The Antiviral Restriction Factors IFITM1, 2 and 3 Do Not Inhibit Infection of Human Papillomavirus, Cytomegalovirus and Adenovirus
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{"title"=>"The antiviral restriction factors IFITM1, 2 and 3 do not inhibit infection of human papillomavirus, cytomegalovirus and adenovirus", "type"=>"journal", "authors"=>[{"first_name"=>"Cody J.", "last_name"=>"Warren", "scopus_author_id"=>"56177442800"}, {"first_name"=>"Laura M.", "last_name"=>"Griffin", "scopus_author_id"=>"55261654700"}, {"first_name"=>"Alexander S.", "last_name"=>"Little", "scopus_author_id"=>"46062269200"}, {"first_name"=>"I. Chueh", "last_name"=>"Huang", "scopus_author_id"=>"8574051200"}, {"first_name"=>"Michael", "last_name"=>"Farzan", "scopus_author_id"=>"7003535041"}, {"first_name"=>"Dohun", "last_name"=>"Pyeon", "scopus_author_id"=>"6506727649"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84901366269", "issn"=>"19326203", "pui"=>"373152972", "sgr"=>"84901366269", "isbn"=>"1932-6203", "pmid"=>"24827144", "doi"=>"10.1371/journal.pone.0096579"}, "id"=>"b8cc061a-be70-30fe-a99d-db8cb4e1c057", "abstract"=>"Type I interferons (IFN-α and β) induce dynamic host defense mechanisms to inhibit viral infections. It has been recently recognized that the interferon-inducible transmembrane proteins (IFITM) 1, 2 and 3 can block entry of a broad spectrum of RNA viruses. However, no study to date has focused on the role of IFITM proteins in DNA virus restriction. Here, we demonstrate that IFN-α or -β treatment of keratinocytes substantially decreases human papillomavirus 16 (HPV16) infection while robustly inducing IFITM1, 2 and 3 expression. However, IFITM1, 2 and 3 overexpression did not inhibit HPV16 infection; rather, IFITM1 and IFITM3 modestly enhanced HPV16 infection in various cell types including primary keratinocytes. Moreover, IFITM1, 2 and 3 did not inhibit infection by two other DNA viruses, human cytomegalovirus (HCMV) and adenovirus type 5 (Ad5). Taken together, we reveal that the entry of several DNA viruses, including HPV, HCMV, and Ad5 is not affected by IFITM1, 2 and 3 expression. These results imply that HPV, and other DNA viruses, may bypass IFITM restriction during intracellular trafficking.", "link"=>"http://www.mendeley.com/research/antiviral-restriction-factors-ifitm1-2-3-not-inhibit-infection-human-papillomavirus-cytomegalovirus", "reader_count"=>32, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>5, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>9, "Student > Master"=>6, "Other"=>1, "Student > Bachelor"=>6}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>5, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>9, "Student > Master"=>6, "Other"=>1, "Student > Bachelor"=>6}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>8, "Agricultural and Biological Sciences"=>16, "Medicine and Dentistry"=>1, "Arts and Humanities"=>1, "Immunology and Microbiology"=>5}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>5}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>16}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}, "Unspecified"=>{"Unspecified"=>1}, "Arts and Humanities"=>{"Arts and Humanities"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1497267"], "description"=>"<p>(A) Total RNA was isolated from HeLa cells stably expressing scrambled shRNA or shRNA targeting IFITM1 or IFITM3. Expression levels of IFITM1 and IFITM3 mRNA were measured by RT-qPCR and normalized by β-actin mRNA levels. Data are presented as percent change in mRNA expression of knockdown cells compared to cells with scrambled shRNA. (B) Cells in (A) were infected with HPV16-LucF and analyzed as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0096579#pone-0096579-g001\" target=\"_blank\">Figure 1</a>.</p>", "links"=>[], "tags"=>["immunology", "Immune system", "Innate immune system", "immunity", "microbiology", "Virology", "Viral transmission and infection", "Viral entry", "Viruses and cancer", "endogenous", "ifitm1", "ifitm3", "hpv16"], "article_id"=>1026412, "categories"=>["Biological Sciences"], "users"=>["Cody J. Warren", "Laura M. Griffin", "Alexander S. Little", "I-Chueh Huang", "Michael Farzan", "Dohun Pyeon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096579.g004", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Knockdown_of_endogenous_IFITM1_or_IFITM3_does_not_affect_HPV16_infectivity_/1026412", "title"=>"Knockdown of endogenous IFITM1 or IFITM3 does not affect HPV16 infectivity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-14 02:48:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/1497275", "https://ndownloader.figshare.com/files/1497276", "https://ndownloader.figshare.com/files/1497277"], "description"=>"<div><p>Type I interferons (IFN-α and β) induce dynamic host defense mechanisms to inhibit viral infections. It has been recently recognized that the interferon-inducible transmembrane proteins (IFITM) 1, 2 and 3 can block entry of a broad spectrum of RNA viruses. However, no study to date has focused on the role of IFITM proteins in DNA virus restriction. Here, we demonstrate that IFN-α or -β treatment of keratinocytes substantially decreases human papillomavirus 16 (HPV16) infection while robustly inducing IFITM1, 2 and 3 expression. However, IFITM1, 2 and 3 overexpression did not inhibit HPV16 infection; rather, IFITM1 and IFITM3 modestly enhanced HPV16 infection in various cell types including primary keratinocytes. Moreover, IFITM1, 2 and 3 did not inhibit infection by two other DNA viruses, human cytomegalovirus (HCMV) and adenovirus type 5 (Ad5). Taken together, we reveal that the entry of several DNA viruses, including HPV, HCMV, and Ad5 is not affected by IFITM1, 2 and 3 expression. These results imply that HPV, and other DNA viruses, may bypass IFITM restriction during intracellular trafficking.</p></div>", "links"=>[], "tags"=>["immunology", "Immune system", "Innate immune system", "immunity", "microbiology", "Virology", "Viral transmission and infection", "Viral entry", "Viruses and cancer", "antiviral", "inhibit", "cytomegalovirus"], "article_id"=>1026420, "categories"=>["Biological Sciences"], "users"=>["Cody J. Warren", "Laura M. Griffin", "Alexander S. Little", "I-Chueh Huang", "Michael Farzan", "Dohun Pyeon"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0096579.s001", "https://dx.doi.org/10.1371/journal.pone.0096579.s002", "https://dx.doi.org/10.1371/journal.pone.0096579.s003"], "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Antiviral_Restriction_Factors_IFITM1_2_and_3_Do_Not_Inhibit_Infection_of_Human_Papillomavirus_Cytomegalovirus_and_Adenovirus_/1026420", "title"=>"The Antiviral Restriction Factors IFITM1, 2 and 3 Do Not Inhibit Infection of Human Papillomavirus, Cytomegalovirus and Adenovirus", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-05-14 02:48:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/1497266"], "description"=>"<p>HeLa cells overexpressing IFITM1, IFITM2, or IFITM3 were infected with recombinant (A) Ad5-CMV-GFP or (B) HCMV TB40E mCherry and infectivity was measured by flow cytometry at 48 hpi. Gates were set based on the uninfected control and the percentage of fluorescent cells was quantified using FlowJo software (A & B). The results are presented from at least three independent experiments with standard error. (C) HeLa cells overexpressing IFITM proteins were infected with S-protein pseudotyped SARS-CoV luciferase viruses. Infectivity was measured by Bright-Glo Luciferase Assay System (Promega), normalized to the vector alone control, and shown as percent infectivity from triplicate samples representative of two independent experiments. <i>P</i>-values were calculated as described in Fig. 1. Significant differences (**<i>p</i> < 0.01) compared to vector-transduced cells are marked by asterisks.</p>", "links"=>[], "tags"=>["immunology", "Immune system", "Innate immune system", "immunity", "microbiology", "Virology", "Viral transmission and infection", "Viral entry", "Viruses and cancer", "hcmv", "infections", "affected", "overexpression"], "article_id"=>1026411, "categories"=>["Biological Sciences"], "users"=>["Cody J. Warren", "Laura M. Griffin", "Alexander S. Little", "I-Chueh Huang", "Michael Farzan", "Dohun Pyeon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096579.g003", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ad5_and_HCMV_infections_are_not_affected_by_overexpression_of_IFITM1_2_and_3_/1026411", "title"=>"Ad5 and HCMV infections are not affected by overexpression of IFITM1, 2 and 3.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-14 02:48:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/1497265"], "description"=>"<p>HeLa (A & B), A549 (C & D), HaCaT (E & F), and HFK (G & H) cells expressing the indicated c-Myc-tagged IFITMs were inoculated with HPV16-LucF pseudovirions and incubated for 48 h. HPV16 infectivity was measured, as described in Fig. 1. Infectivity data was normalized to the vector alone control and shown as mean % infectivity from quadruplicate samples representative of at least two independent experiments with standard error. <i>P</i>-values were calculated as described in Fig. 1. Significant differences (*<i>p</i> <0.05, **<i>p</i> <0.01, ****<i>p</i> <0.0001) compared to vector transduced cells are marked with asterisks. IFITM protein expression in HeLa (B), A549 (D), HaCaT (F) and HFK (H) cells was measured by western blotting with an anti-c-Myc antibody. Detection of β-actin was used as a loading control. PageRuler plus ladder (Thermo) was used to approximate molecular weights: c-Myc-IFITM1, 18 kD; c-Myc-IFITM2 21 kD; c-Myc-IFITM3, 20 kD; β-actin, 46 kD.</p>", "links"=>[], "tags"=>["immunology", "Immune system", "Innate immune system", "immunity", "microbiology", "Virology", "Viral transmission and infection", "Viral entry", "Viruses and cancer", "ifitm1", "hpv16", "epithelial", "lines"], "article_id"=>1026410, "categories"=>["Biological Sciences"], "users"=>["Cody J. Warren", "Laura M. Griffin", "Alexander S. Little", "I-Chueh Huang", "Michael Farzan", "Dohun Pyeon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096579.g002", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overexpression_of_IFITM1_and_3_enhances_HPV16_infection_in_epithelial_cell_lines_and_primary_keratinocytes_/1026410", "title"=>"Overexpression of IFITM1 and 3 enhances HPV16 infection in epithelial cell lines and primary keratinocytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-14 02:48:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/1497260"], "description"=>"<p>Human keratinocyte HaCaT cells were inoculated with HPV16-LucF pseudovirions after 24 h pre-treatment with (A) IFN-α, IFN-β, or vehicle (PBS) or (B) the indicated concentrations of IFN-β. The reporter luciferase activity (A & B) and cell viability (B) were measured by Bright-Glo Luciferase Assay System (Promega) and CellTiter-Glo Luminescent Cell Viability Assay (Promega), respectively. Mean % infectivity and % viability compared to untreated cells with standard deviations are shown. <i>P</i>-values were calculated by Student’s two-tailed <i>t</i>-test using Prism version 6.0 for Mac, GraphPad software (San Diego California USA, <a href=\"http://www.graphpad.com\" target=\"_blank\">www.graphpad.com</a>). Significant differences (*<i>p</i> < 0.05, **<i>p</i> < 0.01, ***<i>p</i> < 0.001 and ****<i>p</i> < 0.0001) compared to PBS treated cells are marked with asterisks. (C) IFITM1, 2 and 3 expression levels were determined by RT-qPCR using IFITM specific primers (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0096579#pone.0096579.s003\" target=\"_blank\">Table S1</a>). Data are presented as fold change compared to untreated cells. (D) HaCaT cells were treated with 100 U/ml of IFN-β or medium alone and endogenous IFITM1 or IFITM3 protein expression in cell lysate was analyzed by western blotting using specific antibodies. PageRuler plus ladder (Thermo) was used to approximate molecular weights in kilodaltons (kD): IFITM1, 15 kD; IFITM3, 17 kD; β-actin, 46 kD.</p>", "links"=>[], "tags"=>["immunology", "Immune system", "Innate immune system", "immunity", "microbiology", "Virology", "Viral transmission and infection", "Viral entry", "Viruses and cancer", "ifns", "efficiently", "inhibit", "hpv16"], "article_id"=>1026405, "categories"=>["Biological Sciences"], "users"=>["Cody J. Warren", "Laura M. Griffin", "Alexander S. Little", "I-Chueh Huang", "Michael Farzan", "Dohun Pyeon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096579.g001", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Type_I_IFNs_efficiently_inhibit_HPV16_entry_into_human_keratinocytes_/1026405", "title"=>"Type I IFNs efficiently inhibit HPV16 entry into human keratinocytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-14 02:48:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/1497273"], "description"=>"<p>HFKs were infected with 10,000 vge/cell of HPV16 virions and placed at 4°C for 1 h to inhibit endocytosis. Unbound virions were washed away and cells were incubated at 37°C for the indicated time points. Cells were trypsinized to remove non-internalized virions, and then lysed to detect internalized virions by western blotting for L1 capsid protein. Detection of β-actin was used as a loading control. Boxed bands are from a longer exposure. M, mock. *Non-specific band.</p>", "links"=>[], "tags"=>["immunology", "Immune system", "Innate immune system", "immunity", "microbiology", "Virology", "Viral transmission and infection", "Viral entry", "Viruses and cancer", "overexpression", "delays", "degradation", "hpv16", "l1", "capsid"], "article_id"=>1026418, "categories"=>["Biological Sciences"], "users"=>["Cody J. Warren", "Laura M. Griffin", "Alexander S. Little", "I-Chueh Huang", "Michael Farzan", "Dohun Pyeon"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0096579.g005", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_IFITM1_overexpression_delays_degradation_of_HPV16_L1_capsid_protein_in_primary_keratinocytes_/1026418", "title"=>"IFITM1 overexpression delays degradation of HPV16 L1 capsid protein in primary keratinocytes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-05-14 02:48:01"}

PMC Usage Stats | Further Information

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Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Medicine and health sciences", "average_usage"=>[285]}, {"subject_area"=>"/Medicine and health sciences/Anatomy", "average_usage"=>[266]}, {"subject_area"=>"/Medicine and health sciences/Urology", "average_usage"=>[287, 446]}]}
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