Transgenerational effects of alcohol on behavioral sensitivity to alcohol in Caenorhabditis elegans

Alcohol abuse and dependence have a substantial heritable component. Although the genome has been considered the sole vehicle of heritable phenotypes, recent studies suggest that drug or alcohol exposure may induce alterations in gene expression that are transmitted across generations. Still, the tr...

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Bibliographic Details
Published in:PloS one 2022-10, Vol.17 (10), p.e0271849
Main Authors: Guzman, Dawn M, Chakka, Keerthana, Shi, Ted, Marron, Alyssa, Fiorito, Ansley E, Rahman, Nima S, Ro, Stephanie, Sucich, Dylan G, Pierce, Jonathan T
Format: Article
Language:English
Subjects:
Alcohol
Alcohol abuse
Alcohol Drinking
Alcohol use
Alcoholic beverages
Alcohols
Animal models
Animals
Bacteria
Biology and Life Sciences
Caenorhabditis elegans
Caenorhabditis elegans - physiology
DNA methylation
Drug abuse
Epigenetics
Ethanol
Ethanol - toxicity
Fertilization
Gene expression
Genetic aspects
Genomes
Health aspects
Heterogeneity
Hypersensitivity
Intoxication
Medicine and Health Sciences
Nematodes
Offspring
Paradigms
Phenotypes
Physical Sciences
Progeny
Properties
Reproduction
Research and Analysis Methods
Sensitivity
Worms
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Summary:Alcohol abuse and dependence have a substantial heritable component. Although the genome has been considered the sole vehicle of heritable phenotypes, recent studies suggest that drug or alcohol exposure may induce alterations in gene expression that are transmitted across generations. Still, the transgenerational impact of alcohol use (and abuse) remains largely unexplored in part because multigenerational studies using rodent models present challenges for time, sample size, and genetic heterogeneity. Here, we took advantage of the extremely short generation time, large broods, and clonal form of reproduction of the nematode Caenorhabditis elegans. We developed a model of pre-fertilization parental alcohol exposure to test alterations in behavioral responses to acute alcohol treatment (referred to in short as intoxication) in subsequent F1, F2 and F3 generations. We found that chronic and intermittent alcohol-treatment paradigms resulted in opposite changes to intoxication sensitivity of F3 progeny that were only apparent when controlling for yoked trials. Chronic alcohol-treatment paradigm in the parental generation resulted in alcohol-naïve F3 progeny displaying moderate resistance to intoxication. Intermittent treatment resulted in alcohol-naïve F3 progeny displaying moderate hypersensitivity to intoxication. Further study of these phenomena using this new C. elegans model may yield mechanistic insights into how transgenerational effects may occur in other animals.
ISSN:1932-6203
1932-6203
DOI:10.1371/journal.pone.0271849