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MINIREVIEW

How To Divorce Engaged Chromosomes?

Department of Gene and Cell Medicine, Mount Sinai School of Medicine, New York, New York

The FEAR network, which is required for mitotic and meiotic progression, activates the phosphatase Cdc14, known to be required for mitotic exit. Mitotic exit is impaired, however, if sister chromatids were not properly aligned, i.e., if sister chromatid cohesion has not been established and resolved at the appropriate time. These processes require the cohesin complex and its destruction—at least for most of the chromosomal regions. Two recent studies describe an unusual behavior of particular chromosome segments such as the rRNA gene cluster, whose segregation also requires a CDC14-dependent, cohesin-independent pathway. Thus, mechanisms that govern chromosome segregation are more diverse than commonly assumed.

During S phase of the cell cycle, the newly synthesized sister chromatids become engaged. That is, they enter into cohesion, where they are physically held together and remain aligned with each other until mitosis. It has long been a puzzle how the sister chromatids are held together, whether by topological entanglements, by a strong protein glue that sticks to both sisters, or by a protein ring that embraces them. Current evidence may favor the ring hypothesis, whereby a ring-like cohesin protein complex may prevent divorce and thus segregation of chromosomes, primarily by its closed structure, i.e., topologically, rather than by acting as a cement bounding the two DNA duplices (14). Cohesin is a four-subunit protein complex, in which a heterodimer of SMC proteins, in this case SMC1/SMC3, associates with two other proteins, the Scc1/RAD21/Mcd1 and Scc3 proteins (Fig. 1A) . In vertebrates there are two variants of Scc3, called SA1 and SA2. Equally intriguing is the question of how the timely segregation of the two sister chromatids is achieved. Although a general mechanism that governs sister chromatid segregation through modification and destruction of one component of the cohesin complex has been described in recent years (reviewed in reference 36), it has become clear that, in addition to cohesin removal, additional pathways are required for segregation of specific regions of the genome.

View larger version (20K): [in this window] [in a new window]   FIG. 1. Schematic representation of cohesin (A) and condensin (B) with their respective subunits as indicated. The SMC proteins are intramolecularly folded and dimerize via their hinge regions, lending flexibility to the complexes.

It has now been observed that during anaphase a related protein complex called condensin accumulates at the rRNA gene (10, 33, 38). Binding of condensin in vivo to rRNA had earlier been noted, as has its association with pericentromeric and peritelomeric sequences (12). Condensin is thought to contribute to chromosome condensation in metaphase perhaps directly, but more likely by establishing the chromosomal scaffold, a protein matrix that supports proper structuring of chromosomes, for example, by localizing topoisomerases (9, 17, 18). Similar to cohesin, the condensin complex features an SMC heterodimer, SMC2/SMC4, and three non-SMC subunits (Fig. 1B). Although linear compaction of Saccharomyces cerevisiae chromosomes is only modest—vertebrate chromosomes need to be condensed by 3,000-fold (24)—it is still essential for chromosome segregation. Why, however, should condensin accumulate in the nucleolus, the site of rRNA clusters, and how is segregation of nucleolar DNA achieved?

The two studies used different approaches to reach similar, yet not entirely identical answers to these questions. Sullivan et al. observed that rRNA remains less condensed in metaphase than most other chromosomal regions and that it completes compaction only in anaphase. Applying a previously established technique to remove the cohesin complex by overexpression of the TEV protease, which cleaves at an artificial TEV cleavage site within the cohesin Scc1p, caused segregation of most chromosomal regions but not of the nucleolus. Thus, cohesin cleavage, which is normally achieved through activation of the protease separase, is not sufficient to segregate rRNA, at least not in metaphase-arrested cells. These authors went on to determine the specific requirements for rRNA segregation and identified a need for the Cdc14 phosphatase. D'Amours et al. started from the failure of the cdc14-3 mutant in the segregation of green fluorescent protein-labeled telomeric DNA, as well as of nucleolar DNA. The rationale behind investigating Cdc14 is based on earlier reports on rRNA condensation deficiencies in a cdc14 mutant (15), on a deficiency to segregate nucleolus-associated antigens in cdc14 mutants (13), on the need for separase to activate Cdc14 (34), and on the requirement for release of Cdc14 from its storage site in the nucleolus through a pathway called the FEAR network (Cdc14 early anaphase release), which is known to be required for anaphase progression (32). In addition to the FEAR network, which acts in early anaphase, a second pathway is required later for mitotic exit, the MEN (mitotic exit network) (reviewed in references 3 and 31). Only the FEAR pathway and the initial release of Cdc14 are necessary for rRNA and telomeric DNA segregation, for MEN mutants are segregation proficient.

Since the initial description of Cdc14 as a mutant deficient in nuclear division (27, 39), it has been extensively studied and found to be essential for inactivation of mitotic cyclin-dependent kinases and for the exit from mitosis (37). In mitosis, Cdc14 is also needed for correct positioning of the nucleus during anaphase and may regulate microtubule-associated force (30). In mammals, two distinct genes encode two variants of Cdc14, Cdc14A, and Cdc14B, which act differently in centromere and chromosome segregation (20, 23). Substrates for the yeast phosphatase include proteins that were phosphorylated by cyclin-dependent kinases (3), and the involvement of Cdc14 in segregation of nucleolar DNA has been noted (7, 13, 35, 38). The two recent reports, which use different alleles of cdc14 mutants, significantly define this role.

Inactivating the FEAR pathway through mutation of components of the network such as spo12 and bns1 or inactivation of Cdc14 leads to significant loss of cell viability, but only during anaphase. A failure to segregate repetitive DNA such as rRNA and telomeres may cause aneuploidy and thus increased cell death. If segregation in cdc14 mutants fails because cohesin cannot be properly removed, then artificial removal of cohesin as achieved in the TEV protease experiment or by inactivation of cohesin, such as in an scc1 mutant, should help segregation. However, it does not, indicating that cohesin removal is not the only critical step in rRNA segregation. Separase is required since lowering its levels affects rRNA and telomeric DNA segregation in particular. Since the cohesin cleavage activity of separase does not seem to be required or at least to be sufficient for rRNA segregation, another role of separase may come to bear. Sullivan and Uhlmann earlier described a protease-independent role of separase in the activation of Cdc14 (34).

Cdc14 must be released from the nucleolus in early anaphase and must be activated in order to fulfill its role in chromosome segregation. That role depends on its phosphatase activity, since an enzymatically dead mutant does not support nucleolar segregation. It also depends on the timely release of Cdc14, since a delay of release in mutant strains causes a parallel delay in segregation of the nucleolus (33, 35). Once released and active, how does Cdc14 promote rRNA and telomeric DNA compaction and segregation? Earlier reports showed that expression of Cdc14 causes morphological changes in rRNA (15) and that condensin mutants show a deficiency in segregation of the nucleolus similar to that observed in cdc14 mutants (5, 12). Therefore, condensin mutants were analyzed, and also other known contributors to chromosome condensation such as topoisomerase II and the aurora B kinase were considered.

Looking at two different subunits of yeast condensin, the Ycg1 or the Ycs4 proteins, the two groups found that condensin accumulation in anaphase in the nucleolus depends on Cdc14 and that Cdc14-induced condensation depends on condensin. In agreement with this, Wang et al. reported that targeting of condensin to the nucleolus in budding yeast requires Cdc14 and the FEAR pathway (38). Topoisomerase II is not required for this condensation process, but aurora B kinase is required (33). That kinase was earlier shown to be required for phosphorylation of the Ycg1 and may directly phosphorylate this condensin subunit. Although Cdc14 dephosphorylates one subunit of aurora B, this is not sufficient to induce rRNA condensation (10, 33), and the relationship between Cdc14, aurora B, and condensin remains to be further elucidated. For resolution of condensin-dependent rRNA cohesion, however, aurora B is not required (10, 33). Amons' group described a second modification of condensin: sumoylation of its Ycs4p component, identified by the reactivity of slower-migrating Ycs4p polypeptides with anti-Smt3 (Sumo) antibody (10). Interestingly, sumoylation of Ycs4p depends at least in part on Cdc14, since anaphase-specific sumoylation is delayed and reduced in the cdc14-3 mutant. Although it probably affects multiple processes, impaired desumoylation, which harms a perhaps critical balance between sumoylation and desumoylation, causes a deficiency in Ycs4p localization to the nucleolus during anaphase and in rRNA segregation. Although this can be indirect, it is suggestive of a role of sumoylation in targeting of condensin to the nucleolus. Thus, multiple posttranslational modifications of condensin linked to Cdc14 activation occur and are likely required for rRNA segregation. Although cohesin may also support cohesion at the rRNA gene and telomeric DNA, these genomic regions require segregation in an Cdc14-dependent, cohesin-independent, condensin-dependent, FEAR-dependent pathway as summarized in Fig. 2. It should be noted that the extent to which Cdc14 is required for telomeric DNA is not yet clear, since Sullivan et al. observed normal segregation in cdc14 mutants (33).

View larger version (47K): [in this window] [in a new window]   FIG. 2. Two pathways of chromosome segregation in Saccharomyces cerevisiae. Separase triggers release of cohesin from chromosomes triggering their segregation, except at the rRNA (rD) and perhaps the telomeric DNA (Tel) regions, whose segregation requires an additional pathway. Together with the FEAR network, separase also activates Cdcd14, which together with condensin is required for condensation and segregation of these DNA regions. Condensation of rRNA, but not resolution, also depends on the aurora B kinase, and posttranslational modifications such as sumoylation of condensin are likely to regulate its activity. The involvement of topoisomerase II needs further clarification, and the mechanisms involved in rRNA (and telomeric DNA) condensation and resolution await identification, as indicated by the question marks.

The role of topoisomerase II is not fully understood. In principle, cohesion can be supported by catenation of sister chromatids, which needs to be resolved through a topoisomerase. Topoisomerase II has been shown to be involved in the segregation of late-separating regions (5), and the nucleolus failed to segregate properly in top2 mutants (top2-4 and top2-5) at a nonpermissive temperature (33). However, D'Amours et al. found efficient segregation of rRNA through the Cdc14 pathway in the top2-4 mutant, indicating that the Cdc14 pathway acts independently of topoisomerase II.

Which properties render rRNA and perhaps telomeric DNA special, so that they require additional pathways to condense and segregate them? An obvious feature is their highly repetitive nature, distinguishing them from the rest of chromosomal sequences in yeast. This is not the case in vertebrates, however, in which extensive clusters and families of repetitive DNA of variable length and variable G/C content exist (reviewed in reference 4). Repetitive sequences constitute about half of the human genome, but only a few regions such as the centromeric region segregate late, rendering repetitive DNA-specific "rare/late-type" cohesion unlikely in these organisms. Thus, it is not repetitiveness per se that seems to determine the pathways for segregation.

Indeed, an artificial cluster of repetitive sequences placed near the centromere segregates efficiently independently of Cdc14 (10). The repetitive design of rRNA and telomeric DNA has other consequences; for example, for DNA recombination. To avoid unwanted recombination between repeats, recombination may be suppressed specifically at these sites, which may require a specific chromatin structure. It should be interesting, although difficult, to study the effect of Cdc14 deficiency on rRNA recombination. One mechanism for maintaining telomeres, in particular if the telomerase is impaired, is through recombination between telomeric sequences. Normally, this mechanism is suppressed to avoid genomic instability, but it can be activated in certain genetic backgrounds (e.g., in pif1 helicase mutants) (reviewed in reference 21). Proteins involved in the repression of recombination between repeats specifically at rRNA and telomeric DNA may affect segregation of these loci.

The heterochromatic nature of rRNA may suggest that silencing of RNA polymerase II-transcribed genes and the associated chromatin proteins such as Sir2p, which exists also at telomeres, requires unusual modes of condensation and segregation. Condensin has been shown to affect the composition of rRNA chromatin, since condensin mutants change the distribution of Sir2p (25). However, removal of Sir2p does not affect rRNA segregation, and at least rRNA transcription is not reduced upon Cdc14-induced condensation (33).

The yeast chromosome investigated by the Amon and Uhlmann groups, chromosome XII, is very long (500 µm; chromosome I is 50 µm). Do long chromosomes require special mechanisms to segregate their ends? Analysis of telomere segregation on other, shorter chromosomes or transfer of rRNA clusters onto shorter chromosomes in yeast should answer this question. Related evidence reported by Freeman et al. suggests that chromosome length is not the key determinant (12). These authors transferred rRNA onto the small chromosome III and, in an assay for chromosome loss, no loss was detected in a wild-type yeast strain, but in smc2 and smc4 mutants the loss rates were high, although chromosomal stability was not impaired because of its increased size after rRNA insertion (12). This indicates that the rRNA region bears unique features.

Is the canonical cohesin complex required at all for rRNA and telomeric DNA cohesion and segregation? Formally this has not yet been proven, although cohesin was not found excluded from telomeres and rRNA in chromatin immunoprecipitation experiments (22). It appears to be less abundant, however, at chromosome ends in silenced regions (6, 22). In vertebrate meiocytes, cohesin proteins were seen by immunofluorescence to also localize near telomeric ends (29) (Jessberger et al., unpublished observations). However, cohesin's role may be limited, and additional factors within the Cdc14 pathway are important. This leaves the question: how is the cohesin-independent form of cohesion achieved at these particular chromosomal locations? Could condensin itself act as a cohesin? There is no evidence supporting this idea, but at first glance the role of condensin in Cdc14-dependent rRNA segregation seems to be different from its function in chromosome condensation function (10). Condensin seems to have additional functions different from mitotic condensation, for example, in the repair of certain types of DNA damage as shown for Schizosaccharomyces pombe (2). Interestingly, the repair deficiency of condensin mutants can be suppressed by the Cti1 protein that is, like Cdc14, stored in the nucleolus and is released upon treatment with hydroxyurea, a DNA-damaging agent causing depletion of nucleotide pools and thus stalled replication forks (8). However, condensin's repair function, like its other functions, may be primarily to support proper chromosome structure, e.g., in building of a scaffold, and may all be explained through this function.

Alternatively, one may ask whether there is an hitherto-undescribed specialized cohesin-like complex, based on a heterodimer of SMC proteins such as condensin and cohesin, but lacking the Scc1p, that is the protein mostly used in the analysis of cohesin? More and more variants of SMC-based complexes appear that contain entirely different non-SMC subunits, rendering this speculation not too far-fetched (reviewed in 16 and 19).

As a further possibility, an unrelated protein or complex may provide this cohesion. An indication for such a complex may be derived from a report on the dissolution of protein bridges between telomeres by tankyrase I, a poly(ADP-ribose)polymerase (PARP) type of protein (11). PARPs are known to be mainly involved in DNA repair, to bind DNA ends, and to modify a range of substrates, mostly DNA repair proteins, by poly(ADP)ribosylation. Thus, it is not yet clear whether the role of tankyrase is direct or indirect in this resolution process and whether this process is related to cohesion.

Finally, as mentioned above, linkage based only on sister chromatid catenation may be considered. As Sullivan et al. (33) point out, the danger of suffering chromosome breaks if the resolution of catenation by topoisomerases is not complete may be tolerable in repetitive DNA such as rRNA. A break can possibly be repaired without a significant loss of genetic information. This may be more problematic, however, at the telomeric ends, which need to be maintained, and it would likely be harmful at the many repeats in vertebrate chromosomes.

Although the studies performed in yeast provide highly significant insights into basic mechanisms, one cannot assume that the results are easily transferable to higher eukaryotes. The great length of vertebrate chromosomes mentioned above, their highly repetitive nature, and the presence of two functionally distinct Cdc14 isoforms are among the many examples that warrant the search for mechanisms in higher eukaryotes distinct from those identified in yeast. The studies by the Amon and Uhlmann groups not only contribute importantly to our understanding of chromosome segregation but also provoke further questions, whose solutions should likewise lead to further insights into mitosis and meiosis, since the FEAR pathway is also required for meiotic chromosome segregation, nucleolus division, and spindle disassembly (7, 26).

ACKNOWLEDGMENTS

I thank Ekaterina Revenkova for helpful discussion.

Work in my laboratory is supported by a grant from the National Institutes of Health (GM62517).

	FOOTNOTES

 
* Corresponding author. Mailing address: Department of Gene and Cell Medicine, Mount Sinai School of Medicine, 1425 Madison Ave., New York, NY 10029. Phone: (212) 659-8259. Fax: (212) 849-2437. E-mail: rolf.jessberger{at}mssm.edu.

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