TY - JOUR
T1 - Flow of energy in the outer retina in darkness and in light
AU - Linton, Jonathan D.
AU - Holzhausen, Lars C.
AU - Babai, Norbert
AU - Song, Hongman
AU - Miyagishima, Kiyoharu J.
AU - Stearns, George W.
AU - Lindsay, Ken
AU - Wei, Junhua
AU - Chertov, Andrei O.
AU - Peters, Theo A.
AU - Caffe, Romeo
AU - Pluk, Helma
AU - Seeliger, Mathias W.
AU - Tanimoto, Naoyuki
AU - Fong, Kimberly
AU - Bolton, Laura
AU - Kuok, Denise L.T.
AU - Sweet, Ian R.
AU - Bartoletti, Theodore M.
AU - Radu, Roxana A.
AU - Travis, Gabriel H.
AU - Zagotta, Willam N.
AU - Townes-Anderson, Ellen
AU - Parker, Ed
AU - Van Der Zee, Catharina E.E.M.
AU - Sampath, Alapakkam P.
AU - Sokolov, Maxim
AU - Thoreson, Wallace B.
AU - Hurley, James B.
PY - 2010/5/11
Y1 - 2010/5/11
N2 - 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.
AB - 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.
KW - Energy metabolism
KW - Phototransduction
UR - http://www.scopus.com/inward/record.url?scp=77952716016&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=77952716016&partnerID=8YFLogxK
U2 - 10.1073/pnas.1002471107
DO - 10.1073/pnas.1002471107
M3 - Article
C2 - 20445106
AN - SCOPUS:77952716016
SN - 0027-8424
VL - 107
SP - 8599
EP - 8604
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 19
ER -