Chromatin configuration and epigenetic landscape at the sex chromosome bivalent during equine spermatogenesis
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Pairing of the sex chromosomes during mammalian meiosis is characterized by the formation of a unique heterochromatin structure at the XY body. The mechanisms underlying the formation of this nuclear domain are reportedly highly conserved from marsupials to mammals. In this study, we demonstrate that in contrast to all eutherian species studied to date, partial synapsis of the heterologous sex chromosomes during pachytene stage in the horse is not associated with the formation of a typical macrochromatin domain at the XY body. While phosphorylated histone H2AX (γH2AX) and macroH2A1.2 are present as a diffuse signal over the entire macrochromatin domain in mouse pachytene spermatocytes, γH2AX, macroH2A1.2, and the cohesin subunit SMC3 are preferentially enriched at meiotic sex chromosome cores in equine spermatocytes. Moreover, although several histone modifications associated with this nuclear domain in the mouse such as H3K4me2 and ubH2A are conspicuously absent in the equine XY body, prominent RNA polymerase II foci persist at the sex chromosomes. Thus, the localization of key marker proteins and histone modifications associated with the XY body in the horse differs significantly from all other mammalian systems described. These results demonstrate that the epigenetic landscape and heterochromatinization of the equine XY body might be regulated by alternative mechanisms and that some features of XY body formation may be evolutionary divergent in the domestic horse. We propose equine spermatogenesis as a unique model system for the study of the regulatory networks leading to the epigenetic control of gene expression during XY body formation.
We thank Dr. W. Earnshaw for the generous gift of human CREST antiserum and Drs. Michaela Kristula and Lauren Greene (Department of Clinical Studies, University of Pennsylvania) for providing equine testicular tissue. We are grateful to E. Amenkhienan for helping with preliminary data collection and to Dr. M.A. Handel for comments and critical reading of the manuscript. This research was supported by research grants from the University of Pennsylvania Research Foundation and the National Institutes of Health NIH 2RO1HDO42740 to R. De La Fuente. The support from McCabe Foundation (M. M. Viveiros) and the Havemeyer Foundation to S. M. McDonnell is also acknowledged.
- De La Fuente R, Viveiros M, Burns K, Adashi E, Matzuk M, Eppig J (2004) Major chromatin remodeling in the germinal vesicle (GV) of mammalian oocytes is dispensable for global transcriptional silencing but required for centromeric heterochromatin function. Dev Biol 275(2):447–458CrossRefGoogle Scholar
- Manders EEM, Verbeek FJ, Aten JA (1993) Measurement of co-localisation of objects in dual-colour confocal images. J Microsc 169:375–382Google Scholar
- Page J, Berrios S, Rufas J, Parra M, Suja J, Heyting C, Fernandez-Donoso R (2003) The pairing of X and Y chromosomes during meiotic prophase in the marsupial species Thylamys elegans is maintained by a dense plate developed from their axial elements. J Cell Sci 116(3):551–560PubMedCrossRefGoogle Scholar
- Pelttari J, Hoja M, Yuan L, Liu J, Brundell E, Moens P, Santucci-Darmanin S, Jessberger R, Barbero J, Heyting C, Hoog C (2001) 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. Mol Cell Biol 21(16):5667–5677PubMedCrossRefGoogle Scholar
- Zinchuk V, Zinchuk O (2008) Quantitative colocalization analysis of confocal fluorescence microscopy images. Curr Protoc Cell Biol 39:4.19.1–4.19.16Google Scholar