Evidence mapPaperPMID 26974308Full record

ArticleNature medicine2016

Retinal lipid and glucose metabolism dictates angiogenesis through the lipid sensor Ffar1.

Jean-Sébastien Joyal, Ye Sun, Marin L Gantner, Zhuo Shao, Lucy P Evans, Nicholas Saba, Thomas Fredrick, Samuel Burnim, Jin Sung Kim, Gauri Patel and 21 more

Erratum issuedOpen access · greenAbstract read
In one paragraph

Article in Nature medicine, 2016. The graph could read no effect estimate from its abstract, so it casts no vote on the map. An erratum has been issued. Cited by 187 papers, 1 of them a synthesis that pooled it.

0numbers the graph read from it
0cells of the map it votes in
187citing papers in PubMed, 1 pooled it
20.7field-weighted citation impact, top 1% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

187 citing papers in PubMed, 1 synthesis or guideline pooled it, 286 citations in OpenAlex.

  1. Pooled it
  2. Polyunsaturated fatty acid metabolism in the retinal pigment epithelium and its association with outer retinal disease.Mammalian genome : official journal of the International Mammalian Genome Society · 2026
    Review
  3. Review
  4. Review
  5. The roles of glycerophospholipids in the aging retina and age-related macular degeneration.Graefe's archive for clinical and experimental ophthalmology = Albrecht von Graefes Archiv fur klinische und experimentelle Ophthalmologie · 2026
    Review
  6. Review
  7. Article
  8. Article
  9. Article
  10. Article
  11. The Multitarget Compound ZLY032 Achieves Treatment of Chronic Wounds.Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2025
    Article
  12. Article
  13. Review
  14. Article
  15. Article
  16. Review
  17. Article
  18. Article
  19. Article
  20. Review

127 more citing papers are in PubMed but not listed here.

4 · The record

Corrections and comments

5 · Who and what money

Authors and funding

31 authors at 10 institutions in 3 countries.

Jean-Sébastien JoyalDepartment of Pediatrics, Centre Hospitalier Universitaire (CHU) Sainte-Justine Research Center, Université de Montréal, Montreal, Quebec, Canada.
Ye SunDepartment of Ophthalmology, Harvard Medical School, Boston Children's Hospital, Boston, Massachusetts, USA.
Marin L GantnerLowy Medical Research Institute, La Jolla, California, USA.
Zhuo ShaoDepartment of Ophthalmology, Harvard Medical School, Boston Children's Hospital, Boston, Massachusetts, USA.
Lucy P EvansDepartment of Ophthalmology, Harvard Medical School, Boston Children's Hospital, Boston, Massachusetts, USA.
Nicholas SabaDepartment of Ophthalmology, Harvard Medical School, Boston Children's Hospital, Boston, Massachusetts, USA.
Thomas FredrickDepartment of Ophthalmology, Harvard Medical School, Boston Children's Hospital, Boston, Massachusetts, USA.
Samuel BurnimDepartment of Ophthalmology, Harvard Medical School, Boston Children's Hospital, Boston, Massachusetts, USA.
Jin Sung KimDepartment of Pharmacology and Therapeutics, McGill University, Montreal, Quebec, Canada.
Gauri PatelDepartment of Pharmacology, Université de Montréal, Montreal, Quebec, Canada.
Aimee M JuanDepartment of Ophthalmology, Harvard Medical School, Boston Children's Hospital, Boston, Massachusetts, USA.
Christian G HurstDepartment of Ophthalmology, Harvard Medical School, Boston Children's Hospital, Boston, Massachusetts, USA.
Colman J HattonDepartment of Ophthalmology, Harvard Medical School, Boston Children's Hospital, Boston, Massachusetts, USA.
Zhenghao CuiDepartment of Ophthalmology, Harvard Medical School, Boston Children's Hospital, Boston, Massachusetts, USA.
Kerry A PierceMetabolite Profiling Platform, The Broad Institute of the Massachusetts Institute of Technology (MIT) and Harvard University, Cambridge, Massachusetts, USA.
Patrick BhererDepartment of Genetics, Université de Sherbrooke, Sherbrooke, Quebec, Canada.
Edith AguilarDepartment of Cell and Molecular Biology, Scripps Research Institute, La Jolla, California, USA.
Michael B PownerInstitute of Ophthalmology, University College London, London, UK.
Kristis VevisInstitute of Ophthalmology, University College London, London, UK.
Michel BoisvertDepartment of Nutrition, Centre Hospitalier Universitaire (CHU) Sainte-Justine Research Center, Université de Montreal, Montreal, Quebec, Canada.
Zhongjie FuDepartment of Ophthalmology, Harvard Medical School, Boston Children's Hospital, Boston, Massachusetts, USA.
Emile LevyDepartment of Nutrition, Centre Hospitalier Universitaire (CHU) Sainte-Justine Research Center, Université de Montreal, Montreal, Quebec, Canada.
Marcus FruttigerInstitute of Ophthalmology, University College London, London, UK.
Alan PackardDepartment of Radiology, Harvard Medical School, Boston Children's Hospital, Boston, Massachusetts. USA.
Flavio A RezendeDepartment of Ophthalmology, Maisonneuve-Rosemont Hospital Research Centre, Université de Montréal, Montreal, Quebec, Canada.
Bruno MarandaDepartment of Genetics, Université de Sherbrooke, Sherbrooke, Quebec, Canada.
Przemyslaw SapiehaDepartment of Ophthalmology, Maisonneuve-Rosemont Hospital Research Centre, Université de Montréal, Montreal, Quebec, Canada.
Jing ChenDepartment of Ophthalmology, Harvard Medical School, Boston Children's Hospital, Boston, Massachusetts, USA.
Martin FriedlanderDepartment of Cell and Molecular Biology, Scripps Research Institute, La Jolla, California, USA.
Clary B ClishMetabolite Profiling Platform, The Broad Institute of the Massachusetts Institute of Technology (MIT) and Harvard University, Cambridge, Massachusetts, USA.ORCID http://orcid.org/0000-0001-8259-9245
Lois E H SmithDepartment of Ophthalmology, Harvard Medical School, Boston Children's Hospital, Boston, Massachusetts, USA.
Boston Children's Hospital · USCentre Hospitalier Universitaire Sainte-Justine · CAUniversity College London · GBBroad Institute · USHôpital Maisonneuve-Rosemont · CAScripps Research Institute · USUniversité de Sherbrooke · CAMcGill University · CAThe Lowy Medical Research Institute · USUniversité de Montréal · CA

Funding

SYNAPTIC MECHANISMS IN HIPPOCAMPAL EPILEPTOGENESISP30HD018655 · NICHD · CHILDREN'S HOSPITAL BOSTON · PI POMEROY, SCOTT LOREN · 1985 to 2015
$26.2M
Dietary control of angiogenesis in retinopathy modelsR01EY017017 · NEI · BOSTON CHILDREN'S HOSPITAL · PI Zhongjie Fu, Lois Smith · 2006 to 2026
$11.8M
INTEGRINS AND OCULAR ANGIOGENESISR01EY011254 · NEI · SCRIPPS RESEARCH INSTITUTE, THE · PI FRIEDLANDER, MARTIN · 1996 to 2016
$11.5M
Novel therapies to inhibit Diabetic RetinopathyR24EY024864 · NEI · UNIVERSITY OF CALIFORNIA-IRVINE · PI KERN, TIMOTHY S · 2015 to 2019
$8.1M
Mouse Neurodevelopmental Behavior CoreU54HD090255 · NICHD · BOSTON CHILDREN'S HOSPITAL · PI FAGIOLINI, MICHELA · 2016 to 2020
$5.2M
RORalpha mediates chronic subretinal inflammation associated with AMDR01EY024963 · NEI · BOSTON CHILDREN'S HOSPITAL · PI CHEN, JING · 2015 to 2025
$4.2M
VASCULAR CELL IMMATURITY IN RETINOPATHY OF PREMATURITYR01EY008670 · NEI · CHILDREN'S HOSPITAL BOSTON · PI SMITH, LOIS · 1992 to 2007
$3.9M
Neuronal guidance molecules control revascularization in retinopathyR01EY022275 · NEI · BOSTON CHILDREN'S HOSPITAL · PI SMITH, LOIS · 2012 to 2014
$1.3M
CIHR 143077NEI NIH HHS EY017017NEI NIH HHS EY022275NEI NIH HHS EY024864NEI NIH HHS EY024963NEI NIH HHS EY11254NEI NIH HHS R01 EY008670NEI NIH HHS R01 EY011254NEI NIH HHS R01 EY017017NEI NIH HHS R01 EY022275NEI NIH HHS R01 EY024963NEI NIH HHS R24 EY024864NICHD NIH HHS P01 HD18655NICHD NIH HHS P30 HD018655NICHD NIH HHS U54 HD090255
6 · The paper itself

Abstract

Tissues with high metabolic rates often use lipids, as well as glucose, for energy, conferring a survival advantage during feast and famine. Current dogma suggests that high-energy-consuming photoreceptors depend on glucose. Here we show that the retina also uses fatty acid β-oxidation for energy. Moreover, we identify a lipid sensor, free fatty acid receptor 1 (Ffar1), that curbs glucose uptake when fatty acids are available. Very-low-density lipoprotein receptor (Vldlr), which is present in photoreceptors and is expressed in other tissues with a high metabolic rate, facilitates the uptake of triglyceride-derived fatty acid. In the retinas of Vldlr(-/-) mice with low fatty acid uptake but high circulating lipid levels, we found that Ffar1 suppresses expression of the glucose transporter Glut1. Impaired glucose entry into photoreceptors results in a dual (lipid and glucose) fuel shortage and a reduction in the levels of the Krebs cycle intermediate α-ketoglutarate (α-KG). Low α-KG levels promotes stabilization of hypoxia-induced factor 1a (Hif1a) and secretion of vascular endothelial growth factor A (Vegfa) by starved Vldlr(-/-) photoreceptors, leading to neovascularization. The aberrant vessels in the Vldlr(-/-) retinas, which invade normally avascular photoreceptors, are reminiscent of the vascular defects in retinal angiomatous proliferation, a subset of neovascular age-related macular degeneration (AMD), which is associated with high vitreous VEGFA levels in humans. Dysregulated lipid and glucose photoreceptor energy metabolism may therefore be a driving force in macular telangiectasia, neovascular AMD and other retinal diseases.

Indexed as

AnimalsFatty AcidsGene Expression RegulationGlucoseHumansKetoglutaric AcidsLipid MetabolismMacular DegenerationMiceOxidation-ReductionPhotoreceptor CellsReceptors, G-Protein-CoupledReceptors, LDLRetinaRetinal NeovascularizationVascular Endothelial Growth Factor AFatty AcidsGlucoseKetoglutaric AcidsReceptors, G-Protein-CoupledReceptors, LDLVascular Endothelial Growth Factor Avascular endothelial growth factor A, mouseVLDL receptor

Identifiers

PMID26974308
PMCPMC4823176
OpenAlexW2298457819

What Socratic holds

Textmetadata
LicenceTDM
Read underepoch 390

Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the Socratic graph.