Circulating miRNA repertoire as a biomarker of metabolic and reproductive states in rainbow trout

Abstract Background Circulating miRNAs (c-miRNAs) are found in most, if not all, biological fluids and are becoming well-established non-invasive biomarkers of many human pathologies. However, their features in non-pathological contexts and whether their expression profiles reflect normal life histo...

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Autores principales: Emilie Cardona, Cervin Guyomar, Thomas Desvignes, Jérôme Montfort, Samia Guendouz, John H. Postlethwait, Sandrine Skiba-Cassy, Julien Bobe
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Publicado: BMC 2021
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spelling oai:doaj.org-article:97463e962710476c93160a61c702fd932021-11-21T12:42:19ZCirculating miRNA repertoire as a biomarker of metabolic and reproductive states in rainbow trout10.1186/s12915-021-01163-51741-7007https://doaj.org/article/97463e962710476c93160a61c702fd932021-11-01T00:00:00Zhttps://doi.org/10.1186/s12915-021-01163-5https://doaj.org/toc/1741-7007Abstract Background Circulating miRNAs (c-miRNAs) are found in most, if not all, biological fluids and are becoming well-established non-invasive biomarkers of many human pathologies. However, their features in non-pathological contexts and whether their expression profiles reflect normal life history events have received little attention, especially in non-mammalian species. The aim of the present study was to investigate the potential of c-miRNAs to serve as biomarkers of reproductive and metabolic states in fish. Results The blood plasma was sampled throughout the reproductive cycle of female rainbow trout subjected to two different feeding regimes that triggered contrasting metabolic states. In addition, ovarian fluid was sampled at ovulation, and all samples were subjected to small RNA-seq analysis, leading to the establishment of a comprehensive miRNA repertoire (i.e., miRNAome) and enabling subsequent comparative analyses to a panel of RNA-seq libraries from a wide variety of tissues and organs. We showed that biological fluid miRNAomes are complex and encompass a high proportion of the overall rainbow trout miRNAome. While sharing a high proportion of common miRNAs, the blood plasma and ovarian fluid miRNAomes exhibited strong fluid-specific signatures. We further revealed that the blood plasma miRNAome significantly changed depending on metabolic and reproductive states. We subsequently identified three evolutionarily conserved muscle-specific miRNAs or myomiRs (miR-1-1/2-3p, miR-133a-1/2-3p, and miR-206-3p) that accumulated in the blood plasma in response to high feeding rates, making these myomiRs strong candidate biomarkers of active myogenesis. We also identified miR-202-5p as a candidate biomarker for reproductive success that could be used to predict ovulation and/or egg quality. Conclusions Together, these promising results reveal the high potential of c-miRNAs, including evolutionarily conserved myomiRs, as physiologically relevant biomarker candidates and pave the way for the use of c-miRNAs for non-invasive phenotyping in various fish species.Emilie CardonaCervin GuyomarThomas DesvignesJérôme MontfortSamia GuendouzJohn H. PostlethwaitSandrine Skiba-CassyJulien BobeBMCarticleBiomarkerBiological fluidNon-invasive phenotypingmir202myomiRmir375Biology (General)QH301-705.5ENBMC Biology, Vol 19, Iss 1, Pp 1-19 (2021)
institution DOAJ
collection DOAJ
language EN
topic Biomarker
Biological fluid
Non-invasive phenotyping
mir202
myomiR
mir375
Biology (General)
QH301-705.5
spellingShingle Biomarker
Biological fluid
Non-invasive phenotyping
mir202
myomiR
mir375
Biology (General)
QH301-705.5
Emilie Cardona
Cervin Guyomar
Thomas Desvignes
Jérôme Montfort
Samia Guendouz
John H. Postlethwait
Sandrine Skiba-Cassy
Julien Bobe
Circulating miRNA repertoire as a biomarker of metabolic and reproductive states in rainbow trout
description Abstract Background Circulating miRNAs (c-miRNAs) are found in most, if not all, biological fluids and are becoming well-established non-invasive biomarkers of many human pathologies. However, their features in non-pathological contexts and whether their expression profiles reflect normal life history events have received little attention, especially in non-mammalian species. The aim of the present study was to investigate the potential of c-miRNAs to serve as biomarkers of reproductive and metabolic states in fish. Results The blood plasma was sampled throughout the reproductive cycle of female rainbow trout subjected to two different feeding regimes that triggered contrasting metabolic states. In addition, ovarian fluid was sampled at ovulation, and all samples were subjected to small RNA-seq analysis, leading to the establishment of a comprehensive miRNA repertoire (i.e., miRNAome) and enabling subsequent comparative analyses to a panel of RNA-seq libraries from a wide variety of tissues and organs. We showed that biological fluid miRNAomes are complex and encompass a high proportion of the overall rainbow trout miRNAome. While sharing a high proportion of common miRNAs, the blood plasma and ovarian fluid miRNAomes exhibited strong fluid-specific signatures. We further revealed that the blood plasma miRNAome significantly changed depending on metabolic and reproductive states. We subsequently identified three evolutionarily conserved muscle-specific miRNAs or myomiRs (miR-1-1/2-3p, miR-133a-1/2-3p, and miR-206-3p) that accumulated in the blood plasma in response to high feeding rates, making these myomiRs strong candidate biomarkers of active myogenesis. We also identified miR-202-5p as a candidate biomarker for reproductive success that could be used to predict ovulation and/or egg quality. Conclusions Together, these promising results reveal the high potential of c-miRNAs, including evolutionarily conserved myomiRs, as physiologically relevant biomarker candidates and pave the way for the use of c-miRNAs for non-invasive phenotyping in various fish species.
format article
author Emilie Cardona
Cervin Guyomar
Thomas Desvignes
Jérôme Montfort
Samia Guendouz
John H. Postlethwait
Sandrine Skiba-Cassy
Julien Bobe
author_facet Emilie Cardona
Cervin Guyomar
Thomas Desvignes
Jérôme Montfort
Samia Guendouz
John H. Postlethwait
Sandrine Skiba-Cassy
Julien Bobe
author_sort Emilie Cardona
title Circulating miRNA repertoire as a biomarker of metabolic and reproductive states in rainbow trout
title_short Circulating miRNA repertoire as a biomarker of metabolic and reproductive states in rainbow trout
title_full Circulating miRNA repertoire as a biomarker of metabolic and reproductive states in rainbow trout
title_fullStr Circulating miRNA repertoire as a biomarker of metabolic and reproductive states in rainbow trout
title_full_unstemmed Circulating miRNA repertoire as a biomarker of metabolic and reproductive states in rainbow trout
title_sort circulating mirna repertoire as a biomarker of metabolic and reproductive states in rainbow trout
publisher BMC
publishDate 2021
url https://doaj.org/article/97463e962710476c93160a61c702fd93
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