Cell Cycle-Dependent Phosphorylation of Theileria annulata Schizont Surface Proteins
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{"title"=>"Cell cycle-dependent phosphorylation of Theileria annulata schizont surface proteins", "type"=>"journal", "authors"=>[{"first_name"=>"Olga", "last_name"=>"Wiens", "scopus_author_id"=>"56303711800"}, {"first_name"=>"Dong", "last_name"=>"Xia", "scopus_author_id"=>"35621040600"}, {"first_name"=>"Conrad", "last_name"=>"Von Schubert", "scopus_author_id"=>"35082789800"}, {"first_name"=>"Jonathan M.", "last_name"=>"Wastling", "scopus_author_id"=>"7003909793"}, {"first_name"=>"Dirk A.E.", "last_name"=>"Dobbelaere", "scopus_author_id"=>"7005945964"}, {"first_name"=>"Volker T.", "last_name"=>"Heussler", "scopus_author_id"=>"6701790107"}, {"first_name"=>"Kerry L.", "last_name"=>"Woods", "scopus_author_id"=>"37032295800"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84905220039", "sgr"=>"84905220039", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0103821", "pmid"=>"25077614", "pui"=>"373675704"}, "id"=>"bdd748cf-1ce4-3b00-aaa8-9b897882d0f8", "abstract"=>"The invasion of Theileria sporozoites into bovine leukocytes is rapidly followed by the destruction of the surrounding host cell membrane, allowing the parasite to establish its niche within the host cell cytoplasm. Theileria infection induces host cell transformation, characterised by increased host cell proliferation and invasiveness, and the activation of anti-apoptotic genes. This process is strictly dependent on the presence of a viable parasite. Several host cell kinases, including PI3-K, JNK, CK2 and Src-family kinases, are constitutively activated in Theileria-infected cells and contribute to the transformed phenotype. Although a number of host cell molecules, including IkB kinase and polo-like kinase 1 (Plk1), are recruited to the schizont surface, very little is known about the schizont molecules involved in host-parasite interactions. In this study we used immunofluorescence to detect phosphorylated threonine (p-Thr), serine (p-Ser) and threonine-proline (p-Thr-Pro) epitopes on the schizont during host cell cycle progression, revealing extensive schizont phosphorylation during host cell interphase. Furthermore, we established a quick protocol to isolate schizonts from infected macrophages following synchronisation in S-phase or mitosis, and used mass spectrometry to detect phosphorylated schizont proteins. In total, 65 phosphorylated Theileria proteins were detected, 15 of which are potentially secreted or expressed on the surface of the schizont and thus may be targets for host cell kinases. In particular, we describe the cell cycle-dependent phosphorylation of two T. annulata surface proteins, TaSP and p104, both of which are highly phosphorylated during host cell S-phase. TaSP and p104 are involved in mediating interactions between the parasite and the host cell cytoskeleton, which is crucial for the persistence of the parasite within the dividing host cell and the maintenance of the transformed state.", "link"=>"http://www.mendeley.com/research/cell-cycledependent-phosphorylation-theileria-annulata-schizont-surface-proteins", "reader_count"=>19, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Researcher"=>3, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>4, "Other"=>1, "Student > Master"=>1, "Student > Bachelor"=>6, "Professor > Associate Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Researcher"=>3, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>4, "Other"=>1, "Student > Master"=>1, "Student > Bachelor"=>6, "Professor > Associate Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>5, "Agricultural and Biological Sciences"=>5, "Medicine and Dentistry"=>1, "Immunology and Microbiology"=>1, "Computer Science"=>1, "Engineering"=>5}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>5}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>5}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>5}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"United States"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1616373", "https://ndownloader.figshare.com/files/1616374", "https://ndownloader.figshare.com/files/1616375", "https://ndownloader.figshare.com/files/1616376", "https://ndownloader.figshare.com/files/1616377", "https://ndownloader.figshare.com/files/1616378", "https://ndownloader.figshare.com/files/1616379", "https://ndownloader.figshare.com/files/1616380", "https://ndownloader.figshare.com/files/1616381", "https://ndownloader.figshare.com/files/1616382", "https://ndownloader.figshare.com/files/1616384", "https://ndownloader.figshare.com/files/1616385", "https://ndownloader.figshare.com/files/1616386", "https://ndownloader.figshare.com/files/1616387"], "description"=>"<div><p>The invasion of <i>Theileria</i> sporozoites into bovine leukocytes is rapidly followed by the destruction of the surrounding host cell membrane, allowing the parasite to establish its niche within the host cell cytoplasm. <i>Theileria</i> infection induces host cell transformation, characterised by increased host cell proliferation and invasiveness, and the activation of anti-apoptotic genes. This process is strictly dependent on the presence of a viable parasite. Several host cell kinases, including PI3-K, JNK, CK2 and Src-family kinases, are constitutively activated in <i>Theileria</i>-infected cells and contribute to the transformed phenotype. Although a number of host cell molecules, including IkB kinase and polo-like kinase 1 (Plk1), are recruited to the schizont surface, very little is known about the schizont molecules involved in host-parasite interactions. In this study we used immunofluorescence to detect phosphorylated threonine (p-Thr), serine (p-Ser) and threonine-proline (p-Thr-Pro) epitopes on the schizont during host cell cycle progression, revealing extensive schizont phosphorylation during host cell interphase. Furthermore, we established a quick protocol to isolate schizonts from infected macrophages following synchronisation in S-phase or mitosis, and used mass spectrometry to detect phosphorylated schizont proteins. In total, 65 phosphorylated <i>Theileria</i> proteins were detected, 15 of which are potentially secreted or expressed on the surface of the schizont and thus may be targets for host cell kinases. In particular, we describe the cell cycle-dependent phosphorylation of two <i>T. annulata</i> surface proteins, TaSP and p104, both of which are highly phosphorylated during host cell S-phase. TaSP and p104 are involved in mediating interactions between the parasite and the host cell cytoskeleton, which is crucial for the persistence of the parasite within the dividing host cell and the maintenance of the transformed state.</p></div>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Post-translational modification", "phosphorylation", "cell biology", "Signal transduction", "Parasitology", "Parasite groups", "apicomplexa", "Theileria", "Veterinary science", "Veterinary parasitology", "cycle-dependent", "schizont"], "article_id"=>1123057, "categories"=>["Biological Sciences"], "users"=>["Olga Wiens", "Dong Xia", "Conrad von Schubert", "Jonathan M. Wastling", "Dirk A. E. Dobbelaere", "Volker T. Heussler", "Kerry L. Woods"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0103821.s001", "https://dx.doi.org/10.1371/journal.pone.0103821.s002", "https://dx.doi.org/10.1371/journal.pone.0103821.s003", "https://dx.doi.org/10.1371/journal.pone.0103821.s004", "https://dx.doi.org/10.1371/journal.pone.0103821.s005", "https://dx.doi.org/10.1371/journal.pone.0103821.s006", "https://dx.doi.org/10.1371/journal.pone.0103821.s007", "https://dx.doi.org/10.1371/journal.pone.0103821.s008", "https://dx.doi.org/10.1371/journal.pone.0103821.s009", "https://dx.doi.org/10.1371/journal.pone.0103821.s010", "https://dx.doi.org/10.1371/journal.pone.0103821.s011", "https://dx.doi.org/10.1371/journal.pone.0103821.s012", "https://dx.doi.org/10.1371/journal.pone.0103821.s013", "https://dx.doi.org/10.1371/journal.pone.0103821.s014"], "stats"=>{"downloads"=>64, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Cell_Cycle_Dependent_Phosphorylation_of_Theileria_annulata_Schizont_Surface_Proteins/1123057", "title"=>"Cell Cycle-Dependent Phosphorylation of <i>Theileria annulata</i> Schizont Surface Proteins", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-07-31 02:58:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1616338"], "description"=>"<p>A: TaC12 cells were fixed (with 4% PFA) and incubated overnight with or without λPPase at 30°C before labelling with anti-p-Ser, p-Thr and p-Thr-Pro antibodies. DNA is visualised with DAPI (blue). Merge: phospho-epitopes (green), anti-schizont (red), DAPI (blue). Scale bar represents 10 µm. B: Lysates of TaC12 cells were incubated overnight with (2) or without (1) λPPase at 30°C prior to Western blot analysis with anti p-Ser, pThr and p-Thr-Pro antibodies. As a control for equal loading the membranes were probed with mouse anti-<i>Theileria</i>-HSP70 antibody.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Post-translational modification", "phosphorylation", "cell biology", "Signal transduction", "Parasitology", "Parasite groups", "apicomplexa", "Theileria", "Veterinary science", "Veterinary parasitology", "specificity", "p-thr", "p-thr-pro"], "article_id"=>1123023, "categories"=>["Biological Sciences"], "users"=>["Olga Wiens", "Dong Xia", "Conrad von Schubert", "Jonathan M. Wastling", "Dirk A. E. Dobbelaere", "Volker T. Heussler", "Kerry L. Woods"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103821.g001", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Validation_of_specificity_of_anti_p_Ser_p_Thr_and_p_Thr_Pro_antibodies_/1123023", "title"=>"Validation of specificity of anti-p-Ser, p-Thr and p-Thr-Pro antibodies.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-31 02:58:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1616340"], "description"=>"<p>Unsynchronised TaC12 cells were fixed with methanol and representative cells from different cell cycle stages are shown. A p-Thr specific antibody was used to detect phosphorylation at threonine residues and the anti-schizont polyclonal antibody is used to label the parasite. DNA is labelled with DAPI. Merge: anti-pThr (green), anti-schizont (red), DAPI (blue). Scale bar represents 10 µm.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Post-translational modification", "phosphorylation", "cell biology", "Signal transduction", "Parasitology", "Parasite groups", "apicomplexa", "Theileria", "Veterinary science", "Veterinary parasitology", "epitopes", "schizont", "interphase"], "article_id"=>1123025, "categories"=>["Biological Sciences"], "users"=>["Olga Wiens", "Dong Xia", "Conrad von Schubert", "Jonathan M. Wastling", "Dirk A. E. Dobbelaere", "Volker T. Heussler", "Kerry L. Woods"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103821.g002", "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_p_Thr_epitopes_are_detected_on_the_schizont_during_host_cell_interphase_and_cytokinesis_/1123025", "title"=>"p-Thr epitopes are detected on the schizont during host cell interphase and cytokinesis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-31 02:58:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1616342"], "description"=>"<p>TaC12 were treated with thymidine for 24 hours or nocodazole for 16 hours to synchronise cells in S-phase or mitosis. Synchronised cells were fixed with 4% PFA and analysed with anti-p-Thr, anti-p-Thr-Pro and anti-p-Ser antibodies. The parasite was detected with anti-p104 or TaSP antibodies and DNA is visualised with DAPI. Merge: phospho-epitopes (green), schizont (red), DAPI (blue). A: Thymidine synchronised TaC12 cells in S-phase. B: Nocodazole synchronised TaC12 cells in mitosis. Scale bar represents 10 µm.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Post-translational modification", "phosphorylation", "cell biology", "Signal transduction", "Parasitology", "Parasite groups", "apicomplexa", "Theileria", "Veterinary science", "Veterinary parasitology", "tac12", "cells", "s-"], "article_id"=>1123027, "categories"=>["Biological Sciences"], "users"=>["Olga Wiens", "Dong Xia", "Conrad von Schubert", "Jonathan M. Wastling", "Dirk A. E. Dobbelaere", "Volker T. Heussler", "Kerry L. Woods"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103821.g003", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Synchronisation_of_TaC12_cells_in_S_and_M_phase_/1123027", "title"=>"Synchronisation of TaC12 cells in S- and M-phase.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-31 02:58:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1616345"], "description"=>"<p>A: Overview of the workflow: TaC12 cells were synchronised in S-phase (thymidine block) or mitosis (nocodazole block). Schizonts were enriched, lysed, and analysed directly by LC MS/MS or after TiO<sub>2</sub> enrichment of phosphopeptides. Raw data were analysed using Progenesis and PEAKS. B: Schizonts were enriched using a Nycodenz step gradient. The sample is shown before (left) and after (right) centrifugation. The fraction containing enriched schizonts is indicated with an arrow. C: Western blot analysis of whole cell lysates (1) compared to purified schizonts (2). Equal amounts of protein from whole TaC12 lysates and enriched schizonts purified from S-phase and mitosis synchronised cells were subjected to Western blotting using an anti-<i>Theileria</i>-HSP70 antiserum to detect the parasite and anti-tubulin to detect host cell tubulin.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Post-translational modification", "phosphorylation", "cell biology", "Signal transduction", "Parasitology", "Parasite groups", "apicomplexa", "Theileria", "Veterinary science", "Veterinary parasitology", "schizonts", "cells", "synchronised", "s-phase"], "article_id"=>1123030, "categories"=>["Biological Sciences"], "users"=>["Olga Wiens", "Dong Xia", "Conrad von Schubert", "Jonathan M. Wastling", "Dirk A. E. Dobbelaere", "Volker T. Heussler", "Kerry L. Woods"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103821.g004", "stats"=>{"downloads"=>0, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Enrichment_of_schizonts_from_cells_synchronised_in_S_phase_or_M_phase_/1123030", "title"=>"Enrichment of schizonts from cells synchronised in S-phase or M-phase.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-31 02:58:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1616346"], "description"=>"<p>The phosphorylation pattern of asynchronous (lane 1) and synchronised TaC12 cells in S-phase (2) and mitosis (3) and corresponding samples with enriched schizonts were analysed with anti-p-Thr, anti-p-Thr-Pro and anti-p-Ser antibodies by Western blot. An equal amount of protein was loaded in each lane. Anti-<i>Theileria</i> HSP70 was used as a loading control. Signal intensity for each lane was quantified and the ratios are indicated underneath (also depicted in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0103821#pone.0103821.s005\" target=\"_blank\">figure S5</a>).</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Post-translational modification", "phosphorylation", "cell biology", "Signal transduction", "Parasitology", "Parasite groups", "apicomplexa", "Theileria", "Veterinary science", "Veterinary parasitology", "blot", "purified", "schizont", "lysates"], "article_id"=>1123031, "categories"=>["Biological Sciences"], "users"=>["Olga Wiens", "Dong Xia", "Conrad von Schubert", "Jonathan M. Wastling", "Dirk A. E. Dobbelaere", "Volker T. Heussler", "Kerry L. Woods"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103821.g005", "stats"=>{"downloads"=>3, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Western_blot_analysis_of_whole_cell_and_purified_schizont_lysates_with_anti_phospho_antibodies_/1123031", "title"=>"Western blot analysis of whole cell and purified schizont lysates with anti-phospho-antibodies.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-31 02:58:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1616349"], "description"=>"<p>A: Identified proteins using Progenesis and PEAKS. B: Mean peptide counts per sample corresponding to <i>T. annulata</i> proteins identified using Progenesis following TiO<sub>2</sub> enrichment of S-phase (n = 3) or mitotic (n = 3) samples. C. Overview of identified <i>T. annulata</i> proteins.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Post-translational modification", "phosphorylation", "cell biology", "Signal transduction", "Parasitology", "Parasite groups", "apicomplexa", "Theileria", "Veterinary science", "Veterinary parasitology", "spectrometry"], "article_id"=>1123034, "categories"=>["Biological Sciences"], "users"=>["Olga Wiens", "Dong Xia", "Conrad von Schubert", "Jonathan M. Wastling", "Dirk A. E. Dobbelaere", "Volker T. Heussler", "Kerry L. Woods"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103821.g006", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overview_of_the_mass_spectrometry_results_/1123034", "title"=>"Overview of the mass spectrometry results.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-31 02:58:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1616350"], "description"=>"<p>Detected phosphorylation sites are indicated with the amino acid number. White circles (P) represent phosphorylation sites detected in both mitotic and S-phase samples. Grey circles (P) represent phosphorylation sites with a significant difference in abundance between S-phase and mitotic samples. TaSP: schematic topology as predicted by TMpred: 1<sup>st</sup> TM: 3-21 aa; 2<sup>nd</sup> TM: 205-223 aa and 3<sup>rd</sup> TM 262-288 aa. Two phosphorylated serines (S303 and S305) in the C-terminal domain were more highly phosphorylated in S-phase schizont-samples (p<0.01). p104 is predicted to have a GPI-anchor (GPI). Phosphorylation of four serines (S601, S607, S800 and S802) was significantly increased in S-phase when compared to mitosis.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Post-translational modification", "phosphorylation", "cell biology", "Signal transduction", "Parasitology", "Parasite groups", "apicomplexa", "Theileria", "Veterinary science", "Veterinary parasitology", "overview", "phosphorylated", "sites", "tasp", "p104"], "article_id"=>1123035, "categories"=>["Biological Sciences"], "users"=>["Olga Wiens", "Dong Xia", "Conrad von Schubert", "Jonathan M. Wastling", "Dirk A. E. Dobbelaere", "Volker T. Heussler", "Kerry L. Woods"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103821.g007", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Schematic_overview_showing_all_phosphorylated_sites_detected_on_A_TaSP_TA17315_and_B_p104_TA08425_/1123035", "title"=>"Schematic overview showing all phosphorylated sites detected on A) TaSP (TA17315) and B) p104 (TA08425).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-31 02:58:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/1616351"], "description"=>"<p>Phospho-epitopes indicated in bold were those found more abundantly in samples from M- or S-phase (p<0.05).</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "Post-translational modification", "phosphorylation", "cell biology", "Signal transduction", "Parasitology", "Parasite groups", "apicomplexa", "Theileria", "Veterinary science", "Veterinary parasitology", "phosphorylated", "transmembrane-domain"], "article_id"=>1123036, "categories"=>["Biological Sciences"], "users"=>["Olga Wiens", "Dong Xia", "Conrad von Schubert", "Jonathan M. Wastling", "Dirk A. E. Dobbelaere", "Volker T. Heussler", "Kerry L. Woods"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0103821.t001", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_List_of_phosphorylated_proteins_with_a_predicted_transmembrane_domain_and_or_a_signal_peptide_/1123036", "title"=>"List of phosphorylated proteins with a predicted transmembrane-domain and/or a signal peptide.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-07-31 02:58:37"}

PMC Usage Stats | Further Information

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Relative Metric

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