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Published 2 September 2003. doi:10.1083/jcb.200305065
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© The Rockefeller University Press, 0021-9525/2003/9/795 $5.00
The Journal of Cell Biology, Volume 162, Number 5, 795-808

Article

Telomere-independent homologue pairing and checkpoint escape of accessory ring chromosomes in male mouse meiosis



Thierry Voet1, Bodo Liebe2, Charlotte Labaere1, Peter Marynen1 and Harry Scherthan2

1 Human Genome Laboratory, Department of Human Genetics, Flanders Interuniversity Institute for Biotechnology, University of Leuven, B-3000 Leuven, Belgium
2 Max-Planck-Institute for Molecular Genetics, D-14195 Berlin, Germany

Address correspondence to Harry Scherthan, Max-Planck-Institute for Molecular Genetics, Dept. Ropers, D-14195 Berlin, Germany. Tel.: 49-30-8413-1251. Fax: 49-89-8413-8313

We analyzed transmission of a ring minichromosome (MC) through mouse spermatogenesis as a monosome and in the presence of a homologue. Mice, either monosomic or disomic for the MC, produced MC+ offspring. In the monosomic condition, most univalents underwent self-synapsis as indicated by STAG3, SCP3, and SCP1 deposition. Fluorescent in situ hybridization and three-dimensional fluorescence microscopy revealed that ring MCs did not participate in meiotic telomere clustering while MC homologues paired at the XY-body periphery. Self-synapsis of MC(s) and association with the XY-body likely allowed them to pass putative pachytene checkpoints. At metaphase I and II, MC kinetochores assembled MAD2 and BUBR1 spindle checkpoint proteins. Unaligned MCs triggered the spindle checkpoint leading to apoptosis of metaphase cells. Other MCs frequently associated with mouse pericentric heterochromatin, which may have allowed them to pass the spindle checkpoint. Our findings indicate a telomere-independent mechanism for pairing of mammalian MCs, illuminate escape routes to meiotic checkpoints, and give clues for genetic engineering of germ line–permissive chromosomal vectors.

Key Words: chromosomal vector; spindle checkpoint; bouquet; synapsis; sex body

T. Voet and B. Liebe contributed equally to this paper.

email: schertha{at}molgen.mpg.de; or Peter Marynen, Center for Human Genetics, Flanders Interuniversity Institute for Biotechnology, University of Leuven, B-3000 Leuven, Belgium. email: peter.marynen{at}Med.Kuleuven.ac.be

Abbreviations used in this paper: 3D, three dimensional; AE, axial element; DSB, DNA double-strand break; IF, immunofluorescent; LE, lateral element; MC, minichromosome; MI, metaphase I; MII, metaphase II; PNA, peptide nucleic acid; SC, synaptonemal complex.


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