Mouse Transgenesis Identifies Conserved Functional Enhancers and cis-Regulatory Motif in the Vertebrate LIM Homeobox Gene Lhx2 Locus
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{"title"=>"Mouse transgenesis identifies conserved functional enhancers and cis-regulatory motif in the vertebrate LIM homeobox gene Lhx2 locus", "type"=>"journal", "authors"=>[{"first_name"=>"Alison P.", "last_name"=>"Lee", "scopus_author_id"=>"35237615600"}, {"first_name"=>"Sydney", "last_name"=>"Brenner", "scopus_author_id"=>"24771944600"}, {"first_name"=>"Byrappa", "last_name"=>"Venkatesh", "scopus_author_id"=>"7006518094"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "sgr"=>"79957501458", "doi"=>"10.1371/journal.pone.0020088", "scopus"=>"2-s2.0-79957501458", "pui"=>"361811656", "pmid"=>"21629789"}, "id"=>"5cd7255d-57bf-34f9-96f2-609df76aca6f", "abstract"=>"The vertebrate Lhx2 is a member of the LIM homeobox family of transcription factors. It is essential for the normal development of the forebrain, eye, olfactory system and liver as well for the differentiation of lymphoid cells. However, despite the highly restricted spatio-temporal expression pattern of Lhx2, nothing is known about its transcriptional regulation. In mammals and chicken, Crb2, Dennd1a and Lhx2 constitute a conserved linkage block, while the intervening Dennd1a is lost in the fugu Lhx2 locus. To identify functional enhancers of Lhx2, we predicted conserved noncoding elements (CNEs) in the human, mouse and fugu Crb2-Lhx2 loci and assayed their function in transgenic mouse at E11.5. Four of the eight CNE constructs tested functioned as tissue-specific enhancers in specific regions of the central nervous system and the dorsal root ganglia (DRG), recapitulating partial and overlapping expression patterns of Lhx2 and Crb2 genes. There was considerable overlap in the expression domains of the CNEs, which suggests that the CNEs are either redundant enhancers or regulating different genes in the locus. Using a large set of CNEs (810 CNEs) associated with transcription factor-encoding genes that express predominantly in the central nervous system, we predicted four over-represented 8-mer motifs that are likely to be associated with expression in the central nervous system. Mutation of one of them in a CNE that drove reporter expression in the neural tube and DRG abolished expression in both domains indicating that this motif is essential for expression in these domains. The failure of the four functional enhancers to recapitulate the complete expression pattern of Lhx2 at E11.5 indicates that there must be other Lhx2 enhancers that are either located outside the region investigated or divergent in mammals and fishes. Other approaches such as sequence comparison between multiple mammals are required to identify and characterize such enhancers.", "link"=>"http://www.mendeley.com/research/mouse-transgenesis-identifies-conserved-functional-enhancers-cisregulatory-motif-vertebrate-lim-home", "reader_count"=>15, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>7, "Student > Ph. D. Student"=>2, "Student > Master"=>2, "Student > Bachelor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>7, "Student > Ph. D. Student"=>2, "Student > Master"=>2, "Student > Bachelor"=>2}, "reader_count_by_subject_area"=>{"Agricultural and Biological Sciences"=>13, "Medicine and Dentistry"=>1, "Biochemistry, Genetics and Molecular Biology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>13}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}}, "reader_count_by_country"=>{"United States"=>1, "United Kingdom"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/772760"], "description"=>"<p>Lateral and dorsal views of a representative transgenic embryo for each\n construct. (A) CNE2/3; Strong <i>lacZ</i> expression was\n observed in the neural tube and dorsal root ganglia. (B) CNE5/6; (C)\n CNE7; <i>lacZ</i> expression was observed in the hindbrain and\n the neural tube for CNE5/6 and CNE7. (D) CNE10. <i>lacZ</i>\n expression extending from the most rostral region of the midbrain to the\n hindbrain and the entire length of the neural tube. Additional ectopic\n <i>lacZ</i> expression was detected in the diencephalon\n for this embryo. Scale bar denotes 1 mm in length. M: midbrain; H:\n hindbrain; NT: neural tube; DRG: dorsal root ganglion.</p>", "links"=>[], "tags"=>["cnes", "various", "tissues"], "article_id"=>443130, "categories"=>["Molecular Biology", "Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Alison P. Lee", "Sydney Brenner", "Byrappa Venkatesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020088.g006", "stats"=>{"downloads"=>4, "page_views"=>24, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lhx2_associated_CNEs_direct_expression_to_various____tissues_in_E11_5_mouse_embryos_/443130", "title"=>"<i>Lhx2-</i>associated CNEs direct expression to various\n tissues in E11.5 mouse embryos.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-23 00:52:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/773157"], "description"=>"<p>Summary of the expression patterns directed by CNE\n constructs.</p>", "links"=>[], "tags"=>["patterns", "directed", "cne"], "article_id"=>443528, "categories"=>["Molecular Biology", "Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Alison P. Lee", "Sydney Brenner", "Byrappa Venkatesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020088.t002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_the_expression_patterns_directed_by_CNE____constructs_/443528", "title"=>"Summary of the expression patterns directed by CNE\n constructs.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-05-23 00:58:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/773218"], "description"=>"<p>TSS: transcription start site.</p>", "links"=>[], "tags"=>["cnes", "tested", "transgenic"], "article_id"=>443590, "categories"=>["Molecular Biology", "Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Alison P. Lee", "Sydney Brenner", "Byrappa Venkatesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020088.t001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Details_of_CNEs_tested_in_transgenic_mice_/443590", "title"=>"Details of CNEs tested in transgenic mice.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-05-23 00:59:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/772366"], "description"=>"<p>Expression patterns (ventral, lateral and dorsal views) as determined by\n whole-mount <i>in situ</i> hybridization at E11.5 for genes\n (A) <i>Lhx2</i>, (B) <i>Crb2</i>, and (C)\n <i>Dennd1a</i>. Three to four embryos were assayed for\n each gene and all embryos gave essentially the same results as these\n representative embryos. Scale bar at lower right corner denotes 1 mm in\n length. F: forebrain; M: midbrain; H: hindbrain; E: eye; NT: neural\n tube.</p>", "links"=>[], "tags"=>["genetics and genomics", "molecular biology", "Computational biology", "Evolutionary biology"], "article_id"=>442737, "categories"=>["Molecular Biology", "Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Alison P. Lee", "Sydney Brenner", "Byrappa Venkatesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020088.g002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_Lhx2_Crb2_____Dennd1a_in_E11_5_mouse_embryos_/442737", "title"=>"Expression of <i>Lhx2</i>, <i>Crb2</i>,\n <i>Dennd1a</i> in E11.5 mouse embryos.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-23 00:45:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/772230"], "description"=>"<p>Rectangles above the line indicate genes on the forward strand, while\n rectangles below the line indicate genes on the reverse strand. Genes in\n blue are syntenic in the 4 species. Not drawn to scale.</p>", "links"=>[], "tags"=>["loci", "and"], "article_id"=>442607, "categories"=>["Molecular Biology", "Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Alison P. Lee", "Sydney Brenner", "Byrappa Venkatesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020088.g001", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lhx2_gene_loci_in_human_mouse_chicken_and____fugu_/442607", "title"=>"<i>Lhx2</i> gene loci in human, mouse, chicken and\n fugu.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-23 00:43:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/772501"], "description"=>"<p><i>Lhx2</i> locus in human, mouse and fugu used for sequence\n alignment. In human and mouse, <i>Crb2</i> and\n <i>Dennd1a</i> overlap by ∼100 bp at their 3′\n ends.</p>", "links"=>[], "tags"=>["conserved", "synteny", "fugu", "for"], "article_id"=>442872, "categories"=>["Molecular Biology", "Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Alison P. Lee", "Sydney Brenner", "Byrappa Venkatesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020088.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Region_of_conserved_synteny_in_human_mouse_and_fugu_used_for____sequence_alignment_/442872", "title"=>"Region of conserved synteny in human, mouse and fugu used for\n sequence alignment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-23 00:47:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/773191"], "description"=>"<p>Human-fugu CNEs of cluster #3 human transcription factor-encoding\n genes were compared against CNEs of non-cluster #3 transcription\n factor-encoding genes. Number of instances of each motif was\n determined by searching each motif in the human-fugu CNEs permitting\n at most 2 mismatches. <i>P</i>-values were calculated\n based on a chi-squared test followed by Bonferroni correction for\n multiple testing. Underlined portion of TFBS sequence indicates\n similarity with motif. TF, transcription factor; TFBS, TF binding\n sites.</p>", "links"=>[], "tags"=>["8-mer", "motifs", "cnes"], "article_id"=>443566, "categories"=>["Molecular Biology", "Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Alison P. Lee", "Sydney Brenner", "Byrappa Venkatesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020088.t003", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Over_represented_8_mer_motifs_in_CNEs_of_cluster_3_genes_/443566", "title"=>"Over-represented 8-mer motifs in CNEs of cluster #3 genes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-05-23 00:59:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/772678"], "description"=>"<p>The exons of protein-coding genes are shown in light/dark blue or green\n rectangles. The CNEs are located within the introns of the upstream gene\n <i>DENND1A</i> are indicated by red rectangles that extend\n above the exons.</p>", "links"=>[], "tags"=>["cnes"], "article_id"=>443051, "categories"=>["Molecular Biology", "Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Alison P. Lee", "Sydney Brenner", "Byrappa Venkatesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020088.g005", "stats"=>{"downloads"=>1, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Location_of_CNEs_in_the_human_LHX2_locus_/443051", "title"=>"Location of CNEs in the human <i>LHX2</i> locus.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-23 00:50:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/772909"], "description"=>"<p>(A, B) Tissue expression patterns of 718 human TF-encoding genes. (A)\n Each of the six panels displays a heat map. The rows and columns of each\n heat map represent human TF-encoding genes and 62 human tissues\n respectively. (B) Each graph represents the average gene expression\n levels of a cluster of TF-encoding genes. Expression cluster #3 consists\n of genes that predominantly express in the central nervous system. (C)\n The table pertains to the CNE density (CNE bases per kb of noncoding\n sequence in a human gene locus), the number and total length of CNEs per\n TF-encoding gene in different expression clusters.</p>", "links"=>[], "tags"=>["genes", "predominantly", "nervous", "enriched"], "article_id"=>443274, "categories"=>["Molecular Biology", "Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Alison P. Lee", "Sydney Brenner", "Byrappa Venkatesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020088.g007", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TF_encoding_genes_predominantly_expressed_in_the_central_nervous____system_are_enriched_with_CNEs_/443274", "title"=>"TF-encoding genes predominantly expressed in the central nervous\n system are enriched with CNEs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-23 00:54:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/772577"], "description"=>"<p>Human, mouse and fugu <i>Lhx2</i> loci were aligned using\n MLAGAN and CNEs (≥65% identity over 50 bp) were predicted with\n VISTA. Fugu served as the base sequence. Pink peaks denote CNEs while\n blue peaks denote conserved coding sequences. The arrows above the blue\n boxes that denote exons indicate the direction of transcription.\n <i>x</i>-axis represents distance along the fugu sequence\n while <i>y</i>-axis shows the percentage identity in each\n pairwise alignment. The pink peaks that are not annotated do not meet\n the thresholds of ≥65% identity over 50 bp.</p>", "links"=>[], "tags"=>["genetics and genomics", "molecular biology", "Computational biology", "Evolutionary biology"], "article_id"=>442949, "categories"=>["Molecular Biology", "Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Alison P. Lee", "Sydney Brenner", "Byrappa Venkatesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020088.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_CNEs_in_the_Lhx2_locus_/442949", "title"=>"CNEs in the <i>Lhx2</i> locus.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-23 00:49:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/773043"], "description"=>"<p>(A) Wild-type and mutant sequences of overlapping motifs in\n <i>CNE2</i>. (B) <i>lacZ</i> expression although\n still detectable in neural tube and dorsal root ganglia, is greatly\n reduced especially in the anterior neural tube. (C, D) Faint\n <i>lacZ</i> expression in neural tube is present in two\n different embryos, and visible under higher magnification in (E, F).\n Yellow scale bar denotes 1 mm in length. Red scale bar denotes 0.2 mm in\n length.</p>", "links"=>[], "tags"=>["mutagenesis", "overlapping", "motifs", "in"], "article_id"=>443416, "categories"=>["Molecular Biology", "Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Alison P. Lee", "Sydney Brenner", "Byrappa Venkatesh"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020088.g008", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Site_directed_mutagenesis_of_overlapping_motifs_in_____CNE2_/443416", "title"=>"Site-directed mutagenesis of overlapping motifs in\n <i>CNE2</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-05-23 00:56:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/387961", "https://ndownloader.figshare.com/files/387998", "https://ndownloader.figshare.com/files/388026", "https://ndownloader.figshare.com/files/388060", "https://ndownloader.figshare.com/files/388097", "https://ndownloader.figshare.com/files/388161", "https://ndownloader.figshare.com/files/388206", "https://ndownloader.figshare.com/files/388248", "https://ndownloader.figshare.com/files/388291", "https://ndownloader.figshare.com/files/388334", "https://ndownloader.figshare.com/files/388372", "https://ndownloader.figshare.com/files/388422", "https://ndownloader.figshare.com/files/388458", "https://ndownloader.figshare.com/files/388512", "https://ndownloader.figshare.com/files/388563", "https://ndownloader.figshare.com/files/388635", "https://ndownloader.figshare.com/files/388677", "https://ndownloader.figshare.com/files/388726", "https://ndownloader.figshare.com/files/388755"], "description"=>"<div><p>The vertebrate <em>Lhx2</em> is a member of the LIM homeobox family of transcription factors. It is essential for the normal development of the forebrain, eye, olfactory system and liver as well for the differentiation of lymphoid cells. However, despite the highly restricted spatio-temporal expression pattern of <em>Lhx2</em>, nothing is known about its transcriptional regulation. In mammals and chicken, <em>Crb2</em>, <em>Dennd1a</em> and <em>Lhx2</em> constitute a conserved linkage block, while the intervening <em>Dennd1a</em> is lost in the fugu <em>Lhx2</em> locus. To identify functional enhancers of <em>Lhx2</em>, we predicted conserved noncoding elements (CNEs) in the human, mouse and fugu <em>Crb2</em>-<em>Lhx2</em> loci and assayed their function in transgenic mouse at E11.5. Four of the eight CNE constructs tested functioned as tissue-specific enhancers in specific regions of the central nervous system and the dorsal root ganglia (DRG), recapitulating partial and overlapping expression patterns of <em>Lhx2</em> and <em>Crb2</em> genes. There was considerable overlap in the expression domains of the CNEs, which suggests that the CNEs are either redundant enhancers or regulating different genes in the locus. Using a large set of CNEs (810 CNEs) associated with transcription factor-encoding genes that express predominantly in the central nervous system, we predicted four over-represented 8-mer motifs that are likely to be associated with expression in the central nervous system. Mutation of one of them in a CNE that drove reporter expression in the neural tube and DRG abolished expression in both domains indicating that this motif is essential for expression in these domains. The failure of the four functional enhancers to recapitulate the complete expression pattern of <em>Lhx2</em> at E11.5 indicates that there must be other <em>Lhx2</em> enhancers that are either located outside the region investigated or divergent in mammals and fishes. Other approaches such as sequence comparison between multiple mammals are required to identify and characterize such enhancers.</p> </div>", "links"=>[], "tags"=>["transgenesis", "identifies", "conserved", "enhancers", "and", "motif", "vertebrate", "lim", "homeobox", "gene", "locus"], "article_id"=>136613, "categories"=>["Molecular Biology", "Biological Sciences", "Genetics", "Evolutionary Biology"], "users"=>["Alison P. Lee", "Sydney Brenner", "Byrappa Venkatesh"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0020088.s001", "https://dx.doi.org/10.1371/journal.pone.0020088.s002", "https://dx.doi.org/10.1371/journal.pone.0020088.s003", "https://dx.doi.org/10.1371/journal.pone.0020088.s004", "https://dx.doi.org/10.1371/journal.pone.0020088.s005", "https://dx.doi.org/10.1371/journal.pone.0020088.s006", "https://dx.doi.org/10.1371/journal.pone.0020088.s007", "https://dx.doi.org/10.1371/journal.pone.0020088.s008", "https://dx.doi.org/10.1371/journal.pone.0020088.s009", "https://dx.doi.org/10.1371/journal.pone.0020088.s010", "https://dx.doi.org/10.1371/journal.pone.0020088.s011", "https://dx.doi.org/10.1371/journal.pone.0020088.s012", "https://dx.doi.org/10.1371/journal.pone.0020088.s013", "https://dx.doi.org/10.1371/journal.pone.0020088.s014", "https://dx.doi.org/10.1371/journal.pone.0020088.s015", "https://dx.doi.org/10.1371/journal.pone.0020088.s016", "https://dx.doi.org/10.1371/journal.pone.0020088.s017", "https://dx.doi.org/10.1371/journal.pone.0020088.s018", "https://dx.doi.org/10.1371/journal.pone.0020088.s019"], "stats"=>{"downloads"=>12, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Mouse_Transgenesis_Identifies_Conserved_Functional_Enhancers_and____cis_Regulatory_Motif_in_the_Vertebrate_LIM_Homeobox_Gene____Lhx2_Locus/136613", "title"=>"Mouse Transgenesis Identifies Conserved Functional Enhancers and\n <em>cis</em>-Regulatory Motif in the Vertebrate LIM Homeobox Gene\n <em>Lhx2</em> Locus", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-05-23 01:50:13"}

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