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

Voet T, Liebe B, Labaere C, Marynen P, Scherthan H - J. Cell Biol. (2003)

Bottom Line: 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.Unaligned MCs triggered the spindle checkpoint leading to apoptosis of metaphase cells.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.

View Article: PubMed Central - PubMed

Affiliation: Human Genome Laboratory, Department of Human Genetics, Flanders Interuniversity Institute for Biotechnology, University of Leuven, Belgium.

ABSTRACT
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.

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MCs contain SCP1. (A–E, G, and H) Disomic pachytene spermatocytes stained for SCP1 (green; IF staining; arrowheads in C–F) and the MC (red; FISH; arrowheads in A, B, G, and H) show either dotlike SCP1 signals at separate (H), juxtaposed (E), and paired (G) MCs, or rodlike (B and C) and dotlike (A and D) SCP1 cores between MCs. The bar in A represents 5 μm and also applies to B, G, and H. (F) Dotlike SCP1 signal (arrowhead) detected at the MC of a monosomic pachytene spermatocyte. (I and J) Frequencies of the different SCP1 staining patterns in monosomic and disomic pachytene nuclei.
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fig3: MCs contain SCP1. (A–E, G, and H) Disomic pachytene spermatocytes stained for SCP1 (green; IF staining; arrowheads in C–F) and the MC (red; FISH; arrowheads in A, B, G, and H) show either dotlike SCP1 signals at separate (H), juxtaposed (E), and paired (G) MCs, or rodlike (B and C) and dotlike (A and D) SCP1 cores between MCs. The bar in A represents 5 μm and also applies to B, G, and H. (F) Dotlike SCP1 signal (arrowhead) detected at the MC of a monosomic pachytene spermatocyte. (I and J) Frequencies of the different SCP1 staining patterns in monosomic and disomic pachytene nuclei.

Mentions: Immunostaining of SCP1, a marker for synapsis (Meuwissen et al., 1992; Dobson et al., 1994), revealed a dotlike SCP1 signal at the MC (Fig. 3, F and I) in 73% of the monosomic pachytene nuclei (n = 100), which suggests that univalent MCs undergo self-synapsis and thereby evade checkpoint control.


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

Voet T, Liebe B, Labaere C, Marynen P, Scherthan H - J. Cell Biol. (2003)

MCs contain SCP1. (A–E, G, and H) Disomic pachytene spermatocytes stained for SCP1 (green; IF staining; arrowheads in C–F) and the MC (red; FISH; arrowheads in A, B, G, and H) show either dotlike SCP1 signals at separate (H), juxtaposed (E), and paired (G) MCs, or rodlike (B and C) and dotlike (A and D) SCP1 cores between MCs. The bar in A represents 5 μm and also applies to B, G, and H. (F) Dotlike SCP1 signal (arrowhead) detected at the MC of a monosomic pachytene spermatocyte. (I and J) Frequencies of the different SCP1 staining patterns in monosomic and disomic pachytene nuclei.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2172825&req=5

fig3: MCs contain SCP1. (A–E, G, and H) Disomic pachytene spermatocytes stained for SCP1 (green; IF staining; arrowheads in C–F) and the MC (red; FISH; arrowheads in A, B, G, and H) show either dotlike SCP1 signals at separate (H), juxtaposed (E), and paired (G) MCs, or rodlike (B and C) and dotlike (A and D) SCP1 cores between MCs. The bar in A represents 5 μm and also applies to B, G, and H. (F) Dotlike SCP1 signal (arrowhead) detected at the MC of a monosomic pachytene spermatocyte. (I and J) Frequencies of the different SCP1 staining patterns in monosomic and disomic pachytene nuclei.
Mentions: Immunostaining of SCP1, a marker for synapsis (Meuwissen et al., 1992; Dobson et al., 1994), revealed a dotlike SCP1 signal at the MC (Fig. 3, F and I) in 73% of the monosomic pachytene nuclei (n = 100), which suggests that univalent MCs undergo self-synapsis and thereby evade checkpoint control.

Bottom Line: 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.Unaligned MCs triggered the spindle checkpoint leading to apoptosis of metaphase cells.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.

View Article: PubMed Central - PubMed

Affiliation: Human Genome Laboratory, Department of Human Genetics, Flanders Interuniversity Institute for Biotechnology, University of Leuven, Belgium.

ABSTRACT
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.

Show MeSH
Related in: MedlinePlus