Tying SUMO modifications to dynamic behaviors of chromosomes during meiotic prophase of Saccharomyces cerevisiae

Cheng, Chun-Hsu; Lin, Feng-Ming; Lo, Yu-Hui; Wang, Ting-Fang

doi:10.1007/s11373-007-9176-0

Cited by 12 publications

(13 citation statements)

References 79 publications

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“…These, as well as Smt3 aggregates, colocalized with Zip1 in the ipl1-mn mutant (Fig. 5H), consistent with the model that Smt3 is a substrate of Zip1 (Cheng et al 2007). …”

Section: Dissociation Of Central and Lateral Element Components Are Dsupporting

confidence: 86%

Ipl1/Aurora B kinase coordinates synaptonemal complex disassembly with cell cycle progression and crossover formation in budding yeast meiosis

Jordan¹,

Copsey²,

Newnham³

et al. 2009

Genes Dev.

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Several protein kinases collaborate to orchestrate and integrate cellular and chromosomal events at the G2/M transition in both mitotic and meiotic cells. During the G2/M transition in meiosis, this includes the completion of crossover recombination, spindle formation, and synaptonemal complex (SC) breakdown. We identified Ipl1/ Aurora B kinase as the main regulator of SC disassembly. Mutants lacking Ipl1 or its kinase activity assemble SCs with normal timing, but fail to dissociate the central element component Zip1, as well as its binding partner, Smt3/SUMO, from chromosomes in a timely fashion. Moreover, lack of Ipl1 activity causes delayed SC disassembly in a cdc5 as well as a CDC5-inducible ndt80 mutant. Crossover levels in the ipl1 mutant are similar to those observed in wild type, indicating that full SC disassembly is not a prerequisite for joint molecule resolution and subsequent crossover formation. Moreover, expression of meiosis I and meiosis II-specific B-type cyclins occur normally in ipl1 mutants, despite delayed formation of anaphase I spindles. These observations suggest that Ipl1 coordinates changes to meiotic chromosome structure with resolution of crossovers and cell cycle progression at the end of meiotic prophase.

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“…These, as well as Smt3 aggregates, colocalized with Zip1 in the ipl1-mn mutant (Fig. 5H), consistent with the model that Smt3 is a substrate of Zip1 (Cheng et al 2007). …”

Section: Dissociation Of Central and Lateral Element Components Are Dsupporting

confidence: 86%

Ipl1/Aurora B kinase coordinates synaptonemal complex disassembly with cell cycle progression and crossover formation in budding yeast meiosis

Jordan¹,

Copsey²,

Newnham³

et al. 2009

Genes Dev.

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“…Therefore, it is possible that Rec10 is only non-covalently bound by SUMO, and other LinE proteins, such as Rec25 and Rec27, are SUMO targets. Also, Pds5 is a possible candidate as it localizes to meiotic chromosome axes (Ding et al 2006) and was shown to be a SUMO target in the budding yeast (see Cheng et al 2007). Rec10 modification then may occur in response to the SUMOylation of one of its interacting partners.…”

Section: Discussionmentioning

confidence: 99%

“…Saccharomyces cerevisiae Zip1 and related proteins of other organisms are the main components of the transversal filaments (see Zickler and Kleckner 1999). In S. cerevisiae, it was found that Zip1 polymerizes along the axial elements concomitantly with their modification by the small ubiquitin-like modifier (SUMO) (see Cheng et al 2007). …”

Section: Introductionmentioning

confidence: 99%

SUMOylation is required for normal development of linear elements and wild-type meiotic recombination in Schizosaccharomyces pombe

et al. 2009

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In the fission yeast, Schizosaccharomyces pombe, synaptonemal complexes (SCs) are not formed during meiotic prophase. However, structures resembling the axial elements of SCs, the so-called linear elements (LinEs) appear. By in situ immunostaining, we found Pmt3 (S. pombe's SUMO protein) transiently along LinEs, suggesting that SUMOylation of some component(s) of LinEs occurs during meiosis. Mutation of the SUMO ligase Pli1 caused aberrant LinE formation and reduced genetic recombination indicating a role for SUMOylation of LinEs for the regulation of meiotic recombination. Western blot analysis of TAP-tagged Rec10 demonstrated that there is a Pli1-dependent posttranslational modification of this protein, which is a major LinE component and a distant homolog of the SC protein Red1. Mass spectrometry (MS) analysis revealed that Rec10 is both phosphorylated and ubiquitylated, but no evidence for SUMOylation of Rec10 was found. These findings indicate that the regulation of LinE and Rec10 function is modulated by Pli1-dependent SUMOylation of LinE protein(s) which directly or indirectly regulates Rec10 modification. On the side, MS analysis confirmed the interaction of Rec10 with the known LinE components Rec25, Rec27, and Hop1 and identified the meiotically upregulated protein Mug20 as a novel putative LinE-associated protein.

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“…Several lines of evidence indicate that protein modification by the ubiquitin-related protein SUMO plays a role in meiosis (28)(29)(30)(31)(32)(33)(34). In particular, the SC itself seems to contain SUMO because the SC can be stained with SUMOspecific antibodies along its entire axis (28).…”

Section: -1-1-red1 Interaction Is Essential For Meiotic Checkpoint Smentioning

confidence: 99%

Synaptonemal complex formation and meiotic checkpoint signaling are linked to the lateral element protein Red1

Eichinger

Jentsch

2010

Proc. Natl. Acad. Sci. U.S.A.

100

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Meiosis generates four haploid daughters from a diploid parental cell. Central steps of meiosis are the pairing and recombination of homologous chromosomes followed by their segregation in two rounds of cell division. Meiotic recombination is monitored by a specialized DNA damage checkpoint pathway and is guided by a unique chromosomal structure called synaptonemal complex (SC), but how these events are coordinated is unclear. Here, we identify the SC protein Red1 as a crucial regulator of early meiosis. Red1 interacts with two subunits of the 9-1-1 checkpoint complex via two distinct 9-1-1 subunit-specific motifs. Association of 9-1-1 with Red1 is essential not only for meiotic checkpoint activation but for SC formation. Moreover, Red1 becomes SUMO-modified, which fosters interaction of Red1 with the central SC element Zip1, thereby securing timely SC formation. Thus, Red1, in addition to its structural role in the SC, is a crucial coordinator of meiosis by coupling checkpoint signaling to SC formation.checkpoint | meiosis | SUMO T he central activity of meiosis is the equal distribution of the genetic material of a diploid cell into four daughter cells. A key step of meiosis occurs in pachytene, in which the homologous chromosomes (i.e., the parental chromosomes, each containing two sister chromatids) align (synapsis). This alignment facilitates the exchange of parental information by homologous recombination and is crucial for chromosome segregation during the first meiotic division.The juxtaposition of the homologs in pachytene involves a unique chromosome structure known as the synaptonemal complex (SC), which assembles along the entire length of the bundled chromosomes (1, 2). The SC-induced arrangement of chromosomes appears to favor genetic exchange between homologs rather than sister chromatids. SC formation starts along each pair of homologous sister chromatids with the assembly of 50-nm-thick fibers, termed axial elements, which later become the so-called "lateral elements" of the SC. The axial elementcoated parental homologs finally associate via components of the central element, which zip the axial elements together, forming the SC. In Saccharomyces cerevisiae, the proteins Hop1 and Red1 are structural components of the lateral element, whereas the coiled-coil protein Zip1, which homo (oligo)-dimerizes during SC formation, forms the "steps" of the ladder-like central region. SC "zipping" is thought to take place by serial Zip1-Red1 interactions along the entire SC axis (1, 2).Early meiosis is under the control of the meiotic recombination checkpoint (called the meiotic checkpoint here; it is also known as the pachytene checkpoint), which prevents meiotic progression in the presence of unrepaired recombination intermediates. A key element of the meiotic surveillance pathway is the ring-shaped, heterotrimeric 9-1-1 complex (the proteins Rad9, Hus1, and Rad1 in mammals; the proteins Ddc1, Mec3, and Rad17 in S. cerevisiae), which is structurally related to the homotrimeric DNA-encircling DNA polymerase...

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Tying SUMO modifications to dynamic behaviors of chromosomes during meiotic prophase of Saccharomyces cerevisiae

Cited by 12 publications

References 79 publications

Ipl1/Aurora B kinase coordinates synaptonemal complex disassembly with cell cycle progression and crossover formation in budding yeast meiosis

Ipl1/Aurora B kinase coordinates synaptonemal complex disassembly with cell cycle progression and crossover formation in budding yeast meiosis

SUMOylation is required for normal development of linear elements and wild-type meiotic recombination in Schizosaccharomyces pombe

Synaptonemal complex formation and meiotic checkpoint signaling are linked to the lateral element protein Red1

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