HIF-1 and SKN-1 Coordinate the Transcriptional Response to Hydrogen Sulfide in Caenorhabditis elegans
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{"title"=>"HIF-1 and SKN-1 coordinate the transcriptional response to hydrogen sulfide in Caenorhabditis elegans", "type"=>"journal", "authors"=>[{"first_name"=>"Dana L.", "last_name"=>"Miller", "scopus_author_id"=>"55413407900"}, {"first_name"=>"Mark W.", "last_name"=>"Budde", "scopus_author_id"=>"35777524900"}, {"first_name"=>"Mark B.", "last_name"=>"Roth", "scopus_author_id"=>"7401440552"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-80053338536", "doi"=>"10.1371/journal.pone.0025476", "sgr"=>"80053338536", "isbn"=>"1932-6203", "pmid"=>"21980473", "issn"=>"19326203", "pui"=>"362661104"}, "id"=>"30e137cb-5978-3b87-8b7d-ff39039a2eaa", "abstract"=>"Hydrogen sulfide (H₂S) has dramatic physiological effects on animals that are associated with improved survival. C. elegans grown in H₂S are long-lived and thermotolerant. To identify mechanisms by which adaptation to H₂S effects physiological functions, we have measured transcriptional responses to H₂S exposure. Using microarray analysis we observe rapid changes in the abundance of specific mRNAs. The number and magnitude of transcriptional changes increased with the duration of H₂S exposure. Functional annotation suggests that genes associated with protein homeostasis are upregulated upon prolonged exposure to H₂S. Previous work has shown that the hypoxia-inducible transcription factor, HIF-1, is required for survival in H₂S. In fact, we show that hif-1 is required for most, if not all, early transcriptional changes in H₂S. Moreover, our data demonstrate that SKN-1, the C. elegans homologue of NRF2, also contributes to H₂S-dependent changes in transcription. We show that these results are functionally important, as skn-1 is essential to survive exposure to H₂S. Our results suggest a model in which HIF-1 and SKN-1 coordinate a broad transcriptional response to H₂S that culminates in a global reorganization of protein homeostasis networks.", "link"=>"http://www.mendeley.com/research/hif1-skn1-coordinate-transcriptional-response-hydrogen-sulfide-caenorhabditis-elegans", "reader_count"=>53, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>4, "Librarian"=>2, "Researcher"=>15, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>2, "Other"=>2, "Student > Master"=>2, "Student > Bachelor"=>7, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>4, "Librarian"=>2, "Researcher"=>15, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>14, "Student > Postgraduate"=>2, "Other"=>2, "Student > Master"=>2, "Student > Bachelor"=>7, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>7, "Agricultural and Biological Sciences"=>32, "Medicine and Dentistry"=>3, "Neuroscience"=>2, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>4, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Neuroscience"=>{"Neuroscience"=>2}, "Chemistry"=>{"Chemistry"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>32}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}, "Unspecified"=>{"Unspecified"=>3}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"United States"=>7, "United Kingdom"=>1, "South Africa"=>1, "Chile"=>1, "India"=>1}, "group_count"=>5}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/368609", "https://ndownloader.figshare.com/files/368747", "https://ndownloader.figshare.com/files/368922", "https://ndownloader.figshare.com/files/368978", "https://ndownloader.figshare.com/files/369024"], "description"=>"<div><p>Hydrogen sulfide (H<sub>2</sub>S) has dramatic physiological effects on animals that are associated with improved survival. <em>C. elegans</em> grown in H<sub>2</sub>S are long-lived and thermotolerant. To identify mechanisms by which adaptation to H<sub>2</sub>S effects physiological functions, we have measured transcriptional responses to H<sub>2</sub>S exposure. Using microarray analysis we observe rapid changes in the abundance of specific mRNAs. The number and magnitude of transcriptional changes increased with the duration of H<sub>2</sub>S exposure. Functional annotation suggests that genes associated with protein homeostasis are upregulated upon prolonged exposure to H<sub>2</sub>S. Previous work has shown that the hypoxia-inducible transcription factor, HIF-1, is required for survival in H<sub>2</sub>S. In fact, we show that <em>hif-1</em> is required for most, if not all, early transcriptional changes in H<sub>2</sub>S. Moreover, our data demonstrate that SKN-1, the <em>C. elegans</em> homologue of NRF2, also contributes to H<sub>2</sub>S-dependent changes in transcription. We show that these results are functionally important, as <em>skn-1</em> is essential to survive exposure to H<sub>2</sub>S. Our results suggest a model in which HIF-1 and SKN-1 coordinate a broad transcriptional response to H<sub>2</sub>S that culminates in a global reorganization of protein homeostasis networks.</p> </div>", "links"=>[], "tags"=>["hif-1", "skn-1", "transcriptional", "hydrogen", "sulfide"], "article_id"=>132841, "categories"=>["Physiology", "Biochemistry", "Cell Biology", "Genetics"], "users"=>["Dana L. Miller", "Mark W. Budde", "Mark B. Roth"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0025476.s001", "https://dx.doi.org/10.1371/journal.pone.0025476.s002", "https://dx.doi.org/10.1371/journal.pone.0025476.s003", "https://dx.doi.org/10.1371/journal.pone.0025476.s004", "https://dx.doi.org/10.1371/journal.pone.0025476.s005"], "stats"=>{"downloads"=>12, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/HIF_1_and_SKN_1_Coordinate_the_Transcriptional_Response_to_Hydrogen_Sulfide_in_Caenorhabditis_elegans_/132841", "title"=>"HIF-1 and SKN-1 Coordinate the Transcriptional Response to Hydrogen Sulfide in <em>Caenorhabditis elegans</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-09-29 00:47:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/730160"], "description"=>"a<p>adjusted p-value, corrected for multiple testing and false discovery rate.</p>", "links"=>[], "tags"=>["mrna", "abundance"], "article_id"=>400519, "categories"=>["Physiology", "Biochemistry", "Cell Biology", "Genetics"], "users"=>["Dana L. Miller", "Mark W. Budde", "Mark B. Roth"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025476.t001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Changes_in_mRNA_abundance_associated_with_exposure_to_H_2_S_/400519", "title"=>"Changes in mRNA abundance associated with exposure to H<sub>2</sub>S.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-29 00:08:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/729851"], "description"=>"<p>A. Experimental design schematic. <i>C. elegans</i> were grown from synchronized first-stage larvae (L1) for 48 h to young adult before being collected for RNA extraction. Each bar represents 48 h from L1 to first-day adult for one experimental group. Time in room air is indicated in white and time in H<sub>2</sub>S indicated in red. Exposure to H<sub>2</sub>S (50 ppm in room air) was always immediately prior to isolating RNA. B. Changes in mRNA abundance measured by microarray. Plots show magnitude of change in transcript level (log<sub>2</sub> FC) as a function of adjusted p-value (log<sub>10</sub> p-value). Each point is data from one gene product. Significant changes (adj. p-value<0.05) are red. After 1 h exposure to H<sub>2</sub>S (left), 16 genes were significantly up-regulated and one was down-regulated (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0025476#pone-0025476-t001\" target=\"_blank\">Table 1</a>). After 12 h exposure to H<sub>2</sub>S (middle), 445 transcripts were significantly changed, with 259 up-regulated (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0025476#pone-0025476-t001\" target=\"_blank\">Tables 1</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0025476#pone.0025476.s001\" target=\"_blank\">S1</a>). After 48 h in H<sub>2</sub>S (right), 5089 transcripts were significantly altered relative to untreated controls (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0025476#pone.0025476.s002\" target=\"_blank\">Table S2</a>).</p>", "links"=>[], "tags"=>["induces", "changes", "mrna"], "article_id"=>400208, "categories"=>["Physiology", "Biochemistry", "Cell Biology", "Genetics"], "users"=>["Dana L. Miller", "Mark W. Budde", "Mark B. Roth"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025476.g001", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Exposure_to_H_2_S_induces_rapid_and_progressive_changes_in_mRNA_abundance_/400208", "title"=>"Exposure to H<sub>2</sub>S induces rapid and progressive changes in mRNA abundance.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-29 00:03:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/730016"], "description"=>"<p>A. Some H<sub>2</sub>S-induced transcriptional changes require <i>skn-1</i>. Changes in mRNA abundance after 1 h exposure to H<sub>2</sub>S were measured by qRT-PCR in N2 animals grown on control RNAi food L4440 (open bars) or on <i>skn-1(RNAi)</i> (filled bars). Three biological replicates for each group were performed, and each PCR reaction was run in duplicate. Error bars represent the standard deviation of the biological replicates, propagated through the ΔΔC<sub>t</sub> and fold-change calculations. *Difference between induction in control is significantly different than <i>skn-1(RNAi)</i> p<0.05. Table shows the frequency that core <i>skn-1</i> consensus sites (RTACT, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0025476#pone.0025476-Oliveira1\" target=\"_blank\">[27]</a>) are found within the upstream 2 kb flanking region of each transcript whose regulation in response to H<sub>2</sub>S was altered by <i>skn-1(RNAi)</i>. <sup>‡</sup>genes reported to have SKN-1 bound in the promoter in the ModENCODE database <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0025476#pone.0025476-Celniker1\" target=\"_blank\">[38]</a>. B. There is little similarity between response to H<sub>2</sub>S and other <i>skn-1</i>-dependent transcriptional responses. The overlap between the H<sub>2</sub>S-regulated genes after 12 h (n = 445) was greater than chance when compared with <i>skn-1</i>-dependent gene products in unstressed conditions (n = 233, 16 common transcripts, hypergeometric probability 0.006) and for genes that require <i>skn-1</i> for arsenic-induced upregulation (n = 118, 10 common transcripts, hypergeometric probability 0.01) <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0025476#pone.0025476-Oliveira1\" target=\"_blank\">[27]</a>. There was not significant overlap between transcripts altered by exposure to H<sub>2</sub>S and <i>skn-1</i> dependent transcripts that are downregulated in unstressed conditions (n = 63, hypergeometric probability 0.13), upregulated by tert-butyl hydroperoxide (n = 64, hypergeometric probability 0.06) or hyperoxia (n = 68, hypergeometric probability 0.15). C. <i>skn-1</i> is required to survive exposure to H<sub>2</sub>S. Unc animals (<i>skn-1/nT1</i> heterozygotes) were compared to non-Unc, <i>skn-1</i> homozygotes for sensitivity to H<sub>2</sub>S (#animals alive/total after exposure to 50 ppm H<sub>2</sub>S).</p>", "links"=>[], "tags"=>["genetics and genomics", "physiology", "cell biology", "Biochemistry"], "article_id"=>400375, "categories"=>["Physiology", "Biochemistry", "Cell Biology", "Genetics"], "users"=>["Dana L. Miller", "Mark W. Budde", "Mark B. Roth"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025476.g003", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SKN_1_is_essential_for_appropriate_response_to_H_2_S_/400375", "title"=>"SKN-1 is essential for appropriate response to H<sub>2</sub>S.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-29 00:06:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/730125"], "description"=>"a<p>12 h gene list included 91 genes whose mRNA was significantly increased after 12 h exposure to H<sub>2</sub>S (greater than 3-fold change in mRNA abundance, corrected p<0.05).</p>b<p>48 h gene list included 95 genes whose mRNA was significantly increased after 48 h exposure to H<sub>2</sub>S (greater than 5.6-fold change in mRNA abundance, corrected p<1×10<sup>−5</sup>).</p>", "links"=>[], "tags"=>["annotation", "products"], "article_id"=>400485, "categories"=>["Physiology", "Biochemistry", "Cell Biology", "Genetics"], "users"=>["Dana L. Miller", "Mark W. Budde", "Mark B. Roth"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025476.t003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Functional_annotation_of_gene_products_increased_after_exposure_to_H_2_S_/400485", "title"=>"Functional annotation of gene products increased after exposure to H<sub>2</sub>S.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-29 00:08:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/729912"], "description"=>"<p>A. H<sub>2</sub>S-induced transcriptional changes require HIF-1. Changes in mRNA abundance after 1 h exposure to H<sub>2</sub>S were measured by qRT-PCR in wild-type (N2, open bars) and <i>hif-1(ia04)</i> mutant animals (filled bars). Three biological replicates for each group were performed, and each PCR reaction was run in duplicate. Error bars represent the standard deviation of the biological replicates, as propagated through the ΔΔC<sub>t</sub> and fold-change calculations. *Difference between induction in wild-type (N2) is statistically different than in <i>hif-1(ia04)</i> mutant animals, p<0.05. Red dashed line demarks where transcript levels in H<sub>2</sub>S are the same as in room air. B. Transcriptional changes after 1 h exposure to H<sub>2</sub>S overlap slightly with <i>hif-1</i>-dependent changes in response to hypoxia. 3 of 16 transcripts upregulated in response to 1 h exposure to H<sub>2</sub>S were identified as <i>hif-1</i>-dependent targets in hypoxia (n = 68) <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0025476#pone.0025476-Shen1\" target=\"_blank\">[15]</a>. The probability of observing this overlap randomly is 0.001. C. There is minimal overlap between the transcriptional responses to hydrogen sulfide and hypoxia. Venn diagram shows overlap between genes induced by exposure to 12 h H<sub>2</sub>S (n = 298) and all genes products that are altered by hypoxia (n = 654) <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0025476#pone.0025476-Shen1\" target=\"_blank\">[15]</a>. The probability of randomly observing an overlap of 8 genes between these datasets is 0.006.</p>", "links"=>[], "tags"=>["transcriptional", "responses"], "article_id"=>400275, "categories"=>["Physiology", "Biochemistry", "Cell Biology", "Genetics"], "users"=>["Dana L. Miller", "Mark W. Budde", "Mark B. Roth"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025476.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HIF_1_is_required_for_early_transcriptional_responses_to_H_2_S_/400275", "title"=>"HIF-1 is required for early transcriptional responses to H<sub>2</sub>S.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-09-29 00:04:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/730094"], "description"=>"a<p>Fold-change of transcript as measured by microarray, as in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0025476#pone-0025476-t001\" target=\"_blank\">Table 1</a>.</p>b<p>Fold-change of transcript as measured by qRT-PCR. Animals were grown on E. coli OP50 strain or the HT115(DE3) strain containing the control RNAi plasmid L440.</p><p>*p<0.05.</p>", "links"=>[], "tags"=>["validation", "changes", "transcript", "abundance"], "article_id"=>400449, "categories"=>["Physiology", "Biochemistry", "Cell Biology", "Genetics"], "users"=>["Dana L. Miller", "Mark W. Budde", "Mark B. Roth"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0025476.t002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_qRT_PCR_Validation_of_changes_in_transcript_abundance_after_1_h_H_2_S_/400449", "title"=>"qRT-PCR Validation of changes in transcript abundance after 1 h H<sub>2</sub>S.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2011-09-29 00:07:29"}

PMC Usage Stats | Further Information

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