Evidence for Almost Complete Sex-reversal in Bovine Freemartin Gonads: Formation of Seminiferous Tubule-like Structures and Transdifferentiation into Typical Testicular Cell Types

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  • HARIKAE Kyoko
    Department of Veterinary Anatomy, The University of Tokyo, Tokyo 113-8657, Japan
  • TSUNEKAWA Naoki
    Department of Veterinary Anatomy, The University of Tokyo, Tokyo 113-8657, Japan
  • HIRAMATSU Ryuji
    Department of Veterinary Anatomy, The University of Tokyo, Tokyo 113-8657, Japan Department of Molecular Embryology, Osaka Medical Center and Research Institute for Maternal and Child Health, Osaka Prefectural Hospital Organization, Osaka 594-1101, Japan
  • TODA Syohei
    Maebashi Institute of Animal Science, Livestock Improvement Association of Japan, Inc., Gunma 371-0121, Japan
  • KUROHMARU Masamichi
    Department of Veterinary Anatomy, The University of Tokyo, Tokyo 113-8657, Japan
  • KANAI Yoshiakira
    Department of Veterinary Anatomy, The University of Tokyo, Tokyo 113-8657, Japan

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During mammalian sex determination of XY fetuses, SRY induces SOX9 in Sertoli cells, resulting in formation of testes with seminiferous tubules, interstitial Leydig cells and peritubular myoid cells. Meanwhile XX fetuses without SRY develop ovaries. In cattle, most XX heifers born with a male twin, so-called freemartins, develop nonfunctioning ovaries and genitalia with an intersex phenotype. Interestingly, freemartins sometimes develop highly masculinized gonads with seminiferous tubule-like structures despite the absence of SRY. However, in these cases, the degree of masculinization in each gonadal somatic cell type is unclear. Here, we report a rare case of a freemartin Japanese black calf with almost complete XX sexreversal. Gross anatomical analysis of this calf revealed the presence of a pair of small testis-like gonads with rudimentary epididymides, in addition to highly masculinized genitalia including a pampiniform plexus, scrotum and vesicular gland. Histological and immunohistochemical analyses of these masculinized gonads revealed well-defined seminiferous tubule-like structures throughout the whole gonadal parenchyma. In epithelia of these tubules, SOX9-positive supporting cells (i.e., Sertoli cells) were found to be arranged regularly along the bases of tubules, and they were also positive for GDNF, one of the major factors for spermatogenesis. 3β-HSD-positive cells (i.e., Leydig cells) and SMA-positive peritubular myoid cells were also identified around tubules. Therefore, for the first time, we found the transdifferentiation of ovarian somatic cells into all testicular somatic cell types in the XX freemartin gonads. These data strongly support the idea of a high sexual plasticity in the ovarian somatic cells of mammalian gonads.

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