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Exposure to Phytoestrogens in the Perinatal Period Affects Androgen Secretion by Testicular Leydig Cells in the Adult Rat

Department of Anatomy, Physiology and Pharmacology (B.T.A., T.D.B., B.W.K., K.D.H., J.D.S.), Auburn University, Auburn, Alabama 36849; and Massachusetts General Hospital (S.J.C., X.H., J.G.S.), Harvard Medical School, Boston, Massachusetts 02114

Address all correspondence and requests for reprints to: Benson T. Akingbemi, D.V.M., Ph.D., Department of Anatomy, Physiology and Pharmacology, 109 Greene Hall, Auburn University, Auburn, Alabama 36849. E-mail: akingbt{at}auburn.edu.

The use of soy-based products in the diet of infants has raised concerns regarding the reproductive toxicity of genistein and daidzein, the predominant isoflavones in soybeans with estrogenic activity. Time-bred Long-Evans dams were fed diets containing 0, 5, 50, 500, or 1000 ppm of soy isoflavones from gestational d 12 until weaning at d 21 postpartum. Male rats in all groups were fed soy-free diets from postnatal d 21 until 90 d of age. The mean ± SD concentration of unconjugated (i.e. biologically active) genistein and daidzein in serum from the group of dams maintained on the diet containing the highest amount of isoflavones (1000 ppm) were 17 ± 27 and 56 ± 30 nM, respectively, at d 21 postpartum. The concentrations were considerably greater in male offspring (genistein: 73 ± 46 nM; daidzein: 106 ± 53 nM). Although steroidogenesis was decreased in individual Leydig cells, male rats from the highest exposure group (1000 ppm diet) exhibited elevated serum levels of the sex steroid hormones androsterone at 21 d (control: 15 ± 1.5 vs.28 ± 3.5 ng/ml; P < 0.05) and testosterone at 90 d of age (control: 7.5 ± 1 vs.17 ± 2 ng/ml; P < 0.05). Testosterone secretion by immature Leydig cells, isolated from 35-d-old male rats, decreased on exposure to 0.1 nM genistein in vitro (control: 175 ± 5 vs. 117 ± 3 ng/10⁶ cells per 24 h; P < 0.05), indicative of direct phytoestrogen action. Thus, phytoestrogens have the ability to regulate Leydig cells, and additional studies to assess potential adverse effects of dietary soy-based products on reproductive tract development in neonates are warranted.