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A glia–neuron alanine/ammonium shuttle is central to energy metabolism in bee retina
Author(s) -
Coles Jonathan A.,
Martiel JeanLouis,
Laskowska Karolina
Publication year - 2008
Publication title -
the journal of physiology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.802
H-Index - 240
eISSN - 1469-7793
pISSN - 0022-3751
DOI - 10.1113/jphysiol.2007.148734
Subject(s) - glycogen , alanine , ammonium , metabolism , chemistry , biochemistry , neuron , medicine , biology , biophysics , endocrinology , neuroscience , amino acid , organic chemistry
It has been proposed that glial cells may supply carbon fuel to neurons and also that there are fluxes of ammonium from neurons to glia. We have investigated both these proposals in Apis retinal slices, in which virtually all the mitochondria are in the photoreceptor neurons. Normally the superfusate contained no substrate of energy metabolism; addition of glucose or alanine did not increase oxygen consumption , confirming that the neurons received adequate substrate from glycogen in the glia. 1,4‐Dideoxy‐1,4‐imino‐ d ‐arabinitol (DAB, 100 μ m ), an inhibitor of glycogen phosphorylase, progressively decreased . This decrease was reversed by alanine but not glucose. Ammonium‐sensitive microelectrodes did not detect significant extracellular [NH 4 + ] ([NH 4 + ] e ) in slices superfused with normal superfusate. Removal of Cl − , necessary for cotransport of NH 4 + into the glia, increased [NH 4 + ] e so that at the end of 2 min photostimulation mean [NH 4 + ] e was 0.442 m m ( s.e.m. = 0.082 m m , n = 16). In 0 Cl − , [NH 4 + ] e was reduced by 2‐(methylamino)isobutyrate (MeAIB) an inhibitor of alanine transport. MeAIB also blocked oxidation of alanine in the presence of DAB, but did not decrease in normal superfusate. Lactate ( l and d ) and pyruvate (but not glucose) increased in DAB and decreased [NH 4 + ] e in 0 Cl − . These results strengthen the evidence that in superfused retinal slices, glucose is metabolized exclusively in the glia, which supply alanine to the neurons, and that ammonium returns to the glia. They also show that another fuel (perhaps lactate) can be supplied by the glia to the neurons.