In addition to androgens that are essential for maintenance of prostate growth and function, nonandrogenic hormones must also be considered to explain some regulatory events occurring in the prostate. The detection of LH/CG receptor (LH/CG-R) gene expression in some nongonadal tissues, has led us to consider LH as a potential regulatory factor of prostatic development and function. In this study, we have demonstrated by RT-nested polymerase chain reaction and Northern blotting that the rat prostate contains the same LH/CG-R transcript as the gonads. Western immunoblotting, ligand blotting, and binding analysis have shown that rat prostate also contains a 93-kDa receptor protein that is able td bind [I-125] hCG specifically and with a high affinity (6.0 x 10(9) M(-1)). Our results also indicated that the concentration of binding sites was lower in the prostate than in the gonads. LH/CG-R sites of expression have been localized in the prostate by immunohistochemistry: specific staining was observed in all the epithelial cells of the gland, but the ventral lobes are much more immunoreative than the lateral and dorsal lobes. Finally, the ability of this prostatic LH/CG-R to induce a physiological response was evaluated in an explant culture system. A timecourse experiment was carried out, and we observed a significant dose-dependent stimulation of cAMP production after 3 h of treatment: 3.0 +/- 0.4, 4.2 +/- 0.4, and 5.0 +/- 0.5 pmol/ml of cAMP for 0, 100, and 500 ng/ml of LH, respectively. In conclusion, LH is able to act directly on the prostatic gland through specific receptors that are structurally and functionally very similar to those expressed in the gonads and are mainly localized in the ventral lobe of the organ. These data suggest that LH plays a significant physiological role in the prostate.