Protein Kinase A Dependent Phosphorylation of Apical Membrane Antigen 1 Plays an Important Role in Erythrocyte Invasion by the Malaria Parasite
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{"title"=>"Protein kinase a dependent phosphorylation of apical membrane antigen 1 plays an important role in erythrocyte invasion by the malaria parasite", "type"=>"journal", "authors"=>[{"first_name"=>"Kerstin", "last_name"=>"Leykauf", "scopus_author_id"=>"6507670561"}, {"first_name"=>"Moritz", "last_name"=>"Treeck", "scopus_author_id"=>"14631235100"}, {"first_name"=>"Paul R.", "last_name"=>"Gilson", "scopus_author_id"=>"7004344898"}, {"first_name"=>"Thomas", "last_name"=>"Nebl", "scopus_author_id"=>"6506065622"}, {"first_name"=>"Thomas", "last_name"=>"Braulke", "scopus_author_id"=>"7005829342"}, {"first_name"=>"Alan F.", "last_name"=>"Cowman", "scopus_author_id"=>"7006258900"}, {"first_name"=>"Tim W.", "last_name"=>"Gilberger", "scopus_author_id"=>"6602766283"}, {"first_name"=>"Brendan S.", "last_name"=>"Crabb", "scopus_author_id"=>"35546737500"}], "year"=>2010, "source"=>"PLoS Pathogens", "identifiers"=>{"issn"=>"15537366", "scopus"=>"2-s2.0-77954665296", "pui"=>"359189102", "doi"=>"10.1371/journal.ppat.1000941", "isbn"=>"1553-7366", "sgr"=>"77954665296", "pmid"=>"20532217"}, "id"=>"1065d875-d79b-392a-a559-070a6fb0d4de", "abstract"=>"Apicomplexan parasites are obligate intracellular parasites that infect a variety of hosts, causing significant diseases in livestock and humans. The invasive forms of the parasites invade their host cells by gliding motility, an active process driven by parasite adhesion proteins and molecular motors. A crucial point during host cell invasion is the formation of a ring-shaped area of intimate contact between the parasite and the host known as a tight junction. As the invasive zoite propels itself into the host-cell, the junction moves down the length of the parasite. This process must be tightly regulated and signalling is likely to play a role in this event. One crucial protein for tight-junction formation is the apical membrane antigen 1 (AMA1). Here we have investigated the phosphorylation status of this key player in the invasion process in the human malaria parasite Plasmodium falciparum. We show that the cytoplasmic tail of P. falciparum AMA1 is phosphorylated at serine 610. We provide evidence that the enzyme responsible for serine 610 phosphorylation is the cAMP regulated protein kinase A (PfPKA). Importantly, mutation of AMA1 serine 610 to alanine abrogates phosphorylation of AMA1 in vivo and dramatically impedes invasion. In addition to shedding unexpected new light on AMA1 function, this work represents the first time PKA has been implicated in merozoite invasion.", "link"=>"http://www.mendeley.com/research/protein-kinase-dependent-phosphorylation-apical-membrane-antigen-1-plays-important-role-erythrocyte-5", "reader_count"=>77, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>19, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>34, "Student > Postgraduate"=>2, "Student > Master"=>10, "Other"=>1, "Student > Bachelor"=>5}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>19, "Student > Doctoral Student"=>3, "Student > Ph. D. Student"=>34, "Student > Postgraduate"=>2, "Student > Master"=>10, "Other"=>1, "Student > Bachelor"=>5}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>8, "Medicine and Dentistry"=>8, "Agricultural and Biological Sciences"=>53, "Pharmacology, Toxicology and Pharmaceutical Science"=>2, "Chemistry"=>3, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>8}, "Chemistry"=>{"Chemistry"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>53}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}, "Unspecified"=>{"Unspecified"=>2}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>2}}, "reader_count_by_country"=>{"Belgium"=>1, "United States"=>3, "Kenya"=>1}, "group_count"=>2}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/421360", "https://ndownloader.figshare.com/files/421398", "https://ndownloader.figshare.com/files/421428", "https://ndownloader.figshare.com/files/421464", "https://ndownloader.figshare.com/files/421523"], "description"=>"<div><p>Apicomplexan parasites are obligate intracellular parasites that infect a variety of hosts, causing significant diseases in livestock and humans. The invasive forms of the parasites invade their host cells by gliding motility, an active process driven by parasite adhesion proteins and molecular motors. A crucial point during host cell invasion is the formation of a ring-shaped area of intimate contact between the parasite and the host known as a tight junction. As the invasive zoite propels itself into the host-cell, the junction moves down the length of the parasite. This process must be tightly regulated and signalling is likely to play a role in this event. One crucial protein for tight-junction formation is the apical membrane antigen 1 (AMA1). Here we have investigated the phosphorylation status of this key player in the invasion process in the human malaria parasite <em>Plasmodium falciparum</em>. We show that the cytoplasmic tail of <em>P. falciparum</em> AMA1 is phosphorylated at serine 610. We provide evidence that the enzyme responsible for serine 610 phosphorylation is the cAMP regulated protein kinase A (<em>Pf</em>PKA). Importantly, mutation of AMA1 serine 610 to alanine abrogates phosphorylation of AMA1 <em>in vivo</em> and dramatically impedes invasion. In addition to shedding unexpected new light on AMA1 function, this work represents the first time PKA has been implicated in merozoite invasion.</p></div>", "links"=>[], "tags"=>["kinase", "phosphorylation", "apical", "membrane", "antigen", "plays", "erythrocyte", "malaria", "parasite"], "article_id"=>143204, "categories"=>["Biochemistry", "Physics", "Microbiology"], "users"=>["Kerstin Leykauf", "Moritz Treeck", "Paul R. Gilson", "Thomas Nebl", "Thomas Braulke", "Alan F. Cowman", "Tim W. Gilberger", "Brendan S. Crabb"], "doi"=>[nil, nil, nil, nil, nil], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Protein_Kinase_A_Dependent_Phosphorylation_of_Apical_Membrane_Antigen_1_Plays_an_Important_Role_in_Erythrocyte_Invasion_by_the_Malaria_Parasite/143204", "title"=>"Protein Kinase A Dependent Phosphorylation of Apical Membrane Antigen 1 Plays an Important Role in Erythrocyte Invasion by the Malaria Parasite", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-06-03 00:53:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/846818"], "description"=>"<p>(<b>A</b>) Schematic representation of AMA1 and the GST-fusion protein used. Signal peptide (blue), prosequence (PS), ectodomains I, II &amp; III, transmembrane domain (grey), cytoplasmic tail (C) and thrombin cleavage site are indicated. (<b>B, C</b>) Auto-radiographs showing phosphorylation of recombinant AMA1 tail by parasite lysates in the presence of 1.5 mM EGTA/1 mM EDTA or 2 mM CaCl<sub>2</sub> or 1 µM cAMP. The AMA1 tail was incubated with schizont (S), merozoite (M) or red blood cell (RBC) lysates and <sup>32</sup>[P]-γ -ATP. After washing the GST part was cleaved off with thrombin. As a loading control the membrane was probed with an anti-AMA1 antibody detecting the AMA1 tail. Molecular sizes are indicated on the left. (<b>D</b>) Quantitation of signal intensities in panel C with Image Gauge software. In the absence of additional EGTA/EDTA or cAMP the strength of the phosphorylation signal in untreated schizont lysate was set to 100% and all other signals are relative to that. The numbers of experimental replicates in <i>in vitro</i> phosphorylation assays are found in the Supplementary data (<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000941#ppat.1000941.s004\" target=\"_blank\">Text S1</a>). Error bars correspond to standard deviation.</p>", "links"=>[], "tags"=>["ama1", "c-terminal", "phosphorylated", "parasite", "lysates", "calcium"], "article_id"=>517255, "categories"=>["Biochemistry", "Physics", "Microbiology"], "users"=>["Kerstin Leykauf", "Moritz Treeck", "Paul R. Gilson", "Thomas Nebl", "Thomas Braulke", "Alan F. Cowman", "Tim W. Gilberger", "Brendan S. Crabb"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000941.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Recombinant_AMA1_C_terminal_tail_is_phosphorylated_i_in_vitro_i_by_i_P_falciparum_i_3D7_line_parasite_lysates_in_a_calcium_and_cAMP_dependent_manner_/517255", "title"=>"Recombinant AMA1 C-terminal tail is phosphorylated <i>in vitro</i> by <i>P. falciparum</i> (3D7 line) parasite lysates in a calcium and cAMP dependent manner.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-06-03 02:00:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/846902"], "description"=>"<p>(<b>A</b>) Multiple alignment of AMA1 C-terminal cytoplasmic domains including protein sequences of nine different <i>Plasmodium</i> species, <i>T. gondii</i>, <i>B. bovis</i> and two <i>Theileria</i> species. The conservation is scored and colour coded by PRALINE (<a href=\"http://www.ibi.vu.nl\" target=\"_blank\">www.ibi.vu.nl</a>). Amino acids predicted to be phosphorylated in <i>P. falciparum</i> AMA1 by NetPhos (<a href=\"http://www.cbs.dtu.dk/services/NetPhos\" target=\"_blank\">www.cbs.dtu.dk/services/NetPhos</a>) are scaled up in font size according to their relative predicted probabilities above the alignment and numbered regarding the protein sequence. As shown below the alignment the GST-fusion protein of the AMA1 tail was mutated at residues S601, S610, T612, T613, Y621 and Y622, respectively. (<b>B, C</b>) SDS-PAGE and radiograph of phosphorylation samples. GST-fusion proteins of the AMA1 tail and mutants were incubated with schizont lysate and <sup>32</sup>[P]- γ -ATP. As a loading control the membrane was probed with an anti-AMA1-C antibody. (<b>C</b>) H89 (50 µM) and KT5720 (10 µM), two inhibitors to PKA reverse the effect of cAMP (1 µM) on AMA1 tail phosphorylation. (<b>D, E</b>) Quantitation of signal intensities in (<b>C</b>) with Image Gauge software. The phosphorylation signal strength in untreated schizont lysate was set to 100% and all other signals were relative to that. The numbers of experimental replicates in <i>in vitro</i> phosphorylation assays are found in the Supplementary data (<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000941#ppat.1000941.s004\" target=\"_blank\">Text S1</a>). Error bars correspond to standard deviation. (<b>F</b>) <i>Pf</i>PKA-HA was immuno-precipitated from lysate of 3D7<i><sub>Pf</sub></i><sub>PKA-HA</sub> transgenic parasites using protein-G-sepharose. <i>Pf</i>PKA-HA was detected by Western Blot analysis using anti-HA antibodies and parasite lysate, washed fraction or sepharose beads. (<b>G</b>) SDS-PAGE and radiograph of <i>in vitro</i> phosphorylation of AMA1-GST using either protein-G-sepharose incubated with 3D7<i><sub>Pf</sub></i><sub>PKA-HA</sub> or with wild type (WT) parasites in the presence of <sup>32</sup>[P]- γ -ATP.</p>", "links"=>[], "tags"=>["phosphorylates", "ama1", "residue"], "article_id"=>517354, "categories"=>["Biochemistry", "Physics", "Microbiology"], "users"=>["Kerstin Leykauf", "Moritz Treeck", "Paul R. Gilson", "Thomas Nebl", "Thomas Braulke", "Alan F. Cowman", "Tim W. Gilberger", "Brendan S. Crabb"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000941.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_i_Pf_i_PKA_phosphorylates_the_AMA1_tail_exclusively_on_residue_S610_/517354", "title"=>"<i>Pf</i>PKA phosphorylates the AMA1 tail exclusively on residue S610.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-06-03 02:02:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/847008"], "description"=>"<p><i>P. falciparum</i> proteins were metabolically labelled with <sup>32</sup>[P], detergent extracted and resulting 2DE blots developed using Deep Purple stain to visualize total protein (<b>A</b>). Autoradiography detected <i>in vivo</i> phosphorylated proteins (<b>B</b>), and Western Blotting with an anti-AMA1 antibody detected the AMA1 tail (<b>C</b>). Isoelectric point and molecular sizes are indicated on the top and left. 2D spots corresponding to the 83 kDa precursor (AMA1<sub>83</sub>) or post-translationally processed ∼66 kDa AMA1 fragment (AMA<sub>66</sub>) are highlighted by bounding boxes, respectively. Magnification of the AMA1<sub>66</sub> region reveals a series of five discrete <sup>32</sup>[P]-labelled (a, c, d) or -unlabelled (b, e) protein spots recognized by anti-AMA1 antibody (arrows). (<b>D-I</b>) all show ∼66 kDa species of AMA1 separated by 2DE and analysed by Western Blot. 3D7 parasites either expressed a transgenic TY1-tagged wild type W2mef AMA1 (AMA1-WT-TY1; <b>D, E</b>), or mutant forms where the W2mef transgene carried the AMA1-S610A mutation (AMA1-S610A-TY1; <b>F, G</b>) or mutations at all putative phosphorylation sites in the cytoplasmic tail AMA1-PM-TY1; <b>H, I</b>). Blots were probed with a mouse monoclonal antibody against TY1 to detect transgenic epitope-tagged AMA1 followed and by an anti-AMA1 antibody against the AMA1 tail to detect both endogenously expressed 3D7 AMA1 as well as the W2mef transgenic species.</p>", "links"=>[], "tags"=>["dimensional", "gel", "analyses", "ama1", "phosphorylated", "s610"], "article_id"=>517453, "categories"=>["Biochemistry", "Physics", "Microbiology"], "users"=>["Kerstin Leykauf", "Moritz Treeck", "Paul R. Gilson", "Thomas Nebl", "Thomas Braulke", "Alan F. Cowman", "Tim W. Gilberger", "Brendan S. Crabb"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000941.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Two_dimensional_gel_analyses_confirm_that_i_P_falciparum_i_AMA1_is_phosphorylated_at_S610_i_in_vivo_i_/517453", "title"=>"Two dimensional gel analyses confirm that <i>P. falciparum</i> AMA1 is phosphorylated at S610 <i>in vivo</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-06-03 02:04:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/847108"], "description"=>"<p>Schizont, merozoite and ring-stage parental 3D7 parasites were analysed from a sequential time-course experiment by two dimensional gel electrophoresis and Western Blotting. Blots were probed with C-terminal AMA1 tail antibodies. Bands representing 83 kDa, 66 kDa and 22 kDa AMA1 species as well as presumed cross-reacting contaminating species (cont) are indicated on the right. Isoelectric points and molecular weight markers are indicated on the top and left of the autoradiographs, respectively.</p>", "links"=>[], "tags"=>["phosphorylated", "ama1"], "article_id"=>517560, "categories"=>["Biochemistry", "Physics", "Microbiology"], "users"=>["Kerstin Leykauf", "Moritz Treeck", "Paul R. Gilson", "Thomas Nebl", "Thomas Braulke", "Alan F. Cowman", "Tim W. Gilberger", "Brendan S. Crabb"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000941.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Maturation_of_phosphorylated_AMA1_species_/517560", "title"=>"Maturation of phosphorylated AMA1 species.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-06-03 02:06:00"}
  • {"files"=>["https://ndownloader.figshare.com/files/847228"], "description"=>"<p>(<b>A</b>) Schematic representation of the ectopically expressed TY1-tagged AMA1. Signal peptide (blue), prosequence (PS), ectodomains I, II &amp; III, transmembrane domain (grey), cytoplasmic tail (C) and TY1-tag (red) are indicated. (<b>B</b>) Mutations introduced into the cytoplasmic tail of W2mef-derived AMA1 are shown in red colour. (<b>C</b>) Expression of W2mef-derived AMA1-TY1 and native 3D7 AMA1 detected by Western Blot analysis using an anti-TY1 and anti-AMA1 (1F9) antibody, respectively (<b>C</b>, left panel). Whereas no AMA1-TY1 protein can be detected in 3D7 wild type parasites, a double band corresponding to AMA1<sub>83</sub>-TY1 and processed AMA1<sub>66</sub>-TY1 can be detected in AMA1-TY1-expressing parasites. (<b>C</b>, right panel) The endogenous 3D7 AMA1 is recognised by the anti-AMA1-1F9 antibody and shows identical proteolytic forms of AMA1 (AMA1<sub>83</sub> and AMA1<sub>66</sub>). (<b>D</b>) Invasion inhibition assays using AMA1-TY1 expressing parasite strains. Assays were performed in the presence of 100 µg/mL R1 peptide and were performed in triplicate in three independent experiments. Error bars correspond to standard deviation. 3D7 and AMA1-WT-TY1 served as control.</p>", "links"=>[], "tags"=>["phosphorylated", "residue", "s610", "merozoite"], "article_id"=>517678, "categories"=>["Biochemistry", "Physics", "Microbiology"], "users"=>["Kerstin Leykauf", "Moritz Treeck", "Paul R. Gilson", "Thomas Nebl", "Thomas Braulke", "Alan F. Cowman", "Tim W. Gilberger", "Brendan S. Crabb"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000941.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_i_Pf_i_PKA_phosphorylated_residue_S610_is_required_for_efficient_merozoite_invasion_/517678", "title"=>"The <i>Pf</i>PKA phosphorylated residue S610 is required for efficient merozoite invasion.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-06-03 02:07:58"}

PMC Usage Stats | Further Information

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