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{"title"=>"EndoE from Enterococcus faecalis hydrolyzes the glycans of the biofilm inhibiting protein lactoferrin and mediates growth", "type"=>"journal", "authors"=>[{"first_name"=>"Julia", "last_name"=>"Garbe", "scopus_author_id"=>"36606227600"}, {"first_name"=>"Jonathan", "last_name"=>"Sjögren", "scopus_author_id"=>"41961816000"}, {"first_name"=>"Eoin F.J.", "last_name"=>"Cosgrave", "scopus_author_id"=>"55237805900"}, {"first_name"=>"Weston B.", "last_name"=>"Struwe", "scopus_author_id"=>"35194578400"}, {"first_name"=>"Marta", "last_name"=>"Bober", "scopus_author_id"=>"36245833400"}, {"first_name"=>"Anders I.", "last_name"=>"Olin", "scopus_author_id"=>"7005071980"}, {"first_name"=>"Pauline M.", "last_name"=>"Rudd", "scopus_author_id"=>"7102279599"}, {"first_name"=>"Mattias", "last_name"=>"Collin", "scopus_author_id"=>"7005808079"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-84897394119", "pui"=>"372731697", "doi"=>"10.1371/journal.pone.0091035", "sgr"=>"84897394119", "pmid"=>"24608122"}, "id"=>"68357f45-4e86-3e63-99b9-b279240697c7", "abstract"=>"Glycosidases are widespread among bacteria. The opportunistic human pathogen Enterococcus faecalis encodes several putative glycosidases but little is known about their functions. The identified endo-β-N-acetylglucosaminidase EndoE has activity on the N-linked glycans of the human immunoglobulin G (IgG). In this report we identified the human glycoprotein lactoferrin (hLF) as a new substrate for EndoE. Hydrolysis of the N-glycans from hLF was investigated using lectin blot, UHPLC and mass spectrometry, showing that EndoE releases major glycoforms from this protein. hLF was shown to inhibit biofilm formation of E. faecalis in vitro. Glycans of hLF influence the binding to E. faecalis, and EndoE-hydrolyzed hLF inhibits biofilm formation to lesser extent than intact hLF indicating that EndoE prevents the inhibition of biofilm. In addition, hLF binds to a surface-associated enolase of E. faecalis. Culture experiments showed that the activity of EndoE enables E. faecalis to use the glycans derived from lactoferrin as a carbon source indicating that they could be used as nutrients in vivo when no other preferred carbon source is available. This report adds important information about the enzymatic activity of EndoE from the commensal and opportunist E. faecalis. The activity on the human glycoprotein hLF, and the functional consequences with reduced inhibition of biofilm formation highlights both innate immunity functions of hLF and a bacterial mechanism to evade this innate immunity function. Taken together, our results underline the importance of glycans in the interplay between bacteria and the human host, with possible implications for both commensalism and opportunism.", "link"=>"http://www.mendeley.com/research/endoe-enterococcus-faecalis-hydrolyzes-glycans-biofilm-inhibiting-protein-lactoferrin-mediates-growt", "reader_count"=>12, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Researcher"=>3, "Student > Ph. D. Student"=>1, "Student > Postgraduate"=>2, "Student > Master"=>2, "Student > Bachelor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Researcher"=>3, "Student > Ph. D. Student"=>1, "Student > Postgraduate"=>2, "Student > Master"=>2, "Student > Bachelor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Nursing and Health Professions"=>1, "Agricultural and Biological Sciences"=>3, "Medicine and Dentistry"=>1, "Chemistry"=>3, "Immunology and Microbiology"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>3}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>3}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Unspecified"=>{"Unspecified"=>2}}, "group_count"=>0}

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• http://doi.org/10.1186/s40168-018-0591-4
• http://doi.org/10.1128/AEM.00547-16
• http://doi.org/10.1038/s41564-019-0466-x
• http://doi.org/10.1074/jbc.M116.737395
• http://doi.org/10.4052/tigg.1764.1E
• http://doi.org/10.2217/fmb.14.71
• http://doi.org/10.1128/mBio.02804-19
• http://doi.org/10.3390/antibiotics9110775
• http://doi.org/10.3389/fimmu.2018.00790
• http://doi.org/10.1139/bcb-2020-0253
• http://doi.org/10.3389/fmicb.2015.01521
• http://doi.org/10.1016/j.tim.2018.06.006
• http://doi.org/10.1039/C6CS00897F
• http://doi.org/10.1111/mmi.14390
• http://doi.org/10.1074/jbc.M114.624593
• http://doi.org/10.4052/tigg.1764.1J

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Figshare

• {"files"=>["https://ndownloader.figshare.com/files/1411609"], "description"=>"<p>Bacterial strains and plasmids used in this study.</p>", "links"=>[], "tags"=>["Biochemistry", "glycobiology", "glycoproteins", "metabolism", "Carbohydrate metabolism", "proteins", "DNA-binding proteins", "Defense proteins", "Immune system proteins", "genetics", "Molecular genetics", "Gene regulation", "microbiology", "Bacterial pathogens", "Gram positive", "bacteriology", "Bacterial biofilms", "immunity", "Innate immunity", "Host-pathogen interaction", "Medical microbiology", "Microbial pathogens", "pathogenesis", "strains", "plasmids"], "article_id"=>955085, "categories"=>["Biological Sciences"], "users"=>["Julia Garbe", "Jonathan Sjögren", "Eoin F. J. Cosgrave", "Weston B. Struwe", "Marta Bober", "Anders I. Olin", "Pauline M. Rudd", "Mattias Collin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0091035.t001", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Bacterial_strains_and_plasmids_used_in_this_study_/955085", "title"=>"Bacterial strains and plasmids used in this study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-03-07 02:47:12"}
• {"files"=>["https://ndownloader.figshare.com/files/1411608"], "description"=>"<p>Growth curve of <i>E. faecalis</i> in diluted THB medium (•) and in diluted THB medium supplemented with 2 mg/ml hLF (▪) or isolated N-linked glycans from hLF (▴). Optical density (OD) at 620 nm was determined at indicated time points. Error bars indicate the standard deviation from the mean of three independent experiments.</p>", "links"=>[], "tags"=>["Biochemistry", "glycobiology", "glycoproteins", "metabolism", "Carbohydrate metabolism", "proteins", "DNA-binding proteins", "Defense proteins", "Immune system proteins", "genetics", "Molecular genetics", "Gene regulation", "microbiology", "Bacterial pathogens", "Gram positive", "bacteriology", "Bacterial biofilms", "immunity", "Innate immunity", "Host-pathogen interaction", "Medical microbiology", "Microbial pathogens", "pathogenesis"], "article_id"=>955084, "categories"=>["Biological Sciences"], "users"=>["Julia Garbe", "Jonathan Sjögren", "Eoin F. J. Cosgrave", "Weston B. Struwe", "Marta Bober", "Anders I. Olin", "Pauline M. Rudd", "Mattias Collin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0091035.g007", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Growth_of_Enterococcus_faecalis_in_the_presence_of_lactoferrin_/955084", "title"=>"Growth of <i>Enterococcus faecalis</i> in the presence of lactoferrin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-07 02:47:12"}
• {"files"=>["https://ndownloader.figshare.com/files/1411605"], "description"=>"<p>The depicted glycan structure is based on the Oxford glycan nomenclature <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0091035#pone.0091035-Harvey1\" target=\"_blank\">[56]</a>. Glycans were detected as [M-2H]²⁻ ions. GU values were generated as previously described <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0091035#pone.0091035-Guile1\" target=\"_blank\">[54]</a>. In situations where chromatographic peaks containing multiple structures, the associated peak area was divided equally among the structures for simplicity.</p>", "links"=>[], "tags"=>["Biochemistry", "glycobiology", "glycoproteins", "metabolism", "Carbohydrate metabolism", "proteins", "DNA-binding proteins", "Defense proteins", "Immune system proteins", "genetics", "Molecular genetics", "Gene regulation", "microbiology", "Bacterial pathogens", "Gram positive", "bacteriology", "Bacterial biofilms", "immunity", "Innate immunity", "Host-pathogen interaction", "Medical microbiology", "Microbial pathogens", "pathogenesis", "released", "n-glycans"], "article_id"=>955081, "categories"=>["Biological Sciences"], "users"=>["Julia Garbe", "Jonathan Sjögren", "Eoin F. J. Cosgrave", "Weston B. Struwe", "Marta Bober", "Anders I. Olin", "Pauline M. Rudd", "Mattias Collin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0091035.g004", "stats"=>{"downloads"=>5, "page_views"=>96, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_PNGaseF_released_N_glycans_identified_from_human_lactoferrin_/955081", "title"=>"PNGaseF released N-glycans identified from human lactoferrin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-07 02:47:12"}
• {"files"=>["https://ndownloader.figshare.com/files/1411602"], "description"=>"<p>The depicted glycan structure is based on the Oxford glycan nomenclature <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0091035#pone.0091035-Harvey1\" target=\"_blank\">[56]</a>. Glycans were detected as [M-H] and [M-2H]²⁻ ions. * denotes single charged ions. Glycan names denoted with a subscript E refer to glycans released using EndoE. GU values were generated as previously described <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0091035#pone.0091035-Guile1\" target=\"_blank\">[54]</a>. In situations where chromatographic peaks containing multiple structures, the associated peak area was divided equally among the structures for simplicity.</p>", "links"=>[], "tags"=>["Biochemistry", "glycobiology", "glycoproteins", "metabolism", "Carbohydrate metabolism", "proteins", "DNA-binding proteins", "Defense proteins", "Immune system proteins", "genetics", "Molecular genetics", "Gene regulation", "microbiology", "Bacterial pathogens", "Gram positive", "bacteriology", "Bacterial biofilms", "immunity", "Innate immunity", "Host-pathogen interaction", "Medical microbiology", "Microbial pathogens", "pathogenesis", "released", "n-glycans"], "article_id"=>955078, "categories"=>["Biological Sciences"], "users"=>["Julia Garbe", "Jonathan Sjögren", "Eoin F. J. Cosgrave", "Weston B. Struwe", "Marta Bober", "Anders I. Olin", "Pauline M. Rudd", "Mattias Collin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0091035.g003", "stats"=>{"downloads"=>1, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_EndoE_released_N_glycans_identified_from_human_lactoferrin_/955078", "title"=>"EndoE released N-glycans identified from human lactoferrin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-07 02:47:12"}
• {"files"=>["https://ndownloader.figshare.com/files/1411610"], "description"=>"<div><p>Glycosidases are widespread among bacteria. The opportunistic human pathogen <i>Enterococcus faecalis</i> encodes several putative glycosidases but little is known about their functions. The identified endo-β-<i>N</i>-acetylglucosaminidase EndoE has activity on the N-linked glycans of the human immunoglobulin G (IgG). In this report we identified the human glycoprotein lactoferrin (hLF) as a new substrate for EndoE. Hydrolysis of the N-glycans from hLF was investigated using lectin blot, UHPLC and mass spectrometry, showing that EndoE releases major glycoforms from this protein. hLF was shown to inhibit biofilm formation of <i>E. faecalis in vitro</i>. Glycans of hLF influence the binding to <i>E. faecalis,</i> and EndoE-hydrolyzed hLF inhibits biofilm formation to lesser extent than intact hLF indicating that EndoE prevents the inhibition of biofilm. In addition, hLF binds to a surface-associated enolase of <i>E. faecalis</i>. Culture experiments showed that the activity of EndoE enables <i>E. faecalis</i> to use the glycans derived from lactoferrin as a carbon source indicating that they could be used as nutrients <i>in vivo</i> when no other preferred carbon source is available. This report adds important information about the enzymatic activity of EndoE from the commensal and opportunist <i>E. faecalis</i>. The activity on the human glycoprotein hLF, and the functional consequences with reduced inhibition of biofilm formation highlights both innate immunity functions of hLF and a bacterial mechanism to evade this innate immunity function. Taken together, our results underline the importance of glycans in the interplay between bacteria and the human host, with possible implications for both commensalism and opportunism.</p></div>", "links"=>[], "tags"=>["Biochemistry", "glycobiology", "glycoproteins", "metabolism", "Carbohydrate metabolism", "proteins", "DNA-binding proteins", "Defense proteins", "Immune system proteins", "genetics", "Molecular genetics", "Gene regulation", "microbiology", "Bacterial pathogens", "Gram positive", "bacteriology", "Bacterial biofilms", "immunity", "Innate immunity", "Host-pathogen interaction", "Medical microbiology", "Microbial pathogens", "pathogenesis", "endoe", "hydrolyzes", "glycans", "biofilm", "inhibiting", "lactoferrin", "mediates"], "article_id"=>955086, "categories"=>["Biological Sciences"], "users"=>["Julia Garbe", "Jonathan Sjögren", "Eoin F. J. Cosgrave", "Weston B. Struwe", "Marta Bober", "Anders I. Olin", "Pauline M. Rudd", "Mattias Collin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0091035", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/EndoE_from_Enterococcus_faecalis_Hydrolyzes_the_Glycans_of_the_Biofilm_Inhibiting_Protein_Lactoferrin_and_Mediates_Growth/955086", "title"=>"EndoE from <i>Enterococcus faecalis</i> Hydrolyzes the Glycans of the Biofilm Inhibiting Protein Lactoferrin and Mediates Growth", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-03-07 02:47:12"}
• {"files"=>["https://ndownloader.figshare.com/files/1411607"], "description"=>"<p>A. Western blot analysis, using anti-lactoferrin antibodies, of human lactoferrin (hLF) bound to <i>E. faecalis</i> OG1. <i>E. faecalis</i> was incubated with indicated concentrations of hLF or EndoE treated hLF (de-hLF). <i>E. faecalis</i> cell extract was separated on 10% SDS-PAGE and electro-blotted onto PVDF membranes. Control: 1 µg hLF. B. Binding of different hLF concentrations to recombinant enolase immobilized to a microtiter plate. Anti-hLF antibodies were used to detect the binding of hLF to the enolase. Error bars indicate the standard deviation from the mean of three independent experiments.</p>", "links"=>[], "tags"=>["Biochemistry", "glycobiology", "glycoproteins", "metabolism", "Carbohydrate metabolism", "proteins", "DNA-binding proteins", "Defense proteins", "Immune system proteins", "genetics", "Molecular genetics", "Gene regulation", "microbiology", "Bacterial pathogens", "Gram positive", "bacteriology", "Bacterial biofilms", "immunity", "Innate immunity", "Host-pathogen interaction", "Medical microbiology", "Microbial pathogens", "pathogenesis", "lactoferrin", "recombinant"], "article_id"=>955083, "categories"=>["Biological Sciences"], "users"=>["Julia Garbe", "Jonathan Sjögren", "Eoin F. J. Cosgrave", "Weston B. Struwe", "Marta Bober", "Anders I. Olin", "Pauline M. Rudd", "Mattias Collin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0091035.g006", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Binding_of_human_lactoferrin_to_the_surface_of_Enterococcus_faecalis_and_recombinant_enolase_/955083", "title"=>"Binding of human lactoferrin to the surface of <i>Enterococcus faecalis</i> and recombinant enolase.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-07 02:47:12"}
• {"files"=>["https://ndownloader.figshare.com/files/1411606"], "description"=>"<p>Biofilm formation of <i>E. faecalis</i> was measured using the crystal violet assay and is expressed as OD₅₅₀. Human lactoferrin (hLF) was added either fully glycosylated (hLF) or deglycosylated (de-hLF) due to the treatment with EndoE. Error bars indicate the standard deviation from the mean of three independent experiments with three replicates. w/o: no hLF added.</p>", "links"=>[], "tags"=>["Biochemistry", "glycobiology", "glycoproteins", "metabolism", "Carbohydrate metabolism", "proteins", "DNA-binding proteins", "Defense proteins", "Immune system proteins", "genetics", "Molecular genetics", "Gene regulation", "microbiology", "Bacterial pathogens", "Gram positive", "bacteriology", "Bacterial biofilms", "immunity", "Innate immunity", "Host-pathogen interaction", "Medical microbiology", "Microbial pathogens", "pathogenesis", "lactoferrin", "biofilm"], "article_id"=>955082, "categories"=>["Biological Sciences"], "users"=>["Julia Garbe", "Jonathan Sjögren", "Eoin F. J. Cosgrave", "Weston B. Struwe", "Marta Bober", "Anders I. Olin", "Pauline M. Rudd", "Mattias Collin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0091035.g005", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Influence_of_human_lactoferrin_on_biofilm_formation_of_Enterococcus_faecalis_/955082", "title"=>"Influence of human lactoferrin on biofilm formation of <i>Enterococcus faecalis</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-07 02:47:12"}
• {"files"=>["https://ndownloader.figshare.com/files/1411601"], "description"=>"<p>Hydrophilic interaction liquid chromatography (HILIC)-fluorescence chromatogram of 2-AB labeled glycans released from human lactoferrin by the endoglycosidase EndoE (A) and the endoglycosidase PNGaseF, respectively (B). Identified glycans are separated into peaks. The numbers correspond to the glycan structures depicted in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0091035#pone-0091035-g003\" target=\"_blank\">Figure 3</a> and <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0091035#pone-0091035-g004\" target=\"_blank\">4</a>.</p>", "links"=>[], "tags"=>["Biochemistry", "glycobiology", "glycoproteins", "metabolism", "Carbohydrate metabolism", "proteins", "DNA-binding proteins", "Defense proteins", "Immune system proteins", "genetics", "Molecular genetics", "Gene regulation", "microbiology", "Bacterial pathogens", "Gram positive", "bacteriology", "Bacterial biofilms", "immunity", "Innate immunity", "Host-pathogen interaction", "Medical microbiology", "Microbial pathogens", "pathogenesis"], "article_id"=>955077, "categories"=>["Biological Sciences"], "users"=>["Julia Garbe", "Jonathan Sjögren", "Eoin F. J. Cosgrave", "Weston B. Struwe", "Marta Bober", "Anders I. Olin", "Pauline M. Rudd", "Mattias Collin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0091035.g002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Glycan_analysis_of_lactoferrin_/955077", "title"=>"Glycan analysis of lactoferrin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-07 02:47:12"}
• {"files"=>["https://ndownloader.figshare.com/files/1411600"], "description"=>"<p>A. Human lactoferrin (hLF) was incubated with EndoE, EndoE(E186Q) and EndoE(E662Q), separated on 10% SDS-PAGE and stained with Coomassie (upper panel), or electro-blotted onto PVDF membranes and was analyzed with ConA lectin (lower panel). Incubation of hLF with PBS was used as a negative control. B. Plasmon surface resonance assay to analyze binding of EndoE to hLF. The plots show binding of EndoE(E186Q) and EndoE(E662Q) to hLF.</p>", "links"=>[], "tags"=>["Biochemistry", "glycobiology", "glycoproteins", "metabolism", "Carbohydrate metabolism", "proteins", "DNA-binding proteins", "Defense proteins", "Immune system proteins", "genetics", "Molecular genetics", "Gene regulation", "microbiology", "Bacterial pathogens", "Gram positive", "bacteriology", "Bacterial biofilms", "immunity", "Innate immunity", "Host-pathogen interaction", "Medical microbiology", "Microbial pathogens", "pathogenesis", "binding", "endoe"], "article_id"=>955076, "categories"=>["Biological Sciences"], "users"=>["Julia Garbe", "Jonathan Sjögren", "Eoin F. J. Cosgrave", "Weston B. Struwe", "Marta Bober", "Anders I. Olin", "Pauline M. Rudd", "Mattias Collin"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0091035.g001", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Activity_on_and_binding_of_EndoE_to_human_lactoferrin_/955076", "title"=>"Activity on and binding of EndoE to human lactoferrin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-03-07 02:47:12"}

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Relative Metric

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F1000Prime