Mechanism of active chloride secretion by shark rectal gland: role of Na-K-ATPase in chloride transport

1977 ◽  
Vol 233 (4) ◽  
pp. F298-F306 ◽  
Author(s):  
P. Silva ◽  
J. Stoff ◽  
M. Field ◽  
L. Fine ◽  
J. N. Forrest ◽  
...  
Keyword(s):  
Chloride Transport ◽  
Sodium Concentration ◽  
Chloride Secretion ◽  
Squalus Acanthias ◽  
Rectal Gland ◽  
Tentative Hypothesis ◽  
Shark Rectal Gland ◽  
Electrochemical Equilibrium

The isolated rectal gland of Squalus acanthias was stimulated to secrete chloride against an electrical and a chemical gradient when perfused in vitro by theophylline and/or dibutyryl cyclic AMP. Chloride secretion was depressed by ouabain which inhibits Na-K-ATPase. Thiocyanate and furosemide also inhibited chloride secretion but ethoxzolamide, a carbonic anhydrase inhibitor, did not. Chloride transport was highly dependent on sodium concentration in the perfusate. The intracellular concentration of chloride averaged 70-80 meq/liter in intact glands, exceeding the level expected at electrochemical equilibrium and suggesting active transport of chloride into the cell. These features suggest a tentative hypothesis for chloride secretion by the rectal gland in which the uphill transport of chloride into the cytoplasm is coupled through a membrane carrier to the downhill movement of sodium along its electrochemical gradient. The latter is maintained by the Na-K-ATPase pump while chloride is extruded into the duct by electrical forces.

scholarly journals AMP-activated protein kinase and adenosine are both metabolic modulators that regulate chloride secretion in the shark rectal gland (Squalus acanthias)

2018 ◽  
Vol 314 (4) ◽  
pp. C473-C482
Author(s):  
Rugina I. Neuman ◽  
Juliette A. M. van Kalmthout ◽  
Daniel J. Pfau ◽  
Dhariyat M. Menendez ◽  
Lawrence H. Young ◽  
...  
Keyword(s):  
Feedback Inhibition ◽  
Short Circuit ◽  
Short Circuit Current ◽  
Chloride Secretion ◽  
Squalus Acanthias ◽  
Catalytic Subunit ◽  
Rectal Gland ◽  
Apical Side ◽  
Shark Rectal Gland ◽  
Amp Activated Protein Kinase

The production of endogenous adenosine during secretagogue stimulation of CFTR leads to feedback inhibition limiting further chloride secretion in the rectal gland of the dogfish shark (Squalus acanthias). In the present study, we examined the role of AMP-kinase (AMPK) as an energy sensor also modulating chloride secretion through CFTR. We found that glands perfused with forskolin and isobutylmethylxanthine (F + I), potent stimulators of chloride secretion in this ancient model, caused significant phosphorylation of the catalytic subunit Thr172 of AMPK. These findings indicate that AMPK is activated during energy-requiring stimulated chloride secretion. In molecular studies, we confirmed that the activating Thr172 site is indeed present in the α-catalytic subunit of AMPK in this ancient gland, which reveals striking homology to AMPKα subunits sequenced in other vertebrates. When perfused rectal glands stimulated with F + I were subjected to severe hypoxic stress or perfused with pharmacologic inhibitors of metabolism (FCCP or oligomycin), phosphorylation of AMPK Thr172 was further increased and chloride secretion was dramatically diminished. The pharmacologic activation of AMPK with AICAR-inhibited chloride secretion, as measured by short-circuit current, when applied to the apical side of shark rectal gland monolayers in primary culture. These results indicate that that activated AMPK, similar to adenosine, transmits an inhibitory signal from metabolism, that limits chloride secretion in the shark rectal gland.

Mode of activation of salt secretion by C-type natriuretic peptide in the shark rectal gland

1999 ◽  
Vol 277 (6) ◽  
pp. R1725-R1732 ◽  
Author(s):  
Patricio Silva ◽  
Richard J. Solomon ◽  
Franklin H. Epstein
Keyword(s):  
Short Circuit ◽  
Short Circuit Current ◽  
Chloride Secretion ◽  
Squalus Acanthias ◽  
Rectal Gland ◽  
Stimulatory Action ◽  
Kinase C ◽  
Shark Rectal Gland ◽  
Pkc Activation ◽  
Stimulation Of

We studied the modes of activation of the salt-secreting rectal gland of the spiny dogfish, Squalus acanthias, by the native cardiac peptide CNP. The stimulatory action of CNP in isolated perfused glands is inhibited by 10 mM procaine, presumably by blocking release of vasoactive intestinal peptide (VIP) from nerves. Procaine reduces the slope of the dose-response curve of human CNP and that of shark CNP (each P < 0.0001). CNP increases short-circuit current in cultured rectal gland cells from 4.8 ± 1.6 to 27.0 ± 7.8 μA/cm2. It also stimulates the secretion of chloride in isolated perfused glands in the presence of 10 mM procaine from 72 ± 31 to 652 ± 173 μeq ⋅ h−1 ⋅ g−1. These results suggest that CNP has a direct cellular action not mediated by the neural release of VIP. The residual stimulation of perfused glands in the presence of procaine was almost completely inhibited by staurosporine [10 nM; an inhibitor of protein kinase C (PKC)] from 652 ± 173 to 237 ± 61 μeq ⋅ h−1 ⋅ g−1. Although CNP stimulates guanylyl cyclase in shark rectal gland, chloride secretion of perfused glands was not elicited by 8-bromoadenosine-cGMP (8-BrcGMP) alone nor by the activator of PKC phorbol ester. The combination of PKC activation and 8-BrcGMP infusion, however, stimulated chloride secretion in perfused glands from 94 ± 30 to 506 ± 61 μeq ⋅ h−1 ⋅ g−1, a level comparable to that observed in glands blocked with procaine. Several parallel pathways appear to be synergistic in activating chloride secretion stimulated by CNP in the rectal gland.

Ultrastructural and cytochemical characterization of cultured dogfish shark rectal gland cells

1996 ◽  
Vol 271 (6) ◽  
pp. C1993-C2003 ◽  
Author(s):  
J. D. Valentich ◽  
K. J. Karnaky ◽  
T. W. Ecay
Keyword(s):  
Smooth Muscle ◽  
Epithelial Cells ◽  
Indirect Effects ◽  
Chloride Secretion ◽  
Cellular Heterogeneity ◽  
Rectal Gland ◽  
Tubular Epithelial Cells ◽  
Shark Rectal Gland ◽  
Dogfish Shark

The dogfish shark rectal gland (SRG) is histologically complex, containing connective, nerve, and smooth muscle tissue and at least three types of epithelial cells: secretory tubule, central duct, and endothelial. This cellular heterogeneity precludes studies of the intact SRG from distinguishing direct tubular effects of mediators that modulate chloride secretion from their indirect effects on nonepithelial cells such as neurons. Primary SRG cultures express high levels of secretagogue-stimulated chloride secretion, suggesting that SRG cells retain a significant level of cytodifferentiation in vitro. However, because nontubular cells could contaminate these cultures, the question of whether secretagogues activate chloride secretion through direct or indirect effects on tubular epithelial cells remains unresolved. To address this issue, detailed ultrastructural and cytochemical analyses of SRG cultures were carried out to assess the level of cellular heterogeneity and the degree of cytodifferentiation expressed by SRG cells in vitro. The results demonstrate that, after 15 days, primary SRG monolayer cultures are composed exclusively of tubular epithelial cells with no detectable contamination by central duct cells, fibroblasts, smooth muscle cells, endothelial cells, or neurons. Tubular epithelial cells express most of the structural features of native SRG cells, including numerous mitochondria, massive basolateral surface amplification, complex tight junctions, and an extensive tubulovesicular system in the apical cytoplasm. Cultured SRG cells also display a striking level of polarization of cytoplasmic organelles and plasma membrane secretagogue receptors. These results account for the exceptionally high rates of electrogenic chloride secretion by SRG tubular epithelial cells in vitro and confirm that the effects of secretagogues on transport activity reflect their direct interaction with tubular epithelial cells.

The effect of organotin compounds on chloride secretion by the in vitro perfused rectal gland of Squalus acanthias

1989 ◽  
Vol 100 (2) ◽  
pp. 307-314 ◽  
Author(s):  
Richard Solomon ◽  
Stephanie Lear ◽  
Robert Cohen ◽  
Kate Spokes ◽  
Patricio Silva ◽  
...  
Keyword(s):  
Chloride Secretion ◽  
Squalus Acanthias ◽  
Organotin Compounds ◽  
Rectal Gland

Osmoregulation by the Prenatal Spiny Dogfish, Squalus Acanthias

1982 ◽  
Vol 101 (1) ◽  
pp. 295-305 ◽  
Author(s):  
DAVID H. EVANS ◽  
AIMO OIKARI ◽  
GREGG A. KORMANIK ◽  
LEIGH MANSBERGER
Keyword(s):  
Sea Water ◽  
Electrical Potential ◽  
Fluid Flows ◽  
Maternal Plasma ◽  
Water Levels ◽  
Squalus Acanthias ◽  
Rectal Gland ◽  
Na Efflux ◽  
Uterine Fluid ◽  
Electrochemical Equilibrium

Late in gestation of the ovoviviparous dogfish, Squalus acanthias, the uterine fluids are essentially sea water, while the plasma of the ‘pup’ is similar to that of the female, i.e. isotonic to sea water/uterine fluids, with significantly less Na and Cl, and substantial concentrations of urea. Early ‘candle’ embryos are bathed in ‘candle’ fluid and uterine fluid which contains Na and Cl concentrations intermediate between maternal plasma and sea water levels, K concentrations above sea water levels, and urea concentrations slightly below those found in the maternal plasma. Both fluids are isotonic to sea water and maternal plasma. Incubation of ‘candles’ with associated embryos in sea water for 4–6 days resulted in significant increases in ‘candle’ fluid Na and Cl concentrations, and a decline in ‘candle’ fluid K and urea levels. However, under these conditions, the ‘candle’ embryo is still able to regulate plasma Na, Cl, K and urea concentrations. The efflux of Cl is approximately 5 times the efflux of Na from the prenatal ‘pup’; however, both effluxes are equivalent to those described for adult elasmobranchs. The transepithelial electrical potential (TEP) across the ‘pup’ is −4.4 mV in sea water, which indicates that both Na and Cl are maintained out of electrochemical equilibrium. Cloacal fluid flows vary diurnally with Na and Cl concentrations significantly above those of the plasma. Rectal gland efflux can account for 50–100% of the Na efflux, but less than 25% of the Cl efflux. Removal of the rectal gland resulted in an increase in plasma Na and Cl concentrations 48 or 72 h after the operation, but in both cases it appears that some extra rectal gland excretory system balances at least some of the net influx of both salts. Our results demonstrate that even very young ‘candle’ embryos of S. acanthias are capable of osmoregulation, and that older embryos (‘pups') osmoregulate against sea water intra-utero and display the major hallmarks of elasmobranch osmoregulation, including a reduced ionic permeability and a functional rectal gland for net extrusion of NaCl. In addition, it appears that other pathways exist for salt extrusion in addition to the rectal gland. Note:

Primary role of volume expansion in stimulation of rectal gland function

1985 ◽  
Vol 248 (5) ◽  
pp. R638-R640 ◽  
Author(s):  
R. Solomon ◽  
M. Taylor ◽  
S. Sheth ◽  
P. Silva ◽  
F. H. Epstein
Keyword(s):  
Plasma Volume ◽  
Plasma Osmolality ◽  
Sodium Concentration ◽  
Chloride Secretion ◽  
Ringer Solution ◽  
Rectal Gland ◽  
Primary Role ◽  
Fourfold Increase ◽  
Gland Function

Chloride secretion by the in vivo rectal gland of the shark is stimulated by the intravascular infusion of salt solutions of varying osmolar and sodium concentration. In a cross-perfused and denervated rectal gland, the infusion of a small amount of a hypertonic salt solution raises plasma osmolality but does not increase plasma volume in the donor fish. Under these conditions, rectal gland chloride secretion is not stimulated. A subsequent infusion of isotonic shark Ringer solution increases plasma volume 50%, decreases plasma osmolality, and produces a fourfold increase in chloride secretion and a threefold decrease in vascular resistance within the gland. Both the vasodilatory and secretory responses also follow the infusion of a hypotonic shark Ringer solution. The data further support the hypothesis that the rectal gland of the shark is involved in the regulation of intravascular volume rather than in osmoregulation.

Sodium Chloride Secretion in Rectal Gland of Dogfish, Squalus acanthias

Physiology ◽  
1986 ◽  
Vol 1 (4) ◽  
pp. 134-136
Author(s):  
R. Greger ◽  
E. Schlatter ◽  
H. Gögelein
Keyword(s):  
Sodium Chloride ◽  
Basic Principle ◽  
Peptide Hormones ◽  
Chloride Secretion ◽  
Hormonal Control ◽  
Squalus Acanthias ◽  
Rectal Gland

The rectal gland of the dogfish is specialized for the secretion of sodium chloride. The secretion is controlled by peptide hormones such as, for example, vasointestinal peptide. The mechanism of sodium chloride secretion is apparently similar to that present in mammalian epithelia such as the colon and trachea. This essay discusses the basic principle of sodium chloride secretion in the rectal gland and the mechanism of its hormonal control.

Atriopeptin stimulation of rectal gland function in Squalus acanthias

1985 ◽  
Vol 249 (3) ◽  
pp. R348-R354 ◽  
Author(s):  
R. Solomon ◽  
M. Taylor ◽  
D. Dorsey ◽  
P. Silva ◽  
F. H. Epstein
Keyword(s):  
Volume Expansion ◽  
Epithelial Transport ◽  
Extracellular Volume ◽  
Chloride Secretion ◽  
Hormonal Control ◽  
Rectal Gland ◽  
Gland Function ◽  
Stimulation Of

The rectal gland of the shark plays a significant role in the homeostasis of extracellular volume. Regulation of rectal gland function is under hormonal control, but the precise identity of the humoral mediator is unknown. Atriopeptin stimulates rectal gland chloride secretion in vivo. This stimulation of epithelial transport is accompanied by systemic and local hemodynamic effects. Atriopeptin also stimulates chloride secretion by the in vitro perfused rectal gland, an effect that is not accompanied by hemodynamic changes. Extracts of shark heart, but not muscle, brain, kidney, or intestine, contain a heat-stable trypsin-sensitive substance capable of in vitro stimulation of rectal gland chloride secretion. Electron micrographic analysis reveals multiple neurosecretory-like granules in atrial cardiocytes that are only rarely seen in ventricular cardiocytes. By using the in vitro perfused gland as a biologic assay, serum obtained after extracellular volume expansion reveals the presence of a rectal gland stimulatory factor that is not present in serum before expansion. These results are consistent with the hypothesis that atriopeptin is present in shark cardiocytes and is released during volume expansion. The atriopeptin stimulates rectal gland chloride secretion, providing a negative feedback mechanism for the regulation of extracellular volume.

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