Literature DB >> 20445106

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

Jonathan D Linton1, 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, 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.   

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.

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Year:  2010        PMID: 20445106      PMCID: PMC2889335          DOI: 10.1073/pnas.1002471107

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  41 in total

1.  Light-induced changes in energy metabolites, guanine nucleotides, and guanylate cyclase within frog retinal layers.

Authors:  F A de Azeredo; W D Lust; J V Passonneau
Journal:  J Biol Chem       Date:  1981-03-25       Impact factor: 5.157

2.  Tissue- and cell-specific distribution of creatine kinase B: a new and highly specific monoclonal antibody for use in immunohistochemistry.

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Journal:  Cell Tissue Res       Date:  1995-05       Impact factor: 5.249

3.  Metabolite channeling: a phosphorylcreatine shuttle to mediate high energy phosphate transport between sperm mitochondrion and tail.

Authors:  R M Tombes; B M Shapiro
Journal:  Cell       Date:  1985-05       Impact factor: 41.582

4.  Recoverin improves rod-mediated vision by enhancing signal transmission in the mouse retina.

Authors:  Alapakkam P Sampath; Katherine J Strissel; Rajesh Elias; Vadim Y Arshavsky; James F McGinnis; Jeannie Chen; Satoru Kawamura; Fred Rieke; James B Hurley
Journal:  Neuron       Date:  2005-05-05       Impact factor: 17.173

5.  Mice deficient in ubiquitous mitochondrial creatine kinase are viable and fertile.

Authors:  K Steeghs; F Oerlemans; B Wieringa
Journal:  Biochim Biophys Acta       Date:  1995-06-30

6.  Nuclear magnetic resonance and biochemical measurements of glucose utilization in the cone-dominant ground squirrel retina.

Authors:  Barry S Winkler; Catherine A Starnes; Brandon S Twardy; Diane Brault; R Craig Taylor
Journal:  Invest Ophthalmol Vis Sci       Date:  2008-06-19       Impact factor: 4.799

7.  Retinoschisin (RS1), the protein encoded by the X-linked retinoschisis gene, is anchored to the surface of retinal photoreceptor and bipolar cells through its interactions with a Na/K ATPase-SARM1 complex.

Authors:  Laurie L Molday; Winco W H Wu; Robert S Molday
Journal:  J Biol Chem       Date:  2007-09-05       Impact factor: 5.157

Review 8.  Retinal oxygen: fundamental and clinical aspects.

Authors:  Norbert D Wangsa-Wirawan; Robert A Linsenmeier
Journal:  Arch Ophthalmol       Date:  2003-04

9.  The active site of creatine kinase. Affinity labeling of cysteine 282 with N-(2,3-epoxypropyl)-N-amidinoglycine.

Authors:  D D Buechter; K F Medzihradszky; A L Burlingame; G L Kenyon
Journal:  J Biol Chem       Date:  1992-02-05       Impact factor: 5.157

10.  Postsynaptic responses of horizontal cells in the tiger salamander retina are mediated by AMPA-preferring receptors.

Authors:  J H Yang; B Maple; F Gao; G Maguire; S M Wu
Journal:  Brain Res       Date:  1998-06-22       Impact factor: 3.252

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  57 in total

Review 1.  Cell signaling and mitochondrial dynamics: Implications for neuronal function and neurodegenerative disease.

Authors:  Theodore J Wilson; Andrew M Slupe; Stefan Strack
Journal:  Neurobiol Dis       Date:  2012-01-24       Impact factor: 5.996

Review 2.  Energy dysfunction in Huntington's disease: insights from PGC-1α, AMPK, and CKB.

Authors:  Tz-Chuen Ju; Yow-Sien Lin; Yijuang Chern
Journal:  Cell Mol Life Sci       Date:  2012-05-25       Impact factor: 9.261

3.  Proteomic profiling of a layered tissue reveals unique glycolytic specializations of photoreceptor cells.

Authors:  Boris Reidel; J Will Thompson; Sina Farsiu; M Arthur Moseley; Nikolai P Skiba; Vadim Y Arshavsky
Journal:  Mol Cell Proteomics       Date:  2010-12-20       Impact factor: 5.911

4.  Facilitative glucose transporter Glut1 is actively excluded from rod outer segments.

Authors:  Sidney M Gospe; Sheila A Baker; Vadim Y Arshavsky
Journal:  J Cell Sci       Date:  2010-10-05       Impact factor: 5.285

Review 5.  Probing Metabolism in the Intact Retina Using Stable Isotope Tracers.

Authors:  Jianhai Du; Jonathan D Linton; James B Hurley
Journal:  Methods Enzymol       Date:  2015-06-14       Impact factor: 1.600

Review 6.  Lateral interactions in the outer retina.

Authors:  Wallace B Thoreson; Stuart C Mangel
Journal:  Prog Retin Eye Res       Date:  2012-05-03       Impact factor: 21.198

7.  Control of creatine metabolism by HIF is an endogenous mechanism of barrier regulation in colitis.

Authors:  Louise E Glover; Brittelle E Bowers; Bejan Saeedi; Stefan F Ehrentraut; Eric L Campbell; Amanda J Bayless; Evgenia Dobrinskikh; Agnieszka A Kendrick; Caleb J Kelly; Adrianne Burgess; Lauren Miller; Douglas J Kominsky; Paul Jedlicka; Sean P Colgan
Journal:  Proc Natl Acad Sci U S A       Date:  2013-11-18       Impact factor: 11.205

Review 8.  Mitochondrial dynamics in neuronal injury, development and plasticity.

Authors:  Kyle H Flippo; Stefan Strack
Journal:  J Cell Sci       Date:  2017-02-02       Impact factor: 5.285

9.  In vivo optoretinography of phototransduction activation and energy metabolism in retinal photoreceptors.

Authors:  Guangying Ma; Taeyoon Son; Tae-Hoon Kim; Xincheng Yao
Journal:  J Biophotonics       Date:  2021-02-18       Impact factor: 3.207

Review 10.  Circadian regulation in the retina: From molecules to network.

Authors:  Gladys Y-P Ko
Journal:  Eur J Neurosci       Date:  2018-10-24       Impact factor: 3.386

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