Physiological IRE-1-XBP-1 and PEK-1 Signaling in Caenorhabditis elegans Larval Development and Immunity
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{"title"=>"Physiological IRE-1-XBP-1 and PEK-1 signaling in Caenorhabditis elegans larval development and immunity", "type"=>"journal", "authors"=>[{"first_name"=>"Claire E.", "last_name"=>"Richardson", "scopus_author_id"=>"36011898400"}, {"first_name"=>"Stephanie", "last_name"=>"Kinkel", "scopus_author_id"=>"36924145400"}, {"first_name"=>"Dennis H.", "last_name"=>"Kim", "scopus_author_id"=>"55944791000"}], "year"=>2011, "source"=>"PLoS Genetics", "identifiers"=>{"isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "pmid"=>"22125500", "pui"=>"362967186", "issn"=>"15537390", "scopus"=>"2-s2.0-81755177847", "sgr"=>"81755177847", "doi"=>"10.1371/journal.pgen.1002391"}, "id"=>"0225baea-d8e0-3896-83e2-ddd73e1bb88d", "abstract"=>"Endoplasmic reticulum (ER) stress activates the Unfolded Protein Response, a compensatory signaling response that is mediated by the IRE-1, PERK/PEK-1, and ATF-6 pathways in metazoans. Genetic studies have implicated roles for UPR signaling in animal development and disease, but the function of the UPR under physiological conditions, in the absence of chemical agents administered to induce ER stress, is not well understood. Here, we show that in Caenorhabditis elegans XBP-1 deficiency results in constitutive ER stress, reflected by increased basal levels of IRE-1 and PEK-1 activity under physiological conditions. We define a dynamic, temperature-dependent requirement for XBP-1 and PEK-1 activities that increases with immune activation and at elevated physiological temperatures in C. elegans. Our data suggest that the negative feedback loops involving the activation of IRE-1-XBP-1 and PEK-1 pathways serve essential roles, not only at the extremes of ER stress, but also in the maintenance of ER homeostasis under physiological conditions.", "link"=>"http://www.mendeley.com/research/physiological-ire1xbp1-pek1-signaling-caenorhabditis-elegans-larval-development-immunity", "reader_count"=>62, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Researcher"=>17, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>23, "Student > Master"=>7, "Other"=>1, "Student > Bachelor"=>5, "Lecturer"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Researcher"=>17, "Student > Doctoral Student"=>5, "Student > Ph. D. Student"=>23, "Student > Master"=>7, "Other"=>1, "Student > Bachelor"=>5, "Lecturer"=>1}, "reader_count_by_subject_area"=>{"Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>9, "Agricultural and Biological Sciences"=>49, "Medicine and Dentistry"=>2, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>49}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>9}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"United States"=>6, "Chile"=>1}, "group_count"=>2}

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Figshare

  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/360497/Figure_S1.tif", "https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/360524/Figure_S2.tif", "https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/360541/Figure_S3.tif"], "description"=>"<div><p>Endoplasmic reticulum (ER) stress activates the Unfolded Protein Response, a compensatory signaling response that is mediated by the IRE-1, PERK/PEK-1, and ATF-6 pathways in metazoans. Genetic studies have implicated roles for UPR signaling in animal development and disease, but the function of the UPR under physiological conditions, in the absence of chemical agents administered to induce ER stress, is not well understood. Here, we show that in <em>Caenorhabditis elegans</em> XBP-1 deficiency results in constitutive ER stress, reflected by increased basal levels of IRE-1 and PEK-1 activity under physiological conditions. We define a dynamic, temperature-dependent requirement for XBP-1 and PEK-1 activities that increases with immune activation and at elevated physiological temperatures in <em>C. elegans</em>. Our data suggest that the negative feedback loops involving the activation of IRE-1-XBP-1 and PEK-1 pathways serve essential roles, not only at the extremes of ER stress, but also in the maintenance of ER homeostasis under physiological conditions.</p> </div>", "links"=>[], "tags"=>["physiological", "ire-1-xbp-1", "pek-1", "signaling", "larval", "immunity"], "article_id"=>131252, "categories"=>["Physiology", "Cell Biology"], "users"=>["Claire E. Richardson", "Stephanie Kinkel", "Dennis H. Kim"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1002391"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/Physiological_IRE_1_XBP_1_and_PEK_1_Signaling_in_Caenorhabditis_elegans_Larval_Development_and_Immunity/131252", "title"=>"Physiological IRE-1-XBP-1 and PEK-1 Signaling in <em>Caenorhabditis elegans</em> Larval Development and Immunity", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2011-11-17 00:20:52"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/710597/Figure_1.tif"], "description"=>"<p>(A) Detection of <i>xbp-1</i> mRNA splicing by IRE-1 in the <i>C. elegans xbp-1(zc12)</i> mutant. Schematic of the unspliced and spliced <i>xbp-1</i> mRNA, noting the position of the premature termination codon present in the <i>xbp-1(zc12)</i> allele. The <i>smg-2(qd101)</i> mutation results in inactivation of the NMD pathway, stabilizing the <i>xbp-1(zc12)</i> mRNA for detection. (B) Quantitative real-time PCR measurements of mRNA levels in the <i>xbp-1(zc12)</i> and <i>smg-2(qd101);xbp-1(zc12)</i> mutants relative to the <i>smg-2(qd101)</i> mutant synchronized in the L3 stage. (C) Quantitative real-time PCR measurements of levels of total and spliced <i>xbp-1</i> mRNA in the <i>smg-2(qd101)</i> strain relative to WT grown to the L3 stage and then shifted to plates with or without tunicamycin (5 µg/mL) for 4 h. (D) Larval development and survival assay showing the proportion of animals of each of the indicated strains that reach the indicated stage after 4 d of development from eggs laid on plates containing tunicamycin (2.5 µg/mL) at 16°C. (E) Quantitative real-time PCR measurements of levels of total and spliced <i>xbp-1</i> mRNA in the <i>smg-2(qd101)</i>; <i>xbp-1(zc12)</i> strain relative to the <i>smg-2(qd101)</i> strain treated as in C. (In B, C, and E, values represent fold change ± s.e.m., n = 3 independent experiments, *P<0.05, ***P<0.001, two-way ANOVA with Bonferroni post test).</p>", "links"=>[], "tags"=>["deficiency", "ire-1"], "article_id"=>380957, "categories"=>["Physiology", "Cell Biology"], "users"=>["Claire E. Richardson", "Stephanie Kinkel", "Dennis H. Kim"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1002391.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_XBP_1_deficiency_results_in_a_dramatic_increase_in_IRE_1_activity_/380957", "title"=>"XBP-1 deficiency results in a dramatic increase in IRE-1 activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-11-17 00:15:57"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/710669/Figure_2.tif"], "description"=>"<p>(A) PEK-1 dependent phosphorylation of eIF2α is induced by high dose (50 ug/ml) tunicamycin. Western blot of P-eIF2α, total eIF2α and tubulin in WT and <i>pek-1(ok275</i>) strains grown to the L4 stage and then shifted to plates with or without tunicamycin (50 µg/mL) for 4 hours. (B) PEK-1 dependent phosphorylation of eIF2α is induced by XBP-1 deficiency. Western blot of P-eIF2α, total eIF2α and tubulin in WT, <i>xbp-1(tm2482)</i>, <i>xbp-1(tm2482)</i>; <i>pek-1(ok275)</i> and <i>pek-1(ok275</i>) strains grown to the L4 stage.</p>", "links"=>[], "tags"=>["deficiency", "increases", "pek-1", "phosphorylation"], "article_id"=>381033, "categories"=>["Physiology", "Cell Biology"], "users"=>["Claire E. Richardson", "Stephanie Kinkel", "Dennis H. Kim"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1002391.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_XBP_1_deficiency_increases_PEK_1_dependent_phosphorylation_of_eIF2_945_/381033", "title"=>"XBP-1 deficiency increases PEK-1 dependent phosphorylation of eIF2α.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-11-17 00:17:13"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/710725/Figure_3.tif"], "description"=>"<p>Quantitative real-time PCR measurements of levels of total and spliced <i>xbp-1</i> mRNA in the indicated strains grown from synchronized L1s for 23 h at 20°C and then shifted to plates with or without <i>P. aeruginos</i>a PA14 at 25°C for (A) 4 h or (B) 11 h. Values represent fold change ± s.e.m. (n = 2 independent experiments, ***P<0.001, two-way ANOVA with Bonferroni post test). The WT strain exposed to either treatment was normalized to WT without <i>P. aeruginosa</i>; all other strains were normalized to <i>smg-2(qd101)</i> without <i>P. aeruginosa</i>.</p>", "links"=>[], "tags"=>["activation", "exacerbates", "er", "levels", "xbp-1", "deficiency"], "article_id"=>381081, "categories"=>["Physiology", "Cell Biology"], "users"=>["Claire E. Richardson", "Stephanie Kinkel", "Dennis H. Kim"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1002391.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Pathogen_induced_immune_activation_exacerbates_ER_stress_levels_in_XBP_1_deficiency_in_C_elegans_/381081", "title"=>"Pathogen-induced immune activation exacerbates ER stress levels in XBP-1 deficiency in <i>C. elegans</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-11-17 00:18:01"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/710769/Figure_4.tif"], "description"=>"<p>(A) Development of the <i>xbp-1(tm2482)</i>; <i>pek-1(ok275)</i> mutant across physiological temperatures. Values represent average fraction of eggs developed to the indicated stage ± s.e.m. (n = 3 independent experiments at 20°C, 2 independent experiments at all other temperatures; ***P<0.001, two-way ANOVA with Bonferroni post test). (B) Lifespan of indicated strains grown at 16°C to the L4 stage, then shifted to either 16°C to 25°C. Results are representative of two independent experiments.</p>", "links"=>[], "tags"=>["lethality"], "article_id"=>381139, "categories"=>["Physiology", "Cell Biology"], "users"=>["Claire E. Richardson", "Stephanie Kinkel", "Dennis H. Kim"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1002391.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Temperature_sensitive_lethality_of_the_xbp_1_pek_1_double_mutant_/381139", "title"=>"Temperature-sensitive lethality of the <i>xbp-1;pek-1</i> double mutant.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-11-17 00:18:59"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/710830/Figure_5.tif"], "description"=>"<p>(A) Development of indicated mutants from eggs to the L4 larval stage or older after 4 d at 16°C on <i>P. aeruginosa</i> PA14. Values represent mean ± s.d. from 1 of 2 representative experiments (n = 4 plates with 20–50 eggs each, ***P<0.001, one-way ANOVA with Bonferroni post test). (B) Development of <i>xbp-1(tm2482)</i>; <i>pek-1(ok275)</i> and <i>xbp-1(tm2482)</i>; <i>pmk-1(km25)</i>; <i>pek-1(ok275)</i> mutants from eggs on <i>E. coli</i> OP50. Values represent average fraction of eggs developed to the indicated stage ± s.e.m. (n = 2 independent experiments, **P<0.01, ***P<0.001, two-way ANOVA with Bonferroni post test). (C) Development of indicated mutants from eggs to the L4 larval stage or older after 2 d at 27°C on <i>E. coli</i> OP50. Values represent mean ± s.e.m. (n = 3 independent experiments, ***P<0.001, one-way ANOVA with Bonferroni post test). (D) Development of indicated mutants from eggs to the L4 larval stage or older after 2 d at 27°C on <i>P. aeruginosa</i> PA14. Values represent mean ± s.d. from 1 of 2 representative experiments (n = 3–4 plates with 20–60 eggs each, ***P<0.001, one-way ANOVA with Bonferroni post test).</p>", "links"=>[], "tags"=>["pek-1", "elevated", "physiological"], "article_id"=>381189, "categories"=>["Physiology", "Cell Biology"], "users"=>["Claire E. Richardson", "Stephanie Kinkel", "Dennis H. Kim"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1002391.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_XBP_1_and_PEK_1_each_protect_against_elevated_physiological_temperature_and_immune_activity_/381189", "title"=>"XBP-1 and PEK-1 each protect against elevated physiological temperature and immune activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-11-17 00:19:49"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/710877/Figure_6.tif"], "description"=>"<p>Larval development and survival assay showing the proportion of animals of each of the indicated strains that reach the indicated stage after 4 d of development from eggs laid on plates containing tunicamycin at 16°C. Values are from either one experiment (0.5 µg/ml and 2.5 µg/ml tunicamycin) or combined from two experiments with similar results (1.5 µg/ml tunicamycin).</p>", "links"=>[], "tags"=>["protects", "exogenously", "induced", "er"], "article_id"=>381244, "categories"=>["Physiology", "Cell Biology"], "users"=>["Claire E. Richardson", "Stephanie Kinkel", "Dennis H. Kim"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1002391.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_PMK_1_protects_against_exogenously_induced_ER_stress_/381244", "title"=>"PMK-1 protects against exogenously induced ER stress.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-11-17 00:20:44"}
  • {"files"=>["https://s3-eu-west-1.amazonaws.com/pstorage-plos-3567654/710945/Figure_7.tif"], "description"=>"<p>(A) The increase in both IRE-1 and PEK-1 activities in XBP-1 deficiency in the absence of exogenous compounds to impose ER stress, combined with the temperature-sensitive lethality of the UPR mutants, implies that UPR signaling maintains ER homeostasis not only in response to the extremes of ER stress, but also under basal physiological conditions. (B) Infection, basal growth and development, and elevated physiological temperature all contribute to ER stress, leading to lethality of UPR mutants as indicated by dashed lines.</p>", "links"=>[], "tags"=>["er", "homeostasis", "activation", "ire-1", "pek-1", "pathways", "basal", "physiological", "conditions"], "article_id"=>381300, "categories"=>["Physiology", "Cell Biology"], "users"=>["Claire E. Richardson", "Stephanie Kinkel", "Dennis H. Kim"], "doi"=>["http://dx.doi.org/10.1371/journal.pgen.1002391.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"http://figshare.com/articles/_Maintenance_of_ER_homeostasis_through_activation_of_the_IRE_1_and_PEK_1_pathways_under_basal_physiological_conditions_during_development_/381300", "title"=>"Maintenance of ER homeostasis through activation of the IRE-1 and PEK-1 pathways under basal physiological conditions during development.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2011-11-17 00:21:40"}

PMC Usage Stats | Further Information

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Relative Metric

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