Independent genomewide screens identify the tumor suppressor VTRNA2-1 as a human epiallele responsive to periconceptional environment

Background Interindividual epigenetic variation that occurs systemically must be established prior to gastrulation in the very early embryo and, because it is systemic, can be assessed in easily biopsiable tissues. We employ two independent genome-wide approaches to search for such variants. Results...

Full description

Bibliographic Details
Main Authors: Silver, M.J., Kessler, N.J., Hennig, B.J., Domínguez Salas, Paula, Laritsky, E., Baker, M.S., Coarfa, C., Hernández Vargas, H., Castelino, J.M., Routledge, M.N., Yun Yun Gong, Herceg, Z., Yong Sun Lee, Kwanbok Lee, Moore, S.E., Fulford, A.J., Prentice, A.M., Waterland, R.A.
Format: Journal Article
Language:Inglés
Published: Springer 2015
Subjects:
Online Access:https://hdl.handle.net/10568/68020
_version_ 1855515501509214208
author Silver, M.J.
Kessler, N.J.
Hennig, B.J.
Domínguez Salas, Paula
Laritsky, E.
Baker, M.S.
Coarfa, C.
Hernández Vargas, H.
Castelino, J.M.
Routledge, M.N.
Yun Yun Gong
Herceg, Z.
Yong Sun Lee
Kwanbok Lee
Moore, S.E.
Fulford, A.J.
Prentice, A.M.
Waterland, R.A.
author_browse Baker, M.S.
Castelino, J.M.
Coarfa, C.
Domínguez Salas, Paula
Fulford, A.J.
Hennig, B.J.
Herceg, Z.
Hernández Vargas, H.
Kessler, N.J.
Kwanbok Lee
Laritsky, E.
Moore, S.E.
Prentice, A.M.
Routledge, M.N.
Silver, M.J.
Waterland, R.A.
Yong Sun Lee
Yun Yun Gong
author_facet Silver, M.J.
Kessler, N.J.
Hennig, B.J.
Domínguez Salas, Paula
Laritsky, E.
Baker, M.S.
Coarfa, C.
Hernández Vargas, H.
Castelino, J.M.
Routledge, M.N.
Yun Yun Gong
Herceg, Z.
Yong Sun Lee
Kwanbok Lee
Moore, S.E.
Fulford, A.J.
Prentice, A.M.
Waterland, R.A.
author_sort Silver, M.J.
collection Repository of Agricultural Research Outputs (CGSpace)
description Background Interindividual epigenetic variation that occurs systemically must be established prior to gastrulation in the very early embryo and, because it is systemic, can be assessed in easily biopsiable tissues. We employ two independent genome-wide approaches to search for such variants. Results First, we screen for metastable epialleles by performing genomewide bisulfite sequencing in peripheral blood lymphocyte (PBL) and hair follicle DNA from two Caucasian adults. Second, we conduct a genomewide screen for genomic regions at which PBL DNA methylation is affected by season of conception in rural Gambia. Remarkably, both approaches identify the genomically imprinted VTRNA2-1 as a top environmentally responsive epiallele. We demonstrate systemic and stochastic interindividual variation in DNA methylation at the VTRNA2-1 differentially methylated region in healthy Caucasian and Asian adults and show, in rural Gambians, that periconceptional environment affects offspring VTRNA2-1 epigenotype, which is stable over at least 10 years. This unbiased screen also identifies over 100 additional candidate metastable epialleles, and shows that these are associated with cis genomic features including transposable elements. Conclusions The non-coding VTRNA2-1 transcript (also called nc886) is a putative tumor suppressor and modulator of innate immunity. Thus, these data indicating environmentally induced loss of imprinting at VTRNA2-1 constitute a plausible causal pathway linking early embryonic environment, epigenetic alteration, and human disease. More broadly, the list of candidate metastable epialleles provides a resource for future studies of epigenetic variation and human disease.
format Journal Article
id CGSpace68020
institution CGIAR Consortium
language Inglés
publishDate 2015
publishDateRange 2015
publishDateSort 2015
publisher Springer
publisherStr Springer
record_format dspace
spelling CGSpace680202023-12-08T19:36:04Z Independent genomewide screens identify the tumor suppressor VTRNA2-1 as a human epiallele responsive to periconceptional environment Silver, M.J. Kessler, N.J. Hennig, B.J. Domínguez Salas, Paula Laritsky, E. Baker, M.S. Coarfa, C. Hernández Vargas, H. Castelino, J.M. Routledge, M.N. Yun Yun Gong Herceg, Z. Yong Sun Lee Kwanbok Lee Moore, S.E. Fulford, A.J. Prentice, A.M. Waterland, R.A. research health Background Interindividual epigenetic variation that occurs systemically must be established prior to gastrulation in the very early embryo and, because it is systemic, can be assessed in easily biopsiable tissues. We employ two independent genome-wide approaches to search for such variants. Results First, we screen for metastable epialleles by performing genomewide bisulfite sequencing in peripheral blood lymphocyte (PBL) and hair follicle DNA from two Caucasian adults. Second, we conduct a genomewide screen for genomic regions at which PBL DNA methylation is affected by season of conception in rural Gambia. Remarkably, both approaches identify the genomically imprinted VTRNA2-1 as a top environmentally responsive epiallele. We demonstrate systemic and stochastic interindividual variation in DNA methylation at the VTRNA2-1 differentially methylated region in healthy Caucasian and Asian adults and show, in rural Gambians, that periconceptional environment affects offspring VTRNA2-1 epigenotype, which is stable over at least 10 years. This unbiased screen also identifies over 100 additional candidate metastable epialleles, and shows that these are associated with cis genomic features including transposable elements. Conclusions The non-coding VTRNA2-1 transcript (also called nc886) is a putative tumor suppressor and modulator of innate immunity. Thus, these data indicating environmentally induced loss of imprinting at VTRNA2-1 constitute a plausible causal pathway linking early embryonic environment, epigenetic alteration, and human disease. More broadly, the list of candidate metastable epialleles provides a resource for future studies of epigenetic variation and human disease. 2015-12 2015-08-24T20:53:16Z 2015-08-24T20:53:16Z Journal Article https://hdl.handle.net/10568/68020 en Open Access Springer Silver, M.J., Kessler, N.J., Hennig, B.J., Dominguez-Salas, P., Laritsky, E., Baker, M.S., Coarfa, C., Hernandez-Vargas, H., Castelino, J.M., Routledge, M.N., Yun Yun Gong, Herceg, Z., Yong Sun Lee, Kwanbok Lee, Moore, S.E., Fulford, A.J., Prentice, A.M. and Waterland, R.A. 2015. Independent genomewide screens identify the tumor suppressor VTRNA2-1 as a human epiallele responsive to periconceptional environment. Genome Biology 16:118
spellingShingle research
health
Silver, M.J.
Kessler, N.J.
Hennig, B.J.
Domínguez Salas, Paula
Laritsky, E.
Baker, M.S.
Coarfa, C.
Hernández Vargas, H.
Castelino, J.M.
Routledge, M.N.
Yun Yun Gong
Herceg, Z.
Yong Sun Lee
Kwanbok Lee
Moore, S.E.
Fulford, A.J.
Prentice, A.M.
Waterland, R.A.
Independent genomewide screens identify the tumor suppressor VTRNA2-1 as a human epiallele responsive to periconceptional environment
title Independent genomewide screens identify the tumor suppressor VTRNA2-1 as a human epiallele responsive to periconceptional environment
title_full Independent genomewide screens identify the tumor suppressor VTRNA2-1 as a human epiallele responsive to periconceptional environment
title_fullStr Independent genomewide screens identify the tumor suppressor VTRNA2-1 as a human epiallele responsive to periconceptional environment
title_full_unstemmed Independent genomewide screens identify the tumor suppressor VTRNA2-1 as a human epiallele responsive to periconceptional environment
title_short Independent genomewide screens identify the tumor suppressor VTRNA2-1 as a human epiallele responsive to periconceptional environment
title_sort independent genomewide screens identify the tumor suppressor vtrna2 1 as a human epiallele responsive to periconceptional environment
topic research
health
url https://hdl.handle.net/10568/68020
work_keys_str_mv AT silvermj independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT kesslernj independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT hennigbj independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT dominguezsalaspaula independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT laritskye independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT bakerms independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT coarfac independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT hernandezvargash independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT castelinojm independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT routledgemn independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT yunyungong independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT hercegz independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT yongsunlee independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT kwanboklee independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT moorese independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT fulfordaj independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT prenticeam independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment
AT waterlandra independentgenomewidescreensidentifythetumorsuppressorvtrna21asahumanepialleleresponsivetopericonceptionalenvironment