Immunological aspects of ovarian follicle ovulation and corpus luteum formation in cattle

Abstract

Ovulation has been described as an inflammatory event, characterized by an influx of leukocytes into the ovulatory follicle and changes in the expression profile of immune factors in both the theca and granulosa tissue layers. Since information on this process is limited in cattle, our objective was to elucidate the contribution of the immune system to dominant follicle luteinization, ovulation and corpus luteum (CL) formation in cattle. Beef heifers (n = 50) were oestrous synchronized, slaughtered and ovarian follicular or luteal tissue collected during a 96 h window around ovulation. Follicular fluid cytokine concentration, temporal immune cell infiltration and inflammatory status were determined by Luminex multiplex analysis, immunohistochemistry and quantitative real-time PCR-analysis, respectively, in pre- and peri-ovulatory follicular tissues. The concentrations of IL10 and VEGF-A were highest in pre-ovulatory and the concentration of CXCL10 was highest in peri-ovulatory follicular fluid samples. The pre and peri-ovulatory follicles play host to a broad repertoire of immune cells, including T-cells, granulocytes and monocytes. Dendritic cells were the most abundant cells in ovulatory follicular and luteal-tissue at all times. The mRNA expression of candidate genes associated with inflammation was highest in pre- and peri-ovulatory tissue, whereas tissue growth and modelling factors were highest in the post-ovulatory follicular and early luteal tissue. In conclusion, ovulation in cattle is characterized by the presence of neutrophils, macrophages and dendritic cells in the ovulatory follicle, reflected in compartmentalized cytokine and growth factor expression. These findings indicate a tightly regulated sterile inflammatory response to the LH surge in the ovulatory follicle which is rapidly resolved in advance of CL formation.