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

Research output: Contribution to journalArticle

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.

Details

Authors
  • Jonathan D. Linton
  • Lars C. Holzhausen
  • Norbert Babai
  • Hongman Song
  • Kiyoharu J. Miyagishima
  • George W. Stearns
  • Ken Lindsay
  • Junhua Wei
  • Andrei O. Chertov
  • Theo A. Peters
  • Romeo Caffé
  • Helma Pluk
  • Mathias W. Seeliger
  • Naoyuki Tanimoto
  • Kimberly Fong
  • Laura Bolton
  • Denise L. T. Kuok
  • Ian R. Sweet
  • Theodore M. Bartoletti
  • Roxana A. Radu
  • And 9 others
  • Gabriel H. Travis
  • Willam N. Zagotta
  • Ellen Townes-Anderson
  • Ed Parker
  • Catharina E. E. M. Van der Zee
  • Alapakkam P. Sampath
  • Maxim Sokolov
  • Wallace B. Thoreson
  • James B. Hurley
Organisations
Research areas and keywords

Subject classification (UKÄ) – MANDATORY

  • Ophthalmology

Keywords

  • energy metabolism, phototransduction
Original languageEnglish
Pages (from-to)8599-8604
JournalProceedings of the National Academy of Sciences
Volume107
Issue number19
Publication statusPublished - 2010
Publication categoryResearch
Peer-reviewedYes