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{"title"=>"The HIF-1 hypoxia-inducible factor modulates lifespan in C. elegans", "type"=>"journal", "authors"=>[{"first_name"=>"Yi", "last_name"=>"Zhang", "scopus_author_id"=>"7601333059"}, {"first_name"=>"Zhiyong", "last_name"=>"Shao", "scopus_author_id"=>"14627922400"}, {"first_name"=>"Zhiwei", "last_name"=>"Zhai", "scopus_author_id"=>"14629791600"}, {"first_name"=>"Chuan", "last_name"=>"Shen", "scopus_author_id"=>"8603630400"}, {"first_name"=>"Jo Anne", "last_name"=>"Powell-Coffman", "scopus_author_id"=>"6602086693"}], "year"=>2009, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "pui"=>"355035949", "doi"=>"10.1371/journal.pone.0006348", "sgr"=>"68149149835", "scopus"=>"2-s2.0-68149149835", "isbn"=>"1932-6203 (Electronic)", "pmid"=>"19633713"}, "id"=>"de62ba3b-3317-3dde-a55c-a64dd0699250", "abstract"=>"During normal development or during disease, animal cells experience hypoxic (low oxygen) conditions, and the hypoxia-inducible factor (HIF) transcription factors implement most of the critical changes in gene expression that enable animals to adapt to this stress. Here, we examine the roles of HIF-1 in post-mitotic aging. We examined the effects of HIF-1 over-expression and of hif-1 loss-of-function mutations on longevity in C. elegans, a powerful genetic system in which adult somatic cells are post-mitotic. We constructed transgenic lines that expressed varying levels of HIF-1 protein and discovered a positive correlation between HIF-1 expression levels and lifespan. The data further showed that HIF-1 acted in parallel to the SKN-1/NRF and DAF-16/FOXO transcription factors to promote longevity. HIF-1 over-expression also conferred increased resistance to heat and oxidative stress. We isolated and characterized additional hif-1 mutations, and we found that each of 3 loss-of-function mutations conferred increased longevity in normal lab culture conditions, but, unlike HIF-1 over-expression, a hif-1 deletion mutation did not extend the lifespan of daf-16 or skn-1 mutants. We conclude that HIF-1 over-expression and hif-1 loss-of-function mutations promote longevity by different pathways. These data establish HIF-1 as one of the key stress-responsive transcription factors that modulate longevity in C. elegans and advance our understanding of the regulatory networks that link oxygen homeostasis and aging.", "link"=>"http://www.mendeley.com/research/hif1-hypoxiainducible-factor-modulates-lifespan-c-elegans", "reader_count"=>89, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>7, "Student > Doctoral Student"=>5, "Researcher"=>18, "Student > Ph. D. Student"=>25, "Student > Postgraduate"=>4, "Other"=>4, "Student > Master"=>9, "Student > Bachelor"=>10, "Lecturer > Senior Lecturer"=>1, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>7, "Student > Doctoral Student"=>5, "Researcher"=>18, "Student > Ph. D. Student"=>25, "Student > Postgraduate"=>4, "Other"=>4, "Student > Master"=>9, "Student > Bachelor"=>10, "Lecturer > Senior Lecturer"=>1, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>11, "Agricultural and Biological Sciences"=>67, "Medicine and Dentistry"=>2, "Neuroscience"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>1, "Psychology"=>1, "Chemical Engineering"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Neuroscience"=>{"Neuroscience"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Psychology"=>{"Psychology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>67}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>11}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Chemical Engineering"=>{"Chemical Engineering"=>1}}, "reader_count_by_country"=>{"Sweden"=>1, "United States"=>3, "United Kingdom"=>1, "Switzerland"=>1, "Germany"=>1}, "group_count"=>4}

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Figshare

• {"files"=>["https://ndownloader.figshare.com/files/890022"], "description"=>"<p>(A, B) <i>hif-1(P621G)</i> transgenes (<i>iaIs32</i> or <i>iaIs34</i>) extend the lifespan of animals carrying loss-of-function mutations in (A) <i>daf-16</i> (<i>p</i><0.0001) or (B) <i>skn-1</i> (<i>p</i><0.0001). (C) The longevity of <i>daf-2(e1370)</i> animals carrying a <i>hif-1 (P621G)</i> transgene is equivalent to that of <i>daf-2(e1370)</i> single mutants.</p>", "links"=>[], "tags"=>["over-expression", "extends", "lifespan"], "article_id"=>560480, "categories"=>["Cell Biology", "Genetics", "Medicine"], "users"=>["Yi Zhang", "Zhiyong Shao", "Zhiwei Zhai", "Chuan Shen", "Jo Anne Powell-Coffman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0006348.g003", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HIF_1_over_expression_extends_the_lifespan_of_daf_16_deficient_and_skn_1_deficient_mutants_/560480", "title"=>"HIF-1 over-expression extends the lifespan of <i>daf-16</i>-deficient and <i>skn-1</i>-deficient mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-07-27 00:08:00"}
• {"files"=>["https://ndownloader.figshare.com/files/890160"], "description"=>"<p>(A,B) Characterization of <i>hif-1</i> mutation alleles. (A) The <i>hif-1</i> locus encodes 4 mRNA isoforms (<a href=\"http://www.wormbase.org\" target=\"_blank\">www.wormbase.org</a>). Exons are depicted as boxes, with coding sequences in black and untranslated regions in grey. The positions of two deletion alleles (<i>ia04</i> and <i>ok2564</i>) and one nonsense mutation (<i>ia07</i>) are shown. (B) The <i>hif-1 (ia07)</i> point mutation introduces an early stop codon; (C) Protein blots show that all three mutations in <i>hif-1</i> repress expression of the <i>Pnhr-57</i>::GFP reporter <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0006348#pone.0006348-Shen2\" target=\"_blank\">[20]</a>. Expression was assayed in <i>vhl-1 (ok161)</i> mutants, which are defective in oxygen-dependent degradation of HIF-1. (D) <i>C. elegans</i> carrying <i>hif-1</i> loss-of-function mutations live longer than wild-type N2 (<i>p</i><0.0001). (E) <i>hif-1(ia04);daf-16(mu86)</i> double mutant animals do not live longer than <i>daf-16(mu86)</i> single mutants. (F) <i>daf-2 (e1370)</i> single mutants and <i>daf-2 (e1370); hif-1(ia04)</i> double mutants have equivalent lifespans. (G) <i>hif-1(ia04);skn-1(zu67)</i> double mutant animals do not live longer than <i>skn-1(zu67)</i> single mutants.</p>", "links"=>[], "tags"=>["loss-of-function", "mutations", "lifespan", "wild-type"], "article_id"=>560610, "categories"=>["Cell Biology", "Genetics", "Medicine"], "users"=>["Yi Zhang", "Zhiyong Shao", "Zhiwei Zhai", "Chuan Shen", "Jo Anne Powell-Coffman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0006348.g005", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_hif_1_loss_of_function_mutations_extend_the_lifespan_of_wild_type_animals_via_pathway_s_that_require_daf_16_and_skn_1_/560610", "title"=>"<i>hif-1</i> loss-of-function mutations extend the lifespan of wild-type animals, via pathway(s) that require <i>daf-16</i> and <i>skn-1</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-07-27 00:10:10"}
• {"files"=>["https://ndownloader.figshare.com/files/890325"], "description"=>"*<p>The <i>p</i> value was calculated by log-rank test as a comparison to <i>daf-16(mu86)</i> worms.</p>†<p>The <i>p</i> value was calculated by log-rank test as a comparison to <i>skn-1(zu67)</i> worms.</p>‡<p>The <i>p</i> value was calculated by log-rank test as a comparison to <i>daf-2(e1370)</i> worms.</p><p>Longevity assays for <i>daf-2</i>-deficient strains were performed at 25°C. All other lifespan assays were conducted at 20°C.</p>", "links"=>[], "tags"=>["hif-1", "over-expression", "loss-of-function", "mutations", "longevity"], "article_id"=>560773, "categories"=>["Cell Biology", "Genetics", "Medicine"], "users"=>["Yi Zhang", "Zhiyong Shao", "Zhiwei Zhai", "Chuan Shen", "Jo Anne Powell-Coffman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0006348.t002", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_HIF_1_over_expression_or_hif_1_loss_of_function_mutations_on_the_longevity_of_daf_16_or_skn_1_mutants_/560773", "title"=>"Effects of HIF-1 over-expression or <i>hif-1</i> loss-of-function mutations on the longevity of <i>daf-16</i> or <i>skn-1</i> mutants.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-07-27 00:12:53"}
• {"files"=>["https://ndownloader.figshare.com/files/890092"], "description"=>"<p>(A) A reduction of function mutation in <i>daf-2</i> does not change the protein levels of epitope-tagged HIF-1 (<i>iaIs28</i>) or HIF-1(P621G) (<i>iaIs32</i>) in young adult animals (<i>p</i>>0.2 from three independent experiments). (B,C) The expression of two HIF-1 targets were assayed in wild-type animals and in animals carrying a loss-of-function mutation in <i>daf-2</i>. (B) <i>Pnhr-57</i>:GFP expression was assayed by protein blots and was not significantly different in these genetic backgrounds (<i>p</i>>0.2 from three independent experiments) (B) Quantitative RT-PCR revealed a marginal differences in the levels of K10H10.2 mRNA (<i>p</i> = 0.09).</p>", "links"=>[], "tags"=>["insulin-like", "receptor", "hif-1"], "article_id"=>560551, "categories"=>["Cell Biology", "Genetics", "Medicine"], "users"=>["Yi Zhang", "Zhiyong Shao", "Zhiwei Zhai", "Chuan Shen", "Jo Anne Powell-Coffman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0006348.g004", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_daf_2_insulin_like_receptor_does_not_regulate_expression_of_HIF_1_protein_or_its_targets_/560551", "title"=>"The <i>daf-2</i> insulin-like receptor does not regulate expression of HIF-1 protein or its targets.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-07-27 00:09:11"}
• {"files"=>["https://ndownloader.figshare.com/files/889879"], "description"=>"<p>(A) Diagram of the minigenes that express epitope-tagged HIF-1. Genomic sequence including the <i>hif-1</i> promoter sequence, exon 1, and intron 1, was fused to cDNA including exons 2–9 for the predominant <i>hif-1</i> mRNA isoform (<i>hif-1a</i>). A myc epitope tag was inserted. A proline to glycine conversion at amino acid residue 621 prevents VHL-1-mediated degradation <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0006348#pone.0006348-Epstein1\" target=\"_blank\">[17]</a>. (B) Representative protein blots show that epitope-tagged HIF-1 is stabilized by loss-of-function mutations in <i>vhl-1</i> or <i>egl-9</i>. AHA-1 is ortholgous to HIFβ/ARNT <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0006348#pone.0006348-PowellCoffman1\" target=\"_blank\">[48]</a>, and the abundance of AHA-1 does not vary significantly in these strains. (C) Western blots show the transgene restores HIF-1-mediated gene expression. <i>Pnhr-57</i>:GFP is a reporter for HIF-1 activity <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0006348#pone.0006348-Shen2\" target=\"_blank\">[20]</a>. Its expression is dramatically reduced in <i>hif-1(ia04)</i> mutants and is restored by the <i>iaIs28</i> integrated <i>hif-1</i> transgene. (D) Oxygen-dependent degradation via the <i>vhl-1/egl-9</i> pathway is abolished when the HIF-1 proline residue 621 is mutated to glycine.</p>", "links"=>[], "tags"=>["genetics and genomics", "cell biology/cellular death and stress responses", "cell biology/gene expression", "developmental biology/aging"], "article_id"=>560330, "categories"=>["Cell Biology", "Genetics", "Medicine"], "users"=>["Yi Zhang", "Zhiyong Shao", "Zhiwei Zhai", "Chuan Shen", "Jo Anne Powell-Coffman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0006348.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Characterization_of_the_hif_1_and_hif_1_P621G_transgenes_/560330", "title"=>"Characterization of the <i>hif-1</i> and <i>hif-1(P621G)</i> transgenes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-07-27 00:05:30"}
• {"files"=>["https://ndownloader.figshare.com/files/441019", "https://ndownloader.figshare.com/files/441076", "https://ndownloader.figshare.com/files/441116"], "description"=>"<div><p>During normal development or during disease, animal cells experience hypoxic (low oxygen) conditions, and the hypoxia-inducible factor (HIF) transcription factors implement most of the critical changes in gene expression that enable animals to adapt to this stress. Here, we examine the roles of HIF-1 in post-mitotic aging. We examined the effects of HIF-1 over-expression and of <em>hif-1</em> loss-of-function mutations on longevity in <em>C. elegans</em>, a powerful genetic system in which adult somatic cells are post-mitotic. We constructed transgenic lines that expressed varying levels of HIF-1 protein and discovered a positive correlation between HIF-1 expression levels and lifespan. The data further showed that HIF-1 acted in parallel to the SKN-1/NRF and DAF-16/FOXO transcription factors to promote longevity. HIF-1 over-expression also conferred increased resistance to heat and oxidative stress. We isolated and characterized additional <em>hif-1</em> mutations, and we found that each of 3 loss-of-function mutations conferred increased longevity in normal lab culture conditions, but, unlike HIF-1 over-expression, a <em>hif-1</em> deletion mutation did not extend the lifespan of <em>daf-16</em> or <em>skn-1</em> mutants. We conclude that HIF-1 over-expression and <em>hif-1</em> loss-of-function mutations promote longevity by different pathways. These data establish HIF-1 as one of the key stress-responsive transcription factors that modulate longevity in <em>C. elegans</em> and advance our understanding of the regulatory networks that link oxygen homeostasis and aging.</p></div>", "links"=>[], "tags"=>["hif-1", "hypoxia-inducible", "modulates", "lifespan"], "article_id"=>146927, "categories"=>["Cell Biology", "Genetics", "Medicine"], "users"=>["Yi Zhang", "Zhiyong Shao", "Zhiwei Zhai", "Chuan Shen", "Jo Anne Powell-Coffman"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0006348.s001", "https://dx.doi.org/10.1371/journal.pone.0006348.s002", "https://dx.doi.org/10.1371/journal.pone.0006348.s003"], "stats"=>{"downloads"=>19, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_HIF_1_Hypoxia_Inducible_Factor_Modulates_Lifespan_in_C_elegans_/146927", "title"=>"The HIF-1 Hypoxia-Inducible Factor Modulates Lifespan in <em>C. elegans</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-07-27 01:55:27"}
• {"files"=>["https://ndownloader.figshare.com/files/890245"], "description"=>"<p>(A, B) Resistance to (A) t-butyl peroxide or (B) heat stress was assayed in <i>hif-1</i> loss-of-function mutants and in animals over-expressing HIF-1. The <i>daf-2 (e1370)</i> and <i>daf-16 (mu86)</i> strains were included as a basis for comparison. Error bars represent the standard error of the means from at least 3 experiments. (*, <i>p</i><0.0001 compared to wild type N2 worms using z-test).</p>", "links"=>[], "tags"=>["loss-of-function", "mutations", "hif-1", "over-expression", "oxidative"], "article_id"=>560696, "categories"=>["Cell Biology", "Genetics", "Medicine"], "users"=>["Yi Zhang", "Zhiyong Shao", "Zhiwei Zhai", "Chuan Shen", "Jo Anne Powell-Coffman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0006348.g006", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_hif_1_loss_of_function_mutations_and_HIF_1_over_expression_increase_oxidative_stress_resistance_and_thermotolerance_/560696", "title"=>"<i>hif-1</i> loss-of-function mutations and HIF-1 over-expression increase oxidative stress resistance and thermotolerance.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-07-27 00:11:36"}
• {"files"=>["https://ndownloader.figshare.com/files/889959"], "description"=>"<p>(A) Protein blots quantitate expression of HIF-1 and HIF-1(P621G) transgenes (tagged with the myc epitope). <i>iaIs27</i> and <i>iaIs28</i> contain integrated copies of the <i>hif-1</i> minigene. <i>iaIs32</i>, <i>iaIs33</i>, and <i>iaIs34</i> carry integrated copies of <i>hif-1 (P621G)</i>. (B) Strains carrying <i>hif-1</i> transgenes live longer (<i>p</i><0.0001). Proportion alive is plotted over time. (C) The mean adult lifespans of strains over-expressing HIF-1 are positively correlated with the HIF-1 expression levels. Error bars represent the standard errors of the means.</p>", "links"=>[], "tags"=>["over-expression", "extends", "longevity", "dose-dependent"], "article_id"=>560411, "categories"=>["Cell Biology", "Genetics", "Medicine"], "users"=>["Yi Zhang", "Zhiyong Shao", "Zhiwei Zhai", "Chuan Shen", "Jo Anne Powell-Coffman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0006348.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_HIF_1_over_expression_extends_longevity_in_a_dose_dependent_manner_/560411", "title"=>"HIF-1 over-expression extends longevity in a dose-dependent manner.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-07-27 00:06:51"}
• {"files"=>["https://ndownloader.figshare.com/files/890360"], "description"=>"*<p>The longevity of each strain was compared to wild-type, and the <i>p</i> values were calculated by log-rank tests.</p>", "links"=>[], "tags"=>["hif-1", "loss-of-function", "mutations", "lifespan"], "article_id"=>560815, "categories"=>["Cell Biology", "Genetics", "Medicine"], "users"=>["Yi Zhang", "Zhiyong Shao", "Zhiwei Zhai", "Chuan Shen", "Jo Anne Powell-Coffman"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0006348.t001", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Over_expression_of_HIF_1_protein_or_hif_1_loss_of_function_mutations_extend_adult_lifespan_in_C_elegans_in_standard_lab_culture_conditions_/560815", "title"=>"Over-expression of HIF-1 protein or <i>hif-1</i> loss-of-function mutations extend adult lifespan in <i>C. elegans</i> in standard lab culture conditions.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2009-07-27 00:13:35"}

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Relative Metric

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F1000Prime