ArticleCell metabolism2016
Effects of Sex, Strain, and Energy Intake on Hallmarks of Aging in Mice.
Open access · bronzeAbstract read
In one paragraph
Article in Cell metabolism, 2016. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 304 papers, 2 of them syntheses that pooled it.
0numbers the graph read from it
0cells of the map it votes in
304citing papers in PubMed, 2 pooled it
22.4field-weighted citation impact, top 1% of its field
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.
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.
Who cites it
304 citing papers in PubMed, 2 syntheses or guidelines pooled it, 469 citations in OpenAlex.
- Rapamycin, Not Metformin, Mirrors Dietary Restriction-Driven Lifespan Extension in Vertebrates: A Meta-Analysis.Aging cell · 2025Pooled it
- Sex differences in pharmacological interventions and their effects on lifespan and healthspan outcomes: a systematic review.Frontiers in aging · 2023Pooled it
- Chaperone-mediated autophagy in physiological homeostasis, disease and ageing.Nature reviews. Molecular cell biology · 2026Review
- Article
- Selective Breeding for Voluntary Wheel-Running Behavior in Mice is not Associated with Reduced Lifetime Reproductive Success or Lifespan Under Long-Term Paired Breeding Conditions.Behavior genetics · 2026Article
- Cryptic transcription in aging.iScience · 2026Review
- Lifelong restriction of dietary valine has sex-specific benefits for health and lifespan in mice.Nature aging · 2026Article
- Untargeted metabolomics reveals effects of calorie restriction on skeletal muscle in older female and male rats.The journals of gerontology. Series A, Biological sciences and medical sciences · 2026Article
- Sex differences in response to longevity interventions.Ageing research reviews · 2026Review
- Article
- Time-restricted feeding extends healthspan in both sexes and lifespan in male C57BL/6 J mice.Nature aging · 2026Article
- Reducing the strain on calorie restriction.Life metabolism · 2026Article
- Genetic regulation of fasting-induced longevity effects.Genetics · 2026Article
- A nutrient-hormone axis pivots an energy trade-off between resting thermogenesis and movement expenditure.Journal of sport and health science · 2026Article
- Dietary restriction in aging and longevity.Nature aging · 2026Review
- Epigenetic profiling of hematopoietic stem cells from male mice identifies KDR and PU.1 as regulators of aging transcriptome and caloric restriction response.Nature communications · 2026Article
- Calorie Restriction Upregulates Islet PD-L1 Signaling and Decreases the Risk of Autoimmune Diabetes Onset in NOD Mice.bioRxiv : the preprint server for biology · 2026Article
- Caloric Restriction and Dietary Taurine Regulate Taurine Homeostasis Through Distinct Tissue-Specific Mechanisms in Mice.Molecular nutrition & food research · 2026Article
- Low protein-induced-FGF-21 signaling remodels adipose tissue on reduced markers of senescence during aging.GeroScience · 2026Article
- Parental fasting effects on offspring immune gene expression, epigenetic patterns, and gut microbiota in a species with male pregnancy (Syngnathus typhle).BMC biology · 2026Article
244 more citing papers are in PubMed but not listed here.
Corrections and comments
PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.
Authors and funding
47 authors at 14 institutions in 4 countries.
Sarah J MitchellTranslational Gerontology Branch, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
Julio Madrigal-MatuteDepartment of Developmental and Molecular Biology, Institute for Aging Studies, Albert Einstein College of Medicine, Bronx, NY 10461, USA.
Morten Scheibye-KnudsenTranslational Gerontology Branch, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA; Laboratory of Molecular Gerontology, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA; Department of Cellular and Molecular Medicine, Center for Healthy Aging, University of Copenhagen, 2200 Copenhagen, Denmark.
Evandro FangLaboratory of Molecular Gerontology, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
Miguel AonLaboratory of Cardiovascular Science, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
José A González-ReyesDepartment of Cell Biology, Physiology and Immunology, University of Córdoba, Agrifood Campus of International Excellence, ceiA3, 14071 Córdoba, Spain.
Sonia CortassaLaboratory of Cardiovascular Science, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
Susmita KaushikDepartment of Developmental and Molecular Biology, Institute for Aging Studies, Albert Einstein College of Medicine, Bronx, NY 10461, USA.
Marta Gonzalez-FreireTranslational Gerontology Branch, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
Bindi PatelDepartment of Developmental and Molecular Biology, Institute for Aging Studies, Albert Einstein College of Medicine, Bronx, NY 10461, USA.
Devin WahlTranslational Gerontology Branch, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
Ahmed AliTranslational Gerontology Branch, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
Miguel Calvo-RubioDepartment of Cell Biology, Physiology and Immunology, University of Córdoba, Agrifood Campus of International Excellence, ceiA3, 14071 Córdoba, Spain.
María I BurónDepartment of Cell Biology, Physiology and Immunology, University of Córdoba, Agrifood Campus of International Excellence, ceiA3, 14071 Córdoba, Spain.
Vincent GuiterrezTranslational Gerontology Branch, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
Theresa M WardTranslational Gerontology Branch, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
Hector H PalaciosTranslational Gerontology Branch, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
Huan CaiLaboratory of Clinical Investigation, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
David W FrederickDepartment of Physiology, Institute for Diabetes, Obesity, and Metabolism, University of Pennsylvania, Philadelphia, PA 19104, USA.
Christopher HineDepartment of Genetics and Complex Diseases, Harvard University, Boston, MA 02115, USA.
Filomena BroeskampInstitute of Molecular Biosciences, NAWI Graz, University of Graz, and BioTechMed Graz, 8010 Graz, Austria.
Lukas HaberingInstitute of Molecular Biosciences, NAWI Graz, University of Graz, and BioTechMed Graz, 8010 Graz, Austria.
John DawsonDepartment of Biostatistics, University of Alabama, Birmingham, AL 35294, USA; GRECC, Birmingham/Atlanta Veterans Administration Hospital, Birmingham, AL 35294, USA.
T Mark BeasleyDepartment of Biostatistics, University of Alabama, Birmingham, AL 35294, USA; GRECC, Birmingham/Atlanta Veterans Administration Hospital, Birmingham, AL 35294, USA.
Junxiang WanLeonard Davis School of Gerontology, University of Southern California, Los Angeles, CA 90089, USA.
Yuji IkenoBarshop Institute for Longevity and Aging Studies, University of Texas Health Science Center at San Antonio, San Antonio, TX 78245-3207, USA.
Gene HubbardBarshop Institute for Longevity and Aging Studies, University of Texas Health Science Center at San Antonio, San Antonio, TX 78245-3207, USA.
Kevin G BeckerLaboratory of Genetics, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
Yongqing ZhangLaboratory of Genetics, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
Vilhelm A BohrLaboratory of Molecular Gerontology, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
Dan L LongoLaboratory of Genetics, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
Placido NavasCentro Andaluz de Biologia del Desarrollo, and CIBERER, Instituto de Salud Carlos III, Universidad Pablo de Olavide-CSIC, 41013 Sevilla, Spain.
Luigi FerrucciTranslational Gerontology Branch, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
David A SinclairDepartment of Genetics, Harvard Medical School, Boston, MA 02115, USA.
Pinchas CohenLeonard Davis School of Gerontology, University of Southern California, Los Angeles, CA 90089, USA.
Josephine M EganLaboratory of Clinical Investigation, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
James R MitchellDepartment of Genetics and Complex Diseases, Harvard University, Boston, MA 02115, USA.
Joseph A BaurDepartment of Physiology, Institute for Diabetes, Obesity, and Metabolism, University of Pennsylvania, Philadelphia, PA 19104, USA.
David B AllisonDepartment of Biostatistics, University of Alabama, Birmingham, AL 35294, USA; GRECC, Birmingham/Atlanta Veterans Administration Hospital, Birmingham, AL 35294, USA.
R Michael AnsonTranslational Gerontology Branch, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
José M VillalbaDepartment of Cell Biology, Physiology and Immunology, University of Córdoba, Agrifood Campus of International Excellence, ceiA3, 14071 Córdoba, Spain.
Frank MadeoInstitute of Molecular Biosciences, NAWI Graz, University of Graz, and BioTechMed Graz, 8010 Graz, Austria.
Ana Maria CuervoDepartment of Developmental and Molecular Biology, Institute for Aging Studies, Albert Einstein College of Medicine, Bronx, NY 10461, USA.
Kevin J PearsonTranslational Gerontology Branch, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA; Graduate Center for Nutritional Sciences, University of Kentucky, C.T. Wethington Building, Room 591, 900 South Limestone, Lexington, KY 40536, USA.
Donald K IngramPennington Biomedical Research Center, Baton Rouge, LA 70809, USA.
Michel BernierTranslational Gerontology Branch, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA.
Rafael de CaboTranslational Gerontology Branch, Intramural Research Program, National Institute on Aging, NIH, 251 Bayview Boulevard, Suite 100, Baltimore, MD 21224, USA. Electronic address: decabora@mail.nih.gov.
National Institute on Aging · USAlbert Einstein College of Medicine · USUniversity of Córdoba · ESHarvard University · USBioTechMed-Graz · ATBirmingham VA Medical Center · USThe University of Texas Health Science Center at San Antonio · USUniversity of Pennsylvania · USUniversity of Southern California · USGeriatric Research Education and Clinical Center · USInstituto de Salud Carlos III · ESPennington Biomedical Research Center · USUniversity of Graz · ATUniversity of Kentucky · US
Funding
Role of Autophagy in T Cell Function and Immunosenescence (Project 3)P01AG031782 · NIA · ALBERT EINSTEIN COLLEGE OF MEDICINE, INC · PI MACIAN, FERNANDO · 2009 to 2024
$36.2MTranslational Research Support CoreP30ES013508 · NIEHS · UNIVERSITY OF PENNSYLVANIA · PI Rebecca A Simmons · 2006 to 2026
$35.3MTRANSGENIC COREP30AG013319 · NIA · UNIVERSITY OF TEXAS HLTH SCIENCE CENTER · PI PETER J HORNSBY · 1995 to 2026
$30.6MTranslational Research CoreP30DK020541 · NIDDK · ALBERT EINSTEIN COLLEGE OF MEDICINE, INC · PI STREAMSON C CHUA · 2015 to 2026
$27.7MSpecial Animal CoreP30DK041296 · NIDDK · YESHIVA UNIVERSITY · PI WOLKOFF, ALLAN W · 1989 to 2018
$22.9MUniversity of Alabama at Birmingham's Diabetes Research CenterP30DK079626 · NIDDK · UNIVERSITY OF ALABAMA AT BIRMINGHAM · PI Kirk Michael Habegger · 2013 to 2026
$19.5MEinstein's Nathan Shock Center of Excellence in Basic Biology of AgingP30AG038072 · NIA · ALBERT EINSTEIN COLLEGE OF MEDICINE, INC · PI VIJG, JAN · 2010 to 2024
$10.8MThe Role of the Glucose-regulated Protein GRP78/BiP in Stress Resistance and AginP01AG034906 · NIA · UNIVERSITY OF SOUTHERN CALIFORNIA · PI LONGO, VALTER D. · 2011 to 2016
$9.3MMitochondrial DNA Repair Processes In Oxidative Stress And AgingZIAAG000733 · NIA · NATIONAL INSTITUTE ON AGING · PI FERRUCCI, LUIGI · 2009 to 2022
$9.2MOxidative DNA Damage And Its ProcessingZIAAG000727 · NIA · NATIONAL INSTITUTE ON AGING · PI FERRUCCI, LUIGI · 2009 to 2022
$8.4MCalorie restriction and agingZIAAG000368 · NIA · NATIONAL INSTITUTE ON AGING · PI DE CABO, RAFAEL · 2009 to 2025
$6.9MTargeting NAD Metabolism to Improve Glucose Homeostasis in Obesity and AgingR01DK098656 · NIDDK · UNIVERSITY OF PENNSYLVANIA · PI Joseph A. Baur · 2013 to 2026
$6.1MAustrian Science Fund FWF P 27893Austrian Science Fund FWF P 29203Intramural NIH HHS ZIA AG000368NIA NIH HHS P01 AG031782NIA NIH HHS P01 AG034906NIA NIH HHS P30 AG013319NIA NIH HHS P30 AG038072NIA NIH HHS R01 AG043483NIDDK NIH HHS P30 DK020541NIDDK NIH HHS P30 DK041296NIDDK NIH HHS P30 DK079626NIDDK NIH HHS R01 DK098656NIEHS NIH HHS P30 ES013508NIEHS NIH HHS R01 ES020812NIGMS NIH HHS R01 GM090311
Abstract
Calorie restriction (CR) is the most robust non-genetic intervention to delay aging. However, there are a number of emerging experimental variables that alter CR responses. We investigated the role of sex, strain, and level of CR on health and survival in mice. CR did not always correlate with lifespan extension, although it consistently improved health across strains and sexes. Transcriptional and metabolomics changes driven by CR in liver indicated anaplerotic filling of the Krebs cycle together with fatty acid fueling of mitochondria. CR prevented age-associated decline in the liver proteostasis network while increasing mitochondrial number, preserving mitochondrial ultrastructure and function with age. Abrogation of mitochondrial function negated life-prolonging effects of CR in yeast and worms. Our data illustrate the complexity of CR in the context of aging, with a clear separation of outcomes related to health and survival, highlighting complexities of translation of CR into human interventions.
Indexed as
Energy IntakeSex CharacteristicsAgingAnimalsAutophagyBiomarkersCaloric RestrictionCluster AnalysisFemaleGene Expression ProfilingGene Expression RegulationGlucoseHomeostasisHydrogen SulfideIslets of LangerhansLiverBiomarkersGlucoseHydrogen SulfideProteasome Endopeptidase ComplexUbiquitin
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