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Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish

Daisuke Uchida^1,2, Michiaki Yamashita^2,*, Takeshi Kitano³ and Taisen Iguchi^1,4,5

¹ Graduate School of Integrated Science, Yokohama City University, Seto, Kanazawa-ku, Yokohama 236-0027, Japan,
² National Research Institute of Fisheries Science, Fukuura, Kanazawa-ku, Yokohama 236-8648, Japan,
³ Department of Materials and Life Science, Graduate School of Science and Technology, Kumamoto University, Kumamoto 860-8555, Japan,
⁴ Center for Integrative Bioscience, Okazaki National Research Institutes, 38 Nishigonaka, Myodaiji, Okazaki 444-8585, Japan and
⁵ Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Corporation (JST)

View larger version (42K): [in a new window]   Fig. 1. Apoptotic oocytes in the ovary-like gonadal tissue. Sections of undifferentiated ovary-like gonads were made at 10 (A,B), 15 (C,D), 17 (E,F) and 19 (G,H) days post-hatching. Apoptotic oocytes were detected by TUNEL staining (B,D,F,H) and were counterstained with haematoxylin and eosin (A,C,E,G). Only a few TUNEL-positive oocytes (black and white arrowheads) were found at 15 days post-hatching (C,D), and apoptotic oocytes were often observed at 17 and 19 days post-hatching (E–H). A TUNEL-positive somatic cell (red arrowhead) was detected in the ovarian cavity at 19 days post-hatching (G,H). ed, early diplotene oocyte; go, gonocyte; oc, ovarian cavity; pa, pachytene oocyte; po, perinucleolar oocyte; sc, somatic cell. Scale bars, 20 µm.

View larger version (51K): [in a new window]   Fig. 2. Apoptotic oocytes and testicular germ cells in the male gonads. Sections were made at 23 (A,B), 25 (C,D) and 27 (E,F) days post-hatching, as the gonads changed from ovary-like tissue to testes, and mature testes were sectioned at 40 (G,H) and 70 (I,J) days post-hatching. Apoptotic cells were detected by TUNEL staining (B,D,F,H,J) and were counterstained with haematoxylin and eosin (A,C,E,G,I). Large numbers of TUNEL-positive oocytes (black and white arrowheads) were detected from 23 to 25 days post-hatching (A–D). Apoptotic spermatocytes (arrows) were detected at 40 days post-hatching (G,H). Large numbers of TUNEL-positive spermatogonia (yellow arrows), spermatocytes (black and white arrows) and spermatids (red arrows) were detected at 70 days post-hatching (I,J). TUNEL-positive somatic cells (red arrowhead) were detected in the ovarian cavity at 25 days post-hatching. An asterisk indicates the fragmented nucleus of an apoptotic oocyte. ed, early diplotene oocyte; oc, ovarian cavity; po, perinucleolar oocyte; sc, somatic cell; sg, spermatogonia; so, spermatocyte; sp, sperm. Scale bars, 20 µm.

View larger version (71K): [in a new window]   Fig. 3. Apoptotic somatic cells in ovarian connective tissues. Ovarian sections were made at 23 (A,B), 25 (C,D), 40 (E,F) and 70 (G,H) days post-hatching. Apoptotic cells were detected by TUNEL staining (B,D,F,H) and were counterstained with haematoxylin and eosin (A,C,E,G). Large numbers of TUNEL-positive somatic cells (black and white arrowheads) were detected in the ovarian connective tissue of genetic all-females from 23 to 50 days post-hatching. ca, cortical alveolar oocyte; oc, ovarian cavity; og, oogonia; po, perinucleolar oocyte; sc, somatic cell. Scale bars, 20 µm.

View larger version (26K): [in a new window]   Fig. 4. Percentage of TUNEL-positive oocytes in gonadal cells. Asterisks indicate significant (P<0.05) differences from genetic all-females (one-way ANOVA). Values are means ± S.E.M., N=10 fish.

View larger version (16K): [in a new window]   Fig. 5. Model for gonadal cell apoptosis. Typical cell types undergoing apoptosis during sex differentiation are illustrated. dph, days post-hatching. The width of each diamond represents the number of apoptotic gonadal cells.