FRET Imaging of Hemoglobin Concentration in Plasmodium falciparum-Infected Red Cells
Publication Date
November 21, 2008
Journal
PLOS ONE
Authors
Alessandro Esposito, Teresa Tiffert, Jakob M. A. Mauritz, Simon Schlachter, et al
Volume
3
Issue
11
Pages
e3780
DOI
https://dx.plos.org/10.1371/journal.pone.0003780
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0003780
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/19023444
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2582953
Europe PMC
http://europepmc.org/abstract/MED/19023444
Web of Science
000265448800001
Scopus
57049189294
Mendeley
http://www.mendeley.com/research/fret-imaging-hemoglobin-concentration-plasmodium-falciparuminfected-red-cells
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Mendeley | Further Information

{"title"=>"FRET imaging of hemoglobin concentration in Plasmodium falciparum-infected red cells", "type"=>"journal", "authors"=>[{"first_name"=>"Alessandro", "last_name"=>"Esposito", "scopus_author_id"=>"56853034900"}, {"first_name"=>"Teresa", "last_name"=>"Tiffert", "scopus_author_id"=>"6603868433"}, {"first_name"=>"Jakob M A", "last_name"=>"Mauritz", "scopus_author_id"=>"25723509900"}, {"first_name"=>"Simon", "last_name"=>"Schlachter", "scopus_author_id"=>"12544590000"}, {"first_name"=>"Lawrence H.", "last_name"=>"Bannister", "scopus_author_id"=>"23054214300"}, {"first_name"=>"Clemens F.", "last_name"=>"Kaminski", "scopus_author_id"=>"7003673210"}, {"first_name"=>"Virgilio L.", "last_name"=>"Lew", "scopus_author_id"=>"7005903159"}], "year"=>2008, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-57049189294", "pmid"=>"19023444", "sgr"=>"57049189294", "doi"=>"10.1371/journal.pone.0003780", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "issn"=>"19326203", "pui"=>"352760930"}, "id"=>"6dc00808-4caa-39ce-8baf-a5915d02f38e", "abstract"=>"Background: During its intraerythrocytic asexual reproduction cycle Plasmodium falciparum consumes up to 80% of the host cell hemoglobin, in large excess over its metabolic needs. A model of the homeostasis of falciparum-infected red blood cells suggested an explanation based on the need to reduce the colloid-osmotic pressure within the host cell to prevent its premature lysis. Critical for this hypothesis was that the hemoglobin concentration within the host cell be progressively reduced from the trophozoite stage onwards.Methodology/Principal Findings: The experiments reported here were designed to test this hypothesis by direct measurements of the hemoglobin concentration in live, infected red cells. We developed a novel, non-invasive method to quantify the hemoglobin concentration in single cells, based on Forster resonance energy transfer between hemoglobin molecules and the fluorophore calcein. Fluorescence lifetime imaging allowed the quantitative mapping of the hemoglobin concentration within the cells. The average fluorescence lifetimes of uninfected cohorts was 270 +/- 30 ps (mean +/- SD; N = 45). In the cytoplasm of infected cells the fluorescence lifetime of calcein ranged from 290 +/- 20 ps for cells with ring stage parasites to 590 +/- 13 ps and 1050 +/- 60 ps for cells with young trophozoites and late stage trophozoite/early schizonts, respectively. This was equivalent to reductions in hemoglobin concentration spanning the range from 7.3 to 2.3 mM, in line with the model predictions. An unexpected ancillary finding was the existence of a microdomain under the host cell membrane with reduced calcein quenching by hemoglobin in cells with mature trophozoite stage parasites.Conclusions/Significance: The results support the predictions of the colloid-osmotic hypothesis and provide a better understanding of the homeostasis of malaria-infected red cells. In addition, they revealed the existence of a distinct peripheral microdomain in the host cell with limited access to hemoglobin molecules indicating the concentration of substantial amounts of parasite-exported material.", "link"=>"http://www.mendeley.com/research/fret-imaging-hemoglobin-concentration-plasmodium-falciparuminfected-red-cells", "reader_count"=>58, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Researcher"=>17, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>15, "Student > Postgraduate"=>1, "Other"=>3, "Student > Master"=>9, "Student > Bachelor"=>1, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>5, "Researcher"=>17, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>15, "Student > Postgraduate"=>1, "Other"=>3, "Student > Master"=>9, "Student > Bachelor"=>1, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Engineering"=>3, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>29, "Medicine and Dentistry"=>4, "Business, Management and Accounting"=>1, "Physics and Astronomy"=>7, "Chemistry"=>8, "Economics, Econometrics and Finance"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>3}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Chemistry"=>{"Chemistry"=>8}, "Physics and Astronomy"=>{"Physics and Astronomy"=>7}, "Economics, Econometrics and Finance"=>{"Economics, Econometrics and Finance"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>29}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"South Korea"=>1, "United States"=>1, "Finland"=>1, "Brazil"=>1, "United Kingdom"=>2, "India"=>1}, "group_count"=>6}

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Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/915117"], "description"=>"<p>The different curves reflect variations in parameter values within ±1SD of experimentally reported values: t<sub>1/2</sub>(NPP) and t<sub>1/2</sub>(Hb) were varied over the range of 27±5 hours <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003780#pone.0003780-Staines1\" target=\"_blank\">[12]</a> and 32±6 hours <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003780#pone.0003780-Krugliak1\" target=\"_blank\">[6]</a>, respectively; the initial hemoglobin concentration and the maximal fraction of digested hemoglobin were set to 6.8±0.5 mM and 80±10% <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003780#pone.0003780-Francis1\" target=\"_blank\">[5]</a>, respectively. The coupling factor (<i>cf</i>) between the volume of cytosol ingested by the parasite and its volume-growth was set at 0.30, 0.65 and 1.00. The vertical column singles out the 32 to 40 hour post-invasion period of the cell samples analysed here. Volume is reported relative to initial red cell volume.</p>", "links"=>[], "tags"=>["changes"], "article_id"=>585574, "categories"=>["Microbiology", "Biophysics", "Infectious Diseases"], "users"=>["Alessandro Esposito", "Teresa Tiffert", "Jakob M. A. Mauritz", "Simon Schlachter", "Lawrence H. Bannister", "Clemens F. Kaminski", "Virgilio L. Lew"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003780.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Predicted_changes_in_Hb_A_and_relative_cell_volume_B_as_a_function_of_time_post_invasion_/585574", "title"=>"Predicted changes in [Hb] (<i>A</i>) and relative cell volume (B) as a function of time post-invasion.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-11-21 01:32:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/452482"], "description"=>"<div><h3>Background</h3><p>During its intraerythrocytic asexual reproduction cycle <em>Plasmodium falciparum</em> consumes up to 80% of the host cell hemoglobin, in large excess over its metabolic needs. A model of the homeostasis of falciparum-infected red blood cells suggested an explanation based on the need to reduce the colloid-osmotic pressure within the host cell to prevent its premature lysis. Critical for this hypothesis was that the hemoglobin concentration within the host cell be progressively reduced from the trophozoite stage onwards.</p><h3>Methodology/Principal Findings</h3><p>The experiments reported here were designed to test this hypothesis by direct measurements of the hemoglobin concentration in live, infected red cells. We developed a novel, non-invasive method to quantify the hemoglobin concentration in single cells, based on Förster resonance energy transfer between hemoglobin molecules and the fluorophore calcein. Fluorescence lifetime imaging allowed the quantitative mapping of the hemoglobin concentration within the cells. The average fluorescence lifetimes of uninfected cohorts was 270±30 ps (mean±SD; N = 45). In the cytoplasm of infected cells the fluorescence lifetime of calcein ranged from 290±20 ps for cells with ring stage parasites to 590±13 ps and 1050±60 ps for cells with young trophozoites and late stage trophozoite/ early schizonts, respectively. This was equivalent to reductions in hemoglobin concentration spanning the range from 7.3 to 2.3 mM, in line with the model predictions. An unexpected ancillary finding was the existence of a microdomain under the host cell membrane with reduced calcein quenching by hemoglobin in cells with mature trophozoite stage parasites.</p><h3>Conclusions/Significance</h3><p>The results support the predictions of the colloid-osmotic hypothesis and provide a better understanding of the homeostasis of malaria-infected red cells. In addition, they revealed the existence of a distinct peripheral microdomain in the host cell with limited access to hemoglobin molecules indicating the concentration of substantial amounts of parasite-exported material.</p></div>", "links"=>[], "tags"=>["fret", "imaging", "hemoglobin", "cells"], "article_id"=>149127, "categories"=>["Microbiology", "Cancer", "Biophysics"], "users"=>["Alessandro Esposito", "Teresa Tiffert", "Jakob M. A. Mauritz", "Simon Schlachter", "Lawrence H. Bannister", "Clemens F. Kaminski", "Virgilio L. Lew"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003780", "stats"=>{"downloads"=>9, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/FRET_Imaging_of_Hemoglobin_Concentration_in_Plasmodium_falciparum_Infected_Red_Cells/149127", "title"=>"FRET Imaging of Hemoglobin Concentration in <em>Plasmodium falciparum</em>-Infected Red Cells", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-11-21 02:32:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/915860"], "description"=>"<p>AB-plots and corresponding segmented regions of the cells shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003780#pone-0003780-g005\" target=\"_blank\">Fig. 5</a>. The segmented regions are shown on cells in green, red and blue colours on the right. A) Uninfected RBC (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003780#pone-0003780-g005\" target=\"_blank\">Fig. 5 B right</a>). B) Ring-IRBC (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003780#pone-0003780-g005\" target=\"_blank\">Fig. 5 B left</a>). C) Young trophozoite-IRBC (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003780#pone-0003780-g005\" target=\"_blank\">Fig. 5 D left</a>). D) Mature trophozoite- / early schizont-IRBC (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003780#pone-0003780-g005\" target=\"_blank\">Fig. 5 E</a>). The centroids of the phasor distributions from the calibration data (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003780#pone-0003780-g003\" target=\"_blank\">Fig. 3</a>) are indicated by the small black circles ranging clockwise along the arc from 0 mM to 6 mM. Three segmented regions are shown in the AB-plots by coloured circles: i) RBC cytosol (red), ii) malaria parasite (green) and iii) a mostly peripheral compartment (blue) within trophozoites / schizonts: see text. Rel. frequency: relative frequency.</p>", "links"=>[], "tags"=>["images", "ab-"], "article_id"=>586313, "categories"=>["Microbiology", "Biophysics", "Infectious Diseases"], "users"=>["Alessandro Esposito", "Teresa Tiffert", "Jakob M. A. Mauritz", "Simon Schlachter", "Lawrence H. Bannister", "Clemens F. Kaminski", "Virgilio L. Lew"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003780.g008", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Segmentation_of_lifetime_images_by_AB_phasor_plots_/586313", "title"=>"Segmentation of lifetime images by AB- (phasor) plots.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-11-21 01:45:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/915637"], "description"=>"<p><i>A</i>) Fluorescence emission (520–570 nm). <i>B</i>) Fluorescence lifetime of calcein showing a decrease from about 4 ns at zero [Hb] down to 250 ps in intact uninfected RBCs. Note the variation in fluorescence intensity and fluorescence lifetime among the cells. These reflect the normal distribution of incorporated calcein and [Hb] in red cells <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003780#pone.0003780-Lew3\" target=\"_blank\">[19]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003780#pone.0003780-Lew4\" target=\"_blank\">[41]</a>. C) [Hb] measured by fluorescence lifetime in RBCs whose [Hb] was reduced by equilibration in hypotonic media (RT: relative tonicity).</p>", "links"=>[], "tags"=>["imaging", "calcein", "loaded"], "article_id"=>586092, "categories"=>["Microbiology", "Biophysics", "Infectious Diseases"], "users"=>["Alessandro Esposito", "Teresa Tiffert", "Jakob M. A. Mauritz", "Simon Schlachter", "Lawrence H. Bannister", "Clemens F. Kaminski", "Virgilio L. Lew"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003780.g006", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Fluorescence_lifetime_imaging_of_calcein_loaded_red_blood_cells_/586092", "title"=>"Fluorescence lifetime imaging of calcein loaded red blood cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-11-21 01:41:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/916070"], "description"=>"<p>The boxes represent the state of the RBC / IRBC cytosol as determined by FRET, with horizontal red, blue and green bars, as for <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003780#pone-0003780-g008\" target=\"_blank\">Figure 8</a>.</p>", "links"=>[], "tags"=>["diagram", "illustrating", "observed", "compartmentation", "parasite"], "article_id"=>586520, "categories"=>["Microbiology", "Biophysics", "Infectious Diseases"], "users"=>["Alessandro Esposito", "Teresa Tiffert", "Jakob M. A. Mauritz", "Simon Schlachter", "Lawrence H. Bannister", "Clemens F. Kaminski", "Virgilio L. Lew"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003780.g010", "stats"=>{"downloads"=>6, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Interpretative_diagram_illustrating_the_observed_Hb_and_compartmentation_effects_throughout_parasite_development_/586520", "title"=>"Interpretative diagram illustrating the observed [Hb] and compartmentation effects throughout parasite development.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-11-21 01:48:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/915452"], "description"=>"<p>A) Average fluorescence lifetime <i>versus</i> [Hb] (mean of three experiments). Experimental values were fitted by equation S6. B) Hb-dependent quenching of calcein at different calcein concentrations (50, 100 and 150 µM).</p>", "links"=>[], "tags"=>["calcein", "hemoglobin"], "article_id"=>585906, "categories"=>["Microbiology", "Biophysics", "Infectious Diseases"], "users"=>["Alessandro Esposito", "Teresa Tiffert", "Jakob M. A. Mauritz", "Simon Schlachter", "Lawrence H. Bannister", "Clemens F. Kaminski", "Virgilio L. Lew"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003780.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Quenching_of_calcein_at_different_calcein_and_hemoglobin_concentrations_/585906", "title"=>"Quenching of calcein at different calcein and hemoglobin concentrations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-11-21 01:38:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/915354"], "description"=>"<p>A) Images show the decrease in fluorescence lifetime of calcein (100 µM) with hemoglobin concentration (0 to 6 mM) in RBC lysates. Fluorescence lifetimes are easily distinguishable in the 0–4 mM range of [Hb]. B) Same calibration data are represented in the phasor space. The centroids of phasor distributions are also shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0003780#pone-0003780-g008\" target=\"_blank\">figure 8</a> (circles). Rel. frequency: relative frequency.</p>", "links"=>[], "tags"=>["calcein"], "article_id"=>585812, "categories"=>["Microbiology", "Biophysics", "Infectious Diseases"], "users"=>["Alessandro Esposito", "Teresa Tiffert", "Jakob M. A. Mauritz", "Simon Schlachter", "Lawrence H. Bannister", "Clemens F. Kaminski", "Virgilio L. Lew"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003780.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Quenching_of_calcein_by_hemoglobin_/585812", "title"=>"Quenching of calcein by hemoglobin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-11-21 01:36:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/915976"], "description"=>"<p>Columns report uninfected cohorts (<i>RBC</i>), IRBCs containing ring-stage parasites (<i>ring</i>), trophozoite stage parasites (<i>T1</i>) and trophozoite-schizont stage parasites (<i>T2</i>), and pooled T1+T2 data (<i>T all</i>). The values shown in the statistical box charts were measured in the host cytoplasm from the phasor-assisted segmentation.</p>", "links"=>[], "tags"=>["cytosolic", "quenched", "calcein", "fractions"], "article_id"=>586424, "categories"=>["Microbiology", "Biophysics", "Infectious Diseases"], "users"=>["Alessandro Esposito", "Teresa Tiffert", "Jakob M. A. Mauritz", "Simon Schlachter", "Lawrence H. Bannister", "Clemens F. Kaminski", "Virgilio L. Lew"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003780.g009", "stats"=>{"downloads"=>1, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Statistical_analysis_of_cytosolic_Hb_A_and_quenched_calcein_fractions_B_/586424", "title"=>"Statistical analysis of cytosolic [Hb] (A) and quenched calcein fractions (B).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-11-21 01:47:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/915239"], "description"=>"<p>A) Curve illustrating the strong dependence of energy transfer efficiency on the relative distance between donor and acceptor fluorophores. B) Spectral overlap between the emission spectrum of a donor and the absorption spectrum of an acceptor fluorophore such as calcein and heme on which FRET depends (<i>abs.</i>, absorption; <i>a.u.</i>, arbitrary units). C) Predicted fluorescence decay of a fluorophore such as calcein, in the presence of 0% (<i>solid line</i>), 50% and 80% (<i>dashed lines</i>) FRET efficiency.</p>", "links"=>[], "tags"=>["Infectious diseases", "biophysics/experimental biophysical methods", "microbiology/parasitology"], "article_id"=>585689, "categories"=>["Microbiology", "Biophysics", "Infectious Diseases"], "users"=>["Alessandro Esposito", "Teresa Tiffert", "Jakob M. A. Mauritz", "Simon Schlachter", "Lawrence H. Bannister", "Clemens F. Kaminski", "Virgilio L. Lew"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003780.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Fluorescence_lifetime_and_FRET_/585689", "title"=>"Fluorescence lifetime and FRET.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-11-21 01:34:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/915564"], "description"=>"<p>[Hb], estimated from eq. 1, is plotted as a function of measured [Hb] (intercept set to zero). The parameter [Hb]<sub>0</sub> was estimated from the slope of the linear fit, as explained in the text. Bars are standard deviation from measurements performed in triplicates.</p>", "links"=>[], "tags"=>["Infectious diseases", "biophysics/experimental biophysical methods", "microbiology/parasitology"], "article_id"=>586014, "categories"=>["Microbiology", "Biophysics", "Infectious Diseases"], "users"=>["Alessandro Esposito", "Teresa Tiffert", "Jakob M. A. Mauritz", "Simon Schlachter", "Lawrence H. Bannister", "Clemens F. Kaminski", "Virgilio L. Lew"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003780.g005", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Measurement_of_Hb_0_/586014", "title"=>"Measurement of [Hb]<sub>0</sub>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-11-21 01:40:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/915723"], "description"=>"<p>Panels A, C and E show fluorescence intensity images of an uninfected RBC (<i>A and C</i>, <i>right</i>), a ring stage (<i>A</i>, <i>left</i>), a young trophozoite (<i>C</i>, <i>left</i>) and a mature trophozoite/early schizont (<i>E</i>). Arrows in panel C and E indicate the appearance of a bright edge in the IRBCs. The correspondent fluorescence lifetime images (<i>B</i>, <i>D and F</i>) reveal a significant increase in fluorescent lifetime in the host cytosol of infected cells relative to that in uninfected RBCs reflecting a decreased hemoglobin concentration.</p>", "links"=>[], "tags"=>["images", "infected"], "article_id"=>586175, "categories"=>["Microbiology", "Biophysics", "Infectious Diseases"], "users"=>["Alessandro Esposito", "Teresa Tiffert", "Jakob M. A. Mauritz", "Simon Schlachter", "Lawrence H. Bannister", "Clemens F. Kaminski", "Virgilio L. Lew"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0003780.g007", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lifetime_images_of_infected_red_blood_cells_/586175", "title"=>"Lifetime images of infected red blood cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-11-21 01:42:55"}

PMC Usage Stats | Further Information

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Relative Metric

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