Renal adaptations by Opsanus tau, a euryhaline aglomerular teleost, to dilute media

Lahlou, B.; Iw, Henderson; Sawyer, WH

doi:10.1152/ajplegacy.1969.216.5.1266

Cited by 69 publications

(13 citation statements)

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“…Alternately, the urinary bladder of the icefish Trematomus bernacchii is completely lined by intensely immunostained columnar cells (Masini et al 2001). Several physiological studies conducted in adult teleosts have reported that the urinary bladder significantly contributes to hyperosmoregulation by reabsorbing Na + and Cl À (review in Marshall 1995)-for example in the toadfish Opsanus tau (Lahlou et al 1969), the winter flounder Pseudopleuronectes americanus (Renfro 1975), and the rainbow trout Oncorhynchus mykiss (Curtis and Wood 1991). Therefore, our study demonstrates for the first time that the occurrence and probable involvement in osmoregulation of these urinary bladder cells start during the early larval stages of euryhaline fish such as D. labrax.…”

Section: Discussionmentioning

confidence: 99%

Morphofunctional ontogeny of the urinary system of the European sea bass Dicentrarchus labrax

et al. 2004

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European sea bass (Dicentrarchus labrax) are euryhaline fish that tolerate wide salinity fluctuations owing to several morphofunctional adaptations. Among the osmoregulatory sites (tegument, branchial chambers, digestive tract, urinary system), little is known about the kidney and the urinary bladder. The present study describes the ontogeny of the urinary system (kidney and urinary bladder) and focuses on the progressive expression of the Na(+)/K(+)-ATPase in the cells of these ion-transporting epithelia. A structural approach has shown that two pronephric urinary tubules are already present at hatching while the urinary bladder starts to differentiate. The glomus, an ultrafiltration site, occurs at day 5 (D5). The opisthonephros differentiates at D19/25 from the pronephric collecting tubules, then it rapidly grows longer and becomes folded. Na(+)/K(+)-ATPase immunolocalization and transmission electron microscopy show that ionocyte-like cells line the urinary tubules and the dorsal wall of the urinary bladder from D2/D5 on. Tubule ionocytes present a basolateral-localized fluorescence. Ionocytes of the collecting ducts and of the dorsal wall of the bladder present a fluorescence distributed in the whole cytoplasm. Fluorescence becomes stronger in later stages, suggesting a progressively increasing functionality of the urinary system in active ion transports. This observation is closely correlated with the ontogeny of osmoregulatory abilities. In juvenile and preadult fish kept in seawater, osmolality measurements demonstrate that urine is isotonic to blood. At low salinity, urine is hypotonic to blood in both stages. The capacity to produce hypotonic urine increases during ontogeny, a fact that suggests an increasing involvement of the urinary system in osmoregulation. The occurrence and the progressive functionality of the urinary system during the ontogeny, along with those of other osmoregulatory sites, are major adaptations allowing the sea bass to live in habitats of variable salinity such as lagoons and estuaries.

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Section: Discussionmentioning

confidence: 99%

Morphofunctional ontogeny of the urinary system of the European sea bass Dicentrarchus labrax

et al. 2004

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“…Opsanus is euryhaline, surviving well for months even in markedly hypo-osmotic 5% seawater (Lahlou et al 1969) and tolerating fresh water for a number of days. Although the toadfish is relatively impermeable to water and ions it still requires some means of water excretion in dilute media which cannot, of course, occur via filtration since toadfish lack glomeruli.…”

Section: The Toadfishmentioning

confidence: 99%

Guppies, toadfish, lungfish, coelacanths and frogs: a scenario for the evolution of urea retention in fishes

Griffith

1991

Environ Biol Fish

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SynopsisThe question of how (and why) the ureosmotic strategy, characteristic of Latimeria chalumnae and the chondrichthians evolved is addressed. There are three requirements for ureosmotic regulation: urea synthesis via the ornithine-urea cycle, urea tolerance involving biochemical and physiological adjustments, and urea retention that requires renal, branchial, metabolic and reproductive adaptations. Several examples of lower vertebrates in which urea plays a physiological role are considered to see whether they might provide insight into the origin of ureosmotic regulation. The guppy shows high urea synthesis and retention during embryonic development, and it is possible that a developmental role of urea is a general phenomenon in fishes. The toadfish, thought to be an enigma with high urea synthesis in the absence of an obvious physiological role of urea, is ureotelic under some conditions. Its urea excretion is likely related to renal function and/or parental care. In lungfish high ureogenesis is associated with estivation in periodically dry habitats. The resultant hyperuremia prevents ammonia toxicity, inhibits water loss and may repress metabolism. Latimeria is a classic marine ureosmotic regulator in which urea is used as an osmolyte that allows osmotic equilibrium with sea water while maintaining low ion levels. Adults of the frog, Rana cancrivora, are also ureosmotic regulators in brackish water. A scenario is proposed that suggests how ureosmotic regulation could have evolved in Latimeria and other fishes. The ornithine-urea cycle (composed of an arginine synthetic pathway and a second pathway that splits arginine into urea) occurred in fossil anadromous agnathans. Here the first pathway functioned in the ammocoete-like larvae for the generation of arginine to supplement a protein-deficient diet of algae, whereas the arginase pathway was important in the embryo for vitellin catabolism. Gnathostome evolution was associated with trends towards large eggs and prolonged development, requiring a complete ornithine-urea cycle for ammonia detoxification in embryos. Retention of a complete ornithine-urea cycle throughout adult life (via paedomorphosis) would preadapt any relatively large, sluggish, euryhaline fish for ureosmotic regulation when it was exposed to sea water. It is suggested that ureosmotic regulators evolved from freshwater or anadromous ancestors that entered the marine habitat. Once early ureosmotic regulators were established in the sea there would have been strong selection for internal fertilization and development, as is seen in Latimeria and many elasmobranchs. It is suggested that ureosmotic regulation was a common strategy in Paleozoic marine gnathostomes.

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“…Studies of teleost osmoregulation in other species have shown that their kidneys are responsible for maintaining body fluid and divalent ion homeostasis [30,31]. They counteract passive movements of water and ions between body compartments (maintained at osmotic homeostasis of about 300 mosmol/kg) and the environment (<40 mosmol/ kg for FW and >1000 mosmol/ kg for SW).…”

Section: Introductionmentioning

confidence: 99%

Population-specific renal proteomes of marine and freshwater three-spined sticklebacks

Kültz

Paguio

et al. 2016

Journal of Proteomics

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Quantitative proteomics was used to reveal biochemical differences in kidneys of marine and freshwater three-spined sticklebacks. More than 1500 unambiguous proteins were identified, 106 of which are robustly co-translationally modified. Amino-terminal acetylation sites for 94 and proline hydroxylation sites for 12 proteins, including 4 protein disulfide isomerases having the consensus motif APWCGHCK, were determined. More than 1500 proteins were quantified by LC-MS/MS yielding 120 proteins with consistent population-specific abundance differences. Twenty-five of these were selected for validation by data-independent acquisition (DIA) and spectral library based MS2 quantitation. A dense biochemical network was revealed, which promotes the synthesis of the organic osmolytes betaine, sorbitol, trimethylamine oxid (TMAO), and urea. It contains 33 of 49 proteins that are elevated in marine compared to freshwater sticklebacks, including the most highly elevated proteins (dimethylaniline monooxygenase, alanine-glyoxylate aminotransferase, glycine N-methyltransferase). Freshwater stickleback kidneys contain elevated levels of proteolytic, cytoskeletal, extracellular matrix, and calcium signaling proteins. Proteins that are most elevated in freshwater sticklebacks are ES1 protein homolog, apoptosis-associated speck-like protein containing a CARD and caspase 1. Protein-abundance network analysis demonstrates significantly higher levels of synchronized abundance control in marine sticklebacks. The significance of these findings for biochemical diversification of renal function in marine and FW sticklebacks is discussed.

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Renal adaptations by Opsanus tau, a euryhaline aglomerular teleost, to dilute media

Cited by 69 publications

References 0 publications

Morphofunctional ontogeny of the urinary system of the European sea bass Dicentrarchus labrax

Morphofunctional ontogeny of the urinary system of the European sea bass Dicentrarchus labrax

Guppies, toadfish, lungfish, coelacanths and frogs: a scenario for the evolution of urea retention in fishes

Population-specific renal proteomes of marine and freshwater three-spined sticklebacks

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