Complex Control of GABA(A) Receptor Subunit mRNA Expression: Variation, Covariation, and Genetic Regulation
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{"title"=>"Complex control of GABA(a) receptor subunit mRNA expression: Variation, covariation, and genetic regulation", "type"=>"journal", "authors"=>[{"first_name"=>"Megan K.", "last_name"=>"Mulligan", "scopus_author_id"=>"7102563323"}, {"first_name"=>"Xusheng", "last_name"=>"Wang", "scopus_author_id"=>"55736881700"}, {"first_name"=>"Adrienne L.", "last_name"=>"Adler", "scopus_author_id"=>"55180246200"}, {"first_name"=>"Khyobeni", "last_name"=>"Mozhui", "scopus_author_id"=>"15728161800"}, {"first_name"=>"Lu", "last_name"=>"Lu", "scopus_author_id"=>"56457005100"}, {"first_name"=>"Robert W.", "last_name"=>"Williams", "scopus_author_id"=>"55674268100"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"22506031", "sgr"=>"84859612421", "doi"=>"10.1371/journal.pone.0034586", "scopus"=>"2-s2.0-84859612421", "pui"=>"364605599", "isbn"=>"1932-6203", "issn"=>"19326203"}, "id"=>"df603391-fad2-3aa3-a22f-d5e5b0c78270", "abstract"=>"GABA type-A receptors are essential for fast inhibitory neurotransmission and are critical in brain function. Surprisingly, expression of receptor subunits is highly variable among individuals, but the cause and impact of this fluctuation remains unknown. We have studied sources of variation for all 19 receptor subunits using massive expression data sets collected across multiple brain regions and platforms in mice and humans. Expression of Gabra1, Gabra2, Gabrb2, Gabrb3, and Gabrg2 is highly variable and heritable among the large cohort of BXD strains derived from crosses of fully sequenced parents--C57BL/6J and DBA/2J. Genetic control of these subunits is complex and highly dependent on tissue and mRNA region. Remarkably, this high variation is generally not linked to phenotypic differences. The single exception is Gabrb3, a locus that is linked to anxiety. We identified upstream genetic loci that influence subunit expression, including three unlinked regions of chromosome 5 that modulate the expression of nine subunits in hippocampus, and that are also associated with multiple phenotypes. Candidate genes within these loci include, Naaa, Nos1, and Zkscan1. We confirmed a high level of coexpression for subunits comprising the major channel--Gabra1, Gabrb2, and Gabrg2--and identified conserved members of this expression network in mice and humans. Gucy1a3, Gucy1b3, and Lis1 are novel and conserved associates of multiple subunits that are involved in inhibitory signaling. Finally, proximal and distal regions of the 3' UTRs of single subunits have remarkably independent expression patterns in both species. However, corresponding regions of different subunits often show congruent genetic control and coexpression (proximal-to-proximal or distal-to-distal), even in the absence of sequence homology. Our findings identify novel sources of variation that modulate subunit expression and highlight the extraordinary capacity of biological networks to buffer 4-100 fold differences in mRNA levels.", "link"=>"http://www.mendeley.com/research/complex-control-gabaa-receptor-subunit-mrna-expression-variation-covariation-genetic-regulation-1", "reader_count"=>34, "reader_count_by_academic_status"=>{"Researcher"=>9, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>3, "Student > Master"=>5, "Other"=>1, "Lecturer"=>1, "Professor"=>2, "Unspecified"=>1, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Researcher"=>9, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>3, "Student > Master"=>5, "Other"=>1, "Lecturer"=>1, "Professor"=>2, "Unspecified"=>1, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>20, "Medicine and Dentistry"=>1, "Neuroscience"=>3, "Psychology"=>2, "Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Neuroscience"=>{"Neuroscience"=>3}, "Psychology"=>{"Psychology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>20}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>3}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Colombia"=>1, "United Kingdom"=>2, "Germany"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/656068"], "description"=>"<p>Genetic regulation of exon, intron, and 3′ UTR features for each of the five subunits regulated by strong <i>cis</i> eQTLs was measured in the hippocampus using the Affymetrix exon platform (database accession number GN206). Each probe set was required to have a mean expression of at least 10 and all probe sets overlapping SNPs were excluded. Blue and red indicate an association between the B6 and D2 allele at each locus and higher probe set expression, respectively. The more intense hue indicates a greater association and a corresponding increase in significance. Only <i>Gabra2</i> shows strong consistency of genetic regulation across mRNA regions.</p>", "links"=>[], "tags"=>["subunits", "transcript"], "article_id"=>326558, "categories"=>["Neuroscience", "Genetics"], "users"=>["Megan K. Mulligan", "Xusheng Wang", "Adrienne L. Adler", "Khyobeni Mozhui", "Lu Lu", "Robert W. Williams"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0034586.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_genetic_regulation_of_GABA_A_R_subunits_across_transcript_features_/326558", "title"=>"Summary of genetic regulation of GABA(A) R subunits across transcript features.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-10 01:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/656188"], "description"=>"<p>Bold lines indicate a correlation between 1 and 0.7 while normal and dashed lines indicate a correlation between 0.7 and 0.5 and 0.5 and 0.3, respectively. Warm colors represent positive correlations while cool colors represent negative correlations. Probes containing SNPs were removed and a principal component analysis (PCA) was used on the remaining probes to capture the component explaining the majority of the expression variation (PC1) in probe expression among BXD strains. PCA was used to extract PC1 for a single subunit when more than two probe sets were strongly correlated (<i>r</i>>0.8) and the average (AVG) was used when two probe sets were strongly correlated. prox = proximal, mid = middle. The highest positive correlations are between subunits targeting the same mRNA region. This is especially true for members of the most common heterotrimeric receptor—<i>Gabra1</i>, <i>Gabrb2</i>, and <i>Gabrg2</i>.</p>", "links"=>[], "tags"=>["receptor", "subunits"], "article_id"=>326683, "categories"=>["Neuroscience", "Genetics"], "users"=>["Megan K. Mulligan", "Xusheng Wang", "Adrienne L. Adler", "Khyobeni Mozhui", "Lu Lu", "Robert W. Williams"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0034586.g004", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Coexpression_of_GABA_A_Receptor_subunits_in_the_hippocampus_/326683", "title"=>"Coexpression of GABA(A) Receptor subunits in the hippocampus.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-10 01:51:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/656444"], "description"=>"<p>HIP = Hippocampus, AVG = Average log2 standardized expression with a mean of 8 and standard deviation of 2, Exon = Exon array platform, M430 = M430 array platform, FC = Fold Change in expression between the highest and lowest strain, () = Measurement includes probes overlapping SNPs as all probe sets are affected, RNAseq = SOLiD platform RNA sequencing, EXPR = Expression. 0 = No expression, 3 = Moderate expression, 5 = High expression in the hippocampal formation. Gene ID = NCBI RefSeq ID, FPKM = read fragments per KB gene model per million sample read fragments.</p>", "links"=>[], "tags"=>["genetics and genomics", "neuroscience"], "article_id"=>326933, "categories"=>["Neuroscience", "Genetics"], "users"=>["Megan K. Mulligan", "Xusheng Wang", "Adrienne L. Adler", "Khyobeni Mozhui", "Lu Lu", "Robert W. Williams"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0034586.t001", "stats"=>{"downloads"=>3, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_GABA_A_R_expression_summary_/326933", "title"=>"GABA(A)R expression summary.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-04-10 01:55:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/655811"], "description"=>"<p>Probe sets represent columns and ascending genomic location for each chromosome represent rows. Only chromosomes with a significant QTL (LRS>15) are shown. Several GABA(A)R subunits are regulated by both <i>cis</i> and <i>trans</i> eQTL (<i>Gabra1</i>, <i>Gabra2</i>, <i>Gabrb2</i>, and <i>Gabrb3</i>) whereas some are modified exclusively in <i>trans</i> (<i>Gabra5</i>, <i>Gabrg1</i>). Hue intensity provides an indication of the strength of the association between gene expression and genomic location. Red and blue alleles indicate that the <i>D</i> or <i>B</i> allele increases trait values, respectively. Arrowheads show the location of each cognate gene. PC1 = first principal component, Chr = Chromosome, Mb = Megabase, Prox = proximal, mid = middle, dist = distal.</p>", "links"=>[], "tags"=>["genetics and genomics", "neuroscience"], "article_id"=>326299, "categories"=>["Neuroscience", "Genetics"], "users"=>["Megan K. Mulligan", "Xusheng Wang", "Adrienne L. Adler", "Khyobeni Mozhui", "Lu Lu", "Robert W. Williams"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0034586.g001", "stats"=>{"downloads"=>4, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_significant_genetic_regulation_in_the_hippocampus_/326299", "title"=>"Summary of significant genetic regulation in the hippocampus.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-10 01:44:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/656301"], "description"=>"<p>(A) <i>Gabra1</i>, <i>Gabrb2</i>, and <i>Gabrg3</i> are generally well coexpressed across species and platforms. The set of highly conserved correlates include many synaptic genes such as <i>Syt1</i> and <i>Sh3gl2</i>. Bold lines indicate a correlation between 1 and 0.7 while normal and dashed lines indicate a correlation between 0.7 and 0.5 and 0.5 and 0.3, respectively. Warm colors represent positive correlations while cool colors represent negative correlations. (B) Expression of conserved module members is regulated by <i>Trans5a</i>. LRS score and additive effect are shown on the Y axis in blue and green, respectively. The blue line plots the strength of the association between gene expression and chromosomal location. The genome wide significant and suggestive threshold is shown by the red and grey horizontal line, respectively. Red and green lines show the effect of the D or B allele on trait values, respectively. The upper X-axis shows location by chromosome and the lower X-axis shows location in megabases.</p>", "links"=>[], "tags"=>["members"], "article_id"=>326799, "categories"=>["Neuroscience", "Genetics"], "users"=>["Megan K. Mulligan", "Xusheng Wang", "Adrienne L. Adler", "Khyobeni Mozhui", "Lu Lu", "Robert W. Williams"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0034586.g005", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Conserved_members_of_the_GABA_A_R_gene_network_/326799", "title"=>"Conserved members of the GABA(A)R gene network.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-10 01:53:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/337016", "https://ndownloader.figshare.com/files/337050", "https://ndownloader.figshare.com/files/337091", "https://ndownloader.figshare.com/files/337115", "https://ndownloader.figshare.com/files/337170", "https://ndownloader.figshare.com/files/337210", "https://ndownloader.figshare.com/files/337259", "https://ndownloader.figshare.com/files/337315", "https://ndownloader.figshare.com/files/337337", "https://ndownloader.figshare.com/files/337354", "https://ndownloader.figshare.com/files/337376", "https://ndownloader.figshare.com/files/337395", "https://ndownloader.figshare.com/files/337421", "https://ndownloader.figshare.com/files/337447", "https://ndownloader.figshare.com/files/337464", "https://ndownloader.figshare.com/files/337488"], "description"=>"<div><p>GABA type-A receptors are essential for fast inhibitory neurotransmission and are critical in brain function. Surprisingly, expression of receptor subunits is highly variable among individuals, but the cause and impact of this fluctuation remains unknown. We have studied sources of variation for all 19 receptor subunits using massive expression data sets collected across multiple brain regions and platforms in mice and humans. Expression of <em>Gabra1</em>, <em>Gabra2</em>, <em>Gabrb2</em>, <em>Gabrb3</em>, and <em>Gabrg2</em> is highly variable and heritable among the large cohort of BXD strains derived from crosses of fully sequenced parents—C57BL/6J and DBA/2J. Genetic control of these subunits is complex and highly dependent on tissue and mRNA region. Remarkably, this high variation is generally not linked to phenotypic differences. The single exception is <em>Gabrb3</em>, a locus that is linked to anxiety. We identified upstream genetic loci that influence subunit expression, including three unlinked regions of chromosome 5 that modulate the expression of nine subunits in hippocampus, and that are also associated with multiple phenotypes. Candidate genes within these loci include, <em>Naaa</em>, <em>Nos1</em>, and <em>Zkscan1</em>. We confirmed a high level of coexpression for subunits comprising the major channel—<em>Gabra1</em>, <em>Gabrb2</em>, and <em>Gabrg2</em>—and identified conserved members of this expression network in mice and humans. <em>Gucy1a3</em>, <em>Gucy1b3</em>, and <em>Lis1</em> are novel and conserved associates of multiple subunits that are involved in inhibitory signaling. Finally, proximal and distal regions of the 3′ UTRs of single subunits have remarkably independent expression patterns in both species. However, corresponding regions of different subunits often show congruent genetic control and coexpression (proximal-to-proximal or distal-to-distal), even in the absence of sequence homology. Our findings identify novel sources of variation that modulate subunit expression and highlight the extraordinary capacity of biological networks to buffer 4–100 fold differences in mRNA levels.</p> </div>", "links"=>[], "tags"=>["receptor", "subunit", "mrna"], "article_id"=>126603, "categories"=>["Neuroscience", "Genetics"], "users"=>["Megan K. Mulligan", "Xusheng Wang", "Adrienne L. Adler", "Khyobeni Mozhui", "Lu Lu", "Robert W. Williams"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0034586.s001", "https://dx.doi.org/10.1371/journal.pone.0034586.s002", "https://dx.doi.org/10.1371/journal.pone.0034586.s003", "https://dx.doi.org/10.1371/journal.pone.0034586.s004", "https://dx.doi.org/10.1371/journal.pone.0034586.s005", "https://dx.doi.org/10.1371/journal.pone.0034586.s006", "https://dx.doi.org/10.1371/journal.pone.0034586.s007", "https://dx.doi.org/10.1371/journal.pone.0034586.s008", "https://dx.doi.org/10.1371/journal.pone.0034586.s009", "https://dx.doi.org/10.1371/journal.pone.0034586.s010", "https://dx.doi.org/10.1371/journal.pone.0034586.s011", "https://dx.doi.org/10.1371/journal.pone.0034586.s012", "https://dx.doi.org/10.1371/journal.pone.0034586.s013", "https://dx.doi.org/10.1371/journal.pone.0034586.s014", "https://dx.doi.org/10.1371/journal.pone.0034586.s015", "https://dx.doi.org/10.1371/journal.pone.0034586.s016"], "stats"=>{"downloads"=>20, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Complex_Control_of_GABA_A_Receptor_Subunit_mRNA_Expression_Variation_Covariation_and_Genetic_Regulation/126603", "title"=>"Complex Control of GABA(A) Receptor Subunit mRNA Expression: Variation, Covariation, and Genetic Regulation", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-04-10 01:50:03"}
  • {"files"=>["https://ndownloader.figshare.com/files/656478"], "description"=>"<p>Chr = Chromosome, Mb = Megabase, N/S = Not significant or suggestive. Shading = Possible SNP artifact as the probe overlaps a SNP between parental strains (rs28224563),</p>*<p> = Probes overlapping SNPs removed and mapping performed with the first principal component of the remaining probes,</p>**<p> = SNP between parental strains (rs28218735) overlapping probe but the allele effect (<i>Cast</i> high) indicates no effect on probe binding. NOTE: ILM4150164 is overlapping rs37397520 which is a SNP between B6 and PWK/PhJ but is probably not segregating in the LXS strains which are derived from A, AKR, BALB/c, C3H/2, C57BL, DBA/2, IS/Bi, and RIII. However the genotype of IS/Bi and RIII is unknown and IS/Bi is now extinct. For <i>Gabra1</i>, a probe from probe set rs28224563 overlaps a SNP between parental strains.</p>", "links"=>[], "tags"=>["subunit", "modulation"], "article_id"=>326972, "categories"=>["Neuroscience", "Genetics"], "users"=>["Megan K. Mulligan", "Xusheng Wang", "Adrienne L. Adler", "Khyobeni Mozhui", "Lu Lu", "Robert W. Williams"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0034586.t002", "stats"=>{"downloads"=>4, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_GABA_A_R_subunit_cis_modulation_among_several_genetic_crosses_/326972", "title"=>"Summary of GABA(A)R subunit <i>cis</i> modulation among several genetic crosses.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-04-10 01:56:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/655905"], "description"=>"<p>Genetic regulation of the 5 subunits regulated by strong <i>cis</i> eQTLs in the hippocampus was compared across three different platforms Affymetrix M430 (WB = whole brain, CB = cerebellum), Affymetrix MoGene 1.0 ST (AMY = amgydala and HYP = hypothalamus), and Illumina (CTX = neocortex, STR = striatum). Each probe set was required to have a mean expression of at least 8 in each tissue database. Blue and red indicate an association between the B6 and D2 allele at each locus and higher probe set expression, respectively. The more intense hue indicates a greater association and a corresponding increase in significance. For all data except the HYP and AMY, probes overlapping SNPs were filtered out and a principal component analysis was performed on remaining probes to capture a component (PC1) explaining the majority of the variation in probe set expression. Percent of variance explained by each PC1 ranged from (∼45% to 95%). Because of the large number of probes included for measurement in the HYP and AMY, a probe level analysis was not possible. Some probe sets (indicated by *) contained 1 to 3 probes overlapping a variant. It is hard to predict the overall effect of these variants but, in general, those probe sets with SNPs that have higher expression associated with the B6 allele (blue) have a higher chance of being false due to SNP artifacts. <i>Cis</i> modulation of expression across tissues is most consistent for <i>Gabra2</i> and <i>Gabra1</i>.</p>", "links"=>[], "tags"=>["modulation"], "article_id"=>326399, "categories"=>["Neuroscience", "Genetics"], "users"=>["Megan K. Mulligan", "Xusheng Wang", "Adrienne L. Adler", "Khyobeni Mozhui", "Lu Lu", "Robert W. Williams"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0034586.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Consistency_of_cis_modulation_across_tissues_/326399", "title"=>"Consistency of <i>cis</i> modulation across tissues.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-04-10 01:46:39"}

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