Biochemistry of Insect Flight

Sacktor, Bertram

doi:10.1007/978-1-4899-3204-4_1

Cited by 13 publications

(8 citation statements)

References 180 publications

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“…8 and Dimitracos consumption (Brazitikos and Tsacopoulos,199 1). The bee retand Tsacopoulos, 1985) and therefore glycolysis in these cells ina, like the flight muscle (Sacktor, 1975) does not produce probably proceeds anaerobically, particularly during photostilactate (Fig. 1).…”

Section: Discussionmentioning

confidence: 97%

Glial cells transform glucose to alanine, which fuels the neurons in the honeybee retina

et al. 1994

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The retina of honeybee drone is a nervous tissue with a crystal-like structure in which glial cells and photoreceptor neurons constitute two distinct metabolic compartments. The phosphorylation of glucose and its subsequent incorporation into glycogen occur in glia, whereas O2 consumption (QO2) occurs in the photoreceptors. Experimental evidence showed that glia phosphorylate glucose and supply the photoreceptors with metabolic substrates. We aimed to identify these transferred substrates. Using ion-exchange and reversed-phase HPLC and gas chromatography-mass spectrometry, we demonstrated that more than 50% of 14C(U)-glucose entering the glia is transformed to alanine by transamination of pyruvate with glutamate. In the absence of extracellular glucose, glycogen is used to make alanine; thus, its pool size in isolated retinas is maintained stable or even increased. Our model proposes that the formation of alanine occurs in the glia, thereby maintaining the redox potential of this cell and contributing to NH3 homeostasis. Alanine is released into the extracellular space and is then transported into photoreceptors using an Na(+)-dependent transport system. Purified suspensions of photoreceptors have similar alanine aminotransferase activity as glial cells and transform 14C- alanine to glutamate, aspartate, and CO2. Therefore, the alanine entering photoreceptors is transaminated to pyruvate, which in turn enters the Krebs cycle. Proline also supplies the Krebs cycle by making glutamate and, in turn, the intermediate alpha-ketoglutarate. Light stimulation caused a 200% increase of QO2 and a 50% decrease of proline and of glutamate. Also, the production of 14CO2 from 14C-proline was increased. The use of these amino acids would sustain about half of the light-induced delta QO2, the other half being sustained by glycogen via alanine formation. The use of proline meets a necessary anaplerotic function in the Krebs cycle, but implies high NH3 production. The results showed that alanine formation fixes NH3 at a rate exceeding glutamine formation. This is consistent with the rise of a glial pool of alanine upon photostimulation. In conclusion, the results strongly support a nutritive function for glia.

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Section: Discussionmentioning

confidence: 97%

Glial cells transform glucose to alanine, which fuels the neurons in the honeybee retina

et al. 1994

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“…It is suggested that an increased cytosolic Ca2+ concentration, generated during the state of high work-load, activates pyruvate dehydrogenase, NAD-linked isocitrate dehydrogenase and 2-oxoglutarate dehydrogenase via enhanced mitochondrial Ca2+ uptake and an increased matrix Ca2+ concentration. At the same time, the mitochondrial glycerol 3-phosphate dehydrogenase, important in the oxidation of glycolytic reducing power in some muscles (for a review see Sacktor, 1975), is also activated by Ca2+ in the range pCa 6-8 (Hansford & Chappell, 1967), but faces the cytosol, rather than the mitochondrial matrix compartment (Klingenberg & Buchholz, 1970), and thus probably senses the pCa of the cytosol directly.…”

Section: Discussionmentioning

confidence: 99%

Effect of micromolar concentrations of free calcium ions on the reduction of heart mitochondrial NAD(P) by 2-oxoglutarate

Hansford¹,

Castro²

1981

Biochemical Journal

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1. The reduction of mitochondrial NAD(P) by 2-oxoglutarate was monitored as a measure of 2-oxoglutarate dehydrogenase activity in its intramitochondrial locale. In the absence of ADP, steady-state reduction of NAD(P) by 0.5 mM-2-oxoglutarate in the presence of 0.5 mM-L-malate was markedly increased by extramitochondrial Ca2+, with 50% activation at pCa 6.58, when the Na+ concentration was 10 mM, the Pi concentration ws 5 mM and the added Mg2+ concentration was 1 mM. Omission of Pi resulted in 50% activation at pCa 6.77; omission of Mg2+ resulted in 50% activation at pCA greater than or equal to 7.3. 2. The activation of 2-oxoglutarate dehydrogenase could be reversed on addition of an excess of EGTA. The rate of inactivation was dependent on the concentration of Na+, with K0.5 2.5 mM, which is consistent with the rate of withdrawal of Ca2+ from the mitochondria being the limiting factor. 3. The steady-state reduction of cytochrome c by 2-oxoglutarate (0.5 mM) also showed a marked dependence on pCa in the absence of ADP; in the presence of an excess of ADP, no such effect of Ca2+ was detectable. 4. Mitochondria from the hearts of senescent rats showed an undiminished rate of dehydrogenase activation by Ca2+ but a rate of inactivation by excess EGTA that was diminished by 40%. Direct studies of Ca2+ egress with Arsenazo III confirmed a decrement in rate with old age. 5. Studies of 2-oxoglutarate dehydrogenase activity as a function of the mitochondrial context of Ca2+, as measured by atomic-absorption spectrophotometry, showed half-maximal activation at a mitochondrial content of 1.0 nmol of Ca2+/mg of protein, and saturation at 3 nmol/mg. 6. These findings support the model advanced by Denton, Richards & Chin [(1978) Biochem. J. 176, 899-906], of a control of the tricarboxylate cycle by intramitochondrial Ca2+, and demonstrate the range of mitochondrial Ca2+ content over which this may occur. In addition, they raise the possibility of a disturbance of this control mechanism in old age.

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“…Glucose is predomi nantly phosphorylated to glucose-6P in the glial cells [29,34] in accordance with recent enzymatic measurements demonstrating predominant hexokinase activity in the cytosolic fraction of glial cells [32], Quantitative high pressure liquid chromatography (HPLC) and HPLC-MS showed that glucose-6P is subsequently incorporated into trehalose and glycogen [35], and is metabolized to pyruvate which in turn is transaminated to alanine [14]. This transamination occurs in the glial cells in order to sustain the redox potential and therefore a high glycolytic flux proceeding anaerobically in these cells and which increases during photostimulation [34], Indeed, the bee retina, like the flight muscle [36], does not produce lac tate [see fig. 1 in 14].…”

Section: Review Of Results Showing Transfer Of Substrates Of Energy Mmentioning

confidence: 99%

The Nutritive Function of Glia in a Crystal-Like Nervous Tissue: The Retina of the Honeybee Drone

Tsacopoulos

Veuthey²

1993

Dev Neurosci

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Among the variety of roles and diverse possible functions that have been attributed to glial cells, the nutritive function is strongly supported by direct experimental evidence obtained in a model of the honeybee drone retina. We have shown that in this nervous tissue, with crystal-like structure, in which glial cells and photoreceptor neurons constitute two distinct metabolic compartments, glial cells transform glucose to alanine and, with proline, fuel the mitochondria of the photoreceptors. Proline supplies the Krebs cycle by making glutamate. The use of proline implies high ammonia production. Pyruvate transamination in the glia fixes ammonia at a rate exceeding glutamine formation. We favor the hypothesis that ammonia rather than K⁺ is the metabolic signal trafficking between neuron and glial cells.

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Biochemistry of Insect Flight

Cited by 13 publications

References 180 publications

Glial cells transform glucose to alanine, which fuels the neurons in the honeybee retina

Glial cells transform glucose to alanine, which fuels the neurons in the honeybee retina

Effect of micromolar concentrations of free calcium ions on the reduction of heart mitochondrial NAD(P) by 2-oxoglutarate

The Nutritive Function of Glia in a Crystal-Like Nervous Tissue: The Retina of the Honeybee Drone

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