Plasma levels of glucose, alanine, lactate, and β-hydroxybutyrate in the unfed spiny dogfish shark (Squalus acanthias) after surgery and following mammalian insulin infusion

deRoos, Roger; deRoos, Carolyn C.; Werner, Carole S.; Werner, Harold V.

doi:10.1016/0016-6480(85)90133-9

Cited by 43 publications

(12 citation statements)

References 38 publications

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“…A similar decrease in blood glucose was shown when dogfish were exposed to exogenous insulin (deRoos et al, 1985). It would be interesting to determine if feeding release of insulin is responsible for this decrease in plasma glucose.…”

Section: Discussionsupporting

confidence: 54%

“…In addition, several observations suggest that both circulating glucose and ketone body concentrations are dynamic and can span a large range, depending upon feeding, season, exercise, etc (e.g. Patent, 1973;Zammit and Newsholme, 1979;deRoos et al, 1985;Gutierrez et al, 1988;deRoos and deRoos, 1992;Richards et al, 2003). It is especially the event of feeding, and the large NaCl load that it generates which must be excreted, that is thought to activate the gland through hormonal, acid-base, and other cues (MacKenzie et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

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Metabolic organization and effects of feeding on enzyme activities of the dogfish shark (Squalus acanthias) rectal gland

Walsh

Kajimura

Mommsen

et al. 2006

Journal of Experimental Biology

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SUMMARY In order to investigate the metabolic poise of the elasmobranch rectal gland, we conducted two lines of experimentation. First, we examined the effects of feeding on plasma metabolites and enzyme activities from several metabolic pathways in several tissues of the dogfish shark, Squalus acanthias, after starvation and at 6, 20, 30 and 48 h post-feeding. We found a rapid and sustained ten-fold decrease in plasma β-hydroxybutyrate at 6 h and beyond compared with starved dogfish, suggesting an upregulation in the use of this substrate, a decrease in production, or both. Plasma acetoacetate levels remain unchanged, whereas there was a slight and transient decrease in plasma glucose levels at 6 h. Several enzymes showed a large increase in activity post-feeding, including β-hydroxybutyrate dehydrogenase in rectal gland and liver, and in rectal gland, isocitrate dehydrogenase, citrate synthase, lactate dehydrogenase, aspartate amino transferase, alanine amino transferase, glutamine synthetase and Na+/K+ ATPase. Also notable in these enzyme measurements was the overall high level of activity in the rectal gland in general. For example, activity of the Krebs' TCA cycle enzyme citrate synthase (over 30 U g-1) was similar to activities in muscle from other species of highly active fish. Surprisingly, lactate dehydrogenase activity in the gland was also high (over 150 U g-1), suggesting either an ability to produce lactate anaerobically or use lactate as an aerobic fuel. Given these interesting observations, in the second aspect of the study we examined the ability of several metabolic substrates (alone and in combination) to support chloride secretion by the rectal gland. Among the substrates tested at physiological concentrations (glucose, β-hydroxybutyrate, lactate,alanine, acetoacetate, and glutamate), only glucose could consistently maintain a viable preparation. Whereas β-hydroxybutyrate could enhance gland activity when presented in combination with glucose, surprisingly it could not sustain chloride secretion when used as a lone substrate. Our results are discussed in the context of the in vivo role of the gland and mechanisms of possible upregulation of enzyme activities.

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Section: Discussionsupporting

confidence: 54%

Section: Introductionmentioning

confidence: 99%

Metabolic organization and effects of feeding on enzyme activities of the dogfish shark (Squalus acanthias) rectal gland

Walsh

Kajimura

Mommsen

et al. 2006

Journal of Experimental Biology

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“…Although little is known about many aspects of glucose metabolism in radial glial cells, it is possible that these cells store glycogen, a molecule that is metabolized upon neuronal activation [62], [63]. Furthermore, the expression of enzymes related to the glycogen metabolism has been found in the brain of rays [47], [64], [65].…”

Section: Discussionmentioning

confidence: 99%

“…Studies of shark brain suggest that it metabolizes ketone bodies [64]. Prior to the present study, MCT expression in the brain had not been analyzed in non-mammalian vertebrates.…”

Section: Discussionmentioning

confidence: 99%

“…However, efflux of lactate from the brain has been reported under starvation conditions [64], suggesting that radial glia may generate important concentrations of lactate that can reach the neuron or be eliminated by the blood [64]. MCT2 is a high-affinity transporter involved in the influx of lactate through the cellular membrane whose expression has been described in mammalian neurons [36], [37].…”

Section: Discussionmentioning

confidence: 99%

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Glucose Transporter 1 and Monocarboxylate Transporters 1, 2, and 4 Localization within the Glial Cells of Shark Blood-Brain-Barriers

et al. 2012

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Although previous studies showed that glucose is used to support the metabolic activity of the cartilaginous fish brain, the distribution and expression levels of glucose transporter (GLUT) isoforms remained undetermined. Optic/ultrastructural immunohistochemistry approaches were used to determine the expression of GLUT1 in the glial blood-brain barrier (gBBB). GLUT1 was observed solely in glial cells; it was primarily located in end-feet processes of the gBBB. Western blot analysis showed a protein with a molecular mass of 50 kDa, and partial sequencing confirmed GLUT1 identity. Similar approaches were used to demonstrate increased GLUT1 polarization to both apical and basolateral membranes in choroid plexus epithelial cells. To explore monocarboxylate transporter (MCT) involvement in shark brain metabolism, the expression of MCTs was analyzed. MCT1, 2 and 4 were expressed in endothelial cells; however, only MCT1 and MCT4 were present in glial cells. In neurons, MCT2 was localized at the cell membrane whereas MCT1 was detected within mitochondria. Previous studies demonstrated that hypoxia modified GLUT and MCT expression in mammalian brain cells, which was mediated by the transcription factor, hypoxia inducible factor-1. Similarly, we observed that hypoxia modified MCT1 cellular distribution and MCT4 expression in shark telencephalic area and brain stem, confirming the role of these transporters in hypoxia adaptation. Finally, using three-dimensional ultrastructural microscopy, the interaction between glial end-feet and leaky blood vessels of shark brain was assessed in the present study. These data suggested that the brains of shark may take up glucose from blood using a different mechanism than that used by mammalian brains, which may induce astrocyte-neuron lactate shuttling and metabolic coupling as observed in mammalian brain. Our data suggested that the structural conditions and expression patterns of GLUT1, MCT1, MCT2 and MCT4 in shark brain may establish the molecular foundation of metabolic coupling between glia and neurons.

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Hypoxia tolerance in the epaulette shark (Hemiscyllium ocellatum)

1998

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The epaulette shark, Hemiscyllium ocellatum, is a tropical reef shark that can live in an environment with cyclic periods of low oxygen concentration, suggesting that it has a well-developed capacity for anaerobic metabolism. Most investigations of hypoxia-tolerant teleosts and reptiles have focused on species that inhabit cold environments. This study was carried out on a tropical reef shark in order to determine whether similar strategies for hypoxia survival are used at higher environmental temperatures. We studied the effects of a single exposure to mild hypoxia and cyclic exposure to extreme hypoxia on blood-lactate concentration and key indicators of neurological function. The basal blood-lactate concentration for the epaulette shark was determined as 0.37 mM and showed a graded increase during hypoxia. After a single exposure to mild hypoxia (20% of normoxia for 4 h), the mean blood-lactate level rose to 3.07 mM (P < 0.01). After cyclic exposure to extreme hypoxia (eight repetitions of a 120-min exposure at 5% of normoxia), there was a rise in mean blood-lactate concentration to 5.43 mM (P < 0.0001). During both hypoxic regimens, there were no observed changes in key indicators of neurological function. We conclude that the epaulette shark is tolerant to both mild hypoxia and to cyclic exposure to extreme hypoxia.

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Plasma levels of glucose, alanine, lactate, and β-hydroxybutyrate in the unfed spiny dogfish shark (Squalus acanthias) after surgery and following mammalian insulin infusion

Cited by 43 publications

References 38 publications

Metabolic organization and effects of feeding on enzyme activities of the dogfish shark (Squalus acanthias) rectal gland

Metabolic organization and effects of feeding on enzyme activities of the dogfish shark (Squalus acanthias) rectal gland

Glucose Transporter 1 and Monocarboxylate Transporters 1, 2, and 4 Localization within the Glial Cells of Shark Blood-Brain-Barriers

Hypoxia tolerance in the epaulette shark (Hemiscyllium ocellatum)

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