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. 2006 Feb 21;103(8):2725-9.
doi: 10.1073/pnas.0509218103. Epub 2006 Feb 10.

Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish

Tomoyuki Okutsu  1 , Kensuke Suzuki, Yutaka Takeuchi, Toshio Takeuchi, Goro Yoshizaki
Affiliations

Testicular germ cells can colonize sexually undifferentiated embryonic gonad and produce functional eggs in fish

Tomoyuki Okutsu et al. Proc Natl Acad Sci U S A. .

Abstract

Understanding the mechanisms that regulate germ-cell development is crucial to reproductive medicine and animal production. Animal gametes originally derive from sexually undifferentiated primordial germ cells (PGCs), which develop into mitotic germ cells (oogonia or spermatogonia) before proceeding to meiosis [Wylie, C. (1999) Cell 96, 165-174]. Spermatogonia are thought to include a population of cells with stem cell activity, which proliferate throughout the lifespan of male animals and produce spermatozoa [Zhao, G. Q. & Garbers, D. L. (2002) Dev. Cell 2, 537-547]. However, the functional differences between PGCs and spermatogonial stem cells are poorly understood. Here we show that transplanted adult testicular germ cells can colonize sexually undifferentiated embryonic gonads and resume gametogenesis. Testicular germ cells containing spermatogonial stem cells isolated from adult male rainbow trout (Oncorhynchus mykiss) were transplanted into the peritoneal cavity of newly hatched embryos of both sexes, and the behavior of the donor cells was observed. The testicular germ cells differentiated into spermatozoa in male recipients and fully functional eggs in female recipients. Furthermore, the donor-derived spermatozoa and eggs obtained from the recipient fish were able to produce normal offspring. These findings indicate that fish testicular germ cells, probably spermatogonial stem cells, possess a high level of developmental plasticity and sexual bipotency, even after the animal reaches maturity. Furthermore, our results suggest that spermatogonial stem cells are at least partly functionally similar to PGCs.

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Conflict of interest statement

Conflict of interest statement: No conflicts declared.

Figures

Fig. 1.
Fig. 1.
Donor germ cells in recipient gonads after transplantation. (a–c) Incorporation of GFP-labeled donor germ cells into a recipient gonad at 20 days pt in bright-field view (a), fluorescent view (b), and highly magnified image of a flame in b (c). Arrowheads indicate donor-derived germ cells showing green fluorescence. (d and e) Proliferation of donor germ cells in a recipient testis at 2 months pt showing a ventral view of a recipient peritoneal cavity (d) and an isolated testis (e). (f–h) Vast proliferation of donor germ cells in a recipient testis at 7 months pt in bright-field view (f), fluorescent view (g), and according to immunohistochemistry using a GFP-specific antibody (h). (i and j) Proliferation of donor testicular germ cells in a recipient ovary at 2 months pt in bright-field view (i) and fluorescent view (j). (k and l) Donor testicular germ cell-derived oocytes in a recipient ovary at 7 months pt in fluorescent view (k) and according to immunohistochemistry using a GFP-specific antibody (l). (Bars: 100 μm, a–e and i–l; 1 mm, f and g; and 20 μm, h.)
Fig. 2.
Fig. 2.
Transplantation of spermatogonia after GFP-dependent flow cytometry. (a) Fluorescent intensity patterns of total testicular cells. The x axis represents the GFP intensity (logarithmic scale), and the y axis indicates the cell counts (linear scale). (b and c) Bright (b) and fluorescent (c) views of cells isolated with gate B. (Bars = 20 μm.) (d) The frequency to produce a GFP-positive germ-cell colony after the transplantation of GFP-positive or GFP-negative cell populations into allogenic recipients. Unsorted testicular cells were also transplanted as a control.
Fig. 3.
Fig. 3.
Donor-derived offspring obtained from progeny tests. (a) Donor-derived F1 offspring showing albino body color (arrow) derived from a male recipient. (b) Genital ridges (arrowheads) containing GFP-labeled germ cells in the donor-derived F1 offspring shown in a. (c) Donor-derived F1 offspring showing albino body color (arrow) derived from a female recipient. (d) Genital ridges (arrowheads) containing GFP-labeled germ cells in the donor-derived F1 offspring shown in c. (e) F1 offspring at 8 months old developed from testicular cell-derived eggs.
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