Cytosolic Peroxidases Protect the Lysosome of Bloodstream African Trypanosomes from Iron-Mediated Membrane Damage
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{"title"=>"Cytosolic Peroxidases Protect the Lysosome of Bloodstream African Trypanosomes from Iron-Mediated Membrane Damage", "type"=>"journal", "authors"=>[{"first_name"=>"Corinna", "last_name"=>"Hiller", "scopus_author_id"=>"55623685200"}, {"first_name"=>"Amrei", "last_name"=>"Nissen", "scopus_author_id"=>"56177749100"}, {"first_name"=>"Diego", "last_name"=>"Benítez", "scopus_author_id"=>"56683181300"}, {"first_name"=>"Marcelo A.", "last_name"=>"Comini", "scopus_author_id"=>"6603435767"}, {"first_name"=>"R. Luise", "last_name"=>"Krauth-Siegel", "scopus_author_id"=>"55078633200"}], "year"=>2014, "source"=>"PLoS Pathogens", "identifiers"=>{"pui"=>"373162943", "doi"=>"10.1371/journal.ppat.1004075", "isbn"=>"10.1371/journal.ppat.1004075", "pmid"=>"24722489", "issn"=>"15537374", "scopus"=>"2-s2.0-84901373130", "sgr"=>"84901373130"}, "id"=>"8539af82-e2a2-3ceb-a40f-81e2bc0b453e", "abstract"=>"African trypanosomes express three virtually identical non-selenium glutathione peroxidase (Px)-type enzymes which preferably detoxify lipid-derived hydroperoxides. As shown previously, bloodstream Trypanosoma brucei lacking the mitochondrial Px III display only a weak and transient proliferation defect whereas parasites that lack the cytosolic Px I and Px II undergo extremely fast lipid peroxidation and cell lysis. The phenotype can completely be rescued by supplementing the medium with the α-tocopherol derivative Trolox. The mechanism underlying the rapid cell death remained however elusive. Here we show that the lysosome is the origin of the cellular injury. Feeding the px I-II knockout parasites with Alexa Fluor-conjugated dextran or LysoTracker in the presence of Trolox yielded a discrete lysosomal staining. Yet upon withdrawal of the antioxidant, the signal became progressively spread over the whole cell body and was completely lost, respectively. T. brucei acquire iron by endocytosis of host transferrin. Supplementing the medium with iron or transferrin induced, whereas the iron chelator deferoxamine and apo-transferrin attenuated lysis of the px I-II knockout cells. Immunofluorescence microscopy with MitoTracker and antibodies against the lysosomal marker protein p67 revealed that disintegration of the lysosome precedes mitochondrial damage. In vivo experiments confirmed the negligible role of the mitochondrial peroxidase: Mice infected with px III knockout cells displayed only a slightly delayed disease development compared to wild-type parasites. Our data demonstrate that in bloodstream African trypanosomes, the lysosome, not the mitochondrion, is the primary site of oxidative damage and cytosolic trypanothione/tryparedoxin-dependent peroxidases protect the lysosome from iron-induced membrane peroxidation. This process appears to be closely linked to the high endocytic rate and distinct iron acquisition mechanisms of the infective stage of T. brucei. The respective knockout of the cytosolic px I-II in the procyclic insect form resulted in cells that were fully viable in Trolox-free medium.", "link"=>"http://www.mendeley.com/research/cytosolic-peroxidases-protect-lysosome-bloodstream-african-trypanosomes-ironmediated-membrane-damage", "reader_count"=>30, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Researcher"=>11, "Student > Ph. D. Student"=>8, "Student > Master"=>3, "Student > Bachelor"=>1, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>1, "Researcher"=>11, "Student > Ph. D. Student"=>8, "Student > Master"=>3, "Student > Bachelor"=>1, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>6, "Agricultural and Biological Sciences"=>13, "Medicine and Dentistry"=>2, "Chemistry"=>2, "Computer Science"=>1, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Chemistry"=>{"Chemistry"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>13}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Czech Republic"=>1, "United Kingdom"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1458668"], "description"=>"<p><b>A.</b> The mutant parasites were incubated for up to 5.5°C in standard medium ±100 µM Trolox in the presence and absence of 100 µM Fe<sup>3+</sup>. WT cells behaved like the mutant cells in the presence of Trolox. <b>B.</b> The <i>px I–II<sup>−/−</sup></i> cells were incubated for 5 h at 22°C and then cultured overnight at 37°C in medium ±100 µM Trolox in the presence and absence of 100 µM deferoxamine (dfx). WT behaved like the mutant cells in the presence of Trolox. <b>C.</b> The <i>px I–II<sup>−/−</sup></i> cells were incubated for 5 h at 19°C and then cultured overnight at 37°C in medium ±10% FCS and/or 100 µM Trolox in the presence and absence of 100 µM Fe<sup>3+</sup>. The behavior of WT cells in the absence of FCS was identical to that of the mutant cells. At the different time points, living cells were counted. The values represent the mean ± SD of three independent experiments.</p>", "links"=>[], "tags"=>["Biochemistry", "enzymology", "Enzyme chemistry", "Enzyme metabolism", "cell biology", "Cell processes", "Cellular stress responses", "Molecular cell biology", "microbiology", "organisms", "protozoans", "Parasitic protozoans", "Trypanosoma", "Parasitology", "lysis", "bs"], "article_id"=>994394, "categories"=>["Biological Sciences"], "users"=>["Corinna Hiller", "Amrei Nissen", "Diego Benítez", "Marcelo A. Comini", "R. Luise Krauth-Siegel"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004075.g003", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Exogenous_iron_promotes_lysis_of_the_px_I_8211_II_8722_8722_BS_cells_/994394", "title"=>"Exogenous iron promotes lysis of the <i>px I–II</i><sup>−/−</sup> BS cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-10 02:53:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1458695", "https://ndownloader.figshare.com/files/1458696", "https://ndownloader.figshare.com/files/1458697", "https://ndownloader.figshare.com/files/1458698", "https://ndownloader.figshare.com/files/1458699", "https://ndownloader.figshare.com/files/1458700"], "description"=>"<div><p>African trypanosomes express three virtually identical non-selenium glutathione peroxidase (Px)-type enzymes which preferably detoxify lipid-derived hydroperoxides. As shown previously, bloodstream <i>Trypanosoma brucei</i> lacking the mitochondrial Px III display only a weak and transient proliferation defect whereas parasites that lack the cytosolic Px I and Px II undergo extremely fast lipid peroxidation and cell lysis. The phenotype can completely be rescued by supplementing the medium with the α-tocopherol derivative Trolox. The mechanism underlying the rapid cell death remained however elusive. Here we show that the lysosome is the origin of the cellular injury. Feeding the <i>px I–II</i> knockout parasites with Alexa Fluor-conjugated dextran or LysoTracker in the presence of Trolox yielded a discrete lysosomal staining. Yet upon withdrawal of the antioxidant, the signal became progressively spread over the whole cell body and was completely lost, respectively. <i>T. brucei</i> acquire iron by endocytosis of host transferrin. Supplementing the medium with iron or transferrin induced, whereas the iron chelator deferoxamine and apo-transferrin attenuated lysis of the <i>px I–II</i> knockout cells. Immunofluorescence microscopy with MitoTracker and antibodies against the lysosomal marker protein p67 revealed that disintegration of the lysosome precedes mitochondrial damage. <i>In vivo</i> experiments confirmed the negligible role of the mitochondrial peroxidase: Mice infected with <i>px III</i> knockout cells displayed only a slightly delayed disease development compared to wild-type parasites. Our data demonstrate that in bloodstream African trypanosomes, the lysosome, not the mitochondrion, is the primary site of oxidative damage and cytosolic trypanothione/tryparedoxin-dependent peroxidases protect the lysosome from iron-induced membrane peroxidation. This process appears to be closely linked to the high endocytic rate and distinct iron acquisition mechanisms of the infective stage of <i>T. brucei</i>. The respective knockout of the cytosolic <i>px I–II</i> in the procyclic insect form resulted in cells that were fully viable in Trolox-free medium.</p></div>", "links"=>[], "tags"=>["Biochemistry", "enzymology", "Enzyme chemistry", "Enzyme metabolism", "cell biology", "Cell processes", "Cellular stress responses", "Molecular cell biology", "microbiology", "organisms", "protozoans", "Parasitic protozoans", "Trypanosoma", "Parasitology", "peroxidases", "lysosome", "bloodstream", "african", "trypanosomes", "iron-mediated", "membrane"], "article_id"=>994421, "categories"=>["Biological Sciences"], "users"=>["Corinna Hiller", "Amrei Nissen", "Diego Benítez", "Marcelo A. Comini", "R. Luise Krauth-Siegel"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1004075.s001", "https://dx.doi.org/10.1371/journal.ppat.1004075.s002", "https://dx.doi.org/10.1371/journal.ppat.1004075.s003", "https://dx.doi.org/10.1371/journal.ppat.1004075.s004", "https://dx.doi.org/10.1371/journal.ppat.1004075.s005", "https://dx.doi.org/10.1371/journal.ppat.1004075.s006"], "stats"=>{"downloads"=>7, "page_views"=>25, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cytosolic_Peroxidases_Protect_the_Lysosome_of_Bloodstream_African_Trypanosomes_from_Iron_Mediated_Membrane_Damage_/994421", "title"=>"Cytosolic Peroxidases Protect the Lysosome of Bloodstream African Trypanosomes from Iron-Mediated Membrane Damage", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-04-10 02:53:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1458676"], "description"=>"<p>The <i>px I–II</i><sup>−/−</sup> BS cells were kept for the indicated times at 37°C in medium ± Trolox and then subjected to immunofluorescence analysis. <b>A.</b> MitoTracker staining (left), overlay of the signals for MitoTracker (red), p67 (green), and DAPI (blue) (middle), and phase contrast images (right). <b>B.</b> Quantitative analysis of the staining pattern of the cells (for details, see text). The phenotypes visible in the respective pictures in (<b>A</b>) are highlighted by bold numbers. For each time point, at least 194 cells were inspected. The data are representative of two independent sets of experiments giving very similar results. (Scale bar: 10 µm).</p>", "links"=>[], "tags"=>["Biochemistry", "enzymology", "Enzyme chemistry", "Enzyme metabolism", "cell biology", "Cell processes", "Cellular stress responses", "Molecular cell biology", "microbiology", "organisms", "protozoans", "Parasitic protozoans", "Trypanosoma", "Parasitology", "disintegration", "precedes"], "article_id"=>994402, "categories"=>["Biological Sciences"], "users"=>["Corinna Hiller", "Amrei Nissen", "Diego Benítez", "Marcelo A. Comini", "R. Luise Krauth-Siegel"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004075.g005", "stats"=>{"downloads"=>0, "page_views"=>30, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lysosomal_disintegration_precedes_damage_of_the_mitochondrion_/994402", "title"=>"Lysosomal disintegration precedes damage of the mitochondrion.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-10 02:53:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1458670"], "description"=>"<p>The mutant cells were incubated <b>A.</b> for 4 h at RT in standard medium ±100 µM Trolox in the presence and absence of 25 µM holo-transferrin (holo-TF), <b>B.</b> for 6 h at RT and then cultured overnight at 37°C in medium ±100 µM Trolox in the presence and absence of 320 µM apo-transferrin (apo-TF), <b>C.</b> for 5 h at RT followed by overnight cultivation at 37°C in standard medium as well as in FCS-free medium ±100 µM Trolox in the presence and absence of 5 µM and 25 µM holo-TF, and <b>D.</b> for 5 h at 20°C in standard medium as well as in transferrin-depleted medium (-TF medium) ±100 µM Trolox in the presence and absence of 5 µM and 25 µM holo-TF. The values represent the mean ± SD of three independent experiments.</p>", "links"=>[], "tags"=>["Biochemistry", "enzymology", "Enzyme chemistry", "Enzyme metabolism", "cell biology", "Cell processes", "Cellular stress responses", "Molecular cell biology", "microbiology", "organisms", "protozoans", "Parasitic protozoans", "Trypanosoma", "Parasitology", "apo-transferrin", "slows", "lysis", "bs"], "article_id"=>994396, "categories"=>["Biological Sciences"], "users"=>["Corinna Hiller", "Amrei Nissen", "Diego Benítez", "Marcelo A. Comini", "R. Luise Krauth-Siegel"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004075.g004", "stats"=>{"downloads"=>1, "page_views"=>24, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Holo_transferrin_induces_whereas_apo_transferrin_slows_down_lysis_of_the_px_I_8211_II_8722_8722_BS_parasites_/994396", "title"=>"Holo-transferrin induces, whereas apo-transferrin slows down lysis of the <i>px I–II</i><sup>−/−</sup> BS parasites.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-10 02:53:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1458667"], "description"=>"<p><b>A.</b> Living parasites were fed at 37°C with Alexa Fluor-488 conjugated dextran and then kept at RT in medium with (+) or without (−) 100 µM Trolox as outlined under <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004075#s4\" target=\"_blank\">Materials and Methods</a>. On the left site, representative cells for the three different phenotypes observed in the remaining intact and fluorescent parasites are shown. The pictures were taken from cells incubated (1) 1 h, + Trolox, (2) 1 and 2 h, - Trolox, and (3) 2 h, - Trolox. On the right site, the quantitative analysis is provided. At each time point, ≥60 parasites were analyzed in three independent experiments and the mean ± SD was calculated. <b>B.</b> LysoTracker Green staining of living parasites incubated for the indicated times at 37°C in the presence or absence of Trolox. <b>C.</b> Immunofluorescence analysis of cells stained with antibodies against p67 (green) and DAPI (blue) to visualize nuclear (large dot) and kinetoplast (small dot) DNA (upper panel) and the corresponding phase contrast pictures (lower panel). At each time point, the p67 signal of at least 130 parasites was analyzed in each of three independent experiments and the mean ± SD was calculated (below). (Scale bar: 10 µm).</p>", "links"=>[], "tags"=>["Biochemistry", "enzymology", "Enzyme chemistry", "Enzyme metabolism", "cell biology", "Cell processes", "Cellular stress responses", "Molecular cell biology", "microbiology", "organisms", "protozoans", "Parasitic protozoans", "Trypanosoma", "Parasitology", "trolox", "morphological", "bs"], "article_id"=>994393, "categories"=>["Biological Sciences"], "users"=>["Corinna Hiller", "Amrei Nissen", "Diego Benítez", "Marcelo A. Comini", "R. Luise Krauth-Siegel"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004075.g002", "stats"=>{"downloads"=>0, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Withdrawal_of_Trolox_results_in_morphological_changes_of_the_px_I_8211_II_8722_8722_BS_cells_/994393", "title"=>"Withdrawal of Trolox results in morphological changes of the <i>px I–II</i><sup>−/−</sup> BS cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-10 02:53:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1458665"], "description"=>"<p>The <i>px I–II<sup>−/−</sup></i> parasites were seeded at a density of 5–9×10<sup>5</sup> cells/ml in standard HMI-9 medium (which contains 10% FCS) supplemented ±100 µM Trolox. The cells were incubated at 37°C, 21°C, and 9°C, respectively. At the indicated time points, living cells were counted. The values represent the mean ± SD of three independent experiments.</p>", "links"=>[], "tags"=>["Biochemistry", "enzymology", "Enzyme chemistry", "Enzyme metabolism", "cell biology", "Cell processes", "Cellular stress responses", "Molecular cell biology", "microbiology", "organisms", "protozoans", "Parasitic protozoans", "Trypanosoma", "Parasitology", "bs", "cells"], "article_id"=>994391, "categories"=>["Biological Sciences"], "users"=>["Corinna Hiller", "Amrei Nissen", "Diego Benítez", "Marcelo A. Comini", "R. Luise Krauth-Siegel"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004075.g001", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lysis_of_the_px_I_8211_II_8722_8722_BS_cells_is_temperature_dependent_/994391", "title"=>"Lysis of the <i>px I–II</i><sup>−/−</sup> BS cells is temperature-dependent.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-10 02:53:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/1458679"], "description"=>"<p><b>A.</b> and <b>B.</b> Female BALB/cJ mice (n = 6/group) were infected intraperitoneally with 10<sup>4</sup> WT parasites or <i>px III</i><sup>−/−</sup> cells that, prior to infection, had been cultivated in medium supplemented with 100 µM Trolox, and <b>C.</b> and <b>D.</b> in medium without Trolox. <b>E.</b> and <b>F.</b> Mice (n = 3/group) were inoculated with <i>px III</i><sup>−/−</sup> and WT parasites isolated from infected animals (for details see <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004075#s4\" target=\"_blank\">Materials and Methods</a>). <b>A.</b>, <b>C.</b>, and <b>E.</b> Kaplan-Meyer plots for animal survival, <b>B.</b>, <b>D.</b>, and <b>F.</b> Average parasite load in blood samples taken from the animals at the indicated times. All data are the mean value ± SD.</p>", "links"=>[], "tags"=>["Biochemistry", "enzymology", "Enzyme chemistry", "Enzyme metabolism", "cell biology", "Cell processes", "Cellular stress responses", "Molecular cell biology", "microbiology", "organisms", "protozoans", "Parasitic protozoans", "Trypanosoma", "Parasitology", "wt"], "article_id"=>994405, "categories"=>["Biological Sciences"], "users"=>["Corinna Hiller", "Amrei Nissen", "Diego Benítez", "Marcelo A. Comini", "R. Luise Krauth-Siegel"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004075.g006", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Infectivity_of_px_III_8722_8722_and_WT_T_brucei_/994405", "title"=>"Infectivity of <i>px III</i><sup>−/−</sup> and WT <i>T. brucei</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-04-10 02:53:36"}

PMC Usage Stats | Further Information

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Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Biochemistry", "average_usage"=>[282]}, {"subject_area"=>"/Biology and life sciences/Cell biology", "average_usage"=>[286]}, {"subject_area"=>"/Medicine and health sciences/Parasitic diseases", "average_usage"=>[418, 848]}]}
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