Endoplasmic Reticulum Stress-Sensing Mechanism Is Activated in Entamoeba histolytica upon Treatment with Nitric Oxide
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{"title"=>"Endoplasmic reticulum stress-sensing mechanism is activated in entamoeba histolytica upon treatment with nitric oxide", "type"=>"journal", "authors"=>[{"first_name"=>"Julien", "last_name"=>"Santi-Rocca", "scopus_author_id"=>"23089369000"}, {"first_name"=>"Sherri", "last_name"=>"Smith", "scopus_author_id"=>"18635389500"}, {"first_name"=>"Christian", "last_name"=>"Weber", "scopus_author_id"=>"55737922200"}, {"first_name"=>"Erika", "last_name"=>"Pineda", "scopus_author_id"=>"56013655400"}, {"first_name"=>"Chung Chau", "last_name"=>"Hon", "scopus_author_id"=>"7003617137"}, {"first_name"=>"Emma", "last_name"=>"Saavedra", "scopus_author_id"=>"6701824235"}, {"first_name"=>"Alfonso", "last_name"=>"Olivos-García", "scopus_author_id"=>"6506452757"}, {"first_name"=>"Sandrine", "last_name"=>"Rousseau", "scopus_author_id"=>"23477894500"}, {"first_name"=>"Marie Agnès", "last_name"=>"Dillies", "scopus_author_id"=>"12771098900"}, {"first_name"=>"Jean Yves", "last_name"=>"Coppée", "scopus_author_id"=>"55916699000"}, {"first_name"=>"Nancy", "last_name"=>"Guillén", "scopus_author_id"=>"7003886496"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"364338048", "sgr"=>"84863179892", "issn"=>"19326203", "pmid"=>"22384074", "scopus"=>"2-s2.0-84863179892", "doi"=>"10.1371/journal.pone.0031777", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)"}, "id"=>"0482e445-ab0f-3c12-b106-d9ce59d6bb61", "abstract"=>"The Endoplasmic Reticulum stores calcium and is a site of protein synthesis and modification. Changes in ER homeostasis lead to stress responses with an activation of the unfolded protein response (UPR). The Entamoeba histolytica endomembrane system is simple compared to those of higher eukaryotes, as a canonical ER is not observed. During amoebiasis, an infection of the human intestine and liver by E. histolytica, nitric oxide (NO) triggers an apoptotic-like event preceded by an impairment of energy production and a loss of important parasite pathogenic features. We address the question of how this ancient eukaryote responds to stress induced by immune components (i.e. NO) and whether stress leads to ER changes and subsequently to an UPR. Gene expression analysis suggested that NO triggers stress responses marked by (i) dramatic up-regulation of hsp genes although a bona fide UPR is absent; (ii) induction of DNA repair and redox gene expression and iii) up-regulation of glycolysis-related gene expression. Enzymology approaches demonstrate that NO directly inhibits glycolysis and enhance cysteine synthase activity. Using live imaging and confocal microscopy we found that NO dramatically provokes extensive ER fragmentation. ER fission in E. histolytica appears as a protective response against stress, as it has been recently proposed for neuron self-defense during neurologic disorders. Chronic ER stress is also involved in metabolic diseases including diabetes, where NO production reduces ER calcium levels and activates cell death. Our data highlighted unique cellular responses of interest to understand the mechanisms of parasite death during amoebiasis.", "link"=>"http://www.mendeley.com/research/endoplasmic-reticulum-stresssensing-mechanism-activated-entamoeba-histolytica-upon-treatment-nitric", "reader_count"=>29, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>7, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>1, "Student > Master"=>7, "Other"=>2, "Student > Bachelor"=>1, "Professor"=>4}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>7, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>1, "Student > Master"=>7, "Other"=>2, "Student > Bachelor"=>1, "Professor"=>4}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>8, "Agricultural and Biological Sciences"=>15, "Medicine and Dentistry"=>3, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>15}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Mexico"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/675533"], "description"=>"<p>The nitric oxide induced changes were quantified using the iMARIS software. An average of 30 amoebas were analyzed per experiment. The total number of labeled compartments and the volume per labeled compartment were determined. The data show that both ER markers, KDEL and CRT, exhibit a similar change with a decrease in the volume of labeled vesicles and an increase in the number of vesicles present (A) . An unpaired t-test was performed and a statistically significant difference was found between treated and untreated samples for both ER markers (** p<0.05 and *** p<0.01). The calreticulin protein level was analyzed, 40,000 amoebas were loaded in each lane for each condition. An anti-actinin-2 antibody was used to control for equal loading of samples. No changes in the calreticulin protein levels were observed. Although there are changes in ER organization, the protein levels remain constant (B). Three independent experiments were conducted.</p>", "links"=>[], "tags"=>["er", "changes", "nitric", "oxide"], "article_id"=>346010, "categories"=>["Biochemistry", "Biological Sciences", "Microbiology", "Infectious Diseases"], "users"=>["Julien Santi-Rocca", "Sherri Smith", "Christian Weber", "Erika Pineda", "Chung-Chau Hon", "Emma Saavedra", "Alfonso Olivos-García", "Sandrine Rousseau", "Marie-Agnès Dillies", "Jean-Yves Coppee", "Nancy Guillén"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0031777.g003", "stats"=>{"downloads"=>2, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Quantification_of_ER_changes_after_nitric_oxide_treatment_/346010", "title"=>"Quantification of ER changes after nitric oxide treatment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-24 01:40:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/675827"], "description"=>"<p>Genes upregulated encoding metabolism enzymes.</p>", "links"=>[], "tags"=>["upregulated", "encoding", "metabolism"], "article_id"=>346301, "categories"=>["Biochemistry", "Biological Sciences", "Microbiology", "Infectious Diseases"], "users"=>["Julien Santi-Rocca", "Sherri Smith", "Christian Weber", "Erika Pineda", "Chung-Chau Hon", "Emma Saavedra", "Alfonso Olivos-García", "Sandrine Rousseau", "Marie-Agnès Dillies", "Jean-Yves Coppee", "Nancy Guillén"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0031777.t002", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genes_upregulated_encoding_metabolism_enzymes_/346301", "title"=>"Genes upregulated encoding metabolism enzymes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-02-24 01:45:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/675728"], "description"=>"<p>Interval of activities in two (<sup>a</sup>) and four (<sup>b</sup>) independent extracts.</p>*<p>Two-tailed Student's t-test for non-paired samples, p<0.02 versus control amebas. One unit of enzyme activity is 1 µmol of substrate transformed in 1 min.</p><p>Trophozoites were incubated for 1 h in culture medium in the absence or presence of SNP. Clarified extracts were prepared under anaerobic conditions and enzymatic activities were then determined. Remaining activities were determined as the ratio of the results obtained after SNP treatment and for untreated parasites.</p>", "links"=>[], "tags"=>["cysteine", "synthase", "enzyme"], "article_id"=>346211, "categories"=>["Biochemistry", "Biological Sciences", "Microbiology", "Infectious Diseases"], "users"=>["Julien Santi-Rocca", "Sherri Smith", "Christian Weber", "Erika Pineda", "Chung-Chau Hon", "Emma Saavedra", "Alfonso Olivos-García", "Sandrine Rousseau", "Marie-Agnès Dillies", "Jean-Yves Coppee", "Nancy Guillén"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0031777.t004", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Glycolytic_and_cysteine_synthase_enzyme_activities_/346211", "title"=>"Glycolytic and cysteine synthase enzyme activities.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-02-24 01:43:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/675432"], "description"=>"<p>Amoebas were treated with SNP and then fixed and labeled with both anti-FLAG and anti-CRT. Four confocal planes are shown for both untreated (A) and treated (B) samples. GFP-KDEL-FLAG (green), CRT (red), and DAPI (blue). The images show that NO treatment dramatically changes the ER and affects multiple ER markers. The two markers are localized to the same compartment in both treated and untreated samples. Images were analyzed using the iMARIS software to generate 3D models (C). The top panel (C) shows the model of the untreated amoeba from A and the bottom panel depicts the model of the treated amoeba from B. Scale bars equal 30 µm.</p>", "links"=>[], "tags"=>["oxide", "endoplasmic", "reticulum", "gfp-kdel-flag"], "article_id"=>345905, "categories"=>["Biochemistry", "Biological Sciences", "Microbiology", "Infectious Diseases"], "users"=>["Julien Santi-Rocca", "Sherri Smith", "Christian Weber", "Erika Pineda", "Chung-Chau Hon", "Emma Saavedra", "Alfonso Olivos-García", "Sandrine Rousseau", "Marie-Agnès Dillies", "Jean-Yves Coppee", "Nancy Guillén"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0031777.g002", "stats"=>{"downloads"=>2, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Nitric_oxide_treatment_effects_on_E_histolytica_endoplasmic_reticulum_with_respect_to_GFP_KDEL_FLAG_and_calreticulin_/345905", "title"=>"Nitric oxide treatment effects on <i>E. histolytica</i> endoplasmic reticulum with respect to GFP-KDEL-FLAG and calreticulin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-24 01:38:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/675873"], "description"=>"<p>Genes modulated by no linked to redox activities.</p>", "links"=>[], "tags"=>["modulated", "linked", "redox"], "article_id"=>346351, "categories"=>["Biochemistry", "Biological Sciences", "Microbiology", "Infectious Diseases"], "users"=>["Julien Santi-Rocca", "Sherri Smith", "Christian Weber", "Erika Pineda", "Chung-Chau Hon", "Emma Saavedra", "Alfonso Olivos-García", "Sandrine Rousseau", "Marie-Agnès Dillies", "Jean-Yves Coppee", "Nancy Guillén"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0031777.t001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genes_modulated_by_no_linked_to_redox_activities_/346351", "title"=>"Genes modulated by no linked to redox activities.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-02-24 01:45:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/675778"], "description"=>"<p>N = 3 biological replicates.</p><p>I. PFOR <i>in vivo</i> inactivation and <i>in vitro</i> reactivation after treatment of amoebae with SNP. Trophozoites were incubated for 30 or 60 min in culture medium in the absence or presence of SNP. Clarified extracts were prepared under anaerobic conditions and PFOR activity (in U/mg protein) was then determined. PFOR <i>in vitro</i> reactivation was performed in extracts of SNP-treated amoebas by incubating with DTT and Fe<sup>2+</sup> for 1 or 2 h.</p><p>II. PFOR <i>in vitro</i> inactivation by SNP. Soluble fractions from control amoebae were prepared under anaerobic conditions. Aliquots were incubated in the presence of SNP and in the absence or presence of PTIO for 20 min; the remaining PFOR activity was determined as the ratio of the results obtained for the tested condition and for untreated extracts. Two independent amoeba extracts were assayed, both with control PFOR activities of 1.2 U/mg cellular protein.</p>", "links"=>[], "tags"=>["activities"], "article_id"=>346256, "categories"=>["Biochemistry", "Biological Sciences", "Microbiology", "Infectious Diseases"], "users"=>["Julien Santi-Rocca", "Sherri Smith", "Christian Weber", "Erika Pineda", "Chung-Chau Hon", "Emma Saavedra", "Alfonso Olivos-García", "Sandrine Rousseau", "Marie-Agnès Dillies", "Jean-Yves Coppee", "Nancy Guillén"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0031777.t003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PFOR_activities_upon_no_treatment_/346256", "title"=>"PFOR activities upon no treatment.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-02-24 01:44:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/675311"], "description"=>"<p>GFP-KDEL-FLAG transfected amoebas were embedded in a type I collagen matrix treated or not with SNP. One set of images was taken every minutes for an hour. Each stack was acquired using a 0.5 µm Z step. Time points are shown for 0, 25 and 45 min after treatment for both untreated (A) and treated (B) samples. During treatment, the normal organization of the ER begins to change around 25 min after treatment and breaks into vesicles that are found throughout the cytosol by 45 min. Scale bar equals 20 µm.</p>", "links"=>[], "tags"=>["time-lapse", "imaging", "endoplasmic", "reticulum"], "article_id"=>345789, "categories"=>["Biochemistry", "Biological Sciences", "Microbiology", "Infectious Diseases"], "users"=>["Julien Santi-Rocca", "Sherri Smith", "Christian Weber", "Erika Pineda", "Chung-Chau Hon", "Emma Saavedra", "Alfonso Olivos-García", "Sandrine Rousseau", "Marie-Agnès Dillies", "Jean-Yves Coppee", "Nancy Guillén"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0031777.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Live_time_lapse_imaging_of_E_histolytica_endoplasmic_reticulum_during_NO_treatment_/345789", "title"=>"Live time-lapse imaging of <i>E. histolytica</i> endoplasmic reticulum during NO treatment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-24 01:36:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/675667"], "description"=>"<p>PFOR of 120 kDa was revealed upon SDS-PAGE and immunobloting of crude extracts from SNP-treated and control trophozoites (4, 2 and 1×10<sup>4</sup> cells). The loaded amount of proteins for each condition is evidenced by actin (43 kDa) immunodetection on the same western blot. Quantification of signal emission did not reveal differences between the tested conditions in 3 independent experiments.</p>", "links"=>[], "tags"=>["pfor", "levels", "snp"], "article_id"=>346134, "categories"=>["Biochemistry", "Biological Sciences", "Microbiology", "Infectious Diseases"], "users"=>["Julien Santi-Rocca", "Sherri Smith", "Christian Weber", "Erika Pineda", "Chung-Chau Hon", "Emma Saavedra", "Alfonso Olivos-García", "Sandrine Rousseau", "Marie-Agnès Dillies", "Jean-Yves Coppee", "Nancy Guillén"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0031777.g004", "stats"=>{"downloads"=>2, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Immunodetection_of_PFOR_levels_upon_SNP_treatment_/346134", "title"=>"Immunodetection of PFOR levels upon SNP treatment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-02-24 01:42:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/346806", "https://ndownloader.figshare.com/files/346848", "https://ndownloader.figshare.com/files/346888", "https://ndownloader.figshare.com/files/346947", "https://ndownloader.figshare.com/files/347058", "https://ndownloader.figshare.com/files/347139", "https://ndownloader.figshare.com/files/347221"], "description"=>"<div><p>The Endoplasmic Reticulum stores calcium and is a site of protein synthesis and modification. Changes in ER homeostasis lead to stress responses with an activation of the unfolded protein response (UPR). The <em>Entamoeba histolytica</em> endomembrane system is simple compared to those of higher eukaryotes, as a canonical ER is not observed. During amoebiasis, an infection of the human intestine and liver by <em>E. histolytica</em>, nitric oxide (NO) triggers an apoptotic-like event preceded by an impairment of energy production and a loss of important parasite pathogenic features. We address the question of how this ancient eukaryote responds to stress induced by immune components (<em>i.e.</em> NO) and whether stress leads to ER changes and subsequently to an UPR. Gene expression analysis suggested that NO triggers stress responses marked by (i) dramatic up-regulation of <em>hsp</em> genes although a <em>bona fide</em> UPR is absent; (ii) induction of DNA repair and redox gene expression and iii) up-regulation of glycolysis-related gene expression. Enzymology approaches demonstrate that NO directly inhibits glycolysis and enhance cysteine synthase activity. Using live imaging and confocal microscopy we found that NO dramatically provokes extensive ER fragmentation. ER fission in <em>E. histolytica</em> appears as a protective response against stress, as it has been recently proposed for neuron self-defense during neurologic disorders. Chronic ER stress is also involved in metabolic diseases including diabetes, where NO production reduces ER calcium levels and activates cell death. Our data highlighted unique cellular responses of interest to understand the mechanisms of parasite death during amoebiasis.</p> </div>", "links"=>[], "tags"=>["endoplasmic", "reticulum", "stress-sensing", "activated", "nitric", "oxide"], "article_id"=>128563, "categories"=>["Biochemistry", "Cancer", "Biological Sciences", "Microbiology"], "users"=>["Julien Santi-Rocca", "Sherri Smith", "Christian Weber", "Erika Pineda", "Chung-Chau Hon", "Emma Saavedra", "Alfonso Olivos-García", "Sandrine Rousseau", "Marie-Agnès Dillies", "Jean-Yves Coppee", "Nancy Guillén"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0031777.s001", "https://dx.doi.org/10.1371/journal.pone.0031777.s002", "https://dx.doi.org/10.1371/journal.pone.0031777.s003", "https://dx.doi.org/10.1371/journal.pone.0031777.s004", "https://dx.doi.org/10.1371/journal.pone.0031777.s005", "https://dx.doi.org/10.1371/journal.pone.0031777.s006", "https://dx.doi.org/10.1371/journal.pone.0031777.s007"], "stats"=>{"downloads"=>4, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Endoplasmic_Reticulum_Stress_Sensing_Mechanism_Is_Activated_in_Entamoeba_histolytica_upon_Treatment_with_Nitric_Oxide/128563", "title"=>"Endoplasmic Reticulum Stress-Sensing Mechanism Is Activated in <em>Entamoeba histolytica</em> upon Treatment with Nitric Oxide", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-02-24 02:22:43"}

PMC Usage Stats | Further Information

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Relative Metric

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