The impact of hypoxia on in vivo glucose uptake in a hypoglycemic fish,Myoxocephalus scorpius

Abstract

The mechanisms controlling carbohydrate utilization in teleost fish are poorly understood, particularly in the heart. Tissue glucose uptake and cardiovascular characteristics were measured in the short-horned sculpin, Myoxocephalus scorpius, a species exhibiting low blood glucose levels, during normoxia and hypoxia to assess the role of adenosine receptors in the control of glucose uptake and anaerobic metabolism. As expected, hypoxia exposure (300 min at 2 mg/l dissolved oxygen) resulted in a bradycardia and plasma lactate accumulation, but glucose uptake rates did not change in heart, brain, gill, spleen, and white muscle. Plasma glucose-to-intracellular glucose ratios indicated that glucose uptake was the rate-limiting step in glucose utilization. The majority of intracellular glucose was unphosphorylated, however, suggesting that hexokinase is also important in controlling the tissue glucose gradient. During hypoxia, the cholinergic blocker atropine resulted in tachycardia but did not significantly change tissue glucose uptake rates or heart and brain adenosine levels. In contrast, the combined treatment of atropine and an adenosine receptor blocker [8-(p-sulfophenyl)theophylline] during hypoxia increased heart glucose uptake to levels fivefold higher than normoxic fish, with no additive effects on cardiovascular parameters. Significant tissue lactate accumulation was observed in this group of fish, signifying that adenosine receptors may depress anaerobic metabolism, even though tissue adenosine accumulation was absent during hypoxia. White muscle accumulated glucose during normoxia, suggesting the presence of gluconeogenic pathways or active uptake mechanisms not previously described in this tissue.

Glucose uptake and metabolism by RBCs from fish with different extracellular glucose levels

“…Most notable is the low glucose level in blood of short-horned sculpin, as previously reported (e.g. MacCormack and Driedzic, 2007). Extracellular glucose sets the upper limit to the diffusion gradient necessary for glucose entry into cells.…”

Extracellular glucose can fuel metabolism in RBCs from high glycemic Atlantic cod (Gadus morhua) but not low glycemic short-horned sculpin (Myoxocephalus scorpius)

“…The difference in metabolism between Atlantic cod and shorthorned sculpin RBCs is most likely to be due to the plasma level of glucose. Low glucose levels have been noted previously for shorthorned sculpin and do not increase above 1 mmol l −1 even under hypoxia (MacCormack and Driedzic, 2007;Driedzic et al, 2013). Glucose metabolism, by isolated RBCS from Atlantic cod and shorthorned sculpin, determined by the radiometric method used here, rises sharply up to 1 mmol l −1 glucose and essentially achieves maximal rates at this concentration (Driedzic et al, 2013).…”

Extracellular glucose supports lactate production but not aerobic metabolism in cardiomyocytes from both normoglycemic Atlantic cod (Gadus morhua) and low glycemic short-horned sculpin (Myoxocephalus scorpius)

“…experiments 3 and 4), the level of extracellular glucose for Atlantic cod myocytes was set to 5 mmol l −1 and for short-horned sculpin myocytes to either 1 mmol l −1 (experiment 1) or 0.5 mmol l −1 (experiments 3 and 4). The concentrations used in these studies were based on anticipated levels from earlier experiments involving fish from the same populations (MacCormack and Driedzic, 2007;Hall et al, 2009;Driedzic et al, 2013Driedzic et al, , 2014). Although the mean glucose level of plasma for the Atlantic cod sampled here was lower than 5 mmol l −1 , four of the 29 specimens had plasma glucose levels of 5 mmol l −1 or higher; as such, the experimentally controlled concentration was within the physiological range.…”