Single-cell transcriptomic architecture and cellular communication circuits of parametrial adipose tissue in pregnant mice

Akiko Yano; Shuang Liu; Yasuyuki Suzuki; Matome Imai; Masaki Mogi; Takashi Sugiyama

doi:10.1016/j.lfs.2023.122214

Single-cell transcriptomic architecture and cellular communication circuits of parametrial adipose tissue in pregnant mice

Life Sci. 2023 Dec 1:334:122214. doi: 10.1016/j.lfs.2023.122214. Epub 2023 Oct 29.

Authors

Akiko Yano¹, Shuang Liu², Yasuyuki Suzuki³, Matome Imai¹, Masaki Mogi⁴, Takashi Sugiyama⁵

Affiliations

¹ Department of Obstetrics & Gynecology, Ehime University School of Medicine, Shitsukawa, Toon, Ehime, Japan; Department of Pharmacology, Ehime University Graduate School of Medicine, Shitsukawa, Toon, Ehime, Japan.
² Department of Pharmacology, Ehime University Graduate School of Medicine, Shitsukawa, Toon, Ehime, Japan. Electronic address: liussmzk@m.ehime-u.ac.jp.
³ Department of Pharmacology, Ehime University Graduate School of Medicine, Shitsukawa, Toon, Ehime, Japan; Department of Anesthesiology, Saiseikai Matsuyama Hospital, Matsuyama, Japan; Research Division, Saiseikai Research Institute of Health Care and Welfare, Tokyo, Japan.
⁴ Department of Pharmacology, Ehime University Graduate School of Medicine, Shitsukawa, Toon, Ehime, Japan.
⁵ Department of Obstetrics & Gynecology, Ehime University School of Medicine, Shitsukawa, Toon, Ehime, Japan.

PMID: 37907153
DOI: 10.1016/j.lfs.2023.122214

Abstract

Aims: The activity and interactions of cellular subpopulations in the adipose tissue microenvironment are critical for the coordination of local and systemic adaptation during pregnancy. With a particular interest in parametrial adipose tissue (PmAT), single-cell RNA-sequencing (scRNA-seq) was utilized to unveil the gestative cellular composition and functional shift.

Materials and methods: To identify cell-type-enriched transcriptome profiles, a total of 18,074 cells in adipose tissue were studied. The cell populations were cataloged, and signaling crosstalk between adipocytes and other composition factions via soluble and membrane-bound factors were evaluated.

Key findings: A marked decline of pregnancy adipocytes and relative elevation of non-adipocyte fractions were observed. A subpopulation of adipocytes, Adipo_5, with unique properties in the response to estrogen and the embryonic processes involved in pregnancy, was defined. Interactome analysis revealed the potential contribution of PmAT to the establishment of maternal-fetal immune tolerance. During gestation, adipocytes shut down outgoing signaling, resulting in deterioration of the resistin-related incoming signaling network in B cells, which would therefore benefit tissue-specific maternal-fetal tolerance. Furthermore, a subpopulation of adipocytes, Aipo_2, was also considered to take part in a paradigm shift in the process of pregnancy-induced chemical stiffness-triggered vesicular remodeling via the THBS signaling pathway network.

Significance: These data-derived findings will encourage investigation into the role of pregnant PmTA in pregnancy-related immunological, hypertensive and metabolic disorders, with the ultimate goal of establishing preventive strategies to mitigate these pregnancy-related health challenges. This translational aspect of our work holds significant promise for improving maternal and fetal well-being.

Keywords: Adipose-immune interaction; Parametrial adipose tissue; Pregnancy; Single-cell RNA-seq, intercellular communication.

MeSH terms

Adipocytes / metabolism
Adipose Tissue* / metabolism
Animals
Cell Communication
Female
Gene Expression Profiling
Mice
Pregnancy
Transcriptome*