High Temperature Disrupts Organelle Distribution and Functions Affecting Meiotic Maturation in Porcine Oocytes

Abstract

Heat stress (HS) has been known to cause reproductive failure in animals, especially in summer. HS severely affects the developmental potential of oocytes and leads to low fertility rates. Previous studies have reported that HS compromises embryo development in bovine oocytes, and reduces ovarian development in mice, thereby impairing reproductive function in animals. However, the effect of high temperature (HT) on the organelles of porcine oocytes is unknown. In this study, we reported that exposure to HT for 24 h (41°C) significantly decreased meiotic maturation in porcine oocytes (p < 0.05). Further experiments on organelles found that HT induced mitochondrial dysfunction, increased abnormal mitochondrial distribution, and decreased mitochondrial membrane potential (MMP). We also found that HT induced abnormal endoplasmic reticulum (ER) distribution and higher expression of glucose regulatory protein 78 (GRP78), suggesting that HT exposure induces ER stress. Our results also indicated that exposure to HT induced abnormal distribution and dysfunction of the Golgi apparatus, which resulted from a decrease in the expression of the vesicle transporter, Ras-related protein Rab-11A (RAB11A). In addition, we found that HT exposure led to lysosomal damage by increasing the expression of lysosome-associated membrane protein 2 (LAMP2) and microtubule-associated protein 1A/1B-light chain 3 (LC3). In summary, our study revealed that HT exposure disrupts organelle dynamics, which further leads to the failure of meiotic maturation in porcine oocytes.

ATF7‐dependent epigenetic changes induced by high temperature during early porcine embryonic development

“…Heat stress is one of the most prevalent environmental stresses that negatively affects embryonic development. HT induces apoptosis in mouse follicles and increases mitochondrial ROS levels in bovine oocytes, while disrupting the arrangement of organelles in porcine oocytes 49–51 . To confirm the changes in ATF7 function in the context of stress, we used HT treatment during early porcine embryonic development.…”

“…HT induces apoptosis in mouse follicles and increases mitochondrial ROS levels in bovine oocytes, while disrupting the arrangement of organelles in porcine oocytes. 49 , 50 , 51 To confirm the changes in ATF7 function in the context of stress, we used HT treatment during early porcine embryonic development. We observed that HT induced the expression of pATF7 by activating P38, thereby reducing the levels of H3K9me2 and HP1 to affect the function of heterochromatin.…”

GRP78 acts as a cAMP/PKA signaling modulator through the MC4R pathway in porcine embryonic development

“…Immunofluorescence staining was performed as described previously. 24 Briefly, the embryos were washed three times with 1% PVA-PBS, fixed in 3.7% paraformaldehyde for 30 min at room temperature, and permeabilized with 1% Triton X-100 in PVA-PBS for 30 min at room temperature. The embryos were then incubated in 3% BSA in PVA-PBS for 1 h at room temperature.…”

Mitofusins: from mitochondria to fertility

“…In mice, the abnormal aggregation of the mitochondria also disables the functionality of MAMs, thus leading to a reduction in mitochondrial OXPHOS and the Krebs cycle. In combination, the imbalance in mitochondrial homeostasis and abnormal mitochondrial distribution caused by abnormal mitochondrial function ultimately leads to meiotic failure [ 127 , 128 ]. The deletion of Mfn2 in mouse oocytes leads to increased levels of ceramide; this induces apoptosis in oocytes by releasing cytochrome C from the mitochondria and activating caspases, thus triggering the arrest of follicular development [ 76 ].…”