Altered non-coding RNA expression profile in F1 progeny 1 year after parental irradiation is linked to adverse effects in zebrafish

Leonardo Martín; Jorke H. Kamstra; Selma Hurem; Leif C. Lindeman; Dag A. Brede; Håvard Aanes; Igor Babiak; Amilcar Arenal; Deborah Oughton; Brit Salbu; Jan Ludvig Lyche; Peter Aleström

doi:10.1038/s41598-021-83345-3

Altered non-coding RNA expression profile in F₁ progeny 1 year after parental irradiation is linked to adverse effects in zebrafish

Leonardo Martín^*
, Jorke H. Kamstra
, Selma Hurem
, Leif C. Lindeman
, Dag A. Brede
, Håvard Aanes
, Igor Babiak
, Amilcar Arenal
, Deborah Oughton
, Brit Salbu
, Jan Ludvig Lyche
, Peter Aleström

^*Corresponding author for this work

IRAS OH Toxicology

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Gamma radiation produces DNA instability and impaired phenotype. Previously, we observed negative effects on phenotype, DNA methylation, and gene expression profiles, in offspring of zebrafish exposed to gamma radiation during gametogenesis. We hypothesize that previously observed effects are accompanied with changes in the expression profile of non-coding RNAs, inherited by next generations. Non-coding RNA expression profile was analysed in F₁ offspring (5.5 h post-fertilization) by high-throughput sequencing 1 year after parental irradiation (8.7 mGy/h, 5.2 Gy total dose). Using our previous F₁-γ genome-wide gene expression data (GSE98539), hundreds of mRNAs were predicted as targets of differentially expressed (DE) miRNAs, involved in pathways such as insulin receptor, NFkB and PTEN signalling, linking to apoptosis and cancer. snRNAs belonging to the five major spliceosomal snRNAs were down-regulated in the F₁-γ group, Indicating transcriptional and post-transcriptional alterations. In addition, DEpiRNA clusters were associated to 9 transposable elements (TEs) (LTR, LINE, and TIR) (p = 0.0024), probable as a response to the activation of these TEs. Moreover, the expression of the lincRNAs malat-1, and several others was altered in the offspring F₁, in concordance with previously observed phenotypical alterations. In conclusion, our results demonstrate diverse gamma radiation-induced alterations in the ncRNA profiles of F₁ offspring observable 1 year after parental irradiation.

Original language	English
Article number	4142
Number of pages	17
Journal	Scientific Reports
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41598-021-83345-3
Publication status	Published - 18 Feb 2021

Bibliographical note

Funding Information:
This research work was supported by the Norwegian Research Council funded through the Centre of Excellence CERAD–Centre for Environmental Radioactivity (project 223268/F50).

Publisher Copyright:
© 2021, The Author(s).

Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.

Funding

This research work was supported by the Norwegian Research Council funded through the Centre of Excellence CERAD–Centre for Environmental Radioactivity (project 223268/F50).

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1038/s41598-021-83345-3Licence: CC BY

s41598-021-83345-3Final published version, 1.9 MBLicence: CC BY

Cite this

Martín, L., Kamstra, J. H., Hurem, S., Lindeman, L. C., Brede, D. A., Aanes, H., Babiak, I., Arenal, A., Oughton, D., Salbu, B., Lyche, J. L., & Aleström, P. (2021). Altered non-coding RNA expression profile in F₁ progeny 1 year after parental irradiation is linked to adverse effects in zebrafish. Scientific Reports, 11(1), Article 4142. https://doi.org/10.1038/s41598-021-83345-3

@article{fe7804049ec04085b638e56f5002e8eb,

title = "Altered non-coding RNA expression profile in F1 progeny 1 year after parental irradiation is linked to adverse effects in zebrafish",

abstract = "Gamma radiation produces DNA instability and impaired phenotype. Previously, we observed negative effects on phenotype, DNA methylation, and gene expression profiles, in offspring of zebrafish exposed to gamma radiation during gametogenesis. We hypothesize that previously observed effects are accompanied with changes in the expression profile of non-coding RNAs, inherited by next generations. Non-coding RNA expression profile was analysed in F1 offspring (5.5 h post-fertilization) by high-throughput sequencing 1 year after parental irradiation (8.7 mGy/h, 5.2 Gy total dose). Using our previous F1-γ genome-wide gene expression data (GSE98539), hundreds of mRNAs were predicted as targets of differentially expressed (DE) miRNAs, involved in pathways such as insulin receptor, NFkB and PTEN signalling, linking to apoptosis and cancer. snRNAs belonging to the five major spliceosomal snRNAs were down-regulated in the F1-γ group, Indicating transcriptional and post-transcriptional alterations. In addition, DEpiRNA clusters were associated to 9 transposable elements (TEs) (LTR, LINE, and TIR) (p = 0.0024), probable as a response to the activation of these TEs. Moreover, the expression of the lincRNAs malat-1, and several others was altered in the offspring F1, in concordance with previously observed phenotypical alterations. In conclusion, our results demonstrate diverse gamma radiation-induced alterations in the ncRNA profiles of F1 offspring observable 1 year after parental irradiation.",

author = "Leonardo Mart{\'i}n and Kamstra, \{Jorke H.\} and Selma Hurem and Lindeman, \{Leif C.\} and Brede, \{Dag A.\} and H{\aa}vard Aanes and Igor Babiak and Amilcar Arenal and Deborah Oughton and Brit Salbu and Lyche, \{Jan Ludvig\} and Peter Alestr{\"o}m",

note = "Funding Information: This research work was supported by the Norwegian Research Council funded through the Centre of Excellence CERAD–Centre for Environmental Radioactivity (project 223268/F50). Publisher Copyright: {\textcopyright} 2021, The Author(s). Copyright: Copyright 2021 Elsevier B.V., All rights reserved.",

year = "2021",

month = feb,

day = "18",

doi = "10.1038/s41598-021-83345-3",

language = "English",

volume = "11",

journal = "Scientific Reports",

issn = "2045-2322",

publisher = "Nature Publishing Group",

number = "1",

}

TY - JOUR

T1 - Altered non-coding RNA expression profile in F1 progeny 1 year after parental irradiation is linked to adverse effects in zebrafish

AU - Martín, Leonardo

AU - Kamstra, Jorke H.

AU - Hurem, Selma

AU - Lindeman, Leif C.

AU - Brede, Dag A.

AU - Aanes, Håvard

AU - Babiak, Igor

AU - Arenal, Amilcar

AU - Oughton, Deborah

AU - Salbu, Brit

AU - Lyche, Jan Ludvig

AU - Aleström, Peter

N1 - Funding Information: This research work was supported by the Norwegian Research Council funded through the Centre of Excellence CERAD–Centre for Environmental Radioactivity (project 223268/F50). Publisher Copyright: © 2021, The Author(s). Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

PY - 2021/2/18

Y1 - 2021/2/18

N2 - Gamma radiation produces DNA instability and impaired phenotype. Previously, we observed negative effects on phenotype, DNA methylation, and gene expression profiles, in offspring of zebrafish exposed to gamma radiation during gametogenesis. We hypothesize that previously observed effects are accompanied with changes in the expression profile of non-coding RNAs, inherited by next generations. Non-coding RNA expression profile was analysed in F1 offspring (5.5 h post-fertilization) by high-throughput sequencing 1 year after parental irradiation (8.7 mGy/h, 5.2 Gy total dose). Using our previous F1-γ genome-wide gene expression data (GSE98539), hundreds of mRNAs were predicted as targets of differentially expressed (DE) miRNAs, involved in pathways such as insulin receptor, NFkB and PTEN signalling, linking to apoptosis and cancer. snRNAs belonging to the five major spliceosomal snRNAs were down-regulated in the F1-γ group, Indicating transcriptional and post-transcriptional alterations. In addition, DEpiRNA clusters were associated to 9 transposable elements (TEs) (LTR, LINE, and TIR) (p = 0.0024), probable as a response to the activation of these TEs. Moreover, the expression of the lincRNAs malat-1, and several others was altered in the offspring F1, in concordance with previously observed phenotypical alterations. In conclusion, our results demonstrate diverse gamma radiation-induced alterations in the ncRNA profiles of F1 offspring observable 1 year after parental irradiation.

AB - Gamma radiation produces DNA instability and impaired phenotype. Previously, we observed negative effects on phenotype, DNA methylation, and gene expression profiles, in offspring of zebrafish exposed to gamma radiation during gametogenesis. We hypothesize that previously observed effects are accompanied with changes in the expression profile of non-coding RNAs, inherited by next generations. Non-coding RNA expression profile was analysed in F1 offspring (5.5 h post-fertilization) by high-throughput sequencing 1 year after parental irradiation (8.7 mGy/h, 5.2 Gy total dose). Using our previous F1-γ genome-wide gene expression data (GSE98539), hundreds of mRNAs were predicted as targets of differentially expressed (DE) miRNAs, involved in pathways such as insulin receptor, NFkB and PTEN signalling, linking to apoptosis and cancer. snRNAs belonging to the five major spliceosomal snRNAs were down-regulated in the F1-γ group, Indicating transcriptional and post-transcriptional alterations. In addition, DEpiRNA clusters were associated to 9 transposable elements (TEs) (LTR, LINE, and TIR) (p = 0.0024), probable as a response to the activation of these TEs. Moreover, the expression of the lincRNAs malat-1, and several others was altered in the offspring F1, in concordance with previously observed phenotypical alterations. In conclusion, our results demonstrate diverse gamma radiation-induced alterations in the ncRNA profiles of F1 offspring observable 1 year after parental irradiation.

UR - https://www.scopus.com/pages/publications/85101244383

U2 - 10.1038/s41598-021-83345-3

DO - 10.1038/s41598-021-83345-3

M3 - Article

C2 - 33602989

AN - SCOPUS:85101244383

SN - 2045-2322

VL - 11

JO - Scientific Reports

JF - Scientific Reports

IS - 1

M1 - 4142

ER -