An Inhibitory Antibody Blocks Interactions between Components of the Malarial Invasion Machinery
Publication Date
January 23, 2009
Journal
PLOS Pathogens
Authors
Christine R. Collins, Chrislaine Withers Martinez, Fiona Hackett & Michael J. Blackman
Volume
5
Issue
1
Pages
e1000273
DOI
https://dx.plos.org/10.1371/journal.ppat.1000273
Publisher URL
http://journals.plos.org/plospathogens/article?id=10.1371%2Fjournal.ppat.1000273
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/19165323
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2621342
Europe PMC
http://europepmc.org/abstract/MED/19165323
Web of Science
000263927800012
Scopus
59249106253
Mendeley
http://www.mendeley.com/research/inhibitory-antibody-blocks-interactions-between-components-malarial-invasion-machinery
Events
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Mendeley | Further Information

{"title"=>"An inhibitory antibody blocks interactions between components of the malarial invasion machinery", "type"=>"journal", "authors"=>[{"first_name"=>"Christine R.", "last_name"=>"Collins", "scopus_author_id"=>"7401740087"}, {"first_name"=>"Chrislaine", "last_name"=>"Withers-Martinez", "scopus_author_id"=>"6603275171"}, {"first_name"=>"Fiona", "last_name"=>"Hackett", "scopus_author_id"=>"6701535246"}, {"first_name"=>"Michael J.", "last_name"=>"Blackman", "scopus_author_id"=>"7102787691"}], "year"=>2009, "source"=>"PLoS Pathogens", "identifiers"=>{"scopus"=>"2-s2.0-59249106253", "pmid"=>"19165323", "sgr"=>"59249106253", "doi"=>"10.1371/journal.ppat.1000273", "isbn"=>"1553-7374 (Electronic)", "issn"=>"15537366", "pui"=>"354135311"}, "id"=>"1db9bc39-dec6-3904-a5f8-28b8df64be64", "abstract"=>"Host cell invasion by apicomplexan pathogens such as the malaria parasite Plasmodium spp. and Toxoplasma gondii involves discharge of proteins from secretory organelles called micronemes and rhoptries. In Toxoplasma a protein complex comprising the microneme apical membrane antigen 1 (AMA1), two rhoptry neck proteins, and a protein called Ts4705, localises to the moving junction, a region of close apposition between parasite and host cell during invasion. Antibodies against AMA1 prevent invasion and are protective in vivo, and so AMA1 is of widespread interest as a malaria vaccine candidate. Here we report that the AMA1 complex identified in Toxoplasma is conserved in Plasmodium falciparum. We demonstrate that the invasion-inhibitory monoclonal antibody (mAb) 4G2, which recognises P. falciparum AMA1 (PfAMA1), cannot bind when PfAMA1 is in a complex with its partner proteins. We further show that a single completely conserved PfAMA1 residue, Tyr251, lying within a conserved hydrophobic groove adjacent to the mAb 4G2 epitope, is required for complex formation. We propose that mAb 4G2 inhibits invasion by preventing PfAMA1 from interacting with other components of the invasion complex. Our findings should aid the rational design of subunit malaria vaccines based on PfAMA1.", "link"=>"http://www.mendeley.com/research/inhibitory-antibody-blocks-interactions-between-components-malarial-invasion-machinery", "reader_count"=>73, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Researcher"=>19, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>25, "Student > Postgraduate"=>2, "Student > Master"=>7, "Other"=>3, "Student > Bachelor"=>7, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Researcher"=>19, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>25, "Student > Postgraduate"=>2, "Student > Master"=>7, "Other"=>3, "Student > Bachelor"=>7, "Lecturer"=>1, "Professor"=>2}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>6, "Medicine and Dentistry"=>7, "Agricultural and Biological Sciences"=>48, "Veterinary Science and Veterinary Medicine"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemistry"=>3, "Computer Science"=>1, "Immunology and Microbiology"=>4, "Economics, Econometrics and Finance"=>1, "Unspecified"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>7}, "Chemistry"=>{"Chemistry"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>4}, "Economics, Econometrics and Finance"=>{"Economics, Econometrics and Finance"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>48}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Unspecified"=>{"Unspecified"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Brazil"=>2, "Germany"=>1}, "group_count"=>1}

CrossRef

Scopus | Further Information

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  • {"files"=>["https://ndownloader.figshare.com/files/911045"], "description"=>"<p>(A). Western blot of immunoprecipitates from parasite lines expressing various mutants of PfAMA1/DIII-HA. IP was performed with the anti-PfRON4 mAb 24C6. (B). Western blot of culture supernatants (CS) collected from the same lines. Blots were probed with either anti-PfAMA1 serum R5 or anti-HA mAb 3F10 (αHA). Parasite lines expressing PfAMA1/DIII-HA and mutants thereof exhibited no discernible growth phenotype (data not shown).</p>", "links"=>[], "tags"=>["4g2", "epitope", "pfama1-pfron4"], "article_id"=>581499, "categories"=>["Microbiology", "Physics", "Biochemistry", "Cell Biology"], "users"=>["Christine R. Collins", "Chrislaine Withers-Martinez", "Fiona Hackett", "Michael J. Blackman"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000273.g004", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mutations_within_the_4G2_epitope_do_not_prevent_PfAMA1_PfRON4_interaction_/581499", "title"=>"Mutations within the 4G2 epitope do not prevent PfAMA1-PfRON4 interaction.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-23 00:24:59"}
  • {"files"=>["https://ndownloader.figshare.com/files/910957"], "description"=>"<p>(A). Western blot of parental 3D7 and transgenic parasite lines harbouring a construct for expression of PfAMA1/DIII-HA. Anti-PfAMA1 serum R5 detected mature and processed forms of PfAMA1 in both parental and transgenic lines, whilst the epitope-tagged protein detected with the anti-HA mAb 3F10 (αHA) was present only in transgenic parasites. S, schizont extracts; CS, culture supernatants. (B)–(D). IFA of the PfAMA1/DIII-HA line probed with the anti-PfRON4 mAb 24C6, a rabbit anti-PfAMA1 polyclonal serum (RbαAMA1), mAb 3F10 (αHA), or a rabbit polyclonal anti-EBA-175 serum (RbαEBA). (E). Proteins immunoprecipitated with anti-PfRON4 mAb 24C6 from extracts of the PfAMA1/DIII-HA and PfSUB2-HA lines, analysed by Western blot with mAb 3F10 (αHA) or anti-PfAMA1 serum R5. Whilst PfAMA1 was efficiently co-precipitated from both extracts, no mAb 3F10-reactive species were co-precipitated from extracts of the PfSUB2-HA clone (note that mature PfSUB2-HA migrates on SDS-PAGE at ∼75 kDa; <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000273#ppat.1000273-Harris1\" target=\"_blank\">[5]</a>).</p>", "links"=>[], "tags"=>["trafficking", "post-translational", "episomally"], "article_id"=>581417, "categories"=>["Microbiology", "Physics", "Biochemistry", "Cell Biology"], "users"=>["Christine R. Collins", "Chrislaine Withers-Martinez", "Fiona Hackett", "Michael J. Blackman"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000273.g003", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Correct_trafficking_and_post_translational_processing_of_episomally_expressed_PfAMA1_/581417", "title"=>"Correct trafficking and post-translational processing of episomally expressed PfAMA1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-23 00:23:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/911264"], "description"=>"<p>(A). Western blot of total schizont extracts (S) and culture supernatants (CS) from parasite lines expressing deletion mutants (PfAMA1/DIII-HA-ΔH1, -ΔH2, and ΔH1+2) and hydrophobic trough mutants (PfAMA1/DIII-HA-HT1 and -HT3). Blots were probed with the anti-HA mAb 3F10 (αHA). (B). Western blot of IPs from extracts of the same lines, probed with anti-HA mAb 3F10 (αHA) or anti-PfAMA1 serum R5. IP was performed using anti-PfRON4 mAb 24C6. (C). IFA of schizonts from lines expressing mutants PfAMA1/DIII-HA-HT1 and -HT3, showing identical sub-cellular localisation of the mutant transgene product, detected by mAb 3F10 (αHA), with the microneme marker EBA-175 (RbαEBA). (D). Western blot of IPs from extracts of the Phe183 and Tyr251 mutants (PfAMA1/DIII-HA-HTFY, -HTF and –HTY), probed with anti-HA mAb 3F10 (αHA) or anti-PfAMA1 serum R5. IP was performed using anti-PfRON4 mAb 24C6. Note that all these mutants except PfAMA1/DIII-HA-ΔH1 and -ΔH1+2 (consistent with our previous findings, <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000273#ppat.1000273-Collins1\" target=\"_blank\">[24]</a>) were reactive with the anti-PfAMA1 mAb 4G2 (<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000273#ppat.1000273.s001\" target=\"_blank\">Figure S1</a>) confirming that they were conformationally correct.</p>", "links"=>[], "tags"=>["hydrophobic", "trough", "residues"], "article_id"=>581716, "categories"=>["Microbiology", "Physics", "Biochemistry", "Cell Biology"], "users"=>["Christine R. Collins", "Chrislaine Withers-Martinez", "Fiona Hackett", "Michael J. Blackman"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000273.g006", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PfAMA1_hydrophobic_trough_residues_are_critical_for_interaction_with_PfRON4_/581716", "title"=>"PfAMA1 hydrophobic trough residues are critical for interaction with PfRON4.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-23 00:28:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/911163"], "description"=>"<p>(A). Two views of the molecular surface representation of the PfAMA1 model based on the x-ray crystal structures of PfAMA1 and PvAMA1. Domain I is shown in red, domain II in blue, domain III in mustard, the hydrophobic trough in grey, the 4G2 epitope in black and the mAb 1F9 epitope residue Glu197 in green, visible on the left in the 90° rotated view. (B). Hydrophobic trough substitution mutants. PfAMA1 view as shown in (A) right-hand side, with from left to right mutants PfAMA1/DIII-HA-HT1 (Phe183, Ile190, Tyr251, Tyr202, Met224 in white), PfAMA1/DIII-HA-HT2 (Val169, Phe183, Tyr251, Ile252, Leu357, Phe367 in white) and PfAMA1/DIII-HA-HT3 (Leu357, Phe367 in white). (C). Deletion mutants. PfAMA1 view as shown in (B) showing in white the domain II loop residues removed in mutants PfAMA1/DIII-HA-ΔH1, PfAMA1/DIII-HA-ΔH2 and PfAMA1/III-HA-ΔH1+2. (D). Phe183/Tyr251 substitution mutants. PfAMA1 view as shown in (B) with, from left to right, mutants PfAMA1/DIII-HA-HTF, -HTY and –HTFY. Residues substituted with alanine are in each case shown in white. Figures were created using PyMOL (DeLano Scientific).</p>", "links"=>[], "tags"=>["mutations", "explored", "flanking", "hydrophobic"], "article_id"=>581616, "categories"=>["Microbiology", "Physics", "Biochemistry", "Cell Biology"], "users"=>["Christine R. Collins", "Chrislaine Withers-Martinez", "Fiona Hackett", "Michael J. Blackman"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000273.g005", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PfAMA1_mutations_explored_within_and_flanking_the_hydrophobic_trough_/581616", "title"=>"PfAMA1 mutations explored within and flanking the hydrophobic trough.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-23 00:26:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/910657"], "description"=>"<p>(A). Western blot of schizont extracts, demonstrating the specificity of binding of anti-PfAMA1 serum N5 and mAb 24C6 for PfAMA1 and PfRON4 respectively. Signals of the expected sizes were obtained, with no evidence for cross-reactivity. (B). Anti-PfAMA1 serum N5 and mAb 24C6 both precipitate PfRON4 and PfAMA1, plus two additional proteins of ∼190 kDa and 110 kDa. These were identified by mass spectrometric tryptic peptide mapping as PfRON2 and Mal8P1.73 respectively (<a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000273#ppat.1000273.s002\" target=\"_blank\">Tables S1</a>, <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000273#ppat.1000273.s003\" target=\"_blank\">S2</a>, <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1000273#ppat.1000273.s004\" target=\"_blank\">S3</a>). IPs were from extracts of biosynthetically radiolabelled schizonts. Note that both the mature and processed forms of PfAMA1 were co-precipitated by mAb 24C6, suggesting that PfRON4 is able to interact with both forms of PfAMA1. NMS, normal mouse serum. Positions of molecular mass marker proteins are indicated (kDa).</p>", "links"=>[], "tags"=>["pfama1", "comprises"], "article_id"=>581113, "categories"=>["Microbiology", "Physics", "Biochemistry", "Cell Biology"], "users"=>["Christine R. Collins", "Chrislaine Withers-Martinez", "Fiona Hackett", "Michael J. Blackman"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000273.g001", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_PfAMA1_complex_comprises_PfAMA1_plus_three_AAPs_/581113", "title"=>"The PfAMA1 complex comprises PfAMA1 plus three AAPs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-23 00:18:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/910816"], "description"=>"<p>(A). Immunoprecipitation from extracts of biosynthetically radiolabelled schizonts with control normal mouse serum (NMS), polyclonal anti-PfAMA1 serum N5, mAb 4G2 and anti-PfRON4 mAb 24C6. Although mAb 4G2 efficiently precipitated PfAMA1, it did not co-precipitate any of the three AAPs (indicated). These results were completely reproducible in 10 independent immunoprecipitation experiments. (B). Immuno-depletion experiments. Schizont extracts were subjected to two consecutive rounds of depletion (labelled 1 and 2) using either anti-PfAMA1 serum N5, or mAb 4G2, or control normal mouse serum (NMS), followed in each case by IP from the depleted extracts with the reciprocal antibody or mAb 24C6. Each track contains proteins eluted with SDS from the immunoprecipitation matrix. Depletion of the PfAMA1-AAP complex could not be achieved using mAb 4G2, even though it efficiently bound free PfAMA1. In all cases, immunoprecipitated proteins were detected by fluorography. Note that the slight differences in profile at ∼50 kDa in some of the tracks is due to the presence of (unlabelled) immunoglobulin heavy chain on the gels, and the fact that the rat mAb 4G2-derived heavy chain migrates slightly higher on SDS PAGE than that of the mouse antibodies.</p>", "links"=>[], "tags"=>["mab", "4g2", "pfama1-aap"], "article_id"=>581271, "categories"=>["Microbiology", "Physics", "Biochemistry", "Cell Biology"], "users"=>["Christine R. Collins", "Chrislaine Withers-Martinez", "Fiona Hackett", "Michael J. Blackman"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000273.g002", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Invasion_inhibitory_mAb_4G2_does_not_bind_the_PfAMA1_AAP_complex_/581271", "title"=>"Invasion-inhibitory mAb 4G2 does not bind the PfAMA1-AAP complex.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-01-23 00:21:11"}
  • {"files"=>["https://ndownloader.figshare.com/files/450388", "https://ndownloader.figshare.com/files/450436", "https://ndownloader.figshare.com/files/450486", "https://ndownloader.figshare.com/files/450554"], "description"=>"<div><p>Host cell invasion by apicomplexan pathogens such as the malaria parasite <em>Plasmodium</em> spp. and <em>Toxoplasma gondii</em> involves discharge of proteins from secretory organelles called micronemes and rhoptries. In <em>Toxoplasma</em> a protein complex comprising the microneme apical membrane antigen 1 (AMA1), two rhoptry neck proteins, and a protein called Ts4705, localises to the moving junction, a region of close apposition between parasite and host cell during invasion. Antibodies against AMA1 prevent invasion and are protective <em>in vivo</em>, and so AMA1 is of widespread interest as a malaria vaccine candidate. Here we report that the AMA1 complex identified in <em>Toxoplasma</em> is conserved in <em>Plasmodium falciparum</em>. We demonstrate that the invasion-inhibitory monoclonal antibody (mAb) 4G2, which recognises <em>P. falciparum</em> AMA1 (PfAMA1), cannot bind when PfAMA1 is in a complex with its partner proteins. We further show that a single completely conserved PfAMA1 residue, Tyr251, lying within a conserved hydrophobic groove adjacent to the mAb 4G2 epitope, is required for complex formation. We propose that mAb 4G2 inhibits invasion by preventing PfAMA1 from interacting with other components of the invasion complex. Our findings should aid the rational design of subunit malaria vaccines based on PfAMA1.</p></div>", "links"=>[], "tags"=>["inhibitory", "antibody", "blocks", "interactions", "components", "malarial", "machinery"], "article_id"=>148772, "categories"=>["Microbiology", "Physics", "Biochemistry", "Cell Biology"], "users"=>["Christine R. Collins", "Chrislaine Withers-Martinez", "Fiona Hackett", "Michael J. Blackman"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1000273.s001", "https://dx.doi.org/10.1371/journal.ppat.1000273.s002", "https://dx.doi.org/10.1371/journal.ppat.1000273.s003", "https://dx.doi.org/10.1371/journal.ppat.1000273.s004"], "stats"=>{"downloads"=>9, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/An_Inhibitory_Antibody_Blocks_Interactions_between_Components_of_the_Malarial_Invasion_Machinery/148772", "title"=>"An Inhibitory Antibody Blocks Interactions between Components of the Malarial Invasion Machinery", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-01-23 02:26:12"}

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

Relative Metric

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