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Leptotene/zygotene chromosome movement via the SUN/KASH protein bridge in Caenorhabditis elegans.

Baudrimont A, Penkner A, Woglar A, Machacek T, Wegrostek C, Gloggnitzer J, Fridkin A, Klein F, Gruenbaum Y, Pasierbek P, Jantsch V - PLoS Genet. (2010)

Bottom Line: Abrogation of synapsis led to a deceleration of SUN-1 aggregate movement.Analysis of matefin/SUN-1 in a double-strand break deficient mutant revealed that repair intermediates influenced matefin/SUN-1 aggregate dynamics.Investigation of movement in meiotic regulator mutants substantiated that proper orchestration of the meiotic program and effective repair of DNA double-strand breaks were necessary for the wild-type behavior of matefin/SUN-1 aggregates.

View Article: PubMed Central - PubMed

Affiliation: Department of Chromosome Biology, Max F. Perutz Laboratories, University of Vienna, Vienna, Austria.

ABSTRACT
The Caenorhabditis elegans inner nuclear envelope protein matefin/SUN-1 plays a conserved, pivotal role in the process of genome haploidization. CHK-2-dependent phosphorylation of SUN-1 regulates homologous chromosome pairing and interhomolog recombination in Caenorhabditis elegans. Using time-lapse microscopy, we characterized the movement of matefin/SUN-1::GFP aggregates (the equivalent of chromosomal attachment plaques) and showed that the dynamics of matefin/SUN-1 aggregates remained unchanged throughout leptonene/zygotene, despite the progression of pairing. Movement of SUN-1 aggregates correlated with chromatin polarization. We also analyzed the requirements for the formation of movement-competent matefin/SUN-1 aggregates in the context of chromosome structure and found that chromosome axes were required to produce wild-type numbers of attachment plaques. Abrogation of synapsis led to a deceleration of SUN-1 aggregate movement. Analysis of matefin/SUN-1 in a double-strand break deficient mutant revealed that repair intermediates influenced matefin/SUN-1 aggregate dynamics. Investigation of movement in meiotic regulator mutants substantiated that proper orchestration of the meiotic program and effective repair of DNA double-strand breaks were necessary for the wild-type behavior of matefin/SUN-1 aggregates.

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Related in: MedlinePlus

Disruption of the SUN/KASH bridge abrogates SUN-1 aggregate movement.Restrained movement in SUN-1(G311V)::GFP (A), displacement tracks (B), distribution of the projected speed of all SUN-1 aggregates inside a nucleus (C), and arcs representing the traveled distance for each track inside a nucleus (D). Blue lines represent values from the first movie, orange lines from the second. Eight out of the eight nuclei analyzed are shown. See Table 1 for number of nuclei analyzed. Scale bar: 2 µm.
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pgen-1001219-g003: Disruption of the SUN/KASH bridge abrogates SUN-1 aggregate movement.Restrained movement in SUN-1(G311V)::GFP (A), displacement tracks (B), distribution of the projected speed of all SUN-1 aggregates inside a nucleus (C), and arcs representing the traveled distance for each track inside a nucleus (D). Blue lines represent values from the first movie, orange lines from the second. Eight out of the eight nuclei analyzed are shown. See Table 1 for number of nuclei analyzed. Scale bar: 2 µm.

Mentions: A point mutation in the SUN domain of SUN-1 results in the absence of a defined TZ, and disturbs the interaction of SUN-1 with ZYG-12 [30]. In the cytoplasm, ZYG-12 interacts with the cytoskeleton via a dynein motor [29], [36]. We performed a time-lapse analysis of the mutated SUN-1(G311V)::GFP transgenic line in the sun-1(ok1282) deletion background and found that, on average, 7.8±2.3 (SD) aggregates inside a nucleus exhibited restrained movement (Table 1, Figure 3A and 3B, and Video S3). The distribution of the projected speed of these aggregates was a sharp bell, with 95% of the aggregates moving within a range of 10–100 nm/s (Figure 3C); the projected speed was significantly reduced compared to wild-type aggregates (Mann-Whitney test, p<0.001). The displacement tracks indicated weak local oscillatory movement (Figure 3B), and the distances traveled were significantly reduced. The arcs varied between 27° and 59° (Figure 3D). No exchange of SUN-1 aggregates was seen (Figure 2A). A functional SUN/KASH bridge mediating the connection to the cytoskeleton was, thus, necessary for the movement of SUN-1 aggregates and correlated with the absence of polarized chromatin.


Leptotene/zygotene chromosome movement via the SUN/KASH protein bridge in Caenorhabditis elegans.

Baudrimont A, Penkner A, Woglar A, Machacek T, Wegrostek C, Gloggnitzer J, Fridkin A, Klein F, Gruenbaum Y, Pasierbek P, Jantsch V - PLoS Genet. (2010)

Disruption of the SUN/KASH bridge abrogates SUN-1 aggregate movement.Restrained movement in SUN-1(G311V)::GFP (A), displacement tracks (B), distribution of the projected speed of all SUN-1 aggregates inside a nucleus (C), and arcs representing the traveled distance for each track inside a nucleus (D). Blue lines represent values from the first movie, orange lines from the second. Eight out of the eight nuclei analyzed are shown. See Table 1 for number of nuclei analyzed. Scale bar: 2 µm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2991264&req=5

pgen-1001219-g003: Disruption of the SUN/KASH bridge abrogates SUN-1 aggregate movement.Restrained movement in SUN-1(G311V)::GFP (A), displacement tracks (B), distribution of the projected speed of all SUN-1 aggregates inside a nucleus (C), and arcs representing the traveled distance for each track inside a nucleus (D). Blue lines represent values from the first movie, orange lines from the second. Eight out of the eight nuclei analyzed are shown. See Table 1 for number of nuclei analyzed. Scale bar: 2 µm.
Mentions: A point mutation in the SUN domain of SUN-1 results in the absence of a defined TZ, and disturbs the interaction of SUN-1 with ZYG-12 [30]. In the cytoplasm, ZYG-12 interacts with the cytoskeleton via a dynein motor [29], [36]. We performed a time-lapse analysis of the mutated SUN-1(G311V)::GFP transgenic line in the sun-1(ok1282) deletion background and found that, on average, 7.8±2.3 (SD) aggregates inside a nucleus exhibited restrained movement (Table 1, Figure 3A and 3B, and Video S3). The distribution of the projected speed of these aggregates was a sharp bell, with 95% of the aggregates moving within a range of 10–100 nm/s (Figure 3C); the projected speed was significantly reduced compared to wild-type aggregates (Mann-Whitney test, p<0.001). The displacement tracks indicated weak local oscillatory movement (Figure 3B), and the distances traveled were significantly reduced. The arcs varied between 27° and 59° (Figure 3D). No exchange of SUN-1 aggregates was seen (Figure 2A). A functional SUN/KASH bridge mediating the connection to the cytoskeleton was, thus, necessary for the movement of SUN-1 aggregates and correlated with the absence of polarized chromatin.

Bottom Line: Abrogation of synapsis led to a deceleration of SUN-1 aggregate movement.Analysis of matefin/SUN-1 in a double-strand break deficient mutant revealed that repair intermediates influenced matefin/SUN-1 aggregate dynamics.Investigation of movement in meiotic regulator mutants substantiated that proper orchestration of the meiotic program and effective repair of DNA double-strand breaks were necessary for the wild-type behavior of matefin/SUN-1 aggregates.

View Article: PubMed Central - PubMed

Affiliation: Department of Chromosome Biology, Max F. Perutz Laboratories, University of Vienna, Vienna, Austria.

ABSTRACT
The Caenorhabditis elegans inner nuclear envelope protein matefin/SUN-1 plays a conserved, pivotal role in the process of genome haploidization. CHK-2-dependent phosphorylation of SUN-1 regulates homologous chromosome pairing and interhomolog recombination in Caenorhabditis elegans. Using time-lapse microscopy, we characterized the movement of matefin/SUN-1::GFP aggregates (the equivalent of chromosomal attachment plaques) and showed that the dynamics of matefin/SUN-1 aggregates remained unchanged throughout leptonene/zygotene, despite the progression of pairing. Movement of SUN-1 aggregates correlated with chromatin polarization. We also analyzed the requirements for the formation of movement-competent matefin/SUN-1 aggregates in the context of chromosome structure and found that chromosome axes were required to produce wild-type numbers of attachment plaques. Abrogation of synapsis led to a deceleration of SUN-1 aggregate movement. Analysis of matefin/SUN-1 in a double-strand break deficient mutant revealed that repair intermediates influenced matefin/SUN-1 aggregate dynamics. Investigation of movement in meiotic regulator mutants substantiated that proper orchestration of the meiotic program and effective repair of DNA double-strand breaks were necessary for the wild-type behavior of matefin/SUN-1 aggregates.

Show MeSH
Related in: MedlinePlus