Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing
- PMID: 8794855
- PMCID: PMC2120985
- DOI: 10.1083/jcb.134.5.1109
Centromere and telomere movements during early meiotic prophase of mouse and man are associated with the onset of chromosome pairing
Abstract
The preconditions and early steps of meiotic chromosome pairing were studied by fluorescence in situ hybridization (FISH) with chromosome-specific DNA probes to mouse and human testis tissue sections. Premeiotic pairing of homologous chromosomes was not detected in spermatogonia of the two species. FISH with centromere- and telomere-specific DNA probes in combination with immunostaining (IS) of synaptonemal complex (SC) proteins to testis sections of prepuberal mice at days 4-12 post partum was performed to study sequentially the meiotic pairing process. Movements of centromeres and then telomeres to the nuclear envelope, and of telomeres along the nuclear envelope leading to the formation of a chromosomal bouquet were detected during mouse prophase. At the bouquet stage, pairing of a mouse chromosome-8-specific probe was observed. SC-IS and simultaneous telomere FISH revealed that axial element proteins appear as large aggregates in mouse meiocytes when telomeres are attached to the nuclear envelope. Axial element formation initiates during tight telomere clustering and transverse filament-IS indicated the initiation of synapsis during this stage. Comparison of telomere and centromere distribution patterns of mouse and human meiocytes revealed movements of centromeres and then telomeres to the nuclear envelope and subsequent bouquet formation as conserved motifs of the pairing process. Chromosome painting in human spermatogonia revealed compacted, largely mutually exclusive chromosome territories. The territories developed into long, thin threads at the onset of meiotic prophase. Based on these results a unified model of the pairing process is proposed.
Similar articles
-
Centromere and telomere redistribution precedes homologue pairing and terminal synapsis initiation during prophase I of cattle spermatogenesis.Cytogenet Cell Genet. 2001;93(3-4):304-14. doi: 10.1159/000057002. Cytogenet Cell Genet. 2001. PMID: 11528130
-
Dynamics of chromosome organization and pairing during meiotic prophase in fission yeast.J Cell Biol. 1994 Oct;127(2):273-85. doi: 10.1083/jcb.127.2.273. J Cell Biol. 1994. PMID: 7929575 Free PMC article.
-
Telomere attachment, meiotic chromosome condensation, pairing, and bouquet stage duration are modified in spermatocytes lacking axial elements.Mol Biol Cell. 2004 Feb;15(2):827-37. doi: 10.1091/mbc.e03-07-0524. Epub 2003 Dec 2. Mol Biol Cell. 2004. PMID: 14657244 Free PMC article.
-
The molecular control of meiotic chromosomal behavior: events in early meiotic prophase in Drosophila oocytes.Annu Rev Physiol. 2012;74:425-51. doi: 10.1146/annurev-physiol-020911-153342. Annu Rev Physiol. 2012. PMID: 22335798 Review.
-
Telomere distribution and dynamics in somatic and meiotic nuclei of Arabidopsis thaliana.Cytogenet Genome Res. 2009;124(3-4):193-201. doi: 10.1159/000218125. Epub 2009 Jun 25. Cytogenet Genome Res. 2009. PMID: 19556773 Review.
Cited by
-
Models of germ cell development and their application for toxicity studies.Environ Mol Mutagen. 2015 Oct;56(8):637-49. doi: 10.1002/em.21946. Epub 2015 Mar 28. Environ Mol Mutagen. 2015. PMID: 25821157 Free PMC article. Review.
-
Meiotic telomere distribution and Sertoli cell nuclear architecture are altered in Atm- and Atm-p53-deficient mice.Mol Cell Biol. 2000 Oct;20(20):7773-83. doi: 10.1128/MCB.20.20.7773-7783.2000. Mol Cell Biol. 2000. PMID: 11003672 Free PMC article.
-
Human imprinted chromosomal regions are historical hot-spots of recombination.PLoS Genet. 2006 Jul;2(7):e101. doi: 10.1371/journal.pgen.0020101. Epub 2006 May 22. PLoS Genet. 2006. PMID: 16839189 Free PMC article.
-
Transmembrane protein Sun2 is involved in tethering mammalian meiotic telomeres to the nuclear envelope.Proc Natl Acad Sci U S A. 2007 May 1;104(18):7426-31. doi: 10.1073/pnas.0609198104. Epub 2007 Apr 23. Proc Natl Acad Sci U S A. 2007. PMID: 17452644 Free PMC article.
-
Identification of two human nuclear proteins that recognise the cytosine-rich strand of human telomeres in vitro.Nucleic Acids Res. 2000 Apr 1;28(7):1564-75. doi: 10.1093/nar/28.7.1564. Nucleic Acids Res. 2000. PMID: 10710423 Free PMC article.
References
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources
Other Literature Sources