Oxygen consumption and Na+,K+-ATPase activity of rectal gland and gill tissue in the spiny dogfish, Squalus acanthias

1997 ◽  
Vol 75 (5) ◽  
pp. 820-825 ◽  
Author(s):  
John D. Morgan ◽  
George K. Iwama ◽  
Jonathan M. Wilson
Keyword(s):  
Oxygen Consumption ◽  
Atpase Activity ◽  
Total Mass ◽  
Gill Tissue ◽  
Squalus Acanthias ◽  
Rectal Gland ◽  
Spiny Dogfish ◽  
Tissue Respiration ◽  
Nacl Transport ◽  
Activity Measurements

Oxygen consumption was measured in rectal gland and gill tissue of the spiny dogfish (Squalus acanthias) to estimate the energy cost of salt (NaCl) transport in these osmoregulatory organs. Ouabain (0.5 mM) was used to specifically inhibit Na+,K+-ATPase activity and thus the portion of tissue respiration required by the Na+/K+ pump. The total mass-specific oxygen consumption of rectal gland tissue (14.2 ± 1.2 μmol O2/(g wet mass∙h)) was significantly higher than measured for the gills (9.6 ± 1.4 μmol O2/(g wet mass∙h)), and ouabain significantly reduced oxygen consumption in both tissues. Ouabain-sensitive oxygen consumption of the rectal gland accounted for 55% of total mass-specific oxygen consumption, compared with 22% for the gill. The higher ion transport capacity of the rectal gland was also evident in Na+,K+-ATPase specific activity measurements of fresh tissue samples, which were sixfold higher in the rectal gland than in the gill. Ouabain-sensitive oxygen consumption was also calculated on the basis of total organ mass to determine the portion of whole-animal oxygen uptake related to organismal NaCl transport. The cost of NaCl secretion was estimated to be 0.5% of standard metabolic rate for the rectal gland compared with 0.14% for the gills, suggesting that this process constitutes a relatively small portion of the total energy budget in the spiny dogfish.

scholarly journals Energy cost of NaCl transport in isolated gills of cutthroat trout

1999 ◽  
Vol 277 (3) ◽  
pp. R631-R639 ◽  
Author(s):  
John D. Morgan ◽  
George K. Iwama
Keyword(s):  
Oxygen Consumption ◽  
Energy Cost ◽  
Resting Metabolic Rate ◽  
Cutthroat Trout ◽  
Gill Tissue ◽  
Tissue Respiration ◽  
Nacl Transport ◽  
Oncorhynchus Clarki Clarki ◽  
The Cost ◽  
Total Tissue

Few studies have made direct estimates of the energy required for ion transport in gills of freshwater (FW) and seawater (SW) fish. Oxygen consumption was measured in excised gill tissue of FW-adapted cutthroat trout ( Oncorhynchus clarki clarki) to estimate the energy cost of NaCl transport in that osmoregulatory organ. Ouabain (0.5 mM) and bafilomycin A1 (1 μM) were used to inhibit the Na+-K+and H+ pumps, respectively. Both inhibitors significantly decreased gill tissue oxygen consumption, accounting for 37% of total tissue respiration. On a whole mass basis, the cost of NaCl uptake in the FW trout gill was estimated to be 1.8% of whole animal oxygen uptake. An isolated, saline-perfused gill arch preparation was also used to compare gill energetics in FW- and SW-adapted trout. The oxygen consumption of FW gills was significantly (33%) higher than SW gills. On a whole animal basis, total gill oxygen consumption in FW and SW trout accounted for 3.9 and 2.4% of resting metabolic rate, respectively. The results of both experiments suggest that the energy cost of NaCl transport in FW and SW trout gills represents a relatively small (<4%) portion of the animal’s total energy budget.

Propionate induces cell swelling and K+ accumulation in shark rectal gland

1989 ◽  
Vol 257 (2) ◽  
pp. C377-C384 ◽  
Author(s):  
G. M. Feldman ◽  
F. N. Ziyadeh ◽  
J. W. Mills ◽  
G. W. Booz ◽  
A. Kleinzeller
Keyword(s):  
Atpase Activity ◽  
Propionic Acid ◽  
Exchange Process ◽  
Squalus Acanthias ◽  
Cell Swelling ◽  
Rectal Gland ◽  
Structural Elements ◽  
Acid Diffusion ◽  
Shark Rectal Gland ◽  
Solute Accumulation

Small organic anions have been reported to induce cell solute accumulation and swelling. To investigate the mechanism of swelling, we utilized preparations of rectal gland cells from Squalus acanthias incubated in medium containing propionate. Propionate causes cells to swell by diffusing across membranes in its nonionic form, acidifying cell contents, and activating the Na+-H+ antiporter. The Na+-H+ exchange process tends to correct intracellular pH (pHi), and thus it maintains a favorable gradient for propionic acid diffusion and allows propionate to accumulate. Activation of the Na+-H+ antiport also facilitates Na+ entry into the cell and Nai accumulation. At the same time Na+-K+-ATPase activity, unaffected by propionate, replaces Nai with Ki, whereas the K+ leak rate, decreased by propionate, allows Ki to accumulate. As judged by 86Rb+ efflux, the reduction in K+ leak was not due to propionate-induced cell acidification or reduction in Cli concentration. Despite inducing cell swelling, propionate did not disrupt cell structural elements and F actin distribution along cell membranes.

Morphology of the rectal gland of the spiny dogfish (Squalus acanthias) shark in response to feeding

2009 ◽  
Vol 87 (5) ◽  
pp. 440-452 ◽  
Author(s):  
Victoria Matey ◽  
Chris M. Wood ◽  
W. Wesley Dowd ◽  
Dietmar Kültz ◽  
Patrick J. Walsh
Keyword(s):  
Early Stage ◽  
Basolateral Membrane ◽  
Small Diameter ◽  
Squalus Acanthias ◽  
Rectal Gland ◽  
Secretory Cells ◽  
Spiny Dogfish ◽  
Apical Surface ◽  
Stratified Epithelium ◽  
Outer Capsule

The morphology of the rectal gland was examined in spiny dogfish ( Squalus acanthias L, 1758) sharks fasted (1 week) or 6 and 20 h postfeeding. The morphology of the fasted gland showed a pattern reflecting a dormant physiology, with thick gland capsule, thick stratified epithelium, and secretory parenchyma with tubules of small diameter and lumen. The secretory cells of the tubular epithelium were enlarged and irregularly shaped with abnormally condensed or highly vacuolized cytoplasm containing numerous lysosomes. Early-stage apoptotic cells were not uncommon. Secretory cells showed signs of low activity, e.g., mitochondria with weakly stained matrix and small cristae, poorly branched infoldings of basolateral membranes, and microvesicle-free subapical cytoplasm. All characteristics examined changed significantly upon feeding, consistent with increased salt and fluid secretion: the outer capsule muscle layer and the stratified epithelium decreased in diameter; the tubules enlarged; the secretory cells showed extensive development of the basolateral membrane, more mitochondria, and abundant apical microvesicles. Secretory cell apical surface was increased. The minor differences between morphology in 6 and 20 h postfeeding indicated that changes took place rapidly and were complete by 6 h. Our results are discussed in the context of prior studies of metabolism, proteomics, and cellular pathways of gland activation.

cAMP-activated Cl- channels in primary cultures of spiny dogfish (Squalus acanthias) rectal gland

1995 ◽  
Vol 268 (1) ◽  
pp. C70-C79 ◽  
Author(s):  
D. C. Devor ◽  
J. N. Forrest ◽  
W. K. Suggs ◽  
R. A. Frizzell
Keyword(s):  
Single Channel ◽  
Primary Cultures ◽  
Squalus Acanthias ◽  
Rectal Gland ◽  
Spiny Dogfish ◽  
Open Probability ◽  
Whole Cell ◽  
Cyclic Monophosphate ◽  
Cl Channels ◽  
Inside Out

Whole cell and single-channel patch-clamp techniques were used to identify and characterize the Cl- currents responsible for adenosine 3',5'-cyclic monophosphate (cAMP)-mediated Cl- secretion in the rectal gland of the spiny dogfish (Squalus acanthias). During whole cell recordings, in cultured rectal gland cells forskolin (10 microM) and 8-(4-chlorophenylthio)adenosine 3',5'-cyclic monophosphate (400 microM) stimulated a 28-fold increase in Cl- conductance (n = 10). This cAMP-activated conductance pathway had a linear current-voltage (I-V) relationship that was time and voltage independent. Substitution of 235 meq Cl- with I- in the bath inhibited the cAMP-activated current at both positive and negative voltages (64%). Glibenclamide (60 microM) abolished the cAMP-stimulated current, and its effect was irreversible (n = 3). During cell-attached recording, increased cellular cAMP activated single Cl- channels in nine previously quiet patches. These channels had a linear I-V relationship with an average single-channel conductance of 5.1 +/- 0.2 pS (n = 6). Similar properties were observed in excised inside-out patches, permitting further characterization of the single-channel properties. Excised quiescent patches could be activated by the addition of ATP and protein kinase A. Replacing bath Cl- with I- inhibited both inward and outward currents (n = 3). In three inside-out patches, glibenclamide (300 microM) reversibly reduced open probability by 74%, with no effect on single-channel current amplitude. Similar results were obtained in four outside-out recordings. These results suggest that increased cellular cAMP in dogfish rectal gland activates a small linear Cl- channel that resembles human cystic fibrosis transmembrane conductance regulator in its biophysical and pharmacological properties.

scholarly journals Sugar uptake, metabolism, and chloride secretion in the rectal gland of the spiny dogfish Squalus acanthias

2020 ◽  
Vol 319 (1) ◽  
pp. R96-R105
Author(s):  
Rolf Kinne ◽  
Katherine C. Spokes ◽  
Patricio Silva
Keyword(s):  
Glycogen Phosphorylase ◽  
Chloride Secretion ◽  
Squalus Acanthias ◽  
Rectal Gland ◽  
Sugar Uptake ◽  
Spiny Dogfish ◽  
Gland Cells ◽  
Exogenous Glucose ◽  
Glucose Transporter 2 ◽  
Rectal Glands

The rectal gland of the spiny dogfish Squalus acanthias secretes a salt solution isosmotic with plasma that maintains the salt homeostasis of the fish. It secretes salt against an electrochemical gradient that requires the expenditure of energy. Isolated rectal glands perfused without glucose secrete salt, albeit at a rate about 30% of glands perfused with 5 mM glucose. Gradually reducing the glucose concentration is associated with a progressive decrease in the secretion of chloride. The apparent Km for the exogenous glucose-dependent chloride secretion is around 2 mM. Phloretin and cytochalasin B, agents that inhibit facilitated glucose carriers of the solute carrier 2 (Slc2) family such as glucose transporter 2 (GLUT2), do not inhibit the secretion of chloride by the perfused rectal glands. Phloridzin, which inhibits Slc5 family of glucose symporters, or α-methyl-d-glucoside, which competitively inhibits the uptake of glucose through Slc5 symporters, inhibit the secretion of chloride. Thus the movement of glucose into the rectal gland cells appears to be mediated by a sodium-glucose symporter. Sodium-glucose cotransporter 1 (SGLT1), the first member of the Slc5 family of sodium-linked glucose symporters, was cloned from the rectal gland. No evidence of GLUT2 was found. The persistence of secretion of chloride in the absence of glucose in the perfusate suggests that there is an additional source of energy within the cells. The use of 2-mercapto-acetate did not result in any change in the secretion of chloride, suggesting that the oxidation of fatty acids is not the source of energy for the secretion of chloride. Perfusion of isolated glands with KCN in the absence of glucose further reduces the secretion of chloride but does not abolish it, again suggesting that there is another source of energy within the cells. Glucose was measured in the rectal gland cells and found to be at concentrations in the range of that in the perfusate. Glycogen measurements indicated that there are significant stores of glucose in the rectal gland. Moreover, glycogen synthase was partially cloned from rectal gland cells. The open reading frame of glycogen phosphorylase was also cloned from rectal gland cells. Measurements of glycogen phosphorylase showed that the enzyme is mostly in its active form in the cells. The cells of the rectal gland of the spiny dogfish require exogenous glucose to fully support the active secretion of salt. They have the means to transport glucose into the cells in the form of SGLT1. The cells also have an endogenous supply of glucose as glycogen and have the necessary elements to synthesize, store, and hydrolyze it.

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