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PubMed2006

The meiosis-specific zip4 protein regulates crossover distribution by promoting synaptonemal complex formation together with zip2.

We have characterized Zip4 (a.k.a. Spo22), a meiosis-specific protein essential for chromosome synapsis in budding yeast. In the absence of Zip4, the synaptonemal complex protein Zip1 fails to polymerize along chromosomes. Zip2 and Zip3 are previously characterized components of the synapsis initiation complex. Zip4 forms a functional unit with Zip2 that is distinct from Zip3. Zip2 and Zip4 are mutually dependent for their chromosomal localization; in polycomplexes, the pattern of Zip2/Zip4 localization is distinct from that of Zip3. Crossing-over is decreased in the zip4 mutant (as in zip1, zip2, and zip3); the remaining crossovers are largely dependent on a parallel pathway utilizing Mms4. zip4 displays a novel phenotype: negative crossover interference, meaning that crossovers tend to cluster. This clustering depends on Zip1. Our results suggest an interaction between crossover pathways such that a protein (Zip1) acting in one pathway influences the distribution of crossovers promoted by a parallel (Mms4-dependent) pathway.

Chromosomal Proteins, Non-Histone↗
PubMed2003

Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination.

Here we probe the relationships between assembly of the synaptonemal complex (SC) and progression of recombination between homologous chromosomes during Caenorhabditis elegans meiosis. We identify SYP-2 as a structural component of the SC central region and show that central region assembly depends on proper morphogenesis of chromosome axes. We find that the SC central region is dispensable for initiation of recombination and for loading of DNA strand-exchange protein RAD-51, despite the fact that extensive RAD-51 loading normally occurs in the context of assembled SC. Further, persistence of RAD-51 foci and absence of crossover products in meiotic mutants suggests that SC central region components and recombination proteins MSH-4 and MSH-5 are required to promote conversion of resected double-strand breaks into stable post-strand exchange intermediates. Our data also suggest that early prophase barriers to utilization of sister chromatids as repair templates do not depend on central region assembly.

Animals↗
PubMed2006

Altered patterns of meiotic recombination in human fetal oocytes with asynapsis and/or synaptonemal complex fragmentation at pachytene.

Meiotic recombination was analysed in human fetal oocytes to determine whether recombination errors are associated with abnormal chromosome synapsis. Immunostaining was used to identify the synaptonemal complex (SC, the meiosis-specific proteinaceous structure that binds homologous chromosomes) and the DNA mismatch repair protein, MLH1, that locates recombination foci. It was found that 57.1-74.2% of zygotene oocytes showed fragmentation and/or defective chromosome synapsis. Fewer such abnormal cells occurred at pachytene (15.8-28.9%). MLH1 foci were present from zygotene to diplotene in both normal and abnormal oocytes. However, the proportions of oocytes having MLH1 foci, and mean numbers of foci per oocyte, were both lower in abnormal oocytes. Oocytes with fragmented SC had more foci than those with synaptic anomalies. Analysis of chromosomes 13, 18, 21 and X by fluorescence in-situ hybridization (FISH) did not implicate particular chromosomes in recombination deficiency. These observations indicate that recombination is disturbed in oocytes with SC fragmentation and/or synaptic abnormalities during meiotic prophase I. Such disturbances might be a risk factor for selection of fetal oocytes for atresia, as occurs for homologous chromosome pairing. Recombination errors may potentially increase the risk of abnormal chromosome segregation in oocytes that survive and contribute to the reserve in the mature ovary.

Adaptor Proteins, Signal Transducing↗
PubMed1998

DNA-binding activities of Hop1 protein, a synaptonemal complex component from Saccharomyces cerevisiae.

The meiosis-specific HOP1 gene is important both for crossing over between homologs and for production of viable spores. hop1 diploids fail to assemble synaptonemal complex (SC), which normally provides the framework for meiotic synapsis. Immunochemical methods have shown that the 70-kDa HOP1 product is a component of the SC. To assess its molecular function, we have purified Hop1 protein to homogeneity and shown that it forms dimers and higher oligomers in solution. Consistent with the zinc-finger motif in its sequence, the purified protein contained about 1 mol equivalent of zinc whereas mutant protein lacking a conserved cysteine within this motif did not. Electrophoretic gel mobility shift assays with different forms of M13 DNA showed that Hop1 binds more readily to linear duplex DNA and negatively superhelical DNA than to nicked circular duplex DNA and even more weakly to single-stranded DNA. Linear duplex DNA binding was enhanced by the addition of Zn2+, was stronger for longer DNA fragments, and was saturable to about 55 bp/protein monomer. Competitive inhibition of this binding by added oligonucleotides suggests preferential affinity for G-rich sequences and weaker binding to poly(dA-dT). Nuclear extracts of meiotic cells caused exonucleolytic degradation of linear duplex DNA if the extracts were prepared from hop1 mutants; addition of purified Hop1 conferred protection against this degradation. These findings suggest that Hop1 acts in meiotic synapsis by binding to sites of double-strand break formation and helping to mediate their processing in the pathway to meiotic recombination.

Cations, Divalent↗
PubMed1987

Electron microscopic investigations of synaptonemal complexes in an infertile human male carrier of a pericentric inversion inv(1)(p32q42). Regular loop formation but defective synapsis including a possible interchromosomal effect.

Electron microscopic investigations of surface spread synaptonemal complexes in spermatocytes from a 37-year-old man ascertained for infertility detected a pericentric inv(1), and subsequent lymphocyte analysis placed the breakpoints at p32 and q42. Most spermatocytes showed a maturation arrest at mid-pachytene explaining the azoospermia. As in two other comparatively large loop-forming pericentric inversions, initiation of synapsis took place in the middle of the inverted segment. Thus there is no indication of interstitial synaptic initiation being restricted to special pairing sites along the length of the chromosome. All spermatocytes investigated at mid-pachytene showed inversion loops, none of which was fully synapsed with a specific delay in pairing of the heterochromatic block 1qh and adjacent segments. The loops were of similar size in all the cells examined and synaptic adjustment had not taken place. There was no indication of a preferential association between the inv(1) bivalent and the XY configuration, and a functional disturbance of the X seems an unlikely reason for the meiotic maturation arrest. The most likely cause may be the failure of adequate synapsis of the inverted segment and the possibly associated pairing abnormalities of other homologues, including asynapsis and/or precocious desynapsis.

Adult↗
PubMed1984

Synaptonemal complex studies in a mosaic 46,XY/47,XXY male.

We describe the results of synaptonemal complex (SCs) studies by light (LM) and electron microscopy (EM) in a sterile 46,XY/47,XXY male mosaic. Meiotic studies showed an arrest at the first spermatocyte level. Pachytene figures showed three types of cells: (1) cells with normal SCs, normal sex vesicle, and a 23,XY constitution; (2) cells with no sex vesicle, normal pairing of SCs, and a 24, (?) constitution; and (3) cells with a normal sex vesicle and fragmented SCs.

Adult↗
PubMed2006

Synaptonemal complexes and XY behavior in two species of Argentinian armadillos: Chaetophractus villosus and Dasypus hybridus (Xenarthra, Dasypodidae).

Spermatocytes from the two armadillo species, C. villosus and D. hybridus were studied in microspreads for synaptonemal complexes (SCs) and in thin sections for electron microscopy (EM). The complete SC karyotype generally agrees with previous reports on mitotic chromosomes, except for the sex chromosomes. The X chromosome is submetacentric in both species and the Y is the shortest one in C. villosus and the second shortest in D. hybridus, and an extremely acrocentric one. A SC is formed along the total length of the Y chromosome, and this SC persists along all the pachytene substages. A single recombination nodule (RN) is located in the region of the SC nearest to the attachment to the nuclear envelope. The lateral element (LE) of the X axis in the SC shows a wavy aspect in most of the SC length distant from the nuclear envelope. Nucleoli are attached to acrocentric or submetacentric bivalents, are visibly double in some cells, and in thin sections show an elaborate nucleolonema. Some differences in the XY are species-specific, as the higher degree of tangling and stronger heteropycnosis in D. hybridus. The effective, single crossover of the XY pair is highly localized, despite the permanence of a long tract of SC.

Animals↗
PubMed1988

Spreading synaptonemal complexes from Zea mays. I. No synaptic adjustment of inversion loops during pachytene.

Four different inversion heterozygotes of maize were examined for the occurrence of synaptic adjustment. Three substages of pachytene were identified in synaptonemal complex (SC) spreads using side-by-side comparisons of chromosome squashes with two-dimensional spreads of SCs. In SC spreads, inversion loop frequency did not change substantially from early through late pachytene for any of the four inversion heterozygotes examined. In addition, the position and size of the inversion loops remained essentially constant throughout pachytene. These results indicate that synaptic adjustment of inversion loops does not occur during pachytene in Zea mays.

Heterozygote↗
PubMed2000

Methods for immunoelectron microscopic and fine structural analysis of synaptonemal complexes and nodules in yeast.

Several gene products involved in meiotic chromosome pairing and recombination in yeast have been identified in recent years. Two nuclear structures play key roles in the meiotic processes: the synaptonemal complex (SC), which is essential for the pairing of the chromosomes, and the recombination nodules (RNs), which mark the sites of recombination. Good morphological representation of the yeast SC and RNs is needed in order to show structural changes caused by specific mutations in protein-coding genes and for fine localization of proteins using immunoelectron microscopy (immuno-EM). This paper presents a newly developed preparation method for EM and immuno-EM that allows analysis of fine structural details and localization of proteins in the SC and RNs in yeast. Structural components of the SC are clearly seen and appear strikingly similar to those in the SC in other organisms. Antibodies against the SC protein Zip1, a transverse filament protein, label the central region of the SC strongly and specifically as expected. The improved method will be an important tool in high-resolution determination of the location of proteins in the meiotic yeast nucleus.

Antibodies↗
PubMed2004

Characterization of all human male synaptonemal complexes by subtelomere multiplex-FISH.

During meiotic prophase I, homologous chromosomes synapse and recombine. Both events are of vital importance for the success of meiosis. When homologous chromosomes synapse, a proteinaceous structure called synaptonemal complex (SC) appears along the pairing axis and meiotic recombination takes place. The existence of immunolabeling techniques for SC proteins (SCP1, SCP2 and SCP3) and for DNA mismatch repair proteins present in late recombination nodules (MLH1) allow analyses of both synapsis and meiotic recombination in the gametocyte I. In situ hybridization methods can be applied afterwards because chromatin is preserved during cell fixation for immunoanalysis. The combination of both methodologies allows the analysis of synapsis and the creation of recombination maps for each bivalent. In this work we apply the seven-fluorochrome subtelomere-specific multiplex FISH assay (stM-FISH) to human male meiotic cells previously labeled by immunofluorescence (SCP1, SCP3, MLH1, CENP) to assess its utility for human SC karyotyping. This FISH method consists of microdissected subtelomeric probes labeled combinatorially with seven different fluorochromes. Results prove its usefulness for the identification of all human SCs. Furthermore, by labeling subtelomeric regions this one-single-step method enables the characterization of interstitial and terminal SC fragments and SC delineation even if superposition is present in pachytene spreads.

Cytogenetic Analysis↗
PubMed1994

Synaptonemal complexes of chains and rings in mice heterozygous for multiple Robertsonian translocations.

Complex Robertsonian translocation heterozygosities in the mouse have been used to test different hypotheses regarding the correlation between male hybrid sterility and chromosomal abnormality. Synaptonemal complexes of meiotic super-chains and super-rings involving 15 to 18 metacentric chromosomes were studied in relation to spermatogenic histology. Both types of multivalents showed a characteristic pachytene pattern of alternating paired and non-paired segments. The amount of unpaired segments in rings was about 18% and in chains about 23% of the total length of multivalent chromosomes. The meiotic chains were associated with the proximal part of the X chromosomes in more than 60% of pachytene cells; a similar tight proximity of rings with X or Y chromosomes was never found. Complete arrest of germ cell maturation correlated with super-chains and inconspicuous testicular histology with super-rings. This demonstrates that an excessive amount of unpaired chromosomal axes does not lead per se to male infertility through gametogenic breakdown. On the contrary, the results clearly indicate spermatogenic impairment in this system of multimetacentric heterozygosity as a reflection of X chromosome super-chain interference.

Animals↗
PubMed1993

ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis.

ZIP1 is a novel meiosis-specific gene required for chromosome synapsis and cell cycle progression in S. cerevisiae. zip1 strains undergo homologous chromosome pairing, but are defective in synaptonemal complex (SC) formation. The zip1 mutation confers a uniform arrest in meiosis prior to the first division. zip1 strains display nearly wild-type levels of commitment to meiotic recombination; however, mature reciprocal recombinants are not formed until cells are released from meiotic arrest by return to growth medium. DNA sequence analysis of ZIP1 reveals structural homology to a number of proteins containing coiled coils. Immunofluorescence experiments using anti-ZIP1 antibodies demonstrate that the ZIP1 protein localizes to synapsed meiotic chromosomes but not to unsynapsed axial elements. Taken together, these data suggest that ZIP1 is a component of the central region of the SC. We propose a model in which ZIP1 acts as a molecular zipper to bring homologous chromosomes in close apposition.

Amino Acid Sequence↗
PubMed1989

Synaptonemal complex analysis of hybrid cattle. I. Pachytene substaging and the normal full bloods.

Meiotic chromosome pairing abnormalities in full-blood and hybrid Bos taurus and B. indicus cattle have been surveyed by electron microscopy of pachytene synaptonemal complex spreads. In this paper the full-blood spreads are described in detail, including the use of XY and nucleolar morphology and other measured parameters for pachytene substaging. Pairing abnormalities were observed in up to 9% of the full-blood spreads. Most of these pairing abnormalities (83%) occurred in early-pachytene spreads, suggesting that the mechanism of synaptic adjustment may operate in cattle.

Animals↗
PubMed1982

Synaptonemal complex analysis of X-7 translocations in male mice. I. R3 and R5 quadrivalents.

The synaptonemal complexes of surface-spread spermatocytes of mice heterozygous for one of two reciprocal translations (R3 and R5) between the X and chromosome 7 have been examined by light and electron microscopy (EM). The break points of R3 were determined to be at 70% of chromosome 7, as measured from the centromere, and at 22% of the X. Translocation quadrivalents were formed almost exclusively. The break points of R5 were at 21% of chromosome 7 as measured from the centromere, and at 83% of the X. There was little indication that the break in the X interfered with sex-chromosome synapsis between the 7X and Y. Univalent Y's were not observed in R3, and only seldom observed (8-14%) in R5. However, in contrast to R3, R5 formed quadrivalents relatively rarely (20% in the EM study of 100 nuclei), and heteromorphic bivalents of 7X-Y and X7-7 quite frequently (72%). Possible causes of this high bivalent frequency are discussed. Light-microscope (LM) analysis alone was found to be inadequate for interpreting synaptic configurations (quadrivalents vs. bivalents) in R5. The LM analysis was further complicated by the occurrence of nonhomologous synapsis in the heteromorphic bivalents of R5, a phenomenon easily recognized and interpreted in the EM portion of the study.

Animals↗
PubMed2006

The synaptonemal complex and meiotic recombination in humans: new approaches to old questions.

Meiotic prophase serves as an arena for the interplay of two important cellular activities, meiotic recombination and synapsis of homologous chromosomes. Synapsis is mediated by the synaptonemal complex (SC), originally characterized as a structure linked to pairing of meiotic chromosomes (Moses (1958) J Biophys Biochem Cytol 4:633-638). In 1975, the first electron micrographs of human pachytene stage SCs were presented (Moses et al. (1975) Science 187:363-365) and over the next 15 years the importance of the SC to normal meiotic progression in human males and females was established (Jhanwar and Chaganti (1980) Hum Genet 54:405-408; Pathak and Elder (1980) Hum Genet 54:171-175; Solari (1980) Chromosoma 81:315-337; Speed (1984) Hum Genet 66:176-180; Wallace and Hulten (1985) Ann Hum Genet 49(Pt 3):215-226). Further, these studies made it clear that abnormalities in the assembly or maintenance of the SC were an important contributor to human infertility (Chaganti et al. (1980) Am J Hum Genet 32:833-848; Vidal et al. (1982) Hum Genet 60:301-304; Bojko (1983) Carlsberg Res Commun 48:285-305; Bojko (1985) Carlsberg Res Commun 50:43-72; Templado et al. (1984) Hum Genet 67:162-165; Navarro et al. (1986) Hum Reprod 1:523-527; Garcia et al. (1989) Hum Genet 2:147-53). However, the utility of these early studies was limited by lack of information on the structural composition of the SC and the identity of other SC-associated proteins. Fortunately, studies of the past 15 years have gone a long way toward remedying this problem. In this minireview, we highlight the most important of these advances as they pertain to human meiosis, focusing on temporal aspects of SC assembly, the relationship between the SC and meiotic recombination, and the contribution of SC abnormalities to human infertility.

Female↗
PubMed2003

Karyotyping of human synaptonemal complexes by cenM-FISH.

The purpose of this work was to adapt the recently described centromere-specific multicolour (cenM-) FISH technique to human meiotic cells, and evaluate the usefulness of this multiplex fluorescence method for karyotyping human synaptonemal complex (SC), previously analysed by immunocytogenetic approaches. The results obtained demonstrate that cenM-FISH is a reliable one-single-step method, which allows for the identification of all SC present in pachytene spreads. Moreover, when cenM-FISH is applied after immunocytogenetic analysis, the number and distribution of MLH1 foci per chromosome can be established and recombination analysis for each chromosome can be performed easily.

Centromere↗
PubMed1999

Architecture of the nuclear periphery of rat pachytene spermatocytes: distribution of nuclear envelope proteins in relation to synaptonemal complex attachment sites.

The nucleus of spermatocytes provides during the first meiotic prophase an interesting model for investigating relationships of the nuclear envelope (NE) with components of the nuclear interior. During the pachytene stage, meiotic chromosomes are synapsed via synaptonemal complexes (SCs) and attached through both ends to the nuclear periphery. This association is dynamic because chromosomes move during the process of synapsis and desynapsis that takes place during meiotic prophase. The NE of spermatocytes possesses some peculiarities (e.g., lower stability than in somatic cells, expression of short meiosis-specific lamin isoforms called C2 and B3) that could be critically involved in this process. For better understanding of the association of chromosomes with the nuclear periphery, in the present study we have investigated the distribution of NE proteins in relation to SC attachment sites. A major outcome was the finding that lamin C2 is distributed in the form of discontinuous domains at the NE of spermatocytes and that SC attachment sites are embedded in these domains. Lamin C2 appears to form part of larger structures as suggested by cell fractionation experiments. According to these results, we propose that the C2-containing domains represent local reinforcements of the NE that are involved in the proper attachment of SCs.

Animals↗