Identification of the Rheumatoid Arthritis Shared Epitope Binding Site on Calreticulin
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{"title"=>"Identification of the rheumatoid arthritis shared epitope binding site on calreticulin", "type"=>"journal", "authors"=>[{"first_name"=>"Song", "last_name"=>"Ling", "scopus_author_id"=>"36245665700"}, {"first_name"=>"Andrew", "last_name"=>"Cheng", "scopus_author_id"=>"57195992251"}, {"first_name"=>"Paul", "last_name"=>"Pumpens", "scopus_author_id"=>"35587026900"}, {"first_name"=>"Marek", "last_name"=>"Michalak", "scopus_author_id"=>"7005541058"}, {"first_name"=>"Joseph", "last_name"=>"Holoshitz", "scopus_author_id"=>"6603824008"}], "year"=>2010, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-77955464552", "sgr"=>"77955464552", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"20661469", "doi"=>"10.1371/journal.pone.0011703", "pui"=>"359322521"}, "id"=>"905b4ca4-b9cd-323c-8f8e-398203408992", "abstract"=>"BACKGROUND: The rheumatoid arthritis (RA) shared epitope (SE), a major risk factor for severe disease, is a five amino acid motif in the third allelic hypervariable region of the HLA-DRbeta chain. The molecular mechanisms by which the SE affects susceptibility to--and severity of--RA are unknown. We have recently demonstrated that the SE acts as a ligand that interacts with cell surface calreticulin (CRT) and activates innate immune signaling. In order to better understand the molecular basis of SE-RA association, here we have undertaken to map the SE binding site on CRT.\\n\\nPRINCIPAL FINDINGS: Surface plasmon resonance (SPR) experiments with domain deletion mutants suggested that the SE binding site is located in the P-domain of CRT. The role of this domain as a SE-binding region was further confirmed by a sulfosuccinimidyl-2-[6-(biotinamido)-2-(p-azido-benzamido) hexanoamido] ethyl-1,3-dithiopropionate (sulfo-SBED) photoactive cross-linking method. In silico analysis of docking interactions between a conformationally intact SE ligand and the CRT P-domain predicted the region within amino acid residues 217-224 as a potential SE binding site. Site-directed mutagenesis demonstrated involvement of residues Glu(217) and Glu(223)--and to a lesser extent residue Asp(220)--in cell-free SPR-based binding and signal transduction assays.\\n\\nSIGNIFICANCE: We have characterized here the molecular basis of a novel ligand-receptor interaction between the SE and CRT. The interaction represents a structurally and functionally well-defined example of cross talk between the adaptive and innate immune systems that could advance our understanding of the pathogenesis of autoimmunity.", "link"=>"http://www.mendeley.com/research/identification-rheumatoid-arthritis-shared-epitope-binding-site-calreticulin", "reader_count"=>21, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Librarian"=>1, "Researcher"=>4, "Student > Ph. D. Student"=>7, "Student > Master"=>2, "Other"=>1, "Student > Bachelor"=>3, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Librarian"=>1, "Researcher"=>4, "Student > Ph. D. Student"=>7, "Student > Master"=>2, "Other"=>1, "Student > Bachelor"=>3, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>1, "Materials Science"=>1, "Agricultural and Biological Sciences"=>13, "Medicine and Dentistry"=>3, "Chemistry"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Materials Science"=>{"Materials Science"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Chemistry"=>{"Chemistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>13}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>1}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Sweden"=>1, "United States"=>1, "Norway"=>1, "India"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/417995", "https://ndownloader.figshare.com/files/418002"], "description"=>"<div><h3>Background</h3><p>The rheumatoid arthritis (RA) shared epitope (SE), a major risk factor for severe disease, is a five amino acid motif in the third allelic hypervariable region of the HLA-DRβ chain. The molecular mechanisms by which the SE affects susceptibility to – and severity of - RA are unknown. We have recently demonstrated that the SE acts as a ligand that interacts with cell surface calreticulin (CRT) and activates innate immune signaling. In order to better understand the molecular basis of SE-RA association, here we have undertaken to map the SE binding site on CRT.</p><h3>Principal Findings</h3><p>Surface plasmon resonance (SPR) experiments with domain deletion mutants suggested that the SE binding site is located in the P-domain of CRT. The role of this domain as a SE-binding region was further confirmed by a sulfosuccinimidyl-2-[6-(biotinamido)-2-(<em>p</em>-azido-benzamido) hexanoamido] ethyl-1,3-dithiopropionate (sulfo-SBED) photoactive cross-linking method. <em>In silico</em> analysis of docking interactions between a conformationally intact SE ligand and the CRT P-domain predicted the region within amino acid residues 217–224 as a potential SE binding site. Site-directed mutagenesis demonstrated involvement of residues Glu<sup>217</sup> and Glu<sup>223</sup> - and to a lesser extent residue Asp<sup>220</sup> - in cell-free SPR-based binding and signal transduction assays.</p><h3>Significance</h3><p>We have characterized here the molecular basis of a novel ligand-receptor interaction between the SE and CRT. The interaction represents a structurally and functionally well-defined example of cross talk between the adaptive and innate immune systems that could advance our understanding of the pathogenesis of autoimmunity.</p></div>", "links"=>[], "tags"=>["rheumatoid", "arthritis", "epitope", "binding", "calreticulin"], "article_id"=>142534, "categories"=>["Immunology"], "users"=>["Song Ling", "Andrew Cheng", "Paul Pumpens", "Marek Michalak", "Joseph Holoshitz"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0011703.s001", "https://dx.doi.org/10.1371/journal.pone.0011703.s002"], "stats"=>{"downloads"=>12, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Identification_of_the_Rheumatoid_Arthritis_Shared_Epitope_Binding_Site_on_Calreticulin/142534", "title"=>"Identification of the Rheumatoid Arthritis Shared Epitope Binding Site on Calreticulin", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-07-22 00:42:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/839595"], "description"=>"<p><b>A</b>. Structural formula of Sulfo-SBED. <b>B</b>. MS analysis of trypsinized sulfo-SBED-labeled CRT fragments. <b>C</b>. MS/MS data of peak 2047.1 (marked as “C” in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011703#pone-0011703-g002\" target=\"_blank\">Fig. 2B</a>) identifying CRT segment 196-KIKDPDASKPEDWDER-211. <b>D</b>. MS/MS data of peak 1838 (marked as “D” in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011703#pone-0011703-g002\" target=\"_blank\">Fig. 2B</a>) identifying CRT segment 262-GEWKPRQIDNPDYK-275. <b>E</b>. Spatial proximity of peaks 2047.1 (red) and 1838 (blue), as predicted by NMR-based tri-dimensional analysis of the CRT P-domain <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011703#pone.0011703-Ellgaard1\" target=\"_blank\">[19]</a>.</p>", "links"=>[], "tags"=>["cross-linking"], "article_id"=>510057, "categories"=>["Immunology"], "users"=>["Song Ling", "Andrew Cheng", "Paul Pumpens", "Marek Michalak", "Joseph Holoshitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011703.g002", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Photoactive_cross_linking_studies_/510057", "title"=>"Photoactive cross-linking studies.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-22 00:00:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/839822"], "description"=>"<p><b>A</b>. A SE-positive HLA-DR4 molecule (PDB ID: 2SEB) interacting with the SE-binding site in the CRT P-domain. The HLA-DRα chain is shown in green, HLA-DRβ chain is in yellow, the SE is in cyan, CRT P-domain is in purple, and the groove peptide is shown in orange. <b>B</b>. A closer view of the interactions between CRT Glu<sup>217</sup> and SE Gln<sup>70</sup> and between CRT Glu<sup>223</sup> and SE Arg<sup>72</sup>.</p>", "links"=>[], "tags"=>["crt-se"], "article_id"=>510284, "categories"=>["Immunology"], "users"=>["Song Ling", "Andrew Cheng", "Paul Pumpens", "Marek Michalak", "Joseph Holoshitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011703.g005", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Proposed_CRT_SE_interaction_model_/510284", "title"=>"Proposed CRT-SE interaction model.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-22 00:04:44"}
  • {"files"=>["https://ndownloader.figshare.com/files/839681"], "description"=>"<p>Graphic representation of the two most significant docking models shown in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011703#pone-0011703-t001\" target=\"_blank\">Table 1:</a> Model A (left) and Model B (right). Closer views of the interactions between CRT (black font) and SE (cyan font) residues are shown in the lower panels.</p>", "links"=>[], "tags"=>["docking"], "article_id"=>510140, "categories"=>["Immunology"], "users"=>["Song Ling", "Andrew Cheng", "Paul Pumpens", "Marek Michalak", "Joseph Holoshitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011703.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SE_CRT_docking_models_/510140", "title"=>"SE-CRT docking models.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-22 00:02:20"}
  • {"files"=>["https://ndownloader.figshare.com/files/839745"], "description"=>"<p><b>A</b>. K42 <i>crt<sup>−/−</sup></i> MEF cells were pre-incubated overnight with 1 µg/ml of WT CRT or its mutants. Then, the SE-expressing HLA-DR tetramer T-DRB1*0401 (24 µg/ml) was added and ROS production rates were measured as fluorescent units per min (FU/minute). <b>B</b>. Representative time-course curves of ROS production in response to T-DRB1*0401 stimulation in K42 cells pre-incubated with either WT CRT (△) or CRT-E217A mutant (•). <b>C</b>. K42 <i>crt<sup>−/−</sup></i> MEF cells were pre-incubated overnight with 1 µg/ml of WT CRT or its point mutants. Then, the SE-expressing ligand HBc*0401 (20 µg/ml) was added and ROS production was measured as in <b>A</b>. <b>D</b>. K42 <i>crt<sup>−/−</sup></i> MEF cells were pre-incubated overnight with 1 µg/ml of WT CRT or its point mutants. Then, HBc*0401 was added and NO production rates were measured. Data are shown as incremental mean ± SEM values, above the levels obtained in the absence of the receptor and/or the ligand, as in previous studies <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0011703#pone.0011703-Ling1\" target=\"_blank\">[4]</a>. *, <i>p</i><0.05 compared to WT CRT.</p>", "links"=>[], "tags"=>["crt", "residues", "se-activated"], "article_id"=>510204, "categories"=>["Immunology"], "users"=>["Song Ling", "Andrew Cheng", "Paul Pumpens", "Marek Michalak", "Joseph Holoshitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011703.g004", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_of_CRT_residues_that_are_critical_for_SE_activated_signaling_/510204", "title"=>"Identification of CRT residues that are critical for SE-activated signaling.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-22 00:03:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/839911"], "description"=>"<p>Docking models: Interactions between SE and CRT residues.</p>", "links"=>[], "tags"=>["interactions", "se", "crt"], "article_id"=>510364, "categories"=>["Immunology"], "users"=>["Song Ling", "Andrew Cheng", "Paul Pumpens", "Marek Michalak", "Joseph Holoshitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011703.t001", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Docking_models_Interactions_between_SE_and_CRT_residues_/510364", "title"=>"Docking models: Interactions between SE and CRT residues.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-07-22 00:06:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/839491"], "description"=>"<p><b>A.</b> A theoretical 3D structure of CRT. Rabbit CRT (Accession No. AAB20096) was computationally modeled based on the known crystal structure of Calnexin (PDB ID: 1JHN), using Modeler 9v7 software (School of Pharmacy, UCSF). CRT N-domain is shown in green, P-domain is in cyan and C-domain is shown in orange. <b>B</b>. Schematic representation of rabbit CRT domain-deletion mutants. <b>C,D.</b> SPR-based interactions between the SE ligand and CRT domain-deletion mutants. WT CRT or its domain-deletion mutants were immobilized on a CM5 biosensor chip surface and the SE peptidic ligands 65-79*0401 (<b>C</b>) or 65-79*0404 (<b>D</b>) were run in the analyte.</p>", "links"=>[], "tags"=>["se", "domain-deleted"], "article_id"=>509948, "categories"=>["Immunology"], "users"=>["Song Ling", "Andrew Cheng", "Paul Pumpens", "Marek Michalak", "Joseph Holoshitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011703.g001", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Interaction_between_the_SE_and_domain_deleted_CRT_/509948", "title"=>"Interaction between the SE and domain-deleted CRT.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-07-22 02:45:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/839874"], "description"=>"<p>Values are shown as mean ± SEM. Significantly lower interactions are shown in bold. </p><p>, <i>p</i><0.05; </p><p>, <i>p</i><0.005. The figures in parentheses represent the number of replicates.</p>", "links"=>[], "tags"=>["interactions", "se", "ligands", "wt", "mutant"], "article_id"=>510334, "categories"=>["Immunology"], "users"=>["Song Ling", "Andrew Cheng", "Paul Pumpens", "Marek Michalak", "Joseph Holoshitz"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0011703.t002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SPR_interactions_between_SE_ligands_and_WT_or_mutant_CRT_/510334", "title"=>"SPR interactions between SE ligands and WT or mutant CRT.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-07-22 00:05:34"}

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