RHOA Is a Modulator of the Cholesterol-Lowering Effects of Statin
Publication Date
November 15, 2012
Journal
PLOS Genetics
Authors
Marisa W. Medina, Elizabeth Theusch, Devesh Naidoo, Frederick Bauzon, et al
Volume
8
Issue
11
Pages
e1003058
DOI
http://doi.org/10.1371/journal.pgen.1003058
Publisher URL
http://journals.plos.org/plosgenetics/article?id=10.1371%2Fjournal.pgen.1003058
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/23166513
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3499361
Europe PMC
http://europepmc.org/abstract/MED/23166513
Web of Science
000311891600044
Scopus
84870674799
Mendeley
http://www.mendeley.com/research/rhoa-modulator-cholesterollowering-effects-statin
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Mendeley | Further Information

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CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/290656", "https://ndownloader.figshare.com/files/290730", "https://ndownloader.figshare.com/files/290827", "https://ndownloader.figshare.com/files/290951", "https://ndownloader.figshare.com/files/291000", "https://ndownloader.figshare.com/files/291110", "https://ndownloader.figshare.com/files/291173"], "description"=>"<div><p>Although statin drugs are generally efficacious for lowering plasma LDL-cholesterol levels, there is considerable variability in response. To identify candidate genes that may contribute to this variation, we used an unbiased genome-wide filter approach that was applied to 10,149 genes expressed in immortalized lymphoblastoid cell lines (LCLs) derived from 480 participants of the Cholesterol and Pharmacogenomics (CAP) clinical trial of simvastatin. The criteria for identification of candidates included genes whose statin-induced changes in expression were correlated with change in expression of <em>HMGCR</em>, a key regulator of cellular cholesterol metabolism and the target of statin inhibition. This analysis yielded 45 genes, from which <em>RHOA</em> was selected for follow-up because it has been found to participate in mediating the pleiotropic but not the lipid-lowering effects of statin treatment. <em>RHOA</em> knock-down in hepatoma cell lines reduced <em>HMGCR, LDLR</em>, and <em>SREBF2</em> mRNA expression and increased intracellular cholesterol ester content as well as apolipoprotein B (APOB) concentrations in the conditioned media. Furthermore, inter-individual variation in statin-induced <em>RHOA</em> mRNA expression measured <em>in vitro</em> in CAP LCLs was correlated with the changes in plasma total cholesterol, LDL-cholesterol, and APOB induced by simvastatin treatment (40 mg/d for 6 wk) of the individuals from whom these cell lines were derived. Moreover, the minor allele of rs11716445, a SNP located in a novel cryptic <em>RHOA</em> exon, dramatically increased inclusion of the exon in <em>RHOA</em> transcripts during splicing and was associated with a smaller LDL-cholesterol reduction in response to statin treatment in 1,886 participants from the CAP and Pravastatin Inflamation and CRP Evaluation (PRINCE; pravastatin 40 mg/d) statin clinical trials. Thus, an unbiased filter approach based on transcriptome-wide profiling identified <em>RHOA</em> as a gene contributing to variation in LDL-cholesterol response to statin, illustrating the power of this approach for identifying candidate genes involved in drug response phenotypes.</p> </div>", "links"=>[], "tags"=>["rhoa", "modulator", "cholesterol-lowering", "effects", "statin"], "article_id"=>117229, "categories"=>["Molecular Biology", "Genetics"], "users"=>["Marisa W. Medina", "Elizabeth Theusch", "Devesh Naidoo", "Frederick Bauzon", "Kristen Stevens", "Lara M. Mangravite", "Yu-Lin Kuang", "Ronald M. Krauss"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003058.s001", "https://dx.doi.org/10.1371/journal.pgen.1003058.s002", "https://dx.doi.org/10.1371/journal.pgen.1003058.s003", "https://dx.doi.org/10.1371/journal.pgen.1003058.s004", "https://dx.doi.org/10.1371/journal.pgen.1003058.s005", "https://dx.doi.org/10.1371/journal.pgen.1003058.s006", "https://dx.doi.org/10.1371/journal.pgen.1003058.s007"], "stats"=>{"downloads"=>11, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/RHOA_Is_a_Modulator_of_the_Cholesterol_Lowering_Effects_of_Statin__/117229", "title"=>"RHOA Is a Modulator of the Cholesterol-Lowering Effects of Statin", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-11-15 02:00:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/541721"], "description"=>"<p>Linear regression of statin-induced changes (delta log) in LDL-cholesterol with adjustment age, sex, BMI, smoking status, and clinical trial was used to test for association with <i>RHOA</i> haplotypes. Graph depicts mean percent change in LDL-cholesterol +/− SE.</p>", "links"=>[], "tags"=>["haplotypes", "h3b", "h2", "statin-induced", "changes", "ldl-cholesterol", "prince"], "article_id"=>212201, "categories"=>["Molecular Biology", "Genetics"], "users"=>["Marisa W. Medina", "Elizabeth Theusch", "Devesh Naidoo", "Frederick Bauzon", "Kristen Stevens", "Lara M. Mangravite", "Yu-Lin Kuang", "Ronald M. Krauss"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003058.g003", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Relationship_between_RHOA_haplotypes_H3B_and_H2_and_statin_induced_changes_in_LDL_cholesterol_response_in_the_CAP_N_580_and_PRINCE_N_1306_clinical_trials_/212201", "title"=>"Relationship between <i>RHOA</i> haplotypes H3B and H2 and statin-induced changes in LDL-cholesterol response in the CAP (N = 580) and PRINCE (N = 1306) clinical trials.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-15 00:36:41"}
  • {"files"=>["https://ndownloader.figshare.com/files/541989"], "description"=>"<p><i>RHOA</i> haplotypes were defined using common HapMap3 SNPs within 10 kb of the gene, with minor alleles in bold italics and the minor allele of rs11716445, the only <i>RHOA</i> SNP that differs between H3A and H3B, in underlined bold italic. Distributions of the haplotypes in the CAP and PRINCE clinical trial populations are also shown.</p>", "links"=>[], "tags"=>["haplotype"], "article_id"=>212486, "categories"=>["Molecular Biology", "Genetics"], "users"=>["Marisa W. Medina", "Elizabeth Theusch", "Devesh Naidoo", "Frederick Bauzon", "Kristen Stevens", "Lara M. Mangravite", "Yu-Lin Kuang", "Ronald M. Krauss"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003058.t003", "stats"=>{"downloads"=>3, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_RHOA_haplotype_definition_/212486", "title"=>"<i>RHOA</i> haplotype definition.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-11-15 00:41:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/541496"], "description"=>"<p>(A) <i>HMGCR</i> and <i>RHOA</i> levels were quantified in 480 CAP LCLs after 24 hour incubation with 2 µM activated simvastatin or sham buffer. HepG2 (n = 12) and Huh7 cells (n = 6) cells were reverse transfected with Silencer Select siRNAs specific for <i>RHOA</i> or a negative control using the NeoSport transfection reagent. (B) After 48 hours, <i>RHOA</i> transcript levels were quantified by real time qPCR and compared to cells treated with the negative control to calculate percent knock-down of the <i>RHOA</i> transcript. (C) HepG2 cells (n = 2) were transfected and the cell lysate probed by immunoblot with antibodies to RHOA and β-actin. (D) <i>HMGCR</i>, <i>SREBF2</i>, and <i>LDLR</i> transcript levels were quantified by qPCR. APOB and APOAI accumulated in the cell culture media were quantified by ELISA. (E) Total and free intracellular cholesterol levels were quantified using the Amplex Red Cholesterol Assay Kit (Invitrogen), with cholesterol ester calculated as the difference of total minus free cholesterol. (F) HepG2 cells (n = 10) were incubated for 24 hours with 2 µM simvastatin +10% LPDS or sham buffer +10% FBS (control conditions), after which cells were harvested and <i>RHOA</i> and <i>HMGCR</i> mRNA were quantified by qPCR, and RHOA and HMGCR protein were quantified by immunoblot. Band densities were quantified using Alphaview SA version 3.4.0. The dashed line indicates a fold change of 1. (G) One representative immunoblot of HepG2 cells incubated as described in section D. (H) HepG2 and Huh7 cells (n = 6 each cell type) were transfected with the Silencer Select siRNA specific for <i>SREBF1, SREBF2</i> or a non-targeting negative control. <i>RHOA, HMGCR</i> and <i>CLPTM1</i> transcript levels were quantified after 48 hours. Statistically significant differences in gene expression, APOB, APOAI and intracellular cholesterol were evaluated by paired two-tailed t-test. All values shown are mean ± standard error. *p<0.05; **p<0.01, ***p<0.001.</p>", "links"=>[], "tags"=>["validation"], "article_id"=>211985, "categories"=>["Molecular Biology", "Genetics"], "users"=>["Marisa W. Medina", "Elizabeth Theusch", "Devesh Naidoo", "Frederick Bauzon", "Kristen Stevens", "Lara M. Mangravite", "Yu-Lin Kuang", "Ronald M. Krauss"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003058.g001", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Functional_validation_of_RHOA_/211985", "title"=>"Functional validation of RHOA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-15 00:33:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/541605"], "description"=>"<p>480 CAP LCLs from Caucasian donors were incubated with 2 µM activated simvastatin or sham buffer for 24 hours, after which genome-wide gene expression was quantified using the Illumina human HT8v3 beadarray, and cell surface LDLR protein was measured by FACS. Greater induction of <i>RHOA</i> transcript levels was positively correlated with greater induction of both <i>LDLR</i> and <i>HMGCR</i> (shown in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003058#pgen-1003058-g001\" target=\"_blank\">Figure 1</a>) mRNA (A) and inversely correlated with induction of cell surface LDLR protein (B). Gene expression values and measures of LDLR protein were adjusted for cellular covariates as described in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003058#pgen-1003058-g001\" target=\"_blank\">Figure 1</a>, log transformed, the delta calculated as the statin-treated minus the sham-treated value, and quantile normalized.</p>", "links"=>[], "tags"=>["mrna", "levels", "cellular"], "article_id"=>212098, "categories"=>["Molecular Biology", "Genetics"], "users"=>["Marisa W. Medina", "Elizabeth Theusch", "Devesh Naidoo", "Frederick Bauzon", "Kristen Stevens", "Lara M. Mangravite", "Yu-Lin Kuang", "Ronald M. Krauss"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003058.g002", "stats"=>{"downloads"=>3, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Association_of_variation_in_RHOA_mRNA_expression_levels_with_other_cellular_phenotypes_/212098", "title"=>"Association of variation in <i>RHOA</i> mRNA expression levels with other cellular phenotypes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-15 00:34:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/542045"], "description"=>"<p>HepG2 (n = 4), Hep3B (n = 3) and 480 LCLs derived from participants of the Cholesterol and Pharmacogenetics (CAP) clinical trial were exposed to either 2 µM activated simvastatin or sham buffer for 24 hours, and gene expression was quantified on the Illumina HTref8v3 bead chip. Genes expressed in both LCLs and normal human liver (n = 60, GEO dataset GSE28893) were identified and tested for evidence of statin-induced changes in gene expression.</p>", "links"=>[], "tags"=>["genes"], "article_id"=>212545, "categories"=>["Molecular Biology", "Genetics"], "users"=>["Marisa W. Medina", "Elizabeth Theusch", "Devesh Naidoo", "Frederick Bauzon", "Kristen Stevens", "Lara M. Mangravite", "Yu-Lin Kuang", "Ronald M. Krauss"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003058.t001", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_of_candidate_genes_associated_with_statin_/212545", "title"=>"Identification of candidate genes associated with statin.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-11-15 00:42:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/542018"], "description"=>"<p>Expression characteristics of identified candidate genes.</p>", "links"=>[], "tags"=>["characteristics"], "article_id"=>212509, "categories"=>["Molecular Biology", "Genetics"], "users"=>["Marisa W. Medina", "Elizabeth Theusch", "Devesh Naidoo", "Frederick Bauzon", "Kristen Stevens", "Lara M. Mangravite", "Yu-Lin Kuang", "Ronald M. Krauss"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003058.t002", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_characteristics_of_identified_candidate_genes_/212509", "title"=>"Expression characteristics of identified candidate genes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-11-15 00:41:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/541830"], "description"=>"<p>(A) <i>RHOA</i> gene structure and location and sequence of exon 2.5. The 5′ and 3′ UTRs are indicated in solid grey, canonical exons are outlined in grey, and the novel exon is shown in red. The location of the three common <i>RHOA</i> exonic SNPs are shown. RNA-Seq libraries were prepared from HepG2, Hep3B, Huh7, and CAP LCLs (n = 3) and sequenced using 100 bp paired-end reads, and the novel exon was discovered by inspecting novel junction spanning reads. (B) Total <i>RHOA</i> expression levels and <i>RHOA</i> exon 2.5 levels were measured using qPCR, the percent containing exon 2.5 were calculated by dividing <i>RHOA</i> exon 2.5 levels by total <i>RHOA</i> levels, adjusted for batch effects using regression, and normal quantile transformed prior to association testing using linear regression. Graphs depict mean +/− SE. (C) CAP LCL cDNAs containing <i>RHOA</i> exon 2.5 were PCR-amplified and Sanger sequenced and the relative amounts of each allele of rs11716445 in exon 2.5 were estimated by measuring the height of the sequencing traces. (D) Representative sequencing traces of the LCL cDNA and genomic DNA of three heterozygous individuals from CAP illustrate that H3B is a cis-acting splicing QTL exhibiting allele-specific expression in <i>RHOA</i> exon 2.5 (rs11716445 and rs2878298) but not exon 5 (rs3448). H3B contains the minor allele [T] of rs11716445, H1 contains the minor allele [G] of rs2878298, and H2 contains the minor allele [A] of rs3448.</p>", "links"=>[], "tags"=>["haplotypes", "exon"], "article_id"=>212321, "categories"=>["Molecular Biology", "Genetics"], "users"=>["Marisa W. Medina", "Elizabeth Theusch", "Devesh Naidoo", "Frederick Bauzon", "Kristen Stevens", "Lara M. Mangravite", "Yu-Lin Kuang", "Ronald M. Krauss"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003058.g004", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Association_between_RHOA_haplotypes_and_expression_of_RHOA_exon_2_5_/212321", "title"=>"Association between <i>RHOA</i> haplotypes and expression of <i>RHOA</i> exon 2.5.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-11-15 00:38:41"}

PMC Usage Stats | Further Information

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Relative Metric

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