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

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 Caffe, Helma Pluk, Mathias W. Seeliger, Naoyuki Tanimoto, Kimberly Fong, Laura Bolton, Denise L T Kuok, Ian R. Sweet, Theodore M. Bartoletti, Roxana A. Radu & 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

Research output: Contribution to journalArticle

66 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)8599-8604
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume107
Issue number19
DOIs
StatePublished - May 11 2010

Fingerprint

Darkness
Retina
Mitochondria
Light
Presynaptic Terminals
Creatine Kinase
Neurons
Synaptic Transmission
Phosphocreatine
Tissue Distribution
Adenosine Triphosphate

Keywords

  • Energy metabolism
  • Phototransduction

ASJC Scopus subject areas

  • General

Cite this

Linton, J. D., Holzhausen, L. C., Babai, N., Song, H., Miyagishima, K. J., Stearns, G. W., ... Hurley, J. B. (2010). Flow of energy in the outer retina in darkness and in light. Proceedings of the National Academy of Sciences of the United States of America, 107(19), 8599-8604. https://doi.org/10.1073/pnas.1002471107

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.; Peters, Theo A.; Caffe, Romeo; Pluk, Helma; Seeliger, Mathias W.; Tanimoto, Naoyuki; Fong, Kimberly; Bolton, Laura; Kuok, Denise L T; Sweet, Ian R.; Bartoletti, Theodore M.; Radu, Roxana A.; Travis, Gabriel H.; Zagotta, Willam N.; Townes-Anderson, Ellen; Parker, Ed; Van Der Zee, Catharina E E M; Sampath, Alapakkam P.; Sokolov, Maxim; Thoreson, Wallace B; Hurley, James B.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 107, No. 19, 11.05.2010, p. 8599-8604.

Research output: Contribution to journalArticle

Linton, JD, Holzhausen, LC, Babai, N, Song, H, Miyagishima, KJ, Stearns, GW, Lindsay, K, Wei, J, Chertov, AO, Peters, TA, Caffe, R, Pluk, H, Seeliger, MW, Tanimoto, N, Fong, K, Bolton, L, Kuok, DLT, Sweet, IR, Bartoletti, TM, Radu, RA, Travis, GH, Zagotta, WN, Townes-Anderson, E, Parker, E, Van Der Zee, CEEM, Sampath, AP, Sokolov, M, Thoreson, WB & Hurley, JB 2010, 'Flow of energy in the outer retina in darkness and in light', Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 19, pp. 8599-8604. https://doi.org/10.1073/pnas.1002471107
Linton, Jonathan D. ; Holzhausen, Lars C. ; Babai, Norbert ; Song, Hongman ; Miyagishima, Kiyoharu J. ; Stearns, George W. ; Lindsay, Ken ; Wei, Junhua ; Chertov, Andrei O. ; Peters, Theo A. ; Caffe, Romeo ; Pluk, Helma ; Seeliger, Mathias W. ; Tanimoto, Naoyuki ; Fong, Kimberly ; Bolton, Laura ; Kuok, Denise L T ; Sweet, Ian R. ; Bartoletti, Theodore M. ; Radu, Roxana A. ; Travis, Gabriel H. ; Zagotta, Willam N. ; Townes-Anderson, Ellen ; Parker, Ed ; Van Der Zee, Catharina E E M ; Sampath, Alapakkam P. ; Sokolov, Maxim ; Thoreson, Wallace B ; Hurley, James B. / Flow of energy in the outer retina in darkness and in light. In: Proceedings of the National Academy of Sciences of the United States of America. 2010 ; Vol. 107, No. 19. pp. 8599-8604.
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AU - Townes-Anderson, Ellen

AU - Parker, Ed

AU - Van Der Zee, Catharina E E M

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