Correspondence to Michael E. Dresser: dresserm{at}omrf.ouhsc.edu
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Introduction |
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In meiosis, the Mcd1p subunit of cohesin largely is replaced by the meiosis-specific subunit Rec8p, which localizes to the meiotic chromosome axes (Klein et al., 1999). Meiotic recombination is also associated with chromosome axes. In meiosis, several cohesin subunits are required both for axis formation and successful completion of DSB repair (Klein et al., 1999; Revenkova et al., 2004). However, close associations between sister chromatids near DSBs could be an impediment for interhomologue recombination. Several lines of evidence indicate requirements for cohesion and cohesins in the repair of DSBs in mitotic cells, where sister-biased recombination is the preferred pathway for the repair of DSBs (Kadyk and Hartwell, 1992). First, in several organisms, genes encoding proteins that are required for cohesion were described to be required for DNA repair (Huynh et al., 1986; Birkenbihl and Subramani, 1992; Denison et al., 1993). Second, mutations in genes encoding subunits of cohesin complexes lead to precocious sister chromatid separation and defective postreplicative repair in yeast (Sjogren and Nasmyth, 2001). Similarly, the depletion of chicken Rad21p/Mcd1p/Scc1p leads to premature sister separation, reduced efficiency of DSB repair, and reduced frequency of sister chromatid exchange (Sonoda et al., 2001). Third, the establishment of cohesion in the preceding S-phase is required for successful DSB repair in G2 (Sjogren and Nasmyth, 2001). Fourth, cohesins are recruited to the sites of induced DSBs both in yeast and in mammals (Kim et al., 2002; Strom et al., 2004; Unal et al., 2004). Newly loaded cohesins are able to hold sister chromatids together (Strom et al., 2004), suggesting that cohesins could promote mitotic DSB repair by ensuring close proximity of sister chromatids. Bias toward interhomologue recombination in meiosis would require disfavoring the sister chromatid as a donor for DSB repair (for example, by locally destroying the close association between sister chromatids). Thus, components of the recombination machinery could remodel cohesion around DSBs to ensure use of the homologue for DSB repair in meiosis.
Efficient interhomologue recombination during vegetative growth and during meiosis requires Tid1p, which is a member of the SWI2/SNF2 family of helicase-like chromatin-remodeling proteins and is a paralogue of the recombination repair protein Rad54p (Eisen et al., 1995; Shiratori et al., 1999). However, in mitotic cells, the major repair pathway for DSBs uses the sister chromatid as a template even when a homologue is present and requires Rad54p and an interacting strand exchange enzyme, Rad51p (Kadyk and Hartwell, 1992; Paques and Haber, 1999; Symington, 2002; Tan et al., 2003). Thus, although Tid1p may interact with Rad51p (Dresser et al., 1997) and can promote the strand exchange activity of Rad51p in vitro (Petukhova et al., 2000), the effect of TID1 deletion on the repair of DSBs and on survival in mitotic cells is subtle unless sister chromatidbased repair is eliminated (Arbel et al., 1999; Lee et al., 2001; Signon et al., 2001; Ira and Haber, 2002).
During meiosis, most DSBs are repaired by a pathway that normally requires Dmc1p (a meiosis-specific paralogue of Rad51p; Bishop et al., 1992) in addition to Rad51p (Shinohara et al., 1992). Tid1p interacts with Dmc1p in the two-hybrid system (Dresser et al., 1997) and promotes Dmc1p colocalization with Rad51p on meiotic chromosomes (Shinohara et al., 2000), suggesting that Tid1p may serve together with Dmc1p during recombination repair to bias meiotic recombination specifically toward interhomologue repair (Dresser et al., 1997; Shinohara et al., 1997, 2003). The deletion of TID1 causes a delay in the processing of meiotic DSBs and increased resection at the broken DNA ends (Shinohara et al., 1997). However, even though mature recombination products do eventually form, at least at an artificial DSB hot spot (Shinohara et al., 1997), the majority of tid1 cells fail to sporulate (Klein, 1997; Shinohara et al., 1997).
We describe a novel phenotype of the deletion of TID1 that implicates Tid1p in the remodeling of chromosome structure (specifically sister chromatid cohesion). Tid1p is required for normal chromosome segregation in both meiotic divisions. The segregation defect in tid1 cells results from a failure of sister chromatid separation. In a spo11
spo13
background, there is no meiotic recombination, and the sole meiotic division requires that sister chromatids (not homologues) are separated. When tid1
is placed in the spo11
spo13
background, two thirds of the cells block in anaphase. This block is not suppressed by REC8 deletion alone. However, in the spo11
spo13
background, the tid1
block is suppressed by mcd1-1 (heat sensitive) if shifted to the nonpermissive temperature before or during meiotic prophase. It is also suppressed by mcd1-1 rec8
if shifted to the nonpermissive temperature at any time before cells begin to lose viability at the block. Moreover, both Mcd1p and Rec8p persist abnormally long in tid1
in an otherwise wild-type background. Our observations suggest that Tid1p plays a role in cohesion remodeling in meiotic prophase that is required for the successful separation of sister chromatids in anaphase.
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Results |
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Deletion of SPO11 suppresses the tid1 pachytene arrest and allows anaphase I segregation
To prove that pachytene arrest of the majority of tid1 cells depends on DSB formation, the SPO11 gene, which encodes the meiosis-specific endonuclease that is responsible for producing DSBs and chiasmata (Cao et al., 1990; Keeney et al., 1997), was deleted, and the progression of cells through meiotic divisions was monitored by staining chromatin with DAPI. spo11
suppresses the pachytene arrest of tid1
, allowing 68% of spo11
tid1
cells to enter the divisions without delay (Fig. 2 B), which supports the idea that the tid1
pachytene arrest is caused by unrepaired DSBs.
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tid1 blocks sister chromatid segregation in the spo11
spo13
background
The effect of TID1 deletion on the ability of cells to separate sister chromatids was tested in a background where sister chromatids segregate instead of homologues. The introduction of spo13 in the spo11
background, where meiotic recombination is eliminated, leads to biorientation of sister kinetochores and subsequent segregation of sister chromatids in the single meiotic division (Fig. 3 A; Klapholz et al., 1985; Shonn et al., 2002). In spo11
spo13
tid1
, 23% of cells complete the separation of chromatin into two masses (binucleates) compared with 66% of cells in spo11
spo13
(Fig. 3 B). Thus, even in the absence of interhomologue recombination, the deletion of TID1 prevents some spo11
spo13
cells from successfully finishing the division, presumably because of the failure to segregate sister chromatids in the absence of Tid1p. Consistently, one reason for the reduction in the percentage of binucleates is the accumulation of dumbbells (Fig. 3 C), which begin degrading at
10 h into sporulation (unpublished data). Another reason is an accumulation of cells with a single unstretched mass of chromatin (mononucleates) and a short spindle. In spo11
spo13
tid1
, only 40% of cells progress past mononucleate stage (Fig. 3 D) compared with 70% in spo11
tid1
(Fig. 2 B), which is higher than the 1525% in tid1
but lower than the 66% in spo11
spo13
(Fig. 3 B). Tagging of spindle tubulin with GFP reveals that the mononucleate cells consist of two classes: cells with a single spindle pole body (SPB) and cells with a short spindle. To determine what percentage of the population is represented by each class, we scored 50 spo11
spo13
mononucleate cells (29% of the total population is mononucleate at 8 h) and 68 spo11
spo13
tid1
mononucleate cells (53% of the total population is mononucleate at 8 h). The fraction of cells with a single SPB is similar in spo11
spo13
and spo11
spo13
tid1
(14% of each total population). However, the fraction of cells with a short spindle is lower in spo11
spo13
than in spo11
spo13
tid1
: 15 versus 39% of the total population, respectively. In addition, the fraction of cells with a short spindle subsequently decreases in spo11
spo13
, whereas it persists essentially unchanged in spo11
spo13
tid1
(unpublished data). Thus, the failure of spo11
spo13
tid1
cells to divide their chromatin into two masses can be attributed to a block with two phenotypes: dumbbells and mononucleate cells with a short spindle. The tid1 K351R allele, which is designed to eliminate ATP hydrolysis (Petukhova et al., 2000), causes a similar block in the spo11
spo13
background (unpublished data). A similar phenotype has been reported in other mutants where sister chromatids fail to segregate, leading to a block with a metaphase-length spindle (Toth et al., 2000; Clyne et al., 2003; Lee and Amon, 2003; Rabitsch et al., 2003).
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Pds1p turnover is not affected by tid1 in the spo11
spo13
background
Failure to separate sister chromatids in tid1 could result from an inhibition of the mechanism that is responsible for dissolving sister chromatid cohesion. Pds1p is down-regulated at anaphase I, and its loss is thought to enable cohesion dissolution by Esp1p/separase action (Petronczki et al., 2003). Therefore, we monitored the turnover of HA-tagged Pds1p in whole permeabilized cells by using anti-HA and antitubulin antibodies after 8 h of sporulation, when the spo11
spo13
tid1
and spo11
spo13
behaviors have just begun to diverge (Fig. 3 B) but before cell degradation. No Pds1p-positive cells with stretched dumbbell nuclei were seen either in spo11
spo13
(eight dumbbells were scored) or spo11
spo13
tid1
(52 dumbbells were scored). The increase in the percentage of cells with a short spindle that was observed in spo11
spo13
tid1
is almost exclusively accounted for by Pds1p-negative cells (Table I). This indicates that the short spindle arrest observed in spo11
spo13
tid1
occurs downstream of Pds1p destruction. Therefore, we conclude that the deletion of TID1 in spo11
spo13
results in a block of two thirds of cells in anaphase (short spindle cells plus dumbbells). The kinetics of Pds1p turnover that was measured in whole cell protein extracts on Western blots is also nearly identical in spo11
spo13
and spo11
spo13
tid1
(unpublished data). Thus, the persistent sister chromatid association that is caused by tid1
does not arise from any mechanism that leads to the persistence of Pds1p. Note that in dumbbells, where there is no detectable Pds1p, a significant fraction nevertheless has tightly associated sisters at telomere IVR (Fig. 3 G, 3 spot class). This result suggests that the persistent connections occur in the presence of active Esp1p.
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Early suppression of tid1 anaphase block by mcd1-1 in a spo11
spo13
background suggests that the misregulation of Mcd1p in the absence of Tid1p occurs before or during prophase. To confirm that tid1
has an effect on Mcd1p during prophase, Mcd1p was visualized by immunolabeling in spread nuclei of pachytene tid1
and wild-type cells, which were identified by the appearance of well-condensed chromosome bivalents. Mcd1p appears as spots on chromatin in spread preparations of pachytene cells (Klein et al., 1999; unpublished data). The number of Mcd1p spots on pachytene chromosomes in tid1
is significantly increased compared with wild type (Fig. 8), suggesting that the functional interaction between Mcd1p and Tid1p begins before or during pachytene. Thus, the misregulation of Mcd1p and, perhaps as a consequence, of Rec8p in or before prophase may lead to sister chromatid connections that persist through both anaphases and prevent chromosome segregation in both divisions of tid1
.
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Discussion |
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Tid1p is required to remodel cohesion before the onset of divisions to allow severing of sister chromatid connections in anaphase
Our data indicate that persistent sister chromatid connections mediated by Mcd1p and Rec8p are the primary reason for the anaphase block in tid1. We propose that Tid1p is required for Mcd1p (and possibly Rec8p) to be removed by an Esp1p-independent mechanism in prophase in preparation for or during DNA repair.
The timely progression into anaphase suggests that pachytene (DNA damage) and spindle checkpoints are not triggered by tid1 in the spo11
spo13
background. The involvement of a checkpoint that was triggered directly by DNA damage arising before the division (for example, in premeiotic S-phase) is possible but seems unlikely because no anaphase arrest was observed in the first division in spo11
tid1
.
A nucleosome remodeling function has been proposed for the Tid1p paralogue Rad54p (Alexeev et al., 2003; Jaskelioff et al., 2003; Wolner and Peterson, 2005). Another member of the SWI2/SNF2 family, SNF2hp, regulates cohesin loading on chromosomes, and ATPase activity is required for this process (Hakimi et al., 2002). We propose that a Tid1p chromatin remodeling function regulates Mcd1p and Rec8p association with chromosomes.
Mcd1p is required for local sister chromatid cohesion in budding yeast meiosis
In budding yeast, Mcd1p appears not to be essential for cohesion between sister chromatids in meiotic prophase, yet it forms discrete foci on pachytene chromosomes rather than localizing along their full lengths as with Rec8p (Klein et al., 1999). However, our results prove that Mcd1p can provide connections between sister chromatids in meiosis of Saccharomyces cerevisiae. Variability of the connections from cell to cell suggests that they could be independent of regular cohesin-binding sites. What leads Mcd1p to be loaded onto chromosomes in discrete, irregularly located spots (unpublished data) rather than along the chromosome axes (as it is in mitotic cells) and loaded as Rec8p is in meiotic cells is an important and unanswered question.
The Tid1p effect on recombination could be exerted through regulation of sister chromatid connections
We propose that Tid1p remodels Mcd1p-mediated cohesion to promote and regulate interhomologue recombination (Fig. 9). In this model, domains of Mcd1p would colocalize with DSBs that initiate meiotic recombination (and may be hot spots for DSBs; Petes, 2001). These domains would initially be prohibitive for impending interhomologue recombination for the following reason. In mitosis, cohesion between sister chromatids that was established during replication and de novo loading of cohesins at a DSB site are required for postreplicative DSB repair (Sjogren and Nasmyth, 2001; Strom et al., 2004; Unal et al., 2004). One of the roles proposed for cohesins in postreplicative repair in mitotic cells is to keep sister chromatids in proximity (Strom et al., 2004; Unal et al., 2004). If so, then in meiosis, additional factors would have to be incorporated at the Mcd1p domains to guide DSB repair to lead to the separation of, rather than the alignment of, sister chromatids. We suggest that Tid1p specifically facilitates this separation, which allows interaction with one of the chromatids of the homologue, perhaps by promoting displacement from the loop to the axis (Blat et al., 2002). In the absence of this loop displacement, the DSB ends would be free to separate and could give rise to the separation of Dmc1p and Rad51p foci that were reported for tid1 (Shinohara et al., 2000). This two-step mechanism for control over the fate of multiple programmed DSBs in meiosis would provide an escape route through sister-based repair in case of a failure to initiate repair involving the homologue as a template. Remodeling of cohesins by Tid1p could be promoted by Tid1p interaction with Dmc1p, which is required for the interhomologue bias of recombination in meiosis (Bishop et al., 1992; Dresser et al., 1997). Thus, Tid1p would serve to remodel chromosome structure, which is promoted by but is not necessarily dependent on DSB metabolism. The model predicts that Mcd1p and proteins involved in DSB repair should colocalize to some degree depending on their relative times of activity and on whether Mcd1p is involved at all or at a subset of DSB sites.
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Very little is known about how sister chromatid cohesion influences interhomologue recombination repair. However, it is clear that chromosome structure is adapted early to promote the programmed essential recombination repair that occurs in meiosis. Our results indicate that Tid1p is involved in this adaptation. Regulation of sister chromatid associations by Tid1p could similarly play a role during vegetative growth in the Tid1p-dependent subset of DSB repair that takes place between homologues in diploid cells (Klein, 1997; Shinohara et al., 1997; Arbel et al., 1999) and during break-induced replication (Signon et al., 2001; Ira and Haber, 2002). Structurefunction genetic analysis by mutations in TID1 and a biochemical description of the proposed remodeling activity of Tid1p will be required to establish the molecular functions of and the biological requirements for Tid1p in mitotic and meiotic cells.
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Materials and methods |
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Strains with a chromosome IV centromere and right telomere marked by GFP spots were constructed in several steps. To integrate a tandem array of 256 copies of the lac operator near the right telomere of chromosome IV, plasmid pMDE780 was constructed by cloning a HindIIISphI fragment of chromosome IV (nt 1,521,0381,522,195) into pAFS59 (Straight et al., 1996). PCYC1-lacI/GFP was introduced by the integration of pAFS152 (provided by A. Straight and A.W. Murray) at URA3 in derivatives of MDY431 and at CYC1 in derivatives of MDY433. PDMC1-lacI/GFP was introduced into strains at LYS2 by the integration of pMDE798, which contains lacI/GFP-NLS from pAFS152 (provided by A. Straight and A.W. Murray) under control of the DMC1 promoter in order to ensure expression during meiosis. To mark chromosome IV with a centromere GFP spot, pXH115 containing an array of 224 tet operator repeats was integrated into the chromosome. PURA3-tetR/GFP was introduced by the integration of pXH123 at LEU2 (He et al., 2000). Construction of strains with a paracentric inversion on chromosome VIIR have been described previously (Dresser et al., 1994). The presence of correct alleles in all strains was confirmed by genetic complementation and/or by PCR.
Cytological analysis
For all cytological experiments, cultures were prepared from freshly mated diploids that were grown in acetate-containing rich medium and were transferred to sporulation medium to sporulate at 8 x 107 cells + buds/ml at 30°C. For an analysis of progression through meiosis, cells were stained with 0.5 µg/ml DAPI in 50% ethanol and were examined by fluorescence microscopy. For experiments requiring the preservation of GFP fluorescence, cells were fixed in 1% PFA for 15 min at RT, washed with PBS and 30% ethanol, and stained with 5 µg/ml DAPI in PBS. Stained cells were embedded in 1% low melting point agarose (GIBCO BRL) in PBS to prevent flattening.
Pds1p-HA and tubulin were visualized in whole cells using antibodies against HA (12CA5; Babco) and tubulin (YL1/2; Abcam). Cells were fixed with 4% PFA in 50 mM phosphate buffer, pH 6.5, containing 0.5 mM magnesium chloride for 10 min and were washed twice with 0.1 M phosphate buffer containing 1.2 M sorbitol (immunofluorescence assay buffer B [IFB]). The cell wall was digested with 20 µg/ml Zymolyase-100T and was washed with IFB. Spheroplasts were permeabilized with 1% Triton X-100 in IFB, washed twice with IFB, and placed on coverslips that were treated with 1% polyethyleneimine. Nonspecific binding of antibodies was blocked by incubating the preparations in 4% nonfat dried milk (Bio-Rad Laboratories) in PBS for 20 min. Coverslips were incubated for 1 h with primary mouse anti-HA antibodies (1:500 final dilution) and rat antitubulin YL1/2 (1:1,000), washed three times with PBS, and incubated with secondary FITC-conjugated donkey antimouse and Rhodamine Red-Xconjugated donkey antirat antibodies (both 1:400 dilution; Jackson ImmunoResearch Laboratories). The preparations were then washed three times with PBS, stained with 10 µg/ml DAPI in PBS for 20 min, rinsed in PBS, and mounted on slides with 1.5% low melting point agarose (GIBCO BRL) in 70% glycerol in PBS. To slow fluorescence fading, Citifluor in glycerol (Ted Pella) was added under the coverslip before examination. This same method was used to visualize telomere and centromere GFP spots with primary rabbit anti-GFP antibodies (1:500; Invitrogen) and Cy2-conjugated donkey antirabbit secondary antibodies (1:400; Jackson ImmunoResearch Laboratories).
Spreads were prepared as described previously (Dresser and Giroux, 1988) on slides that were treated with 1% polyethyleneimine. Labeling with antibodies was performed on slides as described above with the exception of using TBS. To compare the percentage of cells that were arrested with a short spindle in spo11 spo13
rec8 tid1
with in spo11
spo13
rec8
, tubulin was visualized in spread preparations of meiotic nuclei using rat antitubulin YOL1/34 serum (Serotec) diluted 1:50 and Rhodamine Red-Xconjugated donkey antirat antibodies (Jackson ImmunoResearch Laboratories) diluted 1:400. To compare the dissociation of Rec8p from chromatin in wild-type with tid1
, Rec8p-GFP was visualized with chicken anti-GFP antibodies (Chemicon International) diluted 1:5,000 and FITC-conjugated donkey antichicken secondary antibodies (Jackson ImmunoResearch Laboratories) diluted 1:400. Tubulin was visualized as described above. Cross-reaction of the primary chicken anti-GFP antibodies with the rat antitubulin antibodies was noted but did not interfere with the assay. To compare the dissociation of Mcd1p from chromatin in wild-type with tid1
, Mcd1p was visualized with affinity-purified rabbit anti-Mcd1p (5591) antibodies (provided by V. Guacci) diluted 1:4,000 and with Cy3-conjugated donkey antirabbit secondary antibodies (Jackson ImmunoResearch Laboratories) diluted 1:400. Tubulin was visualized using rat antitubulin YL1/2 antibodies (Abcam) diluted 1:1,000 and Rhodamine Red-Xconjugated donkey antirat antibodies (Jackson ImmunoResearch Laboratories) diluted 1:400.
All images were acquired at 12-bit depth at RT on a microscope (Axioplan 2ie; Carl Zeiss MicroImaging, Inc.) using a plan-Apochromat 100x NA 1.4 oil differential interference contrast objective (Carl Zeiss MicroImaging, Inc.) and a camera (Quantix 57; Photometrics) driven by MetaMorph software (Universal Imaging Corp.). Stacks of images were produced by using either a nanopositioner (PolytecPI) or a stage (Carl Zeiss MicroImaging, Inc.) for focusing movements. Image processing was limited to scaling by using either MetaMorph software or AdobePhotoshop. The isointensity surface extraction that was used for three-dimensional reconstruction and maximum intensity projection images were generated by using OMRFQANT (written by M.E. Dresser).
EM
Silver-stained spread preparations of meiotic nuclei were prepared as described previously (Dresser and Giroux, 1988) and were examined in an electron microscope (model 1200EX; JEOL). Electron micrographs were acquired by using a high resolution digital camera (model ES4; Advanced Microscopy Techniques Corp.).
DNA DSB and recombination products analysis
The formation of DNA DSBs was assayed on CHEF gels (Gerring et al., 1991). Samples were run on an electrophoresis system (CHEF II; Bio-Rad Laboratories) in 1% FastLane agarose and 0.25x Tris-borate/EDTA electrophoresis buffer at 12°C and 6 V/cm by using a 2040-s ramp over 24 h. Southern transfer was performed by alkaline capillary transfer (Chomczynski, 1992) onto ZetaProbe membrane (Bio-Rad Laboratories). DSB fragments were visualized by using a radioactively labeled probe that was complementary to a near-telomeric region of chromosome III (Dresser et al., 1997) and were quantified using a phosphoimager (PhosphorImager 425; Molecular Dynamics). The formation of mature recombination products was assayed in a strain that was hererozygous for a paracentric inversion on chromosome VII (Dresser et al., 1994).
Online supplemental material
Table S1 lists yeast strains that were used in this study. Fig. S1 shows the kinetics of SC formation, turnover of DSBs, and formation of mature recombination products in wild-type and tid1. Fig. S2 shows the segregation of chromosome IV with a telomere GFP spot on both homologues in spo13
and spo13
tid1
. Fig. S3 shows control data for Figs. 5 and 6. More detailed information about these results is located in the supplemental text. Online supplemental material is available at http://www.jcb.org/cgi/content/full/jcb.200505020/DC1.
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Acknowledgments |
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This work was supported by grants from the National Institutes of Health (GM-45250-04) and the Oklahoma Center for the Advancement of Science and Technology (HR01-032) to M.E. Dresser.
Submitted: 4 May 2005
Accepted: 17 September 2005
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