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Previous work showed that pharmacological inactivation of Igf-binding proteins (Igfbps), modulators of Igf activity, resulted in an excessive differentiation of type A undifferentiated (A und ) spermatogonia in zebrafish testis in tissue culture when Fsh was present in the incubation medium. Using this testis tissue culture system, we studied here the regulation of  igfbp  transcript levels by Fsh and two of its downstream effectors, Igf3 and 11-ketotestosterone (11-KT). We also explored how Fsh-modulated  igfbp  expression affected spermatogonial proliferation by adding or removing the Igfbp inhibitor NBI-31772 at different times. Fsh (100 ng/mL) decreased the transcript levels of  igfbp1a, -3 , and  -6a  after 1 or 3 days, while increasing  igfbp2a  and  -5b  expression, but only after 5 days of incubation. Igf3 down-regulated the same  igfbp  transcripts as Fsh but with a delay of at least 4 days. 11-KT increased the transcripts ( igfbp2a  and  5b ) that were elevated by Fsh and decreased those of  igfbp6a , as did Fsh, while 11-KT did not change  igfbp1a  or  -3  transcript levels. To evaluate Igfbps effects on spermatogenesis, we quantified under different conditions the mitotic indices and relative section areas occupied by the different spermatogonial generations (type A und , type A differentiating (A diff ), or type B (B) spermatogonia). Igf3 (100 ng/mL) increased the area occupied by A diff  and B while decreasing the one for A und . Interestingly, a concentration of Igf3 that was inactive by itself (25 ng/mL) became active in the presence of the Igfbp inhibitor NBI-31772 and mimicked the effect of 100 ng/mL Igf3 on spermatogonia. Studies exploiting the different dynamics of  igfbp  expression in response to Fsh and adding or removing NBI-31772 at different times showed that the quick downregulation of three  igfbp  as well as the delayed upregulated of two  igfbps  all support Igf3 bioactivity, namely the stimulation of spermatogonial differentiation. We conclude that Fsh modulates, directly or  via  androgens and Igf3,  igfbp  gene expression, supporting Igf3 bioactivity either by decreasing  igfbp1a, -3, -6a  or by increasing  igfbp2a  and - 5b  gene expression.

frontiers in endocrinology

Follicle-Stimulating Hormone Regulates igfbp Gene Expression Directly or via Downstream Effectors to Modulate Igf3 Effects on Zebrafish Spermatogenesis