Centromere and telomere redistribution precedes homologue pairing and terminal synapsis initiation during prophase I of cattle spermatogenesis.
Alterations in nuclear topology associated with meiotic chromosome pairing were studied in premeiotic cells and spermatocytes I of adult bovine males. To this end, we performed FISH with chromosome, pericentromeric satellite-DNA and telomere-specific probes in combination with immunostaining of synaptonemal complex proteins (SCP3, SCP1) on testis tissue sections. Nuclei of premeiotic cells (spermatogonia) exhibited a scattered telomere distribution while pericentromeres formed a few intranuclear clusters. We observed that the chromosome pairing process in cattle prophase I is preceded by repositioning of centromeres and telomeres to the nuclear periphery during preleptotene. Clustering of chromosome ends (bouquet formation) was observed during the transition from leptonema to zygonema and coincided with pairing of a sub-centromeric marker of bovine chromosomes 7. Dissolution of bouquet topology during zygonema left perinuclear telomeres scattered over the nuclear periphery at pachynema. SCP3 staining in frozen tissue sections revealed the appearance of this axial element protein in intranuclear aggregates during preleptotene, followed by extensive axial element formation during leptotene. Synapsis as revealed by SCP1 staining initiated peripherally at earliest zygotene, at this stage nuclei still contained numerous SCP3 clusters. Our observations reveal prominent non-homologous satellite-DNA associations in spermatogonia and indicate the conservation of topological features of the meiotic chromosome pairing process among mammals. The comparison of telomere dynamics in mouse and cattle prophase I suggests that a larger number of chromosomes prolongs the duration of the bouquet stage.
Pfeifer
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Royal Veterinary and Agricultural University, Department of Anatomy and Physiology, Frederiksberg, Denmark.
Thomsen
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PD
Scherthan
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D000818:Animals; D002417:Cattle / Q000235:genetics*; D018797:Cell Cycle Proteins; D002467:Cell Nucleus / Q000235:genetics / Q000378:metabolism; D002503:Centromere / Q000235:genetics / Q000378:metabolism*; D020090:Chromosome Segregation; D004268:DNA-Binding Proteins; D007150:Immunohistochemistry; D017404:In Situ Hybridization, Fluorescence; D007211:Indoles; D008297:Male; D008540:Meiosis / Q000235:genetics*; D009687:Nuclear Proteins / Q000378:metabolism; D011418:Prophase / Q000235:genetics*; D012689:Sequence Homology, Nucleic Acid; D013090:Spermatocytes / Q000166:cytology / Q000378:metabolism; D013091:Spermatogenesis / Q000235:genetics*; D016615:Telomere / Q000235:genetics / Q000378:metabolism*; D013737:Testis / Q000166:cytology / Q000378:metabolism
D018797:Cell Cycle Proteins; D004268:DNA-Binding Proteins; D007211:Indoles; D009687:Nuclear Proteins; C489754:Sycp1 protein, mouse; C490062:Sycp3 protein, mouse; C007293:DAPI