Dietary polyunsaturated fatty acids can influence reproductive performance. In dairy cattle, some high-fat diets resulted in higher blastocyst rates and improved embryo quality. These effects may partly be mediated by a direct action of fatty acids on oocyte development. The present study investigated the effect of linolenic acid (ALA; 18:3 n-3) supplementation on bovine oocyte maturation and early embryo development in vitro. Treatment of cumulus-oocyte complexes (COCs) with 50 muM ALA significantly increased the percentage of oocytes at the metaphase II (MII) stage compared with untreated controls (95% +/- 2% vs. 84% +/- 2%, respectively). Higher doses of ALA were detrimental. Treatment of COCs with 50 muM ALA compared with controls also resulted in a significantly higher percentage of cleaved embryos (77% +/- 9% vs. 69% +/- 9%, respectively) and blastocyst rate (36% +/- 4% vs. 23% +/- 5%, respectively) and better-quality embryos. Furthermore, COCs treated with ALA had significant increases compared with controls in: 1) prostaglandin E(2) (PGE(2)) concentration (233% +/- 41%) in the medium, 2) intracellular cAMP at 3 h of maturation, and 3) phosphorylation of the mitogen-activated protein kinases (MAPKs) during the first 6 h of maturation. Moreover, ALA overcame the suppressive effects of the prostaglandin-endoperoxide synthase 2 inhibitor (NS-398) on oocyte maturation and partially improved the maturation rate in the presence of the MAPK kinase inhibitor (U-0126). Linolenic acid could not, however, recover maturation in the presence of both inhibitors. In conclusion, treatment of bovine COCs with ALA during oocyte maturation affects the molecular mechanisms controlling oocyte nuclear maturation, leading to an increased number of MII-stage oocytes and improved subsequent early embryo development. This effect is mediated both directly through MAPK pathway and indirectly through PGE(2) synthesis.