Decaprenylphosphoryl-β-D-Ribose 2′-Epimerase, the Target of Benzothiazinones and Dinitrobenzamides, Is an Essential Enzyme in Mycobacterium smegmatis
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{"title"=>"Decaprenylphosphoryl-β-D-Ribose 2′-epimerase, the target of benzothiazinones and dinitrobenzamides, is an essential enzyme in Mycobacterium smegmatis", "type"=>"journal", "authors"=>[{"first_name"=>"Paul K.", "last_name"=>"Crellin", "scopus_author_id"=>"6603111849"}, {"first_name"=>"Rajini", "last_name"=>"Brammananth", "scopus_author_id"=>"13908008400"}, {"first_name"=>"Ross L.", "last_name"=>"Coppel", "scopus_author_id"=>"7102913547"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-79951566404", "pmid"=>"21346818", "sgr"=>"79951566404", "doi"=>"10.1371/journal.pone.0016869", "issn"=>"19326203", "pui"=>"361260660"}, "id"=>"238a6cbb-5e48-3eb8-909d-8a39e6316b14", "abstract"=>"BACKGROUND: The unique cell wall of bacteria of the suborder Corynebacterineae is essential for the growth and survival of significant human pathogens including Mycobacterium tuberculosis and Mycobacterium leprae. Drug resistance in mycobacteria is an increasingly common development, making identification of new antimicrobials a priority. Recent studies have revealed potent anti-mycobacterial compounds, the benzothiazinones and dinitrobenzamides, active against DprE1, a subunit of decaprenylphosphoribose 2' epimerase which forms decaprenylphosphoryl arabinose, the arabinose donor for mycobacterial cell wall biosynthesis. Despite the exploitation of Mycobacterium smegmatis in the identification of DprE1 as the target of these new antimicrobials and its use in the exploration of mechanisms of resistance, the essentiality of DprE1 in this species has never been examined. Indeed, direct experimental evidence of the essentiality of DprE1 has not been obtained in any species of mycobacterium. METHODOLOGY/PRINCIPAL FINDINGS: In this study we constructed a conditional gene knockout strain targeting the ortholog of dprE1 in M. smegmatis, MSMEG_6382. Disruption of the chromosomal copy of MSMEG_6382 was only possible in the presence of a plasmid-encoded copy of MSMEG_6382. Curing of this \"rescue\" plasmid from the bacterial population resulted in a cessation of growth, demonstrating gene essentiality. CONCLUSIONS/SIGNIFICANCE: This study provides the first direct experimental evidence for the essentiality of DprE1 in mycobacteria. The essentiality of DprE1 in M. smegmatis, combined with its conservation in all sequenced mycobacterial genomes, suggests that decaprenylphosphoryl arabinose synthesis is essential in all mycobacteria. Our findings indicate a lack of redundancy in decaprenylphosphoryl arabinose synthesis in M. smegmatis, despite the relatively large coding capacity of this species, and suggest that no alternative arabinose donors for cell wall biosynthesis exist. Overall, this study further validates DprE1 as a promising target for new anti-mycobacterial drugs.", "link"=>"http://www.mendeley.com/research/decaprenylphosphoryl%CE%B2dribose-2epimerase-target-benzothiazinones-dinitrobenzamides-essential-enzyme-m", "reader_count"=>44, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Student > Doctoral Student"=>6, "Researcher"=>4, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>1, "Student > Master"=>4, "Other"=>4, "Student > Bachelor"=>9, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Student > Doctoral Student"=>6, "Researcher"=>4, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>1, "Student > Master"=>4, "Other"=>4, "Student > Bachelor"=>9, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>10, "Agricultural and Biological Sciences"=>15, "Medicine and Dentistry"=>1, "Arts and Humanities"=>1, "Veterinary Science and Veterinary Medicine"=>1, "Chemistry"=>15, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Chemistry"=>{"Chemistry"=>15}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>15}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>10}, "Arts and Humanities"=>{"Arts and Humanities"=>1}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1, "United Kingdom"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/800776"], "description"=>"<p>6382CKO was cultured at 30°C in LB containing Kn and Sm. At saturation, 5 ml was used to inoculate 200 ml of LB/Kn medium that had been prewarmed at the permissive (30°C •) or non-permissive (42°C ▪) temperature. Incubation was continued at the two temperatures and both cultures were sampled regularly with serial dilutions plated on LB plates containing Kn to determine colony forming units (CFUs) per ml. A wild-type <i>M. smegmatis</i> mc<sup>2</sup>155 strain containing the kanamycin resistance plasmid pMV261 was included as a control (30°C ▴, 42°C ▾). Unbroken lines represent the 6382CKO strain while broken lines represent the wild type (pMV261) control strain. These data represent means of triplicate samples ± standard deviation and are representative of three independent experiments.</p>", "links"=>[], "tags"=>["lb"], "article_id"=>471148, "categories"=>["Pharmacology", "Infectious Diseases", "Biochemistry", "Microbiology"], "users"=>["Paul K. Crellin", "Rajini Brammananth", "Ross L. Coppel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0016869.g005", "stats"=>{"downloads"=>3, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/MSMEG_6382_is_essential_for_growth_of_i_M_smegmatis_i_in_LB_broth_/471148", "title"=>"MSMEG_6382 is essential for growth of <i>M. smegmatis</i> in LB broth.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 20:47:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/800511"], "description"=>"<p><b>A</b>. The recombination plasmid pPKC72 contained a cloned copy of <i>MSMEG_6382</i> interrupted by a non-polar kanamycin resistance cassette (<i>MSMEG_6382</i>::<i>aphA3</i>), a gentamycin resistance marker (Gm<sup>r</sup>), a temperature-sensitive replication origin for <i>M. smegmatis</i> (ori<i>Ms</i> (ts)), a replication origin for <i>E. coli</i> (ori<i>Ec</i>) and a counterselectable marker encoding sucrose sensitivity (<i>sacB</i>). The construct was introduced into <i>M. smegmatis</i> at the permissive temperature (30°C). Integration of the plasmid by a single crossover at the position indicated was detected by growing the cells at the non-permissive temperature (42°C) in the presence of kanamycin. <b>B</b>. Genetic map of the single crossover, showing key restriction sites and fragments. <b>C.</b> Culturing the single crossover strain containing a rescue plasmid encoding <i>MSMEG_6382</i> gave rise to a disrupted copy of <i>MSMEG_6382</i> in the chromosome, producing the conditional knockout (6382CKO). Since the disruption of <i>MSMEG_6382</i> coincided with the loss of the <i>sacB</i> gene, the conditional knockout strain could be selected on sucrose plates. Double lines indicate chromosomal DNA, single lines indicate plasmid DNA. Restriction fragments hybridising to the <i>MSMEG_6382-</i>specific probe are shown in kilobases (kb).</p>", "links"=>[], "tags"=>["conditional", "disruption"], "article_id"=>470882, "categories"=>["Pharmacology", "Infectious Diseases", "Biochemistry", "Microbiology"], "users"=>["Paul K. Crellin", "Rajini Brammananth", "Ross L. Coppel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0016869.g003", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Genetic_strategy_for_conditional_disruption_of_i_MSMEG_6382_i_/470882", "title"=>"Genetic strategy for conditional disruption of <i>MSMEG_6382</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 20:45:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/800647"], "description"=>"<p>Southern blot of genomic DNA digested with <i>Hin</i>dIII/<i>Not</i>I/<i>Xba</i>I. Lane 1, DNA molecular weight DNA markers of the sizes indicated (kilobases, kb); lane 2, wild-type <i>M. smegmatis</i> mc<sup>2</sup>155; lane 3, single crossover strain used to derive the conditional knockout; lane 4, conditional knockout of <i>MSMEG_6382</i>, designated 6382CKO.</p>", "links"=>[], "tags"=>["disruption"], "article_id"=>471023, "categories"=>["Pharmacology", "Infectious Diseases", "Biochemistry", "Microbiology"], "users"=>["Paul K. Crellin", "Rajini Brammananth", "Ross L. Coppel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0016869.g004", "stats"=>{"downloads"=>2, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Conditional_disruption_of_i_MSMEG_6382_i_/471023", "title"=>"Conditional disruption of <i>MSMEG_6382</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 20:46:21"}
  • {"files"=>["https://ndownloader.figshare.com/files/800303"], "description"=>"<p><b>A</b>. The mycobacterial cell wall is a multilayered structure containing many components unique to these and closely related bacteria, including phosphatidylinositol mannosides (PIM), lipoarabinomannans (LAM), trehalose monomycolates (TMM), trehalose dimycolates (TDM) mycolic acids and arabinogalactan. The biosynthetic pathways for these unique components are a rich source of potential drug targets. Arabinose sugars are shown in orange. <b>B</b>. Decaprenylphosphoryl arabinose (DPA) is formed by the epimerization of decaprenylphosphoryl ribose (DPR) by DprE1 (Rv3790) and DprE2 (Rv3791). DPA serves as an arabinose donor in cell wall biosynthesis, contributing to arabinogalactan and LAM assembly (orange arrows).</p>", "links"=>[], "tags"=>["mycobacterial", "pathway", "dpa"], "article_id"=>470672, "categories"=>["Pharmacology", "Infectious Diseases", "Biochemistry", "Microbiology"], "users"=>["Paul K. Crellin", "Rajini Brammananth", "Ross L. Coppel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0016869.g001", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/The_Mycobacterial_cell_wall_and_pathway_for_DPA_biosynthesis_/470672", "title"=>"The Mycobacterial cell wall and pathway for DPA biosynthesis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 20:44:28"}
  • {"files"=>["https://ndownloader.figshare.com/files/800397"], "description"=>"<p>Homologs from <i>M. leprae</i> (ML0109), <i>M. tuberculosis</i> (Rv3790) and <i>M. smegmatis</i> (MSMEG_6382) were aligned using CLUSTALW <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0016869#pone.0016869-Larkin1\" target=\"_blank\">[25]</a>. Residues that are completely conserved are reverse shaded while similar residues are indicated in grey. The putative FAD-binding domain is shown by a solid line. The conserved cysteine residue that is altered in BTZ-resistant mycobacteria <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0016869#pone.0016869-Makarov2\" target=\"_blank\">[11]</a> is indicated by an asterix.</p>", "links"=>[], "tags"=>["Infectious diseases", "microbiology", "pharmacology", "Biochemistry"], "article_id"=>470764, "categories"=>["Pharmacology", "Infectious Diseases", "Biochemistry", "Microbiology"], "users"=>["Paul K. Crellin", "Rajini Brammananth", "Ross L. Coppel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0016869.g002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/DprE1_alignment_/470764", "title"=>"DprE1 alignment.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 20:45:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/800944"], "description"=>"<p>The conditional knockout strain 6382CKO was cultured at 30°C on Middlebrook 7H10 agar containing Kn and Sm, then subcultured onto Middlebrook 7H10 agar containing Kn at 30°C and 42°C and examined for growth. Wild-type <i>M. smegmatis</i> mc<sup>2</sup>155 control strain cultured at 30°C (<b>A</b>) and 42°C (<b>B</b>) on Middlebrook 7H10 agar without antibiotics; 6382CKO strain cultured at 30°C (<b>C</b>) and 42°C (<b>D</b>) on Middlebrook 7H10 agar containing Kn.</p>", "links"=>[], "tags"=>["middlebrook"], "article_id"=>471318, "categories"=>["Pharmacology", "Infectious Diseases", "Biochemistry", "Microbiology"], "users"=>["Paul K. Crellin", "Rajini Brammananth", "Ross L. Coppel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0016869.g006", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/MSMEG_6382_is_essential_for_growth_of_i_M_smegmatis_i_on_Middlebrook_agar_/471318", "title"=>"MSMEG_6382 is essential for growth of <i>M. smegmatis</i> on Middlebrook agar.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 20:48:01"}

PMC Usage Stats | Further Information

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Relative Metric

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