Cargando…
Impact of the severity of negative energy balance on gene expression in the subcutaneous adipose tissue of periparturient primiparous Holstein dairy cows: Identification of potential novel metabolic signals for the reproductive system
The severity of negative energy balance (NEB) in high-producing dairy cows has a high incidence among health diseases. The cow’s energy status during early lactation critically affects metabolic and reproductive parameters. The first objective of this study was to investigate by RNA-seq analysis and...
Autores principales: | , , , , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2019
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6763198/ https://www.ncbi.nlm.nih.gov/pubmed/31557215 http://dx.doi.org/10.1371/journal.pone.0222954 |
_version_ | 1783454173071671296 |
---|---|
author | Mellouk, Namya Rame, Christelle Naquin, Delphine Jaszczyszyn, Yan Touzé, Jean-Luc Briant, Eric Guillaume, Daniel Ntallaris, Theodoros Humblot, Patrice Dupont, Joëlle |
author_facet | Mellouk, Namya Rame, Christelle Naquin, Delphine Jaszczyszyn, Yan Touzé, Jean-Luc Briant, Eric Guillaume, Daniel Ntallaris, Theodoros Humblot, Patrice Dupont, Joëlle |
author_sort | Mellouk, Namya |
collection | PubMed |
description | The severity of negative energy balance (NEB) in high-producing dairy cows has a high incidence among health diseases. The cow’s energy status during early lactation critically affects metabolic and reproductive parameters. The first objective of this study was to investigate by RNA-seq analysis and RT-qPCR the gene expression profile in white adipose tissue and by gene ontology and upstream regulation tools the relationships with energy metabolism and reproduction in two groups of primiparous dairy cows with extreme NEB statuses (NEB < -9 Mcal/day vs. NEB > -9 Mcal/day) around parturition. The second objective was to determine the potential involvement of a new adipokine identified as a candidate for the regulation of ovarian function in our RNA-seq analysis by using bovine primary granulosa culture, thymidine incorporation to determine cell proliferation and ELISA assays to measure progesterone secretion. The RNA-seq analysis revealed that 514 genes were over-expressed and 695 were under-expressed in the adipose tissue of cows with severe NEB (SNEB) and cows with moderate NEB (MNEB) during the -4 and 16 wkpp period. In addition, 491 genes were over-expressed and 705 genes were under-expressed in the adipose tissue of SNEB cows compared to MNEB cows. Among these differently expressed genes (DEGs), 298 were related to metabolic functions and 264 to reproductive traits. A set of 19 DEGs were validated by RT-qPCR, including CCL21 (C-C motif chemokine ligand 21). Moreover, CCL21, a gene known to be secreted by adipose tissue, was chosen for further analysis in plasma and ovaries. The use of next-generation sequencing technologies allowed us to characterise the transcriptome of white adipose tissue from primiparous cows with different levels of NEB during lactation. This study highlighted the alteration of the expression of genes related to lipid metabolism, including CCL21, which is released in the bloodstream and associated with the in vitro regulation of ovarian functions. |
format | Online Article Text |
id | pubmed-6763198 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-67631982019-10-12 Impact of the severity of negative energy balance on gene expression in the subcutaneous adipose tissue of periparturient primiparous Holstein dairy cows: Identification of potential novel metabolic signals for the reproductive system Mellouk, Namya Rame, Christelle Naquin, Delphine Jaszczyszyn, Yan Touzé, Jean-Luc Briant, Eric Guillaume, Daniel Ntallaris, Theodoros Humblot, Patrice Dupont, Joëlle PLoS One Research Article The severity of negative energy balance (NEB) in high-producing dairy cows has a high incidence among health diseases. The cow’s energy status during early lactation critically affects metabolic and reproductive parameters. The first objective of this study was to investigate by RNA-seq analysis and RT-qPCR the gene expression profile in white adipose tissue and by gene ontology and upstream regulation tools the relationships with energy metabolism and reproduction in two groups of primiparous dairy cows with extreme NEB statuses (NEB < -9 Mcal/day vs. NEB > -9 Mcal/day) around parturition. The second objective was to determine the potential involvement of a new adipokine identified as a candidate for the regulation of ovarian function in our RNA-seq analysis by using bovine primary granulosa culture, thymidine incorporation to determine cell proliferation and ELISA assays to measure progesterone secretion. The RNA-seq analysis revealed that 514 genes were over-expressed and 695 were under-expressed in the adipose tissue of cows with severe NEB (SNEB) and cows with moderate NEB (MNEB) during the -4 and 16 wkpp period. In addition, 491 genes were over-expressed and 705 genes were under-expressed in the adipose tissue of SNEB cows compared to MNEB cows. Among these differently expressed genes (DEGs), 298 were related to metabolic functions and 264 to reproductive traits. A set of 19 DEGs were validated by RT-qPCR, including CCL21 (C-C motif chemokine ligand 21). Moreover, CCL21, a gene known to be secreted by adipose tissue, was chosen for further analysis in plasma and ovaries. The use of next-generation sequencing technologies allowed us to characterise the transcriptome of white adipose tissue from primiparous cows with different levels of NEB during lactation. This study highlighted the alteration of the expression of genes related to lipid metabolism, including CCL21, which is released in the bloodstream and associated with the in vitro regulation of ovarian functions. Public Library of Science 2019-09-26 /pmc/articles/PMC6763198/ /pubmed/31557215 http://dx.doi.org/10.1371/journal.pone.0222954 Text en © 2019 Mellouk et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Mellouk, Namya Rame, Christelle Naquin, Delphine Jaszczyszyn, Yan Touzé, Jean-Luc Briant, Eric Guillaume, Daniel Ntallaris, Theodoros Humblot, Patrice Dupont, Joëlle Impact of the severity of negative energy balance on gene expression in the subcutaneous adipose tissue of periparturient primiparous Holstein dairy cows: Identification of potential novel metabolic signals for the reproductive system |
title | Impact of the severity of negative energy balance on gene expression in the subcutaneous adipose tissue of periparturient primiparous Holstein dairy cows: Identification of potential novel metabolic signals for the reproductive system |
title_full | Impact of the severity of negative energy balance on gene expression in the subcutaneous adipose tissue of periparturient primiparous Holstein dairy cows: Identification of potential novel metabolic signals for the reproductive system |
title_fullStr | Impact of the severity of negative energy balance on gene expression in the subcutaneous adipose tissue of periparturient primiparous Holstein dairy cows: Identification of potential novel metabolic signals for the reproductive system |
title_full_unstemmed | Impact of the severity of negative energy balance on gene expression in the subcutaneous adipose tissue of periparturient primiparous Holstein dairy cows: Identification of potential novel metabolic signals for the reproductive system |
title_short | Impact of the severity of negative energy balance on gene expression in the subcutaneous adipose tissue of periparturient primiparous Holstein dairy cows: Identification of potential novel metabolic signals for the reproductive system |
title_sort | impact of the severity of negative energy balance on gene expression in the subcutaneous adipose tissue of periparturient primiparous holstein dairy cows: identification of potential novel metabolic signals for the reproductive system |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6763198/ https://www.ncbi.nlm.nih.gov/pubmed/31557215 http://dx.doi.org/10.1371/journal.pone.0222954 |
work_keys_str_mv | AT mellouknamya impactoftheseverityofnegativeenergybalanceongeneexpressioninthesubcutaneousadiposetissueofperiparturientprimiparousholsteindairycowsidentificationofpotentialnovelmetabolicsignalsforthereproductivesystem AT ramechristelle impactoftheseverityofnegativeenergybalanceongeneexpressioninthesubcutaneousadiposetissueofperiparturientprimiparousholsteindairycowsidentificationofpotentialnovelmetabolicsignalsforthereproductivesystem AT naquindelphine impactoftheseverityofnegativeenergybalanceongeneexpressioninthesubcutaneousadiposetissueofperiparturientprimiparousholsteindairycowsidentificationofpotentialnovelmetabolicsignalsforthereproductivesystem AT jaszczyszynyan impactoftheseverityofnegativeenergybalanceongeneexpressioninthesubcutaneousadiposetissueofperiparturientprimiparousholsteindairycowsidentificationofpotentialnovelmetabolicsignalsforthereproductivesystem AT touzejeanluc impactoftheseverityofnegativeenergybalanceongeneexpressioninthesubcutaneousadiposetissueofperiparturientprimiparousholsteindairycowsidentificationofpotentialnovelmetabolicsignalsforthereproductivesystem AT brianteric impactoftheseverityofnegativeenergybalanceongeneexpressioninthesubcutaneousadiposetissueofperiparturientprimiparousholsteindairycowsidentificationofpotentialnovelmetabolicsignalsforthereproductivesystem AT guillaumedaniel impactoftheseverityofnegativeenergybalanceongeneexpressioninthesubcutaneousadiposetissueofperiparturientprimiparousholsteindairycowsidentificationofpotentialnovelmetabolicsignalsforthereproductivesystem AT ntallaristheodoros impactoftheseverityofnegativeenergybalanceongeneexpressioninthesubcutaneousadiposetissueofperiparturientprimiparousholsteindairycowsidentificationofpotentialnovelmetabolicsignalsforthereproductivesystem AT humblotpatrice impactoftheseverityofnegativeenergybalanceongeneexpressioninthesubcutaneousadiposetissueofperiparturientprimiparousholsteindairycowsidentificationofpotentialnovelmetabolicsignalsforthereproductivesystem AT dupontjoelle impactoftheseverityofnegativeenergybalanceongeneexpressioninthesubcutaneousadiposetissueofperiparturientprimiparousholsteindairycowsidentificationofpotentialnovelmetabolicsignalsforthereproductivesystem |