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Flow of energy in the outer retina in darkness and in light

Linton, Jonathan D.; Holzhausen, Lars C.; Babai, Norbert; Song, Hongman; Miyagishima, Kiyoharu J.; Stearns, George W.; Lindsay, Ken; Wei, Junhua; Chertov, Andrei O. and Peters, Theo A., et al. (2010) In Proceedings of the National Academy of Sciences 107(19). p.8599-8604
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... (More)
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. (Less)
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publication status
published
subject
keywords
energy metabolism, phototransduction
in
Proceedings of the National Academy of Sciences
volume
107
issue
19
pages
8599 - 8604
publisher
National Acad Sciences
external identifiers
  • wos:000277591200021
  • scopus:77952716016
ISSN
1091-6490
DOI
10.1073/pnas.1002471107
language
English
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yes
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7b81c2eb-729f-418e-9993-7dd29da1337f (old id 1617703)
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http://www.ncbi.nlm.nih.gov/pubmed/20445106
date added to LUP
2010-06-21 13:16:24
date last changed
2018-06-03 03:28:20
@article{7b81c2eb-729f-418e-9993-7dd29da1337f,
  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.},
  author       = {Linton, Jonathan D. and Holzhausen, Lars C. and Babai, Norbert and Song, Hongman and Miyagishima, Kiyoharu J. and Stearns, George W. and Lindsay, Ken and Wei, Junhua and Chertov, Andrei O. and Peters, Theo A. and Caffé, Romeo and Pluk, Helma and Seeliger, Mathias W. and Tanimoto, Naoyuki and Fong, Kimberly and Bolton, Laura and Kuok, Denise L. T. and Sweet, Ian R. and Bartoletti, Theodore M. and Radu, Roxana A. and Travis, Gabriel H. and Zagotta, Willam N. and Townes-Anderson, Ellen and Parker, Ed and Van der Zee, Catharina E. E. M. and Sampath, Alapakkam P. and Sokolov, Maxim and Thoreson, Wallace B. and Hurley, James B.},
  issn         = {1091-6490},
  keyword      = {energy metabolism,phototransduction},
  language     = {eng},
  number       = {19},
  pages        = {8599--8604},
  publisher    = {National Acad Sciences},
  series       = {Proceedings of the National Academy of Sciences},
  title        = {Flow of energy in the outer retina in darkness and in light},
  url          = {http://dx.doi.org/10.1073/pnas.1002471107},
  volume       = {107},
  year         = {2010},
}