Environmentally induced transgenerational epigenetic reprogramming of primordial germ cells and the subsequent germ line

Michael K Skinner; Carlos Guerrero-Bosagna; M Haque; Eric Nilsson; Ramji Bhandari; John R McCarrey

doi:10.1371/journal.pone.0066318

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Environmentally induced transgenerational epigenetic reprogramming of primordial germ cells and the subsequent germ line

Journal article

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Environmentally induced transgenerational epigenetic reprogramming of primordial germ cells and the subsequent germ line

Michael K Skinner, Carlos Guerrero-Bosagna, M Haque, Eric Nilsson, Ramji Bhandari and John R McCarrey

PloS one, Vol.8(7), pp.e66318-e66318

2013

DOI: https://doi.org/10.1371/journal.pone.0066318

Handle:

https://hdl.handle.net/2376/105444

PMCID: PMC3712023

PMID: 23869203

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Abstract

Prenatal Exposure Delayed Effects

Gene Expression Regulation, Developmental - drug effects

Fungicides, Industrial - toxicity

Gene Expression Profiling

Transcriptome - drug effects

Germ Cells

RNA, Messenger - metabolism

Rats, Sprague-Dawley

Oxazoles - toxicity

Sex Determination Processes - drug effects

Epigenesis, Genetic - drug effects

Models, Genetic

DNA Methylation - drug effects

Epigenetics

Pregnancy

A number of environmental factors (e.g. toxicants) have been shown to promote the epigenetic transgenerational inheritance of disease and phenotypic variation. Transgenerational inheritance requires the germline transmission of altered epigenetic information between generations in the absence of direct environmental exposures. The primary periods for epigenetic programming of the germ line are those associated with primordial germ cell development and subsequent fetal germline development. The current study examined the actions of an agricultural fungicide vinclozolin on gestating female (F0 generation) progeny in regards to the primordial germ cell (PGC) epigenetic reprogramming of the F3 generation (i.e. great-grandchildren). The F3 generation germline transcriptome and epigenome (DNA methylation) were altered transgenerationally. Interestingly, disruptions in DNA methylation patterns and altered transcriptomes were distinct between germ cells at the onset of gonadal sex determination at embryonic day 13 (E13) and after cord formation in the testis at embryonic day 16 (E16). A larger number of DNA methylation abnormalities (epimutations) and transcriptional alterations were observed in the E13 germ cells than in the E16 germ cells. These observations indicate that altered transgenerational epigenetic reprogramming and function of the male germline is a component of vinclozolin induced epigenetic transgenerational inheritance of disease. Insights into the molecular control of germline transmitted epigenetic inheritance are provided.

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Title: Environmentally induced transgenerational epigenetic reprogramming of primordial germ cells and the subsequent germ line
Creators: Michael K Skinner - Washington State University, Center for Reproductive Biology
Carlos Guerrero-Bosagna
M Haque
Eric Nilsson
Ramji Bhandari
John R McCarrey
Publication Details: PloS one, Vol.8(7), pp.e66318-e66318
Academic Unit: Biological Sciences, School of
Publisher: Public Library Science; United States
Number of pages: 15
Grant note: NIH NIEHS; United States Department of Health & Human Services; National Institutes of Health (NIH) - USA; NIH National Institute of Environmental Health Sciences (NIEHS)
Identifiers: 99900546931301842
Language: English
Resource Type: Journal article