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

Abstract

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...

Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization.

“…This cytoarchitectural arrangement implies that astrocytes form the first cellular barrier that glucose entering the brain parenchyma encounters, and it makes them a likely site of prevalent glucose uptake. In this context, it is interesting to consider the results obtained by Tsacopoulos and colleagues (26) (26). An increase in 02 consumption is nonetheless measured in photoreceptors.…”

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

“…The following experimen tal results showed that honeybee photoreceptors do not use glucose as a substrate: first, retinal slices were ex posed to 3H-2-deoxyglucose (3H-2DG) for 60 min and then thoroughly washed, freeze-dried, embedded and sectioned. Labeling corresponding to 3H-2DG-6P was exclusively in the glial cells [29], Second, addition to the superfusate of 10 mATDG has no detectable effect upon the oxygen consumption or the electrophysiology of the photoreceptors [28]: if photoreceptors did take up glu cose (and hence DG), then it is expected that 2DG would interfere with their energy metabolism.…”

“…1 of 27] but large quantities of glycogen particles [21,28], Also, only the glial cells stain with the periodic acid-Schiff reaction (PAS), which normally de tects glycogen [28], The simplicity and regularity of the structure of the retina is useful for cell identification and electrophysiological measurements. Thus in tissue sec tions studied by autoradiography, the characteristic rosette shape of the retinula can be discerned and used to distinguish neurons from glia [29].…”

Single type-2 astrocytes show multiple independent sites of Ca2+ signaling in response to histamine.

“…If so, these processes may be important for maintaining or regulating the activities of neurons. The processes may take up and metabolize neurotransmitters (33)(34)(35), regulate local ionic concentrations (36,37), or supply nutrients to neurons (38). It is noteworthy in this respect that the endfeet ofretinal glial cells are reported to have higher densities ofion channels that mediate potassium buffering than the cell bodies have (37).…”