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Coordinating the segregation of sister chromatids during the first meiotic division: evidence for sexual dimorphism

Department of Genetics and Center for Human Genetics, Case Western Reserve University and University Hospitals of Cleveland, Cleveland, Ohio 44106-4955, USA

View larger version (28K): [in a new window]   Fig. 1. Segregation of X chromosome homologs and univalents at MI. Left: Cartoons depict MI segregation of (A) X homologs to the oocyte and polar body in control XX females, (B) intact segregation and (C) precocious segregation of sister chromatids (PSCS) of the univalent X chromosome in oocytes from XO females (Note that the termed ‘precocious’ refers to the fact that sister segregation occurs at MI rather than MII; a physical association is maintained between the sister chromatids until anaphase I). Right: Actual images of oocyte and polar body chromosomes in MII arrested oocytes from XX and XO females, hybridized with an X-chromosome specific probe. In all images, the group of chromosomes (red) segregated to the polar body at MI is on the right and the group remaining in the oocyte is on the left. Each FISH signal (yellow) represents a single X chromatid. (A) Normal MI segregation of homologs results in two X signals (or one doublet) in both the oocyte and polar body; (B) intact segregation of the univalent X is evident either as two signals in the egg or in the polar body (not shown); (C) PSCS of the univalent X chromosome is evident as a single signal in both the oocyte and the polar body.

View larger version (44K): [in a new window]   Fig. 2. Analysis of X chromosome synapsis in pachytene stage oocytes. (A) Pachytene stage oocyte from an XO female mouse immunostained with an antibody to SCP3 (green) to visualize the lateral elements of the SC, and hybridized with X-chromosome specific (purple) and telomere-specific (red) probes. The dispersed X chromosome signal (arrow) is due to the nature of the probe (DXWAS70 detects a multicopy sequence close to the centromere of the X chromosome) and the decondensed state of the chromatin at this stage. (B-F) Synaptic configurations of the univalent X chromosome during pachytene, (B) ‘asynapsed’ X chromosome showing a lateral element with telomeres present at both ends, (C) ‘fully self-synapsed’ X chromosome forming a hairpin structure with overlapping telomeres that appear as a single signal, (D) ‘partial self-synapsis including the centromere’ showing a portion of the lateral element synapsed with both telomeres overlapping and appearing as one, (E) ‘partial self-synapsis excluding the centromere’ showing a portion of the lateral element synapsed with two telomeres distinguishable, (F) ‘X/autosome association’ showing a triradial structure with three telomeres representing the X and an autosomal bivalent.

View larger version (24K): [in a new window]   Fig. 3. Colocalization of SCP1 and SCP3 on the univalent X chromosome. (A-C) Combined SCP3 and SCP1 staining (green and red respectively, with yellow colocalization) and FISH with X-chromosome specific (purple) and telomeric (purple) probes. (D-F) SCP1 staining alone. (A,D) ‘Fully self-synapsed’ X chromosome showing colocalization of SCP3 and SCP1 (yellow) along the length of the SC. (B,E) ‘Asynapsed’ X chromosome showing no evidence of SCP1 staining. (C,F) ‘Asynapsed’ X chromosome showing SCP1 staining along the entire length of the SC. Note: the magnification is the same in all images; however, SC length is dependent upon the stage of the cell (e.g. B,E represent early pachytene) and the synaptic behavior of the X (e.g. the fully self-synapsed X, as in A,D, is half the length of the asynapsed X, as in C,F).

View larger version (17K): [in a new window]   Fig. 4. Percentage of pachytene oocytes with an asynapsed X chromosome on successive days of gestation. The two strains used in this study, C57Bl/6 (squares) and C3H (triangles), exhibit an initial decline in such cells followed by a slight increase while the Swiss Albino strain (diamonds) (used by Speed et al., 1986), exhibits a steady decline.

View larger version (52K): [in a new window]   Fig. 5. SCP2/ SCP3 localization at diakinesis/metaphase I in spermatocytes and oocytes. (A,C) Chromosomes (blue) immunostained with CREST antiserum, which localizes to the centromeres (green). (B,D) Chromosomes (blue) and SCP3 localization (red). (A,B) Two spermatocytes at diakinesis/MI exhibiting SCP3 localization to all centromeres. (C,D) A comparably fixed oocyte showing CREST staining but no SCP3 localization. (Note: the localization pattern of SCP2 is identical.)

View larger version (23K): [in a new window]   Fig. 6. SCP3 localization during the transition from pachytene to dictyate arrest. (A,D,G) CREST localization at the centromeres (red), (B,E,H) SCP3 (green) and (C,F,I) merged images. (A-C) Pachytene stage oocyte with SCP3 localization along the length of the SC. (D-F) Diplotene/early dictyate oocyte showing clustering of centromeres in regions of the nucleus and SCP3 localization at most but not all centromeres. (G-I) Late diplotene/dictyate cell exhibiting clustering of centromeres but no SCP3 staining above background levels. (Note: the temporal localization pattern of SCP2 is similar; see text for details.)