Single-cell transcriptomic characterization of sheep conceptus elongation and implantation

Gong-Xue Jia; Wen-Ji Ma; Zhao-Bo Wu; Shuang Li; Xiao-Qian Zhang; Zhen He; Shi-Xin Wu; Hai-Ping Tao; Yi Fang; Yong-Wu Song; Shang-Rong Xu; Xiao-Qun Wang; Qi-En Yang

doi:10.1016/j.celrep.2023.112860

Single-cell transcriptomic characterization of sheep conceptus elongation and implantation

Cell Rep. 2023 Aug 29;42(8):112860. doi: 10.1016/j.celrep.2023.112860. Epub 2023 Jul 25.

Authors

Gong-Xue Jia¹, Wen-Ji Ma², Zhao-Bo Wu³, Shuang Li⁴, Xiao-Qian Zhang⁴, Zhen He⁵, Shi-Xin Wu⁵, Hai-Ping Tao⁵, Yi Fang⁶, Yong-Wu Song⁷, Shang-Rong Xu⁸, Xiao-Qun Wang⁹, Qi-En Yang¹⁰

Affiliations

¹ Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810001, China; University of Chinese Academy of Sciences, Beijing 100049, China; Qinghai Key Laboratory of Animal Ecological Genomics, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810001, China.
² State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China; Center for Single-Cell Omics, School of Public Health, Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China.
³ State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China.
⁴ Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810001, China.
⁵ Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810001, China; University of Chinese Academy of Sciences, Beijing 100049, China.
⁶ University of Chinese Academy of Sciences, Beijing 100049, China; Jilin Provincial Key Laboratory of Grassland Farming, Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102, China.
⁷ Animal Husbandry and Veterinary Station of Gangcha, Haibei 812300, China.
⁸ Qinghai Academy of Animal Science and Veterinary Medicine, Qinghai University, Xining 810016, China.
⁹ State Key Laboratory of Brain and Cognitive Science, CAS Center for Excellence in Brain Science and Intelligence Technology, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China. Electronic address: xiaoqunwang@ibp.ac.cn.
¹⁰ Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810001, China; University of Chinese Academy of Sciences, Beijing 100049, China; Qinghai Key Laboratory of Animal Ecological Genomics, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810001, China. Electronic address: yangqien@nwipb.cas.cn.

PMID: 37494181
DOI: 10.1016/j.celrep.2023.112860

Abstract

Bidirectional communication between the developing conceptus and endometrium is essential for pregnancy recognition and establishment in ruminants. We dissect the transcriptomic dynamics of sheep conceptus and corresponding endometrium at pre- and peri-implantation stages using single-cell RNA sequencing. Spherical blastocysts contain five cell types, with 68.62% trophectoderm cells. Strikingly, elongated conceptuses differentiate into 17 cell types, indicating dramatic cell fate specifications. Cell-type-specific gene expression delineates the features of distinctive trophectoderm lineages and indicates that the transition from polar trophectoderm to trophoblast increases interferon-tau expression and likely drives elongation initiation. We identify 13 endometrium-derived cell types and elucidate their molecular responses to conceptus development. Integrated analyses uncover multiple paired transcripts mediating the dialogues between extraembryonic membrane and endometrium, including IGF2-IGF1R, FGF19-FGFR1, NPY-NPY1R, PROS1-AXL, and ADGRE5-CD55. These data provide insight into the molecular regulation of conceptus elongation and represent a valuable resource for functional investigations of pre- and peri-implantation ruminant development.

Keywords: CP: Developmental biology; conceptus elongation; endometrium; extraembryonic membrane; interferon-tau; ligand-receptor interaction; lineage determination; peri-implantation development; ruminant; trophectoderm; uterine receptivity.