The Ecm11-Gmc2 complex promotes synaptonemal complex formation through assembly of transverse filaments in budding yeast.

The Ecm11-Gmc2 complex promotes synaptonemal complex formation through assembly of transverse filaments in budding yeast.
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ECM11-GMC2复合物通过在发芽酵母中的横向丝组装来促进突发型复合物的形成。

DOI:
10.1371/journal.pgen.1003194
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发表时间:
2013
期刊:
影响因子:
4.5
通讯作者:
Tsubouchi H
Tsubouchi H
中科院分区:
生物学2区
文献类型:
--
作者:
Humphryes N;Leung WK;Argunhan B;Terentyev Y;Dvorackova M;Tsubouchi H

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在减数分裂过程中,同源染色体在靠近的地方配对形成突触复合体(SC)。这种结合是由横丝蛋白介导的,它将同源染色体的轴沿其整个长度保持在一起。横丝蛋白是高度聚集的,可以形成一种称为多复合体的异常聚集,与染色体无关。在这里,我们发现Ecm11-Gmc2复合物是一种新的SC成分,其功能是促进酵母横丝蛋白Zip1的组装。Ecm11和Gmc2最初定位于突触起始位点,然后遍及成对同源染色体的突触区。Ecm11或Gmc2的缺失极大地损害了Zip1的染色体组装以及多复合物的形成,这表明该复合物是Zip1广泛聚合所必需的。我们还表明,Ecm11以依赖gmc2的方式被sumoylation。值得注意的是,在不可sumoylatable的ecm11突变体中,染色体Zip1的组装仍然受到损害,而多复合体的形成变得频繁。我们认为Ecm11- gmc2复合体促进了Zip1的组装,而Ecm11的SUMOylation对于确保Zip1的染色体组装至关重要,从而抑制了多复合体的形成。减数分裂是有性生殖生物生命周期的核心。第一轮分裂(减数分裂I)对减数分裂来说是独一无二的,因为同源染色体被分离到相反的两极。同源染色体之间的紧密联系对它们的忠实分离至关重要。为了建立这种关联,减数分裂采用一种独特的同源重组依赖机制,促进同源染色体DNA链的识别、关联和相互交换,从而在同源染色体之间提供物理连接。所有这些事件都发生在一个叫做突触复合体(SC)的复杂结构的背景下。在这个复合体中,一条染色体的轴线与其同源物的轴线紧密相连。这种排列沿着染色体对的整个长度延伸,用称为横向丝的拉链状结构将轴固定在一起。在这项工作中,我们发现Ecm11-Gmc2复合物是SC的一个新组成部分,促进横向细丝的组装。重要的是,我们证明了用SUMO(小泛素样修饰剂)对Ecm11进行翻译后修饰对于确保横丝的染色体装载至关重要。因此,我们的工作为同源染色体在减数分裂前期如何紧密结合提供了分子基础。
During meiosis, homologous chromosomes pair at close proximity to form the synaptonemal complex (SC). This association is mediated by transverse filament proteins that hold the axes of homologous chromosomes together along their entire length. Transverse filament proteins are highly aggregative and can form an aberrant aggregate called the polycomplex that is unassociated with chromosomes. Here, we show that the Ecm11-Gmc2 complex is a novel SC component, functioning to facilitate assembly of the yeast transverse filament protein, Zip1. Ecm11 and Gmc2 initially localize to the synapsis initiation sites, then throughout the synapsed regions of paired homologous chromosomes. The absence of either Ecm11 or Gmc2 substantially compromises the chromosomal assembly of Zip1 as well as polycomplex formation, indicating that the complex is required for extensive Zip1 polymerization. We also show that Ecm11 is SUMOylated in a Gmc2-dependent manner. Remarkably, in the unSUMOylatable ecm11 mutant, assembly of chromosomal Zip1 remained compromised while polycomplex formation became frequent. We propose that the Ecm11-Gmc2 complex facilitates the assembly of Zip1 and that SUMOylation of Ecm11 is critical for ensuring chromosomal assembly of Zip1, thus suppressing polycomplex formation. Meiosis is central to the life cycle of sexually reproducing organisms. The first round of division (meiosis I) is unique to meiosis in that homologous chromosomes are segregated to opposite poles. The tight association between homologous chromosomes is essential for their faithful segregation. To establish such association, meiosis employs a unique, homologous recombination-dependent mechanism that facilitates the recognition, association, and reciprocal exchange of DNA strands of homologous chromosomes, thus providing physical connections between homologous chromosomes. All these events take place in the context of an intricate structure called the synaptonemal complex (SC). Within this complex, the axis of one chromosome is aligned at close proximity with the axis of its homologue. This alignment stretches along the entire length of the chromosome pair, with zipper-like structures, called transverse filaments, holding axes together. In this work, we identified the Ecm11-Gmc2 complex as a novel component of the SC, promoting the assembly of transverse filaments. Importantly, we demonstrate that post-translational modification of Ecm11 with SUMO (small ubiquitin-like modifier) is critical for ensuring the chromosomal loading of transverse filaments. Thus, our work provides a molecular basis for how homologous chromosomes become tightly associated during meiotic prophase.
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