Cited by 168Mitochondrial Function and PathologyAutism Spectrum Disorder ResearchAutophagy in Disease and Therapy

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Oxidative Stress Induces Mitochondrial Dysfunction in a Subset of Autism Lymphoblastoid Cell Lines in a Well-Matched Case Control Cohort

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Rose, Shannon, Frye, Richard E., Slattery, John, Wynne, Rebecca, Tippett, Marie, Pavliv, Oleksandra, Melnyk, Stepan, James, S. Jill·2014·PLoS ONE

DOI 10.1371/journal.pone.0085436PMC PMC3885720

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Abstract

There is increasing recognition that mitochondrial dysfunction is associated with the autism spectrum disorders. However, little attention has been given to the etiology of mitochondrial dysfunction or how mitochondrial abnormalities might interact with other physiological disturbances associated with autism, such as oxidative stress. In the current study we used respirometry to examine reserve capacity, a measure of the mitochondrial ability to respond to physiological stress, in lymphoblastoid cell lines (LCLs) derived from children with autistic disorder (AD) as well as age and gender-matched control LCLs. We demonstrate, for the first time, that LCLs derived from children with AD have an abnormal mitochondrial reserve capacity before and after exposure to increasingly higher concentrations of 2,3-dimethoxy-1,4-napthoquinone (DMNQ), an agent that increases intracellular reactive oxygen species (ROS). Specifically, the AD LCLs exhibit a higher reserve capacity at baseline and a sharper depletion of reserve capacity when ROS exposure is increased, as compared to control LCLs. Detailed investigation indicated that reserve capacity abnormalities seen in AD LCLs were the result of higher ATP-linked respiration and maximal respiratory capacity at baseline combined with a marked increase in proton leak respiration as ROS was increased. We further demonstrate that these reserve capacity abnormalities are driven by a subgroup of eight (32%) of 25 AD LCLs. Additional investigation of this subgroup of AD LCLs with reserve capacity abnormalities revealed that it demonstrated a greater reliance on glycolysis and on uncoupling protein 2 to regulate oxidative stress at the inner mitochondria membrane. This study suggests that a significant subgroup of AD children may have alterations in mitochondrial function which could render them more vulnerable to a pro-oxidant microenvironment derived from intrinsic and extrinsic sources of ROS such as immune activation and pro-oxidant environmental toxicants. These findings are consistent with the notion that AD is caused by a combination of genetic and environmental factors.

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Additional file 3 of Cholic and deoxycholic acids induce mitochondrial dysfunction, impaired biogenesis and autophagic flux in skeletal muscle cells
Ábrigo, J., Olguín, H. C., Tacchi, F., Orozco-Aguilar, J., Valero‐Breton, M., Soto, J., Castro‐Sepúlveda, M., Elorza, Á. A., Simon, F., & Cabello‐Verrugio, C. (2024) · Figshare · doi:10.6084/m9.figshare.26595605
Additional file 2 of Cholic and deoxycholic acids induce mitochondrial dysfunction, impaired biogenesis and autophagic flux in skeletal muscle cells
Ábrigo, J., Olguín, H. C., Tacchi, F., Orozco-Aguilar, J., Valero‐Breton, M., Soto, J., Castro‐Sepúlveda, M., Elorza, Á. A., Simon, F., & Cabello‐Verrugio, C. (2024) · Figshare · doi:10.6084/m9.figshare.26595602
Additional file 1 of Cholic and deoxycholic acids induce mitochondrial dysfunction, impaired biogenesis and autophagic flux in skeletal muscle cells
Ábrigo, J., Olguín, H. C., Tacchi, F., Orozco-Aguilar, J., Valero‐Breton, M., Soto, J., Castro‐Sepúlveda, M., Elorza, Á. A., Simon, F., & Cabello‐Verrugio, C. (2024) · Figshare · doi:10.6084/m9.figshare.26595599
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Authors: Rose, S., Frye, R. E., Slattery, J., Wynne, R., Tippett, M., Pavliv, O., Melnyk, S., & James, S. J.
Affiliations: Arkansas Children's Hospital (US)
Corresponding author: Frye, Richard E.
ORCID: Rose, Shannon
Frye, Richard E.
Slattery, John
Pavliv, Oleksandra
Melnyk, Stepan
James, S. Jill
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2014-01-08
Volume: 9
Issue: 1
Pages: e85436
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0085436
PMC: PMC3885720
OpenAlex: W2163485668
Cited by: 168
References: 61
Citations by year: 2026: 9 · 2025: 9 · 2024: 20 · 2023: 7 · 2022: 22 · 2021: 17 · 2020: 18 · 2019: 9 · 2018: 10 · 2017: 12 · 2016: 13 · 2015: 16 · 2014: 6
FWCI: 6.42
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: PLoS ONE (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: Arkansas Biosciences Institute
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Keywords: autism spectrum disorder, mitochondrial dysfunction, oxidative stress, reserve capacity, lymphoblastoid cell lines, reactive oxygen species, UCP2, glycolysis, ATP-linked respiration, mitochondrial heterogeneity
MeSH terms: Uncoupling Protein 2, Autistic Disorder, Cell Line, Child, Child, Preschool, Female, Glycolysis, Humans, Ion Channels, Lymphocytes, Male, Mitochondria, Naphthoquinones, Oxidation-Reduction, Protons, Case-Control Studies, Reactive Oxygen Species, Oxidative Stress, Cell Respiration, Mitochondrial Proteins, Mitochondrial Membranes

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Oxidative Stress Induces Mitochondrial Dysfunction in a Subset of Autism Lymphoblastoid Cell Lines in a Well-Matched Case Control Cohort

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