Phosphoinositide-3 Kinase-Akt Pathway Controls Cellular Entry of Ebola Virus
Publication Date
August 29, 2008
Journal
PLOS Pathogens
Authors
Mohammad F. Saeed, Andrey A. Kolokoltsov, Alexander N. Freiberg, Michael R. Holbrook, et al
Volume
4
Issue
8
Pages
e1000141
DOI
https://dx.plos.org/10.1371/journal.ppat.1000141
Publisher URL
http://journals.plos.org/plospathogens/article?id=10.1371%2Fjournal.ppat.1000141
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/18769720
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2516934
Europe PMC
http://europepmc.org/abstract/MED/18769720
Web of Science
000259783100029
Scopus
50849144350
Mendeley
http://www.mendeley.com/research/phosphoinositide3-kinaseakt-pathway-controls-cellular-entry-ebola-virus
Events
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Mendeley | Further Information

{"title"=>"Phosphoinositide-3 kinase-akt pathway controls cellular entry of ebola virus", "type"=>"journal", "authors"=>[{"first_name"=>"Mohammad F.", "last_name"=>"Saeed", "scopus_author_id"=>"14033127800"}, {"first_name"=>"Andrey A.", "last_name"=>"Kolokoltsov", "scopus_author_id"=>"8048248600"}, {"first_name"=>"Alexander N.", "last_name"=>"Freiberg", "scopus_author_id"=>"24758111700"}, {"first_name"=>"Michael R.", "last_name"=>"Holbrook", "scopus_author_id"=>"7006036112"}, {"first_name"=>"Robert A.", "last_name"=>"Davey", "scopus_author_id"=>"7202083531"}], "year"=>2008, "source"=>"PLoS Pathogens", "identifiers"=>{"pui"=>"352264387", "sgr"=>"50849144350", "pmid"=>"18769720", "scopus"=>"2-s2.0-50849144350", "isbn"=>"1553-7374 (Electronic)", "doi"=>"10.1371/journal.ppat.1000141", "issn"=>"15537366"}, "id"=>"d718382f-ff39-39db-ba02-9518667a5069", "abstract"=>"The phosphoinositide-3 kinase (PI3K) pathway regulates diverse cellular activities related to cell growth, migration, survival, and vesicular trafficking. It is known that Ebola virus requires endocytosis to establish an infection. However, the cellular signals that mediate this uptake were unknown for Ebola virus as well as many other viruses. Here, the involvement of PI3K in Ebola virus entry was studied. A novel and critical role of the PI3K signaling pathway was demonstrated in cell entry of Zaire Ebola virus (ZEBOV). Inhibitors of PI3K and Akt significantly reduced infection by ZEBOV at an early step during the replication cycle. Furthermore, phosphorylation of Akt-1 was induced shortly after exposure of cells to radiation-inactivated ZEBOV, indicating that the virus actively induces the PI3K pathway and that replication was not required for this induction. Subsequent use of pseudotyped Ebola virus and/or Ebola virus-like particles, in a novel virus entry assay, provided evidence that activity of PI3K/Akt is required at the virus entry step. Class 1A PI3Ks appear to play a predominant role in regulating ZEBOV entry, and Rac1 is a key downstream effector in this regulatory cascade. Confocal imaging of fluorescently labeled ZEBOV indicated that inhibition of PI3K, Akt, or Rac1 disrupted normal uptake of virus particles into cells and resulted in aberrant accumulation of virus into a cytosolic compartment that was non-permissive for membrane fusion. We conclude that PI3K-mediated signaling plays an important role in regulating vesicular trafficking of ZEBOV necessary for cell entry. Disruption of this signaling leads to inappropriate trafficking within the cell and a block in steps leading to membrane fusion. These findings extend our current understanding of Ebola virus entry mechanism and may help in devising useful new strategies for treatment of Ebola virus infection.", "link"=>"http://www.mendeley.com/research/phosphoinositide3-kinaseakt-pathway-controls-cellular-entry-ebola-virus", "reader_count"=>100, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Librarian"=>6, "Student > Doctoral Student"=>2, "Researcher"=>22, "Student > Ph. D. Student"=>25, "Student > Postgraduate"=>2, "Student > Master"=>7, "Other"=>5, "Student > Bachelor"=>16, "Lecturer"=>3, "Professor"=>7}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Librarian"=>6, "Student > Doctoral Student"=>2, "Researcher"=>22, "Student > Ph. D. Student"=>25, "Student > Postgraduate"=>2, "Student > Master"=>7, "Other"=>5, "Student > Bachelor"=>16, "Lecturer"=>3, "Professor"=>7}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Agricultural and Biological Sciences"=>49, "Arts and Humanities"=>1, "Veterinary Science and Veterinary Medicine"=>1, "Business, Management and Accounting"=>1, "Chemistry"=>1, "Computer Science"=>1, "Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>6, "Nursing and Health Professions"=>4, "Materials Science"=>1, "Medicine and Dentistry"=>15, "Design"=>1, "Physics and Astronomy"=>1, "Psychology"=>1, "Social Sciences"=>3, "Immunology and Microbiology"=>9}, "reader_count_by_subdiscipline"=>{"Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>15}, "Social Sciences"=>{"Social Sciences"=>3}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Psychology"=>{"Psychology"=>1}, "Unspecified"=>{"Unspecified"=>4}, "Arts and Humanities"=>{"Arts and Humanities"=>1}, "Design"=>{"Design"=>1}, "Engineering"=>{"Engineering"=>1}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>9}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>49}, "Computer Science"=>{"Computer Science"=>1}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>4}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Canada"=>3, "United States"=>5, "United Kingdom"=>1, "Ghana"=>1, "Nigeria"=>1, "Spain"=>2}, "group_count"=>4}

CrossRef

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/923120"], "description"=>"<p>(A) HEK293-mCAT-1 cells were pre-treated with the indicated concentrations of LY294002 for 1 h followed by incubation with ZEBO-VLP (open squares), VSV-VLP (closed squares), EVP (open circle), or VSVP (closed circle) for 3 h in the continued presence of the drug. Entry signals were then measured. Data were normalized to luciferase activity in DMSO (vehicle)-treated cells. (B) HEK293-mCAT-1 cells were pre-treated with the indicated concentrations of Akt inhibitor for 1 h followed by incubation with ZEBO-VLP (open squares), VSV-VLP (closed squares), EVP (open circle), or VSVP (closed circle) for 3 h in the continued presence of the drug. Entry signals were then measured. Data were normalized to luciferase activity in DMSO (vehicle)-treated cells. (C) HEK293-mCAT-1 cells were transfected with either pcDNA3 or pcDNA3 encoding a dominant-negative form of the PI3K p85-α regulatory subunit (Δp85α). Entry assays were performed 36 h after transfection using ZEBO-VLP (open bars) or VSV-VLP (solid bars). Data were normalized to luciferase activity in untransfected cells. Each data point represents the mean±SD of 3 experiments. (D) Wild-type (WT), pik3R1<sup>−/−</sup> (p85α, p55α, and p50α-deficient), or pik3R2<sup>−/−</sup> (p85β -deficient) mouse embryonic fibroblast (MEF) cells were incubated with EVP (open bars) or FrVP (solid bars). After 3 h, cells were washed, and luciferase activity was measured. Each data point represents the mean±SD of 3 independent experiments. (E) HEK293-mCAT-1 cells were pre-treated with LY294002 (50 µM) or Akt-1 inhibitor (1.0 µM) for 1 h at 37°C, followed by incubation with ZEBO-VLPs for 10 min at room temperature. Cells were then washed to remove unbound virus and resuspended in luciferase assay buffer containing triton X-100 detergent; luciferase activity was then measured. Data were normalized to luciferase activity in vehicle-treated samples. Each data point represents the mean±SD of 2 experiments.</p>", "links"=>[], "tags"=>["pathway", "ebola"], "article_id"=>593568, "categories"=>["Medicine", "Virology", "Infectious Diseases", "Mental Health"], "users"=>["Mohammad F. Saeed", "Andrey A. Kolokoltsov", "Alexander N. Freiberg", "Michael R. Holbrook", "Robert A. Davey"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000141.g004", "stats"=>{"downloads"=>1, "page_views"=>141, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PI3K_Akt_1_pathway_plays_a_critical_role_in_Ebola_virus_entry_/593568", "title"=>"PI3K-Akt-1 pathway plays a critical role in Ebola virus entry.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 09:39:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/923283"], "description"=>"<p>(A) HEK293-mCAT-1 cells were treated with indicated concentrations of Rac1 inhibitor, and entry assays were performed using ZEBO-VLP (open squares), VSV-VLP (closed squares), EVP (open circles), or VSVP (closed circles). Data points represent the average±SD of 2 experiments. (B) HEK293-mCAT-1 cells were transfected with either pcDNA3 vector lacking insert, or pcDNA3 encoding dominant-negative Rac1 (Rac1-T17N) or pcDNA3 encoding constitutively active Rac1 (Rac1-G12V). Entry assays were performed 36 h later using ZEBO-VLPs (open bars) or VSV-VLP (solid bars) in the absence or presence of Akt inhibitor. Results are expressed as the percent of luciferase activity in untransfected cells. Each data point represents the mean±SD of 2 experiments. (C) Cells transfected with plasmids encoding HA-tagged Rac1-T17N (left panel), Rac1-G12V (middle panel), or empty vector (right panel) were stained using anti-HA mouse monoclonal antibody and Alexafluor<sub>594</sub>-conjugated anti-mouse IgG.</p>", "links"=>[], "tags"=>["zebov", "serves", "downstream", "effector", "akt-1"], "article_id"=>593728, "categories"=>["Medicine", "Virology", "Infectious Diseases", "Mental Health"], "users"=>["Mohammad F. Saeed", "Andrey A. Kolokoltsov", "Alexander N. Freiberg", "Michael R. Holbrook", "Robert A. Davey"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000141.g005", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Rac1_plays_a_role_in_ZEBOV_entry_and_serves_as_a_downstream_effector_of_Akt_1_signaling_/593728", "title"=>"Rac1 plays a role in ZEBOV entry and serves as a downstream effector of Akt-1 signaling.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 09:40:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/922845"], "description"=>"<p>Vero-E6 cells were incubated with LY294002 (50 µM) or Akt inhibitor (10 µM) for 2 h in the presence of virus. Unbound virus and drug was then removed and cells were cultivated. After 10 d, cells were fixed in formalin and stained with crystal violet; plaques were then counted. Effect of the drugs on VSV (Indiana strain) infection was also tested similarly, except that plaques were counted 2 d after inoculation of cells. Open bars, ZEBOV; solid bars, VSV (* <i>p</i><0.01).</p>", "links"=>[], "tags"=>["zebov"], "article_id"=>593296, "categories"=>["Medicine", "Virology", "Infectious Diseases", "Mental Health"], "users"=>["Mohammad F. Saeed", "Andrey A. Kolokoltsov", "Alexander N. Freiberg", "Michael R. Holbrook", "Robert A. Davey"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000141.g001", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PI3K_is_important_for_early_step_s_during_ZEBOV_infection_/593296", "title"=>"PI3K is important for early step(s) during ZEBOV infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 09:38:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/923380"], "description"=>"<p>(A) HEK293-mCAT-1 cells were grown on chambered coverglass and treated with DMSO (control) or the indicated drugs for 1 h, followed by incubation with fluorescently labeled ZEBOV (red) for 3 h. Cells were fixed, permeabilized, and incubated with Alexafluor488-labeled phalloidin to visualize F-actin and DAPI to stain nuclei (blue). Subsequently, slides were washed and photographed by fluorescence microscopy using a 100× oil immersion objective. Scale bars are shown at lower right and apply to all images in the panel. (B) The observations made using HEK293-mCAT-1 cells were confirmed in Vero-E6 cells by confocal microscopy. (Top panel) Serial optical sections of cells treated for 1 h with DMSO (left) or the PI3K inhibitor LY294002 (right) and then incubated with fluorescently labeled ZEBOV (red) for 2 h. Cells were fixed and stained with phalloidin to label F-actin (green) and DAPI to label cell nuclei (blue). The level of the section is indicated, with 0 on the basolateral cell surface and 6 µm close to the apical surface of the cell. (C) Volume projection of all optical z-sections (computed using ImageJ software) of representative cells incubated in the presence of DMSO or LY294002. In DMSO-treated cells, examples of actin bundles adjacent to virus particles are indicated by arrowheads. Only the red and green fluorescence channels are shown, and the nuclei of chosen cells are indicated with dashed lines.</p>", "links"=>[], "tags"=>["rac1", "intracellular", "clustering", "zebov"], "article_id"=>593832, "categories"=>["Medicine", "Virology", "Infectious Diseases", "Mental Health"], "users"=>["Mohammad F. Saeed", "Andrey A. Kolokoltsov", "Alexander N. Freiberg", "Michael R. Holbrook", "Robert A. Davey"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000141.g006", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Inhibitors_of_PI3K_Akt_and_Rac1_cause_intracellular_clustering_of_ZEBOV_particles_/593832", "title"=>"Inhibitors of PI3K, Akt, and Rac1 cause intracellular clustering of ZEBOV particles.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 09:41:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/923498"], "description"=>"<p>ND, not determined; VLPs do not encode an expressed transgene to allow titer determination.</p>a<p>Pseudotyped virus particles or VLPs were pelleted through sucrose and resuspended in 0.01 volumes of the original culture volume. A total of 0.2 ml of virus was used per assay with 10<sup>6</sup> cells and values were measured after 3 h of incubation.</p>b<p>Virus was prepared as above and used to infect HEK293-mCAT-1 cells. Titer was determined by limiting dilution using GFP reporter expression to count infected cells. Values for titer and entry assay are the mean±SD of 3 independent experiments.</p>", "links"=>[], "tags"=>["luciferase-containing", "pseudotyped", "virus-like", "particles"], "article_id"=>593945, "categories"=>["Medicine", "Virology", "Infectious Diseases", "Mental Health"], "users"=>["Mohammad F. Saeed", "Andrey A. Kolokoltsov", "Alexander N. Freiberg", "Michael R. Holbrook", "Robert A. Davey"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000141.t001", "stats"=>{"downloads"=>4, "page_views"=>26, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Activity_of_luciferase_containing_pseudotyped_virus_and_virus_like_particles_in_the_entry_assay_/593945", "title"=>"Activity of luciferase-containing pseudotyped virus and virus-like particles in the entry assay.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-21 09:41:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/922909"], "description"=>"<p>Serum-starved HEK293 cells were incubated with serum-free medium (−), medium containing 10% FBS (S), and serum-free medium containing γ-radiation–inactivated ZEBOV (E, MOI = 5) or VSV (V, MOI = 5) at 37°C for 30 or 60 min. Subsequently, cells were washed and lysed, and phosphorylated Akt-1 was detected by Western blotting (p-Akt-1; top panel). The same membrane was then stripped and re-probed for total Akt-1 (bottom panel). The bar graph shows a summary of densitometry analysis of bands, which was performed using the ImageJ gel analysis package. The ratio of band intensities of phospho-Akt-1 to total Akt-1 was determined and normalized to the serum-treated control. Each data point represents mean±SD of 3 experiments.</p>", "links"=>[], "tags"=>["particles", "induce", "akt-1", "phosphorylation"], "article_id"=>593356, "categories"=>["Medicine", "Virology", "Infectious Diseases", "Mental Health"], "users"=>["Mohammad F. Saeed", "Andrey A. Kolokoltsov", "Alexander N. Freiberg", "Michael R. Holbrook", "Robert A. Davey"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000141.g002", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ZEBOV_particles_induce_Akt_1_phosphorylation_early_during_infection_/593356", "title"=>"ZEBOV particles induce Akt-1 phosphorylation early during infection.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 09:38:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/922994"], "description"=>"<p>(A) The luciferase entry assay was performed using EVP (open bars) or VSVP (solid bars) or ZEBO-VLP (diagonally hatched bars) on HEK293-mCAT-1 cells in the presence of anti-Ebola virus neutralizing antibody (KZ52, 0.3 µg/ml) or a control antibody of irrelevant specificity (anti-HA, 12CA5; Roche, 0.3 µg/ml). Data were normalized to luciferase activity in cells incubated with untreated virus. Each data point represents the mean±SD of 3 independent experiments. (B) Luciferase entry assays were performed using VSVP, EVP, or FrVP on HEK293-mCAT-1 cells in the presence of either 20 mM ammonium chloride (open bars) or 50 nM bafilomycin A1 (solid bars). Effect of ammonium chloride was also tested on ZEBO-VLP. Data were normalized to luciferase activity for untreated cells. Each data point represents the mean±SD of 3 independent experiments. (C) Kinetics of entry was measured for EVP (open squares), VSVP (closed squares), and ZEBO-VLP (open circles). Each was incubated with HEK293-mCAT1 cells at room temperature. After 10 min, cells were washed to remove unbound virus and incubated at 37°C. At indicated time intervals, aliquots of cells were withdrawn, and luciferase signals were measured. For each virus, luciferase activity at different time points was normalized to the maximum luciferase activity for that virus. Each data point represents the mean±SD of 2 independent experiments.</p>", "links"=>[], "tags"=>["luciferase", "assay", "zebov", "pseudotypes"], "article_id"=>593438, "categories"=>["Medicine", "Virology", "Infectious Diseases", "Mental Health"], "users"=>["Mohammad F. Saeed", "Andrey A. Kolokoltsov", "Alexander N. Freiberg", "Michael R. Holbrook", "Robert A. Davey"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1000141.g003", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Validation_of_luciferase_virus_entry_assay_for_ZEBOV_pseudotypes_and_VLPs_/593438", "title"=>"Validation of luciferase virus entry assay for ZEBOV pseudotypes and VLPs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-21 09:38:57"}

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Relative Metric

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