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Activity, Abundance, Distribution and Expression of Na+/K+-Atpase in the Salt Glands of Crocodylus Porosus Following Chronic Saltwater Acclimation

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Activity, Abundance, Distribution and Expression of Na+/K+-Atpase in the Salt Glands of Crocodylus Porosus Following Chronic Saltwater Acclimation 1301 The Journal of Experimental Biology 213, 1301-1308 © 2010. Published by The Company of Biologists Ltd doi:10.1242/jeb.039305 Activity, abundance, distribution and expression of Na+/K+-ATPase in the salt glands of Crocodylus porosus following chronic saltwater acclimation Rebecca L. Cramp1, Nicholas J. Hudson2 and Craig E. Franklin1,* 1School of Biological Sciences, The University of Queensland, Brisbane, QLD 4072, Australia and 2CSIRO Livestock Industries, Queensland Bioscience Precinct, St Lucia, QLD 4067, Australia *Author for correspondence ([email protected]) Accepted 5 January 2010 SUMMARY Saltwater crocodiles, Crocodylus porosus, possess lingual salt glands which function to remove excess Na+ and Cl– accumulated as a consequence of living in salt water. Little is known about the nature of ion transport systems in C. porosus salt glands and how these systems respond to an osmotic challenge. In the present study, we examined the distribution and regulation of the Na+/K+-ATPase (NKA) pump, specifically the a-(catalytic) subunit in the salt glands of C. porosus chronically acclimated (6 months) to freshwater (FW) or 70% seawater (SW). We hypothesised that in the SW-acclimated C. porosus there would be an up- regulation of the abundance, activity and gene expression of the NKA transporter. NKA was immunolocalised to the lateral and basal membrane of secretory cells. As predicted, the NKA a-subunit was 2-fold more abundant in SW-acclimated C. porosus salt glands. NKA gene expression was also elevated in the salt glands of SW- vs FW-acclimated crocodiles. There was no increase in the specific activity of NKA in SW-acclimated animals and the in vitro rate of oxygen consumption by salt gland slices from SW- acclimated animals was not significantly different from that of FW-acclimated animals. The proportion of tissue oxygen consumption rate attributable to NKA activity was not different between SW- and FW-acclimated animals (approximately 50%). These data suggest that either chronic SW acclimation does not affect NKA in crocodile salt glands in the same manner as seen in other models or crocodiles possess the capacity to moderate NKA activity following prolonged exposure to SW. Key words: acclimation, lingual salt gland, osmoregulation, reptile. INTRODUCTION electrogenic NKA pumps which provide the driving force for the Many marine non-mammalian vertebrates utilise specialised extra- active secretion of Cl–. Basolateral Na+–K+–2Cl–-co-transporters renal salt-secreting tissues (salt glands) to assist in the removal of (NKCC) are responsible for the active uptake of chloride ions from excess sodium and chloride ions. Marine birds utilise orbital salt the blood, while cystic fibrosis transmembrane conductance glands (Schmidt-Nielsen, 1960), turtles have lachrymally located regulator (CFTR)-like Cl– transporters are responsible for the salt glands (Schmidt-Nielsen and Fänge, 1958), sea snakes have secretion of Cl– across the apical membrane. Na+ and K+ gradients sublingual salt glands (Taub and Dunson, 1967; Dunson, 1968) and are actively maintained by basolateral NKA and NKCC pumps and crocodiles have lingual salt glands (Taplin and Grigg, 1981). K+ channels, while Na+ secretion occurs via ion-selective Similarly, elasmobranchs utilise rectal glands for salt excretion paracellular channels in apical tight junctions using the (Bulger, 1963). The morphology of these salt-secreting glands is electrochemical gradient generated by the active secretion of Cl– highly conserved (Kirschner, 1980). Most are typically classified from the apical membrane (reviewed by Shuttleworth and as compound, tubular structures; they are highly vascularised and Hildebrandt, 1999). densely innervated. Salt gland tubules consist of numerous highly Salt glands are highly plastic tissues – both morphologically and modified secretory cells, which are characterised by their highly functionally. Acute exposure to hypersaline drinking water results amplified basolateral membrane surface area. The basolateral in rapid increases in gland size and secretory rate in domestic ducks membranes of salt gland secretory cells are closely apposed to (Schmidt-Nielsen and Kim, 1964). During chronic saltwater surrounding capillary networks. The much smaller apical surface exposure, avian salt gland secretory cells undergo hypertrophy as provides an interface between the cell and the secretory tubule well as hyperplasia (Knight and Peaker, 1979; Bentz et al., 1999). lumen. These tissues are typified by their abundance of ion pumps, In addition, NKA activity and expression increase almost 2-fold including Na+/K+-ATPase (NKA), a basolateral, transmembrane ion within as little as 24 h (Fletcher et al., 1967; Hildebrandt, 1997). pump responsible for the maintenance of cellular electrochemical Similar changes in secretory cell size and NKA activity and gradients through the movement of Na+ and K+ ions against their expression have also been observed in elasmobranch and teleost osmotic gradients. NKA is consistently present in large amounts in models (Piermarini and Evans, 2000; Scott et al., 2004; Pillans et salt gland tissues specialised for active ion transport (Dunson and al., 2005; Evans, 2008). Dunson, 1975). Indeed, avian salt glands and elasmobranch rectal The saltwater crocodile, Crocodylus porosus, possesses lingual glands have become important model tissues for studies of the role salt glands which function to remove excess Na+ and Cl– ions of NKA in active ion transport. accumulated as a consequence of living in marine environments The current model of ion secretion by salt gland cells suggests (Taplin and Grigg, 1981). Saltwater crocodiles display a remarkable that the secretory cells’ basolateral membrane contains numerous degree of euryhalinity; animals have been found to successfully THE JOURNAL OF EXPERIMENTAL BIOLOGY 1302 R. L. Cramp, N. J. Hudson and C. E. Franklin osmoregulate in salinities ranging from 0 to 60‰ (Grigg et al., microrespirometer containing a magnetic stir bar and 1 ml of air- 1986). Like avian salt glands, chronic exposure to hypersaline water saturated crocodile Ringer solution at 25°C. The chamber was sealed results in an increase in C. porosus salt gland size and Na+ secretion and the rate of oxygen consumption by the tissue in the chamber capacity (Cramp et al., 2007; Cramp et al., 2008). In addition, was recorded continuously over a period of 2 h or until the partial chronic saltwater exposure results in increased blood flow to the pressure of oxygen in the chamber had dropped by 50%. At the end gland and changes in the innervation patterns of the tissue (Franklin of this period the chambers were opened and the Ringer solution and Grigg, 1993; Cramp et al., 2007). Very little is known about replaced with fresh air-saturated Ringer solution containing the cellular ion transport processes operating in the salt glands of 1 mmol l–1 ouabain. The chamber was once again sealed and the crocodiles, nor is there much data pertaining to long-term changes rate of oxygen consumption measured over 2 h. Preliminary trials in salt glands as a consequence of prolonged saltwater exposure. were conducted during which time it was established that the rate In the present study we sought to investigate how NKA responds of oxygen consumption by the isolated salt gland sections remained to prolonged SW acclimation in the salt glands of juvenile C. reasonably constant for more than 4h. At the completion of the trial, porosus and to determine whether increases in salt gland secretory tissue pieces were removed from the nylon mesh bags, blotted dry, capacity correlate with increases in the activity and/or abundance weighed and frozen at –20°C for later determination of DNA content. of NKA in salt gland secretory cells. We hypothesised that like Prior to the commencement and at the end of each trial, the rate of many other vertebrate salt glands, saltwater acclimation would background oxygen consumption in the chamber (from contaminants result in an increase in NKA activity, abundance and gene and the electrode) in the absence of any tissue was recorded and expression which would serve to maximise the overall secretory this mean rate subtracted from the tissue rates. In order to minimise capacity of the tissue. bacterial contamination of the chamber, chambers were cleaned prior to trials with 70% ethanol and the chamber Ringer solution was MATERIALS AND METHODS filtered through 0.2mm Millipore syringe filters. Metabolic rate was Animal husbandry determined using inbuilt functions of the Strathkelvin 782 meter All experiments were carried out with the approval of the University normalised to both tissue mass and DNA content (see below). The of Queensland Animal Welfare Unit (permit numbers SIB/257/ proportion of total tissue oxygen consumption associated with NKA 05/ARC/URG and SIB/186/06/ARC/URG) and Queensland Parks activity was determined by subtracting the rate of oxygen and Wildlife Service (permit no. WISP00993703). consumption in the presence of ouabain from that measured in the Estuarine crocodiles (C. porosus Schneider 1801) were obtained absence of ouabain. from Fleays Wildlife Park (West Burleigh, QLD, Australia) as eggs and were incubated in a Clayson IM 1000 incubator (Axyos, Measurement of nucleic acid content Brendale, QLD, Australia) at 30°C in plastic containers covered Total genomic DNA was extracted from salt gland tissues using a in moist vermiculite. Upon hatching, all animals were held in commercially available genomic DNA extraction
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