Comparative omics and feeding manipulations in chicken indicate a shift of the endocrine role of visceral fat towards reproduction

Susanne Bornelöv, Eyal Seroussi, Sara Yosefi, Sharon Benjamini, Shoval Miyara, Mark Ruzal, Manfred Grabherr, Nima Rafati, Anna Maja Molin, Ken Pendavis, Shane C Burgess, Leif Andersson, Miriam Friedman-Einat

Research output: Contribution to journalArticle

4 Citations (Scopus)

Abstract

BACKGROUND: The mammalian adipose tissue plays a central role in energy-balance control, whereas the avian visceral fat hardly expresses leptin, the key adipokine in mammals. Therefore, to assess the endocrine role of adipose tissue in birds, we compared the transcriptome and proteome between two metabolically different types of chickens, broilers and layers, bred towards efficient meat and egg production, respectively. RESULTS: Broilers and layer hens, grown up to sexual maturation under free-feeding conditions, differed 4.0-fold in weight and 1.6-fold in ovarian-follicle counts, yet the relative accumulation of visceral fat was comparable. RNA-seq and mass-spectrometry (MS) analyses of visceral fat revealed differentially expressed genes between broilers and layers, 1106 at the mRNA level (FDR ≤ 0.05), and 203 at the protein level (P ≤ 0.05). In broilers, Ingenuity Pathway Analysis revealed activation of the PTEN-pathway, and in layers increased response to external signals. The expression pattern of genes encoding fat-secreted proteins in broilers and layers was characterized in the RNA-seq and MS data, as well as by qPCR on visceral fat under free feeding and 24 h-feed deprivation. This characterization was expanded using available RNA-seq data of tissues from red junglefowl, and of visceral fat from broilers of different types. These comparisons revealed expression of new adipokines and secreted proteins (LCAT, LECT2, SERPINE2, SFTP1, ZP1, ZP3, APOV1, VTG1 and VTG2) at the mRNA and/or protein levels, with dynamic gene expression patterns in the selected chicken lines (except for ZP1; FDR/P ≤ 0.05) and feed deprivation (NAMPT, SFTPA1 and ZP3) (P ≤ 0.05). In contrast, some of the most prominent adipokines in mammals, leptin, TNF, IFNG, and IL6 were expressed at a low level (FPKM/RPKM< 1) and did not show differential mRNA expression neither between broiler and layer lines nor between fed vs. feed-deprived chickens. CONCLUSIONS: Our study revealed that RNA and protein expression in visceral fat changes with selective breeding, suggesting endocrine roles of visceral fat in the selected phenotypes. In comparison to gene expression in visceral fat of mammals, our findings points to a more direct cross talk of the chicken visceral fat with the reproductive system and lower involvement in the regulation of appetite, inflammation and insulin resistance.

Original languageEnglish (US)
Number of pages1
JournalBMC Genomics
Volume19
Issue number1
DOIs
StatePublished - Apr 26 2018

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Intra-Abdominal Fat
Reproduction
Chickens
Adipokines
RNA
Mammals
Leptin
Proteins
Gene Expression
Messenger RNA
Adipose Tissue
Mass Spectrometry
Activation Analysis
Appetite Regulation
Sexual Maturation
Ovarian Follicle
Proteome
Transcriptome
Meat
Birds

Keywords

  • Adipokines
  • Adipolin
  • Adipose tissue
  • Chickens
  • Mass spectrometry
  • PLIN1
  • PTEN-pathway
  • RNA-seq
  • SFTPA1
  • TNF
  • Yolk proteins

ASJC Scopus subject areas

  • Biotechnology
  • Genetics

Cite this

Comparative omics and feeding manipulations in chicken indicate a shift of the endocrine role of visceral fat towards reproduction. / Bornelöv, Susanne; Seroussi, Eyal; Yosefi, Sara; Benjamini, Sharon; Miyara, Shoval; Ruzal, Mark; Grabherr, Manfred; Rafati, Nima; Molin, Anna Maja; Pendavis, Ken; Burgess, Shane C; Andersson, Leif; Friedman-Einat, Miriam.

In: BMC Genomics, Vol. 19, No. 1, 26.04.2018.

Research output: Contribution to journalArticle

Bornelöv, S, Seroussi, E, Yosefi, S, Benjamini, S, Miyara, S, Ruzal, M, Grabherr, M, Rafati, N, Molin, AM, Pendavis, K, Burgess, SC, Andersson, L & Friedman-Einat, M 2018, 'Comparative omics and feeding manipulations in chicken indicate a shift of the endocrine role of visceral fat towards reproduction', BMC Genomics, vol. 19, no. 1. https://doi.org/10.1186/s12864-018-4675-0
Bornelöv, Susanne ; Seroussi, Eyal ; Yosefi, Sara ; Benjamini, Sharon ; Miyara, Shoval ; Ruzal, Mark ; Grabherr, Manfred ; Rafati, Nima ; Molin, Anna Maja ; Pendavis, Ken ; Burgess, Shane C ; Andersson, Leif ; Friedman-Einat, Miriam. / Comparative omics and feeding manipulations in chicken indicate a shift of the endocrine role of visceral fat towards reproduction. In: BMC Genomics. 2018 ; Vol. 19, No. 1.
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AU - Bornelöv, Susanne

AU - Seroussi, Eyal

AU - Yosefi, Sara

AU - Benjamini, Sharon

AU - Miyara, Shoval

AU - Ruzal, Mark

AU - Grabherr, Manfred

AU - Rafati, Nima

AU - Molin, Anna Maja

AU - Pendavis, Ken

AU - Burgess, Shane C

AU - Andersson, Leif

AU - Friedman-Einat, Miriam

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N2 - BACKGROUND: The mammalian adipose tissue plays a central role in energy-balance control, whereas the avian visceral fat hardly expresses leptin, the key adipokine in mammals. Therefore, to assess the endocrine role of adipose tissue in birds, we compared the transcriptome and proteome between two metabolically different types of chickens, broilers and layers, bred towards efficient meat and egg production, respectively. RESULTS: Broilers and layer hens, grown up to sexual maturation under free-feeding conditions, differed 4.0-fold in weight and 1.6-fold in ovarian-follicle counts, yet the relative accumulation of visceral fat was comparable. RNA-seq and mass-spectrometry (MS) analyses of visceral fat revealed differentially expressed genes between broilers and layers, 1106 at the mRNA level (FDR ≤ 0.05), and 203 at the protein level (P ≤ 0.05). In broilers, Ingenuity Pathway Analysis revealed activation of the PTEN-pathway, and in layers increased response to external signals. The expression pattern of genes encoding fat-secreted proteins in broilers and layers was characterized in the RNA-seq and MS data, as well as by qPCR on visceral fat under free feeding and 24 h-feed deprivation. This characterization was expanded using available RNA-seq data of tissues from red junglefowl, and of visceral fat from broilers of different types. These comparisons revealed expression of new adipokines and secreted proteins (LCAT, LECT2, SERPINE2, SFTP1, ZP1, ZP3, APOV1, VTG1 and VTG2) at the mRNA and/or protein levels, with dynamic gene expression patterns in the selected chicken lines (except for ZP1; FDR/P ≤ 0.05) and feed deprivation (NAMPT, SFTPA1 and ZP3) (P ≤ 0.05). In contrast, some of the most prominent adipokines in mammals, leptin, TNF, IFNG, and IL6 were expressed at a low level (FPKM/RPKM< 1) and did not show differential mRNA expression neither between broiler and layer lines nor between fed vs. feed-deprived chickens. CONCLUSIONS: Our study revealed that RNA and protein expression in visceral fat changes with selective breeding, suggesting endocrine roles of visceral fat in the selected phenotypes. In comparison to gene expression in visceral fat of mammals, our findings points to a more direct cross talk of the chicken visceral fat with the reproductive system and lower involvement in the regulation of appetite, inflammation and insulin resistance.

AB - BACKGROUND: The mammalian adipose tissue plays a central role in energy-balance control, whereas the avian visceral fat hardly expresses leptin, the key adipokine in mammals. Therefore, to assess the endocrine role of adipose tissue in birds, we compared the transcriptome and proteome between two metabolically different types of chickens, broilers and layers, bred towards efficient meat and egg production, respectively. RESULTS: Broilers and layer hens, grown up to sexual maturation under free-feeding conditions, differed 4.0-fold in weight and 1.6-fold in ovarian-follicle counts, yet the relative accumulation of visceral fat was comparable. RNA-seq and mass-spectrometry (MS) analyses of visceral fat revealed differentially expressed genes between broilers and layers, 1106 at the mRNA level (FDR ≤ 0.05), and 203 at the protein level (P ≤ 0.05). In broilers, Ingenuity Pathway Analysis revealed activation of the PTEN-pathway, and in layers increased response to external signals. The expression pattern of genes encoding fat-secreted proteins in broilers and layers was characterized in the RNA-seq and MS data, as well as by qPCR on visceral fat under free feeding and 24 h-feed deprivation. This characterization was expanded using available RNA-seq data of tissues from red junglefowl, and of visceral fat from broilers of different types. These comparisons revealed expression of new adipokines and secreted proteins (LCAT, LECT2, SERPINE2, SFTP1, ZP1, ZP3, APOV1, VTG1 and VTG2) at the mRNA and/or protein levels, with dynamic gene expression patterns in the selected chicken lines (except for ZP1; FDR/P ≤ 0.05) and feed deprivation (NAMPT, SFTPA1 and ZP3) (P ≤ 0.05). In contrast, some of the most prominent adipokines in mammals, leptin, TNF, IFNG, and IL6 were expressed at a low level (FPKM/RPKM< 1) and did not show differential mRNA expression neither between broiler and layer lines nor between fed vs. feed-deprived chickens. CONCLUSIONS: Our study revealed that RNA and protein expression in visceral fat changes with selective breeding, suggesting endocrine roles of visceral fat in the selected phenotypes. In comparison to gene expression in visceral fat of mammals, our findings points to a more direct cross talk of the chicken visceral fat with the reproductive system and lower involvement in the regulation of appetite, inflammation and insulin resistance.

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KW - Adipolin

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KW - Mass spectrometry

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KW - PTEN-pathway

KW - RNA-seq

KW - SFTPA1

KW - TNF

KW - Yolk proteins

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