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Thyroid Hormone Effects on Mouse Oocyte Maturation and Granulosa Cell Aromatase Activity¹

Departments of Experimental Medicine and Science and Biomedical Technologies, University of L’Aquila (S.C., M.P.M., G.R.), 67100 L’Aquila; the Department of Internal Medicine, University of Rome Tor Vergata (M.L.S., C.M.), 00173 Rome; and the Department of Experimental Medicine and Pathology, University of Rome La Sapienza (M.D.), 00161 Rome, Italy

Address all correspondence and requests for reprints to: Dr. Salvatore Ulisse, Department of Experimental Medicine, University of L’Aquila, Via Vetoio, 67100 L’Aquila, Italy. E-mail: ulisse{at}univaq.it

In the present study we evaluated the role of T₃ on the in vitro processes of mouse cumulus cell-oocyte complex expansion, oocyte meiotic maturation, and granulosa cell aromatase activity. Results obtained from cumuli oophori isolated from immature and adult mice ovaries demonstrated that T₃ at all concentrations tested (0.1–100 nM) did not affect basal or FSH-induced cumulus expansion or interfere with oocyte meiotic maturation up to metaphase II stage. On the contrary, T₃ inhibited in a time- and dose-dependent manner FSH-induced aromatase activity in cultured granulosa cells obtained from either adult or immature female mice. The half-maximal dose (ED₅₀) of T₃ inhibition was 0.87 ± 0.21 nM, which is in agreement with the reported dissociation constant of T₃ nuclear receptor (K_d = 0.4–5 nM) in mammalian granulosa cells. Time-course experiments demonstrated higher sensitivity to T₃ of adult granulosa cells with respect to immature granulosa cells in culture. Indeed, in immature granulosa cells T₃ inhibition became significantly evident only after 6 days of hormonal treatment, whereas in adult granulosa cells the inhibitory effect was present after only 2 days of treatment. (Bu)₂cAMP- or 3-isobutyl-1-methyl-xanthine-stimulated aromatase activity was also significantly decreased by T₃, thus suggesting that the inhibition was downstream from cAMP formation. Lastly, analysis of aromatase messenger RNA (mRNA) levels by semiquantitative RT-PCR demonstrated the ability of FSH to increase aromatase mRNA level in cultured granulosa cells by 2.4 ± 0.5-fold. In agreement with the effect on enzyme activity, the stimulatory effect of FSH on aromatase mRNA level was greatly reduced after T₃ cotreatment. In conclusion, T₃ inhibition of aromatase activity may be of physiological relevance in the complex multihormonal regulation of mammalian follicle development and may contribute to explaining the alteration in female reproductive functions after thyroid hormone hypo- or hypersecretion.

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