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MBC in Press, published online ahead of print December 2, 2003
Mol. Biol. Cell 10.1091/mbc.E03-07-0524

A more recent version of this article appeared on February 1, 2004
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Submitted on July 24, 2003
Revised on October 24, 2003
Accepted on October 24, 2003

Telomere attachment, meiotic chromosome condensation, pairing and bouquet stage duration are modified in spermatocytes lacking axial elements

Bodo Liebe1, Manfred Alsheimer2, Christer Höög3, Ricardo Benavente2, and Harry Scherthan1*

1 Max-Planck-Institut für Molekulare Genetik, Ihnestr. 73, D-14195 Berlin, Germany
2 Department. of Cell & Developmental Biology, Biocenter, Univ. of Würzburg, Am Hubland, D-97074 Würzburg, Germany
3 Department of Cell & Molecular Biology, Karolinska Institute, Stockholm, Sweden

* Corresponding author. E-mail address: schertha{at}molgen.mpg.de.

During the extended prophase to the meiosis I division chromosomes assemble axial elements (AE) along replicated sister chromatids whose ends attach to the inner nuclear membrane (NM) via a specialized conical thickening. Here, we show at the EM level that in Sycp3-/- spermatocytes chromosomes lack the AE and the conical end thickening. Still they attach their telomeres to the inner NM with an electron-dense plate that contains T2AG3 repeats. Immunofluorescence detected telomere proteins, SCP2 and the meiosis-specific cohesin STAG3 at the Sycp3-/- telomere. Bouquet stage spermatocytes were ~threefold enriched and the number of telomere but not centromere signals was reduced to the haploid in advanced Sycp3-/- spermatocytes, which indicates a special mode of homologue pairing at the mammalian telomere. FISH with mouse chromosome 8 and 12-specific subsatellite probes uncovered reduced levels of regional homologue pairing, while painting of chromosomes 13 revealed partial or complete juxtaposition of homologues, however, condensation of Sycp3-/- bivalents was defective. EM analysis of AE-deficient spermatocytes revealed that transverse filaments formed short structures reminiscent of the SC central region, which likely mediate stable homologue pairing. It appears that the AE is required for chromosome condensation, rapid exit from the bouquet stage and fine-tuning of homologue pairing.




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