Skewed X-inactivation is common in the general female population

X-inactivation is a well-established dosage compensation mechanism ensuring that X-chromosomal genes are expressed at comparable levels in males and females. Skewed X-inactivation is often explained by negative selection of one of the alleles. We demonstrate that imbalanced expression of the paterna...

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Main Authors: Shvetsova, E., Sofronova, A., Monajemi, R., Gagalova, Kristina, Draisma, H.H.M., White, S.J., Santen, G.W.E., Chuva de Sousa Lopes, S.M., Heijmans, B.T., van Meurs, J., Jansen, R., Franke, L., Kiełbasa, S.M., den Dunnen, J.T., ‘t Hoen, P.A.C., Boomsma, D.I., Pool, R., van Dongen, J., Hottenga, J.J., van Greevenbroek, M.M., Stehouwer, C.D., van der Kallen, C.J., Schalkwijk, C.G., Wijmenga, C., Zhernakova, S., Tigchelaar, E.F., Slagboom, P.E., Beekman, M., Deelen, J., van Heemst, D., Veldink, J.H., van den Berg, L.H., van Duijn, C.M., Hofman, B.A., Uitterlinden, A.G., Jhamai, P.M., Verbiest, M., Suchiman, H.E.D., Verkerk, M., van der Breggen, R., van Rooij, J., Lakenberg, N., Mei, H., Bot, J., Zhernakova, D.V., van ’t Hof, P., Deelen, P., Nooren, I., Moed, M., Vermaat, M., Luijk, R., Jan Bonder, M., van Iterson, M., van Dijk, F., van Galen, M., Arindrarto, W., Swertz, M.A., van Zwet, E.W., Isaacs, A., Francioli, L., Menelaou, A., Pulit, S., Palamara, P., Elbers, C., Neerincx, P., Ye, K., Guryev, V., Kloosterman, W., Abdellaoui, A., van Leeuwen, E., van Oven, M., Li, M., Laros, J., Karssen, L., Kanterakis, A., Amin, N., Hottenga, J., Lameijer, E., Kattenberg, M., Dijkstra, M., Byelas, H., van Setten, J., van Schaik, B., Nijman, I., Renkens, I., Marschall, T., Schönhuth, A., Hehir-Kwa, J., Handsaker, R., Polak, P., Sohail, M., Vuzman, D.
Format: Journal Article
Language:English
Published: 2019
Subjects:
Online Access:http://hdl.handle.net/20.500.11937/96875
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author Shvetsova, E.
Sofronova, A.
Monajemi, R.
Gagalova, Kristina
Draisma, H.H.M.
White, S.J.
Santen, G.W.E.
Chuva de Sousa Lopes, S.M.
Heijmans, B.T.
van Meurs, J.
Jansen, R.
Franke, L.
Kiełbasa, S.M.
den Dunnen, J.T.
‘t Hoen, P.A.C.
Boomsma, D.I.
Pool, R.
van Dongen, J.
Hottenga, J.J.
van Greevenbroek, M.M.
Stehouwer, C.D.
van der Kallen, C.J.
Schalkwijk, C.G.
Wijmenga, C.
Zhernakova, S.
Tigchelaar, E.F.
Slagboom, P.E.
Beekman, M.
Deelen, J.
van Heemst, D.
Veldink, J.H.
van den Berg, L.H.
van Duijn, C.M.
Hofman, B.A.
Uitterlinden, A.G.
Jhamai, P.M.
Verbiest, M.
Suchiman, H.E.D.
Verkerk, M.
van der Breggen, R.
van Rooij, J.
Lakenberg, N.
Mei, H.
Bot, J.
Zhernakova, D.V.
van ’t Hof, P.
Deelen, P.
Nooren, I.
Moed, M.
Vermaat, M.
Luijk, R.
Jan Bonder, M.
van Iterson, M.
van Dijk, F.
van Galen, M.
Arindrarto, W.
Swertz, M.A.
van Zwet, E.W.
Isaacs, A.
Francioli, L.
Menelaou, A.
Pulit, S.
Palamara, P.
Elbers, C.
Neerincx, P.
Ye, K.
Guryev, V.
Kloosterman, W.
Abdellaoui, A.
van Leeuwen, E.
van Oven, M.
Li, M.
Laros, J.
Karssen, L.
Kanterakis, A.
Amin, N.
Hottenga, J.
Lameijer, E.
Kattenberg, M.
Dijkstra, M.
Byelas, H.
van Setten, J.
van Schaik, B.
Nijman, I.
Renkens, I.
Marschall, T.
Schönhuth, A.
Hehir-Kwa, J.
Handsaker, R.
Polak, P.
Sohail, M.
Vuzman, D.
author_facet Shvetsova, E.
Sofronova, A.
Monajemi, R.
Gagalova, Kristina
Draisma, H.H.M.
White, S.J.
Santen, G.W.E.
Chuva de Sousa Lopes, S.M.
Heijmans, B.T.
van Meurs, J.
Jansen, R.
Franke, L.
Kiełbasa, S.M.
den Dunnen, J.T.
‘t Hoen, P.A.C.
Boomsma, D.I.
Pool, R.
van Dongen, J.
Hottenga, J.J.
van Greevenbroek, M.M.
Stehouwer, C.D.
van der Kallen, C.J.
Schalkwijk, C.G.
Wijmenga, C.
Zhernakova, S.
Tigchelaar, E.F.
Slagboom, P.E.
Beekman, M.
Deelen, J.
van Heemst, D.
Veldink, J.H.
van den Berg, L.H.
van Duijn, C.M.
Hofman, B.A.
Uitterlinden, A.G.
Jhamai, P.M.
Verbiest, M.
Suchiman, H.E.D.
Verkerk, M.
van der Breggen, R.
van Rooij, J.
Lakenberg, N.
Mei, H.
Bot, J.
Zhernakova, D.V.
van ’t Hof, P.
Deelen, P.
Nooren, I.
Moed, M.
Vermaat, M.
Luijk, R.
Jan Bonder, M.
van Iterson, M.
van Dijk, F.
van Galen, M.
Arindrarto, W.
Swertz, M.A.
van Zwet, E.W.
Isaacs, A.
Francioli, L.
Menelaou, A.
Pulit, S.
Palamara, P.
Elbers, C.
Neerincx, P.
Ye, K.
Guryev, V.
Kloosterman, W.
Abdellaoui, A.
van Leeuwen, E.
van Oven, M.
Li, M.
Laros, J.
Karssen, L.
Kanterakis, A.
Amin, N.
Hottenga, J.
Lameijer, E.
Kattenberg, M.
Dijkstra, M.
Byelas, H.
van Setten, J.
van Schaik, B.
Nijman, I.
Renkens, I.
Marschall, T.
Schönhuth, A.
Hehir-Kwa, J.
Handsaker, R.
Polak, P.
Sohail, M.
Vuzman, D.
author_sort Shvetsova, E.
building Curtin Institutional Repository
collection Online Access
description X-inactivation is a well-established dosage compensation mechanism ensuring that X-chromosomal genes are expressed at comparable levels in males and females. Skewed X-inactivation is often explained by negative selection of one of the alleles. We demonstrate that imbalanced expression of the paternal and maternal X-chromosomes is common in the general population and that the random nature of the X-inactivation mechanism can be sufficient to explain the imbalance. To this end, we analyzed blood-derived RNA and whole-genome sequencing data from 79 female children and their parents from the Genome of the Netherlands project. We calculated the median ratio of the paternal over total counts at all X-chromosomal heterozygous single-nucleotide variants with coverage ≥10. We identified two individuals where the same X-chromosome was inactivated in all cells. Imbalanced expression of the two X-chromosomes (ratios ≤0.35 or ≥0.65) was observed in nearly 50% of the population. The empirically observed skewing is explained by a theoretical model where X-inactivation takes place in an embryonic stage in which eight cells give rise to the hematopoietic compartment. Genes escaping X-inactivation are expressed from both alleles and therefore demonstrate less skewing than inactivated genes. Using this characteristic, we identified three novel escapee genes (SSR4, REPS2, and SEPT6), but did not find support for many previously reported escapee genes in blood. Our collective data suggest that skewed X-inactivation is common in the general population. This may contribute to manifestation of symptoms in carriers of recessive X-linked disorders. We recommend that X-inactivation results should not be used lightly in the interpretation of X-linked variants.
first_indexed 2025-11-14T11:47:25Z
format Journal Article
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institution Curtin University Malaysia
institution_category Local University
language eng
last_indexed 2025-11-14T11:47:25Z
publishDate 2019
recordtype eprints
repository_type Digital Repository
spelling curtin-20.500.11937-968752025-02-13T00:44:21Z Skewed X-inactivation is common in the general female population Shvetsova, E. Sofronova, A. Monajemi, R. Gagalova, Kristina Draisma, H.H.M. White, S.J. Santen, G.W.E. Chuva de Sousa Lopes, S.M. Heijmans, B.T. van Meurs, J. Jansen, R. Franke, L. Kiełbasa, S.M. den Dunnen, J.T. ‘t Hoen, P.A.C. Boomsma, D.I. Pool, R. van Dongen, J. Hottenga, J.J. van Greevenbroek, M.M. Stehouwer, C.D. van der Kallen, C.J. Schalkwijk, C.G. Wijmenga, C. Zhernakova, S. Tigchelaar, E.F. Slagboom, P.E. Beekman, M. Deelen, J. van Heemst, D. Veldink, J.H. van den Berg, L.H. van Duijn, C.M. Hofman, B.A. Uitterlinden, A.G. Jhamai, P.M. Verbiest, M. Suchiman, H.E.D. Verkerk, M. van der Breggen, R. van Rooij, J. Lakenberg, N. Mei, H. Bot, J. Zhernakova, D.V. van ’t Hof, P. Deelen, P. Nooren, I. Moed, M. Vermaat, M. Luijk, R. Jan Bonder, M. van Iterson, M. van Dijk, F. van Galen, M. Arindrarto, W. Swertz, M.A. van Zwet, E.W. Isaacs, A. Francioli, L. Menelaou, A. Pulit, S. Palamara, P. Elbers, C. Neerincx, P. Ye, K. Guryev, V. Kloosterman, W. Abdellaoui, A. van Leeuwen, E. van Oven, M. Li, M. Laros, J. Karssen, L. Kanterakis, A. Amin, N. Hottenga, J. Lameijer, E. Kattenberg, M. Dijkstra, M. Byelas, H. van Setten, J. van Schaik, B. Nijman, I. Renkens, I. Marschall, T. Schönhuth, A. Hehir-Kwa, J. Handsaker, R. Polak, P. Sohail, M. Vuzman, D. Calcium-Binding Proteins Female Humans Intracellular Signaling Peptides and Proteins Male Membrane Glycoproteins Netherlands Polymorphism, Single Nucleotide Population Receptors, Cytoplasmic and Nuclear Receptors, Peptide Septins X Chromosome Inactivation BIOS consortium GoNL consortium Humans Intracellular Signaling Peptides and Proteins Calcium-Binding Proteins Membrane Glycoproteins Receptors, Peptide Receptors, Cytoplasmic and Nuclear Polymorphism, Single Nucleotide Population Netherlands Female Male X Chromosome Inactivation Septins X-inactivation is a well-established dosage compensation mechanism ensuring that X-chromosomal genes are expressed at comparable levels in males and females. Skewed X-inactivation is often explained by negative selection of one of the alleles. We demonstrate that imbalanced expression of the paternal and maternal X-chromosomes is common in the general population and that the random nature of the X-inactivation mechanism can be sufficient to explain the imbalance. To this end, we analyzed blood-derived RNA and whole-genome sequencing data from 79 female children and their parents from the Genome of the Netherlands project. We calculated the median ratio of the paternal over total counts at all X-chromosomal heterozygous single-nucleotide variants with coverage ≥10. We identified two individuals where the same X-chromosome was inactivated in all cells. Imbalanced expression of the two X-chromosomes (ratios ≤0.35 or ≥0.65) was observed in nearly 50% of the population. The empirically observed skewing is explained by a theoretical model where X-inactivation takes place in an embryonic stage in which eight cells give rise to the hematopoietic compartment. Genes escaping X-inactivation are expressed from both alleles and therefore demonstrate less skewing than inactivated genes. Using this characteristic, we identified three novel escapee genes (SSR4, REPS2, and SEPT6), but did not find support for many previously reported escapee genes in blood. Our collective data suggest that skewed X-inactivation is common in the general population. This may contribute to manifestation of symptoms in carriers of recessive X-linked disorders. We recommend that X-inactivation results should not be used lightly in the interpretation of X-linked variants. 2019 Journal Article http://hdl.handle.net/20.500.11937/96875 10.1038/s41431-018-0291-3 eng http://creativecommons.org/licenses/by/4.0/ fulltext
spellingShingle Calcium-Binding Proteins
Female
Humans
Intracellular Signaling Peptides and Proteins
Male
Membrane Glycoproteins
Netherlands
Polymorphism, Single Nucleotide
Population
Receptors, Cytoplasmic and Nuclear
Receptors, Peptide
Septins
X Chromosome Inactivation
BIOS consortium
GoNL consortium
Humans
Intracellular Signaling Peptides and Proteins
Calcium-Binding Proteins
Membrane Glycoproteins
Receptors, Peptide
Receptors, Cytoplasmic and Nuclear
Polymorphism, Single Nucleotide
Population
Netherlands
Female
Male
X Chromosome Inactivation
Septins
Shvetsova, E.
Sofronova, A.
Monajemi, R.
Gagalova, Kristina
Draisma, H.H.M.
White, S.J.
Santen, G.W.E.
Chuva de Sousa Lopes, S.M.
Heijmans, B.T.
van Meurs, J.
Jansen, R.
Franke, L.
Kiełbasa, S.M.
den Dunnen, J.T.
‘t Hoen, P.A.C.
Boomsma, D.I.
Pool, R.
van Dongen, J.
Hottenga, J.J.
van Greevenbroek, M.M.
Stehouwer, C.D.
van der Kallen, C.J.
Schalkwijk, C.G.
Wijmenga, C.
Zhernakova, S.
Tigchelaar, E.F.
Slagboom, P.E.
Beekman, M.
Deelen, J.
van Heemst, D.
Veldink, J.H.
van den Berg, L.H.
van Duijn, C.M.
Hofman, B.A.
Uitterlinden, A.G.
Jhamai, P.M.
Verbiest, M.
Suchiman, H.E.D.
Verkerk, M.
van der Breggen, R.
van Rooij, J.
Lakenberg, N.
Mei, H.
Bot, J.
Zhernakova, D.V.
van ’t Hof, P.
Deelen, P.
Nooren, I.
Moed, M.
Vermaat, M.
Luijk, R.
Jan Bonder, M.
van Iterson, M.
van Dijk, F.
van Galen, M.
Arindrarto, W.
Swertz, M.A.
van Zwet, E.W.
Isaacs, A.
Francioli, L.
Menelaou, A.
Pulit, S.
Palamara, P.
Elbers, C.
Neerincx, P.
Ye, K.
Guryev, V.
Kloosterman, W.
Abdellaoui, A.
van Leeuwen, E.
van Oven, M.
Li, M.
Laros, J.
Karssen, L.
Kanterakis, A.
Amin, N.
Hottenga, J.
Lameijer, E.
Kattenberg, M.
Dijkstra, M.
Byelas, H.
van Setten, J.
van Schaik, B.
Nijman, I.
Renkens, I.
Marschall, T.
Schönhuth, A.
Hehir-Kwa, J.
Handsaker, R.
Polak, P.
Sohail, M.
Vuzman, D.
Skewed X-inactivation is common in the general female population
title Skewed X-inactivation is common in the general female population
title_full Skewed X-inactivation is common in the general female population
title_fullStr Skewed X-inactivation is common in the general female population
title_full_unstemmed Skewed X-inactivation is common in the general female population
title_short Skewed X-inactivation is common in the general female population
title_sort skewed x-inactivation is common in the general female population
topic Calcium-Binding Proteins
Female
Humans
Intracellular Signaling Peptides and Proteins
Male
Membrane Glycoproteins
Netherlands
Polymorphism, Single Nucleotide
Population
Receptors, Cytoplasmic and Nuclear
Receptors, Peptide
Septins
X Chromosome Inactivation
BIOS consortium
GoNL consortium
Humans
Intracellular Signaling Peptides and Proteins
Calcium-Binding Proteins
Membrane Glycoproteins
Receptors, Peptide
Receptors, Cytoplasmic and Nuclear
Polymorphism, Single Nucleotide
Population
Netherlands
Female
Male
X Chromosome Inactivation
Septins
url http://hdl.handle.net/20.500.11937/96875