The Structure of the Oligomerization Domain of Lsr2 from Mycobacterium tuberculosis Reveals a Mechanism for Chromosome Organization and Protection
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{"title"=>"The structure of the Oligomerization domain of Lsr2 from Mycobacterium tuberculosis reveals a mechanism for chromosome organization and protection", "type"=>"journal", "authors"=>[{"first_name"=>"Emma L.", "last_name"=>"Summers", "scopus_author_id"=>"12545665200"}, {"first_name"=>"Kathrin", "last_name"=>"Meindl", "scopus_author_id"=>"56205940300"}, {"first_name"=>"Isabel", "last_name"=>"Usón", "scopus_author_id"=>"7004373162"}, {"first_name"=>"Alok K.", "last_name"=>"Mitra", "scopus_author_id"=>"7402543410"}, {"first_name"=>"Mazdak", "last_name"=>"Radjainia", "scopus_author_id"=>"24449842000"}, {"first_name"=>"Roberto", "last_name"=>"Colangeli", "scopus_author_id"=>"6603411542"}, {"first_name"=>"David", "last_name"=>"Alland", "scopus_author_id"=>"6701345204"}, {"first_name"=>"Vickery L.", "last_name"=>"Arcus", "scopus_author_id"=>"6602776721"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"364996194", "sgr"=>"84862175853", "pmid"=>"22719899", "scopus"=>"2-s2.0-84862175853", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "doi"=>"10.1371/journal.pone.0038542", "issn"=>"19326203"}, "id"=>"6db6f347-1bcd-3587-b8f0-4e915c55f3f2", "abstract"=>"Lsr2 is a small DNA-binding protein present in mycobacteria and related actinobacteria that regulates gene expression and influences the organization of bacterial chromatin. Lsr2 is a dimer that binds to AT-rich regions of chromosomal DNA and physically protects DNA from damage by reactive oxygen intermediates (ROI). A recent structure of the C-terminal DNA-binding domain of Lsr2 provides a rationale for its interaction with the minor groove of DNA, its preference for AT-rich tracts, and its similarity to other bacterial nucleoid-associated DNA-binding domains. In contrast, the details of Lsr2 dimerization (and oligomerization) via its N-terminal domain, and the mechanism of Lsr2-mediated chromosomal cross-linking and protection is unknown. We have solved the structure of the N-terminal domain of Lsr2 (N-Lsr2) at 1.73 Å resolution using crystallographic ab initio approaches. The structure shows an intimate dimer of two ß-ß-a motifs with no close homologues in the structural databases. The organization of individual N-Lsr2 dimers in the crystal also reveals a mechanism for oligomerization. Proteolytic removal of three N-terminal residues from Lsr2 results in the formation of an anti-parallel β-sheet between neighboring molecules and the formation of linear chains of N-Lsr2. Oligomerization can be artificially induced using low concentrations of trypsin and the arrangement of N-Lsr2 into long chains is observed in both monoclinic and hexagonal crystallographic space groups. In solution, oligomerization of N-Lsr2 is also observed following treatment with trypsin. A change in chromosomal topology after the addition of trypsin to full-length Lsr2-DNA complexes and protection of DNA towards DNAse digestion can be observed using electron microscopy and electrophoresis. These results suggest a mechanism for oligomerization of Lsr2 via protease-activation leading to chromosome compaction and protection, and concomitant down-regulation of large numbers of genes. This mechanism is likely to be relevant under conditions of stress where cellular proteases are known to be upregulated.", "link"=>"http://www.mendeley.com/research/structure-oligomerization-domain-lsr2-mycobacterium-tuberculosis-reveals-mechanism-chromosome-organi", "reader_count"=>29, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Student > Doctoral Student"=>1, "Researcher"=>4, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>3, "Student > Master"=>4, "Student > Bachelor"=>5, "Lecturer"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Student > Doctoral Student"=>1, "Researcher"=>4, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>3, "Student > Master"=>4, "Student > Bachelor"=>5, "Lecturer"=>1}, "reader_count_by_subject_area"=>{"Engineering"=>1, "Biochemistry, Genetics and Molecular Biology"=>7, "Agricultural and Biological Sciences"=>17, "Medicine and Dentistry"=>1, "Immunology and Microbiology"=>3}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>1}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>17}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}}, "reader_count_by_country"=>{"Netherlands"=>1, "Hungary"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/624761"], "description"=>"<p>Trypsin (1∶500) initiates the compaction of co-purified DNA by Lsr2 over 1 h as visualised on a 1% agarose gel (SYBR® safe DNA stain). Subsequent digestion of the compacted DNA using DNase shows protection of the DNA by Lsr2. Equivalent samples were run on an SDS-PAGE gel to show the presence of Lsr2 (both monomer and dimer forms) in the sample after trypsin digestion. Components are labeled: C  =  condensation of DNA upon treatment with trypsin; P  =  protection of DNA; D  =  Lsr2 dimer; M  =  Lsr2 monomer).</p>", "links"=>[], "tags"=>["digestion", "full-length", "lsr2", "co-purified", "genomic"], "article_id"=>295250, "categories"=>["Infectious Diseases", "Biochemistry", "Microbiology"], "users"=>["Emma L. Summers", "Kathrin Meindl", "Isabel Usón", "Alok K. Mitra", "Mazdak Radjainia", "Roberto Colangeli", "David Alland", "Vickery L. Arcus"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038542.g005", "stats"=>{"downloads"=>1, "page_views"=>44, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Trypsin_digestion_of_full_length_Lsr2_co_purified_with_i_E_coli_i_genomic_DNA_/295250", "title"=>"Trypsin digestion of full-length Lsr2 co-purified with <i>E. coli</i> genomic DNA.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 03:58:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/625301"], "description"=>"<p>The C-terminal boundaries of Lsr2 N-terminal domain constructs.</p>", "links"=>[], "tags"=>["c-terminal", "boundaries", "lsr2", "n-terminal"], "article_id"=>295791, "categories"=>["Infectious Diseases", "Biochemistry", "Microbiology"], "users"=>["Emma L. Summers", "Kathrin Meindl", "Isabel Usón", "Alok K. Mitra", "Mazdak Radjainia", "Roberto Colangeli", "David Alland", "Vickery L. Arcus"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038542.t001", "stats"=>{"downloads"=>6, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_C_terminal_boundaries_of_Lsr2_N_terminal_domain_constructs_/295791", "title"=>"The C-terminal boundaries of Lsr2 N-terminal domain constructs.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 04:01:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/624929"], "description"=>"<p>(A) Lsr2 co-purified with <i>E. coli</i> genomic DNA; (B) Lsr2 after trypsin digestion (1∶500 ratio) for 30 minutes; Arrows A and B point to condensed structures commonly seen during the trypsin digestion time series. (Scale bars  = 100 nm); (C) A cartoon representation of protein oligomerization and DNA compaction after trypsin digestion. Lsr2 N-terminal dimerization domain is depicted in green and the C-terminal DNA-binding domain is depicted in orange. The downward pointing arrows correlate the features in (B) with their cartoon representations in (C).</p>", "links"=>[], "tags"=>["stained", "complexes", "visualized", "electron", "microscopy", "morphological", "changes", "trypsin"], "article_id"=>295408, "categories"=>["Infectious Diseases", "Biochemistry", "Microbiology"], "users"=>["Emma L. Summers", "Kathrin Meindl", "Isabel Usón", "Alok K. Mitra", "Mazdak Radjainia", "Roberto Colangeli", "David Alland", "Vickery L. Arcus"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038542.g006", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Negatively_stained_Lsr2_DNA_complexes_visualized_by_transmission_electron_microscopy_show_large_morphological_changes_upon_trypsin_treatment_/295408", "title"=>"Negatively stained Lsr2/DNA complexes visualized by transmission electron microscopy show large morphological changes upon trypsin treatment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 03:59:27"}
  • {"files"=>["https://ndownloader.figshare.com/files/625336"], "description"=>"a<p>Numbers in parentheses correspond to the highest resolution shell.</p>", "links"=>[], "tags"=>["refinement"], "article_id"=>295825, "categories"=>["Infectious Diseases", "Biochemistry", "Microbiology"], "users"=>["Emma L. Summers", "Kathrin Meindl", "Isabel Usón", "Alok K. Mitra", "Mazdak Radjainia", "Roberto Colangeli", "David Alland", "Vickery L. Arcus"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038542.t002", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Crystallographic_data_collection_and_refinement_statistics_/295825", "title"=>"Crystallographic data collection and refinement statistics.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 04:01:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/624444"], "description"=>"<p>(A) Relative conservation of amino acids at different positions from a multiple sequence alignment are depicted using HMM Logo (<a href=\"http://pfam.sanger.ac.uk/family/PF11774.2\" target=\"_blank\">http://pfam.sanger.ac.uk/family/PF11774.2</a>). The height of the letters represents the relative entropy and the width represents the relative contribution of the position to the overall protein family. The pink bars represent regions of insertion in the alignment. Amino acid residue colours reflect their biological propertes (red  =  charged; blues  =  polar, uncharged; yellows  =  aliphatic; greens  =  aromatic). The amino acid sequence for Lsr2 from <i>M. tuberculosis</i> is shown across the top of the HMM logo for comparison and residues that are well-conserved are in bold. (B) Cartoon diagram of Lsr2 N-terminal dimerization domain showing conserved residues. The structure is for the <i>P</i>2<sub>1</sub> crystal form. Conserved residues for each chain are shown in yellow and orange respectively. Yellow residues from chain A are labeled. The chain termini are also labeled.</p>", "links"=>[], "tags"=>["amino", "acids", "n-terminal"], "article_id"=>294930, "categories"=>["Infectious Diseases", "Biochemistry", "Microbiology"], "users"=>["Emma L. Summers", "Kathrin Meindl", "Isabel Usón", "Alok K. Mitra", "Mazdak Radjainia", "Roberto Colangeli", "David Alland", "Vickery L. Arcus"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038542.g002", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Conserved_amino_acids_for_the_N_terminal_domain_of_Lsr2_/294930", "title"=>"Conserved amino acids for the N-terminal domain of Lsr2.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 03:56:58"}
  • {"files"=>["https://ndownloader.figshare.com/files/624533"], "description"=>"<p>The interaction between Lys-4 of one monomer (in blue) and the neighboring N-Lsr2 dimer (in yellow and pink). This interaction is present in both crystal forms. Polar interactions are labelled with pink dotted lines and selected residues are labeled. An electron density map contoured at 1σ is shown as blue mesh.</p>", "links"=>[], "tags"=>["oligomeric"], "article_id"=>295028, "categories"=>["Infectious Diseases", "Biochemistry", "Microbiology"], "users"=>["Emma L. Summers", "Kathrin Meindl", "Isabel Usón", "Alok K. Mitra", "Mazdak Radjainia", "Roberto Colangeli", "David Alland", "Vickery L. Arcus"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038542.g003", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_oligomeric_interface_/295028", "title"=>"The oligomeric interface.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 03:57:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/624323"], "description"=>"<p>(A) A depiction of the monomer: the α-helix, β-strands and chain termini are labeled and the chain is colored blue-red (N-terminus to C-terminus); (B) The dimer as seen in the crystal structure, one chain is colored and the other is grey; (C) A view orthogonal to that of B showing residues critical for dimerization; (D) Lsr2 N-terminal domain oligmerization as generated by crystallographic symmetry. The N-terminus of one dimer donates one strand forming an anti-parallel β-sheet. The second strand is presented by a neighboring dimer. The β-sheet linking two dimers is shown as β0; (E) Crystallographic symmetry (in space group <i>P</i>2<sub>1</sub>) showing the unit cell (in green) projected perpendicular to the b-axis. The two-fold screw axis generates alternating Lsr2 chains that lie back-to-back along the horizontal (in this view). For all figures protein depictions were drawn with PYMOL.</p>", "links"=>[], "tags"=>["diagrams", "lsr2", "n-terminal"], "article_id"=>294805, "categories"=>["Infectious Diseases", "Biochemistry", "Microbiology"], "users"=>["Emma L. Summers", "Kathrin Meindl", "Isabel Usón", "Alok K. Mitra", "Mazdak Radjainia", "Roberto Colangeli", "David Alland", "Vickery L. Arcus"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038542.g001", "stats"=>{"downloads"=>2, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Cartoon_diagrams_of_the_Lsr2_N_terminal_domain_in_the_i_P_i_2_sub_1_sub_crystal_structure_/294805", "title"=>"Cartoon diagrams of the Lsr2 N-terminal domain in the <i>P</i>2<sub>1</sub> crystal structure.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 03:56:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/625091"], "description"=>"<p>(A) The N-terminal Lsr2 dimerization domain in the <i>P</i>3<sub>1</sub>21 space group in two orientations; (B) Proposed orientation of DNA (in blue) between N-terminal chains and a 90° rotation illustrating this from above. The C-terminal DNA-binding domains (in orange) have been positioned according to Gordon <i>et al. </i><a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0038542#pone.0038542-Gordon3\" target=\"_blank\">[22]</a>; (C) Our model of full-length Lsr2 binding to DNA and forming chains cross-linking multiple strands of DNA. The dimension at the bottom of the figure is consistent with the compact fibrils seen in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0038542#pone-0038542-g006\" target=\"_blank\">Figure 6B</a>.</p>", "links"=>[], "tags"=>["chromosomal", "dna", "suggested", "hexagonal"], "article_id"=>295578, "categories"=>["Infectious Diseases", "Biochemistry", "Microbiology"], "users"=>["Emma L. Summers", "Kathrin Meindl", "Isabel Usón", "Alok K. Mitra", "Mazdak Radjainia", "Roberto Colangeli", "David Alland", "Vickery L. Arcus"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038542.g007", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/A_model_for_chromosomal_DNA_organization_suggested_by_hexagonal_crystal_packing_/295578", "title"=>"A model for chromosomal DNA organization suggested by hexagonal crystal packing.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 04:00:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/624616"], "description"=>"<p>(A) Size exclusion chromatogram of freshly purified Lsr2 N-terminal domain showing a single dimer peak; (B) A chromatogram of the same protein construct used for crystallography (now 14 wks old) demonstrating larger oligomeric forms in solution; (C) The addition of trypsin (1∶500) for 5 min at room temperature to a fresh sample of Lsr2 N-terminal domain accelerates the formation of large oligomeric species in solution. SDS-PAGE gels showing relevant fractions from the purification: L  =  protein loaded on the column; A, B and C represent protein from fractions as labeled on the chromatogram. The N-terminal domain runs at a higher M<sub>r</sub> than expected on SDS-PAGE gels due to the presence of a 6xHis-tag plus a linker.</p>", "links"=>[], "tags"=>["trypsin", "n-lsr2", "facilitates"], "article_id"=>295103, "categories"=>["Infectious Diseases", "Biochemistry", "Microbiology"], "users"=>["Emma L. Summers", "Kathrin Meindl", "Isabel Usón", "Alok K. Mitra", "Mazdak Radjainia", "Roberto Colangeli", "David Alland", "Vickery L. Arcus"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0038542.g004", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Addition_of_trypsin_to_N_Lsr2_facilitates_oligomerization_/295103", "title"=>"Addition of trypsin to N-Lsr2 facilitates oligomerization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 03:57:50"}

PMC Usage Stats | Further Information

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Relative Metric

{"start_date"=>"2012-01-01T00:00:00Z", "end_date"=>"2012-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Organisms", "average_usage"=>[331, 557, 677, 777, 868, 960, 1050, 1136, 1223, 1307, 1390, 1466, 1536, 1603, 1673, 1741, 1814, 1889, 1954, 2028, 2096, 2164, 2233, 2305, 2362]}, {"subject_area"=>"/Physical sciences/Chemistry", "average_usage"=>[302, 508, 622, 720, 804, 888, 973, 1054, 1141, 1219, 1299, 1370, 1442, 1511, 1574, 1644, 1711, 1782, 1846, 1911, 1971, 2030, 2097, 2155, 2217]}, {"subject_area"=>"/Physical sciences/Physics", "average_usage"=>[298, 476, 578, 665, 743, 821, 891, 962, 1036, 1108, 1174, 1240, 1312, 1371, 1430, 1494, 1551, 1609, 1673, 1736, 1795, 1857, 1913, 1976, 2035]}]}
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