Organ-specific control of glycolysis in anoxic turtles

Abstract

Control of glycolysis during anoxia was investigated in five organs (heart, brain, liver, and red and white skeletal muscles) of the freshwater turtle, Pseudemys scripta, after 1 or 5 h of submergence in N2-bubbled water. Lactate was produced as the metabolic end product, with distinct organ differences in the amount (net lactate accumulation was 2.4-fold higher in brain than white muscle) and rate (lactate production in liver dropped 16-fold after the 1st h) of lactate accumulation. ATP and total adenylate contents of all organs were reduced (by 15-32%) after 1 h of submergence, but energy charge was maintained; after 5 h, adenylate contents had fully recovered. Changes in the levels of hexose and triose phosphate intermediates of glycolysis indicated an activation of glycolysis within the 1st h of anoxia exposure in brain, heart, and skeletal muscles. By 5 h, however, these were reversed, and a glycolytic rate depression was indicated, consistent with the overall metabolic rate depression accompanying long-term anaerobiosis in the turtle. Crossover analysis indicated glycolytic control at the pyruvate kinase reaction in all organs during both glycolytic activation and metabolic depression; regulatory control at the phosphofructokinase locus was primarily important only during glycolytic activation in heart and red muscle. The same analysis indicated a very rapid glycolytic inhibition in liver occurring within the 1st h of anoxia exposure; this allows glycogenolysis to be directed toward glucose export yielding the fermentative fuel used by other organs during anoxia.

Calorespirometry reveals that goldfish prioritize aerobic metabolism over metabolic rate depression in all but near-anoxic environments

“…Elevated levels of lactate and ethanol at Pw O2 ≤1.3 kPa at 1 and 4 h indicate that anaerobic glycolysis also contributed to maintaining MR, though in slightly different ways in anoxia and hypoxia. In anoxia, lactate and ethanol levels continued to increase throughout the 4 h exposure, but their rate of accumulation decreased from 5.81 µmol h −1 g −1 during the first hour to 1.73 µmol h −1 g −1 during the subsequent 3 h. These results are consistent with those observed in tissues from anoxia-exposed turtles (Trachemys scripta elegans), where lactate production rates were elevated during the first hour of anoxia exposure and subsequently decreased between 1 and 5 h anoxia in brain, liver and white muscle (Kelly and Storey, 1988). Combined, these results suggest that there is an initial reliance on anaerobic metabolism upon anoxia exposure that may compensate for the anoxia-induced limitations on aerobic ATP production while MRD is initiated.…”

Endothelial cell tolerance to hypoxia. Potential role of purine nucleotide phosphates.

“…Under these conditions, declining demands for ATP would be so closely matched by ATP synthesis rates that the two processes would stabilize cell nucleotide concentrations. In fact, coupling of energy demand to supply is a highly adaptable characteristic and has been demonstrated in several species (30)(31)(32). Whether the capacity for, and the degree of, this adaptation (metabolic arrest) is similar in all tissues is, as yet, unclear.…”

“…Whether the capacity for, and the degree of, this adaptation (metabolic arrest) is similar in all tissues is, as yet, unclear. Nevertheless, it is considered by some investigators to be the critical mechanism allowing survival without oxygen (29,30,32). Whether similar mechanisms for preservation of guanine nucleotide phosphates exist and/or whether maintenance of these nucleotide concentrations is important in hypoxia-tolerant tissues or cells has not been determined.…”

Adenosine, a “Retaliatory” Metabolite, Promotes Anoxia Tolerance in Turtle Brain

“…In erythrocytes, adeno sine increased the glycolytic rate (Pasteur effect) (Gutierrez-Juarez et aI., 1992). These results sug gest a role of adenosine in the anoxia tolerance of turtle brain (Nilsson and Lutz, 1992) since anoxia induced an increased blood flow (Davies, 1990) and glycolytic rate (Kelly and Storey, 1988; Perez Pinzon et aI., 199 1).…”