Integrative testis transcriptome analysis reveals differentially expressed miRNAs and their mRNA targets during early puberty in Atlantic salmon

Abstract Background Our understanding of the molecular mechanisms implementing pubertal maturation of the testis in vertebrates is incomplete. This topic is relevant in Atlantic salmon aquaculture, since precocious male puberty negatively impacts animal welfare and growth. We hypothesize that certai...

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Main Authors: K. Skaftnesmo, R. Edvardsen, T. Furmanek, D. Crespo, E. Andersson, L. Kleppe, G. Taranger, J. Bogerd, R. Schulz, A. Wargelius
Format: Article in Journal/Newspaper
Language:unknown
Published: Figshare 2017
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Online Access:https://dx.doi.org/10.6084/m9.figshare.c.3908374
https://figshare.com/collections/Integrative_testis_transcriptome_analysis_reveals_differentially_expressed_miRNAs_and_their_mRNA_targets_during_early_puberty_in_Atlantic_salmon/3908374
id ftdatacite:10.6084/m9.figshare.c.3908374
record_format openpolar
spelling ftdatacite:10.6084/m9.figshare.c.3908374 2023-05-15T15:31:56+02:00 Integrative testis transcriptome analysis reveals differentially expressed miRNAs and their mRNA targets during early puberty in Atlantic salmon K. Skaftnesmo R. Edvardsen T. Furmanek D. Crespo E. Andersson L. Kleppe G. Taranger J. Bogerd R. Schulz A. Wargelius 2017 https://dx.doi.org/10.6084/m9.figshare.c.3908374 https://figshare.com/collections/Integrative_testis_transcriptome_analysis_reveals_differentially_expressed_miRNAs_and_their_mRNA_targets_during_early_puberty_in_Atlantic_salmon/3908374 unknown Figshare https://dx.doi.org/10.1186/s12864-017-4205-5 CC BY 4.0 https://creativecommons.org/licenses/by/4.0 CC-BY Biophysics Biochemistry Cell Biology Genetics FOS Biological sciences Molecular Biology 59999 Environmental Sciences not elsewhere classified FOS Earth and related environmental sciences 69999 Biological Sciences not elsewhere classified Developmental Biology Computational Biology Collection article 2017 ftdatacite https://doi.org/10.6084/m9.figshare.c.3908374 https://doi.org/10.1186/s12864-017-4205-5 2021-11-05T12:55:41Z Abstract Background Our understanding of the molecular mechanisms implementing pubertal maturation of the testis in vertebrates is incomplete. This topic is relevant in Atlantic salmon aquaculture, since precocious male puberty negatively impacts animal welfare and growth. We hypothesize that certain miRNAs modulate mRNAs relevant for the initiation of puberty. To explore which miRNAs regulate mRNAs during initiation of puberty in salmon, we performed an integrated transcriptome analysis (miRNA and mRNA-seq) of salmon testis at three stages of development: an immature, long-term quiescent stage, a prepubertal stage just before, and a pubertal stage just after the onset of single cell proliferation activity in the testis. Results Differentially expressed miRNAs clustered into 5 distinct expression profiles related to the immature, prepubertal and pubertal salmon testis. Potential mRNA targets of these miRNAs were predicted with miRmap and filtered for mRNAs displaying negatively correlated expression patterns. In summary, this analysis revealed miRNAs previously known to be regulated in immature vertebrate testis (miR-101, miR-137, miR-92b, miR-18a, miR-20a), but also miRNAs first reported here as regulated in the testis (miR-new289, miR-30c, miR-724, miR-26b, miR-new271, miR-217, miR-216a, miR-135a, miR-new194 and the novel predicted n268). By KEGG enrichment analysis, progesterone signaling and cell cycle pathway genes were found regulated by these differentially expressed miRNAs. During the transition into puberty we found differential expression of miRNAs previously associated (let7a/b/c), or newly associated (miR-15c, miR-2184, miR-145 and the novel predicted n7a and b) with this stage. KEGG enrichment analysis revealed that mRNAs of the Wnt, Hedgehog and Apelin signaling pathways were potential regulated targets during the transition into puberty. Likewise, several regulated miRNAs in the pubertal stage had earlier been associated (miR-20a, miR-25, miR-181a, miR-202, let7c/d/a, miR-125b, miR-222a/b, miR-190a) or have now been found connected (miR-2188, miR-144, miR-731, miR-8157 and the novel n2) to the initiation of puberty. Conclusions This study has - for the first time - linked testis maturation to specific miRNAs and their inversely correlated expressed targets in Atlantic salmon. The study indicates a broad functional conservation of already known miRNAs and associated pathways involved in the transition into puberty in vertebrates. The analysis also reveals miRNAs not previously associated with testis tissue or its maturation, which calls for further functional studies in the testis. Article in Journal/Newspaper Atlantic salmon DataCite Metadata Store (German National Library of Science and Technology)
institution Open Polar
collection DataCite Metadata Store (German National Library of Science and Technology)
op_collection_id ftdatacite
language unknown
topic Biophysics
Biochemistry
Cell Biology
Genetics
FOS Biological sciences
Molecular Biology
59999 Environmental Sciences not elsewhere classified
FOS Earth and related environmental sciences
69999 Biological Sciences not elsewhere classified
Developmental Biology
Computational Biology
spellingShingle Biophysics
Biochemistry
Cell Biology
Genetics
FOS Biological sciences
Molecular Biology
59999 Environmental Sciences not elsewhere classified
FOS Earth and related environmental sciences
69999 Biological Sciences not elsewhere classified
Developmental Biology
Computational Biology
K. Skaftnesmo
R. Edvardsen
T. Furmanek
D. Crespo
E. Andersson
L. Kleppe
G. Taranger
J. Bogerd
R. Schulz
A. Wargelius
Integrative testis transcriptome analysis reveals differentially expressed miRNAs and their mRNA targets during early puberty in Atlantic salmon
topic_facet Biophysics
Biochemistry
Cell Biology
Genetics
FOS Biological sciences
Molecular Biology
59999 Environmental Sciences not elsewhere classified
FOS Earth and related environmental sciences
69999 Biological Sciences not elsewhere classified
Developmental Biology
Computational Biology
description Abstract Background Our understanding of the molecular mechanisms implementing pubertal maturation of the testis in vertebrates is incomplete. This topic is relevant in Atlantic salmon aquaculture, since precocious male puberty negatively impacts animal welfare and growth. We hypothesize that certain miRNAs modulate mRNAs relevant for the initiation of puberty. To explore which miRNAs regulate mRNAs during initiation of puberty in salmon, we performed an integrated transcriptome analysis (miRNA and mRNA-seq) of salmon testis at three stages of development: an immature, long-term quiescent stage, a prepubertal stage just before, and a pubertal stage just after the onset of single cell proliferation activity in the testis. Results Differentially expressed miRNAs clustered into 5 distinct expression profiles related to the immature, prepubertal and pubertal salmon testis. Potential mRNA targets of these miRNAs were predicted with miRmap and filtered for mRNAs displaying negatively correlated expression patterns. In summary, this analysis revealed miRNAs previously known to be regulated in immature vertebrate testis (miR-101, miR-137, miR-92b, miR-18a, miR-20a), but also miRNAs first reported here as regulated in the testis (miR-new289, miR-30c, miR-724, miR-26b, miR-new271, miR-217, miR-216a, miR-135a, miR-new194 and the novel predicted n268). By KEGG enrichment analysis, progesterone signaling and cell cycle pathway genes were found regulated by these differentially expressed miRNAs. During the transition into puberty we found differential expression of miRNAs previously associated (let7a/b/c), or newly associated (miR-15c, miR-2184, miR-145 and the novel predicted n7a and b) with this stage. KEGG enrichment analysis revealed that mRNAs of the Wnt, Hedgehog and Apelin signaling pathways were potential regulated targets during the transition into puberty. Likewise, several regulated miRNAs in the pubertal stage had earlier been associated (miR-20a, miR-25, miR-181a, miR-202, let7c/d/a, miR-125b, miR-222a/b, miR-190a) or have now been found connected (miR-2188, miR-144, miR-731, miR-8157 and the novel n2) to the initiation of puberty. Conclusions This study has - for the first time - linked testis maturation to specific miRNAs and their inversely correlated expressed targets in Atlantic salmon. The study indicates a broad functional conservation of already known miRNAs and associated pathways involved in the transition into puberty in vertebrates. The analysis also reveals miRNAs not previously associated with testis tissue or its maturation, which calls for further functional studies in the testis.
format Article in Journal/Newspaper
author K. Skaftnesmo
R. Edvardsen
T. Furmanek
D. Crespo
E. Andersson
L. Kleppe
G. Taranger
J. Bogerd
R. Schulz
A. Wargelius
author_facet K. Skaftnesmo
R. Edvardsen
T. Furmanek
D. Crespo
E. Andersson
L. Kleppe
G. Taranger
J. Bogerd
R. Schulz
A. Wargelius
author_sort K. Skaftnesmo
title Integrative testis transcriptome analysis reveals differentially expressed miRNAs and their mRNA targets during early puberty in Atlantic salmon
title_short Integrative testis transcriptome analysis reveals differentially expressed miRNAs and their mRNA targets during early puberty in Atlantic salmon
title_full Integrative testis transcriptome analysis reveals differentially expressed miRNAs and their mRNA targets during early puberty in Atlantic salmon
title_fullStr Integrative testis transcriptome analysis reveals differentially expressed miRNAs and their mRNA targets during early puberty in Atlantic salmon
title_full_unstemmed Integrative testis transcriptome analysis reveals differentially expressed miRNAs and their mRNA targets during early puberty in Atlantic salmon
title_sort integrative testis transcriptome analysis reveals differentially expressed mirnas and their mrna targets during early puberty in atlantic salmon
publisher Figshare
publishDate 2017
url https://dx.doi.org/10.6084/m9.figshare.c.3908374
https://figshare.com/collections/Integrative_testis_transcriptome_analysis_reveals_differentially_expressed_miRNAs_and_their_mRNA_targets_during_early_puberty_in_Atlantic_salmon/3908374
genre Atlantic salmon
genre_facet Atlantic salmon
op_relation https://dx.doi.org/10.1186/s12864-017-4205-5
op_rights CC BY 4.0
https://creativecommons.org/licenses/by/4.0
op_rightsnorm CC-BY
op_doi https://doi.org/10.6084/m9.figshare.c.3908374
https://doi.org/10.1186/s12864-017-4205-5
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