scholarly journals Structural damage to meiotic chromosomes impairs DNA recombination and checkpoint control in mammalian oocytes

2006 ◽  
Vol 173 (4) ◽  
pp. 485-495 ◽  
Author(s):  
Hong Wang ◽  
Christer Höög
Keyword(s):  
Structural Damage ◽  
Meiotic Chromosome ◽  
Dna Recombination ◽  
Control Mechanisms ◽  
Checkpoint Control ◽  
Early Postnatal Development ◽  
Meiotic Chromosomes ◽  
Complex Protein ◽  
Synaptonemal Complex Protein ◽  
Related Proteins

Meiosis in human oocytes is a highly error-prone process with profound effects on germ cell and embryo development. The synaptonemal complex protein 3 (SYCP3) transiently supports the structural organization of the meiotic chromosome axis. Offspring derived from murine Sycp3−/− females die in utero as a result of aneuploidy. We studied the nature of the proximal chromosomal defects that give rise to aneuploidy in Sycp3−/− oocytes and how these errors evade meiotic quality control mechanisms. We show that DNA double-stranded breaks are inefficiently repaired in Sycp3−/− oocytes, thereby generating a temporal spectrum of recombination errors. This is indicated by a strong residual γH2AX labeling retained at late meiotic stages in mutant oocytes and an increased persistence of recombination-related proteins associated with meiotic chromosomes. Although a majority of the mutant oocytes are rapidly eliminated at early postnatal development, a subset with a small number of unfinished crossovers evades the DNA damage checkpoint, resulting in the formation of aneuploid gametes.

scholarly journals Phosphorylation of the synaptonemal complex protein SYP-1 promotes meiotic chromosome segregation

2017 ◽  
Author(s):  
Aya Sato-Carlton ◽  
Chihiro Nakamura-Tabuchi ◽  
Stephane Kazuki Chartrand ◽  
Tomoki Uchino ◽  
Peter Mark Carlton
Keyword(s):  
Synaptonemal Complex ◽  
Meiotic Chromosome ◽  
C Elegans ◽  
Chromosome Domains ◽  
Chromatid Cohesion ◽  
Complex Protein ◽  
Chromosomal Passenger ◽  
Synaptonemal Complex Protein ◽  
A Site ◽  
Meiosis I

AbstractChromosomes that have undergone crossing-over in meiotic prophase must maintain sister chromatid cohesion somewhere along their length between the first and second meiotic divisions. While many eukaryotes use the centromere as a site to maintain cohesion, the holocentric organism C. elegans instead creates two chromosome domains of unequal length termed the short arm and long arm, which become the first and second site of cohesion loss at meiosis I and II. The mechanisms that confer distinct functions to the short and long arm domains remain poorly understood. Here, we show that phosphorylation of the synaptonemal complex protein SYP-1 is required to create these domains. Once crossovers are made, phosphorylated SYP-1 and PLK-2 become cooperatively confined to short arms and guide phosphorylated histone H3 and the chromosomal passenger complex to the site of meiosis I cohesion loss. Our results show that PLK-2 and phosphorylated SYP-1 ensure creation of the short arm subdomain, promoting disjunction of chromosomes in meiosis I.

Architecture and Dynamics of Meiotic Chromosomes

2021 ◽  
Vol 55 (1) ◽  
Author(s):  
Sarah N. Ur ◽  
Kevin D. Corbett
Keyword(s):  
Meiotic Prophase ◽  
Morphological Changes ◽  
Meiotic Chromosome ◽  
Dna Recombination ◽  
Chromosome Complement ◽  
Annual Review ◽  
Publication Date ◽  
Meiotic Chromosomes ◽  
Crystal Model ◽  
Chromosome Axis

The specialized two-stage meiotic cell division program halves a cell's chromosome complement in preparation for sexual reproduction. This reduction in ploidy requires that in meiotic prophase, each pair of homologous chromosomes (homologs) identify one another and form physical links through DNA recombination. Here, we review recent advances in understanding the complex morphological changes that chromosomes undergo during meiotic prophase to promote homolog identification and crossing over. We focus on the structural maintenance of chromosomes (SMC) family cohesin complexes and the meiotic chromosome axis, which together organize chromosomes and promote recombination. We then discuss the architecture and dynamics of the conserved synaptonemal complex (SC), which assembles between homologs and mediates local and global feedback to ensure high fidelity in meiotic recombination. Finally, we discuss exciting new advances, including mechanisms for boosting recombination on particular chromosomes or chromosomal domains and the implications of a new liquid crystal model for SC assembly and structure. Expected final online publication date for the Annual Review of Genetics, Volume 55 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

scholarly journals Phosphorylation of the synaptonemal complex protein SYP-1 promotes meiotic chromosome segregation

2017 ◽  
Vol 217 (2) ◽  
pp. 555-570 ◽  
Author(s):  
Aya Sato-Carlton ◽  
Chihiro Nakamura-Tabuchi ◽  
Stephane Kazuki Chartrand ◽  
Tomoki Uchino ◽  
Peter Mark Carlton
Keyword(s):  
Synaptonemal Complex ◽  
Meiotic Chromosome ◽  
Chromosome Domains ◽  
Chromatid Cohesion ◽  
Complex Protein ◽  
Chromosomal Passenger ◽  
Synaptonemal Complex Protein ◽  
A Site ◽  
Unequal Length ◽  
Meiosis I

Chromosomes that have undergone crossing over in meiotic prophase must maintain sister chromatid cohesion somewhere along their length between the first and second meiotic divisions. Although many eukaryotes use the centromere as a site to maintain cohesion, the holocentric organism Caenorhabditis elegans instead creates two chromosome domains of unequal length termed the short arm and long arm, which become the first and second site of cohesion loss at meiosis I and II. The mechanisms that confer distinct functions to the short and long arm domains remain poorly understood. Here, we show that phosphorylation of the synaptonemal complex protein SYP-1 is required to create these domains. Once crossover sites are designated, phosphorylated SYP-1 and PLK-2 become cooperatively confined to short arms and guide phosphorylated histone H3 and the chromosomal passenger complex to the site of meiosis I cohesion loss. Our results show that PLK-2 and phosphorylated SYP-1 ensure creation of the short arm subdomain, promoting disjunction of chromosomes in meiosis I.

ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis

Cell ◽  
1993 ◽  
Vol 72 (3) ◽  
pp. 365-378 ◽  
Author(s):  
Mary Sym ◽  
JoAnne Engebrecht ◽  
G.Shirleen Roeder
Keyword(s):  
Synaptonemal Complex ◽  
Meiotic Chromosome ◽  
Chromosome Synapsis ◽  
Complex Protein ◽  
Synaptonemal Complex Protein

scholarly journals A Meiotic Chromosomal Core Consisting of Cohesin Complex Proteins Recruits DNA Recombination Proteins and Promotes Synapsis in the Absence of an Axial Element in Mammalian Meiotic Cells

2001 ◽  
Vol 21 (16) ◽  
pp. 5667-5677 ◽  
Author(s):  
Jeanette Pelttari ◽  
Mary-Rose Hoja ◽  
Li Yuan ◽  
Jian-Guo Liu ◽  
Eva Brundell ◽  
...  
Keyword(s):  
Protein Structure ◽  
Synaptonemal Complex ◽  
Meiotic Chromosome ◽  
Protein Structures ◽  
Dna Recombination ◽  
Cohesin Complex ◽  
Homologous Chromosomes ◽  
Recombination Proteins ◽  
Meiotic Chromosomes ◽  
Axial Element

ABSTRACT The behavior of meiotic chromosomes differs in several respects from that of their mitotic counterparts, resulting in the generation of genetically distinct haploid cells. This has been attributed in part to a meiosis-specific chromatin-associated protein structure, the synaptonemal complex. This complex consist of two parallel axial elements, each one associated with a pair of sister chromatids, and a transverse filament located between the synapsed homologous chromosomes. Recently, a different protein structure, the cohesin complex, was shown to be associated with meiotic chromosomes and to be required for chromosome segregation. To explore the functions of the two different protein structures, the synaptonemal complex and the cohesin complex, in mammalian male meiotic cells, we have analyzed how absence of the axial element affects early meiotic chromosome behavior. We find that the synaptonemal complex protein 3 (SCP3) is a main determinant of axial-element assembly and is required for attachment of this structure to meiotic chromosomes, whereas SCP2 helps shape the in vivo structure of the axial element. We also show that formation of a cohesin-containing chromosomal core in meiotic nuclei does not require SCP3 or SCP2. Our results also suggest that the cohesin core recruits recombination proteins and promotes synapsis between homologous chromosomes in the absence of an axial element. A model for early meiotic chromosome pairing and synapsis is proposed.

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

2019 ◽  
Vol 116 (37) ◽  
pp. 18423-18428 ◽  
Author(s):  
Huizhong Xu ◽  
Zhisong Tong ◽  
Qing Ye ◽  
Tengqian Sun ◽  
Zhenmin Hong ◽  
...  
Keyword(s):  
Meiotic Chromosome ◽  
Molecular Organization ◽  
Homologous Chromosomes ◽  
Meiotic Chromosomes ◽  
C Terminus ◽  
Stochastic Optical Reconstruction Microscopy ◽  
Optical Reconstruction ◽  
20 Nm ◽  
Chromosome Axis

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.

Association of mammalian SMC1 and SMC3 proteins with meiotic chromosomes and synaptonemal complexes

2000 ◽  
Vol 113 (4) ◽  
pp. 673-682 ◽  
Author(s):  
M. Eijpe ◽  
C. Heyting ◽  
B. Gross ◽  
R. Jessberger
Keyword(s):  
Gene Dosage ◽  
Dna Recombination ◽  
Immunofluorescence Analysis ◽  
Synaptonemal Complexes ◽  
Meiotic Chromosomes ◽  
Chromatid Cohesion ◽  
Specific Proteins ◽  
Experimental Approaches ◽  
Structural Maintenance Of Chromosomes ◽  
Smc Proteins

In somatic cells, the heterodimeric Structural Maintenance of Chromosomes (SMC) proteins are involved in chromosome condensation and gene dosage compensation (SMC2 and 4), and sister chromatid cohesion and DNA recombination (SMC1 and 3). We report here evidence for an involvement of mammalian SMC1 and SMC3 proteins in meiosis. Immunofluorescence analysis of testis sections showed intense chromatin association in meiotic prophase cells, weaker staining in round spermatids and absence of the SMC proteins in elongated spermatids. In spermatocyte nuclei spreads, the SMC1 and SMC3 proteins localize in a beaded structure along the axial elements of synaptonemal complexes of pachytene and diplotene chromosomes. Both SMC proteins are present in rat spermatocytes and enriched in preparations of synaptonemal complexes. Several independent experimental approaches revealed interactions of the SMC proteins with synaptonemal complex-specific proteins SCP2 and SCP3. These results suggest a model for the arrangement of SMC proteins in mammalian meiotic chromatin.

scholarly journals A molecular model for the role of SYCP3 in meiotic chromosome organisation

eLife ◽  
2014 ◽  
Vol 3 ◽  
Author(s):  
Johanna Liinamaria Syrjänen ◽  
Luca Pellegrini ◽  
Owen Richard Davies
Keyword(s):  
Molecular Model ◽  
Meiotic Chromosome ◽  
Lateral Element ◽  
Homologous Chromosomes ◽  
Meiotic Chromosomes ◽  
Double Stranded Dna ◽  
Evolutionarily Conserved ◽  
20 Nm ◽  
Chromosome Organisation

The synaptonemal complex (SC) is an evolutionarily-conserved protein assembly that holds together homologous chromosomes during prophase of the first meiotic division. Whilst essential for meiosis and fertility, the molecular structure of the SC has proved resistant to elucidation. The SC protein SYCP3 has a crucial but poorly understood role in establishing the architecture of the meiotic chromosome. Here we show that human SYCP3 forms a highly-elongated helical tetramer of 20 nm length. N-terminal sequences extending from each end of the rod-like structure bind double-stranded DNA, enabling SYCP3 to link distant sites along the sister chromatid. We further find that SYCP3 self-assembles into regular filamentous structures that resemble the known morphology of the SC lateral element. Together, our data form the basis for a model in which SYCP3 binding and assembly on meiotic chromosomes leads to their organisation into compact structures compatible with recombination and crossover formation.

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