Swimming Exercise and Transient Food Deprivation in Caenorhabditis elegans Promote Mitochondrial Maintenance and Protect Against Chemical-Induced Mitotoxicity

Abstract Exercise and caloric restriction improve health, including reducing risk of cardiovascular disease, neurological disease, and cancer. However, molecular mechanisms underlying these protections are poorly understood, partly due to the cost and time investment of mammalian long-term diet and...

Full description

Bibliographic Details
Main Authors: Jessica H. Hartman, Latasha L. Smith, Kacy L. Gordon, Ricardo Laranjeiro, Monica Driscoll, David R. Sherwood, Joel N. Meyer
Format: Article
Language:English
Published: Nature Portfolio 2018-05-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-018-26552-9
_version_ 1818993686647668736
author Jessica H. Hartman
Latasha L. Smith
Kacy L. Gordon
Ricardo Laranjeiro
Monica Driscoll
David R. Sherwood
Joel N. Meyer
author_facet Jessica H. Hartman
Latasha L. Smith
Kacy L. Gordon
Ricardo Laranjeiro
Monica Driscoll
David R. Sherwood
Joel N. Meyer
author_sort Jessica H. Hartman
collection DOAJ
description Abstract Exercise and caloric restriction improve health, including reducing risk of cardiovascular disease, neurological disease, and cancer. However, molecular mechanisms underlying these protections are poorly understood, partly due to the cost and time investment of mammalian long-term diet and exercise intervention studies. We subjected Caenorhabditis elegans nematodes to a 6-day, twice daily swimming exercise regimen, during which time the animals also experienced brief, transient food deprivation. Accordingly, we included a non-exercise group with the same transient food deprivation, a non-exercise control with ad libitum access to food, and a group that exercised in food-containing medium. Following these regimens, we assessed mitochondrial health and sensitivity to mitochondrial toxicants. Exercise protected against age-related decline in mitochondrial morphology in body-wall muscle. Food deprivation increased organismal basal respiration; however, exercise was the sole intervention that increased spare respiratory capacity and proton leak. We observed increased lifespan in exercised animals compared to both control and transiently food-deprived nematodes. Finally, exercised animals (and to a lesser extent, transiently food-deprived animals) were markedly protected against lethality from acute exposures to the mitotoxicants rotenone and arsenic. Thus, swimming exercise and brief food deprivation provide effective intervention in C. elegans, protecting from age-associated mitochondrial decline and providing resistance to mitotoxicant exposures.
first_indexed 2024-12-20T20:46:00Z
format Article
id doaj.art-72d3f1ab341c44bab535ac51b4bbcded
institution Directory Open Access Journal
issn 2045-2322
language English
last_indexed 2024-12-20T20:46:00Z
publishDate 2018-05-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj.art-72d3f1ab341c44bab535ac51b4bbcded2022-12-21T19:27:03ZengNature PortfolioScientific Reports2045-23222018-05-018111610.1038/s41598-018-26552-9Swimming Exercise and Transient Food Deprivation in Caenorhabditis elegans Promote Mitochondrial Maintenance and Protect Against Chemical-Induced MitotoxicityJessica H. Hartman0Latasha L. Smith1Kacy L. Gordon2Ricardo Laranjeiro3Monica Driscoll4David R. Sherwood5Joel N. Meyer6Nicholas School of the Environment, Duke UniversityDepartment of Pharmacology and Cancer Biology, Duke UniversityDepartment of Biology, Duke UniversityDepartment of Molecular Biology and Biochemistry, Nelson Biological Laboratories, Rutgers, The State University of New JerseyDepartment of Molecular Biology and Biochemistry, Nelson Biological Laboratories, Rutgers, The State University of New JerseyDepartment of Biology, Duke UniversityNicholas School of the Environment, Duke UniversityAbstract Exercise and caloric restriction improve health, including reducing risk of cardiovascular disease, neurological disease, and cancer. However, molecular mechanisms underlying these protections are poorly understood, partly due to the cost and time investment of mammalian long-term diet and exercise intervention studies. We subjected Caenorhabditis elegans nematodes to a 6-day, twice daily swimming exercise regimen, during which time the animals also experienced brief, transient food deprivation. Accordingly, we included a non-exercise group with the same transient food deprivation, a non-exercise control with ad libitum access to food, and a group that exercised in food-containing medium. Following these regimens, we assessed mitochondrial health and sensitivity to mitochondrial toxicants. Exercise protected against age-related decline in mitochondrial morphology in body-wall muscle. Food deprivation increased organismal basal respiration; however, exercise was the sole intervention that increased spare respiratory capacity and proton leak. We observed increased lifespan in exercised animals compared to both control and transiently food-deprived nematodes. Finally, exercised animals (and to a lesser extent, transiently food-deprived animals) were markedly protected against lethality from acute exposures to the mitotoxicants rotenone and arsenic. Thus, swimming exercise and brief food deprivation provide effective intervention in C. elegans, protecting from age-associated mitochondrial decline and providing resistance to mitotoxicant exposures.https://doi.org/10.1038/s41598-018-26552-9
spellingShingle Jessica H. Hartman
Latasha L. Smith
Kacy L. Gordon
Ricardo Laranjeiro
Monica Driscoll
David R. Sherwood
Joel N. Meyer
Swimming Exercise and Transient Food Deprivation in Caenorhabditis elegans Promote Mitochondrial Maintenance and Protect Against Chemical-Induced Mitotoxicity
Scientific Reports
title Swimming Exercise and Transient Food Deprivation in Caenorhabditis elegans Promote Mitochondrial Maintenance and Protect Against Chemical-Induced Mitotoxicity
title_full Swimming Exercise and Transient Food Deprivation in Caenorhabditis elegans Promote Mitochondrial Maintenance and Protect Against Chemical-Induced Mitotoxicity
title_fullStr Swimming Exercise and Transient Food Deprivation in Caenorhabditis elegans Promote Mitochondrial Maintenance and Protect Against Chemical-Induced Mitotoxicity
title_full_unstemmed Swimming Exercise and Transient Food Deprivation in Caenorhabditis elegans Promote Mitochondrial Maintenance and Protect Against Chemical-Induced Mitotoxicity
title_short Swimming Exercise and Transient Food Deprivation in Caenorhabditis elegans Promote Mitochondrial Maintenance and Protect Against Chemical-Induced Mitotoxicity
title_sort swimming exercise and transient food deprivation in caenorhabditis elegans promote mitochondrial maintenance and protect against chemical induced mitotoxicity
url https://doi.org/10.1038/s41598-018-26552-9
work_keys_str_mv AT jessicahhartman swimmingexerciseandtransientfooddeprivationincaenorhabditiseleganspromotemitochondrialmaintenanceandprotectagainstchemicalinducedmitotoxicity
AT latashalsmith swimmingexerciseandtransientfooddeprivationincaenorhabditiseleganspromotemitochondrialmaintenanceandprotectagainstchemicalinducedmitotoxicity
AT kacylgordon swimmingexerciseandtransientfooddeprivationincaenorhabditiseleganspromotemitochondrialmaintenanceandprotectagainstchemicalinducedmitotoxicity
AT ricardolaranjeiro swimmingexerciseandtransientfooddeprivationincaenorhabditiseleganspromotemitochondrialmaintenanceandprotectagainstchemicalinducedmitotoxicity
AT monicadriscoll swimmingexerciseandtransientfooddeprivationincaenorhabditiseleganspromotemitochondrialmaintenanceandprotectagainstchemicalinducedmitotoxicity
AT davidrsherwood swimmingexerciseandtransientfooddeprivationincaenorhabditiseleganspromotemitochondrialmaintenanceandprotectagainstchemicalinducedmitotoxicity
AT joelnmeyer swimmingexerciseandtransientfooddeprivationincaenorhabditiseleganspromotemitochondrialmaintenanceandprotectagainstchemicalinducedmitotoxicity