Lipopolysaccharide O-Antigen Prevents Phagocytosis of Vibrio anguillarum by Rainbow Trout (Oncorhynchus mykiss) Skin Epithelial Cells
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{"title"=>"Lipopolysaccharide O-antigen prevents phagocytosis of vibrio anguillarum by rainbow trout (oncorhynchus mykiss) skin epithelial cells", "type"=>"journal", "authors"=>[{"first_name"=>"Kristoffer", "last_name"=>"Lindell", "scopus_author_id"=>"36157106300"}, {"first_name"=>"Anna", "last_name"=>"Fahlgren", "scopus_author_id"=>"56619724500"}, {"first_name"=>"Erik", "last_name"=>"Hjerde", "scopus_author_id"=>"16636616300"}, {"first_name"=>"Nils Peder", "last_name"=>"Willassen", "scopus_author_id"=>"6603827475"}, {"first_name"=>"Maria", "last_name"=>"Fällman", "scopus_author_id"=>"7004226474"}, {"first_name"=>"Debra L.", "last_name"=>"Milton", "scopus_author_id"=>"55400028400"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "isbn"=>"1932-6203", "sgr"=>"84861473544", "doi"=>"10.1371/journal.pone.0037678", "scopus"=>"2-s2.0-84861473544", "pui"=>"364882915", "pmid"=>"22662189"}, "id"=>"fc4b59f8-7288-3664-83e2-64e863a0597d", "abstract"=>"Colonization of host tissues is a first step taken by many pathogens during the initial stages of infection. Despite the impact of bacterial disease on wild and farmed fish, only a few direct studies have characterized bacterial factors required for colonization of fish tissues. In this study, using live-cell and confocal microscopy, rainbow trout skin epithelial cells, the main structural component of the skin epidermis, were demonstrated to phagocytize bacteria. Mutant analyses showed that the fish pathogen Vibrio anguillarum required the lipopolysaccharide O-antigen to evade phagocytosis and that O-antigen transport required the putative wzm-wzt-wbhA operon, which encodes two ABC polysaccharide transporter proteins and a methyltransferase. Pretreatment of the epithelial cells with mannose prevented phagocytosis of V. anguillarum suggesting that a mannose receptor is involved in the uptake process. In addition, the O-antigen transport mutants could not colonize the skin but they did colonize the intestines of rainbow trout. The O-antigen polysaccharides were also shown to aid resistance to the antimicrobial factors, lysozyme and polymyxin B. In summary, rainbow trout skin epithelial cells play a role in the fish innate immunity by clearing bacteria from the skin epidermis. In defense, V. anguillarum utilizes O-antigen polysaccharides to evade phagocytosis by the epithelial cells allowing it to colonize rapidly fish skin tissues.", "link"=>"http://www.mendeley.com/research/lipopolysaccharide-oantigen-prevents-phagocytosis-vibrio-anguillarum-rainbow-trout-oncorhynchus-myki", "reader_count"=>24, "reader_count_by_academic_status"=>{"Researcher"=>6, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>1, "Other"=>2, "Student > Master"=>2, "Student > Bachelor"=>5, "Professor"=>3, "Lecturer"=>1}, "reader_count_by_user_role"=>{"Researcher"=>6, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>3, "Student > Postgraduate"=>1, "Other"=>2, "Student > Master"=>2, "Student > Bachelor"=>5, "Professor"=>3, "Lecturer"=>1}, "reader_count_by_subject_area"=>{"Agricultural and Biological Sciences"=>22, "Immunology and Microbiology"=>1, "Medicine and Dentistry"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>22}}, "reader_count_by_country"=>{"Colombia"=>2, "Iran"=>1, "Indonesia"=>2}, "group_count"=>0}

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  • {"files"=>["https://ndownloader.figshare.com/files/632422"], "description"=>"<p>(A) Lipopolysaccharides were fractionated by 15%-SDS-PAGE and detected using the Pro-Q® Emerald 300 Lipopolysaccharide Gel Stain Kit (Invitrogen). (B) Exopolysaccharides were extracted from culture supernatants and quantified using an Alcian blue technique described by Plante <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0037678#pone.0037678-Plante1\" target=\"_blank\">[56]</a>. The amount of EPS is given as an OD<sub>620</sub> reading. For both (A) and (B), strains are designated by their mutation. Mutation designations followed by a C are complemented with the respective wild-type gene.</p>", "links"=>[], "tags"=>["exopolysaccharide"], "article_id"=>302916, "categories"=>["Microbiology", "Infectious Diseases"], "users"=>["Kristoffer Lindell", "Anna Fahlgren", "Erik Hjerde", "Nils-Peder Willassen", "Maria Fällman", "Debra L. Milton"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0037678.g003", "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lipopolysaccharide_and_exopolysaccharide_analyses_/302916", "title"=>"Lipopolysaccharide and exopolysaccharide analyses.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-25 00:48:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/632360"], "description"=>"<p>(A) The genetic locus was identified from the draft genome sequence of the NB10 <i>V. anguillarum</i> strain (unpublished data, E. Hjerde, D.L. Milton, and N.P. Willassen). Each open reading frame (Orf) is indicated by a box and the direction of transcription is indicated by an arrowhead within each box. Grey boxes indicate the genes under investigation in this study, which are suggested to be involved in the transport of O-antigen polysaccharide. <i>wbhA</i> encodes a putative S-adenosylmethionine methyltransferase and <i>wzt</i> and <i>wzm</i> encode components of an ABC-2 subfamily of polysaccharide transporters. The four <i>rml</i> genes have homology to proteins involved in the biosynthesis of dTDP-L-rhamnose, a possible O-antigen precursor <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0037678#pone.0037678-Welch1\" target=\"_blank\">[42]</a>. <i>rmlC</i> encodes a dTDP-6-deoxy-D-glucose-3,5-epimerase; <i>rmlD</i> encodes dTDP-6-deoxy-L-mannose dehydrogenase; <i>rmlA</i> encodes glucose-1-phosphate thymidylyltransferase; <i>rmlB</i> encodes dTDP-glucose 4,6-dehydratase. OrfA and OrfB are both part of two putative operons that encode proteins likely involved LPS biosynthesis. Orfs downstream of <i>wbhA</i> encode two putative transposases and a hypothetical protein. (B) A cartoon image of the structure of Gram-negative lipopolysaccharide. The lipopolysaccharide is a component of the outer membrane in Gram-negative bacteria and is composed of lipid A, core polysaccharide, and the O-antigen, which is a repeating sugar unit. OM, outer cell membrane; P, peptidoglycan; IM, inner membrane.</p>", "links"=>[], "tags"=>["o-antigen", "biosynthesis", "containing"], "article_id"=>302853, "categories"=>["Microbiology", "Infectious Diseases"], "users"=>["Kristoffer Lindell", "Anna Fahlgren", "Erik Hjerde", "Nils-Peder Willassen", "Maria Fällman", "Debra L. Milton"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0037678.g002", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genetic_organization_of_the_O_antigen_biosynthesis_gene_cluster_containing_wzm_wzt_wbhA_/302853", "title"=>"Genetic organization of the O-antigen biosynthesis gene cluster containing <i>wzm-wzt-wbhA</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-25 00:47:33"}
  • {"files"=>["https://ndownloader.figshare.com/files/632847"], "description"=>"<p>Cultures of <i>V. anguillarum</i> grown to an OD<sub>600</sub> of 0.2 (10<sup>8</sup> cells ml<sup>−1</sup>) were diluted 10-fold in PBS containing either (A) 10 µg ml<sup>−1</sup> of lysozyme or (B) 10 ng ml<sup>−1</sup> of polymyxin B sulfate. Bacterial survival was measured at room temperature by determining the cfu in each sample at 0 min and 20 min for lysozyme and 0 min and 1 h for polymyxin B sulfate. Percent survival is the average of three experiments. Asterisks indicate a p-value of <0.05 as determined by the Student's t-test. Strains are designated by their mutation. Mutation designations followed by a C are complemented.</p>", "links"=>[], "tags"=>["strains", "antimicrobial"], "article_id"=>303339, "categories"=>["Microbiology", "Infectious Diseases"], "users"=>["Kristoffer Lindell", "Anna Fahlgren", "Erik Hjerde", "Nils-Peder Willassen", "Maria Fällman", "Debra L. Milton"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0037678.g008", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sensitivity_of_V_anguillarum_strains_to_antimicrobial_products_/303339", "title"=>"Sensitivity of <i>V. anguillarum</i> strains to antimicrobial products.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-25 00:55:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/632223"], "description"=>"<p>Using live-cell microscopy, a video clip (<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0037678#pone.0037678.s001\" target=\"_blank\">Video S1</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0037678#pone.0037678.s002\" target=\"_blank\">S2</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0037678#pone.0037678.s003\" target=\"_blank\">S3</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0037678#pone.0037678.s006\" target=\"_blank\">S6</a>, and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0037678#pone.0037678.s007\" target=\"_blank\">S7</a> supporting information) was recorded of the phagocytic activity of rainbow trout skin epithelial cells after infection with the wild type, the KM97 transposon mutant, the Δ<i>wzt</i> mutant, and the Δ<i>wzt</i> mutant complemented with the wild-type <i>wzt</i> gene. Three frames from each video progressing in time from left to right are shown indicating the phagocytic activity of an epithelial cell after contact with each strain. Similar videos were made for the Δ<i>wzm</i> and Δ<i>wbhA</i> mutants, and similar results to that of the Δ<i>wzt</i> mutant were seen (supporting information <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0037678#pone.0037678.s004\" target=\"_blank\">Videos S4</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0037678#pone.0037678.s005\" target=\"_blank\">S5</a>). Thus, the Δ<i>wzt</i> mutant results are given as a representative for all three mutant strains. In the first frame from each video, three bacterial cells were circled and labeled. These three bacteria were followed in the two additional time frames to indicate movement of the bacteria during the movie. If the cell is no longer labeled in frames 2 and 3, then the bacterial cell was displaced from the glass surface and swam away. In the bottom set of frames, the epithelial cells were pretreated with 1 mM mannose before infection with the Δ<i>wzt</i> mutant. The three-image sets are designated by the strain mutation to the left and mutation designations followed by a C are complemented.</p>", "links"=>[], "tags"=>["frames", "points", "live-cell", "microscopy", "videos", "rainbow", "trout", "epithelial", "cells"], "article_id"=>302701, "categories"=>["Microbiology", "Infectious Diseases"], "users"=>["Kristoffer Lindell", "Anna Fahlgren", "Erik Hjerde", "Nils-Peder Willassen", "Maria Fällman", "Debra L. Milton"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0037678.g001", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Image_frames_from_various_time_points_of_live_cell_microscopy_videos_of_rainbow_trout_skin_epithelial_cells_following_infection_with_various_V_anguillarum_strains_/302701", "title"=>"Image frames from various time points of live-cell microscopy videos of rainbow trout skin epithelial cells following infection with various <i>V. anguillarum</i> strains.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-25 00:45:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/632917"], "description"=>"a<p>All strains contain pNQFlaC4-lac:lux, which carries the <i>luxCDABE</i> operon and is integrated into the chromosome.</p>", "links"=>[], "tags"=>["spleen", "infected"], "article_id"=>303407, "categories"=>["Microbiology", "Infectious Diseases"], "users"=>["Kristoffer Lindell", "Anna Fahlgren", "Erik Hjerde", "Nils-Peder Willassen", "Maria Fällman", "Debra L. Milton"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0037678.t001", "stats"=>{"downloads"=>10, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Colonization_frequency_of_the_skin_intestines_and_spleen_in_each_infected_fish_group_/303407", "title"=>"Colonization frequency of the skin, intestines, and spleen in each infected fish group.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-05-25 00:56:47"}
  • {"files"=>["https://ndownloader.figshare.com/files/327541", "https://ndownloader.figshare.com/files/327594", "https://ndownloader.figshare.com/files/327676", "https://ndownloader.figshare.com/files/327754", "https://ndownloader.figshare.com/files/327816", "https://ndownloader.figshare.com/files/327874", "https://ndownloader.figshare.com/files/327927", "https://ndownloader.figshare.com/files/328003", "https://ndownloader.figshare.com/files/328077"], "description"=>"<div><p>Colonization of host tissues is a first step taken by many pathogens during the initial stages of infection. Despite the impact of bacterial disease on wild and farmed fish, only a few direct studies have characterized bacterial factors required for colonization of fish tissues. In this study, using live-cell and confocal microscopy, rainbow trout skin epithelial cells, the main structural component of the skin epidermis, were demonstrated to phagocytize bacteria. Mutant analyses showed that the fish pathogen <em>Vibrio anguillarum</em> required the lipopolysaccharide O-antigen to evade phagocytosis and that O-antigen transport required the putative <em>wzm-wzt-wbhA</em> operon, which encodes two ABC polysaccharide transporter proteins and a methyltransferase. Pretreatment of the epithelial cells with mannose prevented phagocytosis of <em>V. anguillarum</em> suggesting that a mannose receptor is involved in the uptake process. In addition, the O-antigen transport mutants could not colonize the skin but they did colonize the intestines of rainbow trout. The O-antigen polysaccharides were also shown to aid resistance to the antimicrobial factors, lysozyme and polymyxin B. In summary, rainbow trout skin epithelial cells play a role in the fish innate immunity by clearing bacteria from the skin epidermis. In defense, <em>V. anguillarum</em> utilizes O-antigen polysaccharides to evade phagocytosis by the epithelial cells allowing it to colonize rapidly fish skin tissues.</p> </div>", "links"=>[], "tags"=>["lipopolysaccharide", "o-antigen", "prevents", "phagocytosis", "rainbow", "trout", "epithelial", "cells"], "article_id"=>124658, "categories"=>["Cancer", "Microbiology"], "users"=>["Kristoffer Lindell", "Anna Fahlgren", "Erik Hjerde", "Nils-Peder Willassen", "Maria Fällman", "Debra L. Milton"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0037678.s001", "https://dx.doi.org/10.1371/journal.pone.0037678.s002", "https://dx.doi.org/10.1371/journal.pone.0037678.s003", "https://dx.doi.org/10.1371/journal.pone.0037678.s004", "https://dx.doi.org/10.1371/journal.pone.0037678.s005", "https://dx.doi.org/10.1371/journal.pone.0037678.s006", "https://dx.doi.org/10.1371/journal.pone.0037678.s007", "https://dx.doi.org/10.1371/journal.pone.0037678.s008", "https://dx.doi.org/10.1371/journal.pone.0037678.s009"], "stats"=>{"downloads"=>14, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Lipopolysaccharide_O_Antigen_Prevents_Phagocytosis_of_Vibrio_anguillarum_by_Rainbow_Trout_Oncorhynchus_mykiss_Skin_Epithelial_Cells/124658", "title"=>"Lipopolysaccharide O-Antigen Prevents Phagocytosis of <em>Vibrio anguillarum</em> by Rainbow Trout (<em>Oncorhynchus mykiss</em>) Skin Epithelial Cells", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-05-25 01:17:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/632665"], "description"=>"<p><i>Vibrio anguillarum</i> strains carrying pNQFlaC4-lac::lux on the chromosome were grown to 5×10<sup>8</sup> cells ml<sup>−1</sup> and serially diluted in a black 96-well plate. Cfu counts were determined for each culture. A bioluminescent image of the 96-well plate was taken using an IVIS® SPECTRUM system (Xenogen, Caliper Life Sciences) and photon units (photons sec<sup>−1</sup> cm<sup>−2</sup> steradian<sup>−1</sup>) emitting from each well were determined. Strains are designated by their mutation and mutation designations followed by a C are complemented.</p>", "links"=>[], "tags"=>["photon"], "article_id"=>303158, "categories"=>["Microbiology", "Infectious Diseases"], "users"=>["Kristoffer Lindell", "Anna Fahlgren", "Erik Hjerde", "Nils-Peder Willassen", "Maria Fällman", "Debra L. Milton"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0037678.g006", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Correlation_of_photon_emission_with_the_number_of_V_anguillarum_cells_/303158", "title"=>"Correlation of photon emission with the number of <i>V. anguillarum</i> cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-25 00:52:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/632517"], "description"=>"<p>Skin epithelial cells were infected with the wild type and the Δ<i>wzt</i>, Δ<i>wzm</i>, and Δ<i>wbhA</i> mutants. Following fixation, the epithelial cells were visualized by labeling actin with Alexa Fluor 568 phalloidin (red). After permeabilization of the epithelial cell, bacteria were labeled using a whole-cell antiserum and a FITC-conjugated Donkey anti-rabbit IgG (green). Using the NIS-elements AR 3.2 software, a 3D rendering of a confocal microscopy z-stack covering an entire cell was done and is presented as the left most image for each strain. In each image, the phalloidin (red) signal was progressively cropped along the z-axis to reveal internal bacteria. Strains are designated by their mutations and the designations are given to the left of the image.</p>", "links"=>[], "tags"=>["microscopy", "3d-imaging", "rainbow", "trout", "epithelial", "cells"], "article_id"=>303001, "categories"=>["Microbiology", "Infectious Diseases"], "users"=>["Kristoffer Lindell", "Anna Fahlgren", "Erik Hjerde", "Nils-Peder Willassen", "Maria Fällman", "Debra L. Milton"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0037678.g004", "stats"=>{"downloads"=>5, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Confocal_microscopy_3D_imaging_of_rainbow_trout_skin_epithelial_cells_following_infections_/303001", "title"=>"Confocal microscopy 3D-imaging of rainbow trout skin epithelial cells following infections.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-25 00:50:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/632731"], "description"=>"<p>Rainbow trout (20 g) were infected with <i>V. anguillarum</i> strains carrying pNQFlaC4-lac::lux by bathing in infected seawater. At 24 h and 48 h, fish were sacrificed and images of the fish were obtained as described in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0037678#s4\" target=\"_blank\">Materials and Methods</a>. To image internal organs, one side of the fish was removed after the skin was imaged. To measure photons from the intestines, the contents were pushed out the anus and are indicated by a white arrow. A blue arrow indicates the spleen. Strains are designated by their mutation. Mutation designations followed by a C are complemented.</p>", "links"=>[], "tags"=>["imaging", "infections", "rainbow"], "article_id"=>303225, "categories"=>["Microbiology", "Infectious Diseases"], "users"=>["Kristoffer Lindell", "Anna Fahlgren", "Erik Hjerde", "Nils-Peder Willassen", "Maria Fällman", "Debra L. Milton"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0037678.g007", "stats"=>{"downloads"=>2, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bioluminescent_imaging_of_V_anguillarum_infections_in_rainbow_trout_/303225", "title"=>"Bioluminescent imaging of <i>V. anguillarum</i> infections in rainbow trout.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-25 00:53:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/632613"], "description"=>"<p>Epithelial cells were isolated from the skin of rainbow trout and either left untreated (closed bars) or pretreated with 1 mM mannose (open bars) before infection with 10<sup>5</sup> bacteria ml<sup>−1</sup>. Following a 3 h infection, the epithelial cells were fixed and the epithelial cells and bacteria were fluorescently labeled. Confocal 3D-imaging microscopy was done on at least 100 single epithelial cells from three separate experiments to determine the number of cells that contained bacteria. These data are presented as a percent. The <i>V. anguillarum</i> strains that were tested are designated by their mutation. Mutation designations followed by a C are complemented with the respective wild-type gene. Asterisks indicate a p-value of <0.05 as determined by the Student's t-test.</p>", "links"=>[], "tags"=>["phagocytic", "rainbow", "trout", "epithelial", "cells"], "article_id"=>303100, "categories"=>["Microbiology", "Infectious Diseases"], "users"=>["Kristoffer Lindell", "Anna Fahlgren", "Erik Hjerde", "Nils-Peder Willassen", "Maria Fällman", "Debra L. Milton"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0037678.g005", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Quantification_of_phagocytic_activity_by_rainbow_trout_skin_epithelial_cells_following_infection_with_various_V_anguillarum_strains_/303100", "title"=>"Quantification of phagocytic activity by rainbow trout skin epithelial cells following infection with various <i>V. anguillarum</i> strains.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-25 00:51:40"}

PMC Usage Stats | Further Information

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