Elevations in Body Temperature: Impacts on the Transcriptome of the Periovulatory Follicle Components with Direct Effects on the Maturing Cumulus-Oocyte Complex

The mechanisms underlying the negative impact of chronic and/or severe peri-estrual increases in body temperature on reproduction are largely unknown. The working hypothesis for this research is that an acute elevation in body temperature after the LH surge impacts oocyte developmental competence and/or the intra-follicular environment of the periovulatory follicle as a result of perturbations of follicular cells or the interplay between the different types [i.e., granulosa and cumulus-oocyte complex (COC)]. Initial efforts found steady increases in THI to induce varying levels of elevated body temperature after the LH surge impacted the transcriptomes of granulosa and cumulus cells that surround the maturating oocyte at ~16 h post pharmacological induction of the LH surge. Using bulk RNA-sequencing, genes affected in the granulosa cells may impact ovulation and corpus luteum formation. Affected genes in the cumulus cells may have indirect but impactful consequences on the oocyte as it undergoes meiotic maturation.

In retrospect, positive outcomes suggest initial efforts may better represent the normal periovulatory follicle microenvironment resulting from an expected increase in body temperature of estrual females (cows and heifers) rather than chronic/severe conditions. Therefore, subsequent effort was to determine if consequences on the cumulus cell transcriptome were representative of outcomes throughout maturation in COCs that were exposed to an estrual-like heat “shock” [41°C for first 6 h in vitro maturation (hIVM)]. Within the first 4 hIVM, heat shock impacted 36 out of the 47 (76.6%) transcripts targeted for their possible role in cumulus-oocyte complex maturation events. Results suggest changes in genes that may be related to progesterone production and signaling, germinal vesicle breakdown, oocyte meiotic progression, transcriptional activity and/or alternative splicing, cell cycle, cumulus expansion, and/or ovulation. Only 4 transcripts, with unknown biological significance in the COC, demonstrated a delayed impact as changes were not seen until COCs recovered from the initial 6 h heat shock for 4 to 18 h. The findings discussed herein support the notion that a physiologically expected, acute increase in body temperature may promote periovulatory events, including meiotic progression, and could be used to improve reproductive efficiency when temperature is of proper duration and timing.