A Role for SUMO in Meiotic Chromosome Synapsis

Hooker, Gillian W.; Roeder, G. Shirleen

doi:10.1016/j.cub.2006.04.045

Cited by 81 publications

(135 citation statements)

References 22 publications

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“…The staining of whole chromosomes with anti-SUMO antibodies indeed suggests a broad role for SUMO in these complexes (28), perhaps as a "zipping glue." However, the low steady-state level of modified Red1 and our finding that Red1 SUMOylation triggers SC formation timing (rather than SC formation itself) argue for a regulatory role instead.…”

Section: Discussionmentioning

confidence: 92%

“…Notably, Red1 SUMOylation is stimulated by the putative meiotic ligase Zip3, which is known to associate with the MRX complex and concentrates at the first meiotic DSBs (42). Zip3 also binds the central element SC protein Zip1 (42), and these proteins, together with SUMO, first localize to recombination sites before Zip1 and SUMO spread along the entire chromosome (28). Thus, Zip3 may SUMOylate only Red1 molecules that are close to the DSBs, thereby perhaps stimulating the first specific Red1-Zip1 interactions.…”

Section: Discussionmentioning

confidence: 99%

“…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%

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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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Section: Discussionmentioning

confidence: 92%

Section: Discussionmentioning

confidence: 99%

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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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“…The synapsis initiation complex, which includes the Zip3 protein, promotes SC assembly by triggering the polymerization of Zip1 along chromosomes (18). Zip3 has SUMO E3 ligase activity and may sumoylate substrates along the chromosome cores to which Zip1 binds (19,20). In zip3 mutants, Zip1 shows severely delayed and incomplete association with meiotic chromosomes.…”

Section: Zip3 a Component Of The Synapsis Initiation Complex Regulamentioning

confidence: 99%

The synaptonemal complex protein, Zip1, promotes the segregation of nonexchange chromosomes at meiosis I

Newnham

Jordan

Rockmill

et al. 2009

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

Self Cite

132

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Crossing over establishes connections between homologous chromosomes that promote their proper segregation at the first meiotic division. However, there exists a backup system to ensure the correct segregation of those chromosome pairs that fail to cross over. We have found that, in budding yeast, a mutation eliminating the synaptonemal complex protein, Zip1, increases the meiosis I nondisjunction rate of nonexchange chromosomes (NECs). The centromeres of NECs become tethered during meiotic prophase, and this tethering is disrupted by the zip1 mutation. Furthermore, the Zip1 protein often colocalizes to the centromeres of the tethered chromosomes, suggesting that Zip1 plays a direct role in holding NECs together. Zip3, a protein involved in the initiation of synaptonemal complex formation, is also important for NEC segregation. In the absence of Zip3, both the tethering of NECs and the localization of Zip1 to centromeres are impaired. A mutation in the MAD3 gene, which encodes a component of the spindle checkpoint, also increases the nondisjunction of NECs. Together, the zip1 and mad3 mutations have an additive effect, suggesting that these proteins act in parallel pathways to promote NEC segregation. We propose that Mad3 promotes the segregation of NECs that are not tethered by Zip1 at their centromeres.

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“…Immunofluorescence, coimmunoprecipitation and two-hybrid experiments have shown that Zip3 is an upstream player in this process which seems to be recruited at the crossover sites by its interaction with recombination proteins, and which then likely recruits other SIC/ZMM proteins (some of the SIC/ZMM proteins also exhibit interdependence for localization) including Zip2 and Zip1, promoting the latter's polymerization from the crossover sites [26,32,33,35]. Biochemically, Zip3 is a putative E3 SUMO ligase which presumably sumoylates chromosomal proteins including the LE protein Red1 [12][13][14]42]. Zip3-mediated covalent or noncovalent addition of SUMO to Red1 is proposed to trigger installation of the CE by promoting protein-protein interactions, for example, between Red1 and Zip1 [13,14].…”

Section: How Zip1 Is Recruited To Centromere?mentioning

confidence: 99%

Meiotic Chromosome Interactions: Nonhomologous Centromere (Un)Coupling and Homologous Synapsis

Bardhan¹

2012

ISRN Cell Biology

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The fundamental function of meiosis, segregation of the maternal and paternal chromosomes, is facilitated by reciprocal recombination and intimate juxtaposition (synapsis) between the homologous chromosomes in meiotic prophase. Homolog synapsis, mediated by the synaptonemal complex (SC), is preceded by a stage of pairing between the centromeres of nonhomologous chromosomes. This pairing, named nonhomologous centromere coupling (NCC), depends upon the meiotic cohesin Rec8 and the SC protein Zip1. Nonhomologously coupled centromeres (NCCs), if remain tethered, must interfere with complete homolog synapsis (SC formation). Recent experiments demonstrate the existence of a mechanism that regulates NCC. Importantly, this is part of a regulatory network which couples dissolution of the NCCs with SC formation between the homologous chromosomes, thereby ensuring appropriate meiotic chromosome interactions. This paper reviews this network and presents speculations relating to the initiation of SC formation at centromere.

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A Role for SUMO in Meiotic Chromosome Synapsis

Cited by 81 publications

References 22 publications

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

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

The synaptonemal complex protein, Zip1, promotes the segregation of nonexchange chromosomes at meiosis I

Meiotic Chromosome Interactions: Nonhomologous Centromere (Un)Coupling and Homologous Synapsis

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