Transcriptomic responses of porcine cumulus cells to heat exposure during oocytes in vitro maturation

Abstract

The oocyte is vulnerable to various environmental stressors, including heat exposure. Cumulus-oocyte complexes (COCs) comprise functional units for oocytes in vitro maturation, and the cumulus cells provide essential supports and protect the oocyte from environmental insults. Heat exposure results in varied consequences in oocyte, presumably due to different responses of cumulus cells to heat exposure. In this study, we examined whether heat exposure of different duration affects porcine oocytes quality differently, and how such effects, if any, relate to transcriptomic profiles of cumulus cells. COCs were heat-exposed for 4 h (20-24 h, COC4) and 24 h (0-24 h, COC24), respectively, and the quality of oocytes in COC24 group showed significantly impaired with disrupted cumulus expansion and extracellular matrix (ECM) structure. The transcriptomic analysis identified 749 and 1238 differential expression genes (DEGs) in COC4 and COC24, respectively. Moreover, 852 DEGs were found when COC24 was compared with COC4, and the downregulated DEGs were mainly associated with Gene Ontology terms linked with ECM and cell proliferation. In the protein-protein interaction network, HSPE1, TNFAIP6, COL12A1, and COL18A1 were identified as hub genes playing important roles in heat-induced transcriptomic responses. These results indicate that impaired cumulus proliferation and ECM structure are responsible for heat-induced damage in oocytes quality. K E Y W O R D S cumulus cells, heat exposures, pig, transcriptomes 1 | INTRODUCTION Oocytes are surrounded by multilayered cumulus cells (CCs) to form cumulus-oocyte complex (COC), a functional unit for oocyte maturation. COCs can be cultured in vitro for oocytes maturation, and porcine oocytes usually require 42-48 h to reach metaphase II in culture. Cumulus cells are essential in the maturation process of oocytes, not only transmit bioactive substances and energy materials to oocytes, but also protect the oocytes from the interference of the external environment (Gilchrist et al., 2004). During oocytes maturation, cumulus cells proliferate, differentiate, and communicate with each other via extracellular matrix (ECM) and through gap junctions (Campen et al., 2018), adherens (Mora et al., 2012), and tight junctions (Clelland & Kelly, 2010). They also send transzonal projections (Yin et al., 2019) to interact with the enclosed oocyte. ECM not only provides a physical scaffold for cell-cell interactions, but also plays a key role in normal follicular growth, oocyte development, ovulation, and luteinization (Kimura et al., 2007). Oocytes are susceptible to various environmental stresses, including heat exposure. Heat-induced alterations in oocyte quality depend on timing, duration, and the extent of the exposure. For instance, COCs aspirated from multiparous Holstein cows in cold (December-April) seasons had a higher cleavage and blastocyst rates than in hot (May-September) seasons (Gendelman & Roth, 2012).

Comparative Analysis of Epididymis Cauda of Yak before and after Sexual Maturity

“…COL12A1 is significantly expressed in loosely attached embryos. In addition to regulating cell adhesion and migration, COL12A1 is involved in maintaining the structural integrity of the cumulus–oocyte complex [ 42 , 43 ]. This significantly expressed collagen family member may be widely involved in the development of epididymal cauda tissue and promote gonadal maturation.…”

Selective sweep analysis of the adaptability of the Yarkand hare (Lepus yarkandensis) to hot arid environments using SLAF‐seq

“…Heat stress can be considered cytotoxic because it alters biological molecules, disturbs cell functions and induces oxidative cell damage (Belhadj Slimen et al., 2016). HSPE1 encodes a 10 kDa heat shock protein (HSP10) that mediates the correct folding of proteins under stress conditions (Liu et al., 2021). SLC23A1 encodes the sodium‐dependent vitamin C transporter, which mediates the absorption and transport of vitamin C (Corpe et al., 2010).…”