Osmotic and Ion Regulation in Amphibians

Hillyard, Stanley D.; Møbjerg, Nadja; Tanaka, Shigeyasu; Larsen, Erik Hviid

doi:10.1201/9780849380525.ch9

Cited by 15 publications

(33 citation statements)

References 440 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…A reduction in the abundance or activity of transepithelial ion transport proteins such as epithelial sodium channels (ENaC) or the sodiumpotassium pump (Na + /K + -ATPase; NKA) during sloughing may also cause disruption to the transportation of ions. ENaC is a membrane-bound protein channel found in the apical membrane of epithelial cells that is responsible for the uptake of Na + from the environment, while NKA is an active membrane protein pump found in the basolateral layer of epithelial cells that establishes an electrochemical gradient for ion channels like ENaC to transport Na + against their concentration gradients (Hillyard et al, 2008). Thus, examining the relative expression of these proteins in sloughing amphibians relative to non-sloughing amphibians may clarify the mechanism through which this disruption of ion transport during sloughing occurs.…”

Section: Introductionmentioning

confidence: 99%

Living with a leaky skin: upregulation of ion transport proteins during sloughing

Cramp

Franklin

2017

Journal of Experimental Biology

View full text Add to dashboard Cite

Amphibian skin is a multifunctional organ providing protection from the external environment and facilitating the physiological exchange of gases, water and salts with the environment. In order to maintain these functions, the outer layer of skin is regularly replaced in a process called sloughing. During sloughing, the outermost layer of the skin is removed in its entirety, which has the potential to interfere with skin permeability and ion transport, disrupting homeostasis. In this study, we measured, in vivo, the effects of sloughing on the cutaneous efflux of ions in toads Rhinella marina kept in freshwater conditions. We also measured transepithelial potential, cutaneous resistance, active ion transport and the distribution, abundance and gene expression of the key ion transport proteins sodium-potassium ATPase (NKA) and epithelial sodium channel (ENaC) during sloughing. We hypothesised that the increase in transepithelial efflux of ions during sloughing is a consequence of increased permeability and/or a reduction in the abundance or expression of cutaneous ion transport proteins, resulting in disruption of internal ion homeostasis. There was a significant increase in sodium and chloride efflux during sloughing in R. marina. However, although in vitro skin resistance decreased after sloughing, active sodium transport increased commensurate with an increase in NKA and ENaC protein abundance in the skin. These changes in skin function associated with sloughing did not affect the maintenance of internal electrolyte homeostasis. These results suggest that during sloughing, amphibians actively maintain internal homeostasis by increasing cutaneous rates of ion uptake.

show abstract

Section: Introductionmentioning

confidence: 99%

Living with a leaky skin: upregulation of ion transport proteins during sloughing

Cramp

Franklin

2017

Journal of Experimental Biology

View full text Add to dashboard Cite

show abstract

“…1996). The density of these glands in water‐absorbing regions of the skin is quite high and acinar cells in the glands have aquaporin 5 in the apical membrane as do cells in the salivary glands of mammals (Hillyard et al. 2009).…”

Section: Discussionmentioning

confidence: 99%

Chemosensory function of amphibian skin: integrating epithelial transport, capillary blood flow and behaviour

Hillyard

Willumsen

2010

Acta Physiologica

View full text Add to dashboard Cite

Terrestrial anuran amphibians absorb water across specialized regions of skin on the posterioventral region of their bodies. Rapid water absorption is mediated by the insertion of aquaporins into the apical membrane of the outermost cell layer. Water moves out of the epithelium via aquaglyceroporins in the basolateral membrane and into the circulation in conjunction with increased capillary blood flow to the skin and aquaporins in the capillary endothelial cells. These physiological responses are activated by intrinsic stimuli relating to the animals' hydration status and extrinsic stimuli relating to the detection of osmotically available water. The integration of these processes has been studied using behavioural observations in conjunction with neurophysiological recordings and studies of epithelial transport. These studies have identified plasma volume and urinary bladder stores as intrinsic stimuli that activate the formation of angiotensin II (AII) to stimulate water absorption behaviour. The coordinated increase in water permeability and capillary blood flow appears to be mediated primarily by sympathetic stimulation of beta adrenergic receptors, although the neurohypopyseal hormone arginine vasotocin (AVT) may also play a role. Extrinsic stimuli relate primarily to the ionic and osmotic properties of hydration sources. Toads avoid NaCl solutions that have been shown to be harmful in acute exposure, approx. 200-250 mm. The avoidance is partially attenuated by amiloride raising the hypothesis that the mechanism for salt detection by toads resembles that for salt taste in mammals that take in water by mouth. In this model, depolarization of the basolateral membrane of taste cells is coupled to afferent neural stimulation. In toad skin we have identified innervation of skin epithelial cells by branches of spinal nerves and measured neural responses to NaCl solutions that elicit behavioural avoidance. These same concentrations produce depolarization of the basolateral membrane in isolated epithelial preparations. As with salt taste in mammals, the neural responses and depolarization of basolateral membrane potential are partially inhibited by amiloride. In addition, toads are more tolerant of sodium gluconate solution which is consistent with the phenomenon in mammalian taste physiology termed the anion paradox in which sodium salts with larger molecular weight anions produce a reduced intensity of salt taste. Finally, toads also avoid concentrated solutions of a non-electrolyte, mannitol, which differs from NaCl solutions in not affecting transepithelial conductance and requires a longer time to depolarize the basolateral membrane. Osmotic stimuli may mediate sensory processes for longer term detection of conditions with low water potential while ionic stimuli are more important for shorter term analysis of rehydration sources.

show abstract

“…1988) denoted as ‘cross talk’(Schultz 1992). Studies of the regulation of the transport systems of the principal cell compartment were reviewed recently (Hillyard et al. 2009).…”

Section: Functional Organization Of Anuran Skin Epitheliummentioning

confidence: 99%

“…2001). The luminal plasma membrane also expresses an AQP‐x5 like aquaporin as identified by immunofluorescence labelling of the subepidermal glands of Bufo woodhouseii by Stanley Hillyard (Hillyard et al. 2009).…”

Section: Role Of Apical Chloride Channels Of the γ‐Type Mr Cell: Regumentioning

confidence: 99%

“…They have their origin in Copenhagen from the Zoophysiological Laboratory by work of August Krogh and his student Hans Ussing respectively. Directing the attention to the dependence of ion transport on energy metabolism in epithelia, they have had a significant impact on the way we consider ion regulation in animals and man, the methods by which we study epithelial ion transport and the interpretation of the functional organization of transporting epithelia (Andreoli 1999, Reuss 2001, Larsen 2002, Kirschner 2004, Evans 2008, Palmer & Andersen 2008, Hillyard et al. 2009).…”

mentioning

confidence: 99%

See 1 more Smart Citation

Reconciling the Krogh and Ussing interpretations of epithelial chloride transport – presenting a novel hypothesis for the physiological significance of the passive cellular chloride uptake

Larsen

2011

Acta Physiologica

View full text Add to dashboard Cite

In 1937, August Krogh discovered a powerful active Cl(-) uptake mechanism in frog skin. After WWII, Hans Ussing continued the studies on the isolated skin and discovered the passive nature of the chloride uptake. The review concludes that the two modes of transport are associated with a minority cell type denoted as the γ-type mitochondria-rich (MR) cell, which is highly specialized for epithelial Cl(-) uptake whether the frog is in the pond of low [NaCl] or the skin is isolated and studied by Ussing chamber technique. One type of apical Cl(-) channels of the γ-MR cell is activated by binding of Cl(-) to an external binding site and by membrane depolarization. This results in a tight coupling of the uptake of Na(+) by principal cells and Cl(-) by MR cells. Another type of Cl(-) channels (probably CFTR) is involved in isotonic fluid uptake. It is suggested that the Cl(-) channels serve passive uptake of Cl(-) from the thin epidermal film of fluid produced by mucosal glands. The hypothesis is evaluated by discussing the turnover of water and ions of the epidermal surface fluid under terrestrial conditions. The apical Cl(-) channels close when the electrodiffusion force is outwardly directed as it is when the animal is in the pond. With the passive fluxes eliminated, the Cl(-) flux is governed by active transport and evidence is discussed that this is brought about by an exchange of cellular HCO(3) (-) with Cl(-) of the outside bath driven by an apical H(+) V-ATPase.

show abstract

Osmotic and Ion Regulation in Amphibians

Cited by 15 publications

References 440 publications

Living with a leaky skin: upregulation of ion transport proteins during sloughing

Living with a leaky skin: upregulation of ion transport proteins during sloughing

Chemosensory function of amphibian skin: integrating epithelial transport, capillary blood flow and behaviour

Reconciling the Krogh and Ussing interpretations of epithelial chloride transport – presenting a novel hypothesis for the physiological significance of the passive cellular chloride uptake

Contact Info

Product

Resources

About