Cited by 250Genetics, Aging, and Longevity in Model OrganismsAutophagy in Disease and TherapyDietary Effects on Health

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HIF-1 Modulates Dietary Restriction-Mediated Lifespan Extension via IRE-1 in Caenorhabditis elegans

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Chen, Di, Thomas, Emma Lynn, Kapahi, Pankaj·2009·PLoS Genetics

DOI 10.1371/journal.pgen.1000486PMC PMC2676694

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Abstract

Dietary restriction (DR) extends lifespan in various species and also slows the onset of age-related diseases. Previous studies from flies and yeast have demonstrated that the target of rapamycin (TOR) pathway is essential for longevity phenotypes resulting from DR. TOR is a conserved protein kinase that regulates growth and metabolism in response to nutrients and growth factors. While some of the downstream targets of TOR have been implicated in regulating lifespan, it is still unclear whether additional targets of this pathway also modulate lifespan. It has been shown that the hypoxia inducible factor-1 (HIF-1) is one of the targets of the TOR pathway in mammalian cells. HIF-1 is a transcription factor complex that plays key roles in oxygen homeostasis, tumor formation, glucose metabolism, cell survival, and inflammatory response. Here, we describe a novel role for HIF-1 in modulating lifespan extension by DR in Caenorhabditis elegans. We find that HIF-1 deficiency results in extended lifespan, which overlaps with that by inhibition of the RSKS-1/S6 kinase, a key component of the TOR pathway. Using a modified DR method based on variation of bacterial food concentrations on solid agar plates, we find that HIF-1 modulates longevity in a nutrient-dependent manner. The hif-1 loss-of-function mutant extends lifespan under rich nutrient conditions but fails to show lifespan extension under DR. Conversely, a mutation in egl-9, which increases HIF-1 activity, diminishes the lifespan extension under DR. This deficiency is rescued by tissue-specific expression of egl-9 in specific neurons and muscles. Increased lifespan by hif-1 or DR is dependent on the endoplasmic reticulum (ER) stress regulator inositol-requiring protein-1 (IRE-1) and is associated with lower levels of ER stress. Therefore, our results demonstrate a tissue-specific role for HIF-1 in the lifespan extension by DR involving the IRE-1 ER stress pathway.

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Authors: Chen, D., Thomas, E. L., & Kapahi, P.
Affiliations: Buck Institute for Research on Aging (US)
Corresponding author: Kapahi, Pankaj
ORCID: Chen, Di
Kapahi, Pankaj
Venue: PLoS Genetics
Publisher: Public Library of Science (PLoS)
Published: 2009-05-22
Volume: 5
Issue: 5
Pages: e1000486
ISSN: 1553-7390 (ISSN-L)
1553-7404
DOI: 10.1371/journal.pgen.1000486
PMC: PMC2676694
OpenAlex: W2091316238
Cited by: 250
References: 83
Citations by year: 2026: 5 · 2025: 3 · 2024: 7 · 2023: 12 · 2022: 11 · 2021: 15 · 2020: 13 · 2019: 7 · 2018: 6 · 2017: 6 · 2016: 20 · 2015: 13 · 2014: 21 · 2013: 18 · 2012: 17
FWCI: 9.38
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS Genetics (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Figshare (submittedVersion, cc-by)
Funders: Ellison Medical Foundation
Larry L. Hillblom Foundation
American Foundation for Aging Research
National Institutes of Health
U.S. Public Health Service (RL1 AAG032113)
National Institute on Aging (RL1AG032113)
National Center for Research Resources
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Health Sciences › Medicine › Physiology (medical) › Dietary Effects on Health
Keywords: HIF-1, dietary restriction, lifespan extension, IRE1, endoplasmic reticulum stress, TOR signaling, egl-9, Caenorhabditis elegans, tissue-specific gene expression
MeSH terms: Animals, Base Sequence, Endoplasmic Reticulum, Inositol, Longevity, Models, Genetic, Muscles, Mutation, Neurons, Stress, Physiological, Caenorhabditis elegans, Genes, Helminth, DNA Primers, Ribosomal Protein S6 Kinases, Caenorhabditis elegans Proteins, Caloric Restriction, RNA Interference, Hypoxia-Inducible Factor 1

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HIF-1 Modulates Dietary Restriction-Mediated Lifespan Extension via IRE-1 in Caenorhabditis elegans

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