaptation and maladaptation of brain cells to hyponatremia and its correction, and the practical ways of managing hyponatremia. Because the majority of hyponatremia is caused by the non-osmotic release of vasopressin, the recent approval of the vasopressin receptor antagonist conivaptan for euvolemic hyponatremia may simplify hyponatremia management. However, physicians should be aware of the risk of rapid correction of hyponatremia, hypotension, and excessive fluid intake.
Tubulopathy
2007, Medicine
Water and Sodium Retention in Edematous Disorders: Role of Vasopressin and Aldosterone
2006, American Journal of Medicine
Citation Excerpt :
When the vasopressin V2 receptors (V2Rs) on the collecting duct are stimulated, the resultant activation of the adenylate-cyclic AMP pathway increases aquaporin-2 (AQP2) water channel trafficking to the apical membrane of the collecting duct. This sequence of events leads to an increase in water reabsorption and can cause hyponatremia in edematous disorders.19–22 The collecting duct in the distal nephron is also the site of aldosterone action and the natriuretic peptides.
This article discusses the pathophysiology of sodium and water retention in edematous disorders with a particular focus on cardiac failure, cirrhosis, and pregnancy. The body fluid volume hypothesis, which emphasizes the dominant role of arterial baroreceptors in renal sodium and water excretion, is reviewed. With arterial underfilling, either due to a decrease in cardiac output or peripheral arterial vasodilation, the normal central inhibition of the sympathetic nervous system activity and baroreceptor-mediated, nonosmotic arginine vasopressin (AVP) release is attenuated. The resultant increase in renal adrenergic activity stimulates the renin-angiotensin-aldosterone system. Although the resultant increase in systemic vascular resistance compensates for the primary arterial underfilling, this activation of the neurohumoral axis results in diminished sodium and water delivery to the renal collecting duct sites of aldosterone, AVP, and natriuretic peptide action. This diminished distal sodium and water delivery will be discussed as an important factor in the failure to escape from the sodium-retaining effects of aldosterone, the resistance to the natriuretic and diuretic effects of natriuretic peptides, and the diminished maximal solute-free water excretion in patients with edema. The role of the nonosmotic AVP release in water retention and hypo-osmolality/hyponatremia has been demonstrated in patients and experimental animals by administering nonpeptide, orally active vasopressin V₂ receptor antagonists. These agents have been found to increase solute-free water excretion in patients with water-retaining, hyponatremic edema as well as in experimental animals.

View all citing articles on Scopus

View full text

From finch to fish to man: Role of aquaporins in body fluid and brain water regulation

Abstract

Section snippets

Unifying hypothesis of body fluid volume regulation

Acknowledgments

Kidney Int

J Biol Chem

Surg Neurol

Brain Res

Kidney Int

J Biol Chem

Kidney Int

J Biol Chem

Kidney Int

Prog Neurobiol

An alpha-syntrophin-dependent pool of AQP4 in astroglial end-feet confers bidirectional water flow between blood and brain

Proc Natl Acad Sci USA

The molecular basis of water transport in the brain

Nat Rev Neurosci

Delayed K+ clearance associated with aquaporin-4 mislocalization: phenotypic defects in brains of alpha-syntrophin-null mice

Proc Natl Acad Sci USA

Mechanism of effect of thoracic inferior vena cava constriction on renal water excretion

J Clin Invest

Aquaporins in brain: distribution, physiology, and pathophysiology

J Cereb Blood Flow Metab

Disorders of water metabolism

Lecons sur lex phenomenes de la vie communs aux animaux et auz vegetaux

Role of vasopressin in abnormal water excretion in cirrhotic patients

Ann Intern Med

Increased seizure threshold in mice lacking aquaporin-4 water channels

Neuroreport

Urinary excretion of aquaporin-2 water channel during pregnancy

Cell Physiol Biochem

Sodium and water balance in chronic congestive heart failure

J Clin Invest

Plasma norepinephrine as a guide to prognosis in patients with chronic congestive heart failure

N Engl J Med

Regulation of collecting duct water channel expression by vasopressin in Brattleboro rat

Proc Natl Acad Sci USA

Escape from vasopressin-induced antidiuresis: role of vasopressin resistance of the collecting duct

Am J Physiol Renal Physiol

Increased abundance of distal sodium transporters in rat kidney during vasopressin escape

J Am Soc Nephrol

Role of renal aquaporins in escape from vasopressin-induced antidiuresis in rat

J Clin Invest

Localization of MIWC and GLIP water channel homologs in neuromuscular, epithelial and glandular tissues

J Cell Sci

Role of water channel AQP-CD in water retention in SIADH and cirrhotic rats

Am J Physiol

Role of renal water channel (aquaporin-2) in ascites formation in patients with liver cirrhosis: urinary aquaporin-2 excretion and response to vasopressin infusion

Gastroenterology

Cloning and expression of apical membrane water channel of rat kidney collecting tubule

Nature

Aldosterone in congestive heart failure: analysis of determinants and role in sodium retention

Am J Nephrol

Increased urinary excretion of aquaporin 2 in patients with liver cirrhosis

Gut

Molecular characterization of an aquaporin cDNA from brain: candidate osmoreceptor and regulator of water balance

Proc Natl Acad Sci USA

Vasopressin gene expression in rats with experimental cirrhosis

Hepatology

Defective urinary-concentrating ability due to a complete deficiency of aquaporin-1

N Engl J Med

Delayed K⁺ clearance associated with aquaporin-4 mislocalization: phenotypic defects in brains of alpha-syntrophin-null mice