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First published online 15 October 2003
doi: 10.1242/dev.00836

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Meiotic germ cells antagonize mesonephric cell migration and testis cord formation in mouse gonads

Humphrey H.-C. Yao^*, Leo DiNapoli and Blanche Capel

Department of Cell Biology, Duke University, Durham NC 27710, USA

View larger version (68K): [in a new window]   Fig. 3. Co-culture experiments suggest that meiotic germ cells inhibit the testis pathway via short-range effects. An 11.5 or 14.5 dpc XX GFP gonad (green) was cultured on top of an 11.5 dpc XY gonad for 48 hours. In situ hybridization for Sox9 (dark purple) or immunocytochemical staining for laminin (blue) and germ cells and vasculature (red), reveal no interference with the testis pathway. Red and blue broken lines outline the XX and XY components, respectively. Broken white lines outline the mesonephros. Arrows indicate testis cord boundaries.

View larger version (43K): [in a new window]   Fig. 1. In the absence of germ cells, mesonephric cells can be induced to migrate into 14.5 dpc XX gonads. An 11.5 or 14.5 dpc XX gonad from a wild type (+/+), KitW/W-v embryo or busulfan-treated embryo was cultured between an 11.5 dpc XY gonad and an 11.5 dpc GFP mesonephros for 48 hours. Broken blue lines outline the XY components; broken red lines outline the XX components.

View larger version (149K): [in a new window]   Fig. 2. Meiotic germ cells interfere with cord formation. Germ cells and somatic cells were isolated using an immunomagnetic cell sorting system. Somatic cell fractions from 12.5 dpc XY gonads were aggregated with 11.5 dpc XX germ cell fraction (A), 11.5 dpc XY germ cell fraction (B), 14.5 dpc XX somatic fraction (C) or 14.5 dpc XX germ cell fraction (D) and cultured for 48 hours. Formation of testis cords was shown by immunostaining for laminin (green), a component of the basal lamina of testis cords (red arrows).

View larger version (123K): [in a new window]   Fig. 4. Two meiotic markers, SYN/COR (A) and H2AX (B), are expressed in an anterior to posterior pattern in 13.5-15.5 dpc XX gonads: SYN/COR and H2AX (green); germ cells and vasculature (PECAM-1, red). A higher magnification of the region surrounded by the white rectangle is shown below the corresponding image. Consecutive 8 µm sections were stained with each antibody to define the spatial relationship between SYN/COR and H2AX. Arrows indicate the leading front of staining at 14.5 dpc. Arrowheads indicate the first detection of SYN/COR at 13.5 dpc and the filamentous pattern associated with the assembly of homologous chromatid pairs in zygotene/pachytene at 14.5 dpc. A, anterior; P, posterior.

View larger version (109K): [in a new window]   Fig. 5. Meiotic germ cells are present transiently in XY gonads in the region of the rete testis. (A) SYN/COR and (B) H2AX were detected by immunofluorescence (green) in consecutive 8 µm sections; germ cells were labeled with PECAM1 (red). (C) A higher magnification of the region surrounded by the white rectangle in A. (D) At 15.5 dpc, apoptotic cells in this region were labeled with LysoTracker (magenta); germ cells were labeled with PECAM (red); the basal lamina of testis cords was stained for laminin (green). Arrows indicate germ cells. A, anterior; P, posterior; G, gonad; M, mesonephros; MT, mesonephric tubule; TC, testis cord.

View larger version (43K): [in a new window]   Fig. 6. A model for the antagonistic role of meiotic germ cells on the testis pathway. In normal XX gonads, germ cells follow an intrinsic clock and enter meiosis by 13.5 dpc. In normal XY gonads, expression of Sry at 10.5-12.5 dpc initiates cord formation prior to entry of germ cells into meiosis. Cord formation blocks germ cell entry into meiosis. Molecules on the surface of germ cells or short-range diffusible factors from germ cells may be permissive for testis cord formation only until germ cells commit to meiosis when their surface properties may change. A temporal mismatch experimentally created by combining meiotic germ cells with 12.5 dpc XY somatic cells led to failure of testis cord formation.

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