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PubMed1993

Meiotic chromosome asynapsis in a boar with a reciprocal translocation and acquired testicular degeneration.

During a period of performance testing, a boar used for artificial insemination purposes was found responsible for reduced litter size and slightly increased incidence of repeat breeding. The qualitative and quantitative semen characteristics, however, were within normal limits. Later, evaluation of the semen during a period of 3 months revealed a decreased sperm concentration, but sperm cell morphology and mobility were normal. At castration, the boar, which had suffered from scrotal inflammation, was found to have hypoplastic gonads, the right testis being smaller than the left one. Histologically there was spermatogenic arrest at the primary spermatocyte level in almost all tubules of the right testis. In the left testis, histology was more heterogeneous, with some tubules containing all developmental stages, while others had an almost complete spermatogenic arrest. Cytogenetically the boar was carrying a translocation, rcp(2;14)(p14;q23). Synaptonemal complex analysis revealed complete quadrivalent pairing in 21 out of 43 cells analysed. The remaining cells demonstrated quadrivalents with axes moderately or extensively unpaired. There was a distinct difference between cells from the right vs. the left testis. The latter cells showed more completely paired translocation configurations. Moreover, in 14 and 7 cells analysed from the right and left testis, respectively, the translocation configuration could not be identified. This was due to chromosome asynapsis and frequent occurrence of gaps in the chromosomes, including others than those of the translocation, plus an abundant cellular deposit which formed a dense cell background. Association or pairing of the quadrivalent with the sex bivalent was seen in one cell only. At diakinesis-MI, most cells had a ring-shaped quadrivalent. It is believed that the asynapsis of chromosomes during the prophase of meiosis was to a large extent due to the degeneration caused by the inflammation processes.

Animals↗

PubMed2002

Synapsis-dependent and -independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans.

Analysis of Caenorhabditis elegans syp-1 mutants reveals that both synapsis-dependent and -independent mechanisms contribute to stable, productive alignment of homologous chromosomes during meiotic prophase. Early prophase nuclei undergo normal reorganization in syp-1 mutants, and chromosomes initially pair. However, the polarized nuclear organization characteristic of early prophase persists for a prolonged period, and homologs dissociate prematurely; furthermore, the synaptonemal complex (SC) is absent. The predicted structure of SYP-1, its localization at the interface between intimately paired, lengthwise-aligned pachytene homologs, and its kinetics of localization with chromosomes indicate that SYP-1 is an SC structural component. A severe reduction in crossing over together with evidence for accumulated recombination intermediates in syp-1 mutants indicate that initial pairing is not sufficient for completion of exchange and implicates the SC in promoting crossover recombination. Persistence of polarized nuclear organization in syp-1 mutants suggests that SC polymerization may provide a motive force or signal that drives redispersal of chromosomes. Whereas our analysis suggests that the SC is required to stabilize pairing along the entire lengths of chromosomes, striking differences in peak pairing levels for opposite ends of chromosomes in syp-1 mutants reveal the existence of an additional mechanism that can promote local stabilization of pairing, independent of synapsis.

Animals↗

PubMed1993

Synaptonemal polycomplexes in spermatids: a characteristic trait of Orthoptera?

Spermatogenesis was analysed in a cricket, Eneoptera surinamensis (Gryllidae, Orthoptera), using ultrathin serial sections and transmission electron microscopy. Special attention was placed on documentation of the development and structure of synaptonemal polycomplexes (PCs) within spermatid nuclei. Pachytene spermatocytes showed the usual tripartite synaptonemal complexes in the nuclear lumen. PCs were situated close to chromosomes at the periphery of spindles in prometaphase I spermatocytes, where microtubule density was low. The PCs are probably incorporated into the daughter nuclei of both meiotic divisions by adhesion to chromosomes. Finally, PCs end up within spermatid nuclei. Analysis of serial sections through three nuclei of young spermatids revealed at least one PC within each. The PCs were intimately attached to an electron-dense spherical nuclear body. This topographical correlation was confirmed through inspection of random sections. The PCs may have an affinity to the spherical bodies. In more developed spermatids, PCs and nuclear bodies were missing. Disassembly products of the PCs may play a role in spermatid maturation. In a series of other Orthoptera species, PCs have been reported to occur in the cytoplasm or the nuclei of spermatids. In most other systematic groups, PCs do not form at all or disassemble earlier. The presence of PCs in young spermatids, therefore, seems to be typical of Orthoptera.

Animals↗

PubMed1999

Bloom's syndrome protein, BLM, colocalizes with replication protein A in meiotic prophase nuclei of mammalian spermatocytes.

Bloom's syndrome (BS) is a rare autosomal recessive disorder of humans characterized by severe pre- and postnatal growth deficiency, immunodeficiency, genomic instability, and a predisposition to a wide variety of neoplasms. The genomic instability is evidenced in BS somatic cells as a high incidence of gaps and breaks, chromatid exchanges, chromosome rearrangements, and locus-specific mutations. BS arises from a mutation in BLM, a gene encoding a protein with homology to the RecQ helicase family. Men with BS are sterile; women have reduced fertility and a shortened reproductive span. The current immunocytological study on mouse spermatocytes shows that the BLM protein is first evident as discrete foci along the synaptonemal complexes (SCs) of homologously synapsed autosomal bivalents in late zygonema of meiotic prophase. BLM foci progressively dissociate from the synapsed autosomal axes during early pachynema and are no longer seen in mid-pachynema. BLM colocalizes with the single-stranded DNA binding replication protein A, which has been shown to be involved in meiotic synapsis. However, there is a temporal delay in the appearance of BLM protein along the SCs relative to replication protein A, suggesting that BLM is required for a late step in processing of a subset of genomic DNA involved in establishment of interhomologue interactions in early meiotic prophase. In late pachynema and into diplonema, BLM is more dispersed in the nucleoplasm, especially over the chromatin most intimately associated with the SCs, suggesting a possible involvement of BLM in resolution of interlocks in preparation for homologous chromosome disjunction during anaphase I.

Adenosine Triphosphatases↗

PubMed1994

Fine structure of the XY body in the XY1Y2 trivalent of the bat Artibeus lituratus.

Electron microscopy of spread spermatocytes and thin sections has been used to study the sex trivalent (XY1Y2) of the bat Artibeus lituratus. Pachytene spermatocytes in thin sections show an XY body with typical chromatin condensation that is connected to autosomal chromatin through a synaptonemal complex (SC). Microspread spermatocytes show three axes and two SC segments (a short SC and a long one) in the sex trivalent. The short paired region corresponds to synapsis between the 'original' X and Y pieces, while the long paired region corresponds to synapsis between the Y2 element and the homologous, autosomal piece of the compound X-chromosome. The length ratios of the three axes correspond to those of the three mitotic chromosomes, X, Y1 and Y2. The high packing of chromatin corresponds exclusively to the 'original' pieces of the X and Y elements, while the autosomal regions of the X and the Y2 axes are surrounded by autosomal-like chromatin. Thus, in this trivalent the formation of an XY body in the 'original' sex chromosomes is not inhibited by the presence of the autosomal pieces, and typical partial synapsis between the original X and Y elements is conserved. C-banding heterochromatin seems not to be the barrier preventing the spreading of heterochromatinization towards the autosomal piece in this trivalent.

Animals↗

PubMed2002

Sex-dependent synaptic behaviour in triploid turbot, Scophthalmus maximus (Pisces, Scophthalmidae).

A surface-spreading synaptonemal complex (SC) technique was used to analyse spermatocytes and oocytes of triploid turbot (Scophthalmus maximus) in order to visualise the process of chromosome synapsis. The most conspicuous characteristic of triploid oocytes is that, in the trivalents, the lateral elements of the SC were frequently associated in threes, either completely along the length of the trivalent, or partially, forming a variety of forked structures. In these nuclei, synapsis usually occurred among homologous chromosomes and the number of bivalents observed was significantly higher than that expected under the assumption of random chromosome association among all partners. However, the frequency of trivalents was very low in triploid spermatocytes, triple synapsis being also scarce. In these nuclei chromosomes that were excluded from homologous synapsis become engaged in random SC formation, and, therefore a considerable number of non-homologous associations are produced. The causes of the synaptic differences observed in triploid males and females of turbot and their possible relation to the sterility displayed by these animals are discussed.

Animals↗

PubMed1998

Identification of a meiosis-specific protein as a member of the class of cancer/testis antigens.

Little is known about the function of human cancer/testis antigens (CTAs), such as MAGE, BAGE, GAGE, HOM-MEL-40, and NY-ESO-1, the expression of which is restricted to human malignancies and testis. When screening a cDNA expression library enriched for testis-specific representative long transcripts for reactivity with high-titered IgG antibodies from the serum of a patient with renal cell carcinoma, one repeatedly detected antigen, designated HOM-TES-14, turned out to be encoded by the synaptonemal complex protein 1 (SCP-1) gene. SCP-1 is known to be selectively expressed during the meiotic prophase of spermatocytes and is involved in the pairing of homologous chromosomes, an essential step for the generation of haploid cells in meiosis I. Investigation of a broad spectrum of normal and malignant tissues revealed expression of SCP-1 transcripts and antigen selectively in a variety of neoplastic tissues and tumor cell lines. Immunofluorescence microscopy analysis with specific antiserum showed a cell cycle phase-independent nuclear expression of SCP-1 protein in cancer cells. SCP-1 differs from other members of the class of CTA by its localization on chromosome 1 and its frequent expression in malignant gliomas, breast, renal cell, and ovarian cancer. The aberrant expression of SCP-1 in tumors might contribute to their genomic instability and suggests that the functional role of other CTA might also relate to meiosis.

Antigens, Neoplasm↗

PubMed1995

Roles for two RecA homologs in promoting meiotic chromosome synapsis.

Previous studies have shown that the RAD51 and DMC1 genes of Saccharomyces cerevisiae encode homologs of the Escherichia coli RecA strand exchange enzyme. Results presented here demonstrate that the dmc1 and rad51 mutants undergo nearly complete chromosome synapsis, but synaptonemal complex formation is delayed substantially compared with wild type. In the zip1 mutant, chromosomes are paired homologously, but not synapsed, and the protein backbones (axial elements) of each pair of chromosomes are connected intimately to each other at a few sites referred to herein as axial associations. dmc1 zip1 and rad51 zip1 double mutants assemble axial elements that are not obviously associated, demonstrating that the Dmc1 and Rad51 proteins are required to establish or stabilize axial associations. We propose that axial associations serve to promote meiotic chromosome synapsis and that the absence of these associations accounts for the delayed and inefficient synapsis observed in dmc1 and rad51 strains. During meiosis in haploid yeast, chromosome synapsis takes place between nonhomologous chromosome segments. In a zip1 haploid, axial associations are not apparent, suggesting that these associations depend on interactions between homologous sequences.

Alleles↗

PubMed2003

Sex-specific telomere redistribution and synapsis initiation in cattle oogenesis.

The process of homolog pairing is well characterised in meiosis of male mammals, but much less information is available from female meiosis. We have therefore studied telomere dynamics by FISH and synapsis formation by immunostaining of synaptonemal complex proteins (SCP3, SCP1) on ovarian sections from 15 bovine fetuses, which covered the entire female prophase I. Telomeres displayed a dispersed intranuclear distribution in oogonia and relocated to the nuclear periphery during the preleptotene stage. Tight telomere clustering (bouquet formation) coincided with synapsis initiation at the leptotene/zygotene transition. Clustering of telomeres persisted during zygotene and even into the pachytene stage in a subset of nuclei, while it was absent in diplotene/dictyotene stage nuclei. Thus, the bouquet stage in the bovine female lasts significantly longer than in the male. Further, we observed that synapsis in the female initiated both terminally and interstitially in earliest zygotene stage oocytes, which contrasts with the predominantly terminal synapsis initiation in early zygotene spermatocytes of the bovine male. Altogether, our data disclose a sex-specific difference in telomere dynamics and synapsis initiation patterns in male and female bovine germ cells that may be related to the sex-specific differences in recombination rates observed in this and other mammalian species.

Animals↗

PubMed2005

Changes in crossover distribution along a quadrivalent in a man carrier of a reciprocal translocation t(11;14).

A testicular biopsy from an infertile man carrying a heterozygous chromosome translocation t(11;14) was studied with synaptonemal complex analysis and immunolocalization of the protein MLH1 for crossover detection. A full blockage of spermatogenesis at the spermatocyte stage was related to the presence of the translocation quadrivalents at pachytene. Only 2% of the quadrivalents showed full synapsis. Most of the spermatocytes showed asynaptic free ends that frequently mingled with the XY pair. The average number of crossovers per cell was diminished from a mean of 52.7 in controls to a mean of 48 in the patient. The difference between the number of crossovers in the quadrivalent and the normal bivalents was highly significant. The distribution of crossovers over the segment of the quadrivalent corresponding to bivalent #14 was also very different from that of the control. It is concluded that in this translocation, the pattern of crossovers is changed, mainly due to a synaptic hindrance in the quadrivalent, and that the spermatogenesis arrest is mainly due to the quadrivalents that interact with the XY pair.

Chromosomes, Human, Pair 11↗

PubMed1990

[Synapsis in single and double heterozygotes for partially overlapping inversions in chromosome 1 of the house mouse].

Electron microscopic analysis of synaptonemal complexes (SC) in single and double heterozygotes for the partially overlapping inversions In(1)1Icg, In(1)1Rk and In(1)12Rk in the Chromosome 1 of the house mouse reveals a dependence of synapsis and synaptic adjustment on the size and location of the inversions and their interaction. In(1)1Icg contains the insertions of inverted repeats Is(HSR: 1C5)1Icg and Is(HSR: 1I)2Icg as well as inverted euchromatic region. The synaptic adjustment of the D loops by shortening of asynapsed parts of the lateral elements of SC belonging to the insertions occurs at late zygotene-early pachytene stage. After that the synaptic adjustment of the inversion loops takes place. A delay in adjustment was found in diheterozygotes In(1)1Icg/In(1)1Rk and In(1)1Icg/In(1)12Rk. Morphological alterations of the asynapted terminal segments of lateral elements preventing synaptic adjustment were found in single and double heterozygotes for In(1)1Rk and In(1)12Rk. Correspondence between the size of asynapted regions and the probability of association of XY and heteromorphic bivalents was revealed.

Animals↗

PubMed2004

Female-specific features of recombinational double-stranded DNA repair in relation to synapsis and telomere dynamics in human oocytes.

Chromosome segregation errors are a significant cause of aneuploidy among human neonates and often result from errors in female meiosis that occur during fetal life. For the latter reason, little is known about chromosome dynamics during female prophase I. Here, we analyzed chromosome reorganization, and centromere and telomere dynamics in meiosis in the human female by immunofluorescent staining of the SYCP3 and SYCP1 synaptonemal complex proteins and the course of recombinational DNA repair by IF of phospho-histone H2A.X (gamma-H2AX), RPA and MLH1 recombination proteins. We found that SYCP3, but not SYCP1, aggregates appear in the preleptotene nucleus and some persist up to pachytene. Telomere clustering (bouquet stage) in oocytes lasted from late-leptotene to early pachytene-significantly longer than in the male. Leptotene and zygotene oocytes and spermatocytes showed strong gamma-H2AX labeling, while gamma-H2AX patches, which colocalized with RPA, were present on SYCP1-tagged pachytene SCs. This was rarely seen in the male and may suggest that synapsis installs faster with respect to progression of recombinational double-strand break repair or that the latter is slower in the female. It is speculated that the presence of gamma-H2AX into pachytene highlights female-specific peculiarities of recombination, chromosome behavior and checkpoint control that may contribute to female susceptibility for aneuploidy.

Adaptor Proteins, Signal Transducing↗

PubMed1998

Meiotic chromosome morphology and behavior in zip1 mutants of Saccharomyces cerevisiae.

The yeast Zip1 protein (Zip1p) is a component of the central region of the synaptonemal complex (SC). Zip1p is predicted to form a dimer consisting of a coiled-coil domain flanked by globular domains. To analyze the organization of Zip1p within the SC, in-frame deletions of ZIP1 were constructed and analyzed. The results demonstrate that the C terminus but not the N terminus of Zip1p is required for its localization to chromosomes. Deletions in the carboxy half of the predicted coiled-coil region cause decreases in the width of the SC. Based on these results, a model for the organization of Zip1p within the SC is proposed. zip1 deletion mutations were also examined for their effects on sporulation, spore viability, crossing over, and crossover interference. The results demonstrate that the extent of synapsis is positively correlated with the levels of spore viability, crossing over, and crossover interference. In contrast, the role of Zip1p in synapsis is separable from its role in meiotic cell cycle progression. zip1 mutants display interval-specific effects on crossing over.

Antibodies, Fungal↗

PubMed1991

Achiasmatic sex chromosomes in Pitymys duodecimcostatus: mechanisms of association and segregation.

The meiotic behavior of the sex chromosomes of Pitymys duodecimcostatus was studied by electron microscopy of whole-mount synaptonemal complex preparations. The results established that the sex chromosomes of this species are achiasmatic and remain unassociated throughout meiotic prophase I in most spermatocytes. In other cells, nonspecific association of the X and Y occurred by means of filamentous bridges. Pitymys duodecimcostatus represents an additional example of a mammalian species lacking a homologous pairing segment in its sex chromosomes and extends current knowledge about this controversial subject. In this regard, we suggest that sex-chromosome association is a characteristic that probably followed different evolutionary paths in different mammals, leading to loss of the homologous segment in some species and its conservation in others. It is also suggested that in P. duodecimcostatus, and probably in many other species as well, three mechanisms may act in concert to permit joining of the X and Y chromosomes during meiotic prophase, and, consequently, to ensure proper segregation during anaphase I: (1) joining of the sex-chromosome axes at their ends to the nuclear membrane, (2) formation of fibrillar structures to hold the sex chromosomes together, and (3) cohesiveness due to sex-vesicle formation.

Animals↗

PubMed1990

Telomere and centromere DNA are associated with the cores of meiotic prophase chromosomes.

Mouse (Mus musculus) whole-mount, surface-spread, meiotic prophase chromosomes have an axial core structure, the synaptonemal complex, SC, from which extend chromatin loops. This arrangement permits a novel approach to the analysis of chromosome structure. Using in situ hybridization, the types of DNA sequences preferentially associated with the SC and the types located primarily in the chromatin loops can be determined. With biotinylated probes, detected by avidin conjugated to FITC, we present evidence for differential chromatin-SC interaction. The telomere sequence (TTAGGG)n is associated exclusively with the two ends of each autosomal SC rather than with the chromatin loops. The minor satellite DNA sequences are predominantly localized to the centromeric region of the SC, as defined by CREST serum anti-centromere antibodies. In contrast, the major satellite DNA probe hybridizes to the chromatin loops of the centromeric heterochromatin, and a probe containing a LINE sequence hybridizes to chromatin loops in general with no obvious preference for the SC. These observations demonstrate that, depending on the type of DNA sequence, the chromatin has different properties in regard to its association with the SC.

Animals↗

PubMed1997

Genetic interactions between HOP1, RED1 and MEK1 suggest that MEK1 regulates assembly of axial element components during meiosis in the yeast Saccharomyces cerevisiae.

During meiosis, axial elements are generated by the condensation of sister chromatids along a protein core as precursors to the formation of the synaptonemal complex (SC). Functional axial elements are essential for wild-type levels of recombination and proper reductional segregation at meiosis I. Genetic and cytological data suggest that three meiosis-specific genes, HOP1, RED1 and MEK1, are involved in axial element formation in the yeast Saccharomyces cerevisiae. HOP1 and RED1 encode structural components of axial elements while MEK1 encodes a putative protein kinase. Using a partially functional allele of MEK1, new genetic interactions have been found between HOP1, RED1 and MEK1. Overexpression of HOP1 partially suppresses the spore inviability and recombination defects of mek1-974; in contrast, overexpression of RED1 exacerbates the mek1-974 spore inviability. Co-overexpression of HOP1 and RED1 in mek1-974 diploids alleviates the negative effect of overexpressing RED1 alone. Red1p/Red1p as well as Hop1p/Red1p interactions have been reconstituted in two hybrid experiments. Our results suggest a model whereby Mek1 kinase activity controls axial element assembly by regulating the affinity with which Hop1p and Red1p interact with each other.

DNA-Binding Proteins↗

PubMed1997

Extreme axial equalization and wide distribution of recombination nodules in the primitive ZW pair of Rhea americana (Aves, Ratitae).

Pachytene oocytes from the ratite bird Rhea americana were used for synaptonemal complex analysis with a surface spreading technique and phosphotungstic acid staining. The ZW bivalent is slightly smaller than the fourth autosomal bivalent and clearly shows unequal W and Z axes only in 27% of the bivalents. Most of the ZW pairs are completely adjusted and thus the W and Z axes are almost equal in length. A sample of 134 recombination nodules (RNs) from 63 ZW pairs showed a striking departure of number and location of these nodules compared with those of carinate birds. The average number of RNs in the ZW pair of R. americana is 2.13, and the average SC length per RN is 4.2 microm. The locations of the RNs along most of the long arms of the Z and W are not random, and the distances between pairs of RNs show interference. Thus, the pattern of RNs in this mostly euchromatic ZW pair is identical to that of autosomes. From the present and previous data, it is concluded that the ZW pair of R. americana is in a primitive stage of chromosomal differentiation, in which recombination is restricted only in the small short arm and in the pericentromeric region.

Animals↗

PubMed2004

Targeted gene knockout reveals a role in meiotic recombination for ZHP-3, a Zip3-related protein in Caenorhabditis elegans.

The meiotically expressed Zip3 protein is found conserved from Saccharomyces cerevisiae to humans. In baker's yeast, Zip3p has been implicated in synaptonemal complex (SC) formation, while little is known about the protein's function in multicellular organisms. We report here the successful targeted gene disruption of zhp-3 (K02B12.8), the ZIP3 homolog in the nematode Caenorhabditis elegans. Homozygous zhp-3 knockout worms show normal homologue pairing and SC formation. Also, the timing of appearance and the nuclear localization of the recombination protein Rad-51 seem normal in these animals, suggesting proper initiation of meiotic recombination by DNA double-strand breaks. However, the occurrence of univalents during diplotene indicates that C. elegans ZHP-3 protein is essential for reciprocal recombination between homologous chromosomes and thus chiasma formation. In the absence of ZHP-3, reciprocal recombination is abolished and double-strand breaks seem to be repaired via alternative pathways, leading to achiasmatic chromosomes and the occurrence of univalents during meiosis I. Green fluorescent protein-tagged C. elegans ZHP-3 forms lines between synapsed chromosomes and requires the SC for its proper localization.

Amino Acid Sequence↗