DLK-1, SEK-3 and PMK-3 Are Required for the Life Extension Induced by Mitochondrial Bioenergetic Disruption in C. elegans

Mitochondrial dysfunction underlies numerous age-related pathologies. In an effort to uncover how the detrimental effects of mitochondrial dysfunction might be alleviated, we examined how the nematode C. elegans not only adapts to disruption of the mitochondrial electron transport chain, but in many...

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Published inPLoS genetics Vol. 12; no. 7; p. e1006133
Main Authors Munkácsy, Erin, Khan, Maruf H, Lane, Rebecca K, Borror, Megan B, Park, Jae H, Bokov, Alex F, Fisher, Alfred L, Link, Christopher D, Rea, Shane L
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.07.2016
Public Library of Science (PLoS)
Subjects
Alzheimer's disease
Alzheimers disease
Animals
Bioenergetics
Biology and Life Sciences
Biosynthesis
Caenorhabditis elegans
Caenorhabditis elegans - physiology
Caenorhabditis elegans Proteins - physiology
DNA sequencing
Electron Transport
Electron Transport Chain Complex Proteins - physiology
Funding
Gene expression
Gene Expression Regulation
Genes, Reporter
Genetic aspects
Green Fluorescent Proteins - metabolism
MAP Kinase Kinase Kinases - physiology
Medicine and Health Sciences
Methods
Mitochondria
Mitochondria - metabolism
Mitochondrial DNA
Mitogen-Activated Protein Kinases - physiology
Mutation
Nematoda
Nematodes
Oxidative stress
p38 Mitogen-Activated Protein Kinases - metabolism
Pathogens
Phosphotransferases
Physiological aspects
Proteins
Research and Analysis Methods
RNA Interference
Signal Transduction
Surveillance
Unfolded Protein Response
Worms
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Abstract Mitochondrial dysfunction underlies numerous age-related pathologies. In an effort to uncover how the detrimental effects of mitochondrial dysfunction might be alleviated, we examined how the nematode C. elegans not only adapts to disruption of the mitochondrial electron transport chain, but in many instances responds with extended lifespan. Studies have shown various retrograde responses are activated in these animals, including the well-studied ATFS-1-dependent mitochondrial unfolded protein response (UPRmt). Such processes fall under the greater rubric of cellular surveillance mechanisms. Here we identify a novel p38 signaling cascade that is required to extend life when the mitochondrial electron transport chain is disrupted in worms, and which is blocked by disruption of the Mitochondrial-associated Degradation (MAD) pathway. This novel cascade is defined by DLK-1 (MAP3K), SEK-3 (MAP2K), PMK-3 (MAPK) and the reporter gene Ptbb-6::GFP. Inhibition of known mitochondrial retrograde responses does not alter induction of Ptbb-6::GFP, instead induction of this reporter often occurs in counterpoint to activation of SKN-1, which we show is under the control of ATFS-1. In those mitochondrial bioenergetic mutants which activate Ptbb-6::GFP, we find that dlk-1, sek-3 and pmk-3 are all required for their life extension.
AbstractList   Mitochondrial dysfunction underlies numerous age-related pathologies. In an effort to uncover how the detrimental effects of mitochondrial dysfunction might be alleviated, we examined how the nematode C. elegans not only adapts to disruption of the mitochondrial electron transport chain, but in many instances responds with extended lifespan. Studies have shown various retrograde responses are activated in these animals, including the well-studied ATFS-1-dependent mitochondrial unfolded protein response (UPRmt). Such processes fall under the greater rubric of cellular surveillance mechanisms. Here we identify a novel p38 signaling cascade that is required to extend life when the mitochondrial electron transport chain is disrupted in worms, and which is blocked by disruption of the Mitochondrial-associated Degradation (MAD) pathway. This novel cascade is defined by DLK-1 (MAP3K), SEK-3 (MAP2K), PMK-3 (MAPK) and the reporter gene Ptbb-6::GFP. Inhibition of known mitochondrial retrograde responses does not alter induction of Ptbb-6::GFP, instead induction of this reporter often occurs in counterpoint to activation of SKN-1, which we show is under the control of ATFS-1. In those mitochondrial bioenergetic mutants which activate Ptbb-6::GFP, we find that dlk-1, sek-3 and pmk-3 are all required for their life extension.
Mitochondrial dysfunction underlies numerous age-related pathologies. In an effort to uncover how the detrimental effects of mitochondrial dysfunction might be alleviated, we examined how the nematode C. elegans not only adapts to disruption of the mitochondrial electron transport chain, but in many instances responds with extended lifespan. Studies have shown various retrograde responses are activated in these animals, including the well-studied ATFS-1-dependent mitochondrial unfolded protein response (UPRmt). Such processes fall under the greater rubric of cellular surveillance mechanisms. Here we identify a novel p38 signaling cascade that is required to extend life when the mitochondrial electron transport chain is disrupted in worms, and which is blocked by disruption of the Mitochondrial-associated Degradation (MAD) pathway. This novel cascade is defined by DLK-1 (MAP3K), SEK-3 (MAP2K), PMK-3 (MAPK) and the reporter gene Ptbb-6::GFP. Inhibition of known mitochondrial retrograde responses does not alter induction of Ptbb-6::GFP, instead induction of this reporter often occurs in counterpoint to activation of SKN-1, which we show is under the control of ATFS-1. In those mitochondrial bioenergetic mutants which activate Ptbb-6::GFP, we find that dlk-1, sek-3 and pmk-3 are all required for their life extension.
Mitochondrial dysfunction underlies numerous age-related pathologies. In an effort to uncover how the detrimental effects of mitochondrial dysfunction might be alleviated, we examined how the nematode C. elegans not only adapts to disruption of the mitochondrial electron transport chain, but in many instances responds with extended lifespan. Studies have shown various retrograde responses are activated in these animals, including the well-studied ATFS-1-dependent mitochondrial unfolded protein response (UPR.sup.mt). Such processes fall under the greater rubric of cellular surveillance mechanisms. Here we identify a novel p38 signaling cascade that is required to extend life when the mitochondrial electron transport chain is disrupted in worms, and which is blocked by disruption of the Mitochondrial-associated Degradation (MAD) pathway. This novel cascade is defined by DLK-1 (MAP3K), SEK-3 (MAP2K), PMK-3 (MAPK) and the reporter gene Ptbb-6::GFP. Inhibition of known mitochondrial retrograde responses does not alter induction of Ptbb-6::GFP, instead induction of this reporter often occurs in counterpoint to activation of SKN-1, which we show is under the control of ATFS-1. In those mitochondrial bioenergetic mutants which activate Ptbb-6::GFP, we find that dlk-1, sek-3 and pmk-3 are all required for their life extension.
Mitochondrial dysfunction underlies numerous age-related pathologies. In an effort to uncover how the detrimental effects of mitochondrial dysfunction might be alleviated, we examined how the nematode C . elegans not only adapts to disruption of the mitochondrial electron transport chain, but in many instances responds with extended lifespan. Studies have shown various retrograde responses are activated in these animals, including the well-studied ATFS-1-dependent mitochondrial unfolded protein response (UPR mt ). Such processes fall under the greater rubric of cellular surveillance mechanisms. Here we identify a novel p38 signaling cascade that is required to extend life when the mitochondrial electron transport chain is disrupted in worms, and which is blocked by disruption of the Mitochondrial-associated Degradation (MAD) pathway. This novel cascade is defined by DLK-1 (MAP3K), SEK-3 (MAP2K), PMK-3 (MAPK) and the reporter gene Ptbb-6 :: GFP . Inhibition of known mitochondrial retrograde responses does not alter induction of Ptbb-6 :: GFP , instead induction of this reporter often occurs in counterpoint to activation of SKN-1, which we show is under the control of ATFS-1. In those mitochondrial bioenergetic mutants which activate Ptbb-6 :: GFP , we find that dlk-1 , sek-3 and pmk-3 are all required for their life extension. In humans, mitochondrial dysfunction contributes to numerous age-related diseases, and indeed even aging itself. Yet organisms also have an amazing capacity to compensate for mitochondrial impairment, paradoxically sometimes even living longer for it. This is exemplified in the roundworm Caenorhabditis elegans . In this study we examine how C . elegans with disrupted mitochondrial electron transport chains respond to such dysfunction and delineate a novel signaling cascade that is required for their life extension. Significantly, the components of this pathway are well-conserved in humans.
Audience Academic
Author Fisher, Alfred L
Borror, Megan B
Link, Christopher D
Park, Jae H
Rea, Shane L
Khan, Maruf H
Munkácsy, Erin
Lane, Rebecca K
Bokov, Alex F
AuthorAffiliation 6 Geriatric Research, Education and Clinical Center, South Texas VA Health Care System, San Antonio, Texas, United States of America
Stanford University Medical Center, UNITED STATES
7 Center for Healthy Aging, University of Texas Health Science Center at San Antonio, San Antonio, Texas, United States of America
4 Department of Medicine (Division of Geriatrics, Gerontology, and Palliative Medicine), University of Texas Health Science Center at San Antonio, San Antonio, Texas, United States of America
3 Department of Physiology, University of Texas Health Science Center at San Antonio, San Antonio, Texas, United States of America
2 Department of Cellular & Structural Biology, University of Texas Health Science Center at San Antonio, San Antonio, Texas, United States of America
1 The Barshop Institute for Longevity and Aging Studies, University of Texas Health Science Center at San Antonio, San Antonio, Texas, United States of America
8 Institute for Behavioral Genetics & Department of Integrat
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– name: 8 Institute for Behavioral Genetics & Department of Integrative Physiology, University of Colorado at Boulder, Boulder, Colorado, United States of America
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/27420916$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2016 Public Library of Science
2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Genet 12(7): e1006133. doi:10.1371/journal.pgen.1006133
2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Genet 12(7): e1006133. doi:10.1371/journal.pgen.1006133
Copyright_xml – notice: COPYRIGHT 2016 Public Library of Science
– notice: 2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Genet 12(7): e1006133. doi:10.1371/journal.pgen.1006133
– notice: 2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: . PLoS Genet 12(7): e1006133. doi:10.1371/journal.pgen.1006133
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Conceived and designed the experiments: EM SLR. Performed the experiments: EM MHK RKL MBB JHP SLR. Analyzed the data: EM MHK AFB SLR. Contributed reagents/materials/analysis tools: ALF CDL. Wrote the paper: EM SLR. Review and Editing of Manuscript: MHK ALF CDL.
The authors have declared that no competing interests exist.
ORCID 0000-0002-0255-2576
0000-0001-9436-1752
0000-0001-6451-2644
OpenAccessLink https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4946786/
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SSID ssj0035897
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Snippet Mitochondrial dysfunction underlies numerous age-related pathologies. In an effort to uncover how the detrimental effects of mitochondrial dysfunction might be...
  Mitochondrial dysfunction underlies numerous age-related pathologies. In an effort to uncover how the detrimental effects of mitochondrial dysfunction might...
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SubjectTerms Alzheimer's disease
Alzheimers disease
Animals
Bioenergetics
Biology and Life Sciences
Biosynthesis
Caenorhabditis elegans
Caenorhabditis elegans - physiology
Caenorhabditis elegans Proteins - physiology
DNA sequencing
Electron Transport
Electron Transport Chain Complex Proteins - physiology
Funding
Gene expression
Gene Expression Regulation
Genes, Reporter
Genetic aspects
Green Fluorescent Proteins - metabolism
MAP Kinase Kinase Kinases - physiology
Medicine and Health Sciences
Methods
Mitochondria
Mitochondria - metabolism
Mitochondrial DNA
Mitogen-Activated Protein Kinases - physiology
Mutation
Nematoda
Nematodes
Oxidative stress
p38 Mitogen-Activated Protein Kinases - metabolism
Pathogens
Phosphotransferases
Physiological aspects
Proteins
Research and Analysis Methods
RNA Interference
Signal Transduction
Surveillance
Unfolded Protein Response
Worms
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Title DLK-1, SEK-3 and PMK-3 Are Required for the Life Extension Induced by Mitochondrial Bioenergetic Disruption in C. elegans
URI https://www.ncbi.nlm.nih.gov/pubmed/27420916
https://www.proquest.com/docview/1812993837
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https://pubmed.ncbi.nlm.nih.gov/PMC4946786
https://doaj.org/article/52b06c2aa0d54ce68d32d730b18b2ad3
http://dx.doi.org/10.1371/journal.pgen.1006133
Volume 12
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