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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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Influence of meiotic regulators on dynamics of SUN-1 aggregates.prom-1(ok1140) (A), him-19(jf6) (B), irradiated wild type (C), and cra-1(tm2144) (D), showing projection of the cumulative movement of SUN-1::GFP aggregates (i), displacement tracks (ii), distribution of the projected speed (iii), and arcs representing travelled distances (iv). Blue lines represent values from the first movie, orange lines from the second. See Table 1 for number of nuclei analyzed. Scale bar: 2 µm.
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pgen-1001219-g006: Influence of meiotic regulators on dynamics of SUN-1 aggregates.prom-1(ok1140) (A), him-19(jf6) (B), irradiated wild type (C), and cra-1(tm2144) (D), showing projection of the cumulative movement of SUN-1::GFP aggregates (i), displacement tracks (ii), distribution of the projected speed (iii), and arcs representing travelled distances (iv). Blue lines represent values from the first movie, orange lines from the second. See Table 1 for number of nuclei analyzed. Scale bar: 2 µm.

Mentions: In dispersed nuclei with a TZ-like appearance in prom-1(ok1140) mutant worms, SUN-1::GFP aggregates were movement competent (Video S11), and their tracking reconstructed the crescent shape of the chromatin (Figure 6Ai and 6Aii). The number of SUN-1 aggregates in prom-1(ok1140) was reduced compared to wild type (Mann-Whitney test, p<0.05), despite a similar average number of aggregates (Table 1). In this background, SUN-1 aggregates displayed a Maxwellian-shaped projected speed distribution and lacked long tails (Figure 6Aiii; Mann-Whitney test, p<0.05 compared to wild type), although the distance traveled by SUN-1::GFP aggregates was unaffected (from 19° up to 143°; Figure 6Aiv; Mann-Whitney test, p>0.05). Depletion of PROM-1 also reduced the number of exchanged aggregates (Figure 2A). Indeed, in a significant number of nuclei, SUN-1 aggregates were unable to fuse or split, and the number of nuclei showing 6–10 fusion/splitting events was considerably reduced (Table S1). The time period without exchange was significantly increased in prom-1(ok1140) compared to wild type: 47% of SUN-1::GFP aggregates were found to coalesce for less than 1 min and 23% for more than 3 min (Figure 2B and Table S2).


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)

Influence of meiotic regulators on dynamics of SUN-1 aggregates.prom-1(ok1140) (A), him-19(jf6) (B), irradiated wild type (C), and cra-1(tm2144) (D), showing projection of the cumulative movement of SUN-1::GFP aggregates (i), displacement tracks (ii), distribution of the projected speed (iii), and arcs representing travelled distances (iv). Blue lines represent values from the first movie, orange lines from the second. 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-g006: Influence of meiotic regulators on dynamics of SUN-1 aggregates.prom-1(ok1140) (A), him-19(jf6) (B), irradiated wild type (C), and cra-1(tm2144) (D), showing projection of the cumulative movement of SUN-1::GFP aggregates (i), displacement tracks (ii), distribution of the projected speed (iii), and arcs representing travelled distances (iv). Blue lines represent values from the first movie, orange lines from the second. See Table 1 for number of nuclei analyzed. Scale bar: 2 µm.
Mentions: In dispersed nuclei with a TZ-like appearance in prom-1(ok1140) mutant worms, SUN-1::GFP aggregates were movement competent (Video S11), and their tracking reconstructed the crescent shape of the chromatin (Figure 6Ai and 6Aii). The number of SUN-1 aggregates in prom-1(ok1140) was reduced compared to wild type (Mann-Whitney test, p<0.05), despite a similar average number of aggregates (Table 1). In this background, SUN-1 aggregates displayed a Maxwellian-shaped projected speed distribution and lacked long tails (Figure 6Aiii; Mann-Whitney test, p<0.05 compared to wild type), although the distance traveled by SUN-1::GFP aggregates was unaffected (from 19° up to 143°; Figure 6Aiv; Mann-Whitney test, p>0.05). Depletion of PROM-1 also reduced the number of exchanged aggregates (Figure 2A). Indeed, in a significant number of nuclei, SUN-1 aggregates were unable to fuse or split, and the number of nuclei showing 6–10 fusion/splitting events was considerably reduced (Table S1). The time period without exchange was significantly increased in prom-1(ok1140) compared to wild type: 47% of SUN-1::GFP aggregates were found to coalesce for less than 1 min and 23% for more than 3 min (Figure 2B and Table S2).

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