Human meiosis VIII. Chromosome pairing and formation of the synaptonemal complex in oocytes

Abstract

Human oocytes from three foetal ovaries have been investigated by serial sectioning and three dimensional reconstruction of nuclei from electron micrographs. Analysis of three leptotene-early zygotene, five mid zygotene and ten late zygotene oocytes including complete reconstruction of five zygotene nuclei have led to the following observations and conclusions. 1) Formation of the synaptonemal complex involves, as in other organisms, the organization of a lateral component along each chromosome, attachment of the telomere regions to the inner membrane of the nuclear envelope at leptotene, redistribution of the attached telomeres during the formation of a chromosome bouquet at early zygotene and thereafter progressive chromosome pairing with the synaptonemal complex. 2) Chromosome and bivalent interlockings as well as breaks were common at mid zygotene, but absent when pairing and synaptonemal complex formation were almost complete. Most of the breaks had occurred in the vicinity of presumptive interlockings and appear to be instrumental in the resolution of interlockings. 3) Nonhomologous pairing involving short regions of the complement were observed in two of the mid zygotene nuclei, thus resulting in associations of three or more chromosomes. 4) Twelve of the 23 bivalents can be identified by relative lengths, centromere indices and the structural markers on chromosomes 1, 6, 9, 13-15 and 21-22. 5) The length of the lateral component complement exceeds that of the spermatocytes by a factor of two. 6) On an average 58 recombination nodules was observed per nucleus at mid zygotene (61% of the chromosome complement paired) and 70 at late zygotene (98% of the chromosome complement paired). Thus in spite of the twofold longer synaptonemal complexes in the oocytes, the number of nodules is the same in both sexes.

Pairing and synapsis in oocytes from female fetuses with euploid and aneuploid chromosome complements

“…Since the first piece of evidence of telomeric clustering has been detected during the leptotene/zygotene transition in human oocytes (Roig et al 2004(Roig et al , 2005b, as was already proposed in humans (Bojko 1983) and demonstrated in other species (Scherthan 2003), these results seem to support the hypothesis that bouquet topology promotes homologue encounter and facilitates the synaptic process during meiotic prophase.…”

“…However, human female meiosis is still poorly understood because it is initiated during the fetal time period, and the obtainment of samples for the analysis is difficult. Nevertheless, some papers have studied human oocyte I using classical approaches mainly focusing on the establishment of the time frame in which meiotic prophase takes place in the human female, but also analyzing how homologues synapse (Ohno et al 1962, Baker 1963, Blandau 1969, Kurilo 1981, Bojko 1983, Speed 1985, Garcia et al 1987, 1989. Fluorescence in situ hybridization (FISH) has enabled the analysis of particular homologue pairing processes of euploid and aneuploid oocytes using whole chromosome probes (WCP) alone or combined with locus identification probes (Cheng & Gartler 1994, Cheng et al 1995, 1998, Cheng & NaluaiCecchini 2004, Roig et al 2005a or particular sets of probes to study oocytes with rearranged genomes (Cheng et al 1999, Cheng & Naluai-Cecchini 2004.…”

“…More recently, studies have used immunofluorescence (IF) to primarily analyze meiotic recombination (Barlow & Hultén 1997, Hartshorne et al 1999, Roig et al 2004, 2005b, Lenzi et al 2005. In most of these studies, important differences concerning homologue synapsis and the recombination progression process between male and female meiosis are described both in humans (Bojko 1983, Rasmussen & Holm 1984, Roig et al 2004, Lenzi et al 2005, Oliver-Bonet et al 2005) and mice (Morelli & Cohen 2005), suggesting that these may be involved in the differences observed in the origin of human aneuploidy.…”

Diagnostic investigations in individuals with mental retardation: a systematic literature review of their usefulness

“…There is no good explanation for this finding. Theoretically, one can speculate that structural anomalies occur more often in females than in males due to (1) genes on the sex chromosomes which regulate the three-dimensional DNA structure, thereby influencing crossover frequencies or other trans-actions between chromosomes; (2) the decreased degree of condensation during meiosis in females, 119 resulting in more frequent abnormal pairing of chromosome regions, for instance in those harbouring olfactory receptor-gene clusters. 120,121 (3) Structural anomalies occur in both genders with equal frequency, but female predominance is explained by an increased prenatal or early postnatal survival of females with such an aberration.…”

Chromosome 18 pairing behavior in human trisomic oocytes. Presence of an extra chromosome extends bouquet stage

“…In order to promote homologous synapsis, chromosome ends (telomeres) cluster at a limited portion of the nuclear envelope, known as bouquet topology (for reviews see Scherthan 2001 andHarper et al 2004). Studies in cattle and human have revealed that bouquet topology lasts longer in the mammalian female than in the male (Bojko 1983, Pfeifer et al 2003, Roig et al 2004. At pachytene, all homologs are completely paired (bivalents).…”