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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

Effect of DSB formation on SUN-1 aggregate dynamics.spo-11(me44) (A), 2-d-old spo-11(me44) (B) 2 hours after irradiation with projection of cumulative movement (i), displacement tracks (ii), and distribution of the projected speed (iii). Arcs represent traveled distance (iv). Blue lines represent values from the first movie, orange lines from the second. See Table 1 for number of nuclei analyzed. (C) Distribution of SUN-1 foci and patches formed in wild type, spo-11(me44), 2-d-old wild type 2 hours after irradiation and 2-d-old spo-11(me44) 2 hours after irradiation. >400 SUN-1 aggregates counted per genotype. Scale bar: 2 µm.
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pgen-1001219-g007: Effect of DSB formation on SUN-1 aggregate dynamics.spo-11(me44) (A), 2-d-old spo-11(me44) (B) 2 hours after irradiation with projection of cumulative movement (i), displacement tracks (ii), and distribution of the projected speed (iii). Arcs represent traveled distance (iv). Blue lines represent values from the first movie, orange lines from the second. See Table 1 for number of nuclei analyzed. (C) Distribution of SUN-1 foci and patches formed in wild type, spo-11(me44), 2-d-old wild type 2 hours after irradiation and 2-d-old spo-11(me44) 2 hours after irradiation. >400 SUN-1 aggregates counted per genotype. Scale bar: 2 µm.

Mentions: The average number of SUN-1 aggregates was significantly reduced (3.0±0.6, SD, n = 18, Table 1) compared to wild type. Surprisingly, the appearance of SUN-1 displacement tracks was circular in 9 out of the 18 nuclei analyzed (Figure 7Ai and 7Aii). The distribution of the projected speed of SUN-1 aggregates in spo-11(me44) showed only 5% long tails (Figure 7Aiii), and was reduced in terms of speed and distance traveled (Mann-Whitney test, p<0.05) (Figure 7Aiv). In spo-11(me44), the number and frequency of exchanges (Figure 2A and 2B, Tables S1 and S2) were wild type.


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)

Effect of DSB formation on SUN-1 aggregate dynamics.spo-11(me44) (A), 2-d-old spo-11(me44) (B) 2 hours after irradiation with projection of cumulative movement (i), displacement tracks (ii), and distribution of the projected speed (iii). Arcs represent traveled distance (iv). Blue lines represent values from the first movie, orange lines from the second. See Table 1 for number of nuclei analyzed. (C) Distribution of SUN-1 foci and patches formed in wild type, spo-11(me44), 2-d-old wild type 2 hours after irradiation and 2-d-old spo-11(me44) 2 hours after irradiation. >400 SUN-1 aggregates counted per genotype. Scale bar: 2 µm.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1001219-g007: Effect of DSB formation on SUN-1 aggregate dynamics.spo-11(me44) (A), 2-d-old spo-11(me44) (B) 2 hours after irradiation with projection of cumulative movement (i), displacement tracks (ii), and distribution of the projected speed (iii). Arcs represent traveled distance (iv). Blue lines represent values from the first movie, orange lines from the second. See Table 1 for number of nuclei analyzed. (C) Distribution of SUN-1 foci and patches formed in wild type, spo-11(me44), 2-d-old wild type 2 hours after irradiation and 2-d-old spo-11(me44) 2 hours after irradiation. >400 SUN-1 aggregates counted per genotype. Scale bar: 2 µm.
Mentions: The average number of SUN-1 aggregates was significantly reduced (3.0±0.6, SD, n = 18, Table 1) compared to wild type. Surprisingly, the appearance of SUN-1 displacement tracks was circular in 9 out of the 18 nuclei analyzed (Figure 7Ai and 7Aii). The distribution of the projected speed of SUN-1 aggregates in spo-11(me44) showed only 5% long tails (Figure 7Aiii), and was reduced in terms of speed and distance traveled (Mann-Whitney test, p<0.05) (Figure 7Aiv). In spo-11(me44), the number and frequency of exchanges (Figure 2A and 2B, Tables S1 and S2) were wild type.

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