Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing.

Abstract

Abstract. The preconditions and early steps of meiotic chromosome pairing were studied by fluorescence in situ hybridization (FISH) with chromosome-specific DNA probes to mouse and human testis tissue sections. Premeiotic pairing of homologous chromosomes was not detected in spermatogonia of the two species. FISH with centromere-and telomere-specific DNA probes in combination with immunostaining (IS) of synaptonereal complex (SC) proteins to testis sections of prepuberal mice at days 4-12 post partum was performed to study sequentially the meiotic pairing process. Movements of centromeres and then telomeres to the nuclear envelope, and of telomeres along the nuclear envelope leading to the formation of a chromosomal bouquet were detected during mouse prophase. At the bouquet stage, pairing of a mouse chromosome-8-specific probe was observed. SC-IS and simultaneous telomere FISH revealed that axial element proteins appear as large aggregates in mouse meiocytes when telomeres are attached to the nuclear envelope. Axial element formation initiates during tight telomere clustering and transverse filament-IS indicated the initiation of synapsis during this stage. Comparison of telomere and centromere distribution patterns of mouse and human meiocytes revealed movements of centromeres and then telomeres to the nuclear envelope and subsequent bouquet formation as conserved motifs of the pairing process. Chromosome painting in human spermatogonia revealed compacted, largely mutually exclusive chromosome territories. The territories developed into long, thin threads at the onset of meiotic prophase. Based on these results a unified model of the pairing process is proposed. p AIRING of homologous chromosomes during meiotic prophase of sexually reproducing organisms culminates in the formation of the synaptonemal complex (SC) 1 (for reviews see von Wettstein et al., 1984;Giroux, 1988). The SC is composed of axial elements (cores) that connect sister chromatids along their entire length. These become lateral elements when they get interconnected by transverse filaments to result in the well-known tripartite SC structure (Schmekel and Daneholt 1995). While chromosome pairing and meiotic recombination Address all correspondence to H. Scherthan,

Isolation and cytogenetic characterization of zebrafish meiotic prophase I mutants

“…SC formation initiates during the leptotene stage. The expression of a structural component of the SC, Sycp3, appeared as aggregates of this protein in the preleptotene nucleus, as previously described in both zebrafish (Ozaki et al, 2011) and mice (Scherthan et al, 1996). However, there was no development of cells that have the SC structure in the its mutant and the responsible gene may, therefore, be involved in the initiation of SC formation in the leptotene stage.…”

“…The expression of Sycp3 commenced in preleptotene spermatocytes, identified by the presence of one or more intranuclear Sycp3 aggregates (Fig. 5A), which have been shown to mark the onset of prophase I in male germ cells in mouse and cow (Scherthan et al, 1996;Pfeifer et al, 2001). In zebrafish spermatocytes at the leptotene stage, the Sycp3 signals were detectable as short fine threads, starting from one side of the nucleus with a distinct polarity (Fig.…”

Meiosis-specific cohesin mediates homolog recognition in mouse spermatocytes

“…2A). These results are consistent with the previous observations (Scherthan et al 1996) but partly contradictory to a recent study that reports the appearance of a transient pairing peak at late premeiotic S phase (see the Discussion; Boateng et al 2013). Under our experimental conditions, the distance between paired FISH signals decreases to <1.35 mm in 45%;60% of zygotene spermatocytes and in >95% of pachytene spermatocytes (Fig.…”

Evolutionary history of the mammalian synaptonemal complex

“…The telomeres move and cluster in the nuclear membrane close to the cytoplasmic centriole during the transition of leptotene to zygotene (zygos, greek paired). This very transient conformation is called bouquet stage and it is suggested that the telomere clustering supports the homology search and the alignment of the homologs as it coincides with synapsis initiation in many species (Scherthan et al 1996). Synapsis is characterized by the assembly of the central region of the SC.…”