Heat-induced hyperthermia impacts the follicular fluid proteome of the periovulatory follicle in lactating dairy cows

• DOI: 10.1371/journal.pone.0227095
• Publication Date: 2019-12-30T13:37:58Z
• Authors: Louisa A. Rispoli; J. Lannett Edwards; Ky G. Pohler; Stephen Russell; Richard I. Somiari; Rebecca R. Payton; F. Neal Schrick
• Keywords: Ovulation; Proteomics; 2. Zero hunger; 0303 health sciences; Cumulus Cells; Hot Temperature; Proteome; Science; Q; R; Transferrin; Bradykinin; Heat Stress Disorders; Tennessee; Follicular Fluid; Gonadotropin-Releasing Hormone; 03 medical and health sciences; Medicine; Animals; Lactation; Cattle; Female; Animal Husbandry; Research Article

We hypothesized that heat-induced perturbations in cumulus cells surrounding the maturing oocyte may extend to the mural granulosa of the periovulatory follicle in the heat-stressed cow to subsequently the follicular fluid proteome. Lactating Holsteins were pharmacologically stimulated to have a dominant follicle that was capable of responding to a gonadotropin releasing hormone-induced luteinizing hormone surge. Following gonadotropin releasing hormone administration, cows were maintained at ~67 temperature humidity index (THI; thermoneutral conditions) or exposed to conditions simulating an acute heat stress event (71 to 86 THI; heat stress for ~12 h). Dominant follicle collection was conducted in the periovulatory period ~16 h after gonadotropin releasing hormone. Follicular fluid proteome from thermoneutral (n = 5) and hyperthermic (n = 5) cows was evaluated by quantitative tandem mass spectrometry (nano LC-MS/MS). We identified 35 differentially-abundant proteins. Functional annotation revealed numerous immune-related proteins. Subsequent efforts revealed an increase in levels of the proinflammatory mediator bradykinin in follicular fluid (P = 0.0456) but not in serum (P = 0.9319) of hyperthermic cows. Intrafollicular increases in transferrin (negative acute phase protein) in hyperthermic cows (P = 0.0181) coincided with a tendency for levels to be increased in the circulation (P = 0.0683). Nine out of 15 cytokines evaluated were detected in follicular fluid. Heat stress increased intrafollicular interleukin 6 levels (P = 0.0160). Whether hyperthermia-induced changes in the heat-stressed cow's follicular fluid milieu reflect changes in mural granulosa, cumulus, other cell types secretions, and/or transudative changes from circulation remains unclear. Regardless of origin, heat stress/hyperthermia related changes in the follicular fluid milieu may have an impact on components important for ovulation and competence of the cumulus-oocyte complex contained within the periovulatory follicle.