Transcriptomic alterations in the ovine caruncular endometrium due to imbalanced nutrition and FSH-induced ovarian hyperstimulation

Abstract Background Imbalanced diet and exogenous gonadotrophins affect uterine function and morphology. In sheep, FSH-induced superovulation alters implantation-related gene expression, influenced by both treatment and diet. In this study, we used deep RNA sequencing (NGS, RNA-Seq) to expand our un...

Full description

Saved in:
Bibliographic Details
Main Authors: Özlem Bedir, Miguel Tavares Pereira, Hubert Rehrauer, Anna Grazul-Bilska, Mariusz P. Kowalewski
Format: Article
Language:English
Published: BMC 2024-12-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-024-10799-w
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850253970853855232
author Özlem Bedir
Miguel Tavares Pereira
Hubert Rehrauer
Anna Grazul-Bilska
Mariusz P. Kowalewski
author_facet Özlem Bedir
Miguel Tavares Pereira
Hubert Rehrauer
Anna Grazul-Bilska
Mariusz P. Kowalewski
author_sort Özlem Bedir
collection DOAJ
description Abstract Background Imbalanced diet and exogenous gonadotrophins affect uterine function and morphology. In sheep, FSH-induced superovulation alters implantation-related gene expression, influenced by both treatment and diet. In this study, we used deep RNA sequencing (NGS, RNA-Seq) to expand our understanding of these effects on the caruncular endometrium. Methods Ewes (n = 3–5/group) were separated into control fed (CF), overfed (OF), and underfed (UF) groups, with each group subdivided between FSH (superovulated; SOV) or saline (negative controls; CONT) treatment. Caruncular samples were collected on day 10 of diestrus of the subsequent estrous cycle, with samples from CF_CONT also collected on day 5 to assess time-dependent changes. Results The 1484 differentially expressed genes (DEGs, P < 0.01, FDR < 0.05) identified between CF_CONT animals at days 5 and 10 were predominantly associated with increased immune activity and cellular metabolic processes and cellular proliferation. In CONT animals, imbalanced nutrition (i.e., both OF and UF) was associated with enrichment of terms associated with cell adhesion and differentiation, immune response and angiogenesis. The FSH carry-over effects resulted in a higher number of DEGs in CF animals (1374), than in OF (168) or UF (18), mostly associated with dysregulation of cell cycle and hormonal sensitivity. Conclusion The absence of genes concurrently affected by superovulation (SOV) in all feeding regimes indicates that the effects of FSH on the caruncular transcriptome are multidirectional and dependent upon body condition. Therefore, the homeostasis of ovine caruncles is influenced by both body condition and superovulation (SOV), potentially affecting uterine receptivity. Graphical Abstract
format Article
id doaj-art-5170b45b11984a438f04b1978992a3ec
institution OA Journals
issn 1471-2164
language English
publishDate 2024-12-01
publisher BMC
record_format Article
series BMC Genomics
spelling doaj-art-5170b45b11984a438f04b1978992a3ec2025-08-20T01:57:15ZengBMCBMC Genomics1471-21642024-12-0125112310.1186/s12864-024-10799-wTranscriptomic alterations in the ovine caruncular endometrium due to imbalanced nutrition and FSH-induced ovarian hyperstimulationÖzlem Bedir0Miguel Tavares Pereira1Hubert Rehrauer2Anna Grazul-Bilska3Mariusz P. Kowalewski4Institute of Veterinary Anatomy, Vetsuisse Faculty, University of Zurich (UZH)Institute of Veterinary Anatomy, Vetsuisse Faculty, University of Zurich (UZH)Functional Genomics Center Zurich (FGCZ), ETH Zurich and University of ZurichDepartment of Animal Sciences, North Dakota State UniversityInstitute of Veterinary Anatomy, Vetsuisse Faculty, University of Zurich (UZH)Abstract Background Imbalanced diet and exogenous gonadotrophins affect uterine function and morphology. In sheep, FSH-induced superovulation alters implantation-related gene expression, influenced by both treatment and diet. In this study, we used deep RNA sequencing (NGS, RNA-Seq) to expand our understanding of these effects on the caruncular endometrium. Methods Ewes (n = 3–5/group) were separated into control fed (CF), overfed (OF), and underfed (UF) groups, with each group subdivided between FSH (superovulated; SOV) or saline (negative controls; CONT) treatment. Caruncular samples were collected on day 10 of diestrus of the subsequent estrous cycle, with samples from CF_CONT also collected on day 5 to assess time-dependent changes. Results The 1484 differentially expressed genes (DEGs, P < 0.01, FDR < 0.05) identified between CF_CONT animals at days 5 and 10 were predominantly associated with increased immune activity and cellular metabolic processes and cellular proliferation. In CONT animals, imbalanced nutrition (i.e., both OF and UF) was associated with enrichment of terms associated with cell adhesion and differentiation, immune response and angiogenesis. The FSH carry-over effects resulted in a higher number of DEGs in CF animals (1374), than in OF (168) or UF (18), mostly associated with dysregulation of cell cycle and hormonal sensitivity. Conclusion The absence of genes concurrently affected by superovulation (SOV) in all feeding regimes indicates that the effects of FSH on the caruncular transcriptome are multidirectional and dependent upon body condition. Therefore, the homeostasis of ovine caruncles is influenced by both body condition and superovulation (SOV), potentially affecting uterine receptivity. Graphical Abstracthttps://doi.org/10.1186/s12864-024-10799-wSheep (Ovies aries)Nutritional statusFSH-hyperstimulationTranscriptome (RNA-seq)
spellingShingle Özlem Bedir
Miguel Tavares Pereira
Hubert Rehrauer
Anna Grazul-Bilska
Mariusz P. Kowalewski
Transcriptomic alterations in the ovine caruncular endometrium due to imbalanced nutrition and FSH-induced ovarian hyperstimulation
BMC Genomics
Sheep (Ovies aries)
Nutritional status
FSH-hyperstimulation
Transcriptome (RNA-seq)
title Transcriptomic alterations in the ovine caruncular endometrium due to imbalanced nutrition and FSH-induced ovarian hyperstimulation
title_full Transcriptomic alterations in the ovine caruncular endometrium due to imbalanced nutrition and FSH-induced ovarian hyperstimulation
title_fullStr Transcriptomic alterations in the ovine caruncular endometrium due to imbalanced nutrition and FSH-induced ovarian hyperstimulation
title_full_unstemmed Transcriptomic alterations in the ovine caruncular endometrium due to imbalanced nutrition and FSH-induced ovarian hyperstimulation
title_short Transcriptomic alterations in the ovine caruncular endometrium due to imbalanced nutrition and FSH-induced ovarian hyperstimulation
title_sort transcriptomic alterations in the ovine caruncular endometrium due to imbalanced nutrition and fsh induced ovarian hyperstimulation
topic Sheep (Ovies aries)
Nutritional status
FSH-hyperstimulation
Transcriptome (RNA-seq)
url https://doi.org/10.1186/s12864-024-10799-w
work_keys_str_mv AT ozlembedir transcriptomicalterationsintheovinecaruncularendometriumduetoimbalancednutritionandfshinducedovarianhyperstimulation
AT migueltavarespereira transcriptomicalterationsintheovinecaruncularendometriumduetoimbalancednutritionandfshinducedovarianhyperstimulation
AT hubertrehrauer transcriptomicalterationsintheovinecaruncularendometriumduetoimbalancednutritionandfshinducedovarianhyperstimulation
AT annagrazulbilska transcriptomicalterationsintheovinecaruncularendometriumduetoimbalancednutritionandfshinducedovarianhyperstimulation
AT mariuszpkowalewski transcriptomicalterationsintheovinecaruncularendometriumduetoimbalancednutritionandfshinducedovarianhyperstimulation