Host Reticulocytes Provide Metabolic Reservoirs That Can Be Exploited by Malaria Parasites
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{"title"=>"Host Reticulocytes Provide Metabolic Reservoirs That Can Be Exploited by Malaria Parasites", "type"=>"journal", "authors"=>[{"first_name"=>"Anubhav", "last_name"=>"Srivastava", "scopus_author_id"=>"55214921900"}, {"first_name"=>"Darren J.", "last_name"=>"Creek", "scopus_author_id"=>"55489940500"}, {"first_name"=>"Krystal J.", "last_name"=>"Evans", "scopus_author_id"=>"8255601300"}, {"first_name"=>"David", "last_name"=>"De Souza", "scopus_author_id"=>"7005826359"}, {"first_name"=>"Louis", "last_name"=>"Schofield", "scopus_author_id"=>"7006728410"}, {"first_name"=>"Sylke", "last_name"=>"Müller", "scopus_author_id"=>"25223535200"}, {"first_name"=>"Michael P.", "last_name"=>"Barrett", "scopus_author_id"=>"7202188382"}, {"first_name"=>"Malcolm J.", "last_name"=>"McConville", "scopus_author_id"=>"7004657308"}, {"first_name"=>"Andrew P.", "last_name"=>"Waters", "scopus_author_id"=>"7101758887"}], "year"=>2015, "source"=>"PLoS Pathogens", "identifiers"=>{"pmid"=>"26042734", "sgr"=>"84936791319", "doi"=>"10.1371/journal.ppat.1004882", "scopus"=>"2-s2.0-84936791319", "pui"=>"605161971", "issn"=>"15537374"}, "id"=>"f511c533-6939-38c4-aa93-82d689cdd6e6", "abstract"=>"Human malaria parasites proliferate in different erythroid cell types during infection. Whilst Plasmodium vivax exhibits a strong preference for immature reticulocytes, the more pathogenic P. falciparum primarily infects mature erythrocytes. In order to assess if these two cell types offer different growth conditions and relate them to parasite preference, we compared the metabolomes of human and rodent reticulocytes with those of their mature erythrocyte counterparts. Reticulocytes were found to have a more complex, enriched metabolic profile than mature erythrocytes and a higher level of metabolic overlap between reticulocyte resident parasite stages and their host cell. This redundancy was assessed by generating a panel of mutants of the rodent malaria parasite P. berghei with defects in intermediary carbon metabolism (ICM) and pyrimidine biosynthesis known to be important for P. falciparum growth and survival in vitro in mature erythrocytes. P. berghei ICM mutants (pbpepc-, phosphoenolpyruvate carboxylase and pbmdh-, malate dehydrogenase) multiplied in reticulocytes and committed to sexual development like wild type parasites. However, P. berghei pyrimidine biosynthesis mutants (pboprt-, orotate phosphoribosyltransferase and pbompdc-, orotidine 5'-monophosphate decarboxylase) were restricted to growth in the youngest forms of reticulocytes and had a severe slow growth phenotype in part resulting from reduced merozoite production. The pbpepc-, pboprt- and pbompdc- mutants retained virulence in mice implying that malaria parasites can partially salvage pyrimidines but failed to complete differentiation to various stages in mosquitoes. These findings suggest that species-specific differences in Plasmodium host cell tropism result in marked differences in the necessity for parasite intrinsic metabolism. These data have implications for drug design when targeting mature erythrocyte or reticulocyte resident parasites.", "link"=>"http://www.mendeley.com/research/host-reticulocytes-provide-metabolic-reservoirs-exploited-malaria-parasites", "reader_count"=>62, "reader_count_by_academic_status"=>{"Unspecified"=>3, "Professor > Associate Professor"=>2, "Researcher"=>11, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>17, "Student > Postgraduate"=>5, "Student > Master"=>12, "Other"=>4, "Student > Bachelor"=>4, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>3, "Professor > Associate Professor"=>2, "Researcher"=>11, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>17, "Student > Postgraduate"=>5, "Student > Master"=>12, "Other"=>4, "Student > Bachelor"=>4, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>6, "Engineering"=>1, "Environmental Science"=>2, "Biochemistry, Genetics and Molecular Biology"=>9, "Agricultural and Biological Sciences"=>28, "Medicine and Dentistry"=>7, "Chemistry"=>2, "Immunology and Microbiology"=>5, "Economics, Econometrics and Finance"=>1, "Nursing and Health Professions"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>7}, "Chemistry"=>{"Chemistry"=>2}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>5}, "Economics, Econometrics and Finance"=>{"Economics, Econometrics and Finance"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>28}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>9}, "Unspecified"=>{"Unspecified"=>6}, "Environmental Science"=>{"Environmental Science"=>2}}, "reader_count_by_country"=>{"Brazil"=>1, "United Kingdom"=>2, "India"=>1}, "group_count"=>3}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/2096317", "https://ndownloader.figshare.com/files/2096318", "https://ndownloader.figshare.com/files/2096319", "https://ndownloader.figshare.com/files/2096320", "https://ndownloader.figshare.com/files/2096321"], "description"=>"<div><p>Human malaria parasites proliferate in different erythroid cell types during infection. Whilst <i>Plasmodium vivax</i> exhibits a strong preference for immature reticulocytes, the more pathogenic <i>P</i>. <i>falciparum</i> primarily infects mature erythrocytes. In order to assess if these two cell types offer different growth conditions and relate them to parasite preference, we compared the metabolomes of human and rodent reticulocytes with those of their mature erythrocyte counterparts. Reticulocytes were found to have a more complex, enriched metabolic profile than mature erythrocytes and a higher level of metabolic overlap between reticulocyte resident parasite stages and their host cell. This redundancy was assessed by generating a panel of mutants of the rodent malaria parasite <i>P</i>. <i>berghei</i> with defects in intermediary carbon metabolism (ICM) and pyrimidine biosynthesis known to be important for <i>P</i>. <i>falciparum</i> growth and survival <i>in vitro</i> in mature erythrocytes. <i>P</i>. <i>berghei</i> ICM mutants (<i>pbpepc<sup>-</sup></i>, phosphoenolpyruvate carboxylase and <i>pbmdh<sup>-</sup></i>, malate dehydrogenase) multiplied in reticulocytes and committed to sexual development like wild type parasites. However, <i>P</i>. <i>berghei</i> pyrimidine biosynthesis mutants (<i>pboprt<sup>-</sup></i>, orotate phosphoribosyltransferase and <i>pbompdc<sup>-</sup></i>, orotidine 5′-monophosphate decarboxylase) were restricted to growth in the youngest forms of reticulocytes and had a severe slow growth phenotype in part resulting from reduced merozoite production. The <i>pbpepc<sup>-</sup></i>, <i>pboprt<sup>-</sup></i> and <i>pbompdc<sup>-</sup></i> mutants retained virulence in mice implying that malaria parasites can partially salvage pyrimidines but failed to complete differentiation to various stages in mosquitoes. These findings suggest that species-specific differences in <i>Plasmodium</i> host cell tropism result in marked differences in the necessity for parasite intrinsic metabolism. These data have implications for drug design when targeting mature erythrocyte or reticulocyte resident parasites.</p></div>", "links"=>[], "tags"=>["growth conditions", "malaria parasites", "reticulocyte resident parasite stages", "pyrimidine biosynthesis", "rodent reticulocytes", "Whilst Plasmodium vivax exhibits", "intermediary carbon metabolism", "host cell", "berghei pyrimidine biosynthesis mutants", "erythrocyte counterparts", "reticulocyte resident parasites", "host Reticulocytes", "type parasites", "drug design", "falciparum growth", "Malaria Parasites Human malaria parasites", "Plasmodium host cell tropism result", "cell types offer", "erythroid cell types", "Metabolic Reservoirs", "merozoite production", "growth phenotype", "parasite preference", "rodent malaria parasite P", "berghei ICM mutants"], "article_id"=>1437178, "categories"=>["Biological Sciences"], "users"=>["Anubhav Srivastava", "Darren J. Creek", "Krystal J. Evans", "David De Souza", "Louis Schofield", "Sylke Müller", "Michael P. Barrett", "Malcolm J. McConville", "Andrew P. Waters"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1004882.s001", "https://dx.doi.org/10.1371/journal.ppat.1004882.s002", "https://dx.doi.org/10.1371/journal.ppat.1004882.s003", "https://dx.doi.org/10.1371/journal.ppat.1004882.s004", "https://dx.doi.org/10.1371/journal.ppat.1004882.s005"], "stats"=>{"downloads"=>6, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Host_Reticulocytes_Provide_Metabolic_Reservoirs_That_Can_Be_Exploited_by_Malaria_Parasites_/1437178", "title"=>"Host Reticulocytes Provide Metabolic Reservoirs That Can Be Exploited by Malaria Parasites", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2015-06-04 03:33:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/2096308"], "description"=>"<p>A. Top panel: Fold change of relative levels (peak intensities) of metabolites of carbon metabolism in rodent REP compared to wtEP. Dotted line indicates no change and error bars indicate R.S.D. (Relative Standard Deviation) of peak intensities from reticulocyte samples multiplied to the fold change values from n = 3 independent biological replicates. Bottom panel: Schematic representation of intermediary carbon metabolism (ICM) in <i>Plasmodium</i> cytosol. Genes marked with (✓) were deleted in <i>P</i>. <i>berghei</i> blood stages and the ones marked with (✕) could not be deleted even after repeated attempts. <i>pepc</i>: Phosphoenolpyruvate Carboxylase (PBANKA_101790), <i>mdh</i>: Malate Dehydrogenase (PBANKA_111770), <i>aat</i>: Aspartate Amino Transferase (PBANKA_030230). B. Top panel: Fold change of relative levels (peak intensities) of metabolites of pyrimidine biosynthesis in rodent REP compared to wtEP. Dotted line indicates no change and error bars indicate R.S.D. (Relative Standard Deviation) of peak intensities from reticulocyte samples multiplied to the fold change values from n = 3 independent biological replicates. Bottom panel: Schematic representation of pyrimidine biosynthesis pathway in <i>Plasmodium</i> cytosol. Genes marked with (✓) were deleted in <i>P</i>. <i>berghei</i> blood stages and the ones marked with (✕) could not be deleted even after repeated attempts. <i>cpsII</i>: Carbamoyl phosphate synthetase II (PBANKA_140670), <i>act</i>: Aspartate carbamoyltransferase (PBANKA_135770), <i>dhoase</i>: Dihydroorotase (PBANKA_133610), <i>dhodh</i>: Dihydroorotate dehydrogenase (PBANKA_010210), <i>oprt</i>: Orotate phosphoribosyltransferase (PBANKA_111240), <i>ompdc</i>: Orotidine 5′-monophosphate decarboxylase (PBANKA_050740). (Also see Fig B in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004882#ppat.1004882.s001\" target=\"_blank\">S1 Text</a> for gene deletion strategy and confirmation)</p>", "links"=>[], "tags"=>["growth conditions", "malaria parasites", "reticulocyte resident parasite stages", "pyrimidine biosynthesis", "rodent reticulocytes", "Whilst Plasmodium vivax exhibits", "intermediary carbon metabolism", "host cell", "berghei pyrimidine biosynthesis mutants", "erythrocyte counterparts", "reticulocyte resident parasites", "host Reticulocytes", "type parasites", "drug design", "falciparum growth", "Malaria Parasites Human malaria parasites", "Plasmodium host cell tropism result", "cell types offer", "erythroid cell types", "Metabolic Reservoirs", "merozoite production", "growth phenotype", "parasite preference", "rodent malaria parasite P", "berghei ICM mutants"], "article_id"=>1437172, "categories"=>["Biological Sciences"], "users"=>["Anubhav Srivastava", "Darren J. Creek", "Krystal J. Evans", "David De Souza", "Louis Schofield", "Sylke Müller", "Michael P. Barrett", "Malcolm J. McConville", "Andrew P. Waters"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004882.g002", "stats"=>{"downloads"=>0, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Metabolites_of_intermediary_carbon_metabolism_ICM_and_pyrimidine_biosynthesis_are_up_regulated_in_reticulocytes_/1437172", "title"=>"Metabolites of intermediary carbon metabolism (ICM) and pyrimidine biosynthesis are up-regulated in reticulocytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-04 03:33:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/2096314"], "description"=>"<p>A. <i>in vitro</i> ookinete conversion of mutant <i>P</i>. <i>berghei</i> parasites as compared to wt. The error is given as the S.D. of n = 3 independent biological replicates. P-values: **p<0.005, ***p<0.0005, unpaired two tailed t-test. B. <i>in vitro</i> ookinete conversion assay to measure fertility of mutant <i>P</i>. <i>berghei</i> gametocytes. Fertility of mutant <i>P</i>. <i>berghei</i> gametocytes was analysed by their capacity to form ookinetes by crossing gametes with RMgm-348 (Pb270, <i>p47</i><sup><i>-</i></sup>) which produces viable male gametes but non-viable female gametes and RMgm-15 (Pb137, <i>p48/45</i><sup><i>-</i></sup>) which produces viable female gametes but non-viable male gametes. The error is given as the S.D. of n = 2 independent biological replicates. P-values: *p<0.05, **p<0.005, unpaired two tailed t-test. C. Number of mature oocysts at day 14 post infected blood feed in mosquito mid guts. n = 40 mosquitoes cumulative of two independent biological replicates. ***p<0.0005, unpaired two tailed t-test. D. Infection prevalence (percentage of observed mosquitoes found to be infected) and infection load (median of number of oocysts found per mosquito) in mutant <i>P</i>.<i>berghei</i> parasites compared to wt.</p>", "links"=>[], "tags"=>["growth conditions", "malaria parasites", "reticulocyte resident parasite stages", "pyrimidine biosynthesis", "rodent reticulocytes", "Whilst Plasmodium vivax exhibits", "intermediary carbon metabolism", "host cell", "berghei pyrimidine biosynthesis mutants", "erythrocyte counterparts", "reticulocyte resident parasites", "host Reticulocytes", "type parasites", "drug design", "falciparum growth", "Malaria Parasites Human malaria parasites", "Plasmodium host cell tropism result", "cell types offer", "erythroid cell types", "Metabolic Reservoirs", "merozoite production", "growth phenotype", "parasite preference", "rodent malaria parasite P", "berghei ICM mutants"], "article_id"=>1437175, "categories"=>["Biological Sciences"], "users"=>["Anubhav Srivastava", "Darren J. Creek", "Krystal J. Evans", "David De Souza", "Louis Schofield", "Sylke Müller", "Michael P. Barrett", "Malcolm J. McConville", "Andrew P. Waters"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004882.g004", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mosquito_stage_development_of_P_berghei_mutant_parasites_also_see_Fig_D_in_S1_Text_/1437175", "title"=>"Mosquito stage development of <i>P</i>. <i>berghei</i> mutant parasites (also see Fig D in S1 Text).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-04 03:33:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/2096315"], "description"=>"<p>Error bars indicate S.D. from n = 3 biological replicates.</p>", "links"=>[], "tags"=>["growth conditions", "malaria parasites", "reticulocyte resident parasite stages", "pyrimidine biosynthesis", "rodent reticulocytes", "Whilst Plasmodium vivax exhibits", "intermediary carbon metabolism", "host cell", "berghei pyrimidine biosynthesis mutants", "erythrocyte counterparts", "reticulocyte resident parasites", "host Reticulocytes", "type parasites", "drug design", "falciparum growth", "Malaria Parasites Human malaria parasites", "Plasmodium host cell tropism result", "cell types offer", "erythroid cell types", "Metabolic Reservoirs", "merozoite production", "growth phenotype", "parasite preference", "rodent malaria parasite P", "berghei ICM mutants"], "article_id"=>1437176, "categories"=>["Biological Sciences"], "users"=>["Anubhav Srivastava", "Darren J. Creek", "Krystal J. Evans", "David De Souza", "Louis Schofield", "Sylke Müller", "Michael P. Barrett", "Malcolm J. McConville", "Andrew P. Waters"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004882.g005", "stats"=>{"downloads"=>0, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_P_berghei_and_P_falciparum_inhibition_by_dihydroartemisinin_DHA_and_5_fluoroorotic_acid_5FOA_in_vitro_/1437176", "title"=>"<i>P</i>. <i>berghei</i> and <i>P</i>. <i>falciparum</i> inhibition by dihydroartemisinin (DHA) and 5-fluoroorotic acid (5FOA) <i>in vitro</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-04 03:33:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/2096313"], "description"=>"<p>A. <i>in vivo</i> growth assay of mutants in mixed infections in competition with wild type parasites over 12 days. Coloured lines represent non-linear fit of percentage of mutant parasites in total parasite population. Data representative of n = 3 independent biological replicates. (Also see Fig C- A, B and C in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004882#ppat.1004882.s001\" target=\"_blank\">S1 Text</a>.) B. Lethality experiment in C57/B6 mice by wt and mutant <i>P</i>. <i>berghei</i> parasites. 10<sup>4</sup> parasites were injected intra-peritoneally in mice (n = 5) on day 0 and they were monitored for 21 days. The mice were culled humanely when they showed severe malaria pathology. All mutant parasites were found to be lethal to mice. C. Gametocyte conversions during blood stages in mutant <i>P</i>. <i>berghei</i> parasites over 5 days post infection. Data from 2 independent observed gametocyte conversion experiments are shown ± S.D. Gametocyte conversion was observed using a wt parent line which expresses GFP in male gametocytes and RFP in female gametocytes (RMgm-164). <i>P</i>. <i>berghei</i> mutants were generated in the same genetic background and analysed using FACS determining the number of gametocytes in infected blood. P-values: *p<0.05, **p<0.005, ***p<0.0005, paired two tailed t-test. D. Exflagellation (male gamete formation) in mutant <i>P</i>. <i>berghei</i> parasites normalised to wt in <i>in vitro</i> activation assay. The error is given as the SD of n = 3 independent biological replicates. P-values: **p<0.005, ***p<0.0005, paired two tailed t-test. E. Determination of DNA content of male gametocytes over 20 minutes post activation by FACS analysis in mutant <i>P</i>. <i>berghei</i> parasites normalised to wt. DNA content was determined in Hoechst-33258-stained MACS purified gametocytes. Before activation (0minutes) males show low DNA content with increasing amounts post activation reaching maximum levels between 8 to 12 minutes in wt. Data from 3 independent biological replicates are given ± S.D. P-values: **p<0.005, ***p<0.0005, unpaired two tailed t-test (also see Fig C- D in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004882#ppat.1004882.s001\" target=\"_blank\">S1 Text</a>).</p>", "links"=>[], "tags"=>["growth conditions", "malaria parasites", "reticulocyte resident parasite stages", "pyrimidine biosynthesis", "rodent reticulocytes", "Whilst Plasmodium vivax exhibits", "intermediary carbon metabolism", "host cell", "berghei pyrimidine biosynthesis mutants", "erythrocyte counterparts", "reticulocyte resident parasites", "host Reticulocytes", "type parasites", "drug design", "falciparum growth", "Malaria Parasites Human malaria parasites", "Plasmodium host cell tropism result", "cell types offer", "erythroid cell types", "Metabolic Reservoirs", "merozoite production", "growth phenotype", "parasite preference", "rodent malaria parasite P", "berghei ICM mutants"], "article_id"=>1437174, "categories"=>["Biological Sciences"], "users"=>["Anubhav Srivastava", "Darren J. Creek", "Krystal J. Evans", "David De Souza", "Louis Schofield", "Sylke Müller", "Michael P. Barrett", "Malcolm J. McConville", "Andrew P. Waters"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004882.g003", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phenotypic_analyses_of_blood_stage_mutant_P_berghei_parasites_/1437174", "title"=>"Phenotypic analyses of blood stage mutant <i>P</i>. <i>berghei</i> parasites.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-04 03:33:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/2096307"], "description"=>"<p>A. Dynamics of reticulocyte enrichment in peripheral blood <i>in vivo</i> followed by Phenylhydrazine-HCl (phz) treatment of mice. Reticulocytes were harvested at day 5 post phz treatment. The error is given as the standard deviation (S.D.) of 3 independent biological replicates. B. Volcano plot showing distribution of putative metabolites according to their fold change in abundance in REP vs wtEP in rodent blood. All significant changes are represented above the broken horizontal line. Coloured dots indicate metabolites which are: Blue- significantly up-regulated, Red- significantly down-regulated, Yellow- significant but little change, Brown- non-significant. n = 3 independent biological replicates (with four internal technical replicates each). Significance tested by Welch’s T-test (α < 0.05). See Fig A-C in <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004882#ppat.1004882.s001\" target=\"_blank\">S1 Text</a> and <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1004882#ppat.1004882.s002\" target=\"_blank\">S1 Table</a> in for the complete list of detected metabolites and their respective abundance fold changes. C. Representative metabolites up-regulated in reticulocytes compared to mature erythrocytes in human and rodent erythrocytes. Relative levels (peak intensities) are expressed as fold change observed in reticulocyte vs mature erythrocytes. Dotted line indicates no change and error bars indicate R.S.D. (Relative Standard Deviation) of peak intensities from reticulocyte samples multiplied to the fold change values from n = 3 independent biological replicates.</p>", "links"=>[], "tags"=>["growth conditions", "malaria parasites", "reticulocyte resident parasite stages", "pyrimidine biosynthesis", "rodent reticulocytes", "Whilst Plasmodium vivax exhibits", "intermediary carbon metabolism", "host cell", "berghei pyrimidine biosynthesis mutants", "erythrocyte counterparts", "reticulocyte resident parasites", "host Reticulocytes", "type parasites", "drug design", "falciparum growth", "Malaria Parasites Human malaria parasites", "Plasmodium host cell tropism result", "cell types offer", "erythroid cell types", "Metabolic Reservoirs", "merozoite production", "growth phenotype", "parasite preference", "rodent malaria parasite P", "berghei ICM mutants"], "article_id"=>1437171, "categories"=>["Biological Sciences"], "users"=>["Anubhav Srivastava", "Darren J. Creek", "Krystal J. Evans", "David De Souza", "Louis Schofield", "Sylke Müller", "Michael P. Barrett", "Malcolm J. McConville", "Andrew P. Waters"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1004882.g001", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_Reticulocyte_enriched_Erythrocyte_Population_REP_and_wild_type_Erythrocyte_Population_wtEP_reveals_metabolite_enrichment_in_rodent_and_human_reticulocytes_/1437171", "title"=>"Comparison of Reticulocyte enriched Erythrocyte Population (REP) and wild type Erythrocyte Population (wtEP) reveals metabolite enrichment in rodent and human reticulocytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2015-06-04 03:33:33"}

PMC Usage Stats | Further Information

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  • {"unique-ip"=>"23", "full-text"=>"17", "pdf"=>"8", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"6"}
  • {"unique-ip"=>"11", "full-text"=>"12", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2018", "month"=>"8"}
  • {"unique-ip"=>"13", "full-text"=>"12", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"5", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"9"}
  • {"unique-ip"=>"15", "full-text"=>"12", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"3", "supp-data"=>"4", "cited-by"=>"0", "year"=>"2018", "month"=>"11"}
  • {"unique-ip"=>"27", "full-text"=>"24", "pdf"=>"11", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"7", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"10"}
  • {"unique-ip"=>"8", "full-text"=>"6", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2018", "month"=>"12"}
  • {"unique-ip"=>"21", "full-text"=>"26", "pdf"=>"10", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"2", "cited-by"=>"0", "year"=>"2019", "month"=>"2"}
  • {"unique-ip"=>"10", "full-text"=>"9", "pdf"=>"8", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"8", "full-text"=>"9", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"18", "full-text"=>"18", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"4", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"2", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}
  • {"unique-ip"=>"10", "full-text"=>"10", "pdf"=>"1", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"1", "year"=>"2019", "month"=>"9"}
  • {"unique-ip"=>"8", "full-text"=>"9", "pdf"=>"0", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"10"}
  • {"unique-ip"=>"13", "full-text"=>"11", "pdf"=>"3", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"1", "cited-by"=>"0", "year"=>"2019", "month"=>"12"}
  • {"unique-ip"=>"14", "full-text"=>"12", "pdf"=>"6", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2020", "month"=>"2"}

Relative Metric

{"start_date"=>"2015-01-01T00:00:00Z", "end_date"=>"2015-12-31T00:00:00Z", "subject_areas"=>[]}

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