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Difference between random and imprinted X inactivation in common voles

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Abstract

During early development in female mammals, most genes on one of the two X-chromosomes undergo transcriptional silencing. In the extraembryonic lineages of some eutherian species, imprinted X-inactivation of the paternal X-chromosome occurs. In the cells of the embryo proper, the choice of the future inactive X-chromosome is random. We mapped several genes on the X-chromosomes of five common vole species and compared their expression and methylation patterns in somatic and extraembryonic tissues, where random and imprinted X-inactivation occurs, respectively. In extraembryonic tissues, more genes were expressed on the inactive X-chromosome than in somatic tissues. We also found that the methylation status of the X-linked genes was always in accordance with their expression pattern in somatic, but not in extraembryonic tissues. The data provide new evidence that imprinted X-inactivation is less complete and/or stable than the random form and DNA methylation contributes less to its maintenance.

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Acknowledgments

We are grateful to Elena Grigor’eva for trophoblast stem cell culture and Claire Senner for valuable comments and suggestions. This work was supported by the Russian Foundation for Basic Research (grant No. 08-04-00346) and the Program of the Russian Academy of Sciences “Molecular and Cellular Biology.”

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Authors and Affiliations

  1. Russian Academy of Sciences, Siberian Department, Institute of Cytology and Genetics, Novosibirsk, Russia

    Elena V. Dementyeva, Alexander I. Shevchenko, Olga V. Anopriyenko, Nina A. Mazurok, Eugeny A. Elisaphenko & Suren M. Zakian

  2. Department of Biochemistry, University of Oxford, Oxford, UK

    Tatyana B. Nesterova & Neil Brockdorff

  3. Institute of Cytology and Genetics, ac. Lavrentyev Avenue, 10, Novosibirsk, 630090, Russia

    Suren M. Zakian

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  1. Elena V. Dementyeva
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  2. Alexander I. Shevchenko
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  3. Olga V. Anopriyenko
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  4. Nina A. Mazurok
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  5. Eugeny A. Elisaphenko
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Correspondence to Suren M. Zakian.

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Communicated by E. Nigg

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Supplementary Fig. 1

Mapping of genes on the common vole X-chromosomes. a Fluorescence in situ hybridization of phage clones on the metaphase chromosomes of M. rossiaemeridionalis males. Chromosomes were counterstained with DAPI. b Localization of phage clones on the X-chromosomes of five common vole species. R, M. rossiaemeridionalis; T, M. transcaspicus; K, M. kirgisorum; A, M. arvalis; AG, M. agrestis. DAPI-stained X-chromosomes (left panels) and their banding after applying Smartcapture software (right panels) are shown (TIFF 2242 kb)

Supplementary Fig. 1

Low resolution image (JPEG 440 kb)

Supplementary Fig. 2

Characterization of Microtus rossiaemeridionalis × M. arvalis female fibroblast subclones. a Detection of a late replicating X-chromosome. BrdU 5-bromo-2-deoxyuridine (green); Xa and Xi active and inactive X-chromosomes. The X-chromosome of M. rossiaemeridionalis contains a large constitutive heterochromatic block which is late replicating regardless of X-chromosome status. b Localization of Xist RNA (green) and MS4 repeat (red). Metaphase spreads and nuclei were counterstained with DAPI (blue) (TIFF 2059 kb)

Supplementary Fig. 2

Low resolution image. (JPEG 267 kb)

Supplementary table

Primers for studying the expression status of X-linked genes in hybrid females Microtus rossiaemeridionalis x M. arvalis (DOC 44 kb)

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Dementyeva, E.V., Shevchenko, A.I., Anopriyenko, O.V. et al. Difference between random and imprinted X inactivation in common voles. Chromosoma 119, 541–552 (2010). https://doi.org/10.1007/s00412-010-0277-6

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