Abstract
Structural features of neurons create challenges for effective production and distribution of essential metabolic energy. We investigated how metabolic energy is distributed between cellular compartments in photoreceptors. In avascular retinas, aerobic production of energy occurs only in mitochondria that are located centrally within the photoreceptor. Our findings indicate that metabolic energy flows from these central mitochondria as phosphocreatine toward the photoreceptor's synaptic terminal in darkness. In light, it flows in the opposite direction as ATP toward the outer segment. Consistent with this model, inhibition of creatine kinase in avascular retinas blocks synaptic transmission without influencing outer segment activity. Our findings also reveal how vascularization of neuronal tissue can influence the strategies neurons use for energy management. In vascularized retinas, mitochondria in the synaptic terminals of photoreceptors make neurotransmission less dependent on creatine kinase. Thus, vasculature of the tissue and the intracellular distribution of mitochondria can play key roles in setting the strategy for energy distribution in neurons.
Publication types
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Research Support, N.I.H., Extramural
MeSH terms
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Animals
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Creatine Kinase / antagonists & inhibitors
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Creatine Kinase / metabolism
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Darkness*
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Dinitrofluorobenzene / pharmacology
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Electroretinography
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Energy Metabolism / drug effects
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Energy Metabolism / physiology*
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Energy Metabolism / radiation effects
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Glutamates / metabolism
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Mice
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Mitochondria / drug effects
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Mitochondria / enzymology
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Mitochondria / radiation effects
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Models, Biological
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Presynaptic Terminals / drug effects
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Presynaptic Terminals / enzymology
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Presynaptic Terminals / radiation effects
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Protein Kinase Inhibitors / pharmacology
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Retina / drug effects
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Retina / enzymology
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Retina / physiology*
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Retina / radiation effects
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Retinal Cone Photoreceptor Cells / cytology
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Retinal Cone Photoreceptor Cells / drug effects
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Retinal Cone Photoreceptor Cells / enzymology
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Retinal Cone Photoreceptor Cells / radiation effects
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Retinal Photoreceptor Cell Outer Segment / drug effects
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Retinal Photoreceptor Cell Outer Segment / metabolism
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Retinal Photoreceptor Cell Outer Segment / radiation effects
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Retinal Vessels / drug effects
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Retinal Vessels / enzymology
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Retinal Vessels / radiation effects
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Synaptic Transmission / drug effects
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Synaptic Transmission / radiation effects
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Urodela / physiology
Substances
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Glutamates
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Protein Kinase Inhibitors
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Dinitrofluorobenzene
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Creatine Kinase