The effect of light on glycogen turnover in the retina of the intact honeybee drone (Apis mellifera)

Evêquoz, V.; Stadelmann, Andreas M.; Tsacopoulos, M.

doi:10.1007/bf00605289

Cited by 23 publications

(17 citation statements)

References 23 publications

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“…The demonstration that the compound at 23 min was dGlc was provided as follows: the fractions corresponding to the peak were collected, frozen, and lyophilized; the residue was dissolved in water and mixed with a solution containing ATP and hexokinase for 15 min and analyzed again by HPLC. This time the peak appeared at an elution time of 17 min, corresponding to dGlc 6-P. When the retina was incubated with Ringer solution containing [3H]-dGlc (3 1LM) plus 30 mM unlabeled D-glucose, the ratio of 3H in dGlc 6-P to that in dGlc changed to 3:2.5 (average from 4 slices).…”

Section: Resultsmentioning

confidence: 97%

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Honeybee retinal glial cells transform glucose and supply the neurons with metabolic substrate.

Tsacopoulos

Evêquoz-Mercier

Perrottet

et al. 1988

Proc. Natl. Acad. Sci. U.S.A.

100

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The retina of the honeybee drone is a nervous tissue in which glial cells and photoreceptor cells (sensory neurons) constitute two distinct metabolic compartments. Retinal slices incubated with 2-deoxy[3lHjglucose convert this glucose analogue to 2-deoxy[3H~glucose 6-phosphate, but this conversion is made only in the glial cells. Hence, glycolysis occurs only in glial cells. In contrast, the neurons consume 02 and this consumption is sustained by the hydrolysis of glycogen, which is contained in large amounts in the glia. During photostimulation the increased oxidative metabolism of the neurons is sustained by a higher supply of carbohydrates from the glia. This clear case of metabolic interaction between neurons and glial cells supports Golgi's original hypothesis, proposed nearly 100 years ago, about the nutritive function of glial cells in the nervous system. The hypothesis that one ofthe functions of glia in the nervous system is to transfer nutrients from the capillary blood to neurons was proposed by Golgi nearly a century ago (1, 2). This hypothesis seemed reasonable based upon histological evidence, but direct experimental support has so far been either meager or even negative (3). A question, often appearing in textbooks but as yet not answered, that bears upon the truth of this hypothesis is whether glycogenolysis in the glia serves to nourish the neurons. The question arises because histological observations show that in many nervous systems glial cells contain much more glycogen than neurons do (4-6). In the mammalian brain the glycogen is labile and it can be almost depleted by, for example, 1 min of ischemia (7) or hypoxia (8). Hence, it is known that carbohydrate stored as glycogen can be mobilized, but it is not known whether it is transferred from glia to neurons rather than being consumed by the glia themselves (9).We have examined the nutritive role of glial cells in a comparatively simple nervous tissue, the retina of the honeybee (Apis mellifera) drone. In this preparation the separation of metabolic functions between the glial cells and photoreceptor cells (sensory neurons) is exceptionally complete. The photoreceptors contain large numbers of mitochondria and very little glycogen. In contrast, the glial cells contain very few mitochondria, but large quantities of glycogen ,3 particles (10-12). Photoreceptor energy metabolism is obligatorily aerobic, since anoxia and the mitochondrial inhibitor amobarbital rapidly abolish light-induced electrical activity in the drone retina (11,13 MATERIALS AND METHODS Preparation of Slices and Uptake of Labeled Hexoses.Retinal slices (-250 ,um thick) were prepared by making two parallel cuts with a vibrating razor blade, parallel to the ommatidia in the dorsal region of the retina, as described elsewhere (12). When such a slice is exposed to Ringer solution oxygenated with 100% 02, the retina is well oxygenated throughout its full thickness (14). The Ringer solution normally contained 270 mM NaCl, 10 mM KCl, 10 mM MgCl2, 1.6 mM CaC12 and 10 mM t...

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Section: Resultsmentioning

confidence: 97%

“…The total radioactivity was measured in aliquots of homogenate by liquid scintillation counting. The label incorporated into glycogen was measured following a specific extraction (17).…”

mentioning

confidence: 99%

Honeybee retinal glial cells transform glucose and supply the neurons with metabolic substrate.

Tsacopoulos

Evêquoz-Mercier

Perrottet

et al. 1988

Proc. Natl. Acad. Sci. U.S.A.

100

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“…2007). (iii) Glycogenolysis occurs in retina of the intact honeybee during light stimulation (Evêquoz et al. 1983), chick brain during early memory consolidation (Hertz et al.…”

Section: Discussionmentioning

confidence: 99%

A glycogen phosphorylase inhibitor selectively enhances local rates of glucose utilization in brain during sensory stimulation of conscious rats: implications for glycogen turnover

Dienel

Ball

Cruz

2007

Journal of Neurochemistry

117

147

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Glycogen is degraded during brain activation but its role and contribution to functional energetics in normal activated brain have not been established. In the present study, glycogen utilization in brain of normal conscious rats during sensory stimulation was assessed by three approaches, change in concentration, release of 14 C from pre-labeled glycogen and compensatory increase in utilization of blood glucose (CMR glc ) evoked by treatment with a glycogen phosphorylase inhibitor. Glycogen level fell in cortex, 14 C release increased in three structures and inhibitor treatment caused regionally selective compensatory increases in CMR glc over and above the activation-induced rise in vehicle-treated rats. The compensatory rise in CMR glc was highest in sensory-parietal cortex where it corresponded to about half of the stimulus-induced rise in CMR glc in vehicle-treated rats; this response did not correlate with metabolic rate, stimulus-induced rise in CMR glc or sequential station in sensory pathway. Thus, glycogen is an active fuel for specific structures in normal activated brain, not simply an emergency fuel depot and flux-generated pyruvate greatly exceeded net accumulation of lactate or net consumption of glycogen during activation. The metabolic fate of glycogen is unknown, but adding glycogen to the fuel consumed during activation would contribute to a fall in CMR O2 / CMR glc ratio. Keywords: brain activation, brain imaging, energetics, glucose utilization, glycogenolysis, sensory stimulation. The importance of quantifying metabolic fluxes induced by brain activation at a cellular level is emphasized by positron emission tomographic, magnetic resonance spectroscopic (MRS) and optical (infrared or fluorescence) studies of brain function in health and disease that rely on measurement of signals generated from endogenous or exogenous tracers metabolized by energy-producing pathways. Astrocytes are increasingly recognized as having essential roles in both signaling and energetics during brain activation, including modulation of neurotransmission via gliotransmitters, synthesis and cycling of amino acid neurotransmitters, regulation of extracellular glutamate and K + levels and blood flow

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“…Glycogen content was measured using a slightly modified version (see Evequoz et al, 1983) of the fluorometric micromethod described by Nahorski and Rogers (1972).…”

Section: Biochemical Measurementsmentioning

confidence: 99%

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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The effect of light on glycogen turnover in the retina of the intact honeybee drone (Apis mellifera)

Cited by 23 publications

References 23 publications

Honeybee retinal glial cells transform glucose and supply the neurons with metabolic substrate.

Honeybee retinal glial cells transform glucose and supply the neurons with metabolic substrate.

A glycogen phosphorylase inhibitor selectively enhances local rates of glucose utilization in brain during sensory stimulation of conscious rats: implications for glycogen turnover

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

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