Phosphorylation of the Conserved Transcription Factor ATF-7 by PMK-1 p38 MAPK Regulates Innate Immunity in Caenorhabditis elegans
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{"title"=>"Phosphorylation of the conserved transcription factor ATF-7 by PMK-1 p38 MAPK regulates innate immunity in Caenorhabditis elegans", "type"=>"journal", "authors"=>[{"first_name"=>"Robert P.", "last_name"=>"Shivers", "scopus_author_id"=>"7005146946"}, {"first_name"=>"Daniel J.", "last_name"=>"Pagano", "scopus_author_id"=>"35734800200"}, {"first_name"=>"Tristan", "last_name"=>"Kooistra", "scopus_author_id"=>"35336677400"}, {"first_name"=>"Claire E.", "last_name"=>"Richardson", "scopus_author_id"=>"36011898400"}, {"first_name"=>"Kirthi C.", "last_name"=>"Reddy", "scopus_author_id"=>"7402390644"}, {"first_name"=>"Janelle K.", "last_name"=>"Whitney", "scopus_author_id"=>"36179109500"}, {"first_name"=>"Odile", "last_name"=>"Kamanzi", "scopus_author_id"=>"36052867300"}, {"first_name"=>"Kunihiro", "last_name"=>"Matsumoto", "scopus_author_id"=>"7601608039"}, {"first_name"=>"Naoki", "last_name"=>"Hisamoto", "scopus_author_id"=>"6701743944"}, {"first_name"=>"Dennis H.", "last_name"=>"Kim", "scopus_author_id"=>"55944791000"}], "year"=>2010, "source"=>"PLoS Genetics", "identifiers"=>{"pui"=>"358837603", "isbn"=>"1553-7404 (Electronic) 1553-7390 (Linking)", "pmid"=>"20369020", "doi"=>"10.1371/journal.pgen.1000892", "sgr"=>"77952376722", "scopus"=>"2-s2.0-77952376722", "issn"=>"15537390"}, "id"=>"8ad9f182-06a9-3e27-aeaa-c506e18e73c9", "abstract"=>"Innate immunity in Caenorhabditis elegans requires a conserved PMK-1 p38 mitogen-activated protein kinase (MAPK) pathway that regulates the basal and pathogen-induced expression of immune effectors. The mechanisms by which PMK-1 p38 MAPK regulates the transcriptional activation of the C. elegans immune response have not been identified. Furthermore, in mammalian systems the genetic analysis of physiological targets of p38 MAPK in immunity has been limited. Here, we show that C. elegans ATF-7, a member of the conserved cyclic AMP-responsive element binding (CREB)/activating transcription factor (ATF) family of basic-region leucine zipper (bZIP) transcription factors and an ortholog of mammalian ATF2/ATF7, has a pivotal role in the regulation of PMK-1-mediated innate immunity. Genetic analysis of loss-of-function alleles and a gain-of-function allele of atf-7, combined with expression analysis of PMK-1-regulated genes and biochemical characterization of the interaction between ATF-7 and PMK-1, suggest that ATF-7 functions as a repressor of PMK-1-regulated genes that undergoes a switch to an activator upon phosphorylation by PMK-1. Whereas loss-of-function mutations in atf-7 can restore basal expression of PMK-1-regulated genes observed in the pmk-1 null mutant, the induction of PMK-1-regulated genes by pathogenic Pseudomonas aeruginosa PA14 is abrogated. The switching modes of ATF-7 activity, from repressor to activator in response to activated PMK-1 p38 MAPK, are reminiscent of the mechanism of regulation mediated by the corresponding ancestral Sko1p and Hog1p proteins in the yeast response to osmotic stress. Our data point to the regulation of the ATF2/ATF7/CREB5 family of transcriptional regulators by p38 MAPK as an ancient conserved mechanism for the control of innate immunity in metazoans, and suggest that ATF2/ATF7 may function in a similar manner in the regulation of mammalian innate immunity.", "link"=>"http://www.mendeley.com/research/phosphorylation-conserved-transcription-factor-atf7-pmk1-p38-mapk-regulates-innate-immunity-caenorha", "reader_count"=>84, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>8, "Researcher"=>19, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>23, "Student > Postgraduate"=>2, "Other"=>2, "Student > Master"=>14, "Student > Bachelor"=>8, "Lecturer"=>1, "Professor"=>6}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>8, "Researcher"=>19, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>23, "Student > Postgraduate"=>2, "Other"=>2, "Student > Master"=>14, "Student > Bachelor"=>8, "Lecturer"=>1, "Professor"=>6}, "reader_count_by_subject_area"=>{"Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>12, "Agricultural and Biological Sciences"=>66, "Medicine and Dentistry"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Immunology and Microbiology"=>3}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>66}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>12}, "Environmental Science"=>{"Environmental Science"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"United States"=>6, "United Kingdom"=>2, "India"=>1}, "group_count"=>3}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/855716"], "description"=>"<p>(A) Identification of mutations in the <i>C. elegans atf-7</i> gene. Changes shown in amino acid residues are in reference to the coding region of gene model <i>C07G2.2a</i>. (B) Sequence alignment comparing the DNA binding domains of <i>C. elegans</i> ATF-7 and human ATF-2. (C) Phylogenetic analysis grouping <i>C. elegans</i> ATF-7 with the mammalian ATF2/ATF7/CREB5 family of bZIP transcription factors.</p>", "links"=>[], "tags"=>["alleles", "elegans", "ortholog", "mammalian", "bzip", "transcription"], "article_id"=>526139, "categories"=>["Immunology", "Genetics"], "users"=>["Robert P. Shivers", "Daniel J. Pagano", "Tristan Kooistra", "Claire E. Richardson", "Kirthi C. Reddy", "Janelle K. Whitney", "Odile Kamanzi", "Kunihiro Matsumoto", "Naoki Hisamoto", "Dennis H. Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000892.g002", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mutant_alleles_of_C_elegans_atf_7_an_ortholog_of_the_mammalian_ATF2_ATF7_CREB5_family_of_bZIP_transcription_factors_/526139", "title"=>"Mutant alleles of <i>C. elegans atf-7</i>, an ortholog of the mammalian ATF2/ATF7/CREB5 family of bZIP transcription factors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-04-01 01:42:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/856326"], "description"=>"<p>(A) Cos7 cells were transfected with T7-ATF-7 or T7-ATF-7 carrying the P58S <i>qd22</i> mutation, along with HA-PMK-1 and FLAG-SEK-1 as indicated. Whole cell extracts were immunoblotted with antibodies that recognize T7 (top), HA (middle), and FLAG (bottom). (B) Cos7 cells were transfected with T7-ATF-7 or T7-ATF-7 carrying the P58S <i>qd22</i> mutation, along with kinase-dead (KD) HA-PMK-1 and FLAG-SEK-1 as indicated. ATF-7 was immunoprecipitated with anti-T7 and immunoblotted with anti-HA (top). Whole cell extract were immunoblotted with antibodies that recognize T7 (middle top), HA (middle bottom), and FLAG (bottom).</p>", "links"=>[], "tags"=>["atf-7"], "article_id"=>526764, "categories"=>["Immunology", "Genetics"], "users"=>["Robert P. Shivers", "Daniel J. Pagano", "Tristan Kooistra", "Claire E. Richardson", "Kirthi C. Reddy", "Janelle K. Whitney", "Odile Kamanzi", "Kunihiro Matsumoto", "Naoki Hisamoto", "Dennis H. Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000892.g006", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phosphorylation_of_ATF_7_by_PMK_1_/526764", "title"=>"Phosphorylation of ATF-7 by PMK-1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-04-01 01:52:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/855982"], "description"=>"<p>qRT–PCR analysis of the expression of PMK-1-regulated genes. (A) L4 larval stage worms of the indicated genotype were propagated on <i>E. coli</i> OP50 and RNA was prepared as described in the <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000892#s2\" target=\"_blank\">Methods</a>. Expression is relative to wild-type. Shown is the mean from two independent biological replicates with error bars representing SEM. (B) As in (A), except that worms of the indicated geneotype were exposed to <i>P. aeruginosa</i> PA14 for 4 h. Expression is relative to wild-type on <i>E. coli</i> OP50.</p>", "links"=>[], "tags"=>["genetics and genomics/genetics of the immune system", "immunology/innate immunity"], "article_id"=>526421, "categories"=>["Immunology", "Genetics"], "users"=>["Robert P. Shivers", "Daniel J. Pagano", "Tristan Kooistra", "Claire E. Richardson", "Kirthi C. Reddy", "Janelle K. Whitney", "Odile Kamanzi", "Kunihiro Matsumoto", "Naoki Hisamoto", "Dennis H. Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000892.g004", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ATF_7_regulation_of_PMK_1_8211_regulated_genes_/526421", "title"=>"ATF-7 regulation of PMK-1–regulated genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-04-01 01:47:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/856665"], "description"=>"<p>(A) Repression of PMK-1–regulated immune effector gene expression by ATF-7 in the absence of PMK-1 activation. (B) Activation of basal and pathogen-induced immune effector gene expression by PMK-1 phosphorylation of ATF-7, which switches ATF-7 from a repressor to an activator of transcription.</p>", "links"=>[], "tags"=>["atf-7", "innate"], "article_id"=>527110, "categories"=>["Immunology", "Genetics"], "users"=>["Robert P. Shivers", "Daniel J. Pagano", "Tristan Kooistra", "Claire E. Richardson", "Kirthi C. Reddy", "Janelle K. Whitney", "Odile Kamanzi", "Kunihiro Matsumoto", "Naoki Hisamoto", "Dennis H. Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000892.g009", "stats"=>{"downloads"=>3, "page_views"=>83, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Model_for_the_function_of_ATF_7_in_C_elegans_innate_immunity_/527110", "title"=>"Model for the function of ATF-7 in <i>C. elegans</i> innate immunity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-04-01 01:58:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/855584"], "description"=>"<p>(A) Fluorescence microscopy images of GFP expression from the <i>agIs219</i> transgene in wild-type, <i>atf-7(qd22)</i> and <i>atf-7(qd22 qd130)</i> one-day-old adults. (B) Pathogenesis assay of L4 larval stage wild-type worms, <i>atf-7(qd22)</i> and <i>atf-7(qd22 qd130)</i> mutant animals, on <i>P. aeruginosa</i> PA14. All strains carry the <i>agIs219</i> transgene. The differences in susceptibility between <i>atf-7(qd22)</i> mutant animals and wild-type worms, <i>atf-7(qd22)</i> and <i>atf-7(qd22 qd130)</i> mutant animals, and <i>atf-7(qd22 qd130)</i> mutant animals and wild-type worms are all significant (<i>p</i><0.0001 for each comparison). Replicate data can be seen in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000892#pgen.1000892.s010\" target=\"_blank\">Figure S10</a>. (C) Immunoblot analysis of worm lysates from <i>atf-7(qd22)</i> worms. Total PMK-1 was identified using a polyclonal antibody generated against <i>C. elegans</i> PMK-1. Activated PMK-1 levels were identified using an antibody specific for the doubly phosphorylated TGY motif of activated PMK-1. (D) Pathogenesis assay of L4 larval stage wild-type worms; <i>atf-7(qd22 qd130)</i> and <i>atf-7(qd137)</i> mutants; and <i>atf-7(qd22 qd130)/atf-7(+), atf-7(qd137)/atf-7(+)</i>, and <i>atf-7(qd22 qd130)/atf-7(qd137)</i> trans-heterozygotes, on <i>P. aeruginosa</i> PA14. All strains carry the <i>agIs219</i> transgene. The differences in susceptibility between <i>atf-7(qd22 qd130)</i> mutant animals and <i>atf-7(qd22 qd130)/atf-7(+)</i> trans-heterozygotes, and <i>atf-7(qd137)</i> mutants animals and <i>atf-7(qd137)/atf-7(+)</i> trans-heterozygotes are significant (<i>p</i><0.0001 for each comparison). There is no difference in susceptibility between <i>atf-7(qd22 qd130)</i> mutant animals and <i>atf-7(qd22 qd130)/atf-7(qd137)</i> trans-heterozygotes, and <i>atf-7(qd137)</i> mutant animals and <i>atf-7(qd22 qd130)/atf-7(qd137)</i> trans-heterozygotes (<i>p</i>>0.35 for each comparison). Replicate data can be seen in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000892#pgen.1000892.s013\" target=\"_blank\">Figure S13</a>.</p>", "links"=>[], "tags"=>["mutants", "signaling", "downstream", "pmk-1", "p38"], "article_id"=>526001, "categories"=>["Immunology", "Genetics"], "users"=>["Robert P. Shivers", "Daniel J. Pagano", "Tristan Kooistra", "Claire E. Richardson", "Kirthi C. Reddy", "Janelle K. Whitney", "Odile Kamanzi", "Kunihiro Matsumoto", "Naoki Hisamoto", "Dennis H. Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000892.g001", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Characterization_of_atf_7_mutants_that_affect_signaling_downstream_of_PMK_1_p38_MAPK_/526001", "title"=>"Characterization of <i>atf-7</i> mutants that affect signaling downstream of PMK-1 p38 MAPK.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-04-01 01:40:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/856197"], "description"=>"<p>Fluorescence and DIC microscopy of a representative L4-staged wild-type worm carrying an <i>atf-7::GFP</i> transgene under the regulation of the endogenous genomic <i>atf-7</i> promoter and 3′-untranslated region. The red fluorescence from the pharynx is due to a <i>Pmyo-2::RFP</i> co-transformation marker. The rescuing capability of this translational fusion transgene was confirmed in both the <i>atf-7(qd22 qd130)</i> mutant (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000892#pgen.1000892.s005\" target=\"_blank\">Figure S5</a>) and <i>atf-7(qd22 qd130); pmk-1(km25)</i> double mutant (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000892#pgen.1000892.s007\" target=\"_blank\">Figure S7</a>). Scale bar, 100 µm.</p>", "links"=>[], "tags"=>["nuclei", "intestinal", "cells"], "article_id"=>526626, "categories"=>["Immunology", "Genetics"], "users"=>["Robert P. Shivers", "Daniel J. Pagano", "Tristan Kooistra", "Claire E. Richardson", "Kirthi C. Reddy", "Janelle K. Whitney", "Odile Kamanzi", "Kunihiro Matsumoto", "Naoki Hisamoto", "Dennis H. Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000892.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ATF_7_is_expressed_in_the_nuclei_of_intestinal_cells_in_C_elegans_/526626", "title"=>"ATF-7 is expressed in the nuclei of intestinal cells in <i>C. elegans</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-04-01 01:50:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/856581"], "description"=>"<p>Arsenite stress assay of L4 larval stage wild-type worms; <i>atf-7(qd22 qd130), pmk-1(km25)</i>, and <i>sek-1(km4)</i> mutant animals; and <i>atf-7(qd22 qd130); pmk-1(km25)</i> and <i>atf-7(qd22 qd130); sek-1(km4)</i> double mutant animals. Shown is the fraction of worms alive after 18 h. Error bars are standard deviation. The differences in survival between <i>atf-7(qd22 qd130)</i> mutant animals and <i>atf-7(qd22 qd130); pmk-1(km25)</i> double mutant animals, and <i>atf-7(qd22 qd130)</i> mutant animals and <i>atf-7(qd22 qd130); sek-1(km4)</i> double mutant animals are significant (<i>p</i><0.05 for each comparison).</p>", "links"=>[], "tags"=>["arsenite"], "article_id"=>527024, "categories"=>["Immunology", "Genetics"], "users"=>["Robert P. Shivers", "Daniel J. Pagano", "Tristan Kooistra", "Claire E. Richardson", "Kirthi C. Reddy", "Janelle K. Whitney", "Odile Kamanzi", "Kunihiro Matsumoto", "Naoki Hisamoto", "Dennis H. Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000892.g008", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ATF_7_does_not_contribute_to_arsenite_resistance_in_C_elegans_/527024", "title"=>"ATF-7 does not contribute to arsenite resistance in <i>C. elegans</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-04-01 01:57:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/856807"], "description"=>"<p>Mutations in <i>tir-1</i> are in reference to gene model <i>F13B10.1b</i>. The mutation in <i>atf-7</i> is in reference to gene model <i>C07G2.2a</i>.</p>", "links"=>[], "tags"=>["isolates", "mutants", "diminished", "gfp", "transgene", "enhanced", "susceptibility"], "article_id"=>527234, "categories"=>["Immunology", "Genetics"], "users"=>["Robert P. Shivers", "Daniel J. Pagano", "Tristan Kooistra", "Claire E. Richardson", "Kirthi C. Reddy", "Janelle K. Whitney", "Odile Kamanzi", "Kunihiro Matsumoto", "Naoki Hisamoto", "Dennis H. Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000892.t001", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_List_of_isolates_from_a_screen_for_mutants_with_diminished_GFP_expression_from_the_agIs219_transgene_and_enhanced_susceptibility_to_killing_by_P_aeruginosa_PA14_/527234", "title"=>"List of isolates from a screen for mutants with diminished GFP expression from the <i>agIs219</i> transgene and enhanced susceptibility to killing by <i>P. aeruginosa</i> PA14.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-04-01 02:00:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/856428"], "description"=>"<p>(A) Pathogenesis assay of L4 larval stage wild-type worms; <i>atf-7(qd22 qd130)</i> and <i>pmk-1(km25)</i> mutant animals; and <i>atf-7(qd22 qd130); pmk-1(km25)</i> double mutant animals, on <i>S. marcescens</i> Db10. All strains carry the <i>agIs219</i> transgene. The difference in susceptibility between <i>atf-7(qd22 qd130)</i> mutant animals and wild-type worms is significant (<i>p</i><0.0001). (B) Pathogenesis assay of L4 larval stage wild-type worms; <i>atf-7(qd22 qd130)</i> and <i>pmk-1(km25)</i> mutant animals; and <i>atf-7(qd22 qd130); pmk-1(km25)</i> double mutant animals, on <i>E. faecalis</i> MMH594. All strains carry the <i>agIs219</i> transgene. The difference in susceptibility between <i>pmk-1(km25)</i> mutant animals and <i>atf-7(qd22 qd130); pmk-1(km25)</i> double mutant animals is significant (<i>p</i><0.0001). There is no difference in susceptibility between <i>atf-7(qd22 qd130)</i> mutant animals and wild-type worms (<i>p</i>>0.9).</p>", "links"=>[], "tags"=>["atf-7", "bacterial"], "article_id"=>526871, "categories"=>["Immunology", "Genetics"], "users"=>["Robert P. Shivers", "Daniel J. Pagano", "Tristan Kooistra", "Claire E. Richardson", "Kirthi C. Reddy", "Janelle K. Whitney", "Odile Kamanzi", "Kunihiro Matsumoto", "Naoki Hisamoto", "Dennis H. Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000892.g007", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Requirement_for_ATF_7_in_resistance_to_other_bacterial_pathogens_/526871", "title"=>"Requirement for ATF-7 in resistance to other bacterial pathogens.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-04-01 01:54:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/425534", "https://ndownloader.figshare.com/files/425586", "https://ndownloader.figshare.com/files/425640", "https://ndownloader.figshare.com/files/425847", "https://ndownloader.figshare.com/files/425892", "https://ndownloader.figshare.com/files/425945", "https://ndownloader.figshare.com/files/426029", "https://ndownloader.figshare.com/files/426079", "https://ndownloader.figshare.com/files/426229", "https://ndownloader.figshare.com/files/426259", "https://ndownloader.figshare.com/files/426300", "https://ndownloader.figshare.com/files/426343", "https://ndownloader.figshare.com/files/426376", "https://ndownloader.figshare.com/files/426421", "https://ndownloader.figshare.com/files/426454", "https://ndownloader.figshare.com/files/426487", "https://ndownloader.figshare.com/files/426524"], "description"=>"<div><p>Innate immunity in <em>Caenorhabditis elegans</em> requires a conserved PMK-1 p38 mitogen-activated protein kinase (MAPK) pathway that regulates the basal and pathogen-induced expression of immune effectors. The mechanisms by which PMK-1 p38 MAPK regulates the transcriptional activation of the <em>C. elegans</em> immune response have not been identified. Furthermore, in mammalian systems the genetic analysis of physiological targets of p38 MAPK in immunity has been limited. Here, we show that <em>C. elegans</em> ATF-7, a member of the conserved cyclic AMP–responsive element binding (CREB)/activating transcription factor (ATF) family of basic-region leucine zipper (bZIP) transcription factors and an ortholog of mammalian ATF2/ATF7, has a pivotal role in the regulation of PMK-1–mediated innate immunity. Genetic analysis of loss-of-function alleles and a gain-of-function allele of <em>atf-7</em>, combined with expression analysis of PMK-1–regulated genes and biochemical characterization of the interaction between ATF-7 and PMK-1, suggest that ATF-7 functions as a repressor of PMK-1–regulated genes that undergoes a switch to an activator upon phosphorylation by PMK-1. Whereas loss-of-function mutations in <em>atf-7</em> can restore basal expression of PMK-1–regulated genes observed in the <em>pmk-1</em> null mutant, the induction of PMK-1–regulated genes by pathogenic <em>Pseudomonas aeruginosa</em> PA14 is abrogated. The switching modes of ATF-7 activity, from repressor to activator in response to activated PMK-1 p38 MAPK, are reminiscent of the mechanism of regulation mediated by the corresponding ancestral Sko1p and Hog1p proteins in the yeast response to osmotic stress. Our data point to the regulation of the ATF2/ATF7/CREB5 family of transcriptional regulators by p38 MAPK as an ancient conserved mechanism for the control of innate immunity in metazoans, and suggest that ATF2/ATF7 may function in a similar manner in the regulation of mammalian innate immunity.</p></div>", "links"=>[], "tags"=>["phosphorylation", "conserved", "transcription", "atf-7", "pmk-1", "p38", "mapk", "regulates", "innate", "immunity"], "article_id"=>144018, "categories"=>["Immunology", "Genetics"], "users"=>["Robert P. Shivers", "Daniel J. Pagano", "Tristan Kooistra", "Claire E. Richardson", "Kirthi C. Reddy", "Janelle K. Whitney", "Odile Kamanzi", "Kunihiro Matsumoto", "Naoki Hisamoto", "Dennis H. Kim"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000892.s001", "https://dx.doi.org/10.1371/journal.pgen.1000892.s002", "https://dx.doi.org/10.1371/journal.pgen.1000892.s003", "https://dx.doi.org/10.1371/journal.pgen.1000892.s004", "https://dx.doi.org/10.1371/journal.pgen.1000892.s005", "https://dx.doi.org/10.1371/journal.pgen.1000892.s006", "https://dx.doi.org/10.1371/journal.pgen.1000892.s007", "https://dx.doi.org/10.1371/journal.pgen.1000892.s008", "https://dx.doi.org/10.1371/journal.pgen.1000892.s009", "https://dx.doi.org/10.1371/journal.pgen.1000892.s010", "https://dx.doi.org/10.1371/journal.pgen.1000892.s011", "https://dx.doi.org/10.1371/journal.pgen.1000892.s012", "https://dx.doi.org/10.1371/journal.pgen.1000892.s013", "https://dx.doi.org/10.1371/journal.pgen.1000892.s014", "https://dx.doi.org/10.1371/journal.pgen.1000892.s015", "https://dx.doi.org/10.1371/journal.pgen.1000892.s016", "https://dx.doi.org/10.1371/journal.pgen.1000892.s017"], "stats"=>{"downloads"=>19, "page_views"=>27, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Phosphorylation_of_the_Conserved_Transcription_Factor_ATF_7_by_PMK_1_p38_MAPK_Regulates_Innate_Immunity_in_Caenorhabditis_elegans_/144018", "title"=>"Phosphorylation of the Conserved Transcription Factor ATF-7 by PMK-1 p38 MAPK Regulates Innate Immunity in <em>Caenorhabditis elegans</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-04-01 01:06:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/855846"], "description"=>"<p>(A) Fluorescence microscopy images of GFP expression from the <i>agIs219</i> transgene in <i>pmk-1(km25)</i> and <i>atf-7(qd22 qd130); pmk-1(km25)</i> one-day-old adults. (B) Pathogenesis assay of L4 larval stage wild-type worms; <i>atf-7(qd22 qd130)</i> and <i>pmk-1(km25)</i> mutant animals; and <i>atf-7(qd22 qd130); pmk-1(km25)</i> double mutant animals, on <i>P. aeruginosa</i> PA14. All strains carry the <i>agIs219</i> transgene. The difference in susceptibility between <i>pmk-1(km25)</i> mutant animals and <i>atf-7(qd22 qd130); pmk-1(km25)</i> double mutant animals is significant (<i>p</i><0.0001). Replicate data can be seen in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000892#pgen.1000892.s014\" target=\"_blank\">Figure S14</a>. (C) Fluorescence microscopy images of GFP expression from the <i>agIs219</i> transgene in <i>sek-1(km4)</i> and <i>atf-7(qd22 qd130); sek-1(km4)</i> one-day-old adults. (D) Pathogenesis assay of L4 larval stage wild-type worms; <i>atf-7(qd22 qd130)</i> and <i>sek-1(km4)</i> mutant animals; and <i>atf-7(qd22 qd130); sek-1(km4)</i> double mutant animals, on <i>P. aeruginosa</i> PA14. All strains except for KU25 [<i>sek-1(km4)</i>] carry the <i>agIs219</i> transgene. The difference in susceptibility between <i>sek-1(km4)</i> mutant animals and <i>atf-7(qd22 qd130); sek-1(km4)</i> double mutant animals is significant (<i>p</i><0.0001). Replicate data can be seen in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000892#pgen.1000892.s015\" target=\"_blank\">Figure S15</a>.</p>", "links"=>[], "tags"=>["loss-of-function", "mutation", "suppresses", "immunodeficient", "phenotype", "caused", "deficient", "signaling", "pmk-1"], "article_id"=>526271, "categories"=>["Immunology", "Genetics"], "users"=>["Robert P. Shivers", "Daniel J. Pagano", "Tristan Kooistra", "Claire E. Richardson", "Kirthi C. Reddy", "Janelle K. Whitney", "Odile Kamanzi", "Kunihiro Matsumoto", "Naoki Hisamoto", "Dennis H. Kim"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000892.g003", "stats"=>{"downloads"=>1, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_loss_of_function_atf_7_qd22_qd130_mutation_suppresses_the_immunodeficient_phenotype_caused_by_deficient_signaling_in_the_PMK_1_pathway_/526271", "title"=>"The loss-of-function <i>atf-7(qd22 qd130)</i> mutation suppresses the immunodeficient phenotype caused by deficient signaling in the PMK-1 pathway.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-04-01 01:44:31"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"10", "full-text"=>"12", "pdf"=>"5", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"15", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2017", "month"=>"7"}
  • {"unique-ip"=>"13", "full-text"=>"10", "pdf"=>"3", "abstract"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"13", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2017", "month"=>"8"}

Relative Metric

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