Characterization and analysis of transcriptomes of multiple tissues from estrus and diestrus in pigs

Mingzheng Liu; Chunlei Zhang; Jiahao Chen; Qinglei Xu; Shuhan Liu; Xiaohuan Chao; Huan Yang; Tianshuo Wang; Asim Muhammad; Allan P Schinckel; Bo Zhou

doi:10.1016/j.ijbiomac.2023.128324

Characterization and analysis of transcriptomes of multiple tissues from estrus and diestrus in pigs

Int J Biol Macromol. 2024 Jan;256(Pt 1):128324. doi: 10.1016/j.ijbiomac.2023.128324. Epub 2023 Nov 23.

Authors

Mingzheng Liu¹, Chunlei Zhang², Jiahao Chen³, Qinglei Xu⁴, Shuhan Liu⁵, Xiaohuan Chao⁶, Huan Yang⁷, Tianshuo Wang⁸, Asim Muhammad⁹, Allan P Schinckel¹⁰, Bo Zhou¹¹

Affiliations

¹ College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China. Electronic address: liumingzheng@stu.njau.edu.cn.
² College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China. Electronic address: 2020105039@stu.njau.edu.cn.
³ College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China. Electronic address: chenjiahao@stu.njau.edu.cn.
⁴ College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China. Electronic address: 2019205004@njau.edu.cn.
⁵ College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China. Electronic address: 2022105002@stu.njau.edu.cn.
⁶ College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China. Electronic address: 2021205020@stu.njau.edu.cn.
⁷ College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China. Electronic address: 2021105038@stu.njau.edu.cn.
⁸ College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China. Electronic address: 2022805106@stu.njau.edu.cn.
⁹ College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China. Electronic address: 2022105147@stu.njau.edu.cn.
¹⁰ Department of Animal Sciences, Purdue University, West Lafayette, IN 47907-2054, USA. Electronic address: aschinck@purdue.edu.
¹¹ College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China. Electronic address: zhoubo@njau.edu.cn.

PMID: 38007026
DOI: 10.1016/j.ijbiomac.2023.128324

Abstract

A comprehensive understanding of the complex regulatory mechanisms governing estrus and ovulation across multiple tissues in mammals is imperative to improve the reproductive performance of livestock and mitigate ovulation-related disorders in humans. To comprehensively elucidate the regulatory landscape, we analyzed the transcriptome of protein-coding genes and long intergenic non-coding RNAs (lincRNAs) in 58 samples (including the hypothalamus, pituitary, ovary, vagina, and vulva) derived from European Large White gilts and Chinese Mi gilts during estrus and diestrus. We constructed an intricate regulatory network encompassing 358 hub genes across the five examined tissues. Furthermore, our investigation identified 85 differentially expressed lincRNAs that are predicted to target 230 genes associated with critical functions including behavior, receptors, and apoptosis. Importantly, we found that vital components of estrus and ovulation events involve "Apoptosis" pathway in the hypothalamus, "Autophagy" in the ovary, as well as "Hypoxia" and "Angiogenesis" in the vagina and vulva. We have identified several differentially expressed transcription factors (TFs), such as SPI1 and HES2, which regulate these pathways. SPI1 may suppress transcription in the autophagy pathway, promoting apoptosis and inhibiting the proliferation of ovarian granulosa cells. Our study provides the most comprehensive transcriptional profiling information related to estrus and ovulation events.

Keywords: Estrus; Multi-tissue transcriptome; Ovulation; Regulatory network; SPI1.

MeSH terms

Animals
Diestrus / physiology
Estrus / genetics
Female
Humans
RNA, Long Noncoding*
Sus scrofa / genetics
Swine
Transcriptome* / genetics

Substances

RNA, Long Noncoding