The polymeric immunoglobulin receptor (poly Ig-R) mediates transcytosis of IgA and IgM antibodies produced by local plasma cells across epithelial cells of mucosal and glandular tissues. Gene expression of the poly-Ig R was analyzed in rabbit mammary gland during pregnancy and lactation. The poly Ig-R was expressed as early as day 8 (G8) of gestation and mRNA accumulation remained low until about G18. From G21, the mRNA abundance increased and reached steady state levels approximately 5-fold higher at day 15 of lactation (L15) when compared to basal levels at G8. The hormonal regulation of poly-Ig receptor gene expression was assessed in mammary organ cultures. Poly-Ig R mRNA accumulation in mammary explants cultured for 24 or 48 h in the presence of ovine prolactin (oPRL) was significantly increased to a maximal 4-fold level at 1 microgram ml-1 of oPRL. Estradiol (100 pg ml-1) or progesterone (1 microgram ml-1) did not further stimulate poly-Ig R expression. In contrast, their combination resulted in a significant 30-50% decrease of poly-Ig-R mRNA levels. The addition of 1 microgram ml-1 of cortisol to medium in the absence or presence of estradiol or progesterone decreased the amount of poly-Ig-R mRNA. The results suggest that until mid-pregnancy, poly-Ig-R expression is inhibited by elevated progesterone-estradiol concentrations and that the subsequent increase is due to the concomitant decrease of the two circulating steroids and the increase of serum prolactin levels.