Cumuli oophori surrounding ovulated oocytes of B10.BR(Ydel) females (sired by males with the Y-chromosome long-arm deletion) are more resistant to hyaluronidase digestion than cumuli oophori around eggs of genetically identical females but sired by males with the intact Y chromosome (B10.BR). This has been interpreted as a result of differences in paternal genome imprinting, which females of both groups inherit from their fathers. The following study shows that it is not hyaluronan, but rather excessive protein concentration, that makes the cumulus extracellular matrix of B10.BR(Ydel) oocytes more resistant to enzymatic treatment. It was revealed, additionally, that cumulus cells around ovulating oocytes of B10.BR(Ydel) females display higher surface accumulation of prostaglandin EP2 subtype receptors and higher expression of the Ptgs2 gene (encoding a rate-limiting enzyme of prostaglandin E2 synthesis) in relation to the cells of control B10.BR females. The expression levels of the prostaglandin-dependent Tnfaip6 and Ccl2 genes were also altered in B10.BR(Ydel) cumulus cells in a manner indicating increased prostaglandin signalling. The study provides further evidence for the divergence in reproductive phenotypes between B10.BR and B10.BR(Ydel) female mice. It supports the hypothesis that genes of the Y-chromosome long arm may be involved in establishment of epigenetic marks in X-bearing spermatozoa.