Genetic Architecture of Skewed X Inactivation in the Laboratory Mouse
Publication Date
October 03, 2013
Journal
PLOS Genetics
Authors
John D. Calaway, Alan B. Lenarcic, John P. Didion, Jeremy R. Wang, et al
Volume
9
Issue
10
Pages
e1003853
DOI
https://dx.plos.org/10.1371/journal.pgen.1003853
Publisher URL
http://journals.plos.org/plosgenetics/article?id=10.1371%2Fjournal.pgen.1003853
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/24098153
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3789830
Europe PMC
http://europepmc.org/abstract/MED/24098153
Web of Science
000330367200032
Scopus
84887276151
Mendeley
http://www.mendeley.com/research/genetic-architecture-skewed-x-inactivation-laboratory-mouse
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Mendeley | Further Information

{"title"=>"Genetic Architecture of Skewed X Inactivation in the Laboratory Mouse", "type"=>"journal", "authors"=>[{"first_name"=>"John D.", "last_name"=>"Calaway", "scopus_author_id"=>"36052303000"}, {"first_name"=>"Alan B.", "last_name"=>"Lenarcic", "scopus_author_id"=>"55019055900"}, {"first_name"=>"John P.", "last_name"=>"Didion", "scopus_author_id"=>"36052312600"}, {"first_name"=>"Jeremy R.", "last_name"=>"Wang", "scopus_author_id"=>"36610918800"}, {"first_name"=>"Jeremy B.", "last_name"=>"Searle", "scopus_author_id"=>"7102976955"}, {"first_name"=>"Leonard", "last_name"=>"McMillan", "scopus_author_id"=>"7006461052"}, {"first_name"=>"William", "last_name"=>"Valdar", "scopus_author_id"=>"8235236400"}, {"first_name"=>"Fernando", "last_name"=>"Pardo-Manuel de Villena", "scopus_author_id"=>"6601922831"}], "year"=>2013, "source"=>"PLoS Genetics", "identifiers"=>{"isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "pmid"=>"24098153", "doi"=>"10.1371/journal.pgen.1003853", "pui"=>"370217915", "issn"=>"15537390", "sgr"=>"84887276151", "scopus"=>"2-s2.0-84887276151"}, "id"=>"1bb307c2-ea3c-3ccd-a6b6-dfc50fdf476f", "abstract"=>"X chromosome inactivation (XCI) is the mammalian mechanism of dosage compensation that balances X-linked gene expression between the sexes. Early during female development, each cell of the embryo proper independently inactivates one of its two parental X-chromosomes. In mice, the choice of which X chromosome is inactivated is affected by the genotype of a cis-acting locus, the X-chromosome controlling element (Xce). Xce has been localized to a 1.9 Mb interval within the X-inactivation center (Xic), yet its molecular identity and mechanism of action remain unknown. We combined genotype and sequence data for mouse stocks with detailed phenotyping of ten inbred strains and with the development of a statistical model that incorporates phenotyping data from multiple sources to disentangle sources of XCI phenotypic variance in natural female populations on X inactivation. We have reduced the Xce candidate 10-fold to a 176 kb region located approximately 500 kb proximal to Xist. We propose that structural variation in this interval explains the presence of multiple functional Xce alleles in the genus Mus. We have identified a new allele, Xce(e) present in Mus musculus and a possible sixth functional allele in Mus spicilegus. We have also confirmed a parent-of-origin effect on X inactivation choice and provide evidence that maternal inheritance magnifies the skewing associated with strong Xce alleles. Based on the phylogenetic analysis of 155 laboratory strains and wild mice we conclude that Xce(a) is either a derived allele that arose concurrently with the domestication of fancy mice but prior the derivation of most classical inbred strains or a rare allele in the wild. Furthermore, we have found that despite the presence of multiple haplotypes in the wild Mus musculus domesticus has only one functional Xce allele, Xce(b). Lastly, we conclude that each mouse taxa examined has a different functional Xce allele.", "link"=>"http://www.mendeley.com/research/genetic-architecture-skewed-x-inactivation-laboratory-mouse", "reader_count"=>53, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>4, "Researcher"=>21, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>3, "Student > Master"=>4, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>4, "Researcher"=>21, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>3, "Student > Master"=>4, "Student > Bachelor"=>4, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>16, "Mathematics"=>1, "Agricultural and Biological Sciences"=>28, "Neuroscience"=>4, "Veterinary Science and Veterinary Medicine"=>1, "Psychology"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Neuroscience"=>{"Neuroscience"=>4}, "Psychology"=>{"Psychology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>28}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>16}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Belgium"=>1, "United States"=>1}, "group_count"=>8}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1223539"], "description"=>"<p>Shown is allele-specific expression from reciprocal F1 <i>Xce</i> heterozygotes. The X-axis is partitioned according to <i>Xce</i> allele pairs. The Y-axis is the ratio of allele-specific expression from the X chromosome harboring the stronger <i>Xce</i> allele. Ratios were determined using either RNAseq or pyrosequencing.</p>", "links"=>[], "tags"=>["inheritance", "magnifies", "xci"], "article_id"=>813805, "categories"=>["Biological Sciences"], "users"=>["John D. Calaway", "Alan B. Lenarcic", "John P. Didion", "Jeremy R. Wang", "Jeremy B. Searle", "Leonard McMillan", "William Valdar", "Fernando Pardo-Manuel de Villena"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003853.g006", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Maternal_inheritance_magnifies_XCI_skewing_/813805", "title"=>"Maternal inheritance magnifies XCI skewing.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-03 02:11:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1223534"], "description"=>"<p>In panel A, the candidate interval is show as a thick black bar. Below the candidate interval is a dotplot generated from pairwise sequence concordance in the mm9 genome assembly. Diagonal lines slanting down from left to right are duplications, while diagonal lines slanting up from left to right are inversions. Above the dotplot are arrows that show the four duplications (SD1-4) and inversion (I5) identified. Panel B is a phylogenetic tree that depicts the relationship between the duplications. The phylogenetic tree was generated using the CLUSTALW2 alignment software <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003853#pgen.1003853-Larkin1\" target=\"_blank\">[71]</a>. Also shown are the ten MegaMUGA markers used for the PCA analysis and their positions in relation to the segmental duplications. Shown in panel C are probe hybridization plots for two of these markers, UNC31159403 and XiD2 (all plots are provided in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003853#pgen.1003853.s002\" target=\"_blank\">Figure S2</a>). The axes represent hybridization intensities for probes tracking alternative alleles at each marker. The colors correspond to the different functional <i>Xce</i> alleles: gray <i>Xce<sup>a</sup></i>; blue <i>Xce<sup>b</sup></i>; red <i>Xce<sup>e</sup></i>; green <i>Xce<sup>c</sup></i>; yellow <i>Xce<sup>d</sup></i>. Note that these plots do not agree with the expectations for standard biallelic variants. Typically biallelic variant plots show three distinct clusters representing homozygous A, homozygous B, or heterozygous A/B.</p>", "links"=>[], "tags"=>[], "article_id"=>813800, "categories"=>["Biological Sciences"], "users"=>["John D. Calaway", "Alan B. Lenarcic", "John P. Didion", "Jeremy R. Wang", "Jeremy B. Searle", "Leonard McMillan", "William Valdar", "Fernando Pardo-Manuel de Villena"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003853.g004", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sequence_analysis_of_the_candidate_interval_/813800", "title"=>"Sequence analysis of the candidate interval.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-03 02:11:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1223532"], "description"=>"<p>Panel A is a plot of the allele-specific expression data from F1 hybrids, where each colored letter represents an individual gene measurement from brain (“b”), kidney (“k”), and liver (“v”) from an individual female. Panel B is a plot of the posterior mean and confidence intervals for XCI fraction inferred for each genetic cross, based on our statistical model. Throughout, the x-axis reports the fraction of X-linked allele-specific expression from the strain with the unknown <i>Xce</i> allele. The color of each letter (on the right) and each corresponding posterior (on the left) denote the known <i>Xce</i> allele to which it is paired: black <i>Xce<sup>a</sup></i>; blue <i>Xce<sup>b</sup></i> and red <i>Xce<sup>c</sup></i>. Panel C is shows the inbred strains phenotyped for <i>Xce</i>, the strains each were crossed to, the total number of F1 females tested and the <i>Xce</i> alleles excluded and included based on posterior tail probabilities.</p>", "links"=>[], "tags"=>["imbalance", "f1"], "article_id"=>813798, "categories"=>["Biological Sciences"], "users"=>["John D. Calaway", "Alan B. Lenarcic", "John P. Didion", "Jeremy R. Wang", "Jeremy B. Searle", "Leonard McMillan", "William Valdar", "Fernando Pardo-Manuel de Villena"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003853.g003", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Allelic_imbalance_in_selected_female_F1_hybrids_/813798", "title"=>"Allelic imbalance in selected female F1 hybrids.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-03 02:11:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1223529"], "description"=>"<p>Panel A shows the order of <i>Xce</i> allele strength. Panel B shows hypothetical distribution and mean XCI ratio skewing in female populations that are either homozygous or heterozygous for <i>Xce</i> alleles.</p>", "links"=>[], "tags"=>["allelic"], "article_id"=>813795, "categories"=>["Biological Sciences"], "users"=>["John D. Calaway", "Alan B. Lenarcic", "John P. Didion", "Jeremy R. Wang", "Jeremy B. Searle", "Leonard McMillan", "William Valdar", "Fernando Pardo-Manuel de Villena"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003853.g001", "stats"=>{"downloads"=>0, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Xce_allelic_series_/813795", "title"=>"The <i>Xce</i> allelic series.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-03 02:11:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1223536"], "description"=>"<p>Panel A shows a three-dimensional PCA plot based on hybridization intensity of ten MegaMUGA probes (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003853#pgen-1003853-g004\" target=\"_blank\">Figure 4</a> and <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003853#pgen.1003853.s014\" target=\"_blank\">Table S10</a>) within the refined <i>Xce</i> candidate interval. Mouse strains with known <i>Xce</i> alleles are shown as large spheres, while predicted mouse strains and wild-mice are shown as smaller spheres. Mouse samples are shaded according to <i>Xce</i> allele or <i>Xce</i> haplotype: Known <i>Xce<sup>a</sup></i> allele, black; predicted <i>Xce<sup>a</sup></i> allele, gray; known <i>Xce<sup>b</sup></i> allele, blue; predicted <i>Xce<sup>b</sup></i> allele, light blue; known <i>Xce<sup>c</sup></i> allele, green; predicted <i>Xce<sup>c</sup></i> allele, light green; known <i>Xce<sup>d</sup></i> allele, orange; predicted <i>Xce<sup>d</sup></i> allele, yellow; known <i>Xce<sup>d</sup></i> allele, orange; predicted <i>Xce<sup>d</sup></i> allele, yellow; known <i>Xce<sup>e</sup></i> allele, red; predicted <i>Xce<sup>e</sup></i> allele, pink; known <i>Xce<sup>f</sup></i> allele, magenta. Panel B shows a phylogenetic tree based on 18 MDA SNP probes within the new <i>Xce</i> candidate interval. The topography of the tree accurately reflects the genetic relationship between the <i>Xce</i> alleles, however because of the limited number of SNP used to generate the tree and the ascertainment bias of the SNPs present on the MDA <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003853#pgen.1003853-Yang1\" target=\"_blank\">[40]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003853#pgen.1003853-Keane1\" target=\"_blank\">[41]</a>, the tree is misleading with respect to the true genetic distance between <i>Xce</i> haplotypes (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003853#pgen.1003853.s004\" target=\"_blank\">Figure S4</a> for a more accurate representation of branch lengths). Open circles represent classical inbred strains with unknown <i>Xce</i> alleles; filled circles represent wild-derived or wild-caught mice with unknown <i>Xce</i> alleles; open squares represent classical inbred strains phenotyped for <i>Xce</i>; filled squares represent wild-derived strains with known <i>Xce</i> alleles. Strains with whole genome sequence data are shown with a star. We color coded the specific or subspecific origin of the candidate interval for the four major branches of the tree: red, <i>M. m. musculus</i>; blue, <i>M. m. domesticus</i>; green, <i>M. m. castaneus</i>, orange, <i>M. spretus</i>, pink, <i>Mus spicilegus </i><a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003853#pgen.1003853-Yalcin1\" target=\"_blank\">[53]</a>.</p>", "links"=>[], "tags"=>[], "article_id"=>813802, "categories"=>["Biological Sciences"], "users"=>["John D. Calaway", "Alan B. Lenarcic", "John P. Didion", "Jeremy R. Wang", "Jeremy B. Searle", "Leonard McMillan", "William Valdar", "Fernando Pardo-Manuel de Villena"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003853.g005", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Natural_history_of_Xce_/813802", "title"=>"Natural history of <i>Xce</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-03 02:11:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1223556", "https://ndownloader.figshare.com/files/1223557", "https://ndownloader.figshare.com/files/1223558", "https://ndownloader.figshare.com/files/1223559", "https://ndownloader.figshare.com/files/1223560", "https://ndownloader.figshare.com/files/1223561", "https://ndownloader.figshare.com/files/1223562", "https://ndownloader.figshare.com/files/1223563", "https://ndownloader.figshare.com/files/1223564", "https://ndownloader.figshare.com/files/1223565", "https://ndownloader.figshare.com/files/1223566", "https://ndownloader.figshare.com/files/1223568", "https://ndownloader.figshare.com/files/1223569", "https://ndownloader.figshare.com/files/1223570"], "description"=>"<div><p>X chromosome inactivation (XCI) is the mammalian mechanism of dosage compensation that balances X-linked gene expression between the sexes. Early during female development, each cell of the embryo proper independently inactivates one of its two parental X-chromosomes. In mice, the choice of which X chromosome is inactivated is affected by the genotype of a <i>cis</i>-acting locus, the <i>X-chromosome controlling element</i> (<i>Xce</i>). <i>Xce</i> has been localized to a 1.9 Mb interval within the X-inactivation center (<i>Xic</i>), yet its molecular identity and mechanism of action remain unknown. We combined genotype and sequence data for mouse stocks with detailed phenotyping of ten inbred strains and with the development of a statistical model that incorporates phenotyping data from multiple sources to disentangle sources of XCI phenotypic variance in natural female populations on X inactivation. We have reduced the <i>Xce</i> candidate 10-fold to a 176 kb region located approximately 500 kb proximal to <i>Xist</i>. We propose that structural variation in this interval explains the presence of multiple functional <i>Xce</i> alleles in the genus <i>Mus</i>. We have identified a new allele, <i>Xce<sup>e</sup></i> present in <i>Mus musculus</i> and a possible sixth functional allele in <i>Mus spicilegus</i>. We have also confirmed a parent-of-origin effect on X inactivation choice and provide evidence that maternal inheritance magnifies the skewing associated with strong <i>Xce</i> alleles. Based on the phylogenetic analysis of 155 laboratory strains and wild mice we conclude that <i>Xce<sup>a</sup></i> is either a derived allele that arose concurrently with the domestication of fancy mice but prior the derivation of most classical inbred strains or a rare allele in the wild. Furthermore, we have found that despite the presence of multiple haplotypes in the wild <i>Mus musculus domesticus</i> has only one functional <i>Xce</i> allele, <i>Xce<sup>b</sup></i>. Lastly, we conclude that each mouse taxa examined has a different functional <i>Xce</i> allele.</p></div>", "links"=>[], "tags"=>["skewed", "inactivation"], "article_id"=>813815, "categories"=>["Biological Sciences"], "users"=>["John D. Calaway", "Alan B. Lenarcic", "John P. Didion", "Jeremy R. Wang", "Jeremy B. Searle", "Leonard McMillan", "William Valdar", "Fernando Pardo-Manuel de Villena"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003853.s001", "https://dx.doi.org/10.1371/journal.pgen.1003853.s002", "https://dx.doi.org/10.1371/journal.pgen.1003853.s003", "https://dx.doi.org/10.1371/journal.pgen.1003853.s004", "https://dx.doi.org/10.1371/journal.pgen.1003853.s005", "https://dx.doi.org/10.1371/journal.pgen.1003853.s006", "https://dx.doi.org/10.1371/journal.pgen.1003853.s007", "https://dx.doi.org/10.1371/journal.pgen.1003853.s008", "https://dx.doi.org/10.1371/journal.pgen.1003853.s009", "https://dx.doi.org/10.1371/journal.pgen.1003853.s010", "https://dx.doi.org/10.1371/journal.pgen.1003853.s011", "https://dx.doi.org/10.1371/journal.pgen.1003853.s012", "https://dx.doi.org/10.1371/journal.pgen.1003853.s013", "https://dx.doi.org/10.1371/journal.pgen.1003853.s014"], "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genetic_Architecture_of_Skewed_X_Inactivation_in_the_Laboratory_Mouse_/813815", "title"=>"Genetic Architecture of Skewed X Inactivation in the Laboratory Mouse", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-10-03 02:11:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/1223530"], "description"=>"<p>Panel A is a phylogenetic tree that reflects the sequence divergence within the Chadwick candidate interval for inbred mouse strains with known <i>Xce</i> alleles. Inbred strains with a number one superscript have both MDA and Sanger sequencing information available, while mouse strains with a number two superscript have only MDA genotype data available. Inbred strains with no number are assumed to have identical genotypes to a closely related strain that has been genotyped. Blue and green shading denotes the subspecific origin of the Chadwick interval for each strain (<i>M. m. domesticus</i> and <i>M. m. castaneus</i>, respectively). Panel B is a physical map that shows the locations of the previous <i>Xce</i> candidate intervals <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003853#pgen.1003853-Chadwick1\" target=\"_blank\">[26]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003853#pgen.1003853-Cattanach8\" target=\"_blank\">[57]</a>. Below the historical candidate intervals are the results of the SDP analyses using inbred strains selected from Panel A (See Methods). Tick marks represent SDPs classified as consistent (black), inconsistent (red), and partially consistent (gray). SNPs that retain consistent SDPs after inclusion of ALS/LtJ, LEWES/EiJ, PERA/EiJ, SJL/J, TIRANO/EiJ, WSB/EiJ, and ZALENDE/EiJ in the analysis are shown as blue tick marks above consistent SDPs. Our new maximum candidate interval is shown in gray below the tick marks. The minimum candidate interval is shown in black, while regions excluded are shown in red.</p>", "links"=>[], "tags"=>[], "article_id"=>813796, "categories"=>["Biological Sciences"], "users"=>["John D. Calaway", "Alan B. Lenarcic", "John P. Didion", "Jeremy R. Wang", "Jeremy B. Searle", "Leonard McMillan", "William Valdar", "Fernando Pardo-Manuel de Villena"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003853.g002", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Xce_candidate_interval_based_on_historical_data_/813796", "title"=>"The <i>Xce</i> candidate interval based on historical data.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-10-03 02:11:55"}

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Relative Metric

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