Ancestral vinclozolin exposure alters the epigenetic transgenerational inheritance of sperm small noncoding RNAs

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Abstract

Exposure to the agricultural fungicide vinclozolin during gestation promotes a higher incidence of various diseases in the subsequent unexposed F3 and F4 generations. This phenomenon is termed epigenetic transgenerational inheritance and has been shown to in part involve alterations in DNA methylation, but the role of other epigenetic mechanisms remains unknown. The current study investigated the alterations in small noncoding RNA (sncRNA) in the sperm from F3 generation control and vinclozolin lineage rats. Over 200 differentially expressed sncRNAs were identified and the tRNA-derived sncRNAs, namely 5′ halves of mature tRNAs (5′ halves), displayed the most dramatic changes. Gene targets of the altered miRNAs and tRNA 5′ halves revealed associations between the altered sncRNAs and differentially DNA methylated regions. Dysregulated sncRNAs appear to correlate with mRNA profiles associated with the previously observed vinclozolin-induced disease phenotypes. Data suggest potential connections between sperm-borne RNAs and the vinclozolin-induced epigenetic transgenerational inheritance phenomenon.

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Most cited references 32

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DAVID: Database for Annotation, Visualization, and Integrated Discovery.

Glynn Dennis, Brad T. Sherman, Douglas A Hosack … (2003)

Functional annotation of differentially expressed genes is a necessary and critical step in the analysis of microarray data. The distributed nature of biological knowledge frequently requires researchers to navigate through numerous web-accessible databases gathering information one gene at a time. A more judicious approach is to provide query-based access to an integrated database that disseminates biologically rich information across large datasets and displays graphic summaries of functional information. Database for Annotation, Visualization, and Integrated Discovery (DAVID; http://www.david.niaid.nih.gov) addresses this need via four web-based analysis modules: 1) Annotation Tool - rapidly appends descriptive data from several public databases to lists of genes; 2) GoCharts - assigns genes to Gene Ontology functional categories based on user selected classifications and term specificity level; 3) KeggCharts - assigns genes to KEGG metabolic processes and enables users to view genes in the context of biochemical pathway maps; and 4) DomainCharts - groups genes according to PFAM conserved protein domains. Analysis results and graphical displays remain dynamically linked to primary data and external data repositories, thereby furnishing in-depth as well as broad-based data coverage. The functionality provided by DAVID accelerates the analysis of genome-scale datasets by facilitating the transition from data collection to biological meaning.

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GtRNAdb: a database of transfer RNA genes detected in genomic sequence

Patricia P. Chan, Todd Lowe (2009)

Transfer RNAs (tRNAs) represent the single largest, best-understood class of non-protein coding RNA genes found in all living organisms. By far, the major source of new tRNAs is computational identification of genes within newly sequenced genomes. To organize the rapidly growing collection and enable systematic analyses, we created the Genomic tRNA Database (GtRNAdb), currently including over 74 000 tRNA genes predicted from 740 species. The web resource provides overview statistics of tRNA genes within each analyzed genome, including information by isotype and genetic locus, easily downloadable primary sequences, graphical secondary structures and multiple sequence alignments. Direct links for each gene to UCSC eukaryotic and microbial genome browsers provide graphical display of tRNA genes in the context of all other local genetic information. The database can be searched by primary sequence similarity, tRNA characteristics or phylogenetic group. The database is publicly available at http://gtrnadb.ucsc.edu.

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RNA methylation by Dnmt2 protects transfer RNAs against stress-induced cleavage.

Matthias Schaefer, Tim Pollex, Katharina Hanna … (2010)

Dnmt2 proteins are the most conserved members of the DNA methyltransferase enzyme family, but their substrate specificity and biological functions have been a subject of controversy. We show here that, in addition to tRNA(Asp-GTC), tRNA(Val-AAC) and tRNA(Gly-GCC) are also methylated by Dnmt2. Drosophila Dnmt2 mutants showed reduced viability under stress conditions, and Dnmt2 relocalized to stress granules following heat shock. Strikingly, stress-induced cleavage of tRNAs was Dnmt2-dependent, and Dnmt2-mediated methylation protected tRNAs against ribonuclease cleavage. These results uncover a novel biological function of Dnmt2-mediated tRNA methylation, and suggest a role for Dnmt2 enzymes during the biogenesis of tRNA-derived small RNAs.

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Author and article information

Journal

Journal ID (nlm-journal-id): 101675941

Journal ID (pubmed-jr-id): 44874

Journal ID (nlm-ta): Environ Epigenet

Journal ID (iso-abbrev): Environ Epigenet

Title: Environmental epigenetics

ISSN (Electronic): 2058-5888

Publication date Nihms-submitted: 15 March 2016

Publication date (Electronic): 9 March 2016

Publication date (Print): 2016

Publication date PMC-release: 05 July 2016

Volume: 2

Issue: 1

Electronic Location Identifier: dvw001

Affiliations

[1 ]Department of Physiology and Cell Biology, University of Nevada, Reno, NV 89557-0330, USA

[2 ]Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA

Author notes

[* ]Correspondence and requests for materials should be addressed to skinner@ 123456wsu.edu or wyan@ 123456medicine.nevada.edu , Correspondence address. Center for Reproductive Biology, School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA. Tel: +509-335-1524; Fax: +509-335-2176

[‡]

These authors contributed equally to the study.

[†]

Wei Yan, http://orcid.org/0000-0001-9569-9026

Article

Manuscript ID: NIHMS768196

DOI: 10.1093/eep/dvw001

PMC ID: 4933025

PubMed ID: 27390623

SO-VID: fdf8ca69-9c23-4b7e-9f4f-bd5d7deeca26

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This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@ 123456oup.com

Ancestral vinclozolin exposure alters the epigenetic transgenerational inheritance of sperm small noncoding RNAs

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Most cited references 32

DAVID: Database for Annotation, Visualization, and Integrated Discovery.

GtRNAdb: a database of transfer RNA genes detected in genomic sequence

RNA methylation by Dnmt2 protects transfer RNAs against stress-induced cleavage.

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