The width of the lateral element of the synaptonemal complex is determined by a multilayered organization of its components

Ortíz, Rosario; Kouznetsova, Anna; Echeverría-Martínez, Olga M.; Vázquez‐Nin, Gerardo H.; Hernández‐Hernández, Abrahan

doi:10.1016/j.yexcr.2016.03.025

Cited by 11 publications

(12 citation statements)

References 42 publications

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“…This observation indicates that the electron-dense elements that flank the SC may not correspond to assemblies of axis proteins, although some axis proteins appear to localize at or near these structures (22). Although recent work has illuminated some structural details of axis proteins and their interactions (16,(22)(23)(24), the overall organization of the chromosome axis remains largely undetermined.…”

Section: Significancementioning

confidence: 99%

Superresolution microscopy reveals the three-dimensional organization of meiotic chromosome axes in intact Caenorhabditis elegans tissue

Köhler

Wojcik

et al. 2017

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

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When cells enter meiosis, their chromosomes reorganize as linear arrays of chromatin loops anchored to a central axis. Meiotic chromosome axes form a platform for the assembly of the synaptonemal complex (SC) and play central roles in other meiotic processes, including homologous pairing, recombination, and chromosome segregation. However, little is known about the 3D organization of components within the axes, which include cohesin complexes and additional meiosis-specific proteins. Here, we investigate the molecular organization of meiotic chromosome axes in Caenorhabditis elegans through STORM (stochastic optical reconstruction microscopy) and PALM (photo-activated localization microscopy) superresolution imaging of intact germ-line tissue. By tagging one axis protein (HIM-3) with a photoconvertible fluorescent protein, we established a spatial reference for other components, which were localized using antibodies against epitope tags inserted by CRISPR/Cas9 genome editing. Using 3D averaging, we determined the position of all known components within synapsed chromosome axes to high spatial precision in three dimensions. We find that meiosis-specific HORMA domain proteins span a gap between cohesin complexes and the central region of the SC, consistent with their essential roles in SC assembly. Our data further suggest that the two different meiotic cohesin complexes are distinctly arranged within the axes: Although cohesin complexes containing the kleisin REC-8 protrude above and below the plane defined by the SC, complexes containing COH-3 or -4 kleisins form a central core, which may physically separate sister chromatids. This organization may help to explain the role of the chromosome axes in promoting interhomolog repair of meiotic double-strand breaks by inhibiting intersister repair.

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Section: Significancementioning

confidence: 99%

Superresolution microscopy reveals the three-dimensional organization of meiotic chromosome axes in intact Caenorhabditis elegans tissue

Köhler

Wojcik

et al. 2017

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

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“…This notion is supported by the observation that the “cohesin core axis,” which is marked by the cohesin subunits (Eijpe, Heyting, Gross, & Jessberger, ), is formed even in Sycp3 and Sycp2 knockouts (Figure b; Kouznetsova, Novak, Jessberger, & Hoog, ; Pelttari, Hoja, Yuan, Liu, & Brundell, ; Yang, De La Fuente, Leu, Baumann, & McLaughlin, ). Moreover, the chromosome axis, defined by an electron‐dense structure observed under electron microscope, is formed and can be immunolabeled for cohesin in Sycp3 KOs (Ortiz, Kouznetsova, Echeverria‐Martinez, Vazquez‐Nin, & Hernandez‐Hernandez, ), asserting the notion that a “cohesin core axis” acts as the structural basis for chromosome organization during meiosis. Indeed, it has been shown that AE formation depends on meiotic cohesins (Figure c).…”

Section: Meiotic Cohesins Underlie a Structural Basis For Chromosome mentioning

confidence: 99%

The cohesin complex in mammalian meiosis

2018

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Cohesin is an evolutionary conserved multi‐protein complex that plays a pivotal role in chromosome dynamics. It plays a role both in sister chromatid cohesion and in establishing higher order chromosome architecture, in somatic and germ cells. Notably, the cohesin complex in meiosis differs from that in mitosis. In mammalian meiosis, distinct types of cohesin complexes are produced by altering the combination of meiosis‐specific subunits. The meiosis‐specific subunits endow the cohesin complex with specific functions for numerous meiosis‐associated chromosomal events, such as chromosome axis formation, homologue association, meiotic recombination and centromeric cohesion for sister kinetochore geometry. This review mainly focuses on the cohesin complex in mammalian meiosis, pointing out the differences in its roles from those in mitosis. Further, common and divergent aspects of the meiosis‐specific cohesin complex between mammals and other organisms are discussed.

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“…With nanometer resolution, immunogold electron microscopy (EM) studies have suggested that the axis/LE might contain multilayered substructures (2,13) in mammalian SC. However, as the labeling density of immunogold EM is low and multicolor EM is difficult, the construction of localization maps of different proteins with respect to one another in the chromosome axis remains challenging.…”

mentioning

confidence: 99%

Molecular organization of mammalian meiotic chromosome axis revealed by expansion STORM microscopy

Tong

et al. 2019

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

103

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During prophase I of meiosis, chromosomes become organized as loop arrays around the proteinaceous chromosome axis. As homologous chromosomes physically pair and recombine, the chromosome axis is integrated into the tripartite synaptonemal complex (SC) as this structure’s lateral elements (LEs). While the components of the mammalian chromosome axis/LE—including meiosis-specific cohesin complexes, the axial element proteins SYCP3 and SYCP2, and the HORMA domain proteins HORMAD1 and HORMAD2—are known, the molecular organization of these components within the axis is poorly understood. Here, using expansion microscopy coupled with 2-color stochastic optical reconstruction microscopy (STORM) imaging (ExSTORM), we address these issues in mouse spermatocytes at a resolution of 10 to 20 nm. Our data show that SYCP3 and the SYCP2 C terminus, which are known to form filaments in vitro, form a compact core around which cohesin complexes, HORMADs, and the N terminus of SYCP2 are arrayed. Overall, our study provides a detailed structural view of the meiotic chromosome axis, a key organizational and regulatory component of meiotic chromosomes.

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The width of the lateral element of the synaptonemal complex is determined by a multilayered organization of its components

Cited by 11 publications

References 42 publications

Superresolution microscopy reveals the three-dimensional organization of meiotic chromosome axes in intact Caenorhabditis elegans tissue

Superresolution microscopy reveals the three-dimensional organization of meiotic chromosome axes in intact Caenorhabditis elegans tissue

The cohesin complex in mammalian meiosis

Molecular organization of mammalian meiotic chromosome axis revealed by expansion STORM microscopy

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