Reconstruction of the kinetochore: a prelude to meiosis
© Asakawa et al; licensee BioMed Central Ltd. 2007
Received: 18 May 2007
Accepted: 06 June 2007
Published: 06 June 2007
In eukaryotic organisms, chromosomes are spatially organized within the nucleus. Such nuclear architecture provides a physical framework for the genetic activities of chromosomes, and changes its functional organization as the cell moves through the phases of the cell cycle. The fission yeast Schizosaccharomyces pombe provides a striking example of nuclear reorganization during the transition from mitosis to meiosis. In this organism, centromeres remain clustered at the spindle-pole body (SPB; a centrosome-equivalent structure in fungi) during mitotic interphase. In contrast, during meiotic prophase, centromeres dissociate from the SPB and telomeres cluster to the SPB. Recent studies revealed that this repositioning of chromosomes is regulated by mating pheromone signaling. Some centromere proteins disappear from the centromere in response to mating pheromone, leading to dissociation of centromeres from the SPB. Interestingly, mating pheromone signaling is also required for monopolar orientation of the kinetochore which is crucial for proper segregation of sister chromatids during meiosis. When meiosis is induced in the absence of mating pheromone signaling, aberrant chromosome behaviors are observed: the centromere proteins remain at the centromere; the centromere remains associated with the SPB; and sister chromatids segregate precociously in the first meiotic division. These aberrant chromosome behaviors are all normalized by activating the mating pheromone signaling pathway. Thus, action of mating pheromone on the centromere is important for coherent behavior of chromosomes in meiosis. Here we discuss repositioning and reconstruction of the centromere during the transition from mitosis to meiosis, and highlight its significance for proper progression of meiosis.
Eukaryotic chromosomes are spatially organized within the nucleus. While such nuclear architecture provides a physical framework for the genetic activities of chromosomes, this framework however is dynamic, able to change its functional organization during the cell cycle or developmental stages. Local chromatin structures change as chromosomes undergo processes such as replication, transcription, recombination and repair. During chromosome segregation, a specialized structure called kinetochore is formed on the centromeric DNA. Global organization of chromosomes within the nucleus can also change in association with their activities. A prominent example of reconstruction of the nuclear and chromosomal frameworks is observed during the transition from mitosis to meiosis.
Meiosis is a process that produces haploid gametes from parental diploid germ cells in sexually reproducing organisms. In this process, a single round of chromosome replication is followed by two rounds of chromosome segregation. A characteristic feature of meiosis is the behavior of sister chromatids in the first division (meiosis I). In meiosis I, homologous chromosomes segregate while sister chromatids remain held together. Sister chromatids then segregate in the second division (meiosis II). Reductional segregation of homologous chromosomes in meiosis I requires a recombination-mediated physical link between a pair of homologous chromosomes. This regulated segregation of homologous chromosomes and sister chromatids is achieved by selective use of monopolar and bipolar structures of the kinetochore, which provide a structural basis for monopolar and bipolar attachment of the spindle, respectively. Monopolar attachment of the spindle to sister kinetochores leads to movement of sister chromatids to the same pole in meiosis I. Bipolar attachment of the spindle to sister kinetochores causes segregation to the opposite poles in meiosis II (as well as in mitosis).
Meiotic reorganization of the chromosome is associated with assembly of the meiotic chromatin proteins that replace the mitotic counterparts. Cohesin proteins are among such proteins, and affect structures and segregation patterns of chromosomes [1, 2]. The position of centromeres in the nucleus also changes during the transition from mitosis to meiosis. In mitotic interphase, chromosomes are organized in a polarized orientation, with centromeres confined near the centrosome and telomeres positioned at the opposite side of the nucleus (often called the Rabl orientation). In contrast, in meiotic prophase, telomeres become clustered beneath the nuclear envelope near the centrosome; this arrangement of chromosomes bundled at the telomeres is often called the bouquet arrangement because of its shape (reviewed in ). The fission yeast Schizosaccharomyces pombe provides a striking example of the repositioning of centromeres and telomeres upon entering meiosis. Studies on regulatory mechanisms of this phenomenon have elucidated important aspects of centromere reconstruction that may influence the progression of meiosis.
The fission yeast meiosis: an overview
Telomeres are clustered in response to mating pheromone signaling
While telomere clustering in meiotic prophase has been observed in a wide variety of organisms, and its role in meiosis has been inferred (reviewed in ), analyses in S. pombe have demonstrated that telomere clustering and nuclear movement promote homologous chromosome pairing [11, 12]. In S. pombe, telomere clustering is known to take place in response to mating pheromone , and recently the underlying molecular mechanism has been revealed. S. pombe Taz1 (an ortholog of the human TRF1 and TRF2) binds directly to telomeric DNA, and Rap1 binds to the telomere through interaction with Taz1 [15–17]. During the mating pheromone response, meiosis-specific proteins Bqt1 and Bqt2 are expressed and the Bqt1/Bqt2 complex recruits Sad1 (an SPB component) to Rap1 at the telomere . In the presence of Bqt1 and Bqt2, Sad1, which is usually localized at the SPB, becomes accumulated at the scattered telomeres to form multiple foci on the nuclear envelope, and subsequently the Sad1 foci converge to the SPB together with telomeres. In this process, Sad1 binds to another SPB component Kms1, which interacts with the dynein motor protein [18, 19], and Sad1-bound telomeres are then clustered to the SPB through interaction with the dynein motor complex along microtubules. Horsetail nuclear movement is also mediated by cytoplasmic microtubules and the dynein motor complex [19–21]. Thus, telomeres are clustered to the SPB via the meiosis-specific connector proteins Bqt1 and Bqt2 in response to mating pheromone signaling, and remain connected to the SPB throughout the horsetail nuclear movement.
Centromeres are disassembled in response to mating pheromone signaling
Monopolar sister kinetochore is formed in response to mating pheromone signaling
Studies of meiosis in S. pombe have revealed that centromere dissociation from the SPB and formation of the monopolar sister kinetochore are both regulated by mating pheromone signaling. This correlation was first suggested by analyses using the pat1 mutant [26, 27]. Pat1 kinase is a key negative regulator of meiosis. In wild-type cells, mating pheromone signaling is required to inactivate Pat1 upon meiosis initiation. This requirement for mating pheromone signaling can be bypassed by inactivation of Pat1 by temperature-sensitive mutation. Mutational inactivation of Pat1 induces cells to enter meiosis even under conditions that the cell normally never enters meiosis, e.g., in the haploid state [28, 29]. In these experiments, cells are arrested in G1 phase by nitrogen starvation prior to induction of meiosis. Interestingly, in cells induced into meiosis by mutational inactivation of Pat1, in the absence of meting pheromone signaling, telomeres are clustered to the SPB, but centromeres often remain at the SPB in meiotic prophase . In those cells, the NMS complex localizes to centromeres attached to the SPB [22, 23]. Furthermore, sister chromatids are precociously segregated to opposite poles in meiosis I, indicating a deficiency in monopolar attachment of the sister kinetochores .
Meiotic defects caused by mutational inactivation of Pat1 are due to the lack of mating pheromone signaling. When the pat1 mutant cells are induced to meiosis in the presence of mating pheromone signaling, NMS complex proteins disappear from centromeres and centromeres are fully dissociated from the SPB [22, 23]. Moreover, sister chromatids correctly moves to the same spindle pole, indicating the monopolar sister kinetochore has been established . These findings demonstrate that the monopolar sister kinetochore is formed in response to the mating pheromone, causing reorganization of centromere proteins in meiotic prophase.
As the sister kinetochore is constructed during DNA replication, it is possible that the timing of DNA replication is affected by the presence or absence of mating pheromone. The timing of meiotic DNA synthesis can be determined in meiosis synchronously induced by temperature shifting G1 cells of the pat1 mutant. When meiosis is induced by pat1 mutation without mating pheromone, DNA synthesis occurs after 4 hours; on the other hand, when meiosis is induced in the presence of mating pheromone signaling, DNA synthesis occurs after 2 hours . Thus the mating pheromone signaling may also induce meiotic S-phase earlier. Importantly, in the pat1 mutation-induced meiosis without mating pheromone, the NMS complex remains at the centromere, and centromeres often remain associated with the SPB at the time of meiotic S-phase [22, 23, 27]. In contrast, in meiosis induced by the mutational inactivation of Pat1, in the presence of the mating pheromone signaling, the NMS complex disappears from the centromere, and centromeres are dissociated from the SPB before meiotic S-phase like in the normal process of meiosis [22, 23]. These results suggest that formation of the monopolar kinetochore correlates with removal of the NMS protein complex and consequent separation of centromeres from the SPB at the time of DNA replication, although no evidence has been found to support direct causality.
Centromere loading of Sgo1, but not of Rec8 or Moa1, depends on mating pheromone signaling
Some meiosis-specific proteins are known to play a role in the monopolar attachment of sister kinetochores in S. pombe. Meiotic cohesin Rec8 holds sister kinetochores together until anaphase II . Along with Rec8, Moa1 is essential in establishing the monopolar kinetochore . During meiotic S-phase, Rec8 is loaded onto the sister chromatids . Moa1 is loaded to the centromere in an early stage of horsetail nuclear movement , probably corresponding to S-phase similarly to Rec8 (Figure 3B). The loading of Rec8 and Moa1 does not require mating pheromone signaling [23, 26]. In addition, Rec8 and Moa1 can locate to the centromere when ectopically expressed in mitotic interphase cells [31, 33], while the NMS complex remains bound to the centromere. Thus, the removal of the NMS complex may be unnecessary for loading of Rec8 and Moa1 to the centromere. Monopolar sister kinetochore formation further requires mating pheromone signaling, suggesting that centromere loading of Rec8 and Moa1 is necessary, but not sufficient for formation of the monopolar kinetochore. Additional alteration of the kinetochore may occur in response to the mating pheromone signaling.
Localization of another meiosis-specific protein, Sgo1, to the centromere is regulated by mating pheromone signaling. Sgo1 protects Rec8 at the centromere to maintain cohesion between sister kinetochores until meiosis II . Sgo1 appears at the centromere during late-stage horsetail nuclear movement, as does the NMS complex  (Figure 3B). Importantly, when meiosis is induced by pat1 mutation in the absence of mating pheromone signaling, loading of Sgo1 to the centromere is severely diminished . This suggests that loading of Sgo1 is regulated downstream of mating pheromone signaling. Rec8 is expressed in pat1 mutation-induced meiosis in the absence of mating pheromone signaling as well as normal meiosis in wild type cells. Because Sgo1 is capable of localizing to centromeres in proliferating cells when ectopically coexpressed with Rec8 , diminished localization of Sgo1 in the pat1 mutant might be due to insufficient expression. Details of the mechanism of Sgo1 regulation by mating pheromone signaling are yet to be elucidated.
Regulatory pathways downstream of the mating pheromone
Recently, a transcription factor, Ste11, was reported to function downstream of Spk1 . Ste11, originally identified as an HMG family transcription factor, can bind to a specific sequence upstream of target genes . Ste11 is primarily expressed upon nitrogen starvation, and expression is further increased in response to mating pheromone . Spk1 phosphorylates two threonine residues of Ste11 (residues 305 and 317) in vitro, and phosphorylation of these residues is required for haploid meiosis induced by ectopic activation of the MAPK cascade . Thus, factors regulated by Ste11 may be involved in meiotic centromere reconstruction. Alternatively, unknown factors that are directly phosphorylated by Spk1 may be involved. Recent DNA microarray analyses have identified more genes whose expression is induced by mating pheromone signaling [14, 44, 45]. A more comprehensive search of factors downstream of mating pheromone signaling will lead to further understanding of meiotic regulation of the centromere.
Regulation of centromeres in other organisms
Several pieces of evidence for centromere-telomere repositioning and regulation of centromere proteins in the transition from mitosis to meiosis have been reported in other eukaryotes. In the budding yeast Saccharomyces cerevisiae, repositioning of chromosomes takes place during meiosis, although the telomere clustering is less prominent and shorter in time than that in S. pombe [8, 46]. At the time of repositioning, one of the Ndc80 complex proteins, Nuf2, disappears from the centromere, suggesting that the repositioning probably involves reorganization of centromere proteins as in S. pombe . In S. cerevisiae, proteins crucial for monopolar attachment of sister kinetochores to the spindle have been identified [47–53], but the correlation with spatial regulation of centromeres has not been examined. It is unlikely that the mating pheromone response regulates monopolar sister kinetochore formation because although the mating pheromone induces cell fusion, it does not induce meiosis directly in this organism.
In the nematode Caenorhabditis elegans, spatial reorganization of the nucleus occurs at the onset of meiotic prophase. Chromosomes asymmetrically cluster to one side of the nucleus, which in turn becomes crescent-shaped , although it is unclear whether reorganization of chromosomes involves repositioning of centromeres and telomeres. In C. elegans, several centromere proteins such as Cenp-C, Him-10 and KNL-1 are localized only during chromosome segregation both in mitosis and meiosis [55–59]. Remarkably, histone H3 variant, Cenp-A, loses the localization selectively during meiotic prophase, while it remains at the centromere throughout the mitotic cell cycle [55, 60]. It is not known, however, whether the disappearance of these proteins is related to meiotic reorganization of the nucleus and monopolar kinetochore formation in C. elegans.
In higher eukaryotes, reorganization of the nucleus occurs during meiosis . A large number of kinetochore proteins, including homologues of S. pombe proteins, has been reported. However, it is largely unknown how the kinetochore proteins behave during meiosis in higher eukaryotes.
We thank Y. Chikashige for providing the FISH pictures. This work was supported by Grant-in Aids for Scientific Research on Priority Areas 16084208 to TH and for Young Scientists (B) 18770188 to HA from the Japanese Ministry MEXT, and by CREST, JST to TH and YH.
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