Kinetic Analysis of Ex Vivo Human Blood Infection by Leishmania
Publication Date
July 13, 2010
Journal
PLOS Neglected Tropical Diseases
Authors
Inmaculada Moreno, Mercedes Domínguez, Darío Cabañes, Carmen Aizpurua, et al
Volume
4
Issue
7
Pages
e743
DOI
http://doi.org/10.1371/journal.pntd.0000743
Publisher URL
http://journals.plos.org/plosntds/article?id=10.1371%2Fjournal.pntd.0000743
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/20644618
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2903471
Europe PMC
http://europepmc.org/abstract/MED/20644618
Web of Science
000280412300013
Scopus
77957896064
Mendeley
http://www.mendeley.com/research/kinetic-analysis-ex-vivo-human-blood-infection-leishmania
Events
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Mendeley | Further Information

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CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/418601", "https://ndownloader.figshare.com/files/418617", "https://ndownloader.figshare.com/files/418622", "https://ndownloader.figshare.com/files/418639", "https://ndownloader.figshare.com/files/418647", "https://ndownloader.figshare.com/files/418658"], "description"=>"<div><p>The leishmanioses, vector-borne diseases caused by the trypanosomatid protozoan <em>Leishmania</em>, are transmitted to susceptible mammals by infected phlebotomine sand flies that inoculate promastigotes into hemorrhagic pools created in host skin. We assumed that promastigotes are delivered to a blood pool, and analyzed early promastigote interactions (0–5 min) with host components, which lead to parasite endocytosis by blood leukocytes, and to host infection. Promastigotes were incubated with NHS or with heparinized blood in near-physiological conditions, and we used cell radioimmunoassay and flow cytometry to measure the on-rate constants (k<sub>+1</sub>) of promastigote interactions with natural opsonins and erythrocytes. We obtained quantitative data for parasitized cells to determine the time-course of promastigote binding and internalization by blood leukocytes. In these reactions, promastigotes bind natural opsonins, immune adhere to erythrocytes and activate complement cytolysis, which kills ∼95% of promastigotes by 2 min post-infection. C3-promastigote binding is a key step in opsonization; nascent C3-promastigotes are the substrate for two simultaneous reactions, C3-promastigote immune adherence (IA) to erythrocytes and complement-mediated promastigote killing. The k<sub>+1</sub> for IA was 75-fold greater than that for promastigote killing, showing that IA facilitates promastigote endocytosis and circumvents lysis. At 5 min post-infection, when reaction velocity is still linear and promastigote concentration is not limiting, 17.4% of granulocytes and 10.7% of monocytes had bound promastigotes, of which ∼50% and ∼25%, respectively, carried surface-bound (live) or internalized (live and dead) leishmanias. Of other leukocyte types, 8.5% of B cells bound but did not internalize promastigotes, and T cells, NK cells and CD209<sup>+</sup> dendritic cells did not bind parasites. These data show that, once in contact with blood, promastigote invasion of human leukocytes is an extremely rapid and efficient reaction, and suggest that the IA reaction constitutes a central strategy for this parasite in subverting host innate immune defenses.</p></div>", "links"=>[], "tags"=>["kinetic", "ex", "vivo"], "article_id"=>142674, "categories"=>["Immunology", "Physics", "Medicine"], "users"=>["Inmaculada Moreno", "Mercedes Domínguez", "Darío Cabañes", "Carmen Aizpurua", "Alfredo Toraño"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0000743.s001", "https://dx.doi.org/10.1371/journal.pntd.0000743.s002", "https://dx.doi.org/10.1371/journal.pntd.0000743.s003", "https://dx.doi.org/10.1371/journal.pntd.0000743.s004", "https://dx.doi.org/10.1371/journal.pntd.0000743.s005", "https://dx.doi.org/10.1371/journal.pntd.0000743.s006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Kinetic_Analysis_of_Ex_Vivo_Human_Blood_Infection_by_Leishmania_/142674", "title"=>"Kinetic Analysis of Ex Vivo Human Blood Infection by <em>Leishmania</em>", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-07-13 00:44:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/840179"], "description"=>"<p>Aliquots (50 µl) of <i>L. donovani</i> or <i>L. amazonensis</i> promastigotes (10<sup>7</sup>/ml) were mixed with 50 µl 50% NHS and incubated (37°C) for varying times. Promastigotes were then washed by centrifugation (11,000×g, 1 min) with cold PFS. Untreated promastigotes (5×10<sup>6</sup>) were added to the pellet, washed twice in cold PFS, and promastigote-bound IgM measured with <sup>125</sup>I-goat anti-μ antibody. Each point (mean of triplicate samples) is expressed as a percentage of the point of maximum IgM binding in one representative experiment of five performed for each species. (A) <i>L. donovani</i>, (B) <i>L. amazonensis</i>. Insets: plots of L (IgM<sub>5max</sub>/IgM<sub>5max</sub>−IgM<sub>5ti</sub>) against reaction time (t<sub>i</sub>), from which k<sup>app</sup> values were derived.</p>", "links"=>[], "tags"=>["serum", "igm", "binding"], "article_id"=>510636, "categories"=>["Immunology", "Physics", "Medicine"], "users"=>["Inmaculada Moreno", "Mercedes Domínguez", "Darío Cabañes", "Carmen Aizpurua", "Alfredo Toraño"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0000743.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Time_course_of_normal_serum_IgM_binding_to_L_donovani_and_L_amazonensis_promastigotes_/510636", "title"=>"Time course of normal serum IgM binding to <i>L. donovani</i> and <i>L. amazonensis</i> promastigotes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-13 00:10:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/840244"], "description"=>"<p>Duplicate aliquots (50 µl) of promastigotes (10<sup>7</sup>/ml) were mixed with 50 µl 50% NHS and incubated (37°C) for the times indicated. Promastigotes were then washed twice by centrifugation (11,000×g, 1 min) in cold PFS, and promastigote-bound C3 measured with <sup>125</sup>I-SIM27–49 (anti-human C3α mAb). C3 binding (mean of duplicate values) from one representative experiment. (A) <i>L. donovani</i> (<i>n</i> = 4), (B) <i>L. amazonensis</i> (<i>n</i> = 5). Insets: plots of L (C3<sub>max</sub>/C3<sub>max</sub>−C3<sub>ti</sub>) against time (t<sub>i</sub>), from which k<sup>app</sup> constants of C3 deposition reactions were obtained.</p>", "links"=>[], "tags"=>["c3", "deposition"], "article_id"=>510708, "categories"=>["Immunology", "Physics", "Medicine"], "users"=>["Inmaculada Moreno", "Mercedes Domínguez", "Darío Cabañes", "Carmen Aizpurua", "Alfredo Toraño"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0000743.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Kinetics_of_C3_deposition_on_L_donovani_and_L_amazonensis_promastigotes_/510708", "title"=>"Kinetics of C3 deposition on <i>L. donovani</i> and <i>L. amazonensis</i> promastigotes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-13 00:11:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/840307"], "description"=>"<p>Aliquots (50 µl) of [<sup>111</sup>In]-labeled promastigotes (10<sup>7</sup>cells/ml) were mixed with 50 µl heparinized blood and incubated (37°C) for the times indicated. Samples were then fractionated by centrifugation (500×g/3 min) through 72% Percoll; free and erythrocyte-bound parasites were collected separately and [<sup>111</sup>In] cpm determined in each fraction. The IA kinetic profile is calculated as [<sup>111</sup>In]-promastigote cpm bound to erythrocytes relative to total [<sup>111</sup>In]-promastigote cpm at each time point, and expressed as a percentage of maximum binding of triplicate samples from one representative experiment. (A) <i>L. donovani</i> (<i>n</i> = 6), (B) <i>L. amazonensis</i> (<i>n</i> = 6). Insets: plots of L (IA<sub>max</sub>/IA<sub>max</sub>−IA<sub>ti</sub>) against incubation time (t<sub>i</sub>), from which k<sup>app</sup> values for <i>Leishmania</i> IA reaction were obtained. Blood from three different donors was used and two experiments were performed for each blood sample.</p>", "links"=>[], "tags"=>["adherence"], "article_id"=>510765, "categories"=>["Immunology", "Physics", "Medicine"], "users"=>["Inmaculada Moreno", "Mercedes Domínguez", "Darío Cabañes", "Carmen Aizpurua", "Alfredo Toraño"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0000743.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Kinetics_of_the_Leishmania_immune_adherence_IA_reaction_in_human_blood_/510765", "title"=>"Kinetics of the <i>Leishmania</i> immune adherence (IA) reaction in human blood.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-13 00:12:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/840393"], "description"=>"<p>For each time point, single aliquots (50 µl) of promastigotes (10<sup>7</sup>cells/ml) were mixed with 50 µl 50% pooled NHS and incubated (37°C) for the times indicated. Samples were then transferred into 1 ml PBS containing PI (5 µg/ml), and promastigote membrane damage registered as PI uptake in a flow cytometer. The time course of promastigote PI uptake is shown for a representative experiment. (A) <i>L. donovani</i> (<i>n</i> = 5), and (B) <i>L. amazonensis</i> (<i>n</i> = 4). Insets: plots of L (PI<sub>max</sub>/PI<sub>max</sub>−PI<sub>ti</sub>) against incubation time (t<sub>i</sub>), from which k<sup>app</sup> values were derived for promastigote PI uptake reactions.</p>", "links"=>[], "tags"=>["promastigote", "propidium", "iodide", "uptake"], "article_id"=>510848, "categories"=>["Immunology", "Physics", "Medicine"], "users"=>["Inmaculada Moreno", "Mercedes Domínguez", "Darío Cabañes", "Carmen Aizpurua", "Alfredo Toraño"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0000743.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Kinetics_of_promastigote_propidium_iodide_PI_uptake_in_NHS_/510848", "title"=>"Kinetics of promastigote propidium iodide (PI) uptake in NHS.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-13 00:14:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/840495"], "description"=>"<p>CMFDA-labeled promastigotes were incubated (5 min) with heparinized blood and the percentage of each <i>Leishmania</i>-binding leukocyte subpopulation was measured by flow cytometry. Leukocyte subpopulations were stained with fluorochrome-labeled mAb and identified in a dot plot as side scatter (SSC) vs. the specific fluorescent label. The percentage of each promastigote-binding subpopulation was analyzed in a secondary plot representing the fluorescence intensity of each gated mAb-labeled population vs. that of cell-bound CMFDA-labeled promastigotes. Dot plots of a representative experiment show cells in the gated populations that bound CMFDA-labeled (A) <i>L. amazonensis</i> or (B) <i>L. donovani</i> promastigotes. (C) Cells of each subpopulation that bound promastigotes expressed as a percentage of total leukocytes in the sample. Results are shown as the percentage (mean ± SEM) of 14 experiments performed with blood of six donors. (▪) <i>L. amazonesis</i>, () <i>L. donovani</i> promastigotes.</p>", "links"=>[], "tags"=>["leukocyte", "subpopulations", "promastigotes"], "article_id"=>510951, "categories"=>["Immunology", "Physics", "Medicine"], "users"=>["Inmaculada Moreno", "Mercedes Domínguez", "Darío Cabañes", "Carmen Aizpurua", "Alfredo Toraño"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0000743.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Blood_leukocyte_subpopulations_that_bind_promastigotes_in_early_infection_/510951", "title"=>"Blood leukocyte subpopulations that bind promastigotes in early infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-13 00:15:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/840578"], "description"=>"<p>Aliquots of heparinized human blood were infected with CMFDA-labeled <i>L. amazonensis</i> or <i>L. donovani</i> promastigotes and incubated (37°C) for various times (0–60 min). Samples were then processed as indicated in <a href=\"http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0000743#s2\" target=\"_blank\">Methods</a>. To calculate the percentage of granulocytes and monocytes that bound and internalized parasites, cells were gated by SSC vs. FSC and plotted independently in a secondary plot of SSC vs. FL1 (green, 530 nm). The percentage of cells that internalized promastigotes was determined using trypan blue to quench the extracellular fluorescence emitted by cell-bound complement-killed CMFDA-labeled promastigotes. (A) For <i>L. amazonensis</i> promastigotes: (a) Time course of granulocyte binding and internalization (•) or internalization (○); (b) data from inset (shaded area) in (a); (c) time course of monocyte binding and internalization (•) or internalization (○); (d) data from inset (shaded area) in (c). (B) Data as above (a–d) are shown for <i>L. donovani</i>. Results from seven (<i>L. donovani</i>) and ten (<i>L. amazonensis</i>) experiments with blood from six donors.</p>", "links"=>[], "tags"=>["leukocyte", "binding", "internalization", "promastigotes"], "article_id"=>511038, "categories"=>["Immunology", "Physics", "Medicine"], "users"=>["Inmaculada Moreno", "Mercedes Domínguez", "Darío Cabañes", "Carmen Aizpurua", "Alfredo Toraño"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0000743.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Kinetics_of_leukocyte_binding_and_internalization_of_L_amazonensis_and_L_donovani_promastigotes_in_human_blood_/511038", "title"=>"Kinetics of leukocyte binding and internalization of <i>L. amazonensis</i> and <i>L. donovani</i> promastigotes in human blood.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-13 00:17:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/840652"], "description"=>"<p>Kinetic data are taken from the promastigote opsonization reactions shown in <a href=\"http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0000743#pntd-0000743-g001\" target=\"_blank\">Figs. 1</a><a href=\"http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0000743#pntd-0000743-g002\" target=\"_blank\"></a><a href=\"http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0000743#pntd-0000743-g003\" target=\"_blank\"></a> to <a href=\"http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0000743#pntd-0000743-g004\" target=\"_blank\">4</a>, and from the granulocyte and monocyte binding and internalization reactions in <a href=\"http://www.plosntds.org/article/info:doi/10.1371/journal.pntd.0000743#pntd-0000743-g006\" target=\"_blank\">Fig. 6</a>. Promastigote-IgM binding (▴), promastigote IA reaction (♦), promastigote-C3 binding (▾), promastigote PI uptake (<b>X</b>), granulocytes that bind and internalize promastigotes (•), granulocytes that internalize promastigotes (○), monocytes that bind and internalize promastigotes (▪) and monocytes that internalize promastigotes (□).</p>", "links"=>[], "tags"=>["promastigote", "interactions", "components"], "article_id"=>511116, "categories"=>["Immunology", "Physics", "Medicine"], "users"=>["Inmaculada Moreno", "Mercedes Domínguez", "Darío Cabañes", "Carmen Aizpurua", "Alfredo Toraño"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0000743.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Kinetics_of_L_amazonensis_promastigote_interactions_with_host_components_during_early_infection_in_blood_/511116", "title"=>"Kinetics of <i>L. amazonensis</i> promastigote interactions with host components during early infection in blood.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-13 00:18:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/840785"], "description"=>"<p>Reaction pathway of promastigotes in host hematoma; k<sub>+1</sub> constants show the frequency at which the reactions occur. <i>Leishmania</i> opsonization by natural antibodies and complement triggers promastigote IA reaction and the complement cytolytic cascade that kills the parasite. The velocity of the IA reaction facilitates parasite transfer to granulocytes (1), monocytes (2) and B lymphocytes (3), causing primary infection in granulocytes and monocytes. Infection can be boosted when parasitized granulocytes that become apoptotic (4) release promastigotes, which are phagocytosed by newly recruited macrophages (5).</p>", "links"=>[], "tags"=>["immunology/innate immunity", "infectious diseases/neglected tropical diseases", "infectious diseases/protozoal infections"], "article_id"=>511242, "categories"=>["Immunology", "Physics", "Medicine"], "users"=>["Inmaculada Moreno", "Mercedes Domínguez", "Darío Cabañes", "Carmen Aizpurua", "Alfredo Toraño"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0000743.g008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Kinetic_model_of_Leishmania_infection_in_the_human_blood_pool_/511242", "title"=>"Kinetic model of <i>Leishmania</i> infection in the human blood pool.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-13 00:20:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/840857"], "description"=>"a<p>Mean k<sub>+1</sub> constant for <i>L. amazonensis</i> and <i>L. donovani</i> promastigotes.</p>", "links"=>[], "tags"=>["constants", "opsonization", "adherence", "reactions", "promastigotes"], "article_id"=>511311, "categories"=>["Immunology", "Physics", "Medicine"], "users"=>["Inmaculada Moreno", "Mercedes Domínguez", "Darío Cabañes", "Carmen Aizpurua", "Alfredo Toraño"], "doi"=>["https://dx.doi.org/10.1371/journal.pntd.0000743.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_On_rate_constants_of_opsonization_and_immune_adherence_reactions_of_L_donovani_and_L_amazonensis_promastigotes_in_human_blood_/511311", "title"=>"On-rate constants of opsonization and immune adherence reactions of <i>L. donovani</i> and <i>L. amazonensis</i> promastigotes in human blood.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-07-13 00:21:51"}

PMC Usage Stats | Further Information

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