The Heparin-Binding Activity of Secreted Modular Calcium-Binding Protein 1 (SMOC-1) Modulates Its Cell Adhesion Properties
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{"title"=>"The Heparin-Binding Activity of Secreted Modular Calcium-Binding Protein 1 (SMOC-1) Modulates Its Cell Adhesion Properties", "type"=>"journal", "authors"=>[{"first_name"=>"Marina", "last_name"=>"Klemenčič", "scopus_author_id"=>"55606280000"}, {"first_name"=>"Marko", "last_name"=>"Novinec", "scopus_author_id"=>"12778756900"}, {"first_name"=>"Silke", "last_name"=>"Maier", "scopus_author_id"=>"24438515800"}, {"first_name"=>"Ursula", "last_name"=>"Hartmann", "scopus_author_id"=>"7102393082"}, {"first_name"=>"Brigita", "last_name"=>"Lenarčič", "scopus_author_id"=>"23114830600"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"pmid"=>"23437253", "sgr"=>"84874304182", "doi"=>"10.1371/journal.pone.0056839", "scopus"=>"2-s2.0-84874304182", "pui"=>"368409482", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "issn"=>"19326203"}, "id"=>"9af8e21f-224d-3b79-9a3e-9ab4fb28521b", "abstract"=>"Secreted modular calcium-binding proteins 1 and 2 (SMOC-1 and SMOC-1) are extracellular calcium- binding proteins belonging to the BM-40 family of proteins. In this work we have identified a highly basic region in the extracellular calcium-binding (EC) domain of the SMOC-1 similar to other known glycosaminoglycan-binding motifs. Size-exclusion chromatography shows that full length SMOC-1 as well as its C-terminal EC domain alone bind heparin and heparan sulfate, but not the related chondroitin sulfate or dermatan sulfate glycosaminoglycans. Intrinsic tryptophan fluorescence measurements were used to quantify the binding of heparin to full length SMOC-1 and the EC domain alone. The calculated equilibrium dissociation constants were in the lower micromolar range. The binding site consists of two antiparallel alpha helices and mutagenesis experiments have shown that heparin-binding residues in both helices must be replaced in order to abolish heparin binding. Furthermore, we show that the SMOC-1 EC domain, like the SMOC-2 EC domain, supports the adhesion of epithelial HaCaT cells. Heparin-binding impaired mutants failed to support S1EC-mediated cell adhesion and together with the observation that S1EC in complex with soluble heparin attenuated cell adhesion we conclude that a functional and accessible S1EC heparin-binding site mediates adhesion of epithelial cells to SMOC-1.", "link"=>"http://www.mendeley.com/research/heparinbinding-activity-secreted-modular-calciumbinding-protein-1-smoc1-modulates-cell-adhesion-prop", "reader_count"=>15, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Researcher"=>5, "Student > Ph. D. Student"=>3, "Student > Master"=>1, "Student > Bachelor"=>1, "Lecturer"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>3, "Researcher"=>5, "Student > Ph. D. Student"=>3, "Student > Master"=>1, "Student > Bachelor"=>1, "Lecturer"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>3, "Medicine and Dentistry"=>6, "Agricultural and Biological Sciences"=>3, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>6}, "Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>3}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Ukraine"=>1, "Spain"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/965079"], "description"=>"<p>(<b>A</b>) Ensemble of all docking solutions that are in agreement with experimental data. The largest cluster of docking solutions is running across both helices and over the loop of the second EF hand (from the lower right to the upper left). (<b>B</b>) A selected docking solution from the largest cluster of docking orientations in two different perspectives. Heparin chains are shown as sticks. The surface potential was calculated with APBS software. Images were created with PyMOL (DeLano Scientific; <a href=\"http://www.pymol.org\" target=\"_blank\">http://www.pymol.org</a>).</p>", "links"=>[], "tags"=>["heparin", "octasaccharides", "binding"], "article_id"=>634944, "categories"=>["Chemistry", "Biochemistry", "Cell Biology"], "users"=>["Marina Klemenčič", "Marko Novinec", "Silke Maier", "Ursula Hartmann", "Brigita Lenarčič"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056839.g007", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Docking_of_heparin_octasaccharides_to_the_proposed_binding_site_on_the_S1EC_/634944", "title"=>"Docking of heparin octasaccharides to the proposed binding site on the S1EC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 09:59:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/965074"], "description"=>"<p>(<b>A</b>) Elution profiles of MUTE, MUTF and DBMUT from a Superdex 200 SEC column in the presence and absence of heparin. All runs were performed in 20 mM sodium phosphate buffer pH 7.4 containing 150 mM NaCl. Elution volumes of standard proteins (Dalton Standards MS-II) are given in the diagrams. (<b>B</b>) Changes in intrinsic fluorescence emission spectra of MUTE and MUTF, respectively, exposed to various concentrations of heparin. Proteins (5 µM) were incubated with increasing amounts of heparin (0 to 200 µM). The solid black line represents the best-fit curves calculated by use of <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0056839#pone.0056839.e002\" target=\"_blank\">Equation 2</a>, which was used to derive <i>K</i><sub>d</sub> values for MUTE and MUTF interactions with heparin. (<b>C</b>) HaCaT cells were plated on wells coated with the indicated amounts of wild-type S1EC as a control or mutant proteins MUTE, MUTF or DBMUT. Adhesion assay was performed as described before.</p>", "links"=>[], "tags"=>["binding", "adhesive", "heparin-binding", "impaired"], "article_id"=>634939, "categories"=>["Chemistry", "Biochemistry", "Cell Biology"], "users"=>["Marina Klemenčič", "Marko Novinec", "Silke Maier", "Ursula Hartmann", "Brigita Lenarčič"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056839.g006", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Heparin_binding_and_adhesive_properties_of_heparin_binding_impaired_mutants_/634939", "title"=>"Heparin binding and adhesive properties of heparin-binding impaired mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 09:58:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/965067"], "description"=>"<p>(<b>A, B</b>) Changes in intrinsic fluorescence emission spectra of SMOC-1 and S1EC, respectively, in the presence of various concentrations of heparin. Proteins (5 µM) were incubated with increasing amounts of heparin (0–200 µM, top line to bottom line, respectively). An excitation wavelength of 295 nm was used and spectra recorded from 300 to 500 nm. The observed relative changes in intrinsic fluorescence were plotted as a function of heparin concentration and transformed to degree of saturation. (<b>C, D</b>) Plots of fluorescence intensity versus heparin concentration. The solid black lines represent the best-fit curves calculated with <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0056839#pone.0056839.e002\" target=\"_blank\">Equation 2</a>. Calcium binding of SMOC-1 or S1EC to heparin was also assessed in the presence of 5 mM EDTA. Best-fit curves are shown as grey solid lines. All calculated <i>K</i><sub>d</sub> values are given in the plots. The analysis was performed with GraphPad Prism 5.0 Software.</p>", "links"=>[], "tags"=>["tryptophan", "fluorescence", "smoc-1", "s1ec"], "article_id"=>634932, "categories"=>["Chemistry", "Biochemistry", "Cell Biology"], "users"=>["Marina Klemenčič", "Marko Novinec", "Silke Maier", "Ursula Hartmann", "Brigita Lenarčič"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056839.g004", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Intrinsic_tryptophan_fluorescence_of_SMOC_1_and_S1EC_in_the_presence_of_heparin_/634932", "title"=>"Intrinsic tryptophan fluorescence of SMOC-1 and S1EC in the presence of heparin.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 09:56:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/965063"], "description"=>"<p>(<b>A</b>) Elution profiles of S1FL under different conditions. The GAGs used were heparin (HP), heparin sulfate (HS), chondroitin sulfate (CS) and dermatan sulfate (DS). All runs were performed in 20 mM sodium phosphate buffer pH 7.4 containing 150 mM NaCl. (<b>B</b>) Elution profile of S1EC domain from a Superdex 200 SEC column in the presence and absence of heparin (HP). Both runs were performed in 20 mM sodium phosphate buffer pH 7.4 containing 150 mM NaCl. Elution volumes of standard proteins (Dalton Standards MS-II) are given in both diagrams.</p>", "links"=>[], "tags"=>["chromatography", "smoc-1", "s1ec", "glycosaminoglycans"], "article_id"=>634929, "categories"=>["Chemistry", "Biochemistry", "Cell Biology"], "users"=>["Marina Klemenčič", "Marko Novinec", "Silke Maier", "Ursula Hartmann", "Brigita Lenarčič"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056839.g002", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Size_exclusion_chromatography_of_SMOC_1_and_S1EC_in_the_presence_and_absence_of_glycosaminoglycans_GAGs_/634929", "title"=>"Size-exclusion chromatography of SMOC-1 and S1EC in the presence and absence of glycosaminoglycans (GAGs).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 09:55:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/965059"], "description"=>"<p>(<b>A</b>) Sequence alignment of the part of the EC domain which contains the potential glycosaminoglycan-binding site with other members of BM-40 family. The putative GAG-binding motive is shown in bold, black for SMOC-1 and grey for SMOC-2, and the positions of α-helices E and F are underlined. (<b>B</b>) Homology model of the S1EC domain in cartoon representation. Helices are numbered according to the BM-40 EC domain <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0056839#pone.0056839-Maurer1\" target=\"_blank\">[10]</a> and calcium ions in EF hands are represented as yellow spheres. (<b>C</b>) The putative heparin-binding region in helices E and F. Positively charged residues are shown as sticks. (<b>D</b>) Surface potential of the S1EC domain calculated with APBS Software. (<b>E</b>) Superposition of the S1EC model (shown in orange) and the BM-40 EC domain (shown in blue). All images were prepared with PyMOL (DeLano Scientific; <a href=\"http://www.pymol.org\" target=\"_blank\">http://www.pymol.org</a>).</p>", "links"=>[], "tags"=>["heparin", "binding", "tertiary"], "article_id"=>634927, "categories"=>["Chemistry", "Biochemistry", "Cell Biology"], "users"=>["Marina Klemenčič", "Marko Novinec", "Silke Maier", "Ursula Hartmann", "Brigita Lenarčič"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056839.g001", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Identification_of_the_heparin_binding_site_in_the_primary_and_tertiary_structure_of_S1EC_/634927", "title"=>"Identification of the heparin binding site in the primary and tertiary structure of S1EC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 09:54:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/965070"], "description"=>"<p>(<b>A</b>) HaCaT cells (1 × 10<sup>6</sup> cells/ml) were plated on microtiter wells coated with the indicated amount of S1EC or fibronectin that served as a positive control. Attached cells were stained with cresyl violet and the extracted dye was quantified by absorbance at 590 nm. (<b>B</b>) Bars represent HaCaT cells with 5 mM EGTA in serum-free DMEM media as well as HaCaT cells grown in low-sulfate medium containing 30 mM chlorate without or with addition of 10 mM Na<sub>2</sub>SO<sub>4</sub>. All cells were preincubated with reagents at 37°C for 30 min and then plated on S1EC (5 mg/ml) or fibronectin (1 mg/ml). Data shown are mean ± S.D. of three determinations and are representative of at least three experiments. (<b>C</b>) HaCaT cells grown on either human fibronectin or murine S1EC were stained with a rabbit anti-β6 integrin antibody (green) or with a mouse anti-vinculin antibody (red) to show the recruitment of the integrin to focal adhesions. In the right-most panels the superposition of the two stainings is shown. (<b>D</b>) HaCaT cells were plated on microtiter wells coated with S1EC (5 mg/ml) or fibronectin (1 mg/ml). Increasing amounts of heparin were added to the cells prior to plating. (<b>E</b>) HaCaT cells were cultured in low sulfate medium containing the indicated amount of sodium chlorate for 24 h, washed, harvested, and then plated on S1EC (5 mg/ml) or fibronectin (1 mg/ml).</p>", "links"=>[], "tags"=>["hacat", "cells"], "article_id"=>634935, "categories"=>["Chemistry", "Biochemistry", "Cell Biology"], "users"=>["Marina Klemenčič", "Marko Novinec", "Silke Maier", "Ursula Hartmann", "Brigita Lenarčič"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056839.g005", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Adhesion_of_HaCaT_cells_to_S1EC_/634935", "title"=>"Adhesion of HaCaT cells to S1EC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 09:57:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/965083", "https://ndownloader.figshare.com/files/965085"], "description"=>"<div><p>Secreted modular calcium-binding proteins 1 and 2 (SMOC-1 and SMOC-1) are extracellular calcium- binding proteins belonging to the BM-40 family of proteins. In this work we have identified a highly basic region in the extracellular calcium-binding (EC) domain of the SMOC-1 similar to other known glycosaminoglycan-binding motifs. Size-exclusion chromatography shows that full length SMOC-1 as well as its C-terminal EC domain alone bind heparin and heparan sulfate, but not the related chondroitin sulfate or dermatan sulfate glycosaminoglycans. Intrinsic tryptophan fluorescence measurements were used to quantify the binding of heparin to full length SMOC-1 and the EC domain alone. The calculated equilibrium dissociation constants were in the lower micromolar range. The binding site consists of two antiparallel alpha helices and mutagenesis experiments have shown that heparin-binding residues in both helices must be replaced in order to abolish heparin binding. Furthermore, we show that the SMOC-1 EC domain, like the SMOC-2 EC domain, supports the adhesion of epithelial HaCaT cells. Heparin-binding impaired mutants failed to support S1EC-mediated cell adhesion and together with the observation that S1EC in complex with soluble heparin attenuated cell adhesion we conclude that a functional and accessible S1EC heparin-binding site mediates adhesion of epithelial cells to SMOC-1.</p> </div>", "links"=>[], "tags"=>["heparin-binding", "secreted", "modular", "calcium-binding", "modulates", "adhesion", "properties"], "article_id"=>634948, "categories"=>["Chemistry", "Biochemistry", "Cell Biology"], "users"=>["Marina Klemenčič", "Marko Novinec", "Silke Maier", "Ursula Hartmann", "Brigita Lenarčič"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0056839.s001", "https://dx.doi.org/10.1371/journal.pone.0056839.s002"], "stats"=>{"downloads"=>4, "page_views"=>45, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Heparin_Binding_Activity_of_Secreted_Modular_Calcium_Binding_Protein_1_SMOC_1_Modulates_Its_Cell_Adhesion_Properties__/634948", "title"=>"The Heparin-Binding Activity of Secreted Modular Calcium-Binding Protein 1 (SMOC-1) Modulates Its Cell Adhesion Properties", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-02-22 09:59:45"}
  • {"files"=>["https://ndownloader.figshare.com/files/965064"], "description"=>"<p>Spectra were recorded using a protein concentration of 5 µM in 20 mM HEPES containing 50 mM NaCl and 2 mM CaCl<sub>2.</sub> The solid line represents S1EC in the presence of 2 mM calcium ions, the dotted line represents S1EC in the presence of 5 mM EDTA and the dashed line S1EC in the presence of 50 µM heparin.</p>", "links"=>[], "tags"=>["dichroism", "spectra"], "article_id"=>634930, "categories"=>["Chemistry", "Biochemistry", "Cell Biology"], "users"=>["Marina Klemenčič", "Marko Novinec", "Silke Maier", "Ursula Hartmann", "Brigita Lenarčič"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0056839.g003", "stats"=>{"downloads"=>1, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Circular_dichroism_spectra_of_S1EC_/634930", "title"=>"Circular dichroism spectra of S1EC.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-22 09:55:55"}

PMC Usage Stats | Further Information

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Relative Metric

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