Cited by 1,059Genetics, Aging, and Longevity in Model OrganismsMitochondrial Function and PathologyAutophagy in Disease and Therapy

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The Cell Non-Autonomous Nature of Electron Transport Chain-Mediated Longevity

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Durieux, Jenni, Wolff, Suzanne, Dillin, Andrew·2011·Cell

DOI 10.1016/j.cell.2010.12.016PMC PMC3062502

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Abstract

The life span of C. elegans can be increased via reduced function of the mitochondria; however, the extent to which mitochondrial alteration in a single, distinct tissue may influence aging in the whole organism remains unknown. We addressed this question by asking whether manipulations to ETC function can modulate aging in a cell-non-autonomous fashion. We report that the alteration of mitochondrial function in key tissues is essential for establishing and maintaining a prolongevity cue. We find that regulators of mitochondrial stress responses are essential and specific genetic requirements for the electron transport chain (ETC) longevity pathway. Strikingly, we find that mitochondrial perturbation in one tissue is perceived and acted upon by the mitochondrial stress response pathway in a distal tissue. These results suggest that mitochondria may establish and perpetuate the rate of aging for the whole organism independent of cell-autonomous functions.

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Age-related Changes in the Neuronal Architecture of Caenorhabditis Elegans: A Dissertation
Khandekar, A. (2015) · The Journal of the American Medical Association (JAMA) Network (American Medical Association) · doi:10.13028/m2m88h · Cited by 1
“mechanisms that trigger mitochondrial stress response in non-neuronal tissues [52].”
Background
Caenorhabditis elegans as a research tool to study mitochondrial diseases associated with defects in tRNA modification
GONZÁLEZ, M. D. C. N. (2016) · doi:10.4995/thesis/10251/61978
Functional Analysis of Genomic Variation and Impact on Molecular and Higher Order Phenotypes
Pandey, A. K. (2015) · doi:10.21007/etd.cghs.2015.0237
“Various disturbances have been shown to induce the UPR, including treatment with paraquat, a pesticide that strongly induces reactive oxygen species[278], activation of mitochondrial biogenesis[87], overexpression of aggregation-prone mitochondrial proteins[279], and interference with electron transport chain protein…”
Background
Integrity of the Barrier Epithelium in Drosophila Gut is Mediated by Factors That Regulate Intestinal Stem Cell Activity
Kinion, A. A. (2016) · Dominican Scholar (Dominican University of California) · doi:10.33015/dominican.edu/2016.bio.10
“Over a species’ lifespan, the dysfunctional ETC-driven loss in metabolic homeostasis is in part due to the inability of mitochondria to 2 manage ATP output (Martinus, 1996) (Broderick, 2014) (Durieux, 2011).”
Background
Chapter 13 Shining a Light on Parkinson’s Disease
Johnstone, D. M., Moro, C., Stone, J., Benabid, A., & Mitrofanis, J. (2016) · Pan Stanford Publishing Pte. Ltd. eBooks · doi:10.1201/9781315364827-14
Mechanisms Underlying Longevity Regulation and Extension by Genetic, Dietary and Pharmacological Interventions in the Yeast Saccharomyces Cerevisiae
Kyryakov, P. (2012) · Spectrum Research Repository (Concordia University)
Proteostasis perturbation destabilizes respiratory complex assembly-intermediates via aggregation of subunitsPreprint
Rawat, S., Valpadashi, A., Jha, M., Sreedurgalakshmi, K., Ghosh, A., Ganguly, D., & Raychaudhuri, S. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/312793
“Rather, our data indicate that aggregation-prone RCC subunits Ndufa5 and Ndufa6 may be cleared from the MG132 treated cells by unconventional secretion mechanisms (Durieux et al., 2011; Lee et al., 2016).”
Background
Effects of AMP-activated kinase modulators on intracellular Ca2+ signalling and C. elegans lifespan
Arias-del-Val, J. (2018) · UVaDOC UVaDOC University of Valladolid Documentary Repository (University of Valladolid) · doi:10.35376/10324/33455
Translational control in nutrient response and aging
Harris, M. S. (2016)
FSHR-1/GPCR activates the mitochondrial unfolded protein response in Caenorhabditis elegansPreprint
Kim, S., & Sieburth, D. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/586883
“Failure to appropriately control and maintain protein homeostasis in the mitochondria is associated with the development of numerous diseases, neurodegeneration, and ageing (Durieux et al. 2011; Liu et al. 2014; Pellegrino et al. 2014; Nargund et al. 2015; Fiorese et al. 2016; Martinez et al. 2017).”
Background
A resource for analyzing C. elegans ’ gene expression data using transcriptional gene modules and module-weighted annotationsPreprint
Cary, M. P., Podshivalova, K., & Kenyon, C. J. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/678482
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Molenaars, M., Janssens, G. E., Santermans, T., Lezzerini, M., Jelier, R., MacInnes, A. W., & Houtkooper, R. H. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/308858
“Besides hits in the UPR and stress resistance, both already described in clk-1 mutants (Durieux et al., 2011), the results also revealed possible involvement of the mTOR signaling pathway in the clk-1 mutants.”
Background
Mechanisms underlying the functions of sleep in aging during starvation in Caenorhabditis elegans
Wu, Y. (2019) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-7601
Consequences of Persistent Mitochondrial DNA Damage and Increased Oxidative Stress
Donoghue, L. J. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/j0ze-ft34
Causes and Consequences of Mitochondrial Variation in Caenorhabditid Nematodes
Hicks, K. A. (2000) · doi:10.15760/etd.928
“Indeed, mitochondrial ETC function appears to affect such diverse processes as a cell-non-autonomous pathway of organismal longevity (Durieux et al. 2011) and nuclear gene expression (Droge 2002).”
Background
Cell Competition: A Choreographed Dance of Death
Lima, A., & Rodríguez, T. A. (2021) · Current Biology · doi:10.1016/j.cub.2021.01.017
An HSP90 Cochaperone Ids2 Maintains the Stability of Mitochondrial DNA and ATP SynthasePreprint
Jiang, P.-H., Hou, C.-Y., & Teng, S. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3803608
A tRNA processing enzyme is a central regulator of the mitochondrial unfolded protein responsePreprint
Held, J. P., Saunders, B. R., Pereira, C. V., & Patel, M. R. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.06.22.449331
Ye Tian: Surveilling stress to live longer
Morgado-Palacin, L. (2021) · The Journal of Cell Biology · doi:10.1083/jcb.202108098
Later-life Effects of Mitochondrial DNA Damage During Development in the Whole Organism Model Caenorhabditis elegans
Leung, M. C. K. (2012) · DukeSpace (Duke University)
Glia of C. elegans coordinate the heat shock response independent of the neuronal thermosensory circuit and serotoninPreprint
Gildea, H. K., Frankino, P. A., Tronnes, S. U., Pender, C. L., Choi, H. O., Hunter, T. D., Cheung, S. S., Frakes, A. E., Sukarto, E., & Dillin, A. G. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.01.31.478522
Faculty Opinions recommendation of Secreted VAPB/ALS8 major sperm protein domains modulate mitochondrial localization and morphology via growth cone guidance receptors.
Volk, T. (2012) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.13976959.15432059
Formbildung
Penzlin, H. (2015) · Springer eBooks · doi:10.1007/978-3-662-48128-8_10
Faculty Opinions recommendation of The hallmarks of aging.
Hickson, I. D., & Mankouri, H. W. (2013) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.718061760.793481794
Faculty Opinions recommendation of HSB-1/HSF-1 pathway modulates histone H4 in mitochondria to control mtDNA transcription and longevity.
Lee, S., & Jung, Y. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.738873555.793581304
Faculty Opinions recommendation of The C. elegans microRNA mir-71 acts in neurons to promote germline-mediated longevity through regulation of DAF-16/FOXO.
Tavernarakis, N., & Markaki, M. (2012) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.714197805.791452865
Mitochondria Preconditioning Promotes C. elegans Healthspan via Ferroptosis InhibitionPreprint
Schiavi, A., Runci, A., Salveridou, E., Maiorino, T., Brinkmann, V., Shaik, A., Barenys, M., Fritsche, E., Menzel, R., Kalyanasundaram, S., et al. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4064104
The roles of macrophages in mediating the homeostatic process
Mitra, A., & Cho, J. Y. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-822368-0.00018-9
Neuroendocrine control of the proteostatic network by HPK-1 delays agingPreprint
Lázaro‐Peña, M. I., Díaz-Balzac, C. A., Das, R., & Samuelson, A. V. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.04.02.486836
“elegans nervous system can initiate a number of distinct stress and longevity signals cell non-autonomously, which activates comparable changes in gene expression peripheral tissues (15, 16, 18, 19, 51-55).”
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The discovery and consequences of the central role of the nervous system in the control of protein homeostasis
Prahlad, V. (2022) · CRC Press eBooks · doi:10.1201/9781003239758-36
A conserved role of CBP/p300 in mitochondrial stress response and longevityPreprint
Li, T. Y., Sleiman, M. S. B., Li, H., Gao, A. W., Mottis, A., Bachmann, A., Alam, G. E., Goeminne, L. J. E., Li, X., Schoonjans, K., et al. (2020) · doi:10.21203/rs.3.rs-86465/v1
Mitohormesis
Machado, I. F., Teodoro, J. S., Castela, A. C., Palmeira, C. M., & Rolo, A. P. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-821562-3.00035-6

Authors: Durieux, J., Wolff, S., & Dillin, A.
Affiliations: Salk Institute for Biological Studies (US)
Scripps Research Institute (US)
Corresponding author: Dillin, Andrew
ORCID: Durieux, Jenni
Dillin, Andrew
Venue: Cell
Publisher: Elsevier BV
Published: 2011-01
Volume: 144
Issue: 1
Pages: 79-91
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2010.12.016
PMC: PMC3062502
OpenAlex: W2023402149
Cited by: 1,059
References: 60
Citations by year: 2026: 54 · 2025: 52 · 2024: 80 · 2023: 58 · 2022: 82 · 2021: 78 · 2020: 70 · 2019: 62 · 2018: 74 · 2017: 59 · 2016: 82 · 2015: 73 · 2014: 88 · 2013: 62 · 2012: 60
FWCI: 26.93
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 928 d)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Institute on Aging (R01AG024365)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Keywords: electron transport chain, longevity, aging, mitochondrial stress response, non-cell-autonomous signaling, Caenorhabditis elegans, mitochondrial function
MeSH terms: Aging, Animals, Electron Transport, Longevity, Mitochondria, Cellular Senescence, Caenorhabditis elegans, Oxidative Stress, Unfolded Protein Response

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The Cell Non-Autonomous Nature of Electron Transport Chain-Mediated Longevity

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